Expansion of CD133+ colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery

British Journal of Cancer

Volumn 102, Issue 8, 2010, Pages 1265-1275

  Fang, D D ^a,c   Kim, Y J ^a,d   Lee, C N ^a   Aggarwal, S ^a   McKinnon, K ^a   Mesmer, D ^a   Norton, J ^a   Birse, C E ^a   He, T ^a,c   Ruben, S M ^a   Moore, P A ^a,b  

^a Celera Genomics   (United States)

^b Analytical Sciences   (United States)

^c PFIZER INC   (United States)

^d BRISTOL MYERS SQUIBB   (United States)

Author keywords

CD133; Colon cancer; CSC; Drug resistance; Drug target; Mass spectrometry

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; BETA1 INTEGRIN; BIGLYCAN; CADHERIN; CD133 ANTIGEN; HERMES ANTIGEN; IRINOTECAN;

ANTIGEN EXPRESSION; ARTICLE; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; COLON CANCER; COLORECTAL CANCER; HUMAN; IN VITRO PROPAGATION; IN VITRO STUDY; MASS SPECTROMETRY; PHENOTYPE; PRIORITY JOURNAL; PROGENY; SPHEROID CELL; THERAPY RESISTANCE; TUMOR SPHEROID;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, CD; ATP-BINDING CASSETTE TRANSPORTERS; CELL DIFFERENTIATION; COLONIC NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; GLYCOPROTEINS; HUMANS; MALE; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; MICE, NUDE; MICE, SCID; MIDDLE AGED; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PEPTIDES; PROTEOMICS; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 77950863856     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605610     Document Type: Article

