Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2

Molecular Cancer Therapeutics

Volumn 10, Issue 2, 2011, Pages 325-335

  Rizzo, Siân ^a   Hersey, Jenny M ^a   Mellor, Paul ^a   Dai, Wei ^b   Santos Silva, Alessandra ^a   Liber, Daniel ^b   Luk, Louisa ^b,c   Titley, Ian ^a   Carden, Craig P ^a   Box, Garry ^a   Hudson, David L ^a   Kaye, Stanley B ^a   Brown, Robert ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; CISPLATIN; DOXORUBICIN; ETOPOSIDE; MEGESTROL; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR EZH2;

ADULT; AGED; ARTICLE; ASCITES; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RECURRENCE; CANCER STEM CELL; CELL SUBPOPULATION; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; OVARY CANCER; PRIORITY JOURNAL; SIDE POPULATION CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; ASCITES; CARBOPLATIN; CELL LINE, TUMOR; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, SCID; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79951825513     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-10-0788     Document Type: Article

References (46)

1. Agarwal R, Kaye SB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 2003;3:502-6.
2. Dean M. ABC transporters, drug resistance, and cancer stem cells. J Mammary Gland Biol Neoplasia 2009;14:3-9.
3. Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer 2008;18:506-14. (Pubitemid 351668323)
4. 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;65:3025-29. (Pubitemid 40524578)
5. Szotek P P, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, et al. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci U S A 2006;103:11154-59. (Pubitemid 44156488)
6. Moserle L, Indraccolo S, Ghisi M, Frasson C, Fortunato E, Canevari S, et al. The side population of ovarian cancer cells is a primary target of IFN-alpha antitumor effects. Cancer Res 2008;68:5658-68.
7. Zhang S, Balch C, Chan MW, Lai H, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008;68:4311-20.
8. Hu L, McArthur C, Jaffe RB. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br J Cancer 2010; 102:1276-83.
9. Wang J, Guo LP, Chen LZ, Zeng YX, Lu SH. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res 2007;67:3716-24. (Pubitemid 46762157)
10. 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 U S A 2004;101:781-6. (Pubitemid 38121035)
11. Hirschmann-Jax C, Foster AE, Wulf GG, Goodell MA, Brenner MKA. distinct "side population" of cells in human tumor cells: implications for tumor biology and therapy. Cell Cycle 2005;4:203-5.
12. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, Mori M. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006;24:506-13. (Pubitemid 44464754)
13. Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007;67:4827-33. (Pubitemid 46910191)
14. Wu C, Alman BA. Side population cells in human cancers. Cancer Lett 2008;268:1-9.
15. Sauvageau M, Sauvageau G. Polycomb group genes: keeping stem cell activity in balance. PLoS Biol 2008;6:e113.
16. Lee TI, Jenner RG, Boyer LA, Guenther M, Levine SS, Kumar RM, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006;125:301-13. (Pubitemid 44313811)
17. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-56. (Pubitemid 41345211)
18. Suva ML, Riggi N, Janiszewska M, Radovanovic I, Provero P, Stehle JC, et al. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 2009;69:9211-18.
19. Simon JA, Lange CA. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 2008;647:21-29.
20. Cao R, Zhang Y.The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004;14:155-64. (Pubitemid 38520143)
21. Matsukawa Y, Semba S, Kato H, Ito A, Yanagihara K, Yokozaki H. Expression of the enhancer of zeste homolog 2 is correlated with poor prognosis in human gastric cancer. Cancer Sci 2006;97:484-91. (Pubitemid 43811589)
22. Bryant RJ, Cross NA, Eaton CL, Hamdy FC, Cunliffe VT. EZH2 promotes proliferation and invasiveness of prostate cancer cells. Prostate 2007;67:547-56. (Pubitemid 46536947)
