Identification of cancer stem cells provides novel tumor models for drug discovery

Douglas D. Fang, Danyi Wen, Yajun Xu

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Front. Med. ›› 2012, Vol. 6 ›› Issue (2) : 112-121. DOI: 10.1007/s11684-012-0199-1
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Identification of cancer stem cells provides novel tumor models for drug discovery

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Abstract

Cancer stem cells (CSCs) have received considerable attention from the research community since they were first reported in human acute myeloid leukemia 15 years ago. Accumulating evidence suggests that CSCs are responsible for tumor initiation and progression, drug resistance, and metastasis in both liquid and solid tumors. These findings lead to the development of novel compounds targeting CSC populations that is becoming increasingly important for eradicating CSCs in heterogeneous tumor masses and to cure the cancer. Since 2003, we have participated in CSC studies and encountered crucial early events in the field. This article reviews the history of CSC biology, clarifies the term and its definition, and further addresses the issue of how to utilize CSCs in therapeutic target discovery and drug development based on our substantial experience.

Keywords

cancer stem cell / tumor model / drug discovery

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Douglas D. Fang, Danyi Wen, Yajun Xu. Identification of cancer stem cells provides novel tumor models for drug discovery. Front Med, 2012, 6(2): 112‒121 https://doi.org/10.1007/s11684-012-0199-1

