New insights on the pathogenesis of ovarian carcinoma: molecular basis and clinical implications

References

• Holschneider CH, Berek JS. Ovarian cancer: epidemiology, biology, and prognostic factors. Semin Surg Oncol 2000;19:3–10.
   PubMed Web of Science ®Google Scholar
• Permuth-Wey J, Sellers TA. Epidemiology of ovarian cancer. Methods Mol Biol 2009;472:413–437.
   PubMedGoogle Scholar
• Fleming JS, Beaugié CR, Haviv I, Chenevix-Trench G, Tan OL. Incessant ovulation, inflammation and epithelial ovarian carcinogenesis: revisiting old hypotheses. Mol Cell Endocrinol 2006;247:4–21.
   PubMed Web of Science ®Google Scholar
• Rodriguez G. New insights regarding pharmacologic approaches for ovarian cancer prevention. Hematol Oncol Clin North Am 2003;17:1007–20.
   PubMed Web of Science ®Google Scholar
• Purdie DM, Bain CJ, Siskind V, Webb PM, Green AC. Ovulation and risk of epithelial ovarian cancer. Int J Cancer 2003;104:228–232.
   PubMed Web of Science ®Google Scholar
• Gadducci A, Cosio S, Gargini A, Genazzani AR. Sex-steroid hormones, gonadotropin and ovarian carcinogenesis: a review of epidemiological and experimental data. Gynecol Endocrinol 2004;19:216–228.
   PubMed Web of Science ®Google Scholar
• Rodriguez GC, Walmer DK, Cline M, Krigman H, Lessey BA, Whitaker RS, Dodge R, Hughes CL. Effect of progestin on the ovarian epithelium of macaques: cancer prevention through apoptosis? J Soc Gynecol Investig 1998;5:271–276.
   PubMedGoogle Scholar
• Rodriguez GC, Nagarsheth NP, Lee KL, Bentley RC, Walmer DK, Cline M, Whitaker RS, et al. Progestin-induced apoptosis in the Macaque ovarian epithelium: differential regulation of transforming growth factor-β. J Natl Cancer Inst 2002;94:50–60.
   PubMed Web of Science ®Google Scholar
• Syed V, Ho SM. Progesterone-induced apoptosis in immortalized normal and malignant human ovarian surface epithelial cells involves enhanced expression of FasL. Oncogene 2003;22:6883–6890.
   PubMed Web of Science ®Google Scholar
• Schildkraut JM, Calingaert B, Marchbanks PA, Moorman PG, Rodriguez GC. Impact of progestin and estrogen potency in oral contraceptives on ovarian cancer risk. J Natl Cancer Inst 2002;94:32–38.
   PubMed Web of Science ®Google Scholar
• Lacey JV Jr, Mink PJ, Lubin JH, Sherman ME, Troisi R, Hartge P, Schatzkin A, Schairer C. Menopausal hormone replacement therapy and risk of ovarian cancer. JAMA 2002;288:334–341.
   PubMed Web of Science ®Google Scholar
• Riman T, Dickman PW, Nilsson S, Correia N, Nordlinder H, Magnusson CM, Weiderpass E, Persson IR. Hormone replacement therapy and the risk of invasive epithelial ovarian cancer in Swedish women. J Natl Cancer Inst 2002;94:497–504.
   PubMed Web of Science ®Google Scholar
• Evangelou A, Jindal SK, Brown TJ, Letarte M. Down-regulation of transforming growth factor β receptors by androgen in ovarian cancer cells. Cancer Res 2000;60:929–935.
   PubMed Web of Science ®Google Scholar
• Shih IeM Kurman, RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 2004;164:1511–1518.
   PubMedGoogle Scholar
• Kurman RJ, Shih IeM. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer–shifting the paradigm. Hum Pathol 2011;42:918–931.
   PubMed Web of Science ®Google Scholar
• Kurman RJ, Shih IeM. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 2010;34:433–443.
   PubMed Web of Science ®Google Scholar
• Mok SC, Bell DA, Knapp RC, Fishbaugh PM, Welch WR, Muto MG, Berkowitz RS, Tsao SW. Mutation of K-ras protooncogene in human ovarian epithelial tumors of borderline malignancy. Cancer Res 1993;53:1489–1492.
   PubMed Web of Science ®Google Scholar
• Singer G, Oldt R 3rd, Cohen Y, Wang BG, Sidransky D, Kurman RJ, Shih IeM Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst 2003;95:484–486.
   PubMed Web of Science ®Google Scholar
• Catasús L, Bussaglia E, Rodrguez I, Gallardo A, Pons C, Irving JA, Prat J. Molecular genetic alterations in endometrioid carcinomas of the ovary: similar frequency of beta-catenin abnormalities but lower rate of microsatellite instability and PTEN alterations than in uterine endometrioid carcinomas. Hum Pathol 2004;35:1360–1368.
