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Published in: Medical Oncology 9/2014

01-09-2014 | Review Article

Cancer stem cell detection and isolation

Authors: Meysam Moghbeli, Faezeh Moghbeli, Mohammad Mahdi Forghanifard, Mohammad Reza Abbaszadegan

Published in: Medical Oncology | Issue 9/2014

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Abstract

Only 10 % of cancer-related deaths result from primary tumors; most are caused by metastatic tumors. It is believed that the metastatic power of tumor cells is attributed to features of a stem cell-like subpopulation of tumor cells known as cancer stem cells (CSCs). Cancer stem cells are resistant to chemotherapeutic treatments and can induce dormancy in tumor cells for long periods. Detection, isolation, and characterization of CSCs in solid tumors are hallmarks of cancer-targeted therapies in recent years. There are inevitable similarities between normal and cancer stem cells; therefore, finding specific methods or markers to differentiate them is critical to cancer therapies. Considering CSCs involvement in tumor relapse and chemotherapeutic resistance, identification of such cells in tumors is imperative for effective targeted therapy. The present review introduces practical and specific protocols used to isolate CSCs from solid tumors from colon, esophagus, liver, breast, brain, and cervix.
Literature
1.
go back to reference Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell. 2005;7(1):17–23.PubMedPubMedCentral Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell. 2005;7(1):17–23.PubMedPubMedCentral
2.
go back to reference Moghbeli M, Moghbeli F, Forghanifard MM, Garayali A, Abbaszadegan MR. Cancer stem cell markers in esophageal cancer. Am J Cancer Sci. 2013;2(1):37–50. Moghbeli M, Moghbeli F, Forghanifard MM, Garayali A, Abbaszadegan MR. Cancer stem cell markers in esophageal cancer. Am J Cancer Sci. 2013;2(1):37–50.
3.
go back to reference Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea—a paradigm shift. Cancer Res. 2006;66(4):1883–90 discussion 95-6.PubMedCrossRef Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea—a paradigm shift. Cancer Res. 2006;66(4):1883–90 discussion 95-6.PubMedCrossRef
5.
go back to reference Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med. 2007;58:267–84.PubMedCrossRef Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med. 2007;58:267–84.PubMedCrossRef
7.
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(6464):645–8.PubMedCrossRef 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(6464):645–8.PubMedCrossRef
8.
go back to reference Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64(19):7011–21.PubMedCrossRef Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64(19):7011–21.PubMedCrossRef
9.
go back to reference Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res. 2005;65(14):6207–19.PubMedCrossRef Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res. 2005;65(14):6207–19.PubMedCrossRef
11.
go back to reference Biddle A, Gammon L, Fazil B, Mackenzie IC. CD44 staining of cancer stem-like cells is influenced by down-regulation of CD44 variant isoforms and up-regulation of the standard CD44 isoform in the population of cells that have undergone epithelial-to-mesenchymal transition. PLoS One. 2013;8(2):e57314.PubMedCrossRefPubMedCentral Biddle A, Gammon L, Fazil B, Mackenzie IC. CD44 staining of cancer stem-like cells is influenced by down-regulation of CD44 variant isoforms and up-regulation of the standard CD44 isoform in the population of cells that have undergone epithelial-to-mesenchymal transition. PLoS One. 2013;8(2):e57314.PubMedCrossRefPubMedCentral
12.
go back to reference Hill RP. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res. 2006;66(4):1891–5 discussion 0.PubMedCrossRef Hill RP. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res. 2006;66(4):1891–5 discussion 0.PubMedCrossRef
13.
go back to reference Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009;27(5):1006–20.PubMedCrossRefPubMedCentral Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009;27(5):1006–20.PubMedCrossRefPubMedCentral
14.
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(3):446–53.PubMedCrossRef 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(3):446–53.PubMedCrossRef
15.
16.
