Epigenetic targeting of ovarian cancer stem cells

Cancer Research

Volumn 74, Issue 17, 2014, Pages 4922-4936

  Wang, Yinu ^a   Cardenas, Horacio ^a   Fang, Fang ^a   Condello, Salvatore ^a   Taverna, Pietro ^b   Segar, Matthew ^a   Liu, Yunlong ^a,c   Nephew, Kenneth P ^a,c,d   Matei, Daniela ^a,c,e  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ASTEX PHARMACEUTICALS   (United Kingdom)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INDIANA UNIVERSITY   (United States)

^e VA Roudebush Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; AZACITIDINE; CARBOPLATIN; SGI-110;

ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CANCER STEM CELL; CELL DIFFERENTIATION; DNA METHYLATION; DRUG EFFECTS; EPIGENETICS; FEMALE; GENETIC EPIGENESIS; GENETICS; HUMAN; MOUSE; NUDE MOUSE; OVARIAN NEOPLASMS; PROCEDURES; TUMOR CELL LINE;

ALDEHYDE DEHYDROGENASE; ANIMALS; AZACITIDINE; CARBOPLATIN; CELL DIFFERENTIATION; CELL LINE, TUMOR; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS;

EID: 84907043116     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1022     Document Type: Article

References (49)

1. Bukowski RM, Ozols RF, Markman M. The management of recurrent ovarian cancer. Semin Oncol 2007;34:S1-15.
2. Vaughan S, Coward JI, Bast RC, Berchuck A, Berek JS, Brenton JD, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011;11:719-25.
3. Liu CM. Cancer of the ovary. N Engl J Med 2005;352:1268-9.
4. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008;68:4311-20.
5. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006;355:1253-61.
6. Shah MM, Landen CN. Ovarian cancer stem cells: are they real and why are they important? Gynecol Oncol 2014;132:483-9.
7. 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;65:3025-9.
8. Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, et al. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 2009;27:2875-83.
9. Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu Rev Cell Dev Biol 2007;23:675-99.
10. Deng S, Yang X, Lassus H, Liang S, Kaur S, Ye Q, et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS ONE 2010;5:e10277.
11. Landen CN, Goodman B, Katre AA, Steg AD, Nick AM, Stone RL, et al. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 2010;9:3186-99.
12. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, et al.Achromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010;141:69-80.
13. Balch C, Fang F, Matei DE, Huang THM, Nephew KP. Epigenetic changes in ovarian cancer. Endocrinology 2009;150:4003-11.
14. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128: 683-92.
15. Tsai HC, Li H, Van Neste L, Cai Y, Robert C, Rassool FV, et al. Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell 2012; 21:430-46.
16. Plumb JA, Strathdee G, Sludden J, Kaye SB, Brown R. Reversal of drug resistance in human tumor xenografts by 20-deoxy-5-azacytidineinduced demethylation of the hMLH1 gene promoter. Cancer Res 2000;60:6039-44.
17. Frost P, Abbruzzese JL, Hunt B, Lee D, Ellis M. Synergistic cytotoxicity using 20-deoxy-5-azacytidine and cisplatin or 4-hydroperoxycyclophosphamide with human tumor cells. Cancer Res 1990; 50:4572-7.
18. Fang F, Balch C, Schilder J, Breen T, Zhang S, Shen C, et al. A phase 1 and pharmacodynamic study of decitabine in combination with carboplatin in patients with recurrent, platinum-resistant, epithelial ovarian cancer. Cancer 2010;116:4043-53.
19. Matei DE, Nephew KP. Epigenetic therapies for chemoresensitization of epithelial ovarian cancer. Gynecol Oncol 2010;116:195-201.
20. Balch C, Yan P, Craft T, Young S, Skalnik DG, Huang TH, et al. Antimitogenic and chemosensitizing effects of the methylation inhibitor zebularine in ovarian cancer. Mol Cancer Ther 2005;4:1505-14.
21. Matei D, Fang F, Shen C, Schilder J, Arnold A, Zeng Y, et al. Epigenetic resensitization to platinum in ovarian cancer. Cancer Res 2012;72: 2197-205.
22. Li M, Balch C, Montgomery JS, Jeong M, Chung JH, Yan P, et al. Integrated analysis of DNA methylation and gene expression reveals specific signaling pathways associated with platinum resistance in ovarian cancer. BMC Med Genomics 2009;2:34.
23. Rafehi H, Orlowski C, Georgiadis GT, Ververis K, El-Osta A, Karagiannis TC. Clonogenic assay: adherent cells. J Vis Exp 2011;49:2573.
