Characterizing cancer cells with cancer stem cell-like features in 293T human embryonic kidney cells

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Debeb, Bisrat G ^a   Zhang, Xiaomei ^b   Krishnamurthy, Savitri ^a   Gao, Hui ^a   Cohen, Evan ^a   Li, Li ^a   Rodriguez, Angel A ^b   Landis, Melissa D ^b   Lucci, Anthony ^a   Ueno, Naoto T ^a   Robertson, Fredika ^a   Xu, Wei ^a   Lacerda, Lara ^a   Buchholz, Thomas A ^a   Cristofanilli, Massimo ^a   Reuben, James M ^a   Lewis, Michael T ^b   Woodward, Wendy A ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CD24 ANTIGEN; CELL PROTEIN; HERMES ANTIGEN; MICRORNA; NERVE CELL ADHESION MOLECULE; NOTCH1 RECEPTOR; PROTEIN ALDH1; PROTEIN MTA1; PROTEIN RHOC; PROTEIN ZEB1; SURVIVIN; TENASCIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL RENEWAL; CELL STRAIN HEK293; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MONOLAYER CULTURE; MOUSE; NONHUMAN; PHENOTYPE; PLASTICITY; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; UPREGULATION; CELL LINE; CYTOLOGY; GENETICS; KIDNEY; NEOPLASM; PATHOLOGY; PRENATAL DEVELOPMENT; PROSPECTIVE STUDY;

GASTROPODA;

CELL LINE; CULTURE MEDIA, SERUM-FREE; HUMANS; KIDNEY; MICRORNAS; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC STEM CELLS; PROSPECTIVE STUDIES; UP-REGULATION;

EID: 77955506627     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-180     Document Type: Article

References (54)