   PubMed Web of Science ®Google Scholar
• Kuo KT, Guan B, Feng Y, Mao TL, Chen X, Jinawath N, Wang Y, et al. Analysis of DNA copy number alterations in ovarian serous tumors identifies new molecular genetic changes in low-grade and high-grade carcinomas. Cancer Res 2009;69:4036–4042.
   PubMedGoogle Scholar
• Kuo KT, Mao TL, Jones S, Veras E, Ayhan A, Wang TL, Glas R, et al. Frequent activating mutations of PIK3CA in ovarian clear cell carcinoma. Am J Pathol 2009;174:1597–1601.
   PubMed Web of Science ®Google Scholar
• Cho KR, Shih IeM. Ovarian cancer. Annu Rev Pathol 2009;4:287–313.
   PubMed Web of Science ®Google Scholar
• Auner V, Kriegshäuser G, Tong D, Horvat R, Reinthaller A, Mustea A, Zeillinger R. KRAS mutation analysis in ovarian samples using a high sensitivity biochip assay. BMC Cancer 2009;9:111.
   PubMedGoogle Scholar
• Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T, Senz J, et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 2010;363:1532–1543.
   PubMed Web of Science ®Google Scholar
• Munksgaard PS, Blaakaer J. The association between endometriosis and ovarian cancer: A review of histological, genetic and molecular alterations. Gynecol Oncol 2012;124:164–169.
   PubMed Web of Science ®Google Scholar
• Salani R, Kurman RJ, Giuntoli R 2nd, Gardner G, Bristow R, Wang TL, Shih IM. Assessment of TP53 mutation using purified tissue samples of ovarian serous carcinomas reveals a higher mutation rate than previously reported and does not correlate with drug resistance. Int J Gynecol Cancer 2008;18:487–491.
   PubMed Web of Science ®Google Scholar
• Jasin M. Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 2002;21:8981–8993.
   PubMed Web of Science ®Google Scholar
• Turner N, Tutt A, Ashworth A. Hallmarks of ‘BRCAness’ in sporadic cancers. Nat Rev Cancer 2004;4:814–819.
   PubMed Web of Science ®Google Scholar
• Bowell DD. The genesis and evolution of high-grade serous ovarian cancer. Nat Rev Cancer 2010;10:803–808.
   PubMedGoogle Scholar
• Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 2001;195:451–456.
   PubMed Web of Science ®Google Scholar
• Lundberg AS, Weinberg RA. Control of the cell cycle and apoptosis. Eur J Cancer 1999;35:531–539.
   PubMed Web of Science ®Google Scholar
• Gadducci A, Cosio S, Tana R, Genazzani AR. Serum and tissue biomarkers as predictive and prognostic variables in epithelial ovarian cancer. Crit Rev Oncol Hematol 2009;69:12–27.
   PubMedGoogle Scholar
• Chen HZ, Tsai SY, Leone G. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 2009;9:785–797.
   PubMed Web of Science ®Google Scholar
• Callahan MJ, Crum CP, Medeiros F, Kindelberger DW, Elvin JA, Garber JE, Feltmate CM, et al. Primary fallopian tube malignancies in BRCA-positive women undergoing surgery for ovarian cancer risk reduction. J Clin Oncol 2007;25:3985–3990.
   PubMed Web of Science ®Google Scholar
• Shaw PA, Rouzbahman M, Pizer ES, Pintilie M, Begley H. Candidate serous cancer precursors in fallopian tube epithelium of BRCA1/2 mutation carriers. Mod Pathol 2009;22:1133–1138.
   PubMed Web of Science ®Google Scholar
• Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am J Surg Pathol 2007;31:161–169.
   PubMed Web of Science ®Google Scholar
• Sehdev AS, Kurman RJ, Kuhn E, Shih IeM. Serous tubal intraepithelial carcinoma upregulates markers associated with high-grade serous carcinomas including Rsf-1 (HBXAP), cyclin E and fatty acid synthase. Mod Pathol 2010;23:844–855.
   PubMed Web of Science ®Google Scholar
• Cosma MP, Tanaka T, Nasmyth K. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 1999;97:299–311.
   PubMed Web of Science ®Google Scholar
• Vignali M, Hassan AH, Neely KE, Workman JL. ATP-dependent chromatin-remodeling complexes. Mol Cell Biol 2000;20:1899–1910.
   PubMedGoogle Scholar
• Loyola A, Huang JY, LeRoy G, Hu S, Wang YH, Donnelly RJ, Lane WS, et al. Functional analysis of the subunits of the chromatin assembly factor RSF. Mol Cell Biol 2003;23:6759–6768.