References

[1]
Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414(6859): 105-111
CrossRef Pubmed Google scholar
[2]
Sirard C, Lapidot T, Vormoor J, Cashman JD, Doedens M, Murdoch B, Jamal N, Messner H, Addey L, Minden M, Laraya P, Keating A, Eaves A, Lansdorp PM, Eaves CJ, Dick JE. Normal and leukemic SCID-repopulating cells (SRC) coexist in the bone marrow and peripheral blood from CML patients in chronic phase, whereas leukemic SRC are detected in blast crisis. Blood 1996; 87(4): 1539-1548
Pubmed
[3]
Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145-1147
CrossRef Pubmed Google scholar
[4]
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): 3983-3988
CrossRef Pubmed Google scholar
[5]
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63(18): 5821-5828
Pubmed
[6]
Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432(7015): 396-401
CrossRef Pubmed Google scholar
[7]
Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005; 65(20): 9328-9337
CrossRef Pubmed Google scholar
[8]
Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K, Coghlan L, Tang DG. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006; 25(12): 1696-1708
CrossRef Pubmed Google scholar
[9]
Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007; 104(3): 973-978
CrossRef Pubmed Google scholar
[10]
Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 2006; 351(4): 820-824
CrossRef Pubmed Google scholar
[11]
Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67(3): 1030-1037
CrossRef Pubmed Google scholar
[12]
Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007; 1(3): 313-323
CrossRef Pubmed Google scholar
[13]
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): 106-110
CrossRef Pubmed Google scholar
[14]
Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445(7123): 111-115
CrossRef Pubmed Google scholar
[15]
Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, Shelton AA, Parmiani G, Castelli C, Clarke MF. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007; 104(24): 10158-10163
CrossRef Pubmed Google scholar
[16]
Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, Gritti A, Piccinini A, Porro D, Santinami M, Invernici G, Parati E, Alessandri G, La Porta CA. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007; 43(5): 935-946
CrossRef Pubmed Google scholar
[17]
Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15(3): 504-514
CrossRef Pubmed Google scholar
[18]
Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008; 68(11): 4311-4320
CrossRef Pubmed Google scholar
[19]
Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH. Identification of cells initiating human melanomas. Nature 2008; 451(7176): 345-349
CrossRef Pubmed Google scholar
[20]
Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008; 13(2): 153-166
CrossRef Pubmed Google scholar
[21]
Suvà ML, Riggi N, Stehle JC, Baumer K, Tercier S, Joseph JM, Suvà D, Clément V, Provero P, Cironi L, Osterheld MC, Guillou L, Stamenkovic I. Identification of cancer stem cells in Ewing’s sarcoma. Cancer Res 2009; 69(5): 1776-1781
CrossRef Pubmed Google scholar
[22]
Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, Huang Z, Bentley RC, Mori S, Fujii S, Marks JR, Berchuck A, Murphy SK. Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 2009; 28(2): 209-218
CrossRef Pubmed Google scholar
[23]
Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. Cancer stem cells—perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66(19): 9339-9344
CrossRef Pubmed Google scholar
[24]
Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5(1): 6
CrossRef Pubmed Google scholar
[25]
Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, Tripodo C, Russo A, Gulotta G, Medema JP, Stassi G. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell2007; 1(4): 389-402
CrossRef Pubmed Google scholar
[26]
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. Oncogene2008; 27(12): 1749-1758
CrossRef Pubmed Google scholar
[27]
Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006; 98(24): 1777-1785
CrossRef Pubmed Google scholar
[28]
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444(7120): 756-760
CrossRef Pubmed Google scholar
[29]
Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S, Clarke MF, Hoey T, Lewicki J, Gurney AL. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 2008; 3(6): e2428
CrossRef Pubmed Google scholar
[30]
Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133(4): 704-715
CrossRef Pubmed Google scholar
[31]
Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, Houvenaeghel G, Extra JM, Bertucci F, Jacquemier J, Xerri L, Dontu G, Stassi G, Xiao Y, Barsky SH, Birnbaum D, Viens P, Wicha MS. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010; 16(1): 45-55
CrossRef Pubmed Google scholar
[32]
Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK, Ng L, Cheung LW, Lan XR, Lan HY, Tan VP, Yau TC, Poon RT, Wong BC. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell2010; 6(6): 603-615
CrossRef Pubmed Google scholar
[33]
Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, Caldwell MA. A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 1998; 85(2): 141-152
CrossRef Pubmed Google scholar
[34]
Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000; 97(26): 14720-14725
CrossRef Pubmed Google scholar
[35]
Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003; 100(25): 15178-15183
CrossRef Pubmed Google scholar
[36]
Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65(13): 5506-5511
CrossRef Pubmed Google scholar
[37]
Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, Steindler DA. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 2005; 7(11): 967-976
CrossRef Pubmed Google scholar
[38]
Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005; 65(8): 3025-3029
Pubmed
[39]
Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, Sesterhenn IA, McLeod DG, Srivastava S, Rhim JS. 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): 3153-3161
CrossRef Pubmed Google scholar
[40]
Gou S, Liu T, Wang C, Yin T, Li K, Yang M, Zhou J. Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas 2007; 34(4): 429-435
CrossRef Pubmed Google scholar
[41]
Yu H, Fang D, Kumar SM, Li L, Nguyen TK, Acs G, Herlyn M, Xu X. Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 2006; 168(6): 1879-1888
CrossRef Pubmed Google scholar
[42]
