Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2003

Open Access 01-12-2003 | Review

Animal models of ovarian cancer

Authors: Barbara C Vanderhyden, Tanya J Shaw, Jean-François Ethier

Published in: Reproductive Biology and Endocrinology | Issue 1/2003

Login to get access

Abstract

Ovarian cancer is the most lethal of all of the gynecological cancers and can arise from any cell type of the ovary, including germ cells, granulosa or stromal cells. However, the majority of ovarian cancers arise from the surface epithelium, a single layer of cells that covers the surface of the ovary. The lack of a reliable and specific method for the early detection of epithelial ovarian cancer results in diagnosis occurring most commonly at late clinical stages, when treatment is less effective. In part, the deficiency in diagnostic tools is due to the lack of markers for the detection of preneoplastic or early neoplastic changes in the epithelial cells, which reflects our rather poor understanding of this process. Animal models which accurately represent the cellular and molecular changes associated with the initiation and progression of human ovarian cancer have significant potential to facilitate the development of better methods for the early detection and treatment of ovarian cancer. This review describes some of the experimental animal models of ovarian tumorigenesis that have been reported, including those involving specific reproductive factors and environmental toxins. Consideration has also been given to the recent progress in modeling ovarian cancer using genetically engineered mice.
Appendix
Available only for authorised users
Literature
2.
go back to reference Tillmann T, Kamino K, Mohr U: Incidence and spectrum of spontaneous neoplasms in male and female CBA/J mice. Exp Toxicol Pathol. 2000, 52: 221-225.PubMed Tillmann T, Kamino K, Mohr U: Incidence and spectrum of spontaneous neoplasms in male and female CBA/J mice. Exp Toxicol Pathol. 2000, 52: 221-225.PubMed
3.
go back to reference Walsh KM, Poteracki J: Spontaneous neoplasms in control Wistar rats. Fundam Appl Toxicol. 1994, 22: 65-72. 10.1006/faat.1994.1009.PubMed Walsh KM, Poteracki J: Spontaneous neoplasms in control Wistar rats. Fundam Appl Toxicol. 1994, 22: 65-72. 10.1006/faat.1994.1009.PubMed
4.
go back to reference Gregson RL, Lewis DJ, Abbott DP: Spontaneous ovarian neoplasms of the laboratory rat. Vet Pathol. 1984, 21: 292-299.PubMed Gregson RL, Lewis DJ, Abbott DP: Spontaneous ovarian neoplasms of the laboratory rat. Vet Pathol. 1984, 21: 292-299.PubMed
5.
go back to reference Liebelt AG, Sass B, Lombard LS: Mouse ovarian tumors – a review including classification and induction of neoplastic lesions and description of several previously unreported types. J Exp Pathol. 1987, 3: 115-145.PubMed Liebelt AG, Sass B, Lombard LS: Mouse ovarian tumors – a review including classification and induction of neoplastic lesions and description of several previously unreported types. J Exp Pathol. 1987, 3: 115-145.PubMed
6.
go back to reference Beamer WG, Hoppe PC, Whitten WK: Spontaneous malignant granulosa cell tumors in ovaries of young SWR mice. Cancer Res. 1985, 45: 5575-5581.PubMed Beamer WG, Hoppe PC, Whitten WK: Spontaneous malignant granulosa cell tumors in ovaries of young SWR mice. Cancer Res. 1985, 45: 5575-5581.PubMed
7.
go back to reference Tennent BJ, Shultz KL, Beamer WG: Genetic susceptibility for C19 androgen induction of ovarian granulosa cell tumorigenesis in SWXJ strains of mice. Cancer Res. 1993, 53: 1059-1063.PubMed Tennent BJ, Shultz KL, Beamer WG: Genetic susceptibility for C19 androgen induction of ovarian granulosa cell tumorigenesis in SWXJ strains of mice. Cancer Res. 1993, 53: 1059-1063.PubMed
8.
go back to reference Eppig JJ, Wigglesworth K, Varnum DS, Nadeau JH: Genetic regulation of traits essential for spontaneous ovarian teratocarcinogenesis in strain LT/Sv mice: aberrant meiotic cell cycle, oocyte activation, and parthenogenetic development. Cancer Res. 1996, 56: 5047-5054.PubMed Eppig JJ, Wigglesworth K, Varnum DS, Nadeau JH: Genetic regulation of traits essential for spontaneous ovarian teratocarcinogenesis in strain LT/Sv mice: aberrant meiotic cell cycle, oocyte activation, and parthenogenetic development. Cancer Res. 1996, 56: 5047-5054.PubMed
9.
go back to reference Colledge WH, Carlton MB, Udy GB, Evans MJ: Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature. 1994, 370: 65-68. 10.1038/370065a0.PubMed Colledge WH, Carlton MB, Udy GB, Evans MJ: Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature. 1994, 370: 65-68. 10.1038/370065a0.PubMed
10.
go back to reference Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N, Ikawa Y et al.: Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature. 1994, 370: 68-71. 10.1038/370068a0.PubMed Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N, Ikawa Y et al.: Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature. 1994, 370: 68-71. 10.1038/370068a0.PubMed
11.
go back to reference St John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow AF, McGrath J, Xu T: Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet. 1999, 21: 182-186. 10.1038/5965.PubMed St John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow AF, McGrath J, Xu T: Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet. 1999, 21: 182-186. 10.1038/5965.PubMed
12.
go back to reference Weiss NS, Homonchuk T, Young JLJ: Incidence of the histologic types of ovarian cancer: the US Third National Cancer Survey, 1969–1971. Gynecol Oncol. 1977, 5: 161-167.PubMed Weiss NS, Homonchuk T, Young JLJ: Incidence of the histologic types of ovarian cancer: the US Third National Cancer Survey, 1969–1971. Gynecol Oncol. 1977, 5: 161-167.PubMed
13.
go back to reference Papadaki L, Beilby JO: The fine structure of the surface epithelium of the human ovary. J Cell Sci. 1971, 8: 445-465.PubMed Papadaki L, Beilby JO: The fine structure of the surface epithelium of the human ovary. J Cell Sci. 1971, 8: 445-465.PubMed
14.
go back to reference Blaustein A, Lee H: Surface cells of the ovary and pelvic peritoneum: a histochemical and ultrastructure comparison. Gynecol Oncol. 1979, 8: 34-43.PubMed Blaustein A, Lee H: Surface cells of the ovary and pelvic peritoneum: a histochemical and ultrastructure comparison. Gynecol Oncol. 1979, 8: 34-43.PubMed
15.
go back to reference Moore KL: The pelvis and perineum. In: Clinically oriented anatomy. Edited by: Satterfield TS, Napora L, Lumpkin K. 1992, Baltimore, Williams & Williams, 281-289. Moore KL: The pelvis and perineum. In: Clinically oriented anatomy. Edited by: Satterfield TS, Napora L, Lumpkin K. 1992, Baltimore, Williams & Williams, 281-289.
