Integrated Analyses Identify a Master MicroRNA Regulatory Network for the Mesenchymal Subtype in Serous Ovarian Cancer

Cancer Cell

Volumn 23, Issue 2, 2013, Pages 186-199

  Yang, Da ^a,e   Sun, Yan ^a,b,e   Hu, Limei ^a,e   Zheng, Hong ^b,e   Ji, Ping ^a   Pecot, Chad V ^a   Zhao, Yanrui ^b   Reynolds, Sheila ^c   Cheng, Hanyin ^a   Rupaimoole, Rajesha ^a   Cogdell, David ^a   Nykter, Matti ^d   Broaddus, Russell ^a   Rodriguez Aguayo, Cristian ^a   Lopez Berestein, Gabriel ^a   Liu, Jinsong ^a   Shmulevich, Ilya ^c   Sood, Anil K ^a   Chen, Kexin ^b   Zhang, Wei ^a  

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

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MICRORNA; MICRORNA 141; MICRORNA 200A; MICRORNA 506; TRANSCRIPTION FACTOR SLUG; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIM PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; COPY NUMBER VARIATION; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE TARGETING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MESENCHYME CELL; MOUSE; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA METHYLATION; SEROUS OVARIAN CANCER;

EID: 84873582060     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.12.020     Document Type: Article

References (45)