Fang DD, Kim YJ, Lee CN, Aggarwal S, McKinnon K, Mesmer D, Norton J, Birse CE, He T, Ruben SM, Moore PA. 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
CrossRef Pubmed Google scholar
[43]
Fang DD, Cao J, Jani J, Tsaparikos K, Blasina A, Kornmann J, Lira ME, Wang J, Bingham J, VanArsdale T, Los G, Hostomsky Z. Establishing a three-dimensional in vitro tumor spheroid model with cancer stem cell characteristics for drug evaluation (AACR annual meeting, Apr 18-22, 2009; Denver, CO)
[44]
Fang DD, Gu Y, Tsaparikos K, Thiel M, Jackson-Fisher A, Cao J, Zong Q, Lira ME, Jani J, Hayashi T, Schwab R, Wong A, John-Baptiste A, Lappin PB, Cheng H, Bender S, Bagrodia S, Yin MJ, VanArsdale T. Establishing patient-derived colorectal cancer stem cell models with a PIK3CA mutation for the development of inhibitory drugs as targeted therapies (AACR annual meeting, Apr 17-21, 2010; Washington DC)
[45]
Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006; 9(5): 391-403
CrossRef Pubmed Google scholar
[46]
De Witt Hamer PC, Van Tilborg AA, Eijk PP, Sminia P, Troost D, Van Noorden CJ, Ylstra B, Leenstra S. The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 2008; 27(14): 2091-2096
CrossRef Pubmed Google scholar
[47]
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): 781-786
CrossRef Pubmed Google scholar
[48]
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): 3722-3727
CrossRef Pubmed Google scholar
[49]
Rappa G, Mercapide J, Anzanello F, Prasmickaite L, Xi Y, Ju J, Fodstad O, Lorico A. Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets. Exp Cell Res 2008; 314(10): 2110-2122
CrossRef Pubmed Google scholar
[50]
Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101(39): 14228-14233
CrossRef Pubmed Google scholar
[51]
Fukaya R, Ohta S, Yamaguchi M, Fujii H, Kawakami Y, Kawase T, Toda M. Isolation of cancer stem-like cells from a side population of a human glioblastoma cell line, SK-MG-1. Cancer Lett 2010; 291(2): 150-157
CrossRef Pubmed Google scholar
[52]
Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009; 69(4): 1302-1313
CrossRef Pubmed Google scholar
[53]
Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, Korkaya H, Heath A, Dutcher J, Kleer CG, Jung Y, Dontu G, Taichman R, Wicha MS. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 2011; 71(2): 614-624
CrossRef Pubmed Google scholar
[54]
Goldstein RH, Reagan MR, Anderson K, Kaplan DL, Rosenblatt M. Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis. Cancer Res 2010; 70(24): 10044-10050
CrossRef Pubmed Google scholar
[55]
Studeny M, Marini FC, Dembinski JL, Zompetta C, Cabreira-Hansen M, Bekele BN, Champlin RE, Andreeff M. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 2004; 96(21): 1593-1603
CrossRef Pubmed Google scholar
[56]
Mishra PJ, Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, Ganesan S, Glod JW, Banerjee D. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 2008; 68(11): 4331-4339
CrossRef Pubmed Google scholar
[57]
Spaeth EL, Dembinski JL, Sasser AK, Watson K, Klopp A, Hall B, Andreeff M, Marini F. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS ONE 2009; 4(4): e4992
CrossRef Pubmed Google scholar
[58]
Bagley RG, Weber W, Rouleau C, Yao M, Honma N, Kataoka S, Ishida I, Roberts BL, Teicher BA. Human mesenchymal stem cells from bone marrow express tumor endothelial and stromal markers. Int J Oncol 2009; 34(3): 619-627
CrossRef Pubmed Google scholar
[59]
Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449(7162): 557-563
CrossRef Pubmed Google scholar
[60]
Shinagawa K, Kitadai Y, Tanaka M, Sumida T, Kodama M, Higashi Y, Tanaka S, Yasui W, Chayama K. Mesenchymal stem cells enhance growth and metastasis of colon cancer. Int J Cancer 2010; 127(10): 2323-2333
CrossRef Pubmed Google scholar
[61]
Lis R, Touboul C, Mirshahi P, Ali F, Mathew S, Nolan DJ, Maleki M, Abdalla SA, Raynaud CM, Querleu D, Al-Azwani E, Malek J, Mirshahi M, Rafii A. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer 2011; 128(3): 715-725
CrossRef Pubmed Google scholar
[62]
McMillin DW, Delmore J, Weisberg E, Negri JM, Geer DC, Klippel S, Mitsiades N, Schlossman RL, Munshi NC, Kung AL, Griffin JD, Richardson PG, Anderson KC, Mitsiades CS. Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat Med 2010; 16(4): 483-489
CrossRef Pubmed Google scholar
[63]
Lee J, Fassnacht M, Nair S, Boczkowski D, Gilboa E. Tumor immunotherapy targeting fibroblast activation protein, a product expressed in tumor-associated fibroblasts. Cancer Res 2005; 65(23): 11156-11163
CrossRef Pubmed Google scholar
[64]
Schwartz DL, Powis G, Thitai-Kumar A, He Y, Bankson J, Williams R, Lemos R, Oh J, Volgin A, Soghomonyan S, Nishii R, Alauddin M, Mukhopadhay U, Peng Z, Bornmann W, Gelovani J. The selective hypoxia inducible factor-1 inhibitor PX-478 provides in vivo radiosensitization through tumor stromal effects. Mol Cancer Ther 2009; 8(4): 947-958
CrossRef Pubmed Google scholar
[65]
Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, Frese KK, Denicola G, Feig C, Combs C, Winter SP, Ireland-Zecchini H, Reichelt S, Howat WJ, Chang A, Dhara M, Wang L, Rückert F, Grützmann R, Pilarsky C, Izeradjene K, Hingorani SR, Huang P, Davies SE, Plunkett W, Egorin M, Hruban RH, Whitebread N, McGovern K, Adams J, Iacobuzio-Donahue C, Griffiths J, Tuveson DA. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324(5933): 1457-1461
CrossRef Pubmed Google scholar
[66]
Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 2009; 457(7229): 603-607
CrossRef Pubmed Google scholar
[67]
Liu HK, Wang Y, Belz T, Bock D, Takacs A, Radlwimmer B, Barbus S, Reifenberger G, Lichter P, Schütz G. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev 2010; 24(7): 683-695
CrossRef Pubmed Google scholar
[68]
Youssef KK, Van Keymeulen A, Lapouge G, Beck B, Michaux C, Achouri Y, Sotiropoulou PA, Blanpain C. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 2010; 12(3): 299-305
Pubmed
[69]
Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, kConFab, Fox SB, Yan M, French JD, Brown MA, Smyth GK, Visvader JE, Lindeman GJ. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009; 15(8): 907-913
CrossRef Pubmed Google scholar
[70]
Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, Tamaki Y, Noguchi S. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 2009; 15(12): 4234-4241
CrossRef Pubmed Google scholar

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