16.
go back to reference Benjamin E, Law S, Bobrow LG: Intermediate filaments, cytokeratin and vimentin in ovarian sex cord-stromal tumours with correlative studies in adult and fetal ovaries. J Pathol. 1987, 152: 253-263.PubMed Benjamin E, Law S, Bobrow LG: Intermediate filaments, cytokeratin and vimentin in ovarian sex cord-stromal tumours with correlative studies in adult and fetal ovaries. J Pathol. 1987, 152: 253-263.PubMed
17.
go back to reference Isola J, Kallioniemi OP, Korte JM, Wahlstrom T, Aine R, Helle M, Helin H: Steroid receptors and Ki-67 reactivity in ovarian cancer and in normal ovary: correlation with DNA flow cytometry, biochemical receptor assay, and patient survival. J Pathol. 1990, 162: 295-301.PubMed Isola J, Kallioniemi OP, Korte JM, Wahlstrom T, Aine R, Helle M, Helin H: Steroid receptors and Ki-67 reactivity in ovarian cancer and in normal ovary: correlation with DNA flow cytometry, biochemical receptor assay, and patient survival. J Pathol. 1990, 162: 295-301.PubMed
18.
go back to reference Czernobilsky B, Moll R, Levy R, Franke WW: Co-expression of cytokeratin and vimentin filaments in mesothelial, granulosa and rete ovarii cells of the human ovary. Eur J Cell Biol. 1985, 37: 175-190.PubMed Czernobilsky B, Moll R, Levy R, Franke WW: Co-expression of cytokeratin and vimentin filaments in mesothelial, granulosa and rete ovarii cells of the human ovary. Eur J Cell Biol. 1985, 37: 175-190.PubMed
19.
go back to reference Jindal SK, Ishii E, Letarte M, Vera S, Teerds K, Dorrington JH: Regulation of transforming growth factor-α gene expression in an ovarian surface epithelial cell line derived from a human carcinoma. Biol Reprod. 1995, 52: 1027-1037.PubMed Jindal SK, Ishii E, Letarte M, Vera S, Teerds K, Dorrington JH: Regulation of transforming growth factor-α gene expression in an ovarian surface epithelial cell line derived from a human carcinoma. Biol Reprod. 1995, 52: 1027-1037.PubMed
20.
go back to reference Rodriguez GC, Berchuck A, Whitaker RS, Schlossman D, Clarke-Pearson DL, Bast RCJ: Epidermal growth factor receptor expression in normal ovarian epithelium and ovarian cancer. II. Relationship between receptor expression and response to epidermal growth factor. Am J Obstet Gynecol. 1991, 164: 745-750.PubMed Rodriguez GC, Berchuck A, Whitaker RS, Schlossman D, Clarke-Pearson DL, Bast RCJ: Epidermal growth factor receptor expression in normal ovarian epithelium and ovarian cancer. II. Relationship between receptor expression and response to epidermal growth factor. Am J Obstet Gynecol. 1991, 164: 745-750.PubMed
21.
go back to reference Bjersing L, Cajander S: Ovulation and the mechanism of follicle rupture. V. Ultrastructure of tunica albuginea and theca externa of rabbit graafian follicles prior to induced ovulation. Cell Tissue Res. 1974, 153: 15-30.PubMed Bjersing L, Cajander S: Ovulation and the mechanism of follicle rupture. V. Ultrastructure of tunica albuginea and theca externa of rabbit graafian follicles prior to induced ovulation. Cell Tissue Res. 1974, 153: 15-30.PubMed
22.
go back to reference Ackerman RC, Murdoch WJ: Prostaglandin-induced apoptosis of ovarian surface epithelial cells. Prostaglandins. 1993, 45: 475-485. 10.1016/0090-6980(93)90123-O.PubMed Ackerman RC, Murdoch WJ: Prostaglandin-induced apoptosis of ovarian surface epithelial cells. Prostaglandins. 1993, 45: 475-485. 10.1016/0090-6980(93)90123-O.PubMed
23.
go back to reference Osterholzer HO, Johnson JH, Nicosia SV: An autoradiographic study of rabbit ovarian surface epithelium before and after ovulation. Biol Reprod. 1985, 33: 729-738.PubMed Osterholzer HO, Johnson JH, Nicosia SV: An autoradiographic study of rabbit ovarian surface epithelium before and after ovulation. Biol Reprod. 1985, 33: 729-738.PubMed
24.
go back to reference Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC: Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev. 2001, 22: 255-288. 10.1210/er.22.2.255.PubMed Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC: Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev. 2001, 22: 255-288. 10.1210/er.22.2.255.PubMed
25.
26.
go back to reference Hamilton TC: Ovarian cancer, Part I: Biology. Curr Probl Cancer. 1992, 16: 1-57.PubMed Hamilton TC: Ovarian cancer, Part I: Biology. Curr Probl Cancer. 1992, 16: 1-57.PubMed
27.
go back to reference Salazar H, Godwin AK, Daly MB, Laub PB, Hogan WM, Rosenblum N, Boente MP, Lynch HT, Hamilton TC: Microscopic benign and invasive malignant neoplasms and a cancer-prone phenotype in prophylactic oophorectomies. J Natl Cancer Inst. 1996, 88: 1810-1820.PubMed Salazar H, Godwin AK, Daly MB, Laub PB, Hogan WM, Rosenblum N, Boente MP, Lynch HT, Hamilton TC: Microscopic benign and invasive malignant neoplasms and a cancer-prone phenotype in prophylactic oophorectomies. J Natl Cancer Inst. 1996, 88: 1810-1820.PubMed
28.
go back to reference Deligdisch L, Gil J: Characterization of ovarian dysplasia by interactive morphometry. Cancer. 1989, 63: 748-755.PubMed Deligdisch L, Gil J: Characterization of ovarian dysplasia by interactive morphometry. Cancer. 1989, 63: 748-755.PubMed
29.
go back to reference Scully RE: Early de novo ovarian cancer and cancer developing in benign ovarian lesions. Int J Gynaecol Obstet. 1995, 49 (Suppl): S9-15. 10.1016/0020-7292(95)02404-Z.PubMed Scully RE: Early de novo ovarian cancer and cancer developing in benign ovarian lesions. Int J Gynaecol Obstet. 1995, 49 (Suppl): S9-15. 10.1016/0020-7292(95)02404-Z.PubMed
30.
