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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Evaluating the progenitor cells of ovarian cancer: analysis of current animal models

  • King, Shelby M. (Department of Medicinal Chemistry and Pharmacognosy, University of Illinois at Chicago) ;
  • Burdette, Joanna E. (Department of Medicinal Chemistry and Pharmacognosy, University of Illinois at Chicago)
  • Received : 2011.06.08
  • Published : 2011.07.31
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Abstract

Serous ovarian cancer is one of the most lethal gynecological malignancies. Progress on effective diagnostics and therapeutics for this disease are hampered by ambiguity as to the cellular origins of this histotype of ovarian cancer, as well as limited suitable animal models to analyze early stages of disease. In this report, we will review current animal models with respect to the two proposed progenitor cells for serous ovarian cancer, the ovarian surface epithelium and the fallopian tube epithelium.

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References

  1. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J. and Thun, M. J. (2009) Cancer statistics, 2009. CA Cancer. J. Clin. 59, 225-249. https://doi.org/10.3322/caac.20006
  2. Auersperg, N., Maines-Bandiera, S. L. and Dyck, H. G. (1997) Ovarian carcinogenesis and the biology of ovarian surface epithelium. J. Cell. Physiol. 173, 261-265. https://doi.org/10.1002/(SICI)1097-4652(199711)173:2<261::AID-JCP32>3.0.CO;2-G
  3. Bell, D. A. (2005) Origins and molecular pathology of ovarian cancer. Mod. Pathol. 18 (Suppl 2), S19-32. https://doi.org/10.1038/modpathol.3800306
  4. Gilks, C. B. (2010) Molecular abnormalities in ovarian cancer subtypes other than high-grade serous carcinoma. J. Oncol. 2010, 740968.
  5. Shih Ie, M. and Kurman, R. J. (2004) Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol. 164, 1511-1518. https://doi.org/10.1016/S0002-9440(10)63708-X
  6. Auersperg, N., Ota, T. and Mitchell, G. W. (2002) Early events in ovarian epithelial carcinogenesis: progress and problems in experimental approaches. Int. J. Gynecol. Cancer 12, 691-703. https://doi.org/10.1046/j.1525-1438.2002.01152.x
  7. Scully, R. E. (1995) Early de novo ovarian cancer and cancer developing in benign ovarian lesions. Int. J. Gynaecol. Obstet. 49 (Suppl), S9-15. https://doi.org/10.1016/0020-7292(95)02404-Z
  8. Lee, Y., Miron, A., Drapkin, R., Nucci, M. R., Medeiros, F., Saleemuddin, A., Garber, J., Birch, C., Mou, H., Gordon, R. W., Cramer, D. W., McKeon, F. D. and Crum, C. P. (2007) A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J. Pathol. 211, 26-35. https://doi.org/10.1002/path.2091
  9. Auersperg, N., Wong, A. S., Choi, K. C., Kang, S. K. and Leung, P. C. (2001) Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr. Rev. 22, 255-288. https://doi.org/10.1210/er.22.2.255
  10. Burdette, J. E., Kurley, S. J., Kilen, S. M., Mayo, K. E. and Woodruff, T. K. (2006) Gonadotropin-induced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 147, 2338-2345. https://doi.org/10.1210/en.2005-1629
  11. Auersperg, N., Woo, M. M. and Gilks, C. B. (2008) The origin of ovarian carcinomas: a developmental view. Gynecol. Oncol. 110, 452-454. https://doi.org/10.1016/j.ygyno.2008.05.031
  12. Fathalla, M. F. (1971) Incessant ovulation--a factor in ovarian neoplasia? Lancet 2, 163.
  13. Wright, J. W., Pejovic, T., Fanton, J. and Stouffer, R. L. (2008) Induction of proliferation in the primate ovarian surface epithelium in vivo. Hum. Reprod. 23, 129-138.
  14. Parrott, J. A., Doraiswamy, V., Kim, G., Mosher, R. and Skinner, M. K. (2001) Expression and actions of both the follicle stimulating hormone receptor and the luteinizing hormone receptor in normal ovarian surface epithelium and ovarian cancer. Mol. Cell Endocrinol. 172, 213-222. https://doi.org/10.1016/S0303-7207(00)00340-3
  15. Konishi, I., Kuroda, H. and Mandai, M. (1999) Review: gonadotropins and development of ovarian cancer. Oncology 57 (Suppl 2), 45-48. https://doi.org/10.1159/000055274
  16. Edmondson, R. J., Monaghan, J. M. and Davies, B. R. (2006) Gonadotropins mediate DNA synthesis and protection from spontaneous cell death in human ovarian surface epithelium. Int. J. Gynecol. Cancer 16, 171-177. https://doi.org/10.1111/j.1525-1438.2006.00274.x
  17. Chakravarti, S., Collins, W. P., Forecast, J. D., Newton, J. R., Oram, D. H. and Studd, J. W. (1976) Hormonal profiles after the menopause. Br. Med. J. 2, 784-787. https://doi.org/10.1136/bmj.2.6039.784
  18. Espey, L. L. (1994) Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol. Reprod. 50, 233-238. https://doi.org/10.1095/biolreprod50.2.233