1. Bagga S., Bracht J., Hunter S., Massirer K., Holtz J., Eachus R., Pasquinelli A.E. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563.
2. Bast R.C., Hennessy B., Mills G.B. The biology of ovarian cancer: new opportunities for translation. Nat. Rev. Cancer 2009, 9:415-428.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B. 1995, 57:289-300.
4. Bentink S., Haibe-Kains B., Risch T., Fan J.B., Hirsch M.S., Holton K., Rubio R., April C., Chen J., Wickham-Garcia E., et al. Angiogenic mRNA and microRNA gene expression signature predicts a novel subtype of serous ovarian cancer. PLoS ONE 2012, 7:e30269.
5. Bonome T., Levine D.A., Shih J., Randonovich M., Pise-Masison C.A., Bogomolniy F., Ozbun L., Brady J., Barrett J.C., Boyd J., Birrer M.J. A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer Res. 2008, 68:5478-5486.
6. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615. Cancer Genome Atlas Research Network.
7. Cao L., Shao M., Schilder J., Guise T., Mohammad K.S., Matei D. Tissue transglutaminase links TGF-beta, epithelial to mesenchymal transition and a stem cell phenotype in ovarian cancer. Oncogene 2011, 31:2521-2534.
8. Carvalho J., van Grieken N.C., Pereira P.M., Sousa S., Tijssen M., Buffart T.E., Diosdado B., Grabsch H., Santos M.A., Meijer G., et al. Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 up-regulation in intestinal gastric cancer. J. Pathol. 2012, 228:31-44.
9. Ein-Dor L., Kela I., Getz G., Givol D., Domany E. Outcome signature genes in breast cancer: is there a unique set?. Bioinformatics 2005, 21:171-178.
10. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
11. Esquela-Kerscher A., Trang P., Wiggins J.F., Patrawala L., Cheng A., Ford L., Weidhaas J.B., Brown D., Bader A.G., Slack F.J. The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 2008, 7:759-764.
12. Evangelisti C., Florian M.C., Massimi I., Dominici C., Giannini G., Galardi S., Buè M.C., Massalini S., McDowell H.P., Messi E., et al. MiR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasiveness. FASEB J. 2009, 23:4276-4287.
13. Garzon R., Marcucci G., Croce C.M. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat. Rev. Drug Discov. 2010, 9:775-789.
14. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
15. Jemal A., Tiwari R.C., Murray T., Ghafoor A., Samuels A., Ward E., Feuer E.J., Thun M.J. Cancer statistics, 2004. CA Cancer J. Clin. 2004, 54:8-29. American Cancer Society.
16. Kurrey N.K., K A., Bapat S.A. Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol. 2005, 97:155-165.
17. Lewis B.P., Shih I.H., Jones-Rhoades M.W., Bartel D.P., Burge C.B. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798.
18. Liu C., Kelnar K., Liu B., Chen X., Calhoun-Davis T., Li H., Patrawala L., Yan H., Jeter C., Honorio S., et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med. 2011, 17:211-215.
19. Mateescu B., Batista L., Cardon M., Gruosso T., de Feraudy Y., Mariani O., Nicolas A., Meyniel J.P., Cottu P., Sastre-Garau X., Mechta-Grigoriou F. miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat. Med. 2011, 17:1627-1635.
20. Naora H., Montell D.J. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat. Rev. Cancer 2005, 5:355-366.
21. Noushmehr H., Weisenberger D.J., Diefes K., Phillips H.S., Pujara K., Berman B.P., Pan F., Pelloski C.E., Sulman E.P., Bhat K.P., et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522. Cancer Genome Atlas Research Network.
22. Park S.M., Gaur A.B., Lengyel E., Peter M.E. 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.
23. Pecot C.V., Calin G.A., Coleman R.L., Lopez-Berestein G., Sood A.K. RNA interference in the clinic: challenges and future directions. Nat. Rev. Cancer 2011, 11:59-67.
24. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 2007, 7:415-428.
25. Pramanik D., Campbell N.R., Karikari C., Chivukula R., Kent O.A., Mendell J.T., Maitra A. Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol. Cancer Ther. 2011, 10:1470-1480.
26. Rapley E.A., Crockford G.P., Teare D., Biggs P., Seal S., Barfoot R., Edwards S., Hamoudi R., Heimdal K., Fossâ S.D., et al. Localization to Xq27 of a susceptibility gene for testicular germ-cell tumours. Nat. Genet. 2000, 24:197-200.
27. Rosanò L., Cianfrocca R., Spinella F., Di Castro V., Nicotra M.R., Lucidi A., Ferrandina G., Natali P.G., Bagnato A. Acquisition of chemoresistance and EMT phenotype is linked with activation of the endothelin A receptor pathway in ovarian carcinoma cells. Clin. Cancer Res. 2011, 17:2350-2360.
28. Rupaimoole R., Han H.D., Lopez-Berestein G., Sood A.K. MicroRNA therapeutics: principles, expectations, and challenges. Chin J Cancer 2011, 30:368-370.
29. Santoro M.R., Bray S.M., Warren S.T. Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 2012, 7:219-245.
30. Sengupta S., den Boon J.A., Chen I.H., Newton M.A., Stanhope S.A., Cheng Y.J., Chen C.J., Hildesheim A., Sugden B., Ahlquist P. MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc. Natl. Acad. Sci. USA 2008, 105:5874-5878.
31. Siegel R., DeSantis C., Virgo K., Stein K., Mariotto A., Smith T., Cooper D., Gansler T., Lerro C., Fedewa S., et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J. Clin. 2012, 62:220-241.
32. Tellez C.S., Juri D.E., Do K., Bernauer A.M., Thomas C.L., Damiani L.A., Tessema M., Leng S., Belinsky S.A. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res. 2011, 71:3087-3097.
33. Tessema M., Willink R., Do K., Yu Y.Y., Yu W., Machida E.O., Brock M., Van Neste L., Stidley C.A., Baylin S.B., Belinsky S.A. Promoter methylation of genes in and around the candidate lung cancer susceptibility locus 6q23-25. Cancer Res. 2008, 68:1707-1714.
34. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
35. Tothill R.W., Tinker A.V., George J., Brown R., Fox S.B., Lade S., Johnson D.S., Trivett M.K., Etemadmoghadam D., Locandro B., et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res. 2008, 14:5198-5208. Australian Ovarian Cancer Study Group.
36. Trang P., Medina P.P., Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Homer R., Brown D., Bader A.G., Weidhaas J.B., Slack F.J. Regression of murine lung tumors by the let-7 microRNA. Oncogene 2010, 29:1580-1587.
37. Varambally S., Cao Q., Mani R.S., Shankar S., Wang X., Ateeq B., Laxman B., Cao X., Jing X., Ramnarayanan K., et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008, 322:1695-1699.
38. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010, 17:98-110. Cancer Genome Atlas Research Network.
39. Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Patrawala L., Brown D., Bader A.G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010, 70:5923-5930.
40. Xu L., Xie K., Mukaida N., Matsushima K., Fidler I.J. Hypoxia-induced elevation in interleukin-8 expression by human ovarian carcinoma cells. Cancer Res. 1999, 59:5822-5829.
41. Yang D., Khan S., Sun Y., Hess K., Shmulevich I., Sood A.K., Zhang W. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. JAMA 2011, 306:1557-1565.
42. Zhang L., Volinia S., Bonome T., Calin G.A., Greshock J., Yang N., Liu C.G., Giannakakis A., Alexiou P., Hasegawa K., et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc. Natl. Acad. Sci. USA 2008, 105:7004-7009.
43. Zhao Y., Liu H., Li Y., Wu J., Greenlee A.R., Yang C., Jiang Y. The role of miR-506 in transformed 16HBE cells induced by anti-benzo[a]pyrene-trans-7,8-dihydrodiol-9,10-epoxide. Toxicol. Lett. 2011, 205:320-326.
44. Zhou L., Chen J., Li Z., Li X., Hu X., Huang Y., Zhao X., Liang C., Wang Y., Sun L., et al. Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS ONE 2010, 5:e15224.
45. Zhu Y., Nilsson M., Sundfeldt K. Phenotypic plasticity of the ovarian surface epithelium: TGF-beta 1 induction of epithelial to mesenchymal transition (EMT) in vitro. Endocrinology 2010, 151:5497-5505.