go back to reference Auersperg N, Siemens CH, Myrdal SE: Human ovarian surface epithelium in primary culture. In Vitro. 1984, 20: 743-755.PubMed Auersperg N, Siemens CH, Myrdal SE: Human ovarian surface epithelium in primary culture. In Vitro. 1984, 20: 743-755.PubMed
31.
go back to reference Adams AT, Auersperg N: Transformation of cultured rat ovarian surface epithelial cells by Kirsten murine sarcoma virus. Cancer Res. 1981, 41: 2063-2072.PubMed Adams AT, Auersperg N: Transformation of cultured rat ovarian surface epithelial cells by Kirsten murine sarcoma virus. Cancer Res. 1981, 41: 2063-2072.PubMed
32.
go back to reference Leung EH, Leung PC, Auersperg N: Differentiation and growth potential of human ovarian surface epithelial cells expressing temperature-sensitive SV40 T antigen. In Vitro Cell Dev Biol Anim. 2001, 37: 515-521. 10.1290/1071-2690(2001)037<0515:DAGPOH>2.0.CO;2.PubMed Leung EH, Leung PC, Auersperg N: Differentiation and growth potential of human ovarian surface epithelial cells expressing temperature-sensitive SV40 T antigen. In Vitro Cell Dev Biol Anim. 2001, 37: 515-521. 10.1290/1071-2690(2001)037<0515:DAGPOH>2.0.CO;2.PubMed
33.
go back to reference Auersperg N, Pan J, Grove BD, Peterson T, Fisher J, Maines-Bandiera S, Somasiri A, Roskelley CD: E-cadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium. Proc Natl Acad Sci USA. 1999, 96: 6249-6254. 10.1073/pnas.96.11.6249.PubMedCentralPubMed Auersperg N, Pan J, Grove BD, Peterson T, Fisher J, Maines-Bandiera S, Somasiri A, Roskelley CD: E-cadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium. Proc Natl Acad Sci USA. 1999, 96: 6249-6254. 10.1073/pnas.96.11.6249.PubMedCentralPubMed
34.
go back to reference Ong A, Maines-Bandiera SL, Roskelley CD, Auersperg N: An ovarian adenocarcinoma line derived from SV40/E-cadherin-transfected normal human ovarian surface epithelium. Int J Cancer. 2000, 85: 430-437. 10.1002/(SICI)1097-0215(20000201)85:3<430::AID-IJC21>3.3.CO;2-H.PubMed Ong A, Maines-Bandiera SL, Roskelley CD, Auersperg N: An ovarian adenocarcinoma line derived from SV40/E-cadherin-transfected normal human ovarian surface epithelium. Int J Cancer. 2000, 85: 430-437. 10.1002/(SICI)1097-0215(20000201)85:3<430::AID-IJC21>3.3.CO;2-H.PubMed
35.
go back to reference Gregoire L, Rabah R, Schmelz EM, Munkarah A, Roberts PC, Lancaster WD: Spontaneous malignant transformation of human ovarian surface epithelial cells in vitro. Clin Cancer Res. 2001, 7: 4280-4287.PubMed Gregoire L, Rabah R, Schmelz EM, Munkarah A, Roberts PC, Lancaster WD: Spontaneous malignant transformation of human ovarian surface epithelial cells in vitro. Clin Cancer Res. 2001, 7: 4280-4287.PubMed
36.
go back to reference Adams AT, Auersperg N: A cell line, ROSE 199, derived from normal rat ovarian surface epithelium. Exp Cell Biol. 1985, 53: 181-188.PubMed Adams AT, Auersperg N: A cell line, ROSE 199, derived from normal rat ovarian surface epithelium. Exp Cell Biol. 1985, 53: 181-188.PubMed
37.
go back to reference Hoffman AG, Burghardt RC, Tilley R, Auersperg N: An in vitro model of ovarian epithelial carcinogenesis: changes in cell-cell communication and adhesion occuring during neoplastic progression. Int J Cancer. 1993, 54: 828-838.PubMed Hoffman AG, Burghardt RC, Tilley R, Auersperg N: An in vitro model of ovarian epithelial carcinogenesis: changes in cell-cell communication and adhesion occuring during neoplastic progression. Int J Cancer. 1993, 54: 828-838.PubMed
38.
go back to reference Godwin AK, Testa JR, Handel LM, Liu Z, Vanderveer LA, Tracey PA, Hamilton TC: Spontaneous transformation of rat ovarian surface epithelial cells: association with cytogenetic changes and implications of repeated ovulation in the etiology of ovarian cancer. J Natl Cancer Inst. 1992, 84: 592-601.PubMed Godwin AK, Testa JR, Handel LM, Liu Z, Vanderveer LA, Tracey PA, Hamilton TC: Spontaneous transformation of rat ovarian surface epithelial cells: association with cytogenetic changes and implications of repeated ovulation in the etiology of ovarian cancer. J Natl Cancer Inst. 1992, 84: 592-601.PubMed
39.
go back to reference Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, Persons DL, Smith PG, Terranova PF: Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis. 2000, 21: 585-591. 10.1093/carcin/21.4.585.PubMed Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, Persons DL, Smith PG, Terranova PF: Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis. 2000, 21: 585-591. 10.1093/carcin/21.4.585.PubMed
40.
go back to reference Orsulic S, Li Y, Soslow RA, Vitale-Cross LA, Gutkind JS, Varmus HE: Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell. 2002, 1: 53-62. 10.1016/S1535-6108(01)00002-2.PubMedCentralPubMed Orsulic S, Li Y, Soslow RA, Vitale-Cross LA, Gutkind JS, Varmus HE: Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell. 2002, 1: 53-62. 10.1016/S1535-6108(01)00002-2.PubMedCentralPubMed
41.
go back to reference Tonin PN, Hudson TJ, Rodier F, Bossolasco M, Lee PD, Novak J, Manderson EN, Provencher D, Mes-Masson AM: Microarray analysis of gene expression mirrors the biology of an ovarian cancer model. Oncogene. 2001, 20: 6617-6626. 10.1038/sj.onc.1204804.PubMed Tonin PN, Hudson TJ, Rodier F, Bossolasco M, Lee PD, Novak J, Manderson EN, Provencher D, Mes-Masson AM: Microarray analysis of gene expression mirrors the biology of an ovarian cancer model. Oncogene. 2001, 20: 6617-6626. 10.1038/sj.onc.1204804.PubMed
42.
go back to reference Roberts D, Williams SJ, Cvetkovic D, Weinstein JK, Godwin AK, Johnson SW, Hamilton TC: Decreased expression of retinol-binding proteins is associated with malignant transformation of the ovarian surface epithelium. DNA Cell Biol. 2002, 21: 11-19. 10.1089/10445490252810276.PubMed Roberts D, Williams SJ, Cvetkovic D, Weinstein JK, Godwin AK, Johnson SW, Hamilton TC: Decreased expression of retinol-binding proteins is associated with malignant transformation of the ovarian surface epithelium. DNA Cell Biol. 2002, 21: 11-19. 10.1089/10445490252810276.PubMed
43.
