Skip to main content
Top
Published in: Experimental Hematology & Oncology 1/2013

Open Access 01-12-2013 | Review

CD133: a stem cell biomarker and beyond

Author: Zhong Li

Published in: Experimental Hematology & Oncology | Issue 1/2013

Login to get access

Abstract

Cancer stem cells (CSCs) or tumor initiating cells (TICs) contribute to tumorigenesis, metastasis, recurrence and chemoresistance. CD133, a pentaspan membrane glycoprotein, has been used as a stem cell biomarker for isolation of stem-like cells from a variety of normal and pathological tissues as well as cell lines since its discovery in 1999. Recent studies are focusing on the functionality of CD133. In this review, we summarize new insights into CD133 regulation and the involvement of CD133 in cell self-renewal, tumorigenesis, metastasis, resistance, metabolism, differentiation, autophagy, apoptosis, and regeneration.
Appendix
Available only for authorised users
Literature
1.
go back to reference Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW: A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 1997,90(12):5013–5021.PubMed Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW: A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 1997,90(12):5013–5021.PubMed
2.
go back to reference Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW: AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997,90(12):5002–5012.PubMed Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW: AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997,90(12):5002–5012.PubMed
3.
go back to reference Weigmann 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 U S A 1997,94(23):12425–12430.PubMedCentralPubMedCrossRef Weigmann 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 U S A 1997,94(23):12425–12430.PubMedCentralPubMedCrossRef
4.
go back to reference Shmelkov SV, St Clair R, Lyden D, Rafii S: AC133/CD133/Prominin-1. Int J Biochem Cell Biol 2005,37(4):715–719.PubMedCrossRef Shmelkov SV, St Clair R, Lyden D, Rafii S: AC133/CD133/Prominin-1. Int J Biochem Cell Biol 2005,37(4):715–719.PubMedCrossRef
5.
go back to reference Corbeil D, Roper K, Fargeas CA, Joester A, Huttner WB: Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2001,2(2):82–91.PubMedCrossRef Corbeil D, Roper K, Fargeas CA, Joester A, Huttner WB: Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2001,2(2):82–91.PubMedCrossRef
6.
go back to reference Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L: Stem cell marker prominin-1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas 2008,36(1):e1-e6.PubMedCrossRef Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L: Stem cell marker prominin-1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas 2008,36(1):e1-e6.PubMedCrossRef
7.
go back to reference Campos B, Herold-Mende CC: Insight into the complex regulation of CD133 in glioma. Int J Cancer 2011,128(3):501–510.PubMedCrossRef Campos B, Herold-Mende CC: Insight into the complex regulation of CD133 in glioma. Int J Cancer 2011,128(3):501–510.PubMedCrossRef
8.
go back to reference Lottaz C, Beier D, Meyer K, Kumar P, Hermann A, Schwarz J, Junker M, Oefner PJ, Bogdahn U, Wischhusen J, et al.: Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Res 2010,70(5):2030–2040.PubMedCrossRef Lottaz C, Beier D, Meyer K, Kumar P, Hermann A, Schwarz J, Junker M, Oefner PJ, Bogdahn U, Wischhusen J, et al.: Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Res 2010,70(5):2030–2040.PubMedCrossRef
9.
go back to reference Wu Y, Wu PY: CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev 2009,18(8):1127–1134.PubMedCrossRef Wu Y, Wu PY: CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev 2009,18(8):1127–1134.PubMedCrossRef
10.
go back to reference Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr, Gillespie GY: CD133 is a marker of bioenergetic stress in human glioma. PLoS One 2008,3(11):e3655.PubMedCentralPubMedCrossRef Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr, Gillespie GY: CD133 is a marker of bioenergetic stress in human glioma. PLoS One 2008,3(11):e3655.PubMedCentralPubMedCrossRef
11.
go back to reference Hashimoto O, Shimizu K, Semba S, Chiba S, Ku Y, Yokozaki H, Hori Y: Hypoxia induces tumor aggressiveness and the expansion of CD133-positive cells in a hypoxia-inducible factor-1alpha-dependent manner in pancreatic cancer cells. Pathobiology 2011,78(4):181–192.PubMedCrossRef Hashimoto O, Shimizu K, Semba S, Chiba S, Ku Y, Yokozaki H, Hori Y: Hypoxia induces tumor aggressiveness and the expansion of CD133-positive cells in a hypoxia-inducible factor-1alpha-dependent manner in pancreatic cancer cells. Pathobiology 2011,78(4):181–192.PubMedCrossRef
12.
go back to reference Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, et al.: Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009,28(45):3949–3959.PubMedCrossRef Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, et al.: Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009,28(45):3949–3959.PubMedCrossRef
14.
go back to reference Matsumoto K, Arao T, Tanaka K, Kaneda H, Kudo K, Fujita Y, Tamura D, Aomatsu K, Tamura T, Yamada Y, et al.: mTOR signal and hypoxia-inducible factor-1 alpha regulate CD133 expression in cancer cells. Cancer Res 2009,69(18):7160–7164.PubMedCrossRef Matsumoto K, Arao T, Tanaka K, Kaneda H, Kudo K, Fujita Y, Tamura D, Aomatsu K, Tamura T, Yamada Y, et al.: mTOR signal and hypoxia-inducible factor-1 alpha regulate CD133 expression in cancer cells. Cancer Res 2009,69(18):7160–7164.PubMedCrossRef
15.
go back to reference Yang Z, Zhang L, Ma A, Liu L, Li J, Gu J, Liu Y: Transient mTOR inhibition facilitates continuous growth of liver tumors by modulating the maintenance of CD133+ cell populations. PLoS One 2011,6(12):e28405.PubMedCentralPubMedCrossRef Yang Z, Zhang L, Ma A, Liu L, Li J, Gu J, Liu Y: Transient mTOR inhibition facilitates continuous growth of liver tumors by modulating the maintenance of CD133+ cell populations. PLoS One 2011,6(12):e28405.PubMedCentralPubMedCrossRef
16.
go back to reference You H, Ding W, Rountree CB: Epigenetic regulation of cancer stem cell marker CD133 by transforming growth factor-beta. Hepatology 2010,51(5):1635–1644.PubMedCentralPubMedCrossRef You H, Ding W, Rountree CB: Epigenetic regulation of cancer stem cell marker CD133 by transforming growth factor-beta. Hepatology 2010,51(5):1635–1644.PubMedCentralPubMedCrossRef
17.