17.
go back to reference Song J, Chang I, Chen Z, Kang M, Wang CY. Characterization of side populations in HNSCC: highly invasive, chemoresistant and abnormal Wnt signaling. PLoS One. 2010;5(7):e11456.PubMedCrossRefPubMedCentral Song J, Chang I, Chen Z, Kang M, Wang CY. Characterization of side populations in HNSCC: highly invasive, chemoresistant and abnormal Wnt signaling. PLoS One. 2010;5(7):e11456.PubMedCrossRefPubMedCentral
19.
go back to reference Li L, Li B, Shao J, Wang X. Chemotherapy sorting can be used to identify cancer stem cell populations. Mol Biol Rep. 2012;39(11):9955–63.PubMedCrossRef Li L, Li B, Shao J, Wang X. Chemotherapy sorting can be used to identify cancer stem cell populations. Mol Biol Rep. 2012;39(11):9955–63.PubMedCrossRef
20.
go back to reference Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer. 2010;46(4):765–81.PubMedCrossRef Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer. 2010;46(4):765–81.PubMedCrossRef
21.
go back to reference Mosavi-Jarrahi A, Ahmadi-Jouibari T, Najafi F, Mehrabi Y, Aghaei A. Estimation of esophageal cancer incidence in Tehran by log-linear method using population-based cancer registry data. Asian Pac J Cancer Prev. 2013;14(9):5367–70.PubMedCrossRef Mosavi-Jarrahi A, Ahmadi-Jouibari T, Najafi F, Mehrabi Y, Aghaei A. Estimation of esophageal cancer incidence in Tehran by log-linear method using population-based cancer registry data. Asian Pac J Cancer Prev. 2013;14(9):5367–70.PubMedCrossRef
22.
go back to reference Roshandel G, Semnani S, Malekzadeh R, Dawsey SM. Polycyclic aromatic hydrocarbons and esophageal squamous cell carcinoma. Arch Iran Med. 2012;15(11):713–22.PubMed Roshandel G, Semnani S, Malekzadeh R, Dawsey SM. Polycyclic aromatic hydrocarbons and esophageal squamous cell carcinoma. Arch Iran Med. 2012;15(11):713–22.PubMed
23.
go back to reference Zhao JS, Li WJ, Ge D, Zhang PJ, Li JJ, Lu CL, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One. 2011;6(6):e21419.PubMedCrossRefPubMedCentral Zhao JS, Li WJ, Ge D, Zhang PJ, Li JJ, Lu CL, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One. 2011;6(6):e21419.PubMedCrossRefPubMedCentral
24.
go back to reference Misra S, Hascall VC, Berger FG, Markwald RR, Ghatak S. Hyaluronan, CD44, and cyclooxygenase-2 in colon cancer. Connect Tissue Res. 2008;49(3):219–24.PubMedCrossRef Misra S, Hascall VC, Berger FG, Markwald RR, Ghatak S. Hyaluronan, CD44, and cyclooxygenase-2 in colon cancer. Connect Tissue Res. 2008;49(3):219–24.PubMedCrossRef
25.
go back to reference Misra S, Toole BP, Ghatak S. Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells. J Biol Chem. 2006;281(46):34936–41.PubMedCrossRef Misra S, Toole BP, Ghatak S. Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells. J Biol Chem. 2006;281(46):34936–41.PubMedCrossRef
26.
go back to reference Gotoda T, Matsumura Y, Kondo H, Ono H, Kanamoto A, Kato H, et al. Expression of CD44 variants and prognosis in oesophageal squamous cell carcinoma. Gut. 2000;46(1):14–9.PubMedCrossRefPubMedCentral Gotoda T, Matsumura Y, Kondo H, Ono H, Kanamoto A, Kato H, et al. Expression of CD44 variants and prognosis in oesophageal squamous cell carcinoma. Gut. 2000;46(1):14–9.PubMedCrossRefPubMedCentral
27.
go back to reference Kalish ED, Iida N, Moffat FL, Bourguignon LY. A new CD44V3-containing isoform is involved in tumor cell growth and migration during human breast carcinoma progression. Front Biosci. 1999;4:A1–8.PubMedCrossRef Kalish ED, Iida N, Moffat FL, Bourguignon LY. A new CD44V3-containing isoform is involved in tumor cell growth and migration during human breast carcinoma progression. Front Biosci. 1999;4:A1–8.PubMedCrossRef
28.
