Global miRNA expression analysis of serous and clear cell ovarian carcinomas identifies differentially expressed miRNAs including miR-200c-3p as a prognostic marker

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Vilming Elgaaen, Bente ^a   Olstad, Ole K ^b   Haug, Kari Bente F ^b   Brusletto, Berit ^b   Sandvik, Leiv ^b,c   Staff, Anne C ^b,c   Gautvik, Kaare M ^b,c   Davidson, Ben ^a,c  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b Cancer and Surgery Clinic OUH   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Microarray; MicroRNA; Ovarian carcinoma; Quantitative PCR; Survival

Indexed keywords

ADENOCARCINOMA, CLEAR CELL; ADULT; AGED; AGED, 80 AND OVER; CYSTADENOCARCINOMA, SEROUS; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MIDDLE AGED; OVARIAN NEOPLASMS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84893697547     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-80     Document Type: Article

References (60)

1. Cancer Registry of Norway Cancer in Norway 2010 - Cancer incidence, mortality, survival and prevalence in Norway 2012, Oslo: Cancer Registry of Norway, Cancer Registry of Norway.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62:10-29. 10.3322/caac.20138, 22237781.
3. Prat J. Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Arch 2012, 460:237-249. 10.1007/s00428-012-1203-5, 22322322.
4. Anglesio MS, Carey MS, Kobel M, Mackay H, Huntsman DG. Clear cell carcinoma of the ovary: a report from the first ovarian clear cell symposium, June 24th, 2010. Gynecol Oncol 2011, 121:407-415. 10.1016/j.ygyno.2011.01.005, 21276610.
5. Vang R, Shih I, Kurman RJ. Ovarian low-grade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv Anat Pathol 2009, 16:267-282. 10.1097/PAP.0b013e3181b4fffa, 2745605, 19700937.
6. Shih I, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 2004, 164:1511-1518. 10.1016/S0002-9440(10)63708-X, 1615664, 15111296.
7. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011, 12:99-110. 10.1038/nrg2936, 21245828.
8. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838. 10.1038/nature03702, 15944708.
9. Torres A, Torres K, Maciejewski R, Harvey WH. MicroRNAs and their role in gynecological tumors. Med Res Rev 2011, 31:895-923. 10.1002/med.20205, 20358579.
10. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006, 103:2257-2261. 10.1073/pnas.0510565103, 1413718, 16461460.
11. Kuhlmann JD, Rasch J, Wimberger P. Kasimir-Bauer S: microRNA and the pathogenesis of ovarian cancer-a new horizon for molecular diagnostics and treatment?. Clin Chem Lab Med 2012, 50:601-615.
12. Dahiya N, Morin PJ. MicroRNAs in ovarian carcinomas. Endocr Relat Cancer 2010, 17:F77-F89. 10.1677/ERC-09-0203, 2856347, 19903743.
13. Vaksman O, Stavnes HT, Kaern J, Trope CG, Davidson B, Reich R. miRNA profiling along tumour progression in ovarian carcinoma. J Cell Mol Med 2011, 15:1593-1602. 10.1111/j.1582-4934.2010.01148.x, 20716115.
14. Li SD, Zhang JR, Wang YQ, Wan XP. The role of microRNAs in ovarian cancer initiation and progression. J Cell Mol Med 2010, 14:2240-2249. 10.1111/j.1582-4934.2010.01058.x, 20345848.
15. Dahiya N, Sherman-Baust CA, Wang TL, Davidson B, Shih I, Zhang Y, Wood W, Becker KG, Morin PJ. MicroRNA expression and identification of putative miRNA targets in ovarian cancer. PLoS One 2008, 3:e2436. 10.1371/journal.pone.0002436, 2410296, 18560586.
16. Zhang L, Volinia S, Bonome T, Calin GA, Greshock J, Yang N, Liu CG, Giannakakis A, Alexiou P, Hasegawa K, Johnstone CN, Megraw MS, Adams S, Lassus H, Huang J, Kaur S, Liang S, Sethupathy P, Leminen A, Simossis VA, Sandaltzopoulos R, Naomoto Y, Katsaros D, Gimotty PA, DeMichele A, Huang Q, Butzow R, Rustgi AK, Weber BL, Birrer MJ, et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc Natl Acad Sci U S A 2008, 105:7004-7009. 10.1073/pnas.0801615105, 2383982, 18458333.
17. Yang H, Kong W, He L, Zhao JJ, O'Donnell JD, Wang J, Wenham RM, Coppola D, Kruk PA, Nicosia SV, Cheng JQ. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res 2008, 68:425-433. 10.1158/0008-5472.CAN-07-2488, 18199536.
18. Shih KK, Qin LX, Tanner EJ, Zhou Q, Bisogna M, Dao F, Olvera N, Viale A, Barakat RR, Levine DA. A microRNA survival signature (MiSS) for advanced ovarian cancer. Gynecol Oncol 2011, 121:444-450. 10.1016/j.ygyno.2011.01.025, 21354599.