go back to reference Ward BG, Wallace K: Localization of the monoclonal antibody HMFG2 after intravenous and intraperitoneal injection into nude mice bearing subcutaneous and intraperitoneal human ovarian cancer xenografts. Cancer Res. 1987, 47: 4714-4718.PubMed Ward BG, Wallace K: Localization of the monoclonal antibody HMFG2 after intravenous and intraperitoneal injection into nude mice bearing subcutaneous and intraperitoneal human ovarian cancer xenografts. Cancer Res. 1987, 47: 4714-4718.PubMed
44.
go back to reference Hamilton TC, Young RC, Louie KG, Behrens BC, McKoy WM, Grotzinger KR, Ozols RF: Characterization of a xenograft model of human ovarian carcinoma which produces ascites and intraabdominal carcinomatosis in mice. Cancer Res. 1984, 44: 5286-5290.PubMed Hamilton TC, Young RC, Louie KG, Behrens BC, McKoy WM, Grotzinger KR, Ozols RF: Characterization of a xenograft model of human ovarian carcinoma which produces ascites and intraabdominal carcinomatosis in mice. Cancer Res. 1984, 44: 5286-5290.PubMed
45.
go back to reference Massazza G, Tomasoni A, Lucchini V, Allavena P, Erba E, Colombo N, Mantovani A, D'Incalci M, Mangioni C, Giavazzi R: Intraperitoneal and subcutaneous xenografts of human ovarian carcinoma in nude mice and their potential in experimental therapy. Int J Cancer. 1989, 44: 494-500.PubMed Massazza G, Tomasoni A, Lucchini V, Allavena P, Erba E, Colombo N, Mantovani A, D'Incalci M, Mangioni C, Giavazzi R: Intraperitoneal and subcutaneous xenografts of human ovarian carcinoma in nude mice and their potential in experimental therapy. Int J Cancer. 1989, 44: 494-500.PubMed
46.
go back to reference Fu X, Hoffman RM: Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer Res. 1993, 13: 283-286.PubMed Fu X, Hoffman RM: Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer Res. 1993, 13: 283-286.PubMed
47.
go back to reference Scully RE, Young RH, Clement PB: Tumors of the Ovary, Maldeveloped Gonads, Fallopian Tube, and Broad Ligament. 1996, Washington DC, Armed Forces Institute of Pathology Scully RE, Young RH, Clement PB: Tumors of the Ovary, Maldeveloped Gonads, Fallopian Tube, and Broad Ligament. 1996, Washington DC, Armed Forces Institute of Pathology
48.
go back to reference Fathalla MF: Incessant ovulation – a factor in ovarian neoplasia?. Lancet. 1971, 2: 163-PubMed Fathalla MF: Incessant ovulation – a factor in ovarian neoplasia?. Lancet. 1971, 2: 163-PubMed
49.
go back to reference Whittemore AS, Harris R, Itnyre J: Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies. IV. The pathogenesis of epithelial ovarian cancer Collaborative Ovarian Cancer Group. Am J Epidemiol. 1992, 136: 1212-1220.PubMed Whittemore AS, Harris R, Itnyre J: Characteristics relating to ovarian cancer risk: collaborative analysis of 12 US case-control studies. IV. The pathogenesis of epithelial ovarian cancer Collaborative Ovarian Cancer Group. Am J Epidemiol. 1992, 136: 1212-1220.PubMed
50.
go back to reference La Vecchia C, Franceschi S: Oral contraceptives and ovarian cancer. Eur J Cancer Prev. 1999, 8: 297-304.PubMed La Vecchia C, Franceschi S: Oral contraceptives and ovarian cancer. Eur J Cancer Prev. 1999, 8: 297-304.PubMed
51.
go back to reference Clow OL, Hurst PR, Fleming JS: Changes in the mouse ovarian surface epithelium with age and ovulation number. Mol Cell Endocrinol. 2002, 191: 105-111. 10.1016/S0303-7207(02)00061-8.PubMed Clow OL, Hurst PR, Fleming JS: Changes in the mouse ovarian surface epithelium with age and ovulation number. Mol Cell Endocrinol. 2002, 191: 105-111. 10.1016/S0303-7207(02)00061-8.PubMed
52.
go back to reference Cramer DW, Welch WR: Determinants of ovarian cancer risk. II. Inferences regarding pathogenesis. J Natl Cancer Inst. 1983, 71: 717-721.PubMed Cramer DW, Welch WR: Determinants of ovarian cancer risk. II. Inferences regarding pathogenesis. J Natl Cancer Inst. 1983, 71: 717-721.PubMed
53.
go back to reference Sell A, Bertelsen K, Andersen JE, Stroyer I, Panduro J: Randomized study of whole-abdomen irradiation versus pelvic irradiation plus cyclophosphamide in treatment of early ovarian cancer. Gynecol Oncol. 1990, 37: 367-373.PubMed Sell A, Bertelsen K, Andersen JE, Stroyer I, Panduro J: Randomized study of whole-abdomen irradiation versus pelvic irradiation plus cyclophosphamide in treatment of early ovarian cancer. Gynecol Oncol. 1990, 37: 367-373.PubMed
54.
go back to reference Chakravarti S, Collins WP, Forecast JD, Newton JR, Oram DH, Studd JW: Hormonal profiles after the menopause. Br Med J. 1976, 2: 784-787.PubMedCentralPubMed Chakravarti S, Collins WP, Forecast JD, Newton JR, Oram DH, Studd JW: Hormonal profiles after the menopause. Br Med J. 1976, 2: 784-787.PubMedCentralPubMed
55.
go back to reference Zheng WX, Magid MS, Kramer EE, Chen YT: Follicle-stimulating hormone receptor is expressed in human ovarian surface epithelium and fallopian tube. Am J Pathol. 1996, 148: 47-53.PubMedCentralPubMed Zheng WX, Magid MS, Kramer EE, Chen YT: Follicle-stimulating hormone receptor is expressed in human ovarian surface epithelium and fallopian tube. Am J Pathol. 1996, 148: 47-53.PubMedCentralPubMed
56.
go back to reference Konishi I, Kuroda H, Mandai M: Review: gonadotropins and development of ovarian cancer. Oncology. 1999, 57 (Suppl 2): 45-48. 10.1159/000055274.PubMed Konishi I, Kuroda H, Mandai M: Review: gonadotropins and development of ovarian cancer. Oncology. 1999, 57 (Suppl 2): 45-48. 10.1159/000055274.PubMed
57.