go back to reference Grimm M, Kim M, Rosenwald A, Heemann U, Germer CT, Waaga-Gasser AM, Gasser M: Toll-like receptor (TLR) 7 and TLR8 expression on CD133+ cells in colorectal cancer points to a specific role for inflammation-induced TLRs in tumourigenesis and tumour progression. Eur J Cancer 2010,46(15):2849–2857.PubMedCrossRef Grimm M, Kim M, Rosenwald A, Heemann U, Germer CT, Waaga-Gasser AM, Gasser M: Toll-like receptor (TLR) 7 and TLR8 expression on CD133+ cells in colorectal cancer points to a specific role for inflammation-induced TLRs in tumourigenesis and tumour progression. Eur J Cancer 2010,46(15):2849–2857.PubMedCrossRef
18.
go back to reference Storci G, Sansone P, Mari S, D'Uva G, Tavolari S, Guarnieri T, Taffurelli M, Ceccarelli C, Santini D, Chieco P, et al.: TNFalpha up-regulates SLUG via the NF-kappaB/HIF1alpha axis, which imparts breast cancer cells with a stem cell-like phenotype. J Cell Physiol 2010,225(3):682–691.PubMedCentralPubMedCrossRef Storci G, Sansone P, Mari S, D'Uva G, Tavolari S, Guarnieri T, Taffurelli M, Ceccarelli C, Santini D, Chieco P, et al.: TNFalpha up-regulates SLUG via the NF-kappaB/HIF1alpha axis, which imparts breast cancer cells with a stem cell-like phenotype. J Cell Physiol 2010,225(3):682–691.PubMedCentralPubMedCrossRef
19.
20.
go back to reference Ma S, Tang KH, Chan YP, Lee TK, Kwan PS, Castilho A, Ng I, Man K, Wong N, To KF, et al.: miR-130b Promotes CD133(+) liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 2010,7(6):694–707.PubMedCrossRef Ma S, Tang KH, Chan YP, Lee TK, Kwan PS, Castilho A, Ng I, Man K, Wong N, To KF, et al.: miR-130b Promotes CD133(+) liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 2010,7(6):694–707.PubMedCrossRef
21.
go back to reference Shi L, Wan Y, Sun G, Gu X, Qian C, Yan W, Zhang S, Pan T, Wang Z, You Y: Functional differences of miR-125b on the invasion of primary glioblastoma CD133-negative cells and CD133-positive cells. Neuromolecular Med 2012,14(4):303–316.PubMedCrossRef Shi L, Wan Y, Sun G, Gu X, Qian C, Yan W, Zhang S, Pan T, Wang Z, You Y: Functional differences of miR-125b on the invasion of primary glioblastoma CD133-negative cells and CD133-positive cells. Neuromolecular Med 2012,14(4):303–316.PubMedCrossRef
22.
go back to reference Bissels U, Wild S, Tomiuk S, Hafner M, Scheel H, Mihailovic A, Choi YH, Tuschl T, Bosio A: Combined characterization of microRNA and mRNA profiles delineates early differentiation pathways of CD133+ and CD34+ hematopoietic stem and progenitor cells. Stem Cells 2011,29(5):847–857.PubMedCentralPubMedCrossRef Bissels U, Wild S, Tomiuk S, Hafner M, Scheel H, Mihailovic A, Choi YH, Tuschl T, Bosio A: Combined characterization of microRNA and mRNA profiles delineates early differentiation pathways of CD133+ and CD34+ hematopoietic stem and progenitor cells. Stem Cells 2011,29(5):847–857.PubMedCentralPubMedCrossRef
23.
go back to reference Garzia L, Andolfo I, Cusanelli E, Marino N, Petrosino G, De Martino D, Esposito V, Galeone A, Navas L, Esposito S, et al.: MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma. PLoS One 2009,4(3):e4998.PubMedCentralPubMedCrossRef Garzia L, Andolfo I, Cusanelli E, Marino N, Petrosino G, De Martino D, Esposito V, Galeone A, Navas L, Esposito S, et al.: MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma. PLoS One 2009,4(3):e4998.PubMedCentralPubMedCrossRef
24.
go back to reference Huang S, Guo W, Tang Y, Ren D, Zou X, Peng X: miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells. Oncol Rep 2012,28(5):1831–1837.PubMed Huang S, Guo W, Tang Y, Ren D, Zou X, Peng X: miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells. Oncol Rep 2012,28(5):1831–1837.PubMed
25.
go back to reference Zhang J, Luo N, Luo Y, Peng Z, Zhang T, Li S: microRNA-150 inhibits human CD133-positive liver cancer stem cells through negative regulation of the transcription factor c-Myb. Int J Oncol 2012,40(3):747–756.PubMed Zhang J, Luo N, Luo Y, Peng Z, Zhang T, Li S: microRNA-150 inhibits human CD133-positive liver cancer stem cells through negative regulation of the transcription factor c-Myb. Int J Oncol 2012,40(3):747–756.PubMed
26.
go back to reference Hibi K, Sakata M, Kitamura YH, Sakuraba K, Shirahata A, Goto T, Mizukami H, Saito M, Ishibashi K, Kigawa G, et al.: Demethylation of the CD133 gene is frequently detected in advanced colorectal cancer. Anticancer Res 2009,29(6):2235–2237.PubMed Hibi K, Sakata M, Kitamura YH, Sakuraba K, Shirahata A, Goto T, Mizukami H, Saito M, Ishibashi K, Kigawa G, et al.: Demethylation of the CD133 gene is frequently detected in advanced colorectal cancer. Anticancer Res 2009,29(6):2235–2237.PubMed
27.
go back to reference Hibi K, Sakata M, Kitamura YH, Sakuraba K, Shirahata A, Goto T, Mizukami H, Saito M, Ishibashi K, Kigawa G, et al.: Demethylation of the CD133 gene is frequently detected in early gastric carcinoma. Anticancer Res 2010,30(4):1201–1203.PubMed Hibi K, Sakata M, Kitamura YH, Sakuraba K, Shirahata A, Goto T, Mizukami H, Saito M, Ishibashi K, Kigawa G, et al.: Demethylation of the CD133 gene is frequently detected in early gastric carcinoma. Anticancer Res 2010,30(4):1201–1203.PubMed
28.
go back to reference Tabu K, Sasai K, Kimura T, Wang L, Aoyanagi E, Kohsaka S, Tanino M, Nishihara H, Tanaka S: Promoter hypomethylation regulates CD133 expression in human gliomas. Cell Res 2008,18(10):1037–1046.PubMedCrossRef Tabu K, Sasai K, Kimura T, Wang L, Aoyanagi E, Kohsaka S, Tanino M, Nishihara H, Tanaka S: Promoter hypomethylation regulates CD133 expression in human gliomas. Cell Res 2008,18(10):1037–1046.PubMedCrossRef
29.
go back to reference Yi JM, Tsai HC, Glockner SC, Lin S, Ohm JE, Easwaran H, James CD, Costello JF, Riggins G, Eberhart CG, et al.: Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res 2008,68(19):8094–8103.PubMedCentralPubMedCrossRef Yi JM, Tsai HC, Glockner SC, Lin S, Ohm JE, Easwaran H, James CD, Costello JF, Riggins G, Eberhart CG, et al.: Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res 2008,68(19):8094–8103.PubMedCentralPubMedCrossRef
30.
