MicroRNAs as prognostic markers in ovarian cancer

Molecular and Cellular Endocrinology

Volumn 390, Issue 1-2, 2014, Pages 73-84

  Llauradó, Marta ^a,b   Majem, Blanca ^b   Altadill, Tatiana ^b   Lanau, Lucia ^b   Castellví, Josep ^b   Sánchez Iglesias, Jose Luis ^b   Cabrera, Silvia ^b   De la Torre, Javier ^b   Díaz Feijoo, Berta ^b   Pérez Benavente, Asuncion ^b   Colás, Eva ^b   Olivan, Mireia ^b   Doll, Andreas ^b   Alameda, Francesc ^c   Matias Guiu, Xavier ^d   Moreno Bueno, Gema ^e,i   Carey, Mark S ^f   Del Campo, Josep Maria ^b   Gil Moreno, Antonio ^b,c   Reventós, Jaume ^b,c,g,h   Rigau, Marina ^b   more..

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d HOSPITAL UNIVERSITARI ARNAU DE VILANOVA   (Spain)

^e INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g UNIVERSITAT INTERNACIONAL DE CATALUNYA   (Spain)

^h BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

ⁱ MD ANDERSON CANCER CENTER   (Spain)

Author keywords

Chemotherapy; MiRNAs; Ovarian cancer; Prediction; Prognosis; Tumor resistance

Indexed keywords

CISPLATIN; CYCLOPHOSPHAMIDE; MICRORNA; MICRORNA 100; MICRORNA 125B; MICRORNA 129 5P; MICRORNA 199A; MICRORNA 200A; MICRORNA 21; MICRORNA 214; MICRORNA 22; MICRORNA 23A; MICRORNA 24 2; MICRORNA 27A; MICRORNA 320A; MICRORNA 449B; NOTCH RECEPTOR; PACLITAXEL; PLATINUM COMPLEX; UNCLASSIFIED DRUG; TUMOR MARKER;

3' UNTRANSLATED REGION; CANCER PROGNOSIS; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; DISEASE SEVERITY; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE CONTROL; GENE MUTATION; HISTONE MODIFICATION; HUMAN; MICROARRAY ANALYSIS; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT RESPONSE; ANIMAL; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARIAN NEOPLASMS; PROGNOSIS; RNA INTERFERENCE;

ANIMALS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; OVARIAN NEOPLASMS; PROGNOSIS; RNA INTERFERENCE; TUMOR MARKERS, BIOLOGICAL;

EID: 84899806802     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.03.006     Document Type: Review

References (85)