1. 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, 66:9339-9344. 10.1158/0008-5472.CAN-06-3126, 16990346.
2. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, Houvenaeghel G, Extra JM, Bertucci F, Jacquemier J, et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2009, 16:45-55. 10.1158/1078-0432.CCR-09-1630, 20028757.
3. Li F, Tiede B, Massague J, Kang Y. Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res 2007, 17:3-14. 10.1038/sj.cr.7310118, 17179981.
4. Wicha MS. Cancer stem cells and metastasis: lethal seeds. Clin Cancer Res 2006, 12:5606-5607. 10.1158/1078-0432.CCR-06-1537, 17020960.
5. Debeb BG, Xu W, Woodward WA. Radiation resistance of breast cancer stem cells: understanding the clinical framework. J Mammary Gland Biol Neoplasia 2009, 14:11-17. 10.1007/s10911-009-9114-z, 19252973.
6. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783. 10.1038/nature07733, 2778612, 19194462.
7. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679. 10.1093/jnci/djn123, 18445819.
8. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98:1777-1785.
9. Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, Rosen JM. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 2007, 104:618-623. 10.1073/pnas.0606599104, 1766434, 17202265.
10. 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, 100:3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
11. 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, 432:396-401. 10.1038/nature03128, 15549107.
12. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17:1253-1270. 10.1101/gad.1061803, 196056, 12756227.
13. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009, 11:1487-1495. 10.1038/ncb1998, 19935649.
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, 445:111-115. 10.1038/nature05384, 17122771.
15. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009, 69:1302-1313. 10.1158/0008-5472.CAN-08-2741, 2819227, 19190339.
16. Debeb BG, Xu W, Mok H, Li L, Robertson F, Ueno NT, Reuben J, Lucci A, Cristofanilli M, Woodward WA. Differential radiosensitizing effect of valproic acid in differentiation versus self-renewal promoting culture conditions. Int J Radiat Oncol Biol Phys 2010, 76:889-895.
17. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008, 10:R25. 10.1186/bcr1982, 2397524, 18366788.
18. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
19. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567. 10.1016/j.stem.2007.08.014, 2423808, 18371393.
20. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, Boman BM. 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, 69:3382-3389. 10.1158/0008-5472.CAN-08-4418, 2789401, 19336570.
21. Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, Guan XY. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 2008, 6:1146-1153. 10.1158/1541-7786.MCR-08-0035, 18644979.
22. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, Murter C, Hong SM, Koorstra JB, Rajeshkumar NV, He X, et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102:340-351.
23. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659. 10.1016/j.cell.2009.06.034, 19682730.
24. Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a Human Cell Line Transformed by DNA from Human Adenovirus Type-5. Journal of General Virology 1977, 36:59-72. 10.1099/0022-1317-36-1-59, 886304.
25. Guan LS, Li GC, Chen CC, Liu LQ, Wang ZY. Rb-associated protein 46 (RbAp46) suppresses the tumorigenicity of adenovirus-transformed human embryonic kidney 293 cells. Int J Cancer 2001, 93:333-338. 10.1002/ijc.1338, 11433396.
26. Shen C, Gu M, Song C, Miao L, Hu L, Liang D, Zheng C. The tumorigenicity diversification in human embryonic kidney 293 cell line cultured in vitro. Biologicals 2008, 36:263-268. 10.1016/j.biologicals.2008.02.002, 18378163.
27. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872. 10.1016/j.cell.2007.11.019, 18035408.
28. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676. 10.1016/j.cell.2006.07.024, 16904174.
29. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007, 448:318-324. 10.1038/nature05944, 17554336.
30. Clark EA, Golub TR, Lander ES, Hynes RO. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 2000, 406:532-535. 10.1038/35020106, 10952316.
31. Hakem A, Sanchez-Sweatman O, You-Ten A, Duncan G, Wakeham A, Khokha R, Mak TW. RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev 2005, 19:1974-1979. 10.1101/gad.1310805, 1199568, 16107613.
32. Kleer CG, Teknos TN, Islam M, Marcus B, Lee JS, Pan Q, Merajver SD. RhoC GTPase expression as a potential marker of lymph node metastasis in squamous cell carcinomas of the head and neck. Clin Cancer Res 2006, 12:4485-4490. 10.1158/1078-0432.CCR-06-0376, 16899593.
33. Kondo T, Sentani K, Oue N, Yoshida K, Nakayama H, Yasui W. Expression of RHOC is associated with metastasis of gastric carcinomas. Pathobiology 2004, 71:19-25. 10.1159/000072958, 14555841.
34. Hancox RA, Allen MD, Holliday DL, Edwards DR, Pennington CJ, Guttery DS, Shaw JA, Walker RA, Pringle JH, Jones JL. Tumour-associated tenascin-C isoforms promote breast cancer cell invasion and growth by matrix metalloproteinase-dependent and independent mechanisms. Breast Cancer Res 2009, 11:R24. 10.1186/bcr2251, 2688953, 19405959.
35. Qian H, Lu N, Xue L, Liang X, Zhang X, Fu M, Xie Y, Zhan Q, Liu Z, Lin C. Reduced MTA1 expression by RNAi inhibits in vitro invasion and migration of esophageal squamous cell carcinoma cell line. Clin Exp Metastasis 2005, 22:653-662. 10.1007/s10585-006-9005-2, 16703414.
36. Sarkar S, Nuttall RK, Liu S, Edwards DR, Yong VW. Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Res 2006, 66:11771-11780. 10.1158/0008-5472.CAN-05-0470, 17178873.
37. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007, 131:1109-1123. 10.1016/j.cell.2007.10.054, 18083101.
38. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008, 10:593-601. 10.1038/ncb1722, 18376396.
39. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152. 10.1038/nature06487, 2782491, 18185580.
40. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008, 22:894-907. 10.1101/gad.1640608, 2279201, 18381893.
41. Shaw G, Morse S, Ararat M, Graham FL. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 2002, 16:869-871.
42. Bru T, Clarke C, McGrew MJ, Sang HM, Wilmut I, Blow JJ. Rapid induction of pluripotency genes after exposure of human somatic cells to mouse ES cell extracts. Exp Cell Res 2008, 314:2634-2642. 10.1016/j.yexcr.2008.05.009, 2577761, 18571647.
43. Hansis C, Barreto G, Maltry N, Niehrs C. Nuclear reprogramming of human somatic cells by xenopus egg extract requires BRG1. Curr Biol 2004, 14:1475-1480. 10.1016/j.cub.2004.08.031, 15324664.
44. Taranger CK, Noer A, Sorensen AL, Hakelien AM, Boquest AC, Collas P. Induction of dedifferentiation, genomewide transcriptional programming, and epigenetic reprogramming by extracts of carcinoma and embryonic stem cells. Mol Biol Cell 2005, 16:5719-5735. 10.1091/mbc.E05-06-0572, 1289416, 16195347.
45. Liu Y, Clem B, Zuba-Surma EK, El-Naggar S, Telang S, Jenson AB, Wang Y, Shao H, Ratajczak MZ, Chesney J, Dean DC. Mouse fibroblasts lacking RB1 function form spheres and undergo reprogramming to a cancer stem cell phenotype. Cell Stem Cell 2009, 4:336-347. 10.1016/j.stem.2009.02.015, 2743858, 19341623.
46. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality?. Nat Med 2009, 15:1010-1012. 10.1038/nm0909-1010, 19734877.
47. Meyer MJ, Fleming JM, Ali MA, Pesesky MW, Ginsburg E, Vonderhaar BK. Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Res 2009, 11:R82. 10.1186/bcr2449, 2815544, 19906290.
48. Woodward WA, Debeb BG, Xu W, Buchholz TA. Overcoming Radiation Resistance in Inflammatory Breast Cancer. Cancer 2010, 116:2840-2845. 10.1002/cncr.25173, 20503417.
49. Chen MS, Woodward WA, Behbod F, Peddibhotla S, Alfaro MP, Buchholz TA, Rosen JM. Wnt/beta-catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J Cell Sci 2007, 120:468-477. 10.1242/jcs.03348, 17227796.
50. 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, 444:756-760. 10.1038/nature05236, 17051156.
51. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000, 148:779-790. 10.1083/jcb.148.4.779, 2169367, 10684258.
52. Kiemer AK, Takeuchi K, Quinlan MP. Identification of genes involved in epithelial-mesenchymal transition and tumor progression. Oncogene 2001, 20:6679-6688. 10.1038/sj.onc.1204872, 11709702.
53. Kim JB, Islam S, Kim YJ, Prudoff RS, Sass KM, Wheelock MJ, Johnson KR. N-Cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J Cell Biol 2000, 151:1193-1206. 10.1083/jcb.151.6.1193, 2190584, 11121435.
54. DeOme KB, Faulkin LJ, Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 1959, 19:515-520.