go back to reference Kuhn S, Koch M, Nubel T, Ladwein M, Antolovic D, Klingbeil P, et al. A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol Cancer Res. 2007;5(6):553–67.PubMedCrossRef Kuhn S, Koch M, Nubel T, Ladwein M, Antolovic D, Klingbeil P, et al. A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol Cancer Res. 2007;5(6):553–67.PubMedCrossRef
29.
go back to reference Kuniyasu H, Oue N, Tsutsumi M, Tahara E, Yasui W. Heparan sulfate enhances invasion by human colon carcinoma cell lines through expression of CD44 variant exon 3. Clin Cancer Res. 2001;7(12):4067–72.PubMed Kuniyasu H, Oue N, Tsutsumi M, Tahara E, Yasui W. Heparan sulfate enhances invasion by human colon carcinoma cell lines through expression of CD44 variant exon 3. Clin Cancer Res. 2001;7(12):4067–72.PubMed
30.
go back to reference Liu WK, Fu Q, Li YM, Jiang XY, Zhang MP, Zhang ZX. The relationship between cyclooxygenase-2, CD44v6, and nm23H1 in esophageal squamous cell carcinoma. Onkologie. 2009;32(10):574–8.PubMedCrossRef Liu WK, Fu Q, Li YM, Jiang XY, Zhang MP, Zhang ZX. The relationship between cyclooxygenase-2, CD44v6, and nm23H1 in esophageal squamous cell carcinoma. Onkologie. 2009;32(10):574–8.PubMedCrossRef
31.
go back to reference Sano A, Kato H, Sakurai S, Sakai M, Tanaka N, Inose T, et al. CD24 expression is a novel prognostic factor in esophageal squamous cell carcinoma. Ann Surg Oncol. 2009;16(2):506–14.PubMedCrossRef Sano A, Kato H, Sakurai S, Sakai M, Tanaka N, Inose T, et al. CD24 expression is a novel prognostic factor in esophageal squamous cell carcinoma. Ann Surg Oncol. 2009;16(2):506–14.PubMedCrossRef
32.
go back to reference Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F. A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res. 2009;69(17):6790–8.PubMedCrossRefPubMedCentral Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F. A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res. 2009;69(17):6790–8.PubMedCrossRefPubMedCentral
33.
go back to reference Schabath H, Runz S, Joumaa S, Altevogt P. CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci. 2006;119(Pt 2):314–25.PubMedCrossRef Schabath H, Runz S, Joumaa S, Altevogt P. CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci. 2006;119(Pt 2):314–25.PubMedCrossRef
34.
go back to reference Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA, et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med. 2009;13(8B):2236–52.PubMedCrossRef Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA, et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med. 2009;13(8B):2236–52.PubMedCrossRef
35.
go back to reference Chute JP, Muramoto GG, Whitesides J, Colvin M, Safi R, Chao NJ, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA. 2006;103(31):11707–12.PubMedCrossRefPubMedCentral Chute JP, Muramoto GG, Whitesides J, Colvin M, Safi R, Chao NJ, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA. 2006;103(31):11707–12.PubMedCrossRefPubMedCentral
36.
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(5):2162–9.PubMedCrossRefPubMedCentral 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(5):2162–9.PubMedCrossRefPubMedCentral
37.
go back to reference Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, et al. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck. 2010;32(9):1195–201.PubMedCrossRefPubMedCentral Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, et al. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck. 2010;32(9):1195–201.PubMedCrossRefPubMedCentral
38.
go back to reference Forghanifard MM, Moaven O, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, et al. Expression analysis elucidates the roles of MAML1 and Twist1 in esophageal squamous cell carcinoma aggressiveness and metastasis. Ann Surg Oncol. 2012;19(3):743–9.PubMedCrossRef Forghanifard MM, Moaven O, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, et al. Expression analysis elucidates the roles of MAML1 and Twist1 in esophageal squamous cell carcinoma aggressiveness and metastasis. Ann Surg Oncol. 2012;19(3):743–9.PubMedCrossRef
39.