1. Abdallah B.Y., Horne S.D., Kurkinen M., Stevens J.B., Liu G., Ye C.J., Barbat J., Bremer S.W., Heng H.H. Ovarian cancer evolution through stochastic genome alterations: defining the genomic role in ovarian cancer. Syst. Biol. Reprod. Med. 2014, 60:2-13.
2. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
3. Andaloussi S.E.L., Mager I., Breakefield X.O., Wood M.J. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov. 2013, 12:347-357.
4. Bader A.G., Brown D., Stoudemire J., Lammers P. Developing therapeutic microRNAs for cancer. Gene Ther. 2011, 18:1121-1126.
5. Barlin J.N., Jelinic P., Olvera N., Bogomolniy F., Bisogna M., Dao F., Barakat R.R., Chi D.S., Levine D.A. Validated gene targets associated with curatively treated advanced serous ovarian carcinoma. Gynecol. Oncol. 2013, 128:512-517.
6. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
7. Bast R.C., Hennessy B., Mills G.B. The biology of ovarian cancer: new opportunities for translation. Nat. Rev. Cancer. 2009, 9:415-428.
8. Boren T., Xiong Y., Hakam A., Wenham R., Apte S., Chan G., Kamath S.G., Chen D.T., Dressman H., Lancaster J.M. MicroRNAs and their target messenger RNAs associated with ovarian cancer response to chemotherapy. Gynecol. Oncol. 2009, 113:249-255.
9. Braun R., Finney R., Yan C., Chen Q.R., Hu Y., Edmonson M., Meerzaman D., Buetow K. Discovery analysis of TCGA data reveals association between germline genotype and survival in ovarian cancer patients. PLoS ONE 2013, 8:e55037.
10. Breving K., Esquela-Kerscher A. The complexities of microRNA regulation: mirandering around the rules. Int. J. Biochem. Cell Biol. 2010, 42:1316-1329.
11. Bushati N., Cohen S.M. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
12. Cai J., Yang C., Yang Q., Ding H., Jia J., Guo J., Wang J., Wang Z. Deregulation of let-7e in epithelial ovarian cancer promotes the development of resistance to cisplatin. Oncogenesis 2013, 2:e75.
13. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006, 6:857-866.
14. Calin G.A., Dumitru C.D., Shimizu M., Bichi R., Zupo S., Noch E., Aldler H., Rattan S., Keating M., Rai K., Rassenti L., Kipps T., Negrini M., Bullrich F., Croce C.M. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 2002, 99:15524-15529.
15. Ceruti M., Crosasso P., Brusa P., Arpicco S., Dosio F., Cattel L. Preparation, characterization, cytotoxicity and pharmacokinetics of liposomes containing water-soluble prodrugs of paclitaxel. J. Control Release 2000, 63:141-153.
16. Chen N., Chon H.S., Xiong Y., Marchion D.C., Judson P.L., Hakam A., Gonzalez-Bosquet J., Permuth-Wey J., Wenham R.M., Apte S.M., Cheng J.Q., Sellers T.A., Lancaster J.M. Human cancer cell line microRNAs associated with in vitro sensitivity to paclitaxel. Oncol. Rep. 2014, 31:376-383.
17. Croce C.M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009, 10:704-714.
18. Eitan R., Kushnir M., Lithwick-Yanai G., David M.B., Hoshen M., Glezerman M., Hod M., Sabah G., Rosenwald S., Levavi H. Tumor microRNA expression patterns associated with resistance to platinum based chemotherapy and survival in ovarian cancer patients. Gynecol. Oncol. 2009, 114:253-259.
19. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
20. Fu X., Tian J., Zhang L., Chen Y., Hao Q. Involvement of microRNA-93, a new regulator of PTEN/Akt signaling pathway, in regulation of chemotherapeutic drug cisplatin chemosensitivity in ovarian cancer cells. FEBS Lett. 2012, 586:1279-1286.
21. Gangaraju V.K., Lin H. MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 2009, 10:116-125.
22. Garzon R., Marcucci G., Croce C.M. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat. Rev. Drug Discov. 2010, 9:775-789.
23. Gibbons D.L., Lin W., Creighton C.J., Rizvi Z.H., Gregory P.A., Goodall G.J., Thilaganathan N., Du L., Zhang Y., Pertsemlidis A., Kurie J.M. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev. 2009, 23:2140-2151.