go back to reference Zhang C, Xu Y, Zhao J, Fan L, Jiang G, Li R, Ling Y, Wu M, Wei L: Elevated Expression of the Stem Cell Marker CD133 Associated with Line-1 Demethylation in Hepatocellular Carcinoma. Ann Surg Oncol 2011,18(8):2373–2380.PubMedCrossRef Zhang C, Xu Y, Zhao J, Fan L, Jiang G, Li R, Ling Y, Wu M, Wei L: Elevated Expression of the Stem Cell Marker CD133 Associated with Line-1 Demethylation in Hepatocellular Carcinoma. Ann Surg Oncol 2011,18(8):2373–2380.PubMedCrossRef
31.
go back to reference Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, Huang Z, Bentley RC, Mori S, Fujii S, et al.: Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 2009,28(2):209–218.PubMedCrossRef Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, Huang Z, Bentley RC, Mori S, Fujii S, et al.: Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 2009,28(2):209–218.PubMedCrossRef
32.
go back to reference Kemper K, Versloot M, Cameron K, Colak S, DeSousa EMelo F, DeJong JH, Bleackley J, Vermeulen L, Versteeg R, Koster J: Mutations in the Ras-Raf Axis underlie the prognostic value of CD133 in colorectal cancer. Clin Cancer Res 2012,18(11):3132–3141.PubMedCrossRef Kemper K, Versloot M, Cameron K, Colak S, DeSousa EMelo F, DeJong JH, Bleackley J, Vermeulen L, Versteeg R, Koster J: Mutations in the Ras-Raf Axis underlie the prognostic value of CD133 in colorectal cancer. Clin Cancer Res 2012,18(11):3132–3141.PubMedCrossRef
33.
go back to reference Fang DD, Kim YJ, Lee CN, Aggarwal S, McKinnon K, Mesmer D, Norton J, Birse CE, He T, Ruben SM, et al.: Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br J Cancer 2010,102(8):1265–1275.PubMedCentralPubMedCrossRef Fang DD, Kim YJ, Lee CN, Aggarwal S, McKinnon K, Mesmer D, Norton J, Birse CE, He T, Ruben SM, et al.: Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br J Cancer 2010,102(8):1265–1275.PubMedCentralPubMedCrossRef
34.
go back to reference Shi CJ, Gao J, Wang M, Wang X, Tian R, Zhu F, Shen M, Qin RY: CD133(+) gallbladder carcinoma cells exhibit self-renewal ability and tumorigenicity. World J Gastroenterol 2011,17(24):2965–2971.PubMedCentralPubMedCrossRef Shi CJ, Gao J, Wang M, Wang X, Tian R, Zhu F, Shen M, Qin RY: CD133(+) gallbladder carcinoma cells exhibit self-renewal ability and tumorigenicity. World J Gastroenterol 2011,17(24):2965–2971.PubMedCentralPubMedCrossRef
35.
go back to reference Kusumbe AP, Mali AM, Bapat SA: CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 2009,27(3):498–508.PubMedCrossRef Kusumbe AP, Mali AM, Bapat SA: CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 2009,27(3):498–508.PubMedCrossRef
36.
go back to reference Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY: CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008,27(12):1749–1758.PubMedCrossRef Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY: CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008,27(12):1749–1758.PubMedCrossRef
37.
go back to reference Tang KH, Ma S, Lee TK, Chan YP, Kwan PS, Tong CM, Ng IO, Man K, To KF, Lai PB, et al.: CD133(+) liver tumor-initiating cells promote tumor angiogenesis, growth, and self-renewal through neurotensin/interleukin-8/CXCL1 signaling. Hepatology 2012,55(3):807–820.PubMedCrossRef Tang KH, Ma S, Lee TK, Chan YP, Kwan PS, Tong CM, Ng IO, Man K, To KF, Lai PB, et al.: CD133(+) liver tumor-initiating cells promote tumor angiogenesis, growth, and self-renewal through neurotensin/interleukin-8/CXCL1 signaling. Hepatology 2012,55(3):807–820.PubMedCrossRef
38.
go back to reference Boivin D, Labbe D, Fontaine N, Lamy S, Beaulieu E, Gingras D, Beliveau R: The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry 2009,48(18):3998–4007.PubMedCrossRef Boivin D, Labbe D, Fontaine N, Lamy S, Beaulieu E, Gingras D, Beliveau R: The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry 2009,48(18):3998–4007.PubMedCrossRef
39.
go back to reference Wei Y, Jiang Y, Zou F, Liu Y, Wang S, Xu N, Xu W, Cui C, Xing Y, Cao B, et al.: Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells. Proc Natl Acad Sci U S A 2013,110(17):6829–6834.PubMedCentralPubMedCrossRef Wei Y, Jiang Y, Zou F, Liu Y, Wang S, Xu N, Xu W, Cui C, Xing Y, Cao B, et al.: Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells. Proc Natl Acad Sci U S A 2013,110(17):6829–6834.PubMedCentralPubMedCrossRef
40.
go back to reference Neuzil J, Stantic M, Zobalova R, Chladova J, Wang X, Prochazka L, Dong L, Andera L, Ralph SJ: Tumour-initiating cells vs. cancer 'stem' cells and CD133: what's in the name? Biochem Biophys Res Commun 2007,355(4):855–859.PubMedCrossRef Neuzil J, Stantic M, Zobalova R, Chladova J, Wang X, Prochazka L, Dong L, Andera L, Ralph SJ: Tumour-initiating cells vs. cancer 'stem' cells and CD133: what's in the name? Biochem Biophys Res Commun 2007,355(4):855–859.PubMedCrossRef
41.
go back to reference Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, et al.: CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008,118(6):2111–2120.PubMedCentralPubMed Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, et al.: CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008,118(6):2111–2120.PubMedCentralPubMed
42.
go back to reference Wang YK, Zhu YL, Qiu FM, Zhang T, Chen ZG, Zheng S, Huang J: Activation of Akt and MAPK pathways enhances the tumorigenicity of CD133+ primary colon cancer cells. Carcinogenesis 2010,31(8):1376–1380.PubMedCrossRef Wang YK, Zhu YL, Qiu FM, Zhang T, Chen ZG, Zheng S, Huang J: Activation of Akt and MAPK pathways enhances the tumorigenicity of CD133+ primary colon cancer cells. Carcinogenesis 2010,31(8):1376–1380.PubMedCrossRef
43.