go back to reference Moghbeli M, Abbaszadegan MR, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, et al. Association of PYGO2 and EGFR in esophageal squamous cell carcinoma. Med Oncol. 2013;30(2):516.PubMedCrossRef Moghbeli M, Abbaszadegan MR, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, et al. Association of PYGO2 and EGFR in esophageal squamous cell carcinoma. Med Oncol. 2013;30(2):516.PubMedCrossRef
40.
go back to reference Moghbeli M, Forghanifard MM, Aarabi A, Mansourian A, Abbaszadegan MR. Clinicopathological sex- related relevance of Musashi1 mRNA Expression in Esophageal Squamous Cell Carcinoma Patients. Pathol Oncol Res. 2014;20:427–33. Moghbeli M, Forghanifard MM, Aarabi A, Mansourian A, Abbaszadegan MR. Clinicopathological sex- related relevance of Musashi1 mRNA Expression in Esophageal Squamous Cell Carcinoma Patients. Pathol Oncol Res. 2014;20:427–33.
41.
go back to reference Kimura O, Takahashi T, Ishii N, Inoue Y, Ueno Y, Kogure T, et al. Characterization of the epithelial cell adhesion molecule (EpCAM)+ cell population in hepatocellular carcinoma cell lines. Cancer Sci. 2010;101(10):2145–55.PubMedCrossRef Kimura O, Takahashi T, Ishii N, Inoue Y, Ueno Y, Kogure T, et al. Characterization of the epithelial cell adhesion molecule (EpCAM)+ cell population in hepatocellular carcinoma cell lines. Cancer Sci. 2010;101(10):2145–55.PubMedCrossRef
42.
go back to reference Tomuleasa C, Soritau O, Rus-Ciuca D, Pop T, Todea D, Mosteanu O, et al. Isolation and characterization of hepatic cancer cells with stem-like properties from hepatocellular carcinoma. J Gastrointestin Liver Dis. 2010;19(1):61–7.PubMed Tomuleasa C, Soritau O, Rus-Ciuca D, Pop T, Todea D, Mosteanu O, et al. Isolation and characterization of hepatic cancer cells with stem-like properties from hepatocellular carcinoma. J Gastrointestin Liver Dis. 2010;19(1):61–7.PubMed
43.
go back to reference Zhu Z, Hao X, Yan M, Yao M, Ge C, Gu J, et al. Cancer stem/progenitor cells are highly enriched in CD133+ CD44+ population in hepatocellular carcinoma. Int J Cancer. 2010;126(9):2067–78.PubMed Zhu Z, Hao X, Yan M, Yao M, Ge C, Gu J, et al. Cancer stem/progenitor cells are highly enriched in CD133+ CD44+ population in hepatocellular carcinoma. Int J Cancer. 2010;126(9):2067–78.PubMed
44.
go back to reference Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology. 2006;44(1):240–51.PubMedCrossRef Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology. 2006;44(1):240–51.PubMedCrossRef
45.
go back to reference Udomsakdi C, Eaves CJ, Sutherland HJ, Lansdorp PM. Separation of functionally distinct subpopulations of primitive human hematopoietic cells using rhodamine-123. Exp Hematol. 1991;19(5):338–42.PubMed Udomsakdi C, Eaves CJ, Sutherland HJ, Lansdorp PM. Separation of functionally distinct subpopulations of primitive human hematopoietic cells using rhodamine-123. Exp Hematol. 1991;19(5):338–42.PubMed
46.
go back to reference Bertoncello I, Williams B. Hematopoietic stem cell characterization by Hoechst 33342 and rhodamine 123 staining. Methods Mol Biol. 2004;263:181–200.PubMed Bertoncello I, Williams B. Hematopoietic stem cell characterization by Hoechst 33342 and rhodamine 123 staining. Methods Mol Biol. 2004;263:181–200.PubMed
47.