24. Gordanpour A., Nam R.K., Sugar L., Bacopoulos S., Seth A. MicroRNA detection in prostate tumors by quantitative real-time PCR (qPCR). J. Vis. Exp. 2012, 2012(63):e3874.
25. Helleman J., Jansen M.P., Burger C., van der Burg M.E., Berns E.M. Integrated genomics of chemotherapy resistant ovarian cancer: a role for extracellular matrix, TGFbeta and regulating microRNAs. Int. J. Biochem. Cell Biol. 2010, 42:25-30.
26. Heng H.H., Stevens J.B., Bremer S.W., Liu G., Abdallah B.Y., Ye C.J. Evolutionary mechanisms and diversity in cancer. Adv. Cancer Res. 2011, 112:217-253.
27. Hoskins W.J., McGuire W.P., Brady M.F., Homesley H.D., Creasman W.T., Berman M., Ball H., Berek J.S. The effect of diameter of largest residual disease on survival after primary cytoreductive surgery in patients with suboptimal residual epithelial ovarian carcinoma. Am. J. Obstet. Gynecol. 1994, 170:974-979. discussion 979-80.
28. Hsu F.H., Serpedin E., Hsiao T.H., Bishop A.J., Dougherty E.R., Chen Y. Reducing confounding and suppression effects in TCGA data: an integrated analysis of chemotherapy response in ovarian cancer. BMC Genomics. 2012, 13(Suppl 6):S13.
29. Hu X., Macdonald D.M., Huettner P.C., Feng Z., El Naqa I.M., Schwarz J.K., Mutch D.G., Grigsby P.W., Powell S.N., Wang X. A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol. Oncol. 2009, 114:457-464.
30. Huang S. Genetic and non-genetic instability in tumor progression: link between the fitness landscape and the epigenetic landscape of cancer cells. Cancer Metastasis Rev. 2013, 32:423-448.
31. Iorio M.V., Ferracin M., Liu C.G., Veronese A., Spizzo R., Sabbioni S., Magri E., Pedriali M., Fabbri M., Campiglio M., Menard S., Palazzo J.P., Rosenberg A., Musiani P., Volinia S., Nenci I., Calin G.A., Querzoli P., Negrini M., Croce C.M. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005, 65:7065-7070.
32. Iorio M.V., Visone R., Di Leva G., Donati V., Petrocca F., Casalini P., Taccioli C., Volinia S., Liu C.G., Alder H., Calin G.A., Menard S., Croce C.M. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007, 67:8699-8707.
33. Johnatty S.E., Beesley J., Gao B., Chen X., Lu Y., Law M.H., Henderson M.J., Russell A.J., Hedditch E.L., Emmanuel C., Fereday S., Webb P.M., Goode E.L., Vierkant R.A., Fridley B.L., Cunningham J.M., Fasching P.A., Beckmann M.W., Ekici A.B., Hogdall E., Kjaer S.K., Jensen A., Hogdall C., Brown R., Paul J., Lambrechts S., Despierre E., Vergote I., Lester J., Karlan B.Y., Heitz F., du Bois A., Harter P., Schwaab I., Bean Y., Pejovic T., Levine D.A., Goodman M.T., Camey M.E., Thompson P.J., Lurie G., Shildkraut J., Berchuck A., Terry K.L., Cramer D.W., Norris M.D., Haber M., MacGregor S., deFazio A., Chenevix-Trench G. ABCB1 (MDR1) polymorphisms and ovarian cancer progression and survival: a comprehensive analysis from the Ovarian Cancer Association Consortium and The Cancer Genome Atlas. Gynecol. Oncol. 2013, 131:8-14.
34. Kang J., D'Andrea A.D., Kozono D. A DNA repair pathway-focused score for prediction of outcomes in ovarian cancer treated with platinum-based chemotherapy. J. Natl. Cancer Inst. 2012, 104:670-681.
35. Koonings P.P., Campbell K., Mishell D.R., Grimes D.A. Relative frequency of primary ovarian neoplasms: a 10-year review. Obstet. Gynecol. 1989, 74:921-926.
36. Koshiol J., Wang E., Zhao Y., Marincola F., Landi M.T. Strengths and limitations of laboratory procedures for microRNA detection. Cancer Epidemiol. Biomarkers Prev. 2010, 19:907-911.
37. Kumar M.S., Lu J., Mercer K.L., Golub T.R., Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 2007, 39:673-677.
38. Kumar S., Kumar A., Shah P.P., Rai S.N., Panguluri S.K., Kakar S.S. MicroRNA signature of cis-platin resistant vs. cis-platin sensitive ovarian cancer cell lines. J. Ovarian Res. 2011, 4:17.