   PubMedGoogle Scholar
• Wang HQ, Altomare DA, Skele KL, Poulikakos PI, Kuhajda FP, Di Cristofano A, Testa JR. Positive feedback regulation between AKT activation and fatty acid synthase expression in ovarian carcinoma cells. Oncogene 2005;24:3574–3582.
   PubMed Web of Science ®Google Scholar
• Zhou W, Han WF, Landree LE, Thupari JN, Pinn ML, Bililign T, Kim EK, et al. Fatty acid synthase inhibition activates AMP-activated protein kinase in SKOV3 human ovarian cancer cells. Cancer Res 2007;67:2964–2971.
   PubMed Web of Science ®Google Scholar
• Grunt TW, Wagner R, Grusch M, Berger W, Singer CF, Marian B, Zielinski CC, Lupu R. Interaction between fatty acid synthase- and ErbB-systems in ovarian cancer cells. Biochem Biophys Res Commun 2009;385:454–459.
   PubMed Web of Science ®Google Scholar
• Comer MT, Leese HJ, Southgate J. Induction of a differentiated ciliated cell phenotype in primary cultures of Fallopian tube epithelium. Hum Reprod 1998;13:3114–3120.
   PubMed Web of Science ®Google Scholar
• Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, et al. 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.
   PubMedGoogle Scholar
• Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, et al. 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.
   PubMed Web of Science ®Google Scholar
• Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, et al. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 2007;211:26–35.
   PubMed Web of Science ®Google Scholar
• Norquist BM, Garcia RL, Allison KH, Jokinen CH, Kernochan LE, Pizzi CC, Barrow BJ, et al. The molecular pathogenesis of hereditary ovarian carcinoma: alterations in the tubal epithelium of women with BRCA1 and BRCA2 mutations. Cancer 2010;116:5261–5271.
   PubMed Web of Science ®Google Scholar
• Riches LC, Lynch AM, Gooderham NJ. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 2008;23:331–339.
   PubMedGoogle Scholar
• Vicus D, Shaw PA, Finch A, Rosen B, Murphy J, Armel S, Sun P, Narod SA. Risk factors for non-invasive lesions of the fallopian tube in BRCA mutation carriers. Gynecol Oncol 2010;118:295–298.
   PubMedGoogle Scholar
• Marquez RT, Baggerly KA, Patterson AP, Liu J, Broaddus R, Frumovitz M, Atkinson EN, et al. Patterns of gene expression in different histotypes of epithelial ovarian cancer correlate with those in normal fallopian tube, endometrium, and colon. Clin Cancer Res 2005;11:6116–6126.
   PubMedGoogle Scholar
• Gagner JP, Mittal K. Malignant mixed Mullerian tumor of the fimbriated end of the fallopian tube: origin as an intraepithelial carcinoma. Gynecol Oncol 2005;97:219–222.
   PubMedGoogle Scholar
• Veras E, Mao TL, Ayhan A, Ueda S, Lai H, Hayran M, Shih IeM, Kurman RJ. Cystic and adenofibromatous clear cell carcinomas of the ovary: distinctive tumors that differ in their pathogenesis and behavior: a clinicopathologic analysis of 122 cases. Am J Surg Pathol 2009;33:844–853.
   PubMedGoogle Scholar
• Singh N. Pathology of malignant and borderline ovarian tumours. In: Ayhan A, Reed N, Gultekin M, Dursun P, Editors. “Textbook of Gynaecological Oncology”. Ankara, Instanbul, Kosuyolu: Gunes Publishing; 2012. pp 333–338.
   Google Scholar
• Bulun SE. Endometriosis. N Engl J Med 2009;360:268–279.
   PubMed Web of Science ®Google Scholar
• Martin DC. Cancer and endometriosis: do we need to be concerned? Semin Reprod Endocrinol 1997;15:319–324.
   PubMedGoogle Scholar
• Rosenblatt KA, Thomas DB. Reduced risk of ovarian cancer in women with a tubal ligation or hysterectomy. The World Health Organization Collaborative Study of Neoplasia and Steroid Contraceptives. Cancer Epidemiol Biomarkers Prev 1996;5:933–935.
   PubMedGoogle Scholar
• Banet N, Shih IeM Kurman, RJ. The Origin and pathogenesis of epithelial ovarian cancer. In: Ayhan A, Reed N, Gultekin M, Dursun P, Editors. “Textbook of Gynaecological Oncology”. Ankara, Instanbul, Kosuyolu: Gunes Publishing; 2012. pp 422–428.
   Google Scholar
• Vang R, Gown AM, Zhao C, Barry TS, Isacson C, Richardson MS, Ronnett BM. Ovarian mucinous tumors associated with mature cystic teratomas: morphologic and immunohistochemical analysis identifies a subset of potential teratomatous origin that shares features of lower gastrointestinal tract mucinous tumors more commonly encountered as secondary tumors in the ovary. Am J Surg Pathol 2007;31:854–869.