48.
go back to reference Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895–902.PubMedCrossRef Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895–902.PubMedCrossRef
49.
go back to reference Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 1996;175(1):1–13.PubMedCrossRef Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 1996;175(1):1–13.PubMedCrossRef
50.
go back to reference Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell. 2011;8(5):486–98.PubMedCrossRefPubMedCentral Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell. 2011;8(5):486–98.PubMedCrossRefPubMedCentral
51.
go back to reference Liu J, Ma L, Xu J, Liu C, Zhang J, Liu J, et al. Spheroid body-forming cells in the human gastric cancer cell line MKN-45 possess cancer stem cell properties. Int J Oncol. 2013;42(2):453–9.PubMedPubMedCentral Liu J, Ma L, Xu J, Liu C, Zhang J, Liu J, et al. Spheroid body-forming cells in the human gastric cancer cell line MKN-45 possess cancer stem cell properties. Int J Oncol. 2013;42(2):453–9.PubMedPubMedCentral
52.
go back to reference Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, et al. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011;11:71.PubMedCrossRefPubMedCentral Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, et al. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011;11:71.PubMedCrossRefPubMedCentral
53.
go back to reference Yamamoto N, Yamamoto S, Inagaki F, Kawaichi M, Fukamizu A, Kishi N, et al. Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J Biol Chem. 2001;276(48):45031–40.PubMedCrossRef Yamamoto N, Yamamoto S, Inagaki F, Kawaichi M, Fukamizu A, Kishi N, et al. Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J Biol Chem. 2001;276(48):45031–40.PubMedCrossRef
54.
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(7123):106–10.PubMedCrossRef 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(7123):106–10.PubMedCrossRef
55.
go back to reference Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396–401.PubMedCrossRef Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396–401.PubMedCrossRef
56.
go back to reference Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100(7):3983–8.PubMedCrossRefPubMedCentral Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100(7):3983–8.PubMedCrossRefPubMedCentral
57.
go back to reference Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, et al. Highly tumorigenic lung cancer CD133 + cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA. 2009;106(38):16281–6.PubMedCrossRefPubMedCentral Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, et al. Highly tumorigenic lung cancer CD133 + cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA. 2009;106(38):16281–6.PubMedCrossRefPubMedCentral
58.
go back to reference Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells. 2010;28(1):5–16.PubMedPubMedCentral Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells. 2010;28(1):5–16.PubMedPubMedCentral
59.
go back to reference Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res. 2008;6(7):1146–53.PubMedCrossRef Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res. 2008;6(7):1146–53.PubMedCrossRef
60.
go back to reference Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, et al. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol. 2011;64(11):937–46.PubMedCrossRef Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, et al. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol. 2011;64(11):937–46.PubMedCrossRef
61.
62.
go back to reference Auvinen P, Tammi R, Tammi M, Johansson R, Kosma VM. Expression of CD 44s, CD 44 v 3 and CD 44 v 6 in benign and malignant breast lesions: correlation and colocalization with hyaluronan. Histopathology. 2005;47(4):420–8.PubMedCrossRef Auvinen P, Tammi R, Tammi M, Johansson R, Kosma VM. Expression of CD 44s, CD 44 v 3 and CD 44 v 6 in benign and malignant breast lesions: correlation and colocalization with hyaluronan. Histopathology. 2005;47(4):420–8.PubMedCrossRef
63.
go back to reference Wang SJ, Wong G, de Heer AM, Xia W, Bourguignon LY. CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope. 2009;119(8):1518–30.PubMedCrossRefPubMedCentral Wang SJ, Wong G, de Heer AM, Xia W, Bourguignon LY. CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope. 2009;119(8):1518–30.PubMedCrossRefPubMedCentral
64.
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 USA. 2007;104(24):10158–63.PubMedCrossRefPubMedCentral 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 USA. 2007;104(24):10158–63.PubMedCrossRefPubMedCentral
65.