39. Landen C.N., Birrer M.J., Sood A.K. Early events in the pathogenesis of epithelial ovarian cancer. J. Clin. Oncol. 2008, 26:995-1005.
40. Lawrie T.A., Bryant A., Cameron A., Gray E., Morrison J. Pegylated liposomal doxorubicin for relapsed epithelial ovarian cancer. Cochrane Database Syst. Rev. 2013, 7. CD006910.
41. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
42. Lee H., Park C.S., Deftereos G., Morihara J., Stern J.E., Hawes S.E., Swisher E., Kiviat N.B., Feng Q. MicroRNA expression in ovarian carcinoma and its correlation with clinicopathological features. World J. Surg. Oncol. 2012, 10:174.
43. Leskela S., Leandro-Garcia L.J., Mendiola M., Barriuso J., Inglada-Perez L., Munoz I., Martinez-Delgado B., Redondo A., de Santiago J., Robledo M., Hardisson D., Rodriguez-Antona C. The miR-200 family controls beta-tubulin III expression and is associated with paclitaxel-based treatment response and progression-free survival in ovarian cancer patients. Endocr. Relat. Cancer 2011, 18:85-95.
44. Li X., Lu Y., Chen Y., Lu W., Xie X. MicroRNA profile of paclitaxel-resistant serous ovarian carcinoma based on formalin-fixed paraffin-embedded samples. BMC Cancer 2013, 13:216.
45. Liu Y., Sun Y., Broaddus R., Liu J., Sood A.K., Shmulevich I., Zhang W. Integrated analysis of gene expression and tumor nuclear image profiles associated with chemotherapy response in serous ovarian carcinoma. PLoS ONE 2012, 7:e36383.
46. Lu Y., Xiao J., Lin H., Bai Y., Luo X., Wang Z., Yang B. A single anti-microRNA antisense oligodeoxyribonucleotide (AMO) targeting multiple microRNAs offers an improved approach for microRNA interference. Nucleic Acids Res. 2009, 37:e24.
47. Lu L., Schwartz P., Scarampi L., Rutherford T., Canuto E.M., Yu H., Katsaros D. MicroRNA let-7a: a potential marker for selection of paclitaxel in ovarian cancer management. Gynecol. Oncol. 2011, 122:366-371.
48. Marchini S., Cavalieri D., Fruscio R., Calura E., Garavaglia D., Nerini I.F., Mangioni C., Cattoretti G., Clivio L., Beltrame L., Katsaros D., Scarampi L., Menato G., Perego P., Chiorino G., Buda A., Romualdi C., D'Incalci M. Association between miR-200c and the survival of patients with stage I epithelial ovarian cancer: a retrospective study of two independent tumour tissue collections. Lancet Oncol. 2011, 12:273-285.
49. Markman M., Bookman M.A. Second-line treatment of ovarian cancer. Oncologist 2000, 5:26-35.
50. Miska E.A. How microRNAs control cell division, differentiation and death. Curr. Opin. Genet. Dev. 2005, 15:563-568.
51. Nam E.J., Yoon H., Kim S.W., Kim H., Kim Y.T., Kim J.H., Kim J.W., Kim S. MicroRNA expression profiles in serous ovarian carcinoma. Clin. Cancer Res. 2008, 14:2690-2695.
52. Nazarenko I., Rupp A.K., Altevogt P. Exosomes as a potential tool for a specific delivery of functional molecules. Methods Mol. Biol. 2013, 1049:495-511.
53. Nishimura M., Jung E.J., Shah M.Y., Lu C., Spizzo R., Shimizu M., Han H.D., Ivan C., Rossi S., Zhang X., Nicoloso M.S., Wu S.Y., Almeida M.I., Bottsford-Miller J., Pecot C.V., Zand B., Matsuo K., Shahzad M.M., Jennings N.B., Rodriguez-Aguayo C., Lopez-Berestein G., Sood A.K., Calin G.A. Therapeutic synergy between microRNA and siRNA in ovarian cancer treatment. Cancer Discov. 2013, 3:1302-1315.
54. Olson P., Lu J., Zhang H., Shai A., Chun M.G., Wang Y., Libutti S.K., Nakakura E.K., Golub T.R., Hanahan D. MicroRNA dynamics in the stages of tumorigenesis correlate with hallmark capabilities of cancer. Genes Dev. 2009, 23:2152-2165.
55. Pelkmans L. Cell Biology. Using cell-to-cell variability-a new era in molecular biology. Science 2012, 336:425-426.