References (47)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988 (Pubitemid 36418143)
2. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760 (Pubitemid 44949604)
3. Bapat SA, Mali AM, Koppikar CB, Kurrey NK (2005) Stem and progenitorlike cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65: 3025-3029
4. Beier D, Wischhusen J, Dietmaier W, Hau P, Proescholdt M, Brawanski A, Bogdahn U, Beier CP (2008) CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors. Brain Pathol 18: 370-377 (Pubitemid 351782845)
5. Blumenthal RD, Hansen HJ, Goldenberg DM (2005) Inhibition of adhesion, invasion, and metastasis by antibodies targeting CEACAM6 (NCA-90) and CEACAM5 (carcinoembryonic antigen). Cancer Res 65: 8809-8817
6. Bobbitt JM (1956) Periodate oxidation of carbohydrates. Adv Carbohydr Chem 48: 1-41
7. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737 (Pubitemid 27298715)
8. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83
9. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM (2006) Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344 (Pubitemid 44623625)
10. Costello RT, Mallet F, Gaugler B, Sainty D, Arnoulet C, Gastaut JA, Olive D (2000) Human acute myeloid leukemia CD34+/CD38- progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res 60: 4403-4411 (Pubitemid 32103618)
11. 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 (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104: 10158-10163 (Pubitemid 47175279)
12. De Witt Hamer PC, Van Tilborg AA, Eijk PP, Sminia P, Troost D, Van Noorden CJ, Ylstra B, Leenstra S (2008) The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 27: 2091-2096 (Pubitemid 351442747)
13. Dick JE (2009) Looking ahead in cancer stem cell research. Nat Biotechnol 27: 44-46
14. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504-514 (Pubitemid 351267301)
15. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, Eberhart CG (2006) Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66: 7445-7452 (Pubitemid 44289197)
16. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65: 9328-9337 (Pubitemid 41508000)
17. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659
18. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100: 15178-15183 (Pubitemid 37518036)
19. Hinoi T, Lucas PC, Kuick R, Hanash S, Cho KR, Fearon ER (2002) CDX2 regulates liver intestine-cadherin expression in normal and malignant colon epithelium and intestinal metaplasia. Gastroenterology 123: 1565-1577 (Pubitemid 35231656)
20. Ishida H, Miwa H, Tatsuta M, Masutani S, Imamura H, Shimizu J, Ezumi K, Kato H, Kawasaki T, Furukawa H, Kawakami H (2004) Ki-67 and CEA expression as prognostic markers in Dukes' C colorectal cancer. Cancer Lett 207: 109-115 (Pubitemid 38429893)
21. Kim YJ, Feild B, Fitzhugh W, Heidbrink JL, Duff JW, Heil J, Ruben SM, He T (2009) Reference map for liquid chromatography- mass spectrometrybased quantitative proteomics. Anal Biochem 393: 155-162
22. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serumcultured cell lines. Cancer Cell 9: 391-403 (Pubitemid 43668737)
23. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260 (Pubitemid 40852690)
24. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037 (Pubitemid 46270758)
25. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5: 67 (Pubitemid 44942887)
26. 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 (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715 (Pubitemid 351636299)
27. Nishimura S, Wakabayashi N, Toyoda K, Kashima K, Mitsufuji S (2003) Expression of Musashi-1 in human normal colon crypt cells: a possible stem cell marker of human colon epithelium. Dig Dis Sci 48: 1523-1529 (Pubitemid 36936688)
28. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110 (Pubitemid 46067310)
29. 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 (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25: 1696-1708
30. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(/low)/ CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785 (Pubitemid 46017929)
31. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi AL (2006) Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765 (Pubitemid 44949605)
32. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511 (Pubitemid 40911148)
33. Rebetz J, Tian D, Persson A, Widegren B, Salford LG, Englund E, Gisselsson D, Fan X (2008) Glial progenitor-like phenotype in low-grade glioma and enhanced CD133-expression and neuronal lineage differentiation potential in high-grade glioma. PLoS ONE 3: e1936 (Pubitemid 351984112)
34. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancerinitiating cells. Nature 445: 111-115 (Pubitemid 46067311)
35. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D, De Rossi M (2006) Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54: 850-860 (Pubitemid 44671990)
36. 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 (2008) Identification of cells initiating human melanomas. Nature 451: 345-349
37. Schiess R, Mueller LN, Schmidt A, Mueller M, Wollscheid B, Aebersold R (2009) Analysis of cell surface proteome changes via label-free, quantitative mass spectrometry. Mol Cell Proteomics 8: 624-638
38. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, Chadburn A, Murphy AJ, Valenzuela DM, Gale NW, Thurston G, Yancopoulos GD, D'Angelica M, Kemeny N, Lyden D, Rafii S (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 118: 2111-2120 (Pubitemid 351872330)
39. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828 (Pubitemid 37187480)
40. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401 (Pubitemid 39551674)
41. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, Tripodo C, Russo A, Gulotta G, Medema JP, Stassi G (2007) Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 1: 389-402 (Pubitemid 47506537)
42. Van Orden KL, Birse CE, He T, Smith LM, McKinnon K, Lee C, FitzHugh W, Duniho S, Nesterova A, McCaffery I, Kim YJ, Aggarwal S, Mesmer D, Carter PJ, Moore PA, Ruben SM (2007) Proteomic analysis of colorectal tumor cells identifies CD133/prominin-1, a cancer stem cell marker, as a target for antibody-based therapy. [abstract 1324]. Proceedings of the 98th Annual Meeting of the AACR
43. Vermeulen L, Todaro M, De Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, Richel DJ, Stassi G, Medema JP (2008) Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA 105: 13427-13432
44. Weber CK, Sommer G, Michl P, Fensterer H, Weimer M, Gansauge F, Leder G, Adler G, Gress TM (2001) Biglycan is overexpressed in pancreatic cancer and induces G1-arrest in pancreatic cancer cell lines. Gastroenterology 121: 657-667 (Pubitemid 32822581)
45. Yu H, Fang D, Kumar SM, Li L, Nguyen TK, Acs G, Herlyn M, Xu X (2006) Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 168: 1879-1888 (Pubitemid 43825308)
46. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP (2008) Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68: 4311-4320
47. Zhou J, Wang CY, Liu T, Wu B, Zhou F, Xiong JX, Wu HS, Tao J, Zhao G, Yang M, Gou SM (2008) Persistence of side population cells with high drug efflux capacity in pancreatic cancer. World J Gastroenterol 14: 925-930 (Pubitemid 351325033)