go back to reference Borrego-Diaz E, Terai K, Lialyte K, Wise AL, Esfandyari T, Behbod F, Mautner VF, Spyra M, Taylor S, Parada LF, et al.: Overactivation of Ras signaling pathway in CD133+ MPNST cells. J Neurooncol 2012,108(3):423–434.PubMedCrossRef Borrego-Diaz E, Terai K, Lialyte K, Wise AL, Esfandyari T, Behbod F, Mautner VF, Spyra M, Taylor S, Parada LF, et al.: Overactivation of Ras signaling pathway in CD133+ MPNST cells. J Neurooncol 2012,108(3):423–434.PubMedCrossRef
44.
go back to reference Iida H, Suzuki M, Goitsuka R, Ueno H: Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 2012,40(1):71–79.PubMed Iida H, Suzuki M, Goitsuka R, Ueno H: Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 2012,40(1):71–79.PubMed
45.
go back to reference Zhang SS, Han ZP, Jing YY, Tao SF, Li TJ, Wang H, Wang Y, Li R, Yang Y, Zhao X, et al.: CD133+CXCR4+ colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med 2012, 10: 85.PubMedCentralPubMedCrossRef Zhang SS, Han ZP, Jing YY, Tao SF, Li TJ, Wang H, Wang Y, Li R, Yang Y, Zhao X, et al.: CD133+CXCR4+ colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med 2012, 10: 85.PubMedCentralPubMedCrossRef
46.
go back to reference Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW, Liang HJ: Highly enriched CD133(+)CD44(+) stem-like cells with CD133(+)CD44(high) metastatic subset in HCT116 colon cancer cells. Clin Exp Metastasis 2011,28(8):751–763.PubMedCrossRef Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW, Liang HJ: Highly enriched CD133(+)CD44(+) stem-like cells with CD133(+)CD44(high) metastatic subset in HCT116 colon cancer cells. Clin Exp Metastasis 2011,28(8):751–763.PubMedCrossRef
47.
go back to reference Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K, Kamohara Y, Inoue H, Mori M: CD133+CD44+ population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 2008,15(10):2927–2933.PubMedCrossRef Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K, Kamohara Y, Inoue H, Mori M: CD133+CD44+ population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 2008,15(10):2927–2933.PubMedCrossRef
48.
go back to reference Huang X, Sheng Y, Guan M: Co-expression of stem cell genes CD133 and CD44 in colorectal cancers with early liver metastasis. Surg Oncol 2012,21(2):103–107.PubMedCrossRef Huang X, Sheng Y, Guan M: Co-expression of stem cell genes CD133 and CD44 in colorectal cancers with early liver metastasis. Surg Oncol 2012,21(2):103–107.PubMedCrossRef
49.
go back to reference Hou Y, Zou Q, Ge R, Shen F, Wang Y: The critical role of CD133(+)CD44(+/high) tumor cells in hematogenous metastasis of liver cancers. Cell Res 2012,22(1):259–272.PubMedCentralPubMedCrossRef Hou Y, Zou Q, Ge R, Shen F, Wang Y: The critical role of CD133(+)CD44(+/high) tumor cells in hematogenous metastasis of liver cancers. Cell Res 2012,22(1):259–272.PubMedCentralPubMedCrossRef
50.
go back to reference Bellizzi A, Sebastian S, Ceglia P, Centonze M, Divella R, Manzillo EF, Azzariti A, Silvestris N, Montemurro S, Caliandro C, et al.: Co-expression of CD133(+)/CD44(+) in human colon cancer and liver metastasis. J Cell Physiol 2013,228(2):408–415.PubMedCrossRef Bellizzi A, Sebastian S, Ceglia P, Centonze M, Divella R, Manzillo EF, Azzariti A, Silvestris N, Montemurro S, Caliandro C, et al.: Co-expression of CD133(+)/CD44(+) in human colon cancer and liver metastasis. J Cell Physiol 2013,228(2):408–415.PubMedCrossRef
51.
go back to reference Wang D, Zhu H, Zhu Y, Liu Y, Shen H, Yin R, Zhang Z, Su Z: CD133(+)/CD44(+)/Oct4(+)/Nestin(+) stem-like cells isolated from Panc-1 cell line may contribute to multi-resistance and metastasis of pancreatic cancer. Acta Histochem 2013,115(4):349–356.PubMedCrossRef Wang D, Zhu H, Zhu Y, Liu Y, Shen H, Yin R, Zhang Z, Su Z: CD133(+)/CD44(+)/Oct4(+)/Nestin(+) stem-like cells isolated from Panc-1 cell line may contribute to multi-resistance and metastasis of pancreatic cancer. Acta Histochem 2013,115(4):349–356.PubMedCrossRef
52.
go back to reference Shi C, Tian R, Wang M, Wang X, Jiang J, Zhang Z, Li X, He Z, Gong W, Qin R: CD44+ CD133+ population exhibits cancer stem cell-like characteristics in human gallbladder carcinoma. Cancer Biol Ther 2010,10(11):1182–1190.PubMedCrossRef Shi C, Tian R, Wang M, Wang X, Jiang J, Zhang Z, Li X, He Z, Gong W, Qin R: CD44+ CD133+ population exhibits cancer stem cell-like characteristics in human gallbladder carcinoma. Cancer Biol Ther 2010,10(11):1182–1190.PubMedCrossRef
53.
go back to reference Okudela K, Woo T, Mitsui H, Tajiri M, Masuda M, Ohashi K: Expression of the potential cancer stem cell markers, CD133, CD44, ALDH1, and beta-catenin, in primary lung adenocarcinoma–their prognostic significance. Pathol Int 2012,62(12):792–801.PubMedCrossRef Okudela K, Woo T, Mitsui H, Tajiri M, Masuda M, Ohashi K: Expression of the potential cancer stem cell markers, CD133, CD44, ALDH1, and beta-catenin, in primary lung adenocarcinoma–their prognostic significance. Pathol Int 2012,62(12):792–801.PubMedCrossRef
54.
go back to reference Wakamatsu Y, Sakamoto N, Oo HZ, Naito Y, Uraoka N, Anami K, Sentani K, Oue N, Yasui W: Expression of cancer stem cell markers ALDH1, CD44 and CD133 in primary tumor and lymph node metastasis of gastric cancer. Pathol Int 2012,62(2):112–119.PubMedCrossRef Wakamatsu Y, Sakamoto N, Oo HZ, Naito Y, Uraoka N, Anami K, Sentani K, Oue N, Yasui W: Expression of cancer stem cell markers ALDH1, CD44 and CD133 in primary tumor and lymph node metastasis of gastric cancer. Pathol Int 2012,62(2):112–119.PubMedCrossRef
55.