56. Polyzos A., Kosmas C., Toufexi H., Malamos N., Lagadas A., Kosmidis C., Ginopoulos P., Ziras N., Kandilis K., Georgoulias V. Docetaxel in combination with irinotecan (CPT-11) in platinum-resistant paclitaxel-pretreated ovarian cancer. Anticancer Res. 2005, 25:3559-3564.
57. Prislei S., Martinelli E., Mariani M., Raspaglio G., Sieber S., Ferrandina G., Shahabi S., Scambia G., Ferlini C. MiR-200c and HuR in ovarian cancer. BMC Cancer 2013, 13:72.
58. Seidman J.D., Horkayne-Szakaly I., Haiba M., Boice C.R., Kurman R.J., Ronnett B.M. The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin. Int. J. Gynecol. Pathol. 2004, 23:41-44.
59. Sfakianos G.P., Iversen E.S., Whitaker R., Akushevich L., Schildkraut J.M., Murphy S.K., Marks J.R., Berchuck A. Validation of ovarian cancer gene expression signatures for survival and subtype in formalin fixed paraffin embedded tissues. Gynecol. Oncol. 2013, 129:159-164.
60. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin. 2013, 63:11-30.
61. Sohn I., Jung W.Y., Sung C.O. Somatic hypermutation and outcomes of platinum based chemotherapy in patients with high grade serous ovarian cancer. Gynecol. Oncol. 2012, 126:103-108.
62. Sorrentino A., Liu C.G., Addario A., Peschle C., Scambia G., Ferlini C. Role of microRNAs in drug-resistant ovarian cancer cells. Gynecol. Oncol. 2008, 111:478-486.
63. Spencer S.L., Gerety R.A., Pienta K.J., Forrest S. Modeling somatic evolution in tumorigenesis. PLoS Comput. Biol. 2006, 2:e108.
64. Stein S.M., Tiersten A., Hochster H.S., Blank S.V., Pothuri B., Curtin J., Shapira I., Levinson B., Ivy P., Joseph B., Guddati A.K., Muggia F. A phase 2 study of oxaliplatin combined with continuous infusion topotecan for patients with previously treated ovarian cancer. Int. J. Gynecol. Cancer 2013, 23:1577-1582.
65. Su A., Zhang J., Pan Z.H., Zhou Q.M., Lv X. Salvage therapy of gemcitabine plus endostar significantly improves progression-free survival (PFS) with platinum-resistant recurrent epithelial ovarian cancer. Asian Pac. J. Cancer Prev. 2013, 14:1841-1846.
66. Tang, Z., Ow, G.S., Thiery, J.P., Ivshina, A.V., Kuznetsov, V.A., 2013. Meta-analysis of transcriptome reveals let-7b as an unfavorable prognostic biomarker and predicts molecular and clinical subclasses in high-grade serous ovarian carcinoma. Int. J. Cancer.
67. TCGA Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
68. 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., Traficante N., Fereday S., Hung J.A., Chiew Y.E., Haviv I., Gertig D., DeFazio A., Bowtell D.D. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res. 2008, 14:5198-5208.
69. van Dommelen S.M., Vader P., Lakhal S., Kooijmans S.A., van Solinge W.W., Wood M.J., Schiffelers R.M. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J. Control Release. 2012, 161:635-644.
70. van Jaarsveld M.T., Helleman J., Berns E.M., Wiemer E.A. MicroRNAs in ovarian cancer biology and therapy resistance. Int. J. Biochem. Cell Biol. 2010, 42:1282-1290.
71. van Jaarsveld M.T., Helleman J., Boersma A.W., van Kuijk P.F., van Ijcken W.F., Despierre E., Vergote I., Mathijssen R.H., Berns E.M., Verweij J., Pothof J., Wiemer E.A. MiR-141 regulates KEAP1 and modulates cisplatin sensitivity in ovarian cancer cells. Oncogene 2013, 32:4284-4293.
72. Vecchione A., Belletti B., Lovat F., Volinia S., Chiappetta G., Giglio S., Sonego M., Cirombella R., Onesti E.C., Pellegrini P., Califano D., Pignata S., Losito S., Canzonieri V., Sorio R., Alder H., Wernicke D., Stoppacciaro A., Baldassarre G., Croce C.M. A microRNA signature defines chemoresistance in ovarian cancer through modulation of angiogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:9845-9850.
73. Vergote I., Trope C.G., Amant F., Kristensen G.B., Ehlen T., Johnson N., Verheijen R.H., van der Burg M.E., Lacave A.J., Panici P.B., Kenter G.G., Casado A., Mendiola C., Coens C., Verleye L., Stuart G.C., Pecorelli S., Reed N.S. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N. Engl. J. Med. 2010, 363:943-953.