   PubMed Web of Science ®Google Scholar
• Vaknin Z, Gotlieb WH. Molecular basis of gynecologic cancers. In: Ayhan A, Reed N, Gultekin M, Dursun P, Editors. “Textbook of Gynaecological Oncology”. Ankara, Instanbul, Kosuyolu: Gunes Publishing; 2012. pp 183–190.
   Google Scholar
• Ho CL, Kurman RJ, Dehari R, Wang TL, Shih IeM. Mutations of BRAF and KRAS precede the development of ovarian serous borderline tumors. Cancer Res 2004;64:6915–6918.
   PubMed Web of Science ®Google Scholar
• Guan B, Wang TL, Shih IeM. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res 2011;71:6718–6727.
   PubMed Web of Science ®Google Scholar
• Dehari R, Kurman RJ, Logani S, Shih IeM. The development of high-grade serous carcinoma from atypical proliferative (borderline) serous tumors and low-grade micropapillary serous carcinoma: a morphologic and molecular genetic analysis. Am J Surg Pathol 2007;31:1007–1012.
   PubMed Web of Science ®Google Scholar
• Skytte AB, Waldstrøm M, Rasmussen AA, Crüger D, Woodward ER, Kølvraa S. Identification of BRCA1-deficient ovarian cancers. Acta Obstet Gynecol Scand 2011;90:593–599.
   Google Scholar
• Janku F, Tsimberidou AM, Garrido-Laguna I, Wang X, Luthra R, Hong DS, Naing A, Falchook GS, Moroney JW, Piha-Paul SA, Wheler JJ, Moulder SL, Fu S, Kurzrock R. PIK3CA mutations in patients with advanced cancers treated with PI3K/AKT/mTOR axis inhibitors. Mol Cancer Ther 2011;10:558–565.
   PubMed Web of Science ®Google Scholar
• Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 2006;7:517–528.
   PubMed Web of Science ®Google Scholar
• Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005;434:913–917.
   PubMed Web of Science ®Google Scholar
• Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917–921.
   PubMed Web of Science ®Google Scholar
• Carden CP, Yap TA, Kaye SB. PARP inhibition: targeting the Achilles’ heel of DNA repair to treat germline and sporadic ovarian cancers. Curr Opin Oncol 2010;22:473–480.
   PubMed Web of Science ®Google Scholar
• Gien LT, Mackay HJ. The emerging role of PARP inhibitors in the treatment of epithelial ovarian cancer. J Oncol 2010;2010:151750.
   PubMedGoogle Scholar
• Ledermann JA. Phase II randomized placebo- controlled study of olaparib (AZD2281) in patients with platinum-sensitive relapsed serous ovarian cancer (PSR SOC). J Clin Oncol 2011;29 (issue 15S): Abstract 5003.
   PubMedGoogle Scholar
• Konstantinopoulos PA, Spentzos D, Karlan BY, Taniguchi T, Fountzilas E, Francoeur N, Levine DA, Cannistra SA. Gene expression profile of BRCAness that correlates with responsiveness to chemotherapy and with outcome in patients with epithelial ovarian cancer. J Clin Oncol 2010;28:3555–3561.
   PubMed Web of Science ®Google Scholar
• Radosa MP, Häfner N, Camara O, Diebolder H, Mothes A, Winzer H, Jansen L, et al. Loss of BRCA1 protein expression as indicator of the BRCAness phenotype is associated with favorable overall survival after complete resection of sporadic ovarian cancer. Int J Gynecol Cancer 2011;21:1399–1406.
   PubMedGoogle Scholar
• Ibragimova I, Cairns P. Assays for hypermethylation of the BRCA1 gene promoter in tumor cells to predict sensitivity to PARP-inhibitor therapy. Methods Mol Biol 2011;780:277–291.
   PubMedGoogle Scholar
• Lièvre A, Bachet JB, Boige V, Cayre A, Le Corre D, Buc E, Ychou M, et al. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J Clin Oncol 2008;26:374–379.
   PubMed Web of Science ®Google Scholar
• van Zandwijk N, Mathy A, Boerrigter L, Ruijter H, Tielen I, de Jong D, Baas P, et al. EGFR and KRAS mutations as criteria for treatment with tyrosine kinase inhibitors: retro- and prospective observations in non-small-cell lung cancer. Ann Oncol 2007;18:99–103.
   PubMed Web of Science ®Google Scholar
• Palayekar MJ, Herzog TJ. The emerging role of epidermal growth factor receptor inhibitors in ovarian cancer. Int J Gynecol Cancer 2008;18:879–890.
   PubMedGoogle Scholar