go back to reference Kohga K, Tatsumi T, Takehara T, Tsunematsu H, Shimizu S, Yamamoto M, Sasakawa A, Miyagi T, Hayashi N: Expression of CD133 confers malignant potential by regulating metalloproteinases in human hepatocellular carcinoma. J Hepatol 2010,52(6):872–879.PubMedCrossRef Kohga K, Tatsumi T, Takehara T, Tsunematsu H, Shimizu S, Yamamoto M, Sasakawa A, Miyagi T, Hayashi N: Expression of CD133 confers malignant potential by regulating metalloproteinases in human hepatocellular carcinoma. J Hepatol 2010,52(6):872–879.PubMedCrossRef
56.
go back to reference Zhang M, Liu Y, Feng H, Bian X, Zhao W, Yang Z, Gu B, Li Z: CD133 Affects the Invasive Ability of HCT116 Cells by Regulating TIMP-2. Am J Pathol 2013,182(2):565–576.PubMedCrossRef Zhang M, Liu Y, Feng H, Bian X, Zhao W, Yang Z, Gu B, Li Z: CD133 Affects the Invasive Ability of HCT116 Cells by Regulating TIMP-2. Am J Pathol 2013,182(2):565–576.PubMedCrossRef
57.
go back to reference Long H, Xie R, Xiang T, Zhao Z, Lin S, Liang Z, Chen Z, Zhu B: Autocrine CCL5 signaling promotes invasion and migration of CD133+ ovarian cancer stem-like cells via NF-kappaB-mediated MMP-9 upregulation. Stem Cells 2012,30(10):2309–2319.PubMedCrossRef Long H, Xie R, Xiang T, Zhao Z, Lin S, Liang Z, Chen Z, Zhu B: Autocrine CCL5 signaling promotes invasion and migration of CD133+ ovarian cancer stem-like cells via NF-kappaB-mediated MMP-9 upregulation. Stem Cells 2012,30(10):2309–2319.PubMedCrossRef
58.
go back to reference Damdinsuren B, Nagano H, Kondo M, Natsag J, Hanada H, Nakamura M, Wada H, Kato H, Marubashi S, Miyamoto A, et al.: TGF-beta1-induced cell growth arrest and partial differentiation is related to the suppression of Id1 in human hepatoma cells. Oncol Rep 2006,15(2):401–408.PubMed Damdinsuren B, Nagano H, Kondo M, Natsag J, Hanada H, Nakamura M, Wada H, Kato H, Marubashi S, Miyamoto A, et al.: TGF-beta1-induced cell growth arrest and partial differentiation is related to the suppression of Id1 in human hepatoma cells. Oncol Rep 2006,15(2):401–408.PubMed
59.
go back to reference Zhang Q, Shi S, Yen Y, Brown J, Ta JQ, Le AD: A subpopulation of CD133(+) cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett 2010,289(2):151–160.PubMedCrossRef Zhang Q, Shi S, Yen Y, Brown J, Ta JQ, Le AD: A subpopulation of CD133(+) cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett 2010,289(2):151–160.PubMedCrossRef
61.
go back to reference Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, Sayegh MH, Sadee W, Frank MH: ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 2005,65(10):4320–4333.PubMedCrossRef Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, Sayegh MH, Sadee W, Frank MH: ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 2005,65(10):4320–4333.PubMedCrossRef
62.
go back to reference Cheung ST, Cheung PF, Cheng CK, Wong NC, Fan ST: Granulin-Epithelin Precursor and ATP-Dependent Binding Cassette (ABC)B5 Regulate Liver Cancer Cell Chemoresistance. Gastroenterology 2011,140(1):344–355. e342PubMedCrossRef Cheung ST, Cheung PF, Cheng CK, Wong NC, Fan ST: Granulin-Epithelin Precursor and ATP-Dependent Binding Cassette (ABC)B5 Regulate Liver Cancer Cell Chemoresistance. Gastroenterology 2011,140(1):344–355. e342PubMedCrossRef
63.
go back to reference Piao LS, Hur W, Kim TK, Hong SW, Kim SW, Choi JE, Sung PS, Song MJ, Lee BC, Hwang D, et al.: CD133(+) liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Cancer Lett 2012,315(2):129–137.PubMedCrossRef Piao LS, Hur W, Kim TK, Hong SW, Kim SW, Choi JE, Sung PS, Song MJ, Lee BC, Hwang D, et al.: CD133(+) liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Cancer Lett 2012,315(2):129–137.PubMedCrossRef
64.
go back to reference Corbeil D, Marzesco AM, Wilsch-Brauninger M, Huttner WB: The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation. FEBS Lett 2010,584(9):1659–1664.PubMedCrossRef Corbeil D, Marzesco AM, Wilsch-Brauninger M, Huttner WB: The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation. FEBS Lett 2010,584(9):1659–1664.PubMedCrossRef
65.
go back to reference Dubreuil V, Marzesco AM, Corbeil D, Huttner WB, Wilsch-Brauninger M: Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol 2007,176(4):483–495.PubMedCentralPubMedCrossRef Dubreuil V, Marzesco AM, Corbeil D, Huttner WB, Wilsch-Brauninger M: Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol 2007,176(4):483–495.PubMedCentralPubMedCrossRef
66.
go back to reference Roper K, Corbeil D, Huttner WB: Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2000,2(9):582–592.PubMedCrossRef Roper K, Corbeil D, Huttner WB: Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2000,2(9):582–592.PubMedCrossRef
67.
go back to reference Corbeil D, Marzesco AM, Fargeas CA, Huttner WB: Prominin-1: a distinct cholesterol-binding membrane protein and the organisation of the apical plasma membrane of epithelial cells. Subcell Biochem 2010, 51: 399–423.PubMedCrossRef Corbeil D, Marzesco AM, Fargeas CA, Huttner WB: Prominin-1: a distinct cholesterol-binding membrane protein and the organisation of the apical plasma membrane of epithelial cells. Subcell Biochem 2010, 51: 399–423.PubMedCrossRef
68.
go back to reference Bourseau-Guilmain E, Griveau A, Benoit JP, Garcion E: The Importance of the Stem Cell Marker Prominin-1/CD133 in the Uptake of Transferrin and in Iron Metabolism in Human Colon Cancer Caco-2 Cells. PLoS One 2011,6(9):e25515.PubMedCentralPubMedCrossRef Bourseau-Guilmain E, Griveau A, Benoit JP, Garcion E: The Importance of the Stem Cell Marker Prominin-1/CD133 in the Uptake of Transferrin and in Iron Metabolism in Human Colon Cancer Caco-2 Cells. PLoS One 2011,6(9):e25515.PubMedCentralPubMedCrossRef
69.
go back to reference Gong L, Cui Z, Yu X, Wei Y, Peng J, Leng X: Hexokinase II in CD133+ and CD133- hepatoma BEL-7402 Cells. Pathol Oncol Res 2012,18(2):377–381.PubMedCrossRef Gong L, Cui Z, Yu X, Wei Y, Peng J, Leng X: Hexokinase II in CD133+ and CD133- hepatoma BEL-7402 Cells. Pathol Oncol Res 2012,18(2):377–381.PubMedCrossRef
70.