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(3):1030–7.PubMedCrossRef Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67(3):1030–7.PubMedCrossRef
66.
go back to reference Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008;68(11):4311–20.PubMedCrossRefPubMedCentral Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008;68(11):4311–20.PubMedCrossRefPubMedCentral
67.
go back to reference Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci USA. 2010;107(8):3722–7.PubMedCrossRefPubMedCentral Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci USA. 2010;107(8):3722–7.PubMedCrossRefPubMedCentral
68.
go back to reference Du L, Wang H, He L, Zhang J, Ni B, Wang X, et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res. 2008;14(21):6751–60.PubMedCrossRef Du L, Wang H, He L, Zhang J, Ni B, Wang X, et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res. 2008;14(21):6751–60.PubMedCrossRef
69.
go back to reference Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW, et al. Highly enriched CD133(+) CD44(+) stem-like cells with CD133(+) CD44(high) metastatic subset in HCT116 colon cancer cells. Clin Exp Metastasis. 2011;28(8):751–63.PubMedCrossRef Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW, et al. Highly enriched CD133(+) CD44(+) stem-like cells with CD133(+) CD44(high) metastatic subset in HCT116 colon cancer cells. Clin Exp Metastasis. 2011;28(8):751–63.PubMedCrossRef
70.
go back to reference Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res. 2007;67(5):2187–96.PubMedCrossRefPubMedCentral Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res. 2007;67(5):2187–96.PubMedCrossRefPubMedCentral
71.
go back to reference Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063–71.PubMedCrossRef Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063–71.PubMedCrossRef
72.
go back to reference Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med. 2009;1(6–7):338–51.PubMedCrossRefPubMedCentral Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med. 2009;1(6–7):338–51.PubMedCrossRefPubMedCentral
73.
go back to reference Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, et al. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA. 2004;101(39):14228–33.PubMedCrossRefPubMedCentral Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, et al. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA. 2004;101(39):14228–33.PubMedCrossRefPubMedCentral
74.
go back to reference Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA. 2004;101(3):781–6.PubMedCrossRefPubMedCentral Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA. 2004;101(3):781–6.PubMedCrossRefPubMedCentral
75.
go back to reference Zhang SL, Wang YS, Zhou T, Yu XW, Wei ZT, Li YL. Isolation and characterization of cancer stem cells from cervical cancer HeLa cells. Cytotechnology. 2012;64(4):477–84.PubMedCrossRefPubMedCentral Zhang SL, Wang YS, Zhou T, Yu XW, Wei ZT, Li YL. Isolation and characterization of cancer stem cells from cervical cancer HeLa cells. Cytotechnology. 2012;64(4):477–84.PubMedCrossRefPubMedCentral
76.
go back to reference Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69(4):1302–13.PubMedCrossRefPubMedCentral Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69(4):1302–13.PubMedCrossRefPubMedCentral
77.
go back to reference Fan X, Liu S, Su F, Pan Q, Lin T. Effective enrichment of prostate cancer stem cells from spheres in a suspension culture system. Urol Oncol. 2012;30(3):314–8.PubMedCrossRef Fan X, Liu S, Su F, Pan Q, Lin T. Effective enrichment of prostate cancer stem cells from spheres in a suspension culture system. Urol Oncol. 2012;30(3):314–8.PubMedCrossRef
78.
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(23):10946–51.PubMedCrossRef Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65(23):10946–51.PubMedCrossRef
79.
go back to reference Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol. 2008;26(17):2862–70.PubMedCrossRef Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol. 2008;26(17):2862–70.PubMedCrossRef
80.
go back to reference Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006;25(12):1696–708.PubMedCrossRef Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006;25(12):1696–708.PubMedCrossRef
81.
go back to reference Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, Mistree T, et al. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis. 2009;26(5):433–46.PubMedCrossRefPubMedCentral Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, Mistree T, et al. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis. 2009;26(5):433–46.PubMedCrossRefPubMedCentral
82.
go back to reference Ding XW, Wu JH, Jiang CP. ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci. 2010;86(17–18):631–7.PubMedCrossRef Ding XW, Wu JH, Jiang CP. ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci. 2010;86(17–18):631–7.PubMedCrossRef
84.
go back to reference Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, et al. Identification of cells initiating human melanomas. Nature. 2008;451(7176):345–9.PubMedCrossRefPubMedCentral Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, et al. Identification of cells initiating human melanomas. Nature. 2008;451(7176):345–9.PubMedCrossRefPubMedCentral
85.
go back to reference Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res. 2007;67(7):3153–61.PubMedCrossRef Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res. 2007;67(7):3153–61.PubMedCrossRef
86.