go back to reference Osterholzer HO, Streibel EJ, Nicosia SV: Growth effects of protein hormones on cultured rabbit ovarian surface epithelial cells. Biol Reprod. 1985, 33: 247-258.PubMed Osterholzer HO, Streibel EJ, Nicosia SV: Growth effects of protein hormones on cultured rabbit ovarian surface epithelial cells. Biol Reprod. 1985, 33: 247-258.PubMed
58.
go back to reference Davies BR, Finnigan DS, Smith SK, Ponder BA: Administration of gonadotropins stimulates proliferation of normal mouse ovarian surface epithelium. Gynecol Endocrinol. 1999, 13: 75-81.PubMed Davies BR, Finnigan DS, Smith SK, Ponder BA: Administration of gonadotropins stimulates proliferation of normal mouse ovarian surface epithelium. Gynecol Endocrinol. 1999, 13: 75-81.PubMed
59.
go back to reference Schiffenbauer YS, Abramovitch R, Meir G, Nevo N, Holzinger M, Itin A, Keshet E, Neeman M: Loss of ovarian function promotes angiogenesis in human ovarian carcinoma. Proc Natl Acad Sci U S A. 1997, 94: 13203-13208. 10.1073/pnas.94.24.13203.PubMedCentralPubMed Schiffenbauer YS, Abramovitch R, Meir G, Nevo N, Holzinger M, Itin A, Keshet E, Neeman M: Loss of ovarian function promotes angiogenesis in human ovarian carcinoma. Proc Natl Acad Sci U S A. 1997, 94: 13203-13208. 10.1073/pnas.94.24.13203.PubMedCentralPubMed
60.
go back to reference Biskind MS, Biskind GS: Development of tumors in the rat ovary after transplantation into the spleen. Proc Soc Exp Biol Med. 1944, 55: 176-179. Biskind MS, Biskind GS: Development of tumors in the rat ovary after transplantation into the spleen. Proc Soc Exp Biol Med. 1944, 55: 176-179.
61.
go back to reference Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A: Alpha-inhibin is a tumor-suppressor gene with gonadal specificity in mice. Nature. 1992, 360: 313-319. 10.1038/360313a0.PubMed Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A: Alpha-inhibin is a tumor-suppressor gene with gonadal specificity in mice. Nature. 1992, 360: 313-319. 10.1038/360313a0.PubMed
62.
go back to reference Nilson JH, Abbud RA, Keri RA, Quirk CC: Chronic hypersecretion of luteinizing hormone in transgenic mice disrupts both ovarian and pituitary function, with some effects modified by the genetic background. Recent Prog Horm Res. 2000, 55: 69-89.PubMed Nilson JH, Abbud RA, Keri RA, Quirk CC: Chronic hypersecretion of luteinizing hormone in transgenic mice disrupts both ovarian and pituitary function, with some effects modified by the genetic background. Recent Prog Horm Res. 2000, 55: 69-89.PubMed
63.
go back to reference Keri RA, Lozada KL, Abdul-Karim FW, Nadeau JH, Nilson JH: Luteinizing hormone induction of ovarian tumors: oligogenic differences between mouse strains dictates tumor disposition. Proc Natl Acad Sci USA. 2000, 97: 383-387. 10.1073/pnas.97.1.383.PubMedCentralPubMed Keri RA, Lozada KL, Abdul-Karim FW, Nadeau JH, Nilson JH: Luteinizing hormone induction of ovarian tumors: oligogenic differences between mouse strains dictates tumor disposition. Proc Natl Acad Sci USA. 2000, 97: 383-387. 10.1073/pnas.97.1.383.PubMedCentralPubMed
64.
go back to reference Danilovich N, Roy I, Sairam MR: Ovarian pathology and high incidence of sex cord tumors in follitropin receptor knockout (FORKO) mice. Endocrinology. 2001, 142: 3673-3684. 10.1210/en.142.8.3673.PubMed Danilovich N, Roy I, Sairam MR: Ovarian pathology and high incidence of sex cord tumors in follitropin receptor knockout (FORKO) mice. Endocrinology. 2001, 142: 3673-3684. 10.1210/en.142.8.3673.PubMed
65.
go back to reference Gondos B: Surface epithelium of the developing ovary. Possible correlation with ovarian neoplasia. Am J Pathol. 1975, 81: 303-321.PubMedCentralPubMed Gondos B: Surface epithelium of the developing ovary. Possible correlation with ovarian neoplasia. Am J Pathol. 1975, 81: 303-321.PubMedCentralPubMed
66.
go back to reference Karlan BY, Jones J, Greenwald M, Lagasse LD: Steroid hormone effects on the proliferation of human ovarian surface epithelium in vitro. Am J Obstet Gynecol. 1995, 173: 97-104.PubMed Karlan BY, Jones J, Greenwald M, Lagasse LD: Steroid hormone effects on the proliferation of human ovarian surface epithelium in vitro. Am J Obstet Gynecol. 1995, 173: 97-104.PubMed
67.
go back to reference Lau KM, Mok SC, Ho SM: Expression of human estrogen receptor-alpha and -beta, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. Proc Natl Acad Sci USA. 1999, 96: 5722-5727. 10.1073/pnas.96.10.5722.PubMedCentralPubMed Lau KM, Mok SC, Ho SM: Expression of human estrogen receptor-alpha and -beta, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. Proc Natl Acad Sci USA. 1999, 96: 5722-5727. 10.1073/pnas.96.10.5722.PubMedCentralPubMed
68.
go back to reference Hamilton TC, Davies P, Criffiths K: Steroid hormone receptor status of the normal and neoplastic ovarian surface germinal epithelium. In Factors regulating ovarian function. Edited by: Greenwald GS, Terranova PF. 1983, New York, Raven Press, 81-85. Hamilton TC, Davies P, Criffiths K: Steroid hormone receptor status of the normal and neoplastic ovarian surface germinal epithelium. In Factors regulating ovarian function. Edited by: Greenwald GS, Terranova PF. 1983, New York, Raven Press, 81-85.