go back to reference Lyshchik A, Higashi T, Hara T, Nakamoto Y, Fujimoto K, Doi R, Imamura M, Saga T, Togashi K: Expression of glucose transporter-1, hexokinase-II, proliferating cell nuclear antigen and survival of patients with pancreatic cancer. Cancer Invest 2007,25(3):154–162.PubMedCrossRef Lyshchik A, Higashi T, Hara T, Nakamoto Y, Fujimoto K, Doi R, Imamura M, Saga T, Togashi K: Expression of glucose transporter-1, hexokinase-II, proliferating cell nuclear antigen and survival of patients with pancreatic cancer. Cancer Invest 2007,25(3):154–162.PubMedCrossRef
71.
go back to reference Kwee SA, Hernandez B, Chan O, Wong L: Choline kinase alpha and hexokinase-2 protein expression in hepatocellular carcinoma: association with survival. PLoS One 2012,7(10):e46591.PubMedCentralPubMedCrossRef Kwee SA, Hernandez B, Chan O, Wong L: Choline kinase alpha and hexokinase-2 protein expression in hepatocellular carcinoma: association with survival. PLoS One 2012,7(10):e46591.PubMedCentralPubMedCrossRef
72.
go back to reference Zhou F, Cui C, Ge Y, Chen H, Li Q, Yang Z, Wu G, Sun S, Chen K, Gu J, et al.: Alpha2,3-Sialylation regulates the stability of stem cell marker CD133. J Biochem 2010,148(3):273–280.PubMedCrossRef Zhou F, Cui C, Ge Y, Chen H, Li Q, Yang Z, Wu G, Sun S, Chen K, Gu J, et al.: Alpha2,3-Sialylation regulates the stability of stem cell marker CD133. J Biochem 2010,148(3):273–280.PubMedCrossRef
73.
go back to reference Swindall AF, Londono-Joshi AI, Schultz MJ, Fineberg N, Buchsbaum DJ, Bellis SL: ST6Gal-I protein expression is upregulated in human epithelial tumors and correlates with stem cell markers in normal tissues and colon cancer cell lines. Cancer Res 2013,73(7):2368–2378.PubMedCentralPubMedCrossRef Swindall AF, Londono-Joshi AI, Schultz MJ, Fineberg N, Buchsbaum DJ, Bellis SL: ST6Gal-I protein expression is upregulated in human epithelial tumors and correlates with stem cell markers in normal tissues and colon cancer cell lines. Cancer Res 2013,73(7):2368–2378.PubMedCentralPubMedCrossRef
74.
go back to reference Hemmoranta H, Satomaa T, Blomqvist M, Heiskanen A, Aitio O, Saarinen J, Natunen J, Partanen J, Laine J, Jaatinen T: N-glycan structures and associated gene expression reflect the characteristic N-glycosylation pattern of human hematopoietic stem and progenitor cells. Exp Hematol 2007,35(8):1279–1292.PubMedCrossRef Hemmoranta H, Satomaa T, Blomqvist M, Heiskanen A, Aitio O, Saarinen J, Natunen J, Partanen J, Laine J, Jaatinen T: N-glycan structures and associated gene expression reflect the characteristic N-glycosylation pattern of human hematopoietic stem and progenitor cells. Exp Hematol 2007,35(8):1279–1292.PubMedCrossRef
75.
go back to reference Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G, et al.: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 2010,70(2):719–729.PubMedCrossRef Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G, et al.: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 2010,70(2):719–729.PubMedCrossRef
76.
go back to reference Lehnus KS, Donovan LK, Huang X, Zhao N, Warr TJ, Pilkington GJ, An Q: CD133 glycosylation is enhanced by hypoxia in cultured glioma stem cells. Int J Oncol 2013,42(3):1011–1017.PubMed Lehnus KS, Donovan LK, Huang X, Zhao N, Warr TJ, Pilkington GJ, An Q: CD133 glycosylation is enhanced by hypoxia in cultured glioma stem cells. Int J Oncol 2013,42(3):1011–1017.PubMed
77.
go back to reference Chen H, Luo Z, Dong L, Tan Y, Yang J, Feng G, Wu M, Li Z, Wang H: CD133/prominin-1-mediated autophagy and glucose uptake beneficial for hepatoma cell survival. PLoS One 2013,8(2):e56878.PubMedCentralPubMedCrossRef Chen H, Luo Z, Dong L, Tan Y, Yang J, Feng G, Wu M, Li Z, Wang H: CD133/prominin-1-mediated autophagy and glucose uptake beneficial for hepatoma cell survival. PLoS One 2013,8(2):e56878.PubMedCentralPubMedCrossRef
78.
go back to reference Shepherd CJ, Rizzo S, Ledaki I, Davies M, Brewer D, Attard G, de Bono J, Hudson DL: Expression profiling of CD133+ and CD133- epithelial cells from human prostate. Prostate 2008,68(9):1007–1024.PubMedCrossRef Shepherd CJ, Rizzo S, Ledaki I, Davies M, Brewer D, Attard G, de Bono J, Hudson DL: Expression profiling of CD133+ and CD133- epithelial cells from human prostate. Prostate 2008,68(9):1007–1024.PubMedCrossRef
79.
go back to reference Jaatinen T, Hemmoranta H, Hautaniemi S, Niemi J, Nicorici D, Laine J, Yli-Harja O, Partanen J: Global gene expression profile of human cord blood-derived CD133+ cells. Stem Cells 2006,24(3):631–641.PubMedCrossRef Jaatinen T, Hemmoranta H, Hautaniemi S, Niemi J, Nicorici D, Laine J, Yli-Harja O, Partanen J: Global gene expression profile of human cord blood-derived CD133+ cells. Stem Cells 2006,24(3):631–641.PubMedCrossRef
80.
go back to reference Yan X, Ma L, Yi D, Yoon JG, Diercks A, Foltz G, Price ND, Hood LE, Tian Q: A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci U S A 2011,108(4):1591–1596.PubMedCentralPubMedCrossRef Yan X, Ma L, Yi D, Yoon JG, Diercks A, Foltz G, Price ND, Hood LE, Tian Q: A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci U S A 2011,108(4):1591–1596.PubMedCentralPubMedCrossRef
81.
go back to reference Hemmoranta H, Hautaniemi S, Niemi J, Nicorici D, Laine J, Yli-Harja O, Partanen J, Jaatinen T: Transcriptional profiling reflects shared and unique characters for CD34+ and CD133+ cells. Stem Cells Dev 2006,15(6):839–851.PubMedCrossRef Hemmoranta H, Hautaniemi S, Niemi J, Nicorici D, Laine J, Yli-Harja O, Partanen J, Jaatinen T: Transcriptional profiling reflects shared and unique characters for CD34+ and CD133+ cells. Stem Cells Dev 2006,15(6):839–851.PubMedCrossRef
82.