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(4):704–15.PubMedCrossRefPubMedCentral 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(4):704–15.PubMedCrossRefPubMedCentral
87.
go back to reference Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells: an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.PubMedCrossRef Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells: an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.PubMedCrossRef
88.
go back to reference Chambers I. The molecular basis of pluripotency in mouse embryonic stem cells. Cloning Stem Cells. 2004;6(4):386–91.PubMedCrossRef Chambers I. The molecular basis of pluripotency in mouse embryonic stem cells. Cloning Stem Cells. 2004;6(4):386–91.PubMedCrossRef
89.
go back to reference Hatefi N, Nouraee N, Parvin M, Ziaee SA, Mowla SJ. Evaluating the expression of oct4 as a prognostic tumor marker in bladder cancer. Iran J Basic Med Sci. 2012;15(6):1154–61.PubMedPubMedCentral Hatefi N, Nouraee N, Parvin M, Ziaee SA, Mowla SJ. Evaluating the expression of oct4 as a prognostic tumor marker in bladder cancer. Iran J Basic Med Sci. 2012;15(6):1154–61.PubMedPubMedCentral
90.
go back to reference Alkatout I, Wiedermann M, Bauer M, Wenners A, Jonat W, Klapper W. Transcription factors associated with epithelial-mesenchymal transition and cancer stem cells in the tumor centre and margin of invasive breast cancer. Exp Mol Pathol. 2013;94(1):168–73.PubMedCrossRef Alkatout I, Wiedermann M, Bauer M, Wenners A, Jonat W, Klapper W. Transcription factors associated with epithelial-mesenchymal transition and cancer stem cells in the tumor centre and margin of invasive breast cancer. Exp Mol Pathol. 2013;94(1):168–73.PubMedCrossRef
91.
go back to reference Tomizawa Y, Wu TT, Wang KK. Epithelial mesenchymal transition and cancer stem cells in esophageal adenocarcinoma originating from Barrett’s esophagus. Oncol Lett. 2012;3(5):1059–63.PubMedPubMedCentral Tomizawa Y, Wu TT, Wang KK. Epithelial mesenchymal transition and cancer stem cells in esophageal adenocarcinoma originating from Barrett’s esophagus. Oncol Lett. 2012;3(5):1059–63.PubMedPubMedCentral
92.
go back to reference Ouyang G, Wang Z, Fang X, Liu J, Yang CJ. Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci. 2010;67(15):2605–18.PubMedCrossRef Ouyang G, Wang Z, Fang X, Liu J, Yang CJ. Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci. 2010;67(15):2605–18.PubMedCrossRef
93.
go back to reference Chen YC, Chang CJ, Hsu HS, Chen YW, Tai LK, Tseng LM, et al. Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral Oncol. 2010;46(3):158–65.PubMedCrossRef Chen YC, Chang CJ, Hsu HS, Chen YW, Tai LK, Tseng LM, et al. Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral Oncol. 2010;46(3):158–65.PubMedCrossRef
94.
go back to reference Yu X, Jiang X, Li H, Guo L, Jiang W, Lu SH. MiR-203 inhibits the proliferation and self-renewal of esophageal cancer stem-like cells by suppressing stem renewal factor Bmi-1. Stem Cells Dev. 2014;23(6):576–85. Yu X, Jiang X, Li H, Guo L, Jiang W, Lu SH. MiR-203 inhibits the proliferation and self-renewal of esophageal cancer stem-like cells by suppressing stem renewal factor Bmi-1. Stem Cells Dev. 2014;23(6):576–85.
Metadata
Title
Cancer stem cell detection and isolation
Authors
Meysam Moghbeli
Faezeh Moghbeli
Mohammad Mahdi Forghanifard
Mohammad Reza Abbaszadegan
Publication date
01-09-2014
Publisher
Springer US
Published in
Medical Oncology / Issue 9/2014
Print ISSN: 1357-0560
Electronic ISSN: 1559-131X
DOI
https://doi.org/10.1007/s12032-014-0069-6

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