69.
go back to reference 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 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
70.
go back to reference Murdoch WJ, Van Kirk EA: Steroid hormonal regulation of proliferative, p53 tumor suppressor, and apoptotic responses of sheep ovarian surface epithelial cells. Mol Cell Endocrinol. 2002, 186: 61-67. 10.1016/S0303-7207(01)00675-X.PubMed Murdoch WJ, Van Kirk EA: Steroid hormonal regulation of proliferative, p53 tumor suppressor, and apoptotic responses of sheep ovarian surface epithelial cells. Mol Cell Endocrinol. 2002, 186: 61-67. 10.1016/S0303-7207(01)00675-X.PubMed
71.
go back to reference Silva EG, Tornos C, Deavers M, Kaisman K, Gray K, Gershenson D: Induction of epithelial neoplasms in the ovaries of guinea pigs by estrogenic stimulation. Gynecol Oncol. 1998, 71: 240-246. 10.1006/gyno.1998.5153.PubMed Silva EG, Tornos C, Deavers M, Kaisman K, Gray K, Gershenson D: Induction of epithelial neoplasms in the ovaries of guinea pigs by estrogenic stimulation. Gynecol Oncol. 1998, 71: 240-246. 10.1006/gyno.1998.5153.PubMed
72.
go back to reference Bai W, Oliveros-Saunders B, Wang Q, Acevedo-Duncan ME, Nicosia SV: Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev Biol Anim. 2000, 36: 657-666. 10.1290/1071-2690(2000)036<0657:ESOOSE>2.0.CO;2.PubMed Bai W, Oliveros-Saunders B, Wang Q, Acevedo-Duncan ME, Nicosia SV: Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev Biol Anim. 2000, 36: 657-666. 10.1290/1071-2690(2000)036<0657:ESOOSE>2.0.CO;2.PubMed
73.
go back to reference Kang SK, Choi KC, Tai CJ, Auersperg N, Leung PC: Estradiol regulates gonadotropin-releasing hormone (GnRH) and its receptor gene expression and antagonizes the growth inhibitory effects of GnRH in human ovarian surface epithelial and ovarian cancer cells. Endocrinology. 2001, 142: 580-588. 10.1210/en.142.2.580.PubMed Kang SK, Choi KC, Tai CJ, Auersperg N, Leung PC: Estradiol regulates gonadotropin-releasing hormone (GnRH) and its receptor gene expression and antagonizes the growth inhibitory effects of GnRH in human ovarian surface epithelial and ovarian cancer cells. Endocrinology. 2001, 142: 580-588. 10.1210/en.142.2.580.PubMed
74.
go back to reference Liu Y, Lin L, Zarnegar R: Modulation of hepatocyte growth factor gene expression by estrogen in mouse ovary. Mol Cell Endocrinol. 1994, 104: 173-181. 10.1016/0303-7207(94)90120-1.PubMed Liu Y, Lin L, Zarnegar R: Modulation of hepatocyte growth factor gene expression by estrogen in mouse ovary. Mol Cell Endocrinol. 1994, 104: 173-181. 10.1016/0303-7207(94)90120-1.PubMed
75.
go back to reference Ilekis JV, Connor JP, Prins GS, Ferrer K, Niederberger C, Scoccia B: Expression of epidermal growth factor and androgen receptors in ovarian cancer. Gynecol Oncol. 1997, 66: 250-254. 10.1006/gyno.1997.4764.PubMed Ilekis JV, Connor JP, Prins GS, Ferrer K, Niederberger C, Scoccia B: Expression of epidermal growth factor and androgen receptors in ovarian cancer. Gynecol Oncol. 1997, 66: 250-254. 10.1006/gyno.1997.4764.PubMed
76.
go back to reference Helzlsouer KJ, Alberg AJ, Gordon GB, Longcope C, Bush TL, Hoffman SC, Comstock GW: Serum gonadotropins and steroid hormones and the development of ovarian cancer. JAMA. 1995, 274: 1926-1930. 10.1001/jama.274.24.1926.PubMed Helzlsouer KJ, Alberg AJ, Gordon GB, Longcope C, Bush TL, Hoffman SC, Comstock GW: Serum gonadotropins and steroid hormones and the development of ovarian cancer. JAMA. 1995, 274: 1926-1930. 10.1001/jama.274.24.1926.PubMed
77.
go back to reference Silva EG, Tornos C, Fritsche HAJ, el-Naggar A, Gray K, Ordonez NG, Luna M, Gershenson D: The induction of benign epithelial neoplasms of the ovaries of guinea pigs by testosterone stimulation: a potential animal model. Mod Pathol. 1997, 10: 879-883.PubMed Silva EG, Tornos C, Fritsche HAJ, el-Naggar A, Gray K, Ordonez NG, Luna M, Gershenson D: The induction of benign epithelial neoplasms of the ovaries of guinea pigs by testosterone stimulation: a potential animal model. Mod Pathol. 1997, 10: 879-883.PubMed
78.
go back to reference Evangelou A, Jindal SK, Brown TJ, Letarte M: Down-regulation of transforming growth factor beta receptors by androgen in ovarian cancer cells. Cancer Res. 2000, 60: 929-935.PubMed Evangelou A, Jindal SK, Brown TJ, Letarte M: Down-regulation of transforming growth factor beta receptors by androgen in ovarian cancer cells. Cancer Res. 2000, 60: 929-935.PubMed
79.
go back to reference Mintz B, Russell ES: Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool. 1957, 134: 207-237.PubMed Mintz B, Russell ES: Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool. 1957, 134: 207-237.PubMed
80.
go back to reference Murphy ED: Hyperplastic and early neoplastic changes in the ovaries of mice after genic deletion of germ cells. J Natl Cancer Inst. 1972, 48: 1283-1295.PubMed Murphy ED: Hyperplastic and early neoplastic changes in the ovaries of mice after genic deletion of germ cells. J Natl Cancer Inst. 1972, 48: 1283-1295.PubMed
81.
go back to reference Murphy ED, Beamer WG: Plasma gonadotropin levels during early stages of ovarian tumorigenesis in mice of the Wx/Wv genotype. Cancer Res. 1973, 33: 721-723.PubMed Murphy ED, Beamer WG: Plasma gonadotropin levels during early stages of ovarian tumorigenesis in mice of the Wx/Wv genotype. Cancer Res. 1973, 33: 721-723.PubMed
82.
go back to reference Ishimura K, Matsuda H, Tatsumi H, Fujita H, Terada N, Kitamura Y: Ultrastructural changes in the ovaries of Sl/Slt mutant mice, showing developmental deficiency of follicles and tubular adenomas. Arch Histol Jpn. 1986, 49: 379-389.PubMed Ishimura K, Matsuda H, Tatsumi H, Fujita H, Terada N, Kitamura Y: Ultrastructural changes in the ovaries of Sl/Slt mutant mice, showing developmental deficiency of follicles and tubular adenomas. Arch Histol Jpn. 1986, 49: 379-389.PubMed
83.
go back to reference Duncan MK, Chada KK: Incidence of tubulostromal adenoma of the ovary in aged germ cell-deficient mice. J Comp Pathol. 1993, 109: 13-19.PubMed Duncan MK, Chada KK: Incidence of tubulostromal adenoma of the ovary in aged germ cell-deficient mice. J Comp Pathol. 1993, 109: 13-19.PubMed
84.