19. Kim TH, Kim YK, Kwon Y, Heo JH, Kang H, Kim G, An HJ. Deregulation of miR-519a, 153, and 485-5p and its clinicopathological relevance in ovarian epithelial tumours. Histopathology 2010, 57:734-743. 10.1111/j.1365-2559.2010.03686.x, 21083603.
20. Wurz K, Garcia RL, Goff BA, Mitchell PS, Lee JH, Tewari M, Swisher EM. MiR-221 and MiR-222 alterations in sporadic ovarian carcinoma: relationship to CDKN1B, CDKNIC and overall survival. Genes Chromosomes Cancer 2010, 49:577-584. 2869465, 20461750.
21. Hu X, Macdonald DM, Huettner PC, Feng Z, El Naqa IM, Schwarz JK, Mutch DG, Grigsby PW, Powell SN, Wang X. A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol 2009, 114:457-464. 10.1016/j.ygyno.2009.05.022, 19501389.
22. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, Kim JH, Kim JW, Kim S. MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res 2008, 14:2690-2695. 10.1158/1078-0432.CCR-07-1731, 18451233.
23. Eitan R, Kushnir M, Lithwick-Yanai G, David MB, 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. 10.1016/j.ygyno.2009.04.024, 19446316.
24. Yang N, Kaur S, Volinia S, Greshock J, Lassus H, Hasegawa K, Liang S, Leminen A, Deng S, Smith L, Johnstone CN, Chen XM, Liu CG, Huang Q, Katsaros D, Calin GA, Weber BL, Butzow R, Croce CM, 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. 10.1158/0008-5472.CAN-08-1954, 2762326, 19074899.
25. Boren T, Xiong Y, Hakam A, Wenham R, Apte S, Chan G, Kamath SG, Chen DT, Dressman H, Lancaster JM. MicroRNAs and their target messenger RNAs associated with ovarian cancer response to chemotherapy. Gynecol Oncol 2009, 113:249-255. 10.1016/j.ygyno.2009.01.014, 19237188.
26. Iorio MV, Visone R, Di LG, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, Calin GA, Menard S, Croce CM. MicroRNA signatures in human ovarian cancer. Cancer Res 2007, 67:8699-8707. 10.1158/0008-5472.CAN-07-1936, 17875710.
27. Elgaaen BV, Haug KB, Wang J, Olstad OK, Fortunati D, Onsrud M, Staff AC, Sauer T, Gautvik KM. POLD2 and KSP37 (FGFBP2) correlate strongly with histology, stage and outcome in ovarian carcinomas. PLoS One 2010, 5:e13837. 10.1371/journal.pone.0013837, 2973954, 21079801.
28. Zorn KK, Jazaeri AA, Awtrey CS, Gardner GJ, Mok SC, Boyd J, Birrer MJ. Choice of normal ovarian control influences determination of differentially expressed genes in ovarian cancer expression profiling studies. Clin Cancer Res 2003, 9:4811-4818.
29. Elgaaen BV, Olstad OK, Sandvik L, Odegaard E, Sauer T, Staff AC, Gautvik KM. ZNF385B and VEGFA are strongly differentially expressed in serous ovarian carcinomas and correlate with survival. PLoS One 2012, 7:e46317. 10.1371/journal.pone.0046317, 3460818, 23029477.
30. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
32. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108. 10.1038/nprot.2008.73, 18546601.
33. Elson-Schwab I, Lorentzen A, Marshall CJ. MicroRNA-200 family members differentially regulate morphological plasticity and mode of melanoma cell invasion. PLoS One 2010, 5: doi: 10.1371/journal.pone.0013176.
34. Volinia S, Galasso M, Sana ME, Wise TF, Palatini J, Huebner K, Croce CM. Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc Natl Acad Sci U S A 2012, 109:3024-3029. 10.1073/pnas.1200010109, 3286983, 22315424.
35. Slaby O, Svoboda M, Michalek J, Vyzula R. MicroRNAs in colorectal cancer: translation of molecular biology into clinical application. Mol Cancer 2009, 8:102. 10.1186/1476-4598-8-102, 2780389, 19912656.
36. Paranjape T, Slack FJ, Weidhaas JB. MicroRNAs: tools for cancer diagnostics. Gut 2009, 58:1546-1554. 10.1136/gut.2009.179531, 2802653, 19834118.
37. 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.
38. Hurteau GJ, Carlson JA, Roos E, Brock GJ. Stable expression of miR-200c alone is sufficient to regulate TCF8 (ZEB1) and restore E-cadherin expression. Cell Cycle 2009, 8:2064-2069. 10.4161/cc.8.13.8883, 19502803.
39. Li Y, VandenBoom TG, Kong D, Wang Z, Ali S, Philip PA, Sarkar FH. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 2009, 69:6704-6712. 10.1158/0008-5472.CAN-09-1298, 2727571, 19654291.