go back to reference Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP: CD133(+) and CD133(−) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007,67(9):4010–4015.PubMedCrossRef Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP: CD133(+) and CD133(−) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007,67(9):4010–4015.PubMedCrossRef
83.
go back to reference Takenobu H, Shimozato O, Nakamura T, Ochiai H, Yamaguchi Y, Ohira M, Nakagawara A, Kamijo T: CD133 suppresses neuroblastoma cell differentiation via signal pathway modification. Oncogene 2011,30(1):97–105.PubMedCrossRef Takenobu H, Shimozato O, Nakamura T, Ochiai H, Yamaguchi Y, Ohira M, Nakagawara A, Kamijo T: CD133 suppresses neuroblastoma cell differentiation via signal pathway modification. Oncogene 2011,30(1):97–105.PubMedCrossRef
84.
go back to reference Aghideh AN, Kheirandish M, Abolghasemi H, Gharehbaghian A: Platelet growth factors suppress ex vivo expansion and enhance differentiation of umbilical cord blood CD133+ stem cells to megakaryocyte progenitor cells. Growth Factors 2010,28(6):409–416.PubMedCrossRef Aghideh AN, Kheirandish M, Abolghasemi H, Gharehbaghian A: Platelet growth factors suppress ex vivo expansion and enhance differentiation of umbilical cord blood CD133+ stem cells to megakaryocyte progenitor cells. Growth Factors 2010,28(6):409–416.PubMedCrossRef
85.
go back to reference Feng JM, Miao ZH, Jiang Y, Chen Y, Li JX, Tong LJ, Zhang J, Huang YR, Ding J: Characterization of the conversion between CD133 (+) and CD133 (−) cells in colon cancer SW620 cell line. Cancer Biol Ther 2012, 13: 14.CrossRef Feng JM, Miao ZH, Jiang Y, Chen Y, Li JX, Tong LJ, Zhang J, Huang YR, Ding J: Characterization of the conversion between CD133 (+) and CD133 (−) cells in colon cancer SW620 cell line. Cancer Biol Ther 2012, 13: 14.CrossRef
86.
go back to reference Ding W, Mouzaki M, You H, Laird JC, Mato J, Lu SC, Rountree CB: CD133+ liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis. Hepatology 2009,49(4):1277–1286.PubMedCentralPubMedCrossRef Ding W, Mouzaki M, You H, Laird JC, Mato J, Lu SC, Rountree CB: CD133+ liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis. Hepatology 2009,49(4):1277–1286.PubMedCentralPubMedCrossRef
87.
go back to reference Zobalova R, Stantic M, Prokopova K, Dong LF, Neuzil J: Cancer cells with high expression of CD133 exert FLIP upregulation and resistance to TRAIL-induced apoptosis. Biofactors 2008,34(3):231–235.PubMedCrossRef Zobalova R, Stantic M, Prokopova K, Dong LF, Neuzil J: Cancer cells with high expression of CD133 exert FLIP upregulation and resistance to TRAIL-induced apoptosis. Biofactors 2008,34(3):231–235.PubMedCrossRef
88.
go back to reference Zobalova R, McDermott L, Stantic M, Prokopova K, Dong LF, Neuzil J: CD133-positive cells are resistant to TRAIL due to up-regulation of FLIP. Biochem Biophys Res Commun 2008,373(4):567–571.PubMedCrossRef Zobalova R, McDermott L, Stantic M, Prokopova K, Dong LF, Neuzil J: CD133-positive cells are resistant to TRAIL due to up-regulation of FLIP. Biochem Biophys Res Commun 2008,373(4):567–571.PubMedCrossRef
89.
go back to reference Elsaba TM, Martinez-Pomares L, Robins AR, Crook S, Seth R, Jackson D, McCart A, Silver AR, Tomlinson IP, Ilyas M: The stem cell marker CD133 associates with enhanced colony formation and cell motility in colorectal cancer. PLoS One 2010,5(5):e10714.PubMedCentralPubMedCrossRef Elsaba TM, Martinez-Pomares L, Robins AR, Crook S, Seth R, Jackson D, McCart A, Silver AR, Tomlinson IP, Ilyas M: The stem cell marker CD133 associates with enhanced colony formation and cell motility in colorectal cancer. PLoS One 2010,5(5):e10714.PubMedCentralPubMedCrossRef
90.
go back to reference Zobalova R, Prokopova K, Stantic M, Stapelberg M, Dong LF, Ralph SJ, Akporiaye E, Neuzil J: The potential role of CD133 in immune surveillance and apoptosis: a mitochondrial connection? Antioxid Redox Signal 2011,15(12):2989–3002.PubMedCrossRef Zobalova R, Prokopova K, Stantic M, Stapelberg M, Dong LF, Ralph SJ, Akporiaye E, Neuzil J: The potential role of CD133 in immune surveillance and apoptosis: a mitochondrial connection? Antioxid Redox Signal 2011,15(12):2989–3002.PubMedCrossRef
91.
go back to reference Nishimura-Sakurai Y, Sakamoto N, Mogushi K, Nagaie S, Nakagawa M, Itsui Y, Tasaka-Fujita M, Onuki-Karakama Y, Suda G, Mishima K, et al.: Comparison of HCV-associated gene expression and cell signaling pathways in cells with or without HCV replicon and in replicon-cured cells. J Gastroenterol 2010,45(5):523–536.PubMedCrossRef Nishimura-Sakurai Y, Sakamoto N, Mogushi K, Nagaie S, Nakagawa M, Itsui Y, Tasaka-Fujita M, Onuki-Karakama Y, Suda G, Mishima K, et al.: Comparison of HCV-associated gene expression and cell signaling pathways in cells with or without HCV replicon and in replicon-cured cells. J Gastroenterol 2010,45(5):523–536.PubMedCrossRef
92.
go back to reference Paprocka M, Krawczenko A, Dus D, Kantor A, Carreau A, Grillon C, Kieda C: CD133 positive progenitor endothelial cell lines from human cord blood. Cytometry A 2011,79(8):594–602.PubMedCrossRef Paprocka M, Krawczenko A, Dus D, Kantor A, Carreau A, Grillon C, Kieda C: CD133 positive progenitor endothelial cell lines from human cord blood. Cytometry A 2011,79(8):594–602.PubMedCrossRef
93.