go back to reference Capen CC, Beamer WG, Tennent BJ, Stitzel KA: Mechanisms of hormone-mediated carcinogenesis of the ovary in mice. Mutat Res. 1995, 333: 143-151. 10.1016/0027-5107(95)00140-9.PubMed Capen CC, Beamer WG, Tennent BJ, Stitzel KA: Mechanisms of hormone-mediated carcinogenesis of the ovary in mice. Mutat Res. 1995, 333: 143-151. 10.1016/0027-5107(95)00140-9.PubMed
85.
go back to reference Tennent BJ, Beamer WG: Ovarian tumors not induced by irradiation and gonadotropins in hypogonadal (hpg) mice. Biol Reprod. 1986, 34: 751-760.PubMed Tennent BJ, Beamer WG: Ovarian tumors not induced by irradiation and gonadotropins in hypogonadal (hpg) mice. Biol Reprod. 1986, 34: 751-760.PubMed
86.
go back to reference Blaakaer J, Baeksted M, Micic S, Albrectsen P, Rygaard J, Bock J: Gonadotropin-releasing hormone agonist suppression of ovarian tumorigenesis in mice of the Wx/Wv genotype. Biol Reprod. 1995, 53: 775-779.PubMed Blaakaer J, Baeksted M, Micic S, Albrectsen P, Rygaard J, Bock J: Gonadotropin-releasing hormone agonist suppression of ovarian tumorigenesis in mice of the Wx/Wv genotype. Biol Reprod. 1995, 53: 775-779.PubMed
87.
go back to reference Gertig DM, Hunter DJ, Cramer DW, Colditz GA, Speizer FE, Willett WC, Hankinson SE: Prospective study of talc use and ovarian cancer. J Natl Cancer Inst. 2000, 92: 249-252. 10.1093/jnci/92.3.249.PubMed Gertig DM, Hunter DJ, Cramer DW, Colditz GA, Speizer FE, Willett WC, Hankinson SE: Prospective study of talc use and ovarian cancer. J Natl Cancer Inst. 2000, 92: 249-252. 10.1093/jnci/92.3.249.PubMed
88.
go back to reference Hamilton TC, Fox H, Buckley CH, Henderson WJ, Griffiths K: Effects of talc on the rat ovary. Br J Exp Pathol. 1984, 65: 101-106.PubMedCentralPubMed Hamilton TC, Fox H, Buckley CH, Henderson WJ, Griffiths K: Effects of talc on the rat ovary. Br J Exp Pathol. 1984, 65: 101-106.PubMedCentralPubMed
89.
go back to reference Sims DE, Singh A, Donald A, Jarrell J, Villeneuve DC: Alteration of primate ovary surface epithelium by exposure to hexachlorobenzene: a quantitative study. Histol Histopathol. 1991, 6: 525-529.PubMed Sims DE, Singh A, Donald A, Jarrell J, Villeneuve DC: Alteration of primate ovary surface epithelium by exposure to hexachlorobenzene: a quantitative study. Histol Histopathol. 1991, 6: 525-529.PubMed
90.
go back to reference Borgeest C, Symonds D, Mayer LP, Hoyer PB, Flaws JA: Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicol Sci. 2002, 68: 473-478. 10.1093/toxsci/68.2.473.PubMed Borgeest C, Symonds D, Mayer LP, Hoyer PB, Flaws JA: Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicol Sci. 2002, 68: 473-478. 10.1093/toxsci/68.2.473.PubMed
91.
go back to reference Maronpot RR: Ovarian toxicity and carcinogenicity in eight recent National Toxicology Program studies. Environ Health Perspect. 1987, 73: 125-130.PubMedCentralPubMed Maronpot RR: Ovarian toxicity and carcinogenicity in eight recent National Toxicology Program studies. Environ Health Perspect. 1987, 73: 125-130.PubMedCentralPubMed
92.
go back to reference Collins JJ, Montali RJ, Manus AG: Toxicological evaluation of 4-vinylcyclohexene. II. Induction of ovarian tumors in female B6C3F1 mice by chronic oral administration of 4-vinylcyclohexene. J Toxicol Environ Health. 1987, 21: 507-524.PubMed Collins JJ, Montali RJ, Manus AG: Toxicological evaluation of 4-vinylcyclohexene. II. Induction of ovarian tumors in female B6C3F1 mice by chronic oral administration of 4-vinylcyclohexene. J Toxicol Environ Health. 1987, 21: 507-524.PubMed
93.
go back to reference Stoica G, Koestner A, Capen CC: Testicular (Sertoli's cell)-like tumors of the ovary induced by N-ethyl-N-nitrosourea (ENU) in rats. Vet Pathol. 1985, 22: 483-491.PubMed Stoica G, Koestner A, Capen CC: Testicular (Sertoli's cell)-like tumors of the ovary induced by N-ethyl-N-nitrosourea (ENU) in rats. Vet Pathol. 1985, 22: 483-491.PubMed
94.
go back to reference Vanderhyden BC, Shaw TJ, Garson K, Tonary AM: Ovarian Carcinogenesis. In: The Ovary. Edited by: Leung PCK, Adashi EY. 2003, San Diego, Elsevier Science Vanderhyden BC, Shaw TJ, Garson K, Tonary AM: Ovarian Carcinogenesis. In: The Ovary. Edited by: Leung PCK, Adashi EY. 2003, San Diego, Elsevier Science
95.
go back to reference Flesken-Nikitin A, Choi K-C, Eng JP, Shmidt EN, Nikitin AY: Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res. 2003 Flesken-Nikitin A, Choi K-C, Eng JP, Shmidt EN, Nikitin AY: Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res. 2003
96.
go back to reference Aunoble B, Sanches R, Didier E, Bignon Y-J: Major oncogenes and tumor suppressor genes involved in epithelial ovarian cancer. Int J Oncol. 2000, 16: 567-576.PubMed Aunoble B, Sanches R, Didier E, Bignon Y-J: Major oncogenes and tumor suppressor genes involved in epithelial ovarian cancer. Int J Oncol. 2000, 16: 567-576.PubMed
97.
go back to reference Gras E, Pons C, Machin P, Matias-Guiu X, Prat J: Loss of heterozygosity at the RB-1 locus and pRB immunostaining in epithelial ovarian tumors: a molecular, immunohistochemical, and clinicopathologic study. Int J Gynecol Pathol. 2001, 20: 335-340. 10.1097/00004347-200110000-00004.PubMed Gras E, Pons C, Machin P, Matias-Guiu X, Prat J: Loss of heterozygosity at the RB-1 locus and pRB immunostaining in epithelial ovarian tumors: a molecular, immunohistochemical, and clinicopathologic study. Int J Gynecol Pathol. 2001, 20: 335-340. 10.1097/00004347-200110000-00004.PubMed
98.