24. Fan MY, Yan PS, Hartman-Frey C, Chen L, Paik H, Oyer SL, et al. Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 2006;66:11954-66.
25. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003;13:2498-504.
26. Liao YP, Chen LY, Huang RL, Su PH, Chan MW, Chang CC, et al. Hypomethylation signature of tumor-initiating cells predicts poor prognosis of ovarian cancer patients. Hum Mol Genet 2014;23:1894-906.
27. Shank JJ, Yang K, Ghannam J, Cabrera L, Johnston CJ, Reynolds RK, et al. Metformin targets ovarian cancer stem cells in vitro and in vivo. Gynecol Oncol 2012;127:390-7.
28. Kuroda T, Hirohashi Y, Torigoe T, Yasuda K, Takahashi A, Asanuma H, et al. ALDH1-high ovarian cancer stem-like cells can be isolated from serous and clear cell adenocarcinoma cells, and ALDH1 high expression is associated with poor prognosis. PLoS ONE 2013;8: e65158.
29. Saw YT, Yang J, Ng SK, Liu S, Singh S, Singh M, et al. Characterization of aldehyde dehydrogenase isozymes in ovarian cancer tissues and sphere cultures. BMC Cancer 2012;12:329.
30. Silva IA, Bai SM, McLean K, Yang K, Griffith K, Thomas D, et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 2011;71:3991-4001.
31. Kanai Y, Hirohashi S. Alterations of DNA methylation associated with abnormalities of DNA methyltransferases in human cancers during transition from a precancerous to a malignant state. Carcinogenesis 2007;28:2434-42.
32. Bai X, Song Z, Fu Y, Yu Z, Zhao L, Zhao H, et al. Clinicopathological significance and prognostic value of DNA methyltransferase 1, 3a, and 3b expressions in sporadic epithelial ovarian cancer. PLoS ONE 2012;7:e40024.
33. 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 drugresistant phenotype in cancer cells. Cancer Res 2006;66:5582-91.
34. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
35. Li Z, Li W, Xie J, Wang Y, Tang A, Li X, et al. Epigenetic inactivation of PCDH10 in human prostate cancer cell lines. Cell Biol Int 2011;35: 671-6.
36. Wong KY, Liang R, So CC, Jin DY, Costello JF, Chim CS. Epigenetic silencing of MIR203 in multiple myeloma. Br J Haematol 2011;154: 569-78.
37. Zheng Y, Wang Z, Bie W, Brauer PM, Perez White BE, Li J, et al. PTK6 activation at the membrane regulates epithelial-mesenchymal transition in prostate cancer. Cancer Res 2013;73:5426-37.
38. Yasuda K, Torigoe T, Morita R, Kuroda T, Takahashi A, Matsuzaki J, et al. Ovarian cancer stem cells are enriched in side population and aldehyde dehydrogenase bright overlapping population. PLoS ONE 2013;8:e68187.
39. Jackson B, Brocker C, Thompson DC, Black W, Vasiliou K, Nebert DW, et al. Update on the aldehyde dehydrogenase gene (ALDH) superfamily. Hum Genomics 2011;5:283-303.
40. Domcke S, Sinha R, Levine DA, Sander C, Schultz N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun 2013;4.
41. Anglesio MS, Wiegand KC, Melnyk N, Chow C, Salamanca C, Prentice LM, et al. Type-specific cell line models for type-specific ovarian cancer research. PLoS ONE 2013;8:e72162.
42. Rattan R, Graham RP, Maguire JL, Giri S, Shridhar V. Metformin suppresses ovarian cancer growth and metastasis with enhancement of cisplatin cytotoxicity in vivo. Neoplasia 2011;13:483-91.
43. Altun G, Loring JF, Laurent LC. DNA methylation in embryonic stem cells. J Cell Biochem 2010;109:1-6.
44. Trowbridge JJ, Orkin SH. DNA methylation in adult stem cells: New insights into self-renewal. Epigenetics 2010;5:pii11374.
45. Gattei V, Aldinucci D, Petti MC, Da Ponte A, Zagonel V, Pinto A. In vitro and in vivo effects of 5-aza-20-deoxycytidine (decitabine) on clonogenic cells from acute myeloid leukemia patients. Leukemia 1993;7 Suppl 1:42-8.
46. Li H, Bitler BG, Vathipadiekal V, Maradeo ME, Slifker M, Creasy CL, et al. ALDH1A1 is a novel EZH2 target gene in epithelial ovarian cancer identified by genome-wide approaches. Cancer Prev Res 2012;5:484-91.
47. Burger RA, Brady MF, Bookman MA, Fleming GF, Monk BJ, Huang H, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med 2011;365:2473-83.
48. Hess LM, Rong N, Monahan PO, Gupta P, Thomaskutty C, Matei D. Continued chemotherapy after complete response to primary therapy among women with advanced ovarian cancer: a meta-analysis. Cancer 2010;116:5251-60.
49. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 2012;366:1382-92.