74. Verhaak R.G., Tamayo P., Yang J.Y., Hubbard D., Zhang H., Creighton C.J., Fereday S., Lawrence M., Carter S.L., Mermel C.H., Kostic A.D., Etemadmoghadam D., Saksena G., Cibulskis K., Duraisamy S., Levanon K., Sougnez C., Tsherniak A., Gomez S., Onofrio R., Gabriel S., Chin L., Zhang N., Spellman P.T., Zhang Y., Akbani R., Hoadley K.A., Kahn A., Kobel M., Huntsman D., Soslow R.A., Defazio A., Birrer M.J., Gray J.W., Weinstein J.N., Bowtell D.D., Drapkin R., Mesirov J.P., Getz G., Levine D.A., Meyerson M. Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J. Clin. Invest. 2013, 123:517-525.
75. Vidal A., Munoz C., Guillen M.J., Moreto J., Puertas S., Martinez-Iniesta M., Figueras A., Padulles L., Garcia-Rodriguez F.J., Berdiel-Acer M., Pujana M.A., Salazar R., Gil-Martin M., Marti L., Ponce J., Mollevi D.G., Capella G., Condom E., Vinals F., Huertas D., Cuevas C., Esteller M., Aviles P., Villanueva A. Lurbinectedin (PM01183), a new DNA minor groove binder, inhibits growth of orthotopic primary graft of cisplatin-resistant epithelial ovarian cancer. Clin. Cancer Res. 2012, 18:5399-5411.
76. Vogelstein B., Kinzler K.W. The multistep nature of cancer. Trends Genet. 1993, 9:138-141.
77. Yang H., Kong W., He L., Zhao J.J., O'Donnell J.D., Wang J., Wenham R.M., Coppola D., Kruk P.A., Nicosia S.V., Cheng J.Q. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008, 68:425-433.
78. Yang N., Kaur S., Volinia S., Greshock J., Lassus H., Hasegawa K., Liang S., Leminen A., Deng S., Smith L., Johnstone C.N., Chen X.M., Liu C.G., Huang Q., Katsaros D., Calin G.A., Weber B.L., Butzow R., Croce C.M., Coukos G., Zhang L. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res. 2008, 68:10307-10314.
79. Yang J.Y., Yoshihara K., Tanaka K., Hatae M., Masuzaki H., Itamochi H., Takano M., Ushijima K., Tanyi J.L., Coukos G., Lu Y., Mills G.B., Verhaak R.G. Predicting time to ovarian carcinoma recurrence using protein markers. J. Clin. Invest. 2013, 123:3740-3750.
80. Yang D., Sun Y., Hu L., Zheng H., Ji P., Pecot C.V., Zhao Y., Reynolds S., Cheng H., Rupaimoole R., Cogdell D., Nykter M., Broaddus R., Rodriguez-Aguayo C., Lopez-Berestein G., Liu J., Shmulevich I., Sood A.K., Chen K., Zhang W. Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell 2013, 23:186-199.
81. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
82. Yoshihara K., Tsunoda T., Shigemizu D., Fujiwara H., Hatae M., Masuzaki H., Katabuchi H., Kawakami Y., Okamoto A., Nogawa T., Matsumura N., Udagawa Y., Saito T., Itamochi H., Takano M., Miyagi E., Sudo T., Ushijima K., Iwase H., Seki H., Terao Y., Enomoto T., Mikami M., Akazawa K., Tsuda H., Moriya T., Tajima A., Inoue I., Tanaka K. High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway. Clin. Cancer Res. 2012, 18:1374-1385.
83. Zaman M.S., Maher D.M., Khan S., Jaggi M., Chauhan S.C. Current status and implications of microRNAs in ovarian cancer diagnosis and therapy. J. Ovarian Res. 2012, 5:44.
84. Zhang L., Volinia S., Bonome T., Calin G.A., Greshock J., Yang N., Liu C.G., Giannakakis A., Alexiou P., Hasegawa K., Johnstone C.N., Megraw M.S., Adams S., Lassus H., Huang J., Kaur S., Liang S., Sethupathy P., Leminen A., Simossis V.A., Sandaltzopoulos R., Naomoto Y., Katsaros D., Gimotty P.A., DeMichele A., Huang Q., Butzow R., Rustgi A.K., Weber B.L., Birrer M.J., Hatzigeorgiou A.G., Croce C.M., Coukos G. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc. Natl. Acad. Sci. USA 2008, 105:7004-7009.
85. Zhang, X., Huang, L., Zhao, Y., Tan, W., 2013. Downregulation of miR-130a contributes to cisplatin resistance in ovarian cancer cells by targeting X-linked inhibitor of apoptosis (XIAP) directly. Acta Biochim. Biophys. Sin. (Shanghai).