23. Collett K, Eide GE, Arnes J, Stefansson IM, Eide J, Braaten A, et al. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin Cancer Res 2006;12:1168-74. (Pubitemid 43342505)
24. Karanikolas BD, Figueiredo ML, Wu L. Polycomb group protein enhancer of zeste 2 is an oncogene that promotes the neoplastic transformation of a benign prostatic epithelial cell line. Mol Cancer Res 2009;7:1456-65.
25. Nikoloski G, Langemeijer SM, Kuiper RP, Knops R, Massop M, Tonnissen ER, et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat Genet 2010;42:665-7.
26. Rao ZY, Cai MY, Yang GF, He LR, Mai SJ, Hua WF, et al. EZH2 supports ovarian carcinoma cell invasion and/or metastasis via regulation of TGF-{beta}1 and is a predictor of outcome in ovarian carcinoma patients. Carcinogenesis 2010;31:1576-83.
27. Hu S, Yu L, Li Z, Shen Y, Wang J, Cai J, et al. Overexpression of EZH2 contributes to acquired cisplatin resistance in ovarian cancer cells in vitro and in vivo. Cancer Biol Ther 2010 Oct 7;10: [Epub ahead of print].
28. Benard J, Da Silva J, De Blois MC, Boyer P, Duvillard P, Chiric E, et al. Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice. Cancer Res 1985: 45:4970-79. (Pubitemid 16236181)
29. Langdon SP, Lawrie SS, Hay FG, Hawkes MM, McDonald A, Hayward IP, et al. Characterization and properties of nine human ovarian adenocarcinoma cell lines. Cancer Res 1988:48:6166-72. (Pubitemid 18266818)
30. Workman P, Balmain A, Hickman JA, McNally NJ, Rohas AM, Mitchison NA, et al. UKCCCR guidelines for the welfare of animals in experimentalneoplasia. LabAnim1988;22:195-201.
31. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64.
32. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50. (Pubitemid 41528093)
33. Efron B, Tibshirani R. On testing the significance of sets of genes. Stanford tech report rep . 2006. Available from:http://www-stat.stanford.edu/ ~tibs/ftp/GSA.pdf.
34. Neumuller RA, Knoblich JA. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 2009;23:2675-99.
35. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005;5:275-284. (Pubitemid 40488633)
36. Ikuta K, Takemura K, Sasaki K, Kihara M, Nishimura M, Ueda N, et al. Expression of multidrug resistance proteins and accumulation of cisplatin in human non-small cell lung cancer cells. Biol Pharm Bull 2005;28:707-12. (Pubitemid 40879942)
37. Nomura M, Matsunami T, Kobayashi K, Uchibayashi T, Koshida K, Tanaka, M, et al. Involvement of ABC transporters in chemosensitivity of human renal cell carcinoma, and regulation of MRP2 expression by conjugated bilirubin. Anticancer Res 2005;25:2729-35.
38. Weaver DA, Crawford EL, Warner KA, Elkhairi F, Khuder SA, Willey JC. ABCC5, ERCC2, XPA and XRCC1 transcript abundance levels correlate with cisplatin chemoresistance in non-small cell lung cancer cell lines. Mol Cancer, 2005;4:18-22.
39. Christgen M, Geffers R, Ballmaier M, Christgen H, Poczkaj J, Krech T, et al. Down-regulation of the fetal stem cell factor SOX17 by H33342: a mechanism responsible for differential gene expression in breast cancer side population cells. J Biol Chem 2010;285:6412-18.
40. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 2009;461:762-67.
41. Shen X, Liu Y, Hsu YJ, Fujiwara Y, Kim J, Mao X, et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 2008;32:491-502.
42. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet, 2008; 40:741-50. (Pubitemid 351748874)
43. Abbosh PH, Montgomery JS, Starkey JA, Novotny M, Zuhowski EG, Egorin MJ, et al. Dominant-negative histone H3 lysine 27 mutant derepresses silenced tumor suppressor genes and reverses the drug-resistant phenotype in cancer cells. Cancer Res 2006;66:5582-91. (Pubitemid 43927108)
44. Wei Y, Xia W, Zhang Z, Liu J, Wang H, Adsay NV, et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog 2008;47: 701-6.
45. Chang Y, Zhang X, Horton JR, Upadhyay AK, Spannhoff A, Liu J, et al. Structural basis for G9a-like protein lysine methyltransferase inhibition by BIX-01294. Nat Struct Mol Biol 2009;16:312-17.
46. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 2007;21:1050-63. (Pubitemid 46686474)