40. Kent OA, Mullendore M, Wentzel EA, Lopez-Romero P, Tan AC, Alvarez H, West K, Ochs MF, Hidalgo M, Arking DE, Maitra A, Mendell JT. A resource for analysis of microRNA expression and function in pancreatic ductal adenocarcinoma cells. Cancer Biol Ther 2009, 8:2013-2024. 10.4161/cbt.8.21.9685, 2824894, 20037478.
41. Davidson B, Trope CG, Reich R. Epithelial-mesenchymal transition in ovarian carcinoma. Front Oncol 2012, 2:33. 3356037, 22655269.
42. Huynh C, Segura MF, Gaziel-Sovran A, Menendez S, Darvishian F, Chiriboga L, Levin B, Meruelo D, Osman I, Zavadil J, Marcusson EG, Hernando E. Efficient in vivo microRNA targeting of liver metastasis. Oncogene 2011, 30:1481-1488. 10.1038/onc.2010.523, 21102518.
43. Muinos-Gimeno M, Guidi M, Kagerbauer B, Martin-Santos R, Navines R, Alonso P, Menchon JM, Gratacos M, Estivill X, Espinosa-Parrilla Y. Allele variants in functional MicroRNA target sites of the neurotrophin-3 receptor gene (NTRK3) as susceptibility factors for anxiety disorders. Hum Mutat 2009, 30:1062-1071. 10.1002/humu.21005, 19370765.
44. Hidaka H, Seki N, Yoshino H, Yamasaki T, Yamada Y, Nohata N, Fuse M, Nakagawa M, Enokida H. Tumor suppressive microRNA-1285 regulates novel molecular targets: aberrant expression and functional significance in renal cell carcinoma. Oncotarget 2012, 3:44-57. 3292891, 22294552.
45. Findlay VJ, Turner DP, Moussa O, Watson DK. MicroRNA-mediated inhibition of prostate-derived Ets factor messenger RNA translation affects prostate-derived Ets factor regulatory networks in human breast cancer. Cancer Res 2008, 68:8499-8506. 10.1158/0008-5472.CAN-08-0907, 2680499, 18922924.
46. Stavnes HT, Nymoen DA, Langerod A, Holth A, Borresen Dale AL, Davidson B. AZGP1 and SPDEF mRNA expression differentiates breast carcinoma from ovarian serous carcinoma. Virchows Arch 2013, 462:163-173. 10.1007/s00428-012-1347-3, 23242172.
47. Marchini S, Cavalieri D, Fruscio R, Calura E, Garavaglia D, Nerini IF, 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. 10.1016/S1470-2045(11)70012-2, 21345725.
48. Leskela S, Leandro-Garcia LJ, 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.
49. Kan CW, Hahn MA, Gard GB, Maidens J, Huh JY, Marsh DJ, Howell VM. Elevated levels of circulating microRNA-200 family members correlate with serous epithelial ovarian cancer. BMC Cancer 2012, 12:627. 10.1186/1471-2407-12-627, 3542279, 23272653.
50. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007, 318:1931-1934. 10.1126/science.1149460, 18048652.
51. Mortensen RD, Serra M, Steitz JA, Vasudevan S. Posttranscriptional activation of gene expression in Xenopus laevis oocytes by microRNA-protein complexes (microRNPs). Proc Natl Acad Sci U S A 2011, 108:8281-8286. 10.1073/pnas.1105401108, 3100953, 21536868.
52. Vasudevan S. Posttranscriptional upregulation by microRNAs. Wiley Interdiscip Rev RNA 2012, 3:311-330. 10.1002/wrna.121, 22072587.
53. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001, 22:255-288.
54. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P, Verheijen RH. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 2001, 195:451-456. 10.1002/path.1000, 11745677.
55. Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 2006, 30:230-236. 10.1097/01.pas.0000180854.28831.77, 16434898.
56. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, Berkowitz RS, Muto MG, Crum CP. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am J Surg Pathol 2007, 31:161-169. 10.1097/01.pas.0000213335.40358.47, 17255760.
57. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD, Crum CP. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 2007, 211:26-35. 10.1002/path.2091, 17117391.
58. Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y, Crum CP. Serous carcinogenesis in the fallopian tube: a descriptive classification. Int J Gynecol Pathol 2008, 27:1-9. 10.1097/pgp.0b013e31814b191f, 18156967.
59. Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S, Crum CP. A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecol Oncol 2008, 109:168-173. 10.1016/j.ygyno.2008.01.012, 2746001, 18342932.
60. Auersperg N. The origin of ovarian carcinomas: a unifying hypothesis. Int J Gynecol Pathol 2011, 30:12-21. 10.1097/PGP.0b013e3181f45f3e, 21131839.