go back to reference Kananen K, Markkula M, Rainio E, Su JG, Hsueh AJ, Huhtaniemi IT: Gonadal tumorigenesis in transgenic mice bearing the mouse inhibin alpha-subunit promoter/simian virus T-antigen fusion gene: characterization of ovarian tumors and establishment of gonadotropin-responsive granulosa cell lines. Mol Endocrinol. 1995, 9: 616-627. 10.1210/me.9.5.616.PubMed Kananen K, Markkula M, Rainio E, Su JG, Hsueh AJ, Huhtaniemi IT: Gonadal tumorigenesis in transgenic mice bearing the mouse inhibin alpha-subunit promoter/simian virus T-antigen fusion gene: characterization of ovarian tumors and establishment of gonadotropin-responsive granulosa cell lines. Mol Endocrinol. 1995, 9: 616-627. 10.1210/me.9.5.616.PubMed
99.
go back to reference Dutertre M, Gouedard L, Xavier F, Long WQ, di Clemente N, Picard JY, Rey R: Ovarian granulosa cell tumors express a functional membrane receptor for anti-Mullerian hormone in transgenic mice. Endocrinology. 2001, 142: 4040-4046. 10.1210/en.142.9.4040.PubMed Dutertre M, Gouedard L, Xavier F, Long WQ, di Clemente N, Picard JY, Rey R: Ovarian granulosa cell tumors express a functional membrane receptor for anti-Mullerian hormone in transgenic mice. Endocrinology. 2001, 142: 4040-4046. 10.1210/en.142.9.4040.PubMed
100.
go back to reference Selvakumaran M, Bao R, Crijns AP, Connolly DC, Weinstein JK, Hamilton TC: Ovarian epithelial cell lineage-specific gene expression using the promoter of a retrovirus-like element. Cancer Res. 2001, 61: 1291-1295.PubMed Selvakumaran M, Bao R, Crijns AP, Connolly DC, Weinstein JK, Hamilton TC: Ovarian epithelial cell lineage-specific gene expression using the promoter of a retrovirus-like element. Cancer Res. 2001, 61: 1291-1295.PubMed
101.
go back to reference Garson K, Macdonald E, Dube M, Bao R, Hamilton TC, Vanderhyden BC: Generation of tumors in transgenic mice expressing the SV40 T antigen under the control of ovarian-specific promoter 1. J Soc Gynecol Investig. 2003, 10: 244-250. 10.1016/S1071-5576(03)00073-X.PubMed Garson K, Macdonald E, Dube M, Bao R, Hamilton TC, Vanderhyden BC: Generation of tumors in transgenic mice expressing the SV40 T antigen under the control of ovarian-specific promoter 1. J Soc Gynecol Investig. 2003, 10: 244-250. 10.1016/S1071-5576(03)00073-X.PubMed
102.
go back to reference Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, Harris SS, Vanderhyden BC, Hamilton TC: Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 2003, 63: 1389-1397.PubMed Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, Harris SS, Vanderhyden BC, Hamilton TC: Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 2003, 63: 1389-1397.PubMed
103.
go back to reference di Clemente N, Wilson C, Faure E, Boussin L, Carmillo P, Tizard R, Picard JY, Vigier B, Josso N, Cate R: Cloning, expression, and alternative splicing of the receptor for anti-Mullerian hormone. Mol Endocrinol. 1994, 8: 1006-1020. 10.1210/me.8.8.1006.PubMed di Clemente N, Wilson C, Faure E, Boussin L, Carmillo P, Tizard R, Picard JY, Vigier B, Josso N, Cate R: Cloning, expression, and alternative splicing of the receptor for anti-Mullerian hormone. Mol Endocrinol. 1994, 8: 1006-1020. 10.1210/me.8.8.1006.PubMed
104.
go back to reference Baarends WM, Uilenbroek JT, Kramer P, Hoogerbrugge JW, van Leeuwen EC, Themmen AP, Grootegoed JA: Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology. 1995, 136: 4951-4962. 10.1210/en.136.11.4951.PubMed Baarends WM, Uilenbroek JT, Kramer P, Hoogerbrugge JW, van Leeuwen EC, Themmen AP, Grootegoed JA: Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology. 1995, 136: 4951-4962. 10.1210/en.136.11.4951.PubMed
105.
go back to reference Baarends WM, van Helmond MJ, Post M, van der Schoot PJ, Hoogerbrugge JW, de Winter JP, Uilenbroek JT, Karels B, Wilming LG, Meijers JH et al.: A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the mullerian duct. Development. 1994, 120: 189-197.PubMed Baarends WM, van Helmond MJ, Post M, van der Schoot PJ, Hoogerbrugge JW, de Winter JP, Uilenbroek JT, Karels B, Wilming LG, Meijers JH et al.: A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the mullerian duct. Development. 1994, 120: 189-197.PubMed
106.
go back to reference Teixeira J, He WW, Shah PC, Morikawa N, Lee MM, Catlin EA, Hudson PL, Wing J, Maclaughlin DT, Donahoe PK: Developmental expression of a candidate mullerian inhibiting substance type II receptor. Endocrinology. 1996, 137: 160-165. 10.1210/en.137.1.160.PubMed Teixeira J, He WW, Shah PC, Morikawa N, Lee MM, Catlin EA, Hudson PL, Wing J, Maclaughlin DT, Donahoe PK: Developmental expression of a candidate mullerian inhibiting substance type II receptor. Endocrinology. 1996, 137: 160-165. 10.1210/en.137.1.160.PubMed
107.
go back to reference Masiakos PT, MacLaughlin DT, Maheswaran S, Teixeira J, Fuller AF Jr, Shah PC, Kehas DJ, Kenneally MK, Dombkowski DM, Ha TU, Preffer FI, Donahoe PK: Human ovarian cancer, cell lines, and primary ascites cells express the human Mullerian inhibiting substance (MIS) type II receptor, bind, and are responsive to MIS. Clin Cancer Res. 1999, 5: 3488-3499.PubMed Masiakos PT, MacLaughlin DT, Maheswaran S, Teixeira J, Fuller AF Jr, Shah PC, Kehas DJ, Kenneally MK, Dombkowski DM, Ha TU, Preffer FI, Donahoe PK: Human ovarian cancer, cell lines, and primary ascites cells express the human Mullerian inhibiting substance (MIS) type II receptor, bind, and are responsive to MIS. Clin Cancer Res. 1999, 5: 3488-3499.PubMed
Metadata
Title
Animal models of ovarian cancer
Authors
Barbara C Vanderhyden
Tanya J Shaw
Jean-François Ethier
Publication date
01-12-2003
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2003
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-1-67

Other articles of this Issue 1/2003

Reproductive Biology and Endocrinology 1/2003 Go to the issue