go back to reference Kamei N, Kwon SM, Alev C, Nakanishi K, Yamada K, Masuda H, Ishikawa M, Kawamoto A, Ochi M, Asahara T: Ex-vivo expanded human blood-derived CD133(+) cells promote repair of injured spinal cord. J Neurol Sci 2013,328(1–2):41–50.PubMedCrossRef Kamei N, Kwon SM, Alev C, Nakanishi K, Yamada K, Masuda H, Ishikawa M, Kawamoto A, Ochi M, Asahara T: Ex-vivo expanded human blood-derived CD133(+) cells promote repair of injured spinal cord. J Neurol Sci 2013,328(1–2):41–50.PubMedCrossRef
94.
go back to reference Kijima Y, Ishikawa M, Sunagawa T, Nakanishi K, Kamei N, Yamada K, Tanaka N, Kawamata S, Asahara T, Ochi M: Regeneration of peripheral nerve after transplantation of CD133+ cells derived from human peripheral blood. J Neurosurg 2009,110(4):758–767.PubMedCrossRef Kijima Y, Ishikawa M, Sunagawa T, Nakanishi K, Kamei N, Yamada K, Tanaka N, Kawamata S, Asahara T, Ochi M: Regeneration of peripheral nerve after transplantation of CD133+ cells derived from human peripheral blood. J Neurosurg 2009,110(4):758–767.PubMedCrossRef
95.
go back to reference Shi M, Ishikawa M, Kamei N, Nakasa T, Adachi N, Deie M, Asahara T, Ochi M: Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 2009,27(4):949–960.PubMedCrossRef Shi M, Ishikawa M, Kamei N, Nakasa T, Adachi N, Deie M, Asahara T, Ochi M: Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 2009,27(4):949–960.PubMedCrossRef
96.
go back to reference Adler DS, Lazarus H, Nair R, Goldberg JL, Greco NJ, Lassar T, Laughlin MJ, Das H, Pompili VJ: Safety and efficacy of bone marrow-derived autologous CD133+ stem cell therapy. Front Biosci 2011, 3: 506–514.CrossRef Adler DS, Lazarus H, Nair R, Goldberg JL, Greco NJ, Lassar T, Laughlin MJ, Das H, Pompili VJ: Safety and efficacy of bone marrow-derived autologous CD133+ stem cell therapy. Front Biosci 2011, 3: 506–514.CrossRef
97.
go back to reference Ahmadi H, Baharvand H, Ashtiani SK, Soleimani M, Sadeghian H, Ardekani JM, Mehrjerdi NZ, Kouhkan A, Namiri M, Madani-Civi M, et al.: Safety analysis and improved cardiac function following local autologous transplantation of CD133(+) enriched bone marrow cells after myocardial infarction. Curr Neurovasc Res 2007,4(3):153–160.PubMedCrossRef Ahmadi H, Baharvand H, Ashtiani SK, Soleimani M, Sadeghian H, Ardekani JM, Mehrjerdi NZ, Kouhkan A, Namiri M, Madani-Civi M, et al.: Safety analysis and improved cardiac function following local autologous transplantation of CD133(+) enriched bone marrow cells after myocardial infarction. Curr Neurovasc Res 2007,4(3):153–160.PubMedCrossRef
98.
go back to reference Nikeghbalian S, Pournasr B, Aghdami N, Rasekhi A, Geramizadeh B, Hosseini Asl SM, Ramzi M, Kakaei F, Namiri M, Malekzadeh R, et al.: Autologous transplantation of bone marrow-derived mononuclear and CD133(+) cells in patients with decompensated cirrhosis. Arch Iran Med 2011,14(1):12–17.PubMed Nikeghbalian S, Pournasr B, Aghdami N, Rasekhi A, Geramizadeh B, Hosseini Asl SM, Ramzi M, Kakaei F, Namiri M, Malekzadeh R, et al.: Autologous transplantation of bone marrow-derived mononuclear and CD133(+) cells in patients with decompensated cirrhosis. Arch Iran Med 2011,14(1):12–17.PubMed
99.
go back to reference AmEsch JS, Knoefel WT, Klein M, Ghodsizad A, Fuerst G, Poll LW, Piechaczek C, Burchardt ER, Feifel N, Stoldt V, et al.: Portal application of autologous CD133+ bone marrow cells to the liver: a novel concept to support hepatic regeneration. Stem Cells 2005,23(4):463–470.CrossRef AmEsch JS, Knoefel WT, Klein M, Ghodsizad A, Fuerst G, Poll LW, Piechaczek C, Burchardt ER, Feifel N, Stoldt V, et al.: Portal application of autologous CD133+ bone marrow cells to the liver: a novel concept to support hepatic regeneration. Stem Cells 2005,23(4):463–470.CrossRef
100.
go back to reference Ceballos MP, Parody JP, Alvarez Mde L, Ingaramo PI, Carnovale CE, Carrillo MC: Interferon-alpha2b and transforming growth factor-beta1 treatments on HCC cell lines: Are Wnt/beta-catenin pathway and Smads signaling connected in hepatocellular carcinoma? Biochem Pharmacol 2011,82(11):1682–1691.PubMedCrossRef Ceballos MP, Parody JP, Alvarez Mde L, Ingaramo PI, Carnovale CE, Carrillo MC: Interferon-alpha2b and transforming growth factor-beta1 treatments on HCC cell lines: Are Wnt/beta-catenin pathway and Smads signaling connected in hepatocellular carcinoma? Biochem Pharmacol 2011,82(11):1682–1691.PubMedCrossRef
101.
go back to reference Cao Y, Zhang W, Gao X, Zhang G, Falzon M, Townsend CM Jr, Hellmich MR, Ko TC: PTHrP is a novel mediator for TGF-beta-induced apoptosis. Regul Pept 2013, 184: 40–46.PubMedCentralPubMedCrossRef Cao Y, Zhang W, Gao X, Zhang G, Falzon M, Townsend CM Jr, Hellmich MR, Ko TC: PTHrP is a novel mediator for TGF-beta-induced apoptosis. Regul Pept 2013, 184: 40–46.PubMedCentralPubMedCrossRef
102.
go back to reference Ueno T, Hashimoto O, Kimura R, Torimura T, Kawaguchi T, Nakamura T, Sakata R, Koga H, Sata M: Relation of type II transforming growth factor-beta receptor to hepatic fibrosis and hepatocellular carcinoma. Int J Oncol 2001,18(1):49–55.PubMed Ueno T, Hashimoto O, Kimura R, Torimura T, Kawaguchi T, Nakamura T, Sakata R, Koga H, Sata M: Relation of type II transforming growth factor-beta receptor to hepatic fibrosis and hepatocellular carcinoma. Int J Oncol 2001,18(1):49–55.PubMed
Metadata
Title
CD133: a stem cell biomarker and beyond
Author
Zhong Li
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Experimental Hematology & Oncology / Issue 1/2013
Electronic ISSN: 2162-3619
DOI
https://doi.org/10.1186/2162-3619-2-17

Other articles of this Issue 1/2013

Experimental Hematology & Oncology 1/2013 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine