CD133, Stem Cells, and Cancer Stem Cells: Myth or Reality?
Tóm tắt
CD133, a member of the prominin family, is found in a variety of tissues with at least three variants. The function of CD133 is not well understood, but its expression is subject to changes in the microenvironment cues including bioenergetic stress. Knockout of CD133 does not affect renewal, but mammary gland branching. A point mutation of CD133 (R733C) leads to retinal disorder. CD133 is found in embryonic stem cells, normal tissue stem cells, stem cell niches, and circulating endothelial progenitors as well as cancer stem cells. Maintenance of stemness in cancer may be attributable to asymmetric cell division in association with a set of embryonic expression signatures in CD133+ tumor cells. CD133 could enrich cancer stem cells, which are associated with chemo- and radiation resistance phenotype. High CD133 is associated with poor survival in a variety of solid tumors, including lung, colon, prostate, etc. Monitoring CD133+ cells in peripheral blood, and targeting CD133 in cancer, may further predict and improve the clinical outcomes.
Tài liệu tham khảo
•• Yin AH, Miraglia S, Zanjani ED, et al.: AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997;90:5002–12. This is the first paper that links AC133, later now named as CD133, to stem cells.
• Miraglia S, Godfrey W, Yin AH, et al.: A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 1997;90:5013–21. This is the first paper to clone the CD133.
Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964–7.
•• Shaked Y, Ciarrocchi A, Franco M, et al.: Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 2006;313:1785–7. This is the first paper to highlight the importance of endothelial progenitor cells.
•• Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al.: Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111–5. This is the first paper to isolate colon cancer stem cells.
Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401.
Zhu L, Gibson P, Currle DS, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457:603–7.
Ma S, Lee TK, Zheng BJ, et al. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene. 2008;27:1749–58.
Chen YC, Hsu HS, Chen YW, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3:e2637.
Stewart JM, Shaw PA, Gedye C, et al. Phenotypic heterogeneity and instability of human ovarian tumor-initiating cells. Proc Natl Acad Sci U S A. 2011;108:6468–73.
Bertolini G, Roz L, Perego P, et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci U S A. 2009;106:16281–6.
Leong KG, Wang BE, Johnson L, Gao WQ. Generation of a prostate from a single adult stem cell. Nature. 2008;456:804–8.
Vermeulen L, Todaro M, de Sousa Mello F, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A. 2008;105:13427–32.
• Wang R, Chadalavada K, Wilshire J, et al.: Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010;468:829–33. This paper links the stem cells to tumor angiogenesis directly via CD133-expressing cells.
Shmelkov SV, Butler JM, Hooper AT, 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;118:2111–20.
Collins AT, Berry PA, Hyde C, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–51.
Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.
Dalerba P, Dylla SJ, Park IK, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A. 2007;104:10158–63.
Huang EH, Hynes MJ, Zhang T, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res. 2009;69:3382–9.
Yin C, Lin Y, Zhang X, et al. Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor-4alpha gene. Hepatology. 2008;48:1528–39.
Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.
Roesch A, Fukunaga-Kalabis M, Schmidt EC, et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell. 2010;141:583–94.
Pece S, Tosoni D, Confalonieri S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010;140:62–73.
Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev. 2008;18:48–53.
Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer. 2011;11:254–67.
Todaro M, Francipane MG, Medema JP, Stassi G. Colon cancer stem cells: promise of targeted therapy. Gastroenterology. 2010;138:2151–62.
Marhaba R, Klingbeil P, Nuebel T, et al. CD44 and EpCAM: cancer-initiating cell markers. Curr Mol Med. 2008;8:784–804.
Fargeas CA, Florek M, Huttner WB, Corbeil D. Characterization of prominin-2, a new member of the prominin family of pentaspan membrane glycoproteins. J Biol Chem. 2003;278:8586–96.
Fargeas CA, Joester A, Missol-Kolka E, et al. Identification of novel Prominin-1/CD133 splice variants with alternative C-termini and their expression in epididymis and testis. J Cell Sci. 2004;117:4301–11.
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;584:1659–64.
Corbeil D, Roper K, Hannah MJ, et al. Selective localization of the polytopic membrane protein prominin in microvilli of epithelial cells - a combination of apical sorting and retention in plasma membrane protrusions. J Cell Sci. 1999;112(Pt 7):1023–33.
• Pine SR, Ryan BM, Varticovski L, et al.: Microenvironmental modulation of asymmetric cell division in human lung cancer cells. Proc Natl Acad Sci U S A 2010;107:2195–200. This is the first paper to link CD133 to asymmetric division in lung cancer cells.
Anderson LH, Boulanger CA, Smith GH, et al.: Stem cell marker prominin-1 regulates branching morphogenesis, but not regenerative capacity, in the mammary gland. Dev Dyn 2011.
Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol. 2008;26:2862–70.
Hermann PC, Huber SL, Herrler T, 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.
Jaksch M, Munera J, Bajpai R, et al. Cell cycle-dependent variation of a CD133 epitope in human embryonic stem cell, colon cancer, and melanoma cell lines. Cancer Res. 2008;68:7882–6.
Kim M, Koh YJ, Kim KE, et al. CXCR4 signaling regulates metastasis of chemoresistant melanoma cells by a lymphatic metastatic niche. Cancer Res. 2010;70:10411–21.
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.
Shimada M, Sugimoto K, Iwahashi S, et al. CD133 expression is a potential prognostic indicator in intrahepatic cholangiocarcinoma. J Gastroenterol. 2010;45:896–902.
Ma S, Chan KW, Lee TK, et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res. 2008;6:1146–53.
Silva IA, Bai S, McLean K, et al.: Aldehyde dehydrogenase and CD133 define angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 2011.
Horst D, Kriegl L, Engel J, et al. CD133 and nuclear beta-catenin: the marker combination to detect high risk cases of low stage colorectal cancer. Eur J Cancer. 2009;45:2034–40.
Matsumoto K, Arao T, Tanaka K, et al. mTOR signal and hypoxia-inducible factor-1 alpha regulate CD133 expression in cancer cells. Cancer Res. 2009;69:7160–4.
Yi JM, Tsai HC, Glockner SC, et al. Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res. 2008;68:8094–103.
Baba T, Convery PA, Matsumura N, et al. Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene. 2009;28:209–18.
Xia H, Cheung WK, Sze J, et al. miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and beta-catenin signaling. J Biol Chem. 2010;285:36995–7004.
Ma S, Tang KH, Chan YP, 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;7:694–707.
Ji Q, Hao X, Zhang M, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 2009;4:e6816.
•• Yan X, Ma L, Yi D, et al.: A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci U S A 2011;108:1591–6. This is the first paper to describe a CD133-related gene expression signature in GBM, and these signatures are shared among other tumor types.
Liang Y, Zhong Z, Huang Y, et al. Stem-like cancer cells are inducible by increasing genomic instability in cancer cells. J Biol Chem. 2010;285:4931–40.
Li CY, Li BX, Liang Y, 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.
Xi HQ, Zhao P: Clinicopathological significance and prognostic value of EphA3 and CD133 expression in colorectal carcinoma. J Clin Pathol 2011.
•• Artells R, Moreno I, Diaz T, et al.: Tumour CD133 mRNA expression and clinical outcome in surgically resected colorectal cancer patients. Eur J Cancer 2010;46:642–9. Prognostic value of CD133 mRNA in colorectal cancer is proposed.
Horst D, Kriegl L, Engel J, et al. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer. 2008;99:1285–9.
Ishigami S, Ueno S, Arigami T, et al. Prognostic impact of CD133 expression in gastric carcinoma. Anticancer Res. 2010;30:2453–7.
Metellus P, Nanni-Metellus I, Delfino C, et al.: Prognostic Impact of CD133 mRNA Expression in 48 Glioblastoma Patients Treated with Concomitant Radiochemotherapy: A Prospective Patient Cohort at a Single Institution. Ann Surg Oncol 2011.
Sasaki A, Kamiyama T, Yokoo H, et al. Cytoplasmic expression of CD133 is an important risk factor for overall survival in hepatocellular carcinoma. Oncol Rep. 2010;24:537–46.
Nakamura M, Kyo S, Zhang B, et al. Prognostic impact of CD133 expression as a tumor-initiating cell marker in endometrial cancer. Hum Pathol. 2010;41:1516–29.
Woo T, Okudela K, Mitsui H, et al. Prognostic value of CD133 expression in stage I lung adenocarcinomas. Int J Clin Exp Pathol. 2010;4:32–42.
Levina V, Marrangoni AM, DeMarco R, et al. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS One. 2008;3:e3077.
Todaro M, Alea MP, Di Stefano AB, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1:389–402.
Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.
Murat A, Migliavacca E, Gorlia T, et al. Stem cell-related “self-renewal” signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol. 2008;26:3015–24.
Saigusa S, Tanaka K, Toiyama Y, et al. Correlation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapy. Ann Surg Oncol. 2009;16:3488–98.
Nagata T, Sakakura C, Komiyama S, et al. Expression of cancer stem cell markers CD133 and CD44 in locoregional recurrence of rectal cancer. Anticancer Res. 2011;31:495–500.
Borovski T, De Sousa EMF, Vermeulen L, Medema JP. Cancer stem cell niche: the place to be. Cancer Res. 2011;71:634–9.
Kaplan RN, Riba RD, Zacharoulis S, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.
•• Lin EH, Hassan M, Li Y, et al.: Elevated circulating endothelial progenitor marker CD133 messenger RNA levels predict colon cancer recurrence. Cancer 2007;110:534–42. This is the first paper to describe the prognostic value of CD133 mRNA in colorectal cancer.
Dome B, Timar J, Dobos J, et al. Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer. Cancer Res. 2006;66:7341–7.
Mehra N, Penning M, Maas J, et al. Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases. Clin Cancer Res. 2006;12:4859–66.
•• Iinuma H, Watanabe T, Mimori K, et al.: Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ Stage B and C Colorectal Cancer. J Clin Oncol 2011. This is the first paper to describe the role of CD133 mRNA in stage B and C colorectal cancer.
Iinuma H, Okinaga K, Egami H, et al. Usefulness and clinical significance of quantitative real-time RT-PCR to detect isolated tumor cells in the peripheral blood and tumor drainage blood of patients with colorectal cancer. Int J Oncol. 2006;28:297–306.
Nakamura K, Iinuma H, Aoyagi Y, et al. Predictive value of cancer stem-like cells and cancer-associated genetic markers for peritoneal recurrence of colorectal cancer in patients after curative surgery. Oncology. 2010;78:309–15.
Tralhao JG, Hoti E, Serodio M, et al. Perioperative tumor cell dissemination in patients with primary or metastatic colorectal cancer. Eur J Surg Oncol. 2010;36:125–9.
Vroling L, Lind JS, de Haas RR, et al. CD133+ circulating haematopoietic progenitor cells predict for response to sorafenib plus erlotinib in non-small cell lung cancer patients. Br J Cancer. 2010;102:268–75.
Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med. 2004;10:145–7.
Calleri A, Bono A, Bagnardi V, et al. Predictive potential of angiogenic growth factors and circulating endothelial cells in breast cancer patients receiving metronomic chemotherapy plus bevacizumab. Clin Cancer Res. 2009;15:7652–7.
Smith LM, Nesterova A, Ryan MC, et al. CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer. 2008;99:100–9.
Gedye C, Quirk J, Browning J, et al. Cancer/testis antigens can be immunological targets in clonogenic CD133+ melanoma cells. Cancer Immunol Immunother. 2009;58:1635–46.
Rappa G, Fodstad O, Lorico A. The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells. 2008;26:3008–17.
Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–59.
Zhou BB, Zhang H, Damelin M, et al. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov. 2009;8:806–23.
Lin E, He X, Yan XW, et al.: Efficiently targeting cancer stem cells requires tactical activation from their dormant state and subsequent exhaustion. Proceedings of American Association of Cancer Research 2010;LB254.