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Published in: Surgery Today 12/2020

01-12-2020 | Metastasis | Review Article

Clinical implications of cancer stem cells in digestive cancers: acquisition of stemness and prognostic impact

Authors: Ryouichi Tsunedomi, Kiyoshi Yoshimura, Nobuaki Suzuki, Shoichi Hazama, Hiroaki Nagano

Published in: Surgery Today | Issue 12/2020

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Abstract

Digestive system cancers are the most frequent cancers worldwide and often associated with poor prognosis because of their invasive and metastatic characteristics. Recent studies have found that the plasticity of cancer cells can impart cancer stem-like properties via the epithelial–mesenchymal transition (EMT). Cancer stem-like properties such as tumor initiation are integral to the formation of metastasis, which is the main cause of poor prognosis. Numerous markers of cancer stem cells (CSCs) have been identified in many types of cancer. Therefore, CSCs, via their stem cell-like functions, may play an important role in prognosis after surgery. While several reports have described prognostic analysis using CSC markers, few reviews have summarized CSCs and their association with prognosis. Herein, we review the prognostic potential of eight CSC markers, CD133, CD44, CD90, ALDH1A1, EPCAM, SOX2, SOX9, and LGR5, in digestive cancers including those of the pancreas, colon, liver, gastric, and esophagus.
Literature
1.
go back to reference Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93.PubMed Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93.PubMed
2.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.PubMed Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.PubMed
4.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.PubMed Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.PubMed
5.
go back to reference El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–766.PubMed El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–766.PubMed
6.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMed Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMed
7.
go back to reference Lamarca A, Asselin MC, Manoharan P, McNamara MG, Trigonis I, Hubner R, et al. 18F-FLT PET imaging of cellular proliferation in pancreatic cancer. Crit Rev Oncol Hematol. 2016;99:158–69.PubMed Lamarca A, Asselin MC, Manoharan P, McNamara MG, Trigonis I, Hubner R, et al. 18F-FLT PET imaging of cellular proliferation in pancreatic cancer. Crit Rev Oncol Hematol. 2016;99:158–69.PubMed
8.
go back to reference Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.PubMed Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.PubMed
9.
go back to reference Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003;362:1907–17.PubMed Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003;362:1907–17.PubMed
10.
go back to reference Shimozawa N, Hanazaki K. Longterm prognosis after hepatic resection for small hepatocellular carcinoma. J Am Coll Surg. 2004;198:356–65.PubMed Shimozawa N, Hanazaki K. Longterm prognosis after hepatic resection for small hepatocellular carcinoma. J Am Coll Surg. 2004;198:356–65.PubMed
11.
go back to reference Lai EC, Lau WY. The continuing challenge of hepatic cancer in Asia. Surgeon. 2005;3:210–5.PubMed Lai EC, Lau WY. The continuing challenge of hepatic cancer in Asia. Surgeon. 2005;3:210–5.PubMed
12.
go back to reference Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med. 2008;359:1995–2004.PubMedPubMedCentral Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med. 2008;359:1995–2004.PubMedPubMedCentral
13.
go back to reference Bruix J, Llovet JM. Major achievements in hepatocellular carcinoma. Lancet. 2009;373:614–6.PubMed Bruix J, Llovet JM. Major achievements in hepatocellular carcinoma. Lancet. 2009;373:614–6.PubMed
14.
go back to reference Wu JC, Huang YH, Chau GY, Su CW, Lai CR, Lee PC, et al. Risk factors for early and late recurrence in hepatitis B-related hepatocellular carcinoma. J Hepatol. 2009;51:890–7.PubMed Wu JC, Huang YH, Chau GY, Su CW, Lai CR, Lee PC, et al. Risk factors for early and late recurrence in hepatitis B-related hepatocellular carcinoma. J Hepatol. 2009;51:890–7.PubMed
15.
go back to reference Chun JM, Kwon HJ, Sohn J, Kim SG, Park JY, Bae HI, et al. Prognostic factors after early recurrence in patients who underwent curative resection for hepatocellular carcinoma. J Surg Oncol. 2011;103:148–51.PubMed Chun JM, Kwon HJ, Sohn J, Kim SG, Park JY, Bae HI, et al. Prognostic factors after early recurrence in patients who underwent curative resection for hepatocellular carcinoma. J Surg Oncol. 2011;103:148–51.PubMed
16.
go back to reference Tsunedomi R, Iizuka N, Tamesa T, Sakamoto K, Hamaguchi T, Somura H, et al. Decreased ID2 promotes metastatic potentials of hepatocellular carcinoma by altering secretion of vascular endothelial growth factor. Clin Cancer Res. 2008;14:1025–31.PubMed Tsunedomi R, Iizuka N, Tamesa T, Sakamoto K, Hamaguchi T, Somura H, et al. Decreased ID2 promotes metastatic potentials of hepatocellular carcinoma by altering secretion of vascular endothelial growth factor. Clin Cancer Res. 2008;14:1025–31.PubMed
17.
go back to reference Bertuccio O, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, et al. Recent patterns in gastric cancer: a global overview. Int J Cancer. 2009;125:666–73.PubMed Bertuccio O, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, et al. Recent patterns in gastric cancer: a global overview. Int J Cancer. 2009;125:666–73.PubMed
18.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386386.PubMed Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386386.PubMed
19.
go back to reference Weigelt B, Peterse JL, van’t Veer LJ. Breast cancer metastasis markers and models. Nat Rev Cancer. 2005;5:591–602.PubMed Weigelt B, Peterse JL, van’t Veer LJ. Breast cancer metastasis markers and models. Nat Rev Cancer. 2005;5:591–602.PubMed
20.
go back to reference Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer. 2006;6:449–58.PubMed Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer. 2006;6:449–58.PubMed
21.
go back to reference Zhang HX, Jin GF, Shen HB. Epidemiologic differences in esophageal cancer between Asian and Western populations. Chin J Cancer. 2012;31:281–6.PubMedPubMedCentral Zhang HX, Jin GF, Shen HB. Epidemiologic differences in esophageal cancer between Asian and Western populations. Chin J Cancer. 2012;31:281–6.PubMedPubMedCentral
22.
go back to reference Tachimor Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y, et al. Supraclavicular node metastasis from thoracic esophageal carcinoma: A surgical series from a Japanese multi-institutional nationwide registry of esophageal cancer. J Thorac Cardiovasc Surg. 2014;148:1224–9. Tachimor Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y, et al. Supraclavicular node metastasis from thoracic esophageal carcinoma: A surgical series from a Japanese multi-institutional nationwide registry of esophageal cancer. J Thorac Cardiovasc Surg. 2014;148:1224–9.
23.
go back to reference Yang D, Sun Y, Hu L, Zheng H, Ji P, Pecot CV, et al. Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell. 2013;23:186–99.PubMedPubMedCentral Yang D, Sun Y, Hu L, Zheng H, Ji P, Pecot CV, et al. Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell. 2013;23:186–99.PubMedPubMedCentral
24.
go back to reference Mitra R, Chen X, Greenawalt EJ, Maulik U, Jiang W, Zhao Z, et al. Decoding critical long non-coding RNA in ovarian cancer epithelial-to-mesenchymal transition. Nat Commun. 2017;8:1604.PubMedPubMedCentral Mitra R, Chen X, Greenawalt EJ, Maulik U, Jiang W, Zhao Z, et al. Decoding critical long non-coding RNA in ovarian cancer epithelial-to-mesenchymal transition. Nat Commun. 2017;8:1604.PubMedPubMedCentral
25.
26.
go back to reference Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial–mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012;22:725–36.PubMedPubMedCentral Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial–mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012;22:725–36.PubMedPubMedCentral
27.
28.
go back to reference Bae YK, Choi JE, Kang SH, Lee SJ. Epithelial–mesenchymal transition phenotype is associated with clinicopathological factors that indicate aggressive biological behavior and poor clinical outcomes in invasive breast cancer. J Breast Cancer. 2015;18:256–63.PubMedPubMedCentral Bae YK, Choi JE, Kang SH, Lee SJ. Epithelial–mesenchymal transition phenotype is associated with clinicopathological factors that indicate aggressive biological behavior and poor clinical outcomes in invasive breast cancer. J Breast Cancer. 2015;18:256–63.PubMedPubMedCentral
29.
go back to reference Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265–73.PubMed Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265–73.PubMed
30.
go back to reference Taneyhill LA, Coles EG, Bronner-Fraser M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development. 2007;134:1481–90.PubMed Taneyhill LA, Coles EG, Bronner-Fraser M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development. 2007;134:1481–90.PubMed
31.
go back to reference Deep G, Jain AK, Ramteke A, Ting H, Vijendra KC, Gangar SC, et al. SNAI1 is critical for the aggressiveness of prostate cancer cells with low E-cadherin. Mol Cancer. 2014;13:37.PubMedPubMedCentral Deep G, Jain AK, Ramteke A, Ting H, Vijendra KC, Gangar SC, et al. SNAI1 is critical for the aggressiveness of prostate cancer cells with low E-cadherin. Mol Cancer. 2014;13:37.PubMedPubMedCentral
32.
go back to reference Campbell K, Whissell G, Franch-Marro X, Batlle E, Casanova J. Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev Cell. 2011;21:1051–61.PubMed Campbell K, Whissell G, Franch-Marro X, Batlle E, Casanova J. Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev Cell. 2011;21:1051–61.PubMed
33.
go back to reference Song K, Li Q, Jiang ZZ, Guo CW, Li P. Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3B1, a novel epithelial–mesenchymal transition inducer in pancreatic cancer. Cancer Biol Ther. 2011;12:388–98.PubMed Song K, Li Q, Jiang ZZ, Guo CW, Li P. Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3B1, a novel epithelial–mesenchymal transition inducer in pancreatic cancer. Cancer Biol Ther. 2011;12:388–98.PubMed
34.
go back to reference Radisky ES, Radisky DC. Matrix metalloproteinase-induced epithelial–mesenchymal transition in breast cancer. J Mammary Gland Biol Neoplasia. 2010;1:201–12. Radisky ES, Radisky DC. Matrix metalloproteinase-induced epithelial–mesenchymal transition in breast cancer. J Mammary Gland Biol Neoplasia. 2010;1:201–12.
35.
go back to reference Ke P, Wu ZD, Wen HS, Ying MX, Long HC, Qing LG. Current evidence on associations between the MMP-7 (-181A%3eG) polymorphism and digestive system cancer risk. Asian Pac J Cancer Rev. 2013;14:2269–72. Ke P, Wu ZD, Wen HS, Ying MX, Long HC, Qing LG. Current evidence on associations between the MMP-7 (-181A%3eG) polymorphism and digestive system cancer risk. Asian Pac J Cancer Rev. 2013;14:2269–72.
36.
go back to reference Brabletz T, Jung A, Hermann K, Günther K, Hohenberger W, Kirchner T. Nuclear overexpression of the oncoprotein β-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract. 1998;194:701–4.PubMed Brabletz T, Jung A, Hermann K, Günther K, Hohenberger W, Kirchner T. Nuclear overexpression of the oncoprotein β-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract. 1998;194:701–4.PubMed
37.
go back to reference Williams ED, Gao D, Redfern A, Thompson EW. Controversies around epithelial–mesenchymal plasticity in cancer metastasis. Nat Rev Cancer. 2019;19:716–32.PubMedPubMedCentral Williams ED, Gao D, Redfern A, Thompson EW. Controversies around epithelial–mesenchymal plasticity in cancer metastasis. Nat Rev Cancer. 2019;19:716–32.PubMedPubMedCentral
38.
39.
go back to reference Gener P, Seras-Franzoso J, Callejo PG, Andrade F, Rafael D, Martínez F, et al. Dynamism, sensitivity, and consequences of mesenchymal and stem-like phenotype of cancer cells. Stem Cells Int. 2018;2018:4516454.PubMedPubMedCentral Gener P, Seras-Franzoso J, Callejo PG, Andrade F, Rafael D, Martínez F, et al. Dynamism, sensitivity, and consequences of mesenchymal and stem-like phenotype of cancer cells. Stem Cells Int. 2018;2018:4516454.PubMedPubMedCentral
40.
go back to reference Chin VL, Lim CL. Epithelial–mesenchymal plasticity—engaging stemness in an interplay of phenotypes. Stem Cell Investig. 2019;6:25.PubMedPubMedCentral Chin VL, Lim CL. Epithelial–mesenchymal plasticity—engaging stemness in an interplay of phenotypes. Stem Cell Investig. 2019;6:25.PubMedPubMedCentral
41.
go back to reference Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580–4.PubMedPubMedCentral Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580–4.PubMedPubMedCentral
42.
go back to reference Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–15.PubMedPubMedCentral Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–15.PubMedPubMedCentral
43.
go back to reference Nishiyama M, Tsunedomi R, Yoshimura K, Hashimoto N, Matsukuma S, Ogihara H, et al. Metastatic ability and the epithelial–mesenchymal transition in induced cancer stem-like hepatoma cells. Cancer Sci. 2018;109:1101–9.PubMedPubMedCentral Nishiyama M, Tsunedomi R, Yoshimura K, Hashimoto N, Matsukuma S, Ogihara H, et al. Metastatic ability and the epithelial–mesenchymal transition in induced cancer stem-like hepatoma cells. Cancer Sci. 2018;109:1101–9.PubMedPubMedCentral
44.
go back to reference Grosse-Wilde A, Fouquier d'Hérouël A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, et al. Stemness of the hybrid epithelial/mesenchymal state in breast cancer and its association with poor survival. PLoS ONE. 2015;10:e0126522.PubMedPubMedCentral Grosse-Wilde A, Fouquier d'Hérouël A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, et al. Stemness of the hybrid epithelial/mesenchymal state in breast cancer and its association with poor survival. PLoS ONE. 2015;10:e0126522.PubMedPubMedCentral
45.
go back to reference Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, et al. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology. 2007;133:937–50.PubMed Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, et al. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology. 2007;133:937–50.PubMed
46.
go back to reference Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.PubMed Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.PubMed
47.
go back to reference Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells—perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339–444.PubMed Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells—perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339–444.PubMed
48.
go back to reference Szakács G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov. 2006;5:219–34.PubMed Szakács G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov. 2006;5:219–34.PubMed
49.
go back to reference Sukowati CHC, Rosso N, Crocè LS, Tiribelli C. Hepatic cancer stem cells and drug resistance: relevance in targeted therapies for hepatocellular carcinoma. World J Hepatol. 2010;2:114–26.PubMedPubMedCentral Sukowati CHC, Rosso N, Crocè LS, Tiribelli C. Hepatic cancer stem cells and drug resistance: relevance in targeted therapies for hepatocellular carcinoma. World J Hepatol. 2010;2:114–26.PubMedPubMedCentral
50.
go back to reference Gillet JP, Gottesman MM. Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer. Curr Pharm Biotechnol. 2011;12:686–92.PubMedPubMedCentral Gillet JP, Gottesman MM. Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer. Curr Pharm Biotechnol. 2011;12:686–92.PubMedPubMedCentral
51.
go back to reference Hashimoto N, Tsunedomi R, Yoshimura K, Watanabe Y, Hazama S, Oka M. Cancer stem-like sphere cells induced from de-differentiated hepatocellular carcinoma-derived cell lines possess the resistance to anti-cancer drugs. BMC Cancer. 2014;14:722.PubMedPubMedCentral Hashimoto N, Tsunedomi R, Yoshimura K, Watanabe Y, Hazama S, Oka M. Cancer stem-like sphere cells induced from de-differentiated hepatocellular carcinoma-derived cell lines possess the resistance to anti-cancer drugs. BMC Cancer. 2014;14:722.PubMedPubMedCentral
52.
go back to reference Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med. 2002;53:615–27.PubMed Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med. 2002;53:615–27.PubMed
53.
go back to reference Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012;10:717–28.PubMed Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012;10:717–28.PubMed
54.
go back to reference Gilbertson RJ, Rich JN. Making a tumour’s bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer. 2007;7:733–6.PubMed Gilbertson RJ, Rich JN. Making a tumour’s bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer. 2007;7:733–6.PubMed
55.
go back to reference Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.PubMed Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.PubMed
56.
go back to reference Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917–20.PubMed Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917–20.PubMed
57.
go back to reference Palk IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141–6. Palk IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141–6.
58.
go back to reference Plaks V, Koopman CD, Werb Z. Cancer. Circulating tumor cells. Science. 2013;341:1186–8.PubMed Plaks V, Koopman CD, Werb Z. Cancer. Circulating tumor cells. Science. 2013;341:1186–8.PubMed
59.
go back to reference Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14:275–91.PubMed Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14:275–91.PubMed
60.
go back to reference Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, et al. Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol. 2015;12:445–64.PubMedPubMedCentral Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, et al. Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol. 2015;12:445–64.PubMedPubMedCentral
61.
go back to reference Zhou L, Yu L, Zhu B, Wu S, Song W, Gong X, et al. Metastasis-associated in colon cancer-1 and aldehyde dehydrogenase 1 are metastatic and prognostic biomarker for non-small cell lung cancer. BMC Cancer. 2016;16:876.PubMedPubMedCentral Zhou L, Yu L, Zhu B, Wu S, Song W, Gong X, et al. Metastasis-associated in colon cancer-1 and aldehyde dehydrogenase 1 are metastatic and prognostic biomarker for non-small cell lung cancer. BMC Cancer. 2016;16:876.PubMedPubMedCentral
62.
go back to reference Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005;65:5506–11.PubMed Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005;65:5506–11.PubMed
63.
go back to reference Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev. 2008;18:48–53.PubMed Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev. 2008;18:48–53.PubMed
64.
go back to reference Polytarchou C, Iliopoulos D, Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. PNAS USA. 2012;109:14470–5.PubMedPubMedCentral Polytarchou C, Iliopoulos D, Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. PNAS USA. 2012;109:14470–5.PubMedPubMedCentral
65.
go back to reference Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, Xu Y, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology. 2012;56:1004–14.PubMed Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, Xu Y, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology. 2012;56:1004–14.PubMed
66.
go back to reference Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-κB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nat commun. 2013;4:2299.PubMed Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-κB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nat commun. 2013;4:2299.PubMed
67.
go back to reference Infanger DW, Cho Y, Lopez BS, Mohanan S, Liu SC, Gursel D, et al. perivascular niche. Cancer Res. 2013;73:7079–89.PubMed Infanger DW, Cho Y, Lopez BS, Mohanan S, Liu SC, Gursel D, et al. perivascular niche. Cancer Res. 2013;73:7079–89.PubMed
68.
go back to reference Lawson DA, Bhakta NR, Kessenbrock K, Prummel KD, Yu Y, Takai K, et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature. 2015;526:131–5.PubMedPubMedCentral Lawson DA, Bhakta NR, Kessenbrock K, Prummel KD, Yu Y, Takai K, et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature. 2015;526:131–5.PubMedPubMedCentral
69.
go back to reference Matsukuma S, Yoshimura K, Ueno T, Oga A, Inoue M, Watanabe Y, et al. Calreticulin is highly expressed in pancreatic cancer stem-like cells. Cancer Sci. 2016;107:1599–609.PubMedPubMedCentral Matsukuma S, Yoshimura K, Ueno T, Oga A, Inoue M, Watanabe Y, et al. Calreticulin is highly expressed in pancreatic cancer stem-like cells. Cancer Sci. 2016;107:1599–609.PubMedPubMedCentral
70.
go back to reference Yang L, Ping YF, Yu X, Qian F, Guo ZJ, Qian C, et al. Gastric cancer stem-like cells possess higher capability of invasion and metastasis in association with a mesenchymal transition phenotype. Cancer Lett. 2011;310:46–52.PubMed Yang L, Ping YF, Yu X, Qian F, Guo ZJ, Qian C, et al. Gastric cancer stem-like cells possess higher capability of invasion and metastasis in association with a mesenchymal transition phenotype. Cancer Lett. 2011;310:46–52.PubMed
71.
go back to reference Yu SC, Bian XW. Enrichment of cancer stem cells based on heterogeneity of invasiveness. Stem Cell Rev. 2009;5:66–71. Yu SC, Bian XW. Enrichment of cancer stem cells based on heterogeneity of invasiveness. Stem Cell Rev. 2009;5:66–71.
72.
go back to reference Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J Immunol. 2012;189:444–53.PubMed Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J Immunol. 2012;189:444–53.PubMed
73.
go back to reference Watanabe Y, Yoshimura K, Yoshikawa K, Tsunedomi R, Shindo Y, Matsukuma S, et al. A stem cell medium containing neural stimulating factor induces a pancreatic cancer stem-like cell-enriched population. Int J Oncol. 2014;45:1857–66.PubMedPubMedCentral Watanabe Y, Yoshimura K, Yoshikawa K, Tsunedomi R, Shindo Y, Matsukuma S, et al. A stem cell medium containing neural stimulating factor induces a pancreatic cancer stem-like cell-enriched population. Int J Oncol. 2014;45:1857–66.PubMedPubMedCentral
74.
go back to reference Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer. 2008;99:1285–9.PubMedPubMedCentral Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer. 2008;99:1285–9.PubMedPubMedCentral
75.
go back to reference Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009;27:844–50.PubMed Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009;27:844–50.PubMed
76.
go back to reference Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, et al. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer. 2010;103:382–90.PubMedPubMedCentral Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, et al. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer. 2010;103:382–90.PubMedPubMedCentral
77.
go back to reference Voglar T, Kriegl L, Horst D, Engel J, Sagebiel S, Schäffauer AJ, et al. The expression pattern of aldehyde dehydrogenase 1 (ALDH1) is an independent prognostic marker for low survival in colorectal tumors. Exp Mol Pathol. 2012;92:111–7. Voglar T, Kriegl L, Horst D, Engel J, Sagebiel S, Schäffauer AJ, et al. The expression pattern of aldehyde dehydrogenase 1 (ALDH1) is an independent prognostic marker for low survival in colorectal tumors. Exp Mol Pathol. 2012;92:111–7.
78.
go back to reference Saito S, Okabe H, Watanabe M, Ishimoto T, Iwatsuki M, Baba Y, et al. CD44v6 expression is related to mesenchymal phenotype and poor prognosis in patients with colorectal cancer. Oncol Rep. 2013;29:1570–8.PubMed Saito S, Okabe H, Watanabe M, Ishimoto T, Iwatsuki M, Baba Y, et al. CD44v6 expression is related to mesenchymal phenotype and poor prognosis in patients with colorectal cancer. Oncol Rep. 2013;29:1570–8.PubMed
79.
go back to reference Goossens-Beumer IJ, Zeestraten EC, Benard A, Christen T, Reimers MS, Keijzer R, et al. Clinical prognostic value of combined analysis of Aldh1, Survivin, and EpCAM expression in colorectal cancer. Br J Cancer. 2014;110:2935–44.PubMedPubMedCentral Goossens-Beumer IJ, Zeestraten EC, Benard A, Christen T, Reimers MS, Keijzer R, et al. Clinical prognostic value of combined analysis of Aldh1, Survivin, and EpCAM expression in colorectal cancer. Br J Cancer. 2014;110:2935–44.PubMedPubMedCentral
80.
go back to reference Ong CE, Chong PY, McArt DG, Chan JY, Tan HT, Kumar AP, et al. The prognostic value of the stem-like group in colorectal cancer using a panel of immunohistochemistry markers. Oncotarget. 2015;6:12763–73.PubMedPubMedCentral Ong CE, Chong PY, McArt DG, Chan JY, Tan HT, Kumar AP, et al. The prognostic value of the stem-like group in colorectal cancer using a panel of immunohistochemistry markers. Oncotarget. 2015;6:12763–73.PubMedPubMedCentral
81.
go back to reference Yin Ah, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 1997;90:5002–12.PubMed Yin Ah, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 1997;90:5002–12.PubMed
82.
go back to reference Weigman A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA. 1997;94:12425–300. Weigman A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA. 1997;94:12425–300.
83.
go back to reference Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med. 2008;86:1025–32.PubMed Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med. 2008;86:1025–32.PubMed
84.
go back to reference Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.PubMed Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.PubMed
85.
go back to reference Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–8.PubMed Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–8.PubMed
86.
go back to reference Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–51.PubMed Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–51.PubMed
87.
go back to reference Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus MC, Cantino D, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol. 2005;166:545–55.PubMedPubMedCentral Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus MC, Cantino D, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol. 2005;166:545–55.PubMedPubMedCentral
88.
go back to reference Florek M, Haase M, Marzesco AM, Freund D, Ehninger G, Huttner WB, et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 2005;319:15–26.PubMed Florek M, Haase M, Marzesco AM, Freund D, Ehninger G, Huttner WB, et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 2005;319:15–26.PubMed
89.
go back to reference Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–4.PubMed Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–4.PubMed
90.
go back to reference Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–55.PubMed Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–55.PubMed
91.
go back to reference O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10.PubMed O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10.PubMed
92.
go back to reference Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007;120:1444–500.PubMed Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007;120:1444–500.PubMed
93.
go back to reference Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132:2542–56.PubMed Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132:2542–56.PubMed
94.
go back to reference Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ, Tahan SR. Increased expression of stem cell markers in malignant melanoma. Mod Pathol. 2007;20:102–7.PubMed Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ, Tahan SR. Increased expression of stem cell markers in malignant melanoma. Mod Pathol. 2007;20:102–7.PubMed
95.
go back to reference Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer. 2007;43:935–46.PubMed Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer. 2007;43:935–46.PubMed
96.
go back to reference Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008;14:123–9.PubMed Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008;14:123–9.PubMed
97.
go back to reference Mizrak D, Brittan M, Alison M. CD133: molecule of the moment. J Pathol. 2008;214:3–9.PubMed Mizrak D, Brittan M, Alison M. CD133: molecule of the moment. J Pathol. 2008;214:3–9.PubMed
98.
go back to reference Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer. 2008;18:506–14.PubMed Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer. 2008;18:506–14.PubMed
99.
go back to reference Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504–14.PubMed Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504–14.PubMed
100.
go back to reference Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J. CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol. 2012;25:456–64.PubMed Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J. CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol. 2012;25:456–64.PubMed
101.
go back to reference Li CY, Li BX, Liang Y, Peng RQ, Ding Y, Xu DZ, et al. Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009;7:56.PubMedPubMedCentral Li CY, Li BX, Liang Y, Peng RQ, Ding Y, Xu DZ, et al. Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009;7:56.PubMedPubMedCentral
102.
go back to reference Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457:603–7.PubMed Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457:603–7.PubMed
103.
go back to reference Tirino V, Camerlingo R, Franco R, Malanga D, La Rocca A, Viglietto G, et al. The role of CD133 in the identification and characterisation of tumour-initiating cells in non-small-cell lung cancer. Eur J Cardiothorac Surg. 2009;36:446–53.PubMed Tirino V, Camerlingo R, Franco R, Malanga D, La Rocca A, Viglietto G, et al. The role of CD133 in the identification and characterisation of tumour-initiating cells in non-small-cell lung cancer. Eur J Cardiothorac Surg. 2009;36:446–53.PubMed
104.
go back to reference Zhang DG, Jiang AG, Lu HY, Zhang LX, Gao XY. Isolation, cultivation and identification of human lung adenocarcinoma stem cells. Oncol Lett. 2015;9:47–544.PubMed Zhang DG, Jiang AG, Lu HY, Zhang LX, Gao XY. Isolation, cultivation and identification of human lung adenocarcinoma stem cells. Oncol Lett. 2015;9:47–544.PubMed
105.
go back to reference Mia-Jan K, Jung SY, Kim IY, Oh SS, Choi E, Chang SJ, et al. CD133 expression is not an independent prognostic factor in stage II and III colorectal cancer but may predict the better outcome in patients with adjuvant therapy. BMC Cancer. 2013;13:166.PubMedPubMedCentral Mia-Jan K, Jung SY, Kim IY, Oh SS, Choi E, Chang SJ, et al. CD133 expression is not an independent prognostic factor in stage II and III colorectal cancer but may predict the better outcome in patients with adjuvant therapy. BMC Cancer. 2013;13:166.PubMedPubMedCentral
106.
go back to reference Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313–23.PubMed Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313–23.PubMed
107.
go back to reference Iseki Y, Shibutani M, Maeda K, Nagahara H, Ikeya T, Hirakawa K. Significance of E-cadherin and CD44 expression in patients with unresectable metastatic colorectal cancer. Oncol Lett. 2017;14:1025–34.PubMedPubMedCentral Iseki Y, Shibutani M, Maeda K, Nagahara H, Ikeya T, Hirakawa K. Significance of E-cadherin and CD44 expression in patients with unresectable metastatic colorectal cancer. Oncol Lett. 2017;14:1025–34.PubMedPubMedCentral
108.
go back to reference Wu Q, Yang Y, Wu S, Li W, Zhang N, Dong X, et al. Evaluation of the correlation of KAI1/CD82, CD44, MMP7 and β-catenin in the prediction of prognosis and metastasis in colorectal carcinoma. Diagn Pathol. 2015;10:176.PubMedPubMedCentral Wu Q, Yang Y, Wu S, Li W, Zhang N, Dong X, et al. Evaluation of the correlation of KAI1/CD82, CD44, MMP7 and β-catenin in the prediction of prognosis and metastasis in colorectal carcinoma. Diagn Pathol. 2015;10:176.PubMedPubMedCentral
109.
go back to reference Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. CD133+CD54+CD44+ circulating tumor cells as a biomarker of treatment selection and liver metastasis in patients with colorectal cancer. Oncotarget. 2016;7:77389–403.PubMedPubMedCentral Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. CD133+CD54+CD44+ circulating tumor cells as a biomarker of treatment selection and liver metastasis in patients with colorectal cancer. Oncotarget. 2016;7:77389–403.PubMedPubMedCentral
110.
go back to reference Choi SL, Kim SY, Lee JH, Kim JY, Cho EW, Kim IG. Osteopontin production by TM4SF4 signaling drives a positive feedback autocrine loop with the STAT3 pathway to maintain cancer stem cell-like properties in lung cancer cells. Oncotarget. 2017;8:101284–97.PubMedPubMedCentral Choi SL, Kim SY, Lee JH, Kim JY, Cho EW, Kim IG. Osteopontin production by TM4SF4 signaling drives a positive feedback autocrine loop with the STAT3 pathway to maintain cancer stem cell-like properties in lung cancer cells. Oncotarget. 2017;8:101284–97.PubMedPubMedCentral
111.
go back to reference Wang HH, Liao CC, Chow NH, Huang LL, Chuang JI, Wei KC, et al. Whether CD44 is an applicable marker for glioma stem cells. Am J Transl Res. 2017;9:4785–806.PubMedPubMedCentral Wang HH, Liao CC, Chow NH, Huang LL, Chuang JI, Wei KC, et al. Whether CD44 is an applicable marker for glioma stem cells. Am J Transl Res. 2017;9:4785–806.PubMedPubMedCentral
112.
go back to reference Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci. 2007;104:10158–63.PubMedPubMedCentral Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci. 2007;104:10158–63.PubMedPubMedCentral
113.
go back to reference Ishimot T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell. 2011;19:387–400. Ishimot T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell. 2011;19:387–400.
114.
go back to reference Nagano O, Okazaki S, Saya H. Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene. 2013;32:5191–8.PubMed Nagano O, Okazaki S, Saya H. Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene. 2013;32:5191–8.PubMed
115.
go back to reference Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, Haussmann I, et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell. 1991;65:13–24.PubMed Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, Haussmann I, et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell. 1991;65:13–24.PubMed
116.
go back to reference Yu Q, Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 1999;13:35–48.PubMedPubMedCentral Yu Q, Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 1999;13:35–48.PubMedPubMedCentral
117.
go back to reference Uchino M, Kojima H, Wada K, Imada M, Onoda F, Satofuka H, et al. Nuclear beta-catenin and CD44 upregulation characterize invasive cell populations in non-aggressive MCF-7 breast cancer cells. BMC Cancer. 2010;10:414.PubMedPubMedCentral Uchino M, Kojima H, Wada K, Imada M, Onoda F, Satofuka H, et al. Nuclear beta-catenin and CD44 upregulation characterize invasive cell populations in non-aggressive MCF-7 breast cancer cells. BMC Cancer. 2010;10:414.PubMedPubMedCentral
118.
go back to reference Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, et al. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial–mesenchymal transition and breast cancer progression. J Clin Invest. 2011;121:1064–74.PubMedPubMedCentral Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, et al. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial–mesenchymal transition and breast cancer progression. J Clin Invest. 2011;121:1064–74.PubMedPubMedCentral
119.
go back to reference Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMed Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMed
120.
go back to reference Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J. 2006;20:1045–54.PubMed Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J. 2006;20:1045–54.PubMed
121.
go back to reference Dan YY, Riehle KJ, Lazaro C, Teoh N, Haque J, Campbell JS, et al. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci USA. 2006;103:9912–7.PubMedPubMedCentral Dan YY, Riehle KJ, Lazaro C, Teoh N, Haque J, Campbell JS, et al. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci USA. 2006;103:9912–7.PubMedPubMedCentral
122.
go back to reference Masson NM, Currie IS, Terrace JD, Garden OJ, Parks RW, Ross JA. Hepatic progenitor cells in human fetal liver express the oval cell marker Thy-1. Am J Physiol Gastrointest Liver Physiol. 2006;291:G45–54.PubMed Masson NM, Currie IS, Terrace JD, Garden OJ, Parks RW, Ross JA. Hepatic progenitor cells in human fetal liver express the oval cell marker Thy-1. Am J Physiol Gastrointest Liver Physiol. 2006;291:G45–54.PubMed
123.
go back to reference Yang ZF, Ngai P, Ho DW, Yu WC, Ng MN, Lau CK, et al. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology. 2008;47:919–28.PubMed Yang ZF, Ngai P, Ho DW, Yu WC, Ng MN, Lau CK, et al. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology. 2008;47:919–28.PubMed
124.
go back to reference Cheng BQ, Jiang Y, Li DL, Fan JJ, Ma M. Up-regulation of thy-1 promotes invasion and metastasis of hepatocarcinomas. Asian Pac J Cancer Prev. 2012;13:1349–53.PubMed Cheng BQ, Jiang Y, Li DL, Fan JJ, Ma M. Up-regulation of thy-1 promotes invasion and metastasis of hepatocarcinomas. Asian Pac J Cancer Prev. 2012;13:1349–53.PubMed
125.
go back to reference Yamaoka R, Ishii T, Kawai T, Yasuchika K, Miyauchi Y, Kojima H, et al. CD90 expression in human intrahepatic cholangiocarcinoma is associated with lymph node metastasis and poor prognosis. J Surg Oncol. 2018;118:664–74.PubMed Yamaoka R, Ishii T, Kawai T, Yasuchika K, Miyauchi Y, Kojima H, et al. CD90 expression in human intrahepatic cholangiocarcinoma is associated with lymph node metastasis and poor prognosis. J Surg Oncol. 2018;118:664–74.PubMed
126.
go back to reference Balzar M, Briaire-de Bruijn IH, Rees-Bakker HA, Prins FA, Helfrich W, de Leij L, et al. Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol Cell Biol. 2001;21:2570–80.PubMedPubMedCentral Balzar M, Briaire-de Bruijn IH, Rees-Bakker HA, Prins FA, Helfrich W, de Leij L, et al. Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol Cell Biol. 2001;21:2570–80.PubMedPubMedCentral
128.
go back to reference Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol. 2009;11:162–71.PubMed Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol. 2009;11:162–71.PubMed
129.
go back to reference Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol. 2007;171:386–95.PubMedPubMedCentral Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol. 2007;171:386–95.PubMedPubMedCentral
130.
go back to reference Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136:1012–4.PubMed Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136:1012–4.PubMed
131.
go back to reference Moreb J, Schweder M, Suresh A, Zucali JR. Overexpression of the human aldehyde dehydrogenase class I results in increased resistance to 4-hydroperoxycyclophosphamide. Cancer Gene Ther. 1996;3:24–30.PubMed Moreb J, Schweder M, Suresh A, Zucali JR. Overexpression of the human aldehyde dehydrogenase class I results in increased resistance to 4-hydroperoxycyclophosphamide. Cancer Gene Ther. 1996;3:24–30.PubMed
132.
go back to reference Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl ACad Sci USA. 1999;96:9118–233.PubMedPubMedCentral Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl ACad Sci USA. 1999;96:9118–233.PubMedPubMedCentral
133.
go back to reference Balicki D. Moving forward in human mammary stem cell biology and breast cancer prognostication using ALDH1. Cell Stem Cell. 2007;1:485–7.PubMed Balicki D. Moving forward in human mammary stem cell biology and breast cancer prognostication using ALDH1. Cell Stem Cell. 2007;1:485–7.PubMed
134.
go back to reference Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.PubMedPubMedCentral Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.PubMedPubMedCentral
135.
go back to reference Corti S, Locatelli F, Papadimitriou D, Donadoni C, Salani S, Del Bo R, et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cell. 2006;24:975–85. Corti S, Locatelli F, Papadimitriou D, Donadoni C, Salani S, Del Bo R, et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cell. 2006;24:975–85.
136.
go back to reference Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, Hole N, et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells. 2004;22:1142–51.PubMed Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, Hole N, et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells. 2004;22:1142–51.PubMed
137.
go back to reference Hess DA, Wirthlin L, Craft TP, Herrbrich PE, Hohm SA, Lahey R, et al. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood. 2006;107:2162–9.PubMedPubMedCentral Hess DA, Wirthlin L, Craft TP, Herrbrich PE, Hohm SA, Lahey R, et al. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood. 2006;107:2162–9.PubMedPubMedCentral
138.
go back to reference Hess DA, Craft TP, Wirthlin L, Hohm S, Zhou P, Eades WC, et al. Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity. Stem Cell. 2008;26:611–20. Hess DA, Craft TP, Wirthlin L, Hohm S, Zhou P, Eades WC, et al. Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity. Stem Cell. 2008;26:611–20.
139.
go back to reference Fleischman AG. ALDH marks leukemia stem cell. Blood. 2012;119:3376–7.PubMed Fleischman AG. ALDH marks leukemia stem cell. Blood. 2012;119:3376–7.PubMed
140.
go back to reference Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res. 2009;15:4234–41.PubMed Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res. 2009;15:4234–41.PubMed
141.
go back to reference Nishikawa S, Konno M, Hamabe A, Hasegawa S, Kano Y, Ohta K, et al. Aldehyde dehydrogenase high gastric cancer stem cells are resistant to chemotherapy. Int J Oncol. 2013;42:1437–42.PubMed Nishikawa S, Konno M, Hamabe A, Hasegawa S, Kano Y, Ohta K, et al. Aldehyde dehydrogenase high gastric cancer stem cells are resistant to chemotherapy. Int J Oncol. 2013;42:1437–42.PubMed
142.
go back to reference Huang CP, Tsai MF, Chang TH, Tang WC, Chen SY, Lai HH, et al. ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett. 2013;328:144–51.PubMed Huang CP, Tsai MF, Chang TH, Tang WC, Chen SY, Lai HH, et al. ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett. 2013;328:144–51.PubMed
143.
go back to reference Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Cell. 2009;7:330–8. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Cell. 2009;7:330–8.
144.
go back to reference Zhang G, Ma L, Xie YK, Miao XB, Jin C. Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity. Mol Med Rep. 2012;6:519–24.PubMed Zhang G, Ma L, Xie YK, Miao XB, Jin C. Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity. Mol Med Rep. 2012;6:519–24.PubMed
145.
go back to reference Fujiwara D, Kato K, Nohara S, Iwanuma Y, Kajiyama Y. The usefulness of three-dimensional cell culture in induction of cancer stem cells from esophageal squamous cell carcinoma cell lines. Biochem Biophys Res Commun. 2013;434:773–8.PubMed Fujiwara D, Kato K, Nohara S, Iwanuma Y, Kajiyama Y. The usefulness of three-dimensional cell culture in induction of cancer stem cells from esophageal squamous cell carcinoma cell lines. Biochem Biophys Res Commun. 2013;434:773–8.PubMed
146.
go back to reference Yang L, Ren Y, Yu X, Qian F, Bian BS, Xiao HL, et al. ALDH1A1 defines invasive cancer stem-like cells and predicts poor prognosis in patients with esophageal squamous cell carcinoma. Mod Pathol. 2014;27:775–83.PubMed Yang L, Ren Y, Yu X, Qian F, Bian BS, Xiao HL, et al. ALDH1A1 defines invasive cancer stem-like cells and predicts poor prognosis in patients with esophageal squamous cell carcinoma. Mod Pathol. 2014;27:775–83.PubMed
147.
go back to reference Sarkar A, Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell. 2013;12:15–30.PubMedPubMedCentral Sarkar A, Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell. 2013;12:15–30.PubMedPubMedCentral
148.
go back to reference Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003;17:126–40.PubMedPubMedCentral Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003;17:126–40.PubMedPubMedCentral
149.
go back to reference Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMed Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMed
150.
go back to reference Li XL, Eishi Y, Bai YQ, Sakai H, Akiyama Y, Tani M, et al. Expression of the SRY-related HMG box protein SOX2 in human gastric carcinoma. Int J Oncol. 2004;24:257–63.PubMed Li XL, Eishi Y, Bai YQ, Sakai H, Akiyama Y, Tani M, et al. Expression of the SRY-related HMG box protein SOX2 in human gastric carcinoma. Int J Oncol. 2004;24:257–63.PubMed
151.
go back to reference Sanada Y, Yoshida K, Ohara M, Oeda M, Konishi K, Tsutani Y. Histopathologic evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas. 2006;32:164–70.PubMed Sanada Y, Yoshida K, Ohara M, Oeda M, Konishi K, Tsutani Y. Histopathologic evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas. 2006;32:164–70.PubMed
152.
go back to reference Forghanifard MM, Ardalan Khales S, Javdani-Mallak A, Rad A, Farshchian M, Abbaszadegan MR. Stemness state regulators SALL4 and SOX2 are involved in progression and invasiveness of esophageal squamous cell carcinoma. Med Oncol. 2014;31:922.PubMed Forghanifard MM, Ardalan Khales S, Javdani-Mallak A, Rad A, Farshchian M, Abbaszadegan MR. Stemness state regulators SALL4 and SOX2 are involved in progression and invasiveness of esophageal squamous cell carcinoma. Med Oncol. 2014;31:922.PubMed
153.
154.
go back to reference Han X, Fang X, Lou X, Hua D, Ding W, Foltz G, et al. Silencing SOX2 induced mesenchymal–epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS ONE. 2012;7:e41335.PubMedPubMedCentral Han X, Fang X, Lou X, Hua D, Ding W, Foltz G, et al. Silencing SOX2 induced mesenchymal–epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS ONE. 2012;7:e41335.PubMedPubMedCentral
155.
go back to reference Basu-Roy U, Seo E, Ramanathapuram L, Rapp TB, Perry JA, Orkin SH, et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene. 2012;31:2270–82.PubMed Basu-Roy U, Seo E, Ramanathapuram L, Rapp TB, Perry JA, Orkin SH, et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene. 2012;31:2270–82.PubMed
156.
go back to reference Lundberg IV, Edin S, Eklöf V, Öberg Å, Palmqvist R, Wikberg ML. SOX2 expression is associated with a cancer stem cell state and down-regulation of CDX2 in colorectal cancer. BMC Cancer. 2016;16:471.PubMedPubMedCentral Lundberg IV, Edin S, Eklöf V, Öberg Å, Palmqvist R, Wikberg ML. SOX2 expression is associated with a cancer stem cell state and down-regulation of CDX2 in colorectal cancer. BMC Cancer. 2016;16:471.PubMedPubMedCentral
157.
go back to reference Liu L, Liu C, Zhang Q, Shen J, Zhang H, Shan J, et al. SIRT1-mediated transcriptional regulation of SOX2 is important for self-renewal of liver cancer stem cells. Hepatology. 2016;64:814–27.PubMed Liu L, Liu C, Zhang Q, Shen J, Zhang H, Shan J, et al. SIRT1-mediated transcriptional regulation of SOX2 is important for self-renewal of liver cancer stem cells. Hepatology. 2016;64:814–27.PubMed
158.
go back to reference Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39:2195–214.PubMedPubMedCentral Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39:2195–214.PubMedPubMedCentral
159.
go back to reference Kadaja M, Keyes BE, Lin M, Pasolli HA, Genander M, Polak L, et al. SOX9: a stem cell transcriptional regulator of secreted niche signaling factors. Genes Dev. 2014;28:328–41.PubMedPubMedCentral Kadaja M, Keyes BE, Lin M, Pasolli HA, Genander M, Polak L, et al. SOX9: a stem cell transcriptional regulator of secreted niche signaling factors. Genes Dev. 2014;28:328–41.PubMedPubMedCentral
160.
go back to reference Bengochea A, de Souza MM, Lefrançois L, Le Roux E, Galy O, Chemin I, et al. Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer. 2008;99:143–50.PubMedPubMedCentral Bengochea A, de Souza MM, Lefrançois L, Le Roux E, Galy O, Chemin I, et al. Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer. 2008;99:143–50.PubMedPubMedCentral
161.
go back to reference Merle P, Kim M, Herrmann M, Gupte A, Lefrançois L, Califano S, et al. Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol. 2005;43:854–62.PubMed Merle P, Kim M, Herrmann M, Gupte A, Lefrançois L, Califano S, et al. Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol. 2005;43:854–62.PubMed
162.
go back to reference Higashihara T, Yoshitomi H, Nakata Y, Kagawa S, Takano S, Shimizu H, et al. Sex determining region y box 9 induces chemoresistance in pancreatic cancer cells by induction of putative cancer stem cell characteristics and its high expression predicts poor prognosis. Pancreas. 2017;46:1296–304.PubMed Higashihara T, Yoshitomi H, Nakata Y, Kagawa S, Takano S, Shimizu H, et al. Sex determining region y box 9 induces chemoresistance in pancreatic cancer cells by induction of putative cancer stem cell characteristics and its high expression predicts poor prognosis. Pancreas. 2017;46:1296–304.PubMed
163.
go back to reference Guo X, Xiong L, Sun T, Peng R, Zou L, Zhu H, et al. Expression features of SOX9 associate with tumor progression and poor prognosis of hepatocellular carcinoma. Diagn Pathol. 2012;7:44.PubMedPubMedCentral Guo X, Xiong L, Sun T, Peng R, Zou L, Zhu H, et al. Expression features of SOX9 associate with tumor progression and poor prognosis of hepatocellular carcinoma. Diagn Pathol. 2012;7:44.PubMedPubMedCentral
164.
go back to reference Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012;148:1015–28.PubMedPubMedCentral Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012;148:1015–28.PubMedPubMedCentral
165.
go back to reference Santos JC, Carrasco-Garcia E, Garcia-Puga M, Aldaz P, Montes M, Fernandez-Reyes M, et al. SOX9 elevation acts with canonical WNT signaling to drive gastric cancer progression. Cancer Res. 2016;76:6735–46.PubMed Santos JC, Carrasco-Garcia E, Garcia-Puga M, Aldaz P, Montes M, Fernandez-Reyes M, et al. SOX9 elevation acts with canonical WNT signaling to drive gastric cancer progression. Cancer Res. 2016;76:6735–46.PubMed
166.
go back to reference Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.PubMed Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.PubMed
167.
go back to reference Brrker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009;457:608–11. Brrker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009;457:608–11.
168.
go back to reference Su S, Hong F, Liang Y, Zhou J, Liang Y, Chen K, et al. Lgr5 methylation in cancer stem cell differentiation and prognosis-prediction in colorectal cancer. PLoS ONE. 2015;10:e0143513.PubMedPubMedCentral Su S, Hong F, Liang Y, Zhou J, Liang Y, Chen K, et al. Lgr5 methylation in cancer stem cell differentiation and prognosis-prediction in colorectal cancer. PLoS ONE. 2015;10:e0143513.PubMedPubMedCentral
169.
go back to reference Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 2005;23:879–94.PubMed Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 2005;23:879–94.PubMed
170.
go back to reference Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, et al. CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer. 2008;98:1389–97.PubMedPubMedCentral Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, et al. CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer. 2008;98:1389–97.PubMedPubMedCentral
171.
go back to reference Li X, Zhao H, Gu J, Zheng L. Prognostic value of cancer stem cell marker CD133 expression in pancreatic ductal adenocarcinoma (PDAC): a systematic review and meta-analysis. Int J Clin Exp Pathol. 2015;8:12084–92.PubMedPubMedCentral Li X, Zhao H, Gu J, Zheng L. Prognostic value of cancer stem cell marker CD133 expression in pancreatic ductal adenocarcinoma (PDAC): a systematic review and meta-analysis. Int J Clin Exp Pathol. 2015;8:12084–92.PubMedPubMedCentral
172.
go back to reference Huang R, Mo D, Wu J, Ai H, Lu Y. CD133 expression correlates with clinicopathologic features and poor prognosis of colorectal cancer patients: an updated meta-analysis of 37 studies. Medicine. 2018;97:e10446.PubMedPubMedCentral Huang R, Mo D, Wu J, Ai H, Lu Y. CD133 expression correlates with clinicopathologic features and poor prognosis of colorectal cancer patients: an updated meta-analysis of 37 studies. Medicine. 2018;97:e10446.PubMedPubMedCentral
173.
go back to reference Nagata T, Sakakura C, Komiyama S, Miyashita A, Nishio M, Murayama Y, et al. Expression of cancer stem cell markers CD133 and CD44 in locoregional recurrence of rectal cancer. Anticancer Res. 2011;31:495–500.PubMed Nagata T, Sakakura C, Komiyama S, Miyashita A, Nishio M, Murayama Y, et al. Expression of cancer stem cell markers CD133 and CD44 in locoregional recurrence of rectal cancer. Anticancer Res. 2011;31:495–500.PubMed
174.
go back to reference Zhong C, Wu JD, Fang MM, Pu LY. Clinicopathological significance and prognostic value of the expression of the cancer stem cell marker CD133 in hepatocellular carcinoma: a meta-analysis. Tumour Biol. 2015;36:7623–30.PubMed Zhong C, Wu JD, Fang MM, Pu LY. Clinicopathological significance and prognostic value of the expression of the cancer stem cell marker CD133 in hepatocellular carcinoma: a meta-analysis. Tumour Biol. 2015;36:7623–30.PubMed
175.
go back to reference Zhao Q, Zhou H, Liu Q, Cao Y, Wang G, Hu A, et al. Prognostic value of the expression of cancer stem cell-related markers CD133 and CD44 in hepatocellular carcinoma: From patients to patient-derived tumor xenograft models. Oncotarget. 2016;7:47431–43.PubMedPubMedCentral Zhao Q, Zhou H, Liu Q, Cao Y, Wang G, Hu A, et al. Prognostic value of the expression of cancer stem cell-related markers CD133 and CD44 in hepatocellular carcinoma: From patients to patient-derived tumor xenograft models. Oncotarget. 2016;7:47431–43.PubMedPubMedCentral
176.
go back to reference Chen YL, Lin PY, Ming YZ, Huang WC, Chen RF, Chen PM, et al. The effects of the location of cancer stem cell marker CD133 on the prognosis of hepatocellular carcinoma patients. BMC Cancer. 2017;17:474.PubMedPubMedCentral Chen YL, Lin PY, Ming YZ, Huang WC, Chen RF, Chen PM, et al. The effects of the location of cancer stem cell marker CD133 on the prognosis of hepatocellular carcinoma patients. BMC Cancer. 2017;17:474.PubMedPubMedCentral
177.
go back to reference Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, et al. Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS ONE. 2013;8:e59154.PubMedPubMedCentral Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, et al. Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS ONE. 2013;8:e59154.PubMedPubMedCentral
178.
go back to reference Yiming L, Yunshan G, Bo M, Yu Z, Tao W, Gengfang L, et al. CD133 overexpression correlates with clinicopathological features of gastric cancer patients and its impact on survival: a systematic review and meta-analysis. Oncotarget. 2015;6:42019–27.PubMedPubMedCentral Yiming L, Yunshan G, Bo M, Yu Z, Tao W, Gengfang L, et al. CD133 overexpression correlates with clinicopathological features of gastric cancer patients and its impact on survival: a systematic review and meta-analysis. Oncotarget. 2015;6:42019–27.PubMedPubMedCentral
179.
go back to reference Wang JH, Huang ST, Zhang L, Liu ZG, Liang RX, Jiang SW, et al. Combined prognostic value of the cancer stem cell markers CD47 and CD133 in esophageal squamous cell carcinoma. Cancer Med. 2019;8:1315–25.PubMedPubMedCentral Wang JH, Huang ST, Zhang L, Liu ZG, Liang RX, Jiang SW, et al. Combined prognostic value of the cancer stem cell markers CD47 and CD133 in esophageal squamous cell carcinoma. Cancer Med. 2019;8:1315–25.PubMedPubMedCentral
180.
go back to reference Leni A, Giuffrè G, Adamo V, Tuccari G. Prognostic impact of CD133 immunoexpression in node-negative invasive breast carcinomas. Anticancer Res. 2011;31:1315–20. Leni A, Giuffrè G, Adamo V, Tuccari G. Prognostic impact of CD133 immunoexpression in node-negative invasive breast carcinomas. Anticancer Res. 2011;31:1315–20.
181.
go back to reference Herpel E, Jensen K, Muley T, Warth A, Schnabel PA, Meister M, et al. The cancer stem cell antigens CD133, BCRP1/ABCG2 and CD117/c-KIT are not associated with prognosis in resected early-stage non-small cell lung cancer. Anticancer Res. 2011;31:4491–500.PubMed Herpel E, Jensen K, Muley T, Warth A, Schnabel PA, Meister M, et al. The cancer stem cell antigens CD133, BCRP1/ABCG2 and CD117/c-KIT are not associated with prognosis in resected early-stage non-small cell lung cancer. Anticancer Res. 2011;31:4491–500.PubMed
182.
go back to reference Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer. 2010;126:950–8.PubMed Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer. 2010;126:950–8.PubMed
183.
go back to reference Salnikov AV, Kusumawidjaja G, Rausch V, Bruns H, Gross W, Khamidjanov A, et al. Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter. Cancer Lett. 2009;275:185–93.PubMed Salnikov AV, Kusumawidjaja G, Rausch V, Bruns H, Gross W, Khamidjanov A, et al. Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter. Cancer Lett. 2009;275:185–93.PubMed
184.
go back to reference Guo Z, Li LQ, Jiang JH, Ou C, Zeng LX, Xiang BD, et al. Cancer stem cell markers correlate with early recurrence and survival in hepatocellular carcinoma. World J Gastroenterol. 2014;20:2098–106.PubMedPubMedCentral Guo Z, Li LQ, Jiang JH, Ou C, Zeng LX, Xiang BD, et al. Cancer stem cell markers correlate with early recurrence and survival in hepatocellular carcinoma. World J Gastroenterol. 2014;20:2098–106.PubMedPubMedCentral
185.
go back to reference Lu C, Xu F, Gu J, Yuan Y, Zhao G, Yu X, et al. Clinical and biological significance of stem-like CD133+ CXCR4+ cells in esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2015;150:386–95.PubMed Lu C, Xu F, Gu J, Yuan Y, Zhao G, Yu X, et al. Clinical and biological significance of stem-like CD133+ CXCR4+ cells in esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2015;150:386–95.PubMed
186.
go back to reference Immervoll H, Hoem D, Sakariassen PØ, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer. 2008;8:48.PubMedPubMedCentral Immervoll H, Hoem D, Sakariassen PØ, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer. 2008;8:48.PubMedPubMedCentral
187.
go back to reference Okamoto H, Fujishima F, Nakamura Y, Zuguchi M, Ozawa Y, Takahashi Y, et al. Significance of CD133 expression in esophageal squamous cell carcinoma. World J Surg Oncol. 2013;11:51.PubMedPubMedCentral Okamoto H, Fujishima F, Nakamura Y, Zuguchi M, Ozawa Y, Takahashi Y, et al. Significance of CD133 expression in esophageal squamous cell carcinoma. World J Surg Oncol. 2013;11:51.PubMedPubMedCentral
188.
go back to reference Fan L, He F, Liu H, Zhu J, Liu Y, Yin Z, et al. CD133: a potential indicator for differentiation and prognosis of human cholangiocarcinoma. BMC Cancer. 2011;11:320.PubMedPubMedCentral Fan L, He F, Liu H, Zhu J, Liu Y, Yin Z, et al. CD133: a potential indicator for differentiation and prognosis of human cholangiocarcinoma. BMC Cancer. 2011;11:320.PubMedPubMedCentral
189.
go back to reference Nakajima TE, Yoshida H, Okamoto N, Nagashima K, Taniguchi H, Yamada Y, et al. Nucleostemin and TWIST as predictive markers for recurrence after neoadjuvant chemotherapy for esophageal carcinoma. Cancer Sci. 2012;103:233–8.PubMed Nakajima TE, Yoshida H, Okamoto N, Nagashima K, Taniguchi H, Yamada Y, et al. Nucleostemin and TWIST as predictive markers for recurrence after neoadjuvant chemotherapy for esophageal carcinoma. Cancer Sci. 2012;103:233–8.PubMed
190.
go back to reference Hang D, Dong HC, Ning T, Dong B, Hou DL, Xu WG. Prognostic value of the stem cell markers CD133 and ABCG2 expression in esophageal squamous cell carcinoma. Dis Esophagus. 2012;25:638–44.PubMed Hang D, Dong HC, Ning T, Dong B, Hou DL, Xu WG. Prognostic value of the stem cell markers CD133 and ABCG2 expression in esophageal squamous cell carcinoma. Dis Esophagus. 2012;25:638–44.PubMed
191.
go back to reference Gotoda T, Matsumura Y, Kondo H, Saitoh D, Shimada Y, Kosuge T, et al. Expression of CD44 variants and its association with survival in pancreatic cancer. Jpn J Cancer Res. 1998;89:1033–40.PubMedPubMedCentral Gotoda T, Matsumura Y, Kondo H, Saitoh D, Shimada Y, Kosuge T, et al. Expression of CD44 variants and its association with survival in pancreatic cancer. Jpn J Cancer Res. 1998;89:1033–40.PubMedPubMedCentral
192.
go back to reference Li XP, Zhang XW, Zheng LZ, Guo WJ. Expression of CD44 in pancreatic cancer and its significance. Int J Clin Exp Pathol. 2015;8:6724–31.PubMedPubMedCentral Li XP, Zhang XW, Zheng LZ, Guo WJ. Expression of CD44 in pancreatic cancer and its significance. Int J Clin Exp Pathol. 2015;8:6724–31.PubMedPubMedCentral
193.
go back to reference Liu Y, Wu T, Lu D, Zhen J, Zhang L. CD44 overexpression related to lymph node metastasis and poor prognosis of pancreatic cancer. Int J Biol Markers. 2018;33:308–13.PubMed Liu Y, Wu T, Lu D, Zhen J, Zhang L. CD44 overexpression related to lymph node metastasis and poor prognosis of pancreatic cancer. Int J Biol Markers. 2018;33:308–13.PubMed
194.
go back to reference Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, et al. CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 2012;72:3414–23.PubMed Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, et al. CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 2012;72:3414–23.PubMed
195.
go back to reference Kodama H, Murata S, Ishida M, Yamamoto H, Yamaguchi T, Kaida S, et al. Prognostic impact of CD44-positive cancer stem-like cells at the invasive front of gastric cancer. Br J Cancer. 2017;116:186–94.PubMed Kodama H, Murata S, Ishida M, Yamamoto H, Yamaguchi T, Kaida S, et al. Prognostic impact of CD44-positive cancer stem-like cells at the invasive front of gastric cancer. Br J Cancer. 2017;116:186–94.PubMed
196.
go back to reference Hu B, Luo W, Hu RT, Zhou Y, Qin SY, Jiang HX. Meta-analysis of prognostic and clinical significance of CD44v6 in esophageal cancer. Medicine. 2015;94:e1238.PubMedPubMedCentral Hu B, Luo W, Hu RT, Zhou Y, Qin SY, Jiang HX. Meta-analysis of prognostic and clinical significance of CD44v6 in esophageal cancer. Medicine. 2015;94:e1238.PubMedPubMedCentral
197.
go back to reference Fang M, Wu J, Lai X, Ai H, Tao Y, Zhu B, et al. CD44 and CD44v6 are correlated with gastric cancer progression and poor patient prognosis: evidence from 42 studies. Cell Physiol Biochem. 2016;40:567–78.PubMed Fang M, Wu J, Lai X, Ai H, Tao Y, Zhu B, et al. CD44 and CD44v6 are correlated with gastric cancer progression and poor patient prognosis: evidence from 42 studies. Cell Physiol Biochem. 2016;40:567–78.PubMed
198.
go back to reference Luo Y, Tan Y. Prognostic value of CD44 expression in patients with hepatocellular carcinoma: meta-analysis. Cancer Cell Int. 2016;16:47.PubMedPubMedCentral Luo Y, Tan Y. Prognostic value of CD44 expression in patients with hepatocellular carcinoma: meta-analysis. Cancer Cell Int. 2016;16:47.PubMedPubMedCentral
199.
go back to reference Wang Z, Tang Y, Xie L, Huang A, Xue C, Gu Z, et al. The prognostic and clinical value of CD44 in colorectal cancer: a meta-analysis. Front Oncol. 2019;9:309.PubMedPubMedCentral Wang Z, Tang Y, Xie L, Huang A, Xue C, Gu Z, et al. The prognostic and clinical value of CD44 in colorectal cancer: a meta-analysis. Front Oncol. 2019;9:309.PubMedPubMedCentral
200.
go back to reference Taniguchi D, Saeki H, Nakashima Y, Kudou K, Nakanishi R, Kubo N, et al. CD44v9 is associated with epithelial–mesenchymal transition and poor outcomes in esophageal squamous cell carcinoma. Cancer Med. 2018;7:6258–68.PubMedPubMedCentral Taniguchi D, Saeki H, Nakashima Y, Kudou K, Nakanishi R, Kubo N, et al. CD44v9 is associated with epithelial–mesenchymal transition and poor outcomes in esophageal squamous cell carcinoma. Cancer Med. 2018;7:6258–68.PubMedPubMedCentral
201.
go back to reference Songun I, Litvinov SV, van de Velde CJ, Pals ST, Hermans J, van Krieken JH. Loss of Ep-CAM (CO17-1A) expression predicts survival in patients with gastric cancer. Br J Cancer. 2005;92:1767–72.PubMedPubMedCentral Songun I, Litvinov SV, van de Velde CJ, Pals ST, Hermans J, van Krieken JH. Loss of Ep-CAM (CO17-1A) expression predicts survival in patients with gastric cancer. Br J Cancer. 2005;92:1767–72.PubMedPubMedCentral
202.
go back to reference Jing F, Kim HJ, Kim CH, Kim YJ, Lee JH, Kim HR. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int J Oncol. 2015;46:1582–8.PubMed Jing F, Kim HJ, Kim CH, Kim YJ, Lee JH, Kim HR. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int J Oncol. 2015;46:1582–8.PubMed
203.
go back to reference Horikawa M, Iinuma H, Inoue T, Ogawa E, Fukushima R. Clinical significance of intraperitoneal CD44 mRNA levels of magnetically separated CD45-negative EpCAM-positive cells for peritoneal recurrence and prognosis in stage II and III gastric cancer patients. Oncol Rep. 2011;25:1413–20.PubMed Horikawa M, Iinuma H, Inoue T, Ogawa E, Fukushima R. Clinical significance of intraperitoneal CD44 mRNA levels of magnetically separated CD45-negative EpCAM-positive cells for peritoneal recurrence and prognosis in stage II and III gastric cancer patients. Oncol Rep. 2011;25:1413–20.PubMed
204.
go back to reference Zhao RC, Zhou J, Chen KF, Gong J, Liu J, He JY, et al. The prognostic value of combination of CD90 and OCT4 for hepatocellular carcinoma after curative resection. Neoplasma. 2016;63:288–98.PubMed Zhao RC, Zhou J, Chen KF, Gong J, Liu J, He JY, et al. The prognostic value of combination of CD90 and OCT4 for hepatocellular carcinoma after curative resection. Neoplasma. 2016;63:288–98.PubMed
205.
go back to reference Zhou L, Zhu Y. The EpCAM overexpression is associated with clinicopathological significance and prognosis in hepatocellular carcinoma patients: a systematic review and meta-analysis. Int J Surg. 2018;56:274–80.PubMed Zhou L, Zhu Y. The EpCAM overexpression is associated with clinicopathological significance and prognosis in hepatocellular carcinoma patients: a systematic review and meta-analysis. Int J Surg. 2018;56:274–80.PubMed
206.
go back to reference Spizzo G, Went P, Dirnhofer S, Obrist P, Simon R, Spichtin H, et al. High Ep-CAM expression is associated with poor prognosis in node-positive breast cancer. Breast Cancer Res Treat. 2004;86:207–13.PubMed Spizzo G, Went P, Dirnhofer S, Obrist P, Simon R, Spichtin H, et al. High Ep-CAM expression is associated with poor prognosis in node-positive breast cancer. Breast Cancer Res Treat. 2004;86:207–13.PubMed
207.
go back to reference Eichelberg C, Chun FK, Bedke J, Heuer R, Adam M, Moch H, et al. Epithelial cell adhesion molecule is an independent prognostic marker in clear cell renal carcinoma. Int J Cancer. 2013;132:2948–55.PubMed Eichelberg C, Chun FK, Bedke J, Heuer R, Adam M, Moch H, et al. Epithelial cell adhesion molecule is an independent prognostic marker in clear cell renal carcinoma. Int J Cancer. 2013;132:2948–55.PubMed
208.
go back to reference Spizzo G, Went P, Dirnhofer S, Obrist P, Moch H, Baeuerle PA, et al. Overexpression of epithelial cell adhesion molecule (Ep-CAM) is an independent prognostic marker for reduced survival of patients with epithelial ovarian cancer. Gynecol Oncol. 2006;103:483–8.PubMed Spizzo G, Went P, Dirnhofer S, Obrist P, Moch H, Baeuerle PA, et al. Overexpression of epithelial cell adhesion molecule (Ep-CAM) is an independent prognostic marker for reduced survival of patients with epithelial ovarian cancer. Gynecol Oncol. 2006;103:483–8.PubMed
209.
go back to reference Prince S, Zeidman A, Dekel Y, Ram E, Koren R. Expression of epithelial cell adhesion molecule in gallbladder carcinoma and its correlation with clinicopathologic variables. Am J Clin Pathol. 2008;129:424–9.PubMed Prince S, Zeidman A, Dekel Y, Ram E, Koren R. Expression of epithelial cell adhesion molecule in gallbladder carcinoma and its correlation with clinicopathologic variables. Am J Clin Pathol. 2008;129:424–9.PubMed
210.
go back to reference Chen XL, Chen XZ, Wang YG, He D, Lu ZH, Liu K, et al. Clinical significance of putative markers of cancer stem cells in gastric cancer: A retrospective cohort study. Oncotarget. 2016;7:62049–69.PubMedPubMedCentral Chen XL, Chen XZ, Wang YG, He D, Lu ZH, Liu K, et al. Clinical significance of putative markers of cancer stem cells in gastric cancer: A retrospective cohort study. Oncotarget. 2016;7:62049–69.PubMedPubMedCentral
211.
go back to reference Han S, Zong S, Shi Q, Li H, Liu S, Yang W, et al. Is Ep-CAM expression a diagnostic and prognostic biomarker for colorectal cancer? A Systematic Meta-Analysis. EBioMedicine. 2017;20:61–9.PubMedPubMedCentral Han S, Zong S, Shi Q, Li H, Liu S, Yang W, et al. Is Ep-CAM expression a diagnostic and prognostic biomarker for colorectal cancer? A Systematic Meta-Analysis. EBioMedicine. 2017;20:61–9.PubMedPubMedCentral
212.
go back to reference Stoecklein NH, Siegmund A, Scheunemann P, Luebke AM, Erbersdobler A, Verde PE, et al. Ep-CAM expression in squamous cell carcinoma of the esophagus: a potential therapeutic target and prognostic marker. BMC Cancer. 2006;6:165.PubMedPubMedCentral Stoecklein NH, Siegmund A, Scheunemann P, Luebke AM, Erbersdobler A, Verde PE, et al. Ep-CAM expression in squamous cell carcinoma of the esophagus: a potential therapeutic target and prognostic marker. BMC Cancer. 2006;6:165.PubMedPubMedCentral
213.
go back to reference Kimura H, Kato H, Faried A, Sohda M, Nakajima M, Fukai Y, et al. Prognostic significance of EpCAM expression in human esophageal cancer. Int J Oncol. 2007;30:171–9.PubMed Kimura H, Kato H, Faried A, Sohda M, Nakajima M, Fukai Y, et al. Prognostic significance of EpCAM expression in human esophageal cancer. Int J Oncol. 2007;30:171–9.PubMed
214.
go back to reference Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, et al. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: a systematic review and meta-analysis. PLoS ONE. 2015;10:e0145164.PubMedPubMedCentral Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, et al. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: a systematic review and meta-analysis. PLoS ONE. 2015;10:e0145164.PubMedPubMedCentral
215.
go back to reference Chen MF, Chen PT, Lu MS, Chen WC. Role of ALDH1 in the prognosis of esophageal cancer and its relationship with tumor microenvironment. Mol Carcinog. 2018;57:78–88.PubMed Chen MF, Chen PT, Lu MS, Chen WC. Role of ALDH1 in the prognosis of esophageal cancer and its relationship with tumor microenvironment. Mol Carcinog. 2018;57:78–88.PubMed
216.
go back to reference Miller TJ, McCoy MJ, Hemmings C, Bulsara MK, Iacopetta B, Platell CF. The prognostic value of cancer stem-like cell markers SOX2 and CD133 in stage III colon cancer is modified by expression of the immune-related markers FoxP3, PD-L1 and CD3. Pathology. 2017;49:721–30.PubMed Miller TJ, McCoy MJ, Hemmings C, Bulsara MK, Iacopetta B, Platell CF. The prognostic value of cancer stem-like cell markers SOX2 and CD133 in stage III colon cancer is modified by expression of the immune-related markers FoxP3, PD-L1 and CD3. Pathology. 2017;49:721–30.PubMed
217.
go back to reference Takeda K, Mizushima T, Yokoyama Y, Hirose H, Wu X, Qian Y, et al. Sox2 is associated with cancer stem-like properties in colorectal cancer. Sci Rep. 2018;8:17639.PubMedPubMedCentral Takeda K, Mizushima T, Yokoyama Y, Hirose H, Wu X, Qian Y, et al. Sox2 is associated with cancer stem-like properties in colorectal cancer. Sci Rep. 2018;8:17639.PubMedPubMedCentral
219.
go back to reference Lundberg IV, Löfgren Burström A, Edin S, Eklöf V, Öberg Å, Stenling R, et al. SOX2 expression is regulated by BRAF and contributes to poor patient prognosis in colorectal cancer. PLoS ONE. 2014;9:e101957.PubMedPubMedCentral Lundberg IV, Löfgren Burström A, Edin S, Eklöf V, Öberg Å, Stenling R, et al. SOX2 expression is regulated by BRAF and contributes to poor patient prognosis in colorectal cancer. PLoS ONE. 2014;9:e101957.PubMedPubMedCentral
220.
go back to reference Luanpitpong S, Li J, Manke A, Brundage K, Ellis E, McLaughlin SL, et al. SLUG is required for SOX9 stabilization and functions to promote cancer stem cells and metastasis in human lung carcinoma. Oncogene. 2016;35:2824–33.PubMed Luanpitpong S, Li J, Manke A, Brundage K, Ellis E, McLaughlin SL, et al. SLUG is required for SOX9 stabilization and functions to promote cancer stem cells and metastasis in human lung carcinoma. Oncogene. 2016;35:2824–33.PubMed
221.
go back to reference Richtig G, Aigelsreiter A, Schwarzenbacher D, Ress AL, Adiprasito JB, Stiegelbauer V, et al. SOX9 is a proliferation and stem cell factor in hepatocellular carcinoma and possess widespread prognostic significance in different cancer types. PLoS ONE. 2017;12:e0187814.PubMedPubMedCentral Richtig G, Aigelsreiter A, Schwarzenbacher D, Ress AL, Adiprasito JB, Stiegelbauer V, et al. SOX9 is a proliferation and stem cell factor in hepatocellular carcinoma and possess widespread prognostic significance in different cancer types. PLoS ONE. 2017;12:e0187814.PubMedPubMedCentral
222.
go back to reference Raspaglio G, Petrillo M, Martinelli E, Li Puma DD, Mariani M, De Donato M, et al. Sox9 and Hif-2α regulate TUBB3 gene expression and affect ovarian cancer aggressiveness. Gene. 2014;542:173–81.PubMed Raspaglio G, Petrillo M, Martinelli E, Li Puma DD, Mariani M, De Donato M, et al. Sox9 and Hif-2α regulate TUBB3 gene expression and affect ovarian cancer aggressiveness. Gene. 2014;542:173–81.PubMed
223.
go back to reference Liu Z, Ren YA, Pangas SA, Adams J, Zhou W, Castrillon DH, et al. FOXO1/3 and PTEN depletion in granulosa cells promotes ovarian granulosa cell tumor development. Mol Endocrinol. 2015;29:1006–244.PubMedPubMedCentral Liu Z, Ren YA, Pangas SA, Adams J, Zhou W, Castrillon DH, et al. FOXO1/3 and PTEN depletion in granulosa cells promotes ovarian granulosa cell tumor development. Mol Endocrinol. 2015;29:1006–244.PubMedPubMedCentral
224.
go back to reference Kawai T, Yasuchika K, Ishii T, Miyauchi Y, Kojima H, Yamaoka R, et al. SOX9 is a novel cancer stem cell marker surrogated by osteopontin in human hepatocellular carcinoma. Sci Rep. 2016;6:30489.PubMedPubMedCentral Kawai T, Yasuchika K, Ishii T, Miyauchi Y, Kojima H, Yamaoka R, et al. SOX9 is a novel cancer stem cell marker surrogated by osteopontin in human hepatocellular carcinoma. Sci Rep. 2016;6:30489.PubMedPubMedCentral
225.
go back to reference Xue TC, Zhang L, Ren ZG, Chen RX, Cui JF, Ge NL, et al. Sex-determination gene SRY potentially associates with poor prognosis but not sex bias in hepatocellular carcinoma. Dig Dis Sci. 2015;60:427–35.PubMed Xue TC, Zhang L, Ren ZG, Chen RX, Cui JF, Ge NL, et al. Sex-determination gene SRY potentially associates with poor prognosis but not sex bias in hepatocellular carcinoma. Dig Dis Sci. 2015;60:427–35.PubMed
226.
go back to reference Lü B, Fang Y, Xu J, Wang L, Xu F, Xu E, et al. Analysis of SOX9 expression in colorectal cancer. Am J Clin Pathol. 2008;130:897–904.PubMed Lü B, Fang Y, Xu J, Wang L, Xu F, Xu E, et al. Analysis of SOX9 expression in colorectal cancer. Am J Clin Pathol. 2008;130:897–904.PubMed
227.
go back to reference Bruun J, Kolberg M, Nesland JM, Svindland A, Nesbakken A, Lothe RA. Prognostic Significance of β-Catenin, E-Cadherin, and SOX9 in colorectal cancer: results from a large population-representative series. Front Oncol. 2014;4:118.PubMedPubMedCentral Bruun J, Kolberg M, Nesland JM, Svindland A, Nesbakken A, Lothe RA. Prognostic Significance of β-Catenin, E-Cadherin, and SOX9 in colorectal cancer: results from a large population-representative series. Front Oncol. 2014;4:118.PubMedPubMedCentral
228.
go back to reference Mesquita P, Freire AF, Lopes N, Gomes R, Azevedo D, Barros R, et al. Expression and clinical relevance of SOX9 in gastric cancer. Dis Markers. 2019;2019:8267021.PubMedPubMedCentral Mesquita P, Freire AF, Lopes N, Gomes R, Azevedo D, Barros R, et al. Expression and clinical relevance of SOX9 in gastric cancer. Dis Markers. 2019;2019:8267021.PubMedPubMedCentral
229.
go back to reference Choi YJ, Song JH, Yoon JH, Choi WS, Nam SW, Lee JY, et al. Aberrant expression of SOX9 is associated with gastrokine 1 inactivation in gastric cancers. Gastric Cancer. 2014;17:247–54.PubMed Choi YJ, Song JH, Yoon JH, Choi WS, Nam SW, Lee JY, et al. Aberrant expression of SOX9 is associated with gastrokine 1 inactivation in gastric cancers. Gastric Cancer. 2014;17:247–54.PubMed
230.
go back to reference McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, et al. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther. 2006;5:419–26.PubMed McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, et al. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther. 2006;5:419–26.PubMed
231.
go back to reference Valladares-Ayerbes M, Blanco-Calvo M, Reboredo M, Lorenzo-Patiño MJ, Iglesias-Díaz P, Haz M, et al. Evaluation of the adenocarcinoma-associated gene AGR2 and the intestinal stem cell marker LGR5 as biomarkers in colorectal cancer. Int J Mol Sci. 2012;13:4367–87.PubMedPubMedCentral Valladares-Ayerbes M, Blanco-Calvo M, Reboredo M, Lorenzo-Patiño MJ, Iglesias-Díaz P, Haz M, et al. Evaluation of the adenocarcinoma-associated gene AGR2 and the intestinal stem cell marker LGR5 as biomarkers in colorectal cancer. Int J Mol Sci. 2012;13:4367–87.PubMedPubMedCentral
232.
go back to reference Liu Z, Dai W, Jiang L, Cheng Y. Over-expression of LGR5 correlates with poor survival of colon cancer in mice as well as in patients. Neoplasma. 2014;61:177–85.PubMed Liu Z, Dai W, Jiang L, Cheng Y. Over-expression of LGR5 correlates with poor survival of colon cancer in mice as well as in patients. Neoplasma. 2014;61:177–85.PubMed
233.
go back to reference Chen Q, Zhang X, Li WM, Ji YQ, Cao HZ, Zheng P. Prognostic value of LGR5 in colorectal cancer: a meta-analysis. PLoS ONE. 2014;9:e107013.PubMedPubMedCentral Chen Q, Zhang X, Li WM, Ji YQ, Cao HZ, Zheng P. Prognostic value of LGR5 in colorectal cancer: a meta-analysis. PLoS ONE. 2014;9:e107013.PubMedPubMedCentral
234.
go back to reference Jiang Y, Li W, He X, Zhang H, Jiang F, Chen Z. Lgr5 expression is a valuable prognostic factor for colorectal cancer: evidence from a meta-analysis. BMC Cancer. 2016;16:12.PubMedPubMedCentral Jiang Y, Li W, He X, Zhang H, Jiang F, Chen Z. Lgr5 expression is a valuable prognostic factor for colorectal cancer: evidence from a meta-analysis. BMC Cancer. 2016;16:12.PubMedPubMedCentral
235.
go back to reference Becker L, Huang Q, Mashimo H. Lgr5, an intestinal stem cell marker, is abnormally expressed in Barrett's esophagus and esophageal adenocarcinoma. Dis Esophagus. 2010;23:168–74.PubMed Becker L, Huang Q, Mashimo H. Lgr5, an intestinal stem cell marker, is abnormally expressed in Barrett's esophagus and esophageal adenocarcinoma. Dis Esophagus. 2010;23:168–74.PubMed
236.
go back to reference von Rahden BH, Kircher S, Lazariotou M, Reiber C, Stuermer L, Otto C, et al. LgR5 expression and cancer stem cell hypothesis: clue to define the true origin of esophageal adenocarcinomas with and without Barrett's esophagus? J Exp Clin Cancer Res. 2011;30:23. von Rahden BH, Kircher S, Lazariotou M, Reiber C, Stuermer L, Otto C, et al. LgR5 expression and cancer stem cell hypothesis: clue to define the true origin of esophageal adenocarcinomas with and without Barrett's esophagus? J Exp Clin Cancer Res. 2011;30:23.
237.
go back to reference Huang T, Qiu X, Xiao J, Wang Q, Wang Y, Zhang Y, et al. The prognostic role of Leucine-rich repeat-containing G-protein-coupled receptor 5 in gastric cancer: a systematic review with meta-analysis. Clin Res Hepatol Gastroenterol. 2016;40:246–53.PubMed Huang T, Qiu X, Xiao J, Wang Q, Wang Y, Zhang Y, et al. The prognostic role of Leucine-rich repeat-containing G-protein-coupled receptor 5 in gastric cancer: a systematic review with meta-analysis. Clin Res Hepatol Gastroenterol. 2016;40:246–53.PubMed
238.
go back to reference Jang BG, Lee BL, Kim WH. Prognostic significance of leucine-rich-repeat-containing G-protein-coupled receptor 5, an intestinal stem cell marker, in gastric carcinomas. Gastric Cancer. 2016;19:767–77.PubMed Jang BG, Lee BL, Kim WH. Prognostic significance of leucine-rich-repeat-containing G-protein-coupled receptor 5, an intestinal stem cell marker, in gastric carcinomas. Gastric Cancer. 2016;19:767–77.PubMed
239.
go back to reference Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer. 2009;9:274–84.PubMed Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer. 2009;9:274–84.PubMed
240.
go back to reference Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559–644.PubMed Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559–644.PubMed
241.
go back to reference Bahnassy AA, Zekri AR, El-Bastawisy A, Fawzy A, Shetta M, Hussein N, et al. Circulating tumor and cancer stem cells in hepatitis C virus-associated liver disease. World J Gastroenterol. 2014;20:18240–8.PubMedPubMedCentral Bahnassy AA, Zekri AR, El-Bastawisy A, Fawzy A, Shetta M, Hussein N, et al. Circulating tumor and cancer stem cells in hepatitis C virus-associated liver disease. World J Gastroenterol. 2014;20:18240–8.PubMedPubMedCentral
242.
go back to reference Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. Prognostic value of CD133+ CD54+ CD44+ circulating tumor cells in colorectal cancer with liver metastasis. Cancer Med. 2017;6:2850–7.PubMedPubMedCentral Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. Prognostic value of CD133+ CD54+ CD44+ circulating tumor cells in colorectal cancer with liver metastasis. Cancer Med. 2017;6:2850–7.PubMedPubMedCentral
243.
go back to reference Tanaka S. Precision medicine based on surgical oncology in the era of genome-scale analysis and genome editing technology. Ann Gastroenterol Surg. 2018;2:106–15.PubMedPubMedCentral Tanaka S. Precision medicine based on surgical oncology in the era of genome-scale analysis and genome editing technology. Ann Gastroenterol Surg. 2018;2:106–15.PubMedPubMedCentral
Metadata
Title
Clinical implications of cancer stem cells in digestive cancers: acquisition of stemness and prognostic impact
Authors
Ryouichi Tsunedomi
Kiyoshi Yoshimura
Nobuaki Suzuki
Shoichi Hazama
Hiroaki Nagano
Publication date
01-12-2020
Publisher
Springer Singapore
Keyword
Metastasis
Published in
Surgery Today / Issue 12/2020
Print ISSN: 0941-1291
Electronic ISSN: 1436-2813
DOI
https://doi.org/10.1007/s00595-020-01968-x

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