  19. Murdoch, W. J. (2008) Ovulatory factor in ovarian carcinogenesis. Adv. Exp. Med. Biol. 622, 119-128. https://doi.org/10.1007/978-0-387-68969-2_10
  20. Murdoch, W. J., Townsend, R. S. and McDonnel, A. C. (2001) Ovulation-induced DNA damage in ovarian surface epithelial cells of ewes: prospective regulatory mechanisms of repair/survival and apoptosis. Biol. Reprod. 65, 1417-1424. https://doi.org/10.1095/biolreprod65.5.1417
  21. Burdette, J. E., Oliver, R. M., Ulyanov, V., Kilen, S. M., Mayo, K. E. and Woodruff, T. K. (2007) Ovarian epithelial inclusion cysts in chronically superovulated CD1 and Smad2 dominant-negative mice. Endocrinology 148, 3595-3604. https://doi.org/10.1210/en.2007-0030
  22. Ghahremani, M., Foghi, A. and Dorrington, J. H. (1999) Etiology of ovarian cancer: a proposed mechanism. Med. Hypotheses 52, 23-26. https://doi.org/10.1054/mehy.1997.0620
  23. Roh, M. H., Kindelberger, D. and Crum, C. P. (2009) Serous tubal intraepithelial carcinoma and the dominant ovarian mass: clues to serous tumor origin? Am. J. Surg. Pathol. 33, 376-383. https://doi.org/10.1097/PAS.0b013e3181868904
  24. Jarboe, E., Folkins, A., Nucci, M. R., Kindelberger, D., Drapkin, R., Miron, A., Lee, Y. and Crum, C. P. (2008) Serous carcinogenesis in the fallopian tube: a descriptive classification. Int. J. Gynecol. Pathol. 27, 1-9. https://doi.org/10.1097/pgp.0b013e31814b191f
  25. Kindelberger, D. W., Lee, Y., Miron, A., Hirsch, M. S., Feltmate, C., Medeiros, F., Callahan, M. J., Garner, E. O., Gordon, R. W., Birch, C., Berkowitz, R. S., Muto, M. G. and Crum, C. P. (2007) Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am. J. Surg. Pathol. 31, 161-169. https://doi.org/10.1097/01.pas.0000213335.40358.47
  26. Sundfeldt, K., Piontkewitz, Y., Ivarsson, K., Nilsson, O., Hellberg, P., Brannstrom, M., Janson, P. O., Enerback, S. and Hedin, L. (1997) E-cadherin expression in human epithelial ovarian cancer and normal ovary. Int. J. Cancer 74, 275-280. https://doi.org/10.1002/(SICI)1097-0215(19970620)74:3<275::AID-IJC7>3.0.CO;2-W
  27. Levanon, K., Ng, V., Piao, H. Y., Zhang, Y., Chang, M. C., Roh, M. H., Kindelberger, D. W., Hirsch, M. S., Crum, C. P., Marto, J. A. and Drapkin, R. (2010) Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29, 1103-1113. https://doi.org/10.1038/onc.2009.402
  28. Kurman, R. J. and Shih Ie, M. (2010) The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am. J. Surg. Pathol. 34, 433-443. https://doi.org/10.1097/PAS.0b013e3181cf3d79
  29. Auersperg, N. (2011) The origin of ovarian carcinomas: a unifying hypothesis. Int. J. Gynecol. Pathol. 30, 12-21. https://doi.org/10.1097/PGP.0b013e3181f45f3e
  30. Crum, C. P., Drapkin, R., Kindelberger, D., Medeiros, F., Miron, A. and Lee, Y. (2007) Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin. Med. Res. 5, 35-44. https://doi.org/10.3121/cmr.2007.702
  31. Press, J. Z., De Luca, A., Boyd, N., Young, S., Troussard, A., Ridge, Y., Kaurah, P., Kalloger, S. E., Blood, K. A., Smith, M., Spellman, P. T., Wang, Y., Miller, D. M., Horsman, D., Faham, M., Gilks, C. B., Gray, J. and Huntsman, D. G. (2008) Ovarian carcinomas with genetic and epigenetic BRCA1 loss have distinct molecular abnormalities. BMC Cancer 8, 17. https://doi.org/10.1186/1471-2407-8-17
  32. Press, J. Z., Wurz, K., Norquist, B. M., Lee, M. K., Pennil, C., Garcia, R., Welcsh, P., Goff, B. A. and Swisher, E. M. (2010) Identification of a preneoplastic gene expression profile in tubal epithelium of BRCA1 mutation carriers. Neoplasia 12, 993-1002. https://doi.org/10.1593/neo.101044
  33. Cass, I., Holschneider, C., Datta, N., Barbuto, D., Walts, A. E. and Karlan, B. Y. (2005) BRCA-mutation-associated fallopian tube carcinoma: a distinct clinical phenotype? Obstet. Gynecol. 106, 1327-1334. https://doi.org/10.1097/01.AOG.0000187892.78392.3f
  34. Xian, W., Miron, A., Roh, M., Semmel, D. R., Yassin, Y., Garber, J., Oliva, E., Goodman, A., Mehra, K., Berkowitz, R. S., Crum, C. P. and Quade, B. J. (2010) The Li-Fraumeni syndrome (LFS): a model for the initiation of p53 signatures in the distal Fallopian tube. J. Pathol. 220, 17-23. https://doi.org/10.1002/path.2624
  35. Alexander, B. M., Van Kirk, E. A., Naughton, L. M. and Murdoch, W. J. (2007) Ovarian morphometrics in TP53-deficient mice. Anat. Rec. (Hoboken) 290, 59-64. https://doi.org/10.1002/ar.20409
  36. Cooper, T. K. and Gabrielson, K. L. (2007) Spontaneous lesions in the reproductive tract and mammary gland of female non-human primates. Birth Defects Res. B. Dev. Reprod. Toxicol. 80, 149-170. https://doi.org/10.1002/bdrb.20105
  37. Marr-Belvin, A. K., Bailey, C. C., Knight, H. L., Klumpp, S. A., Westmoreland, S. V. and Miller, A. D. (2010) Ovarian pathology in rhesus macaques: a 12-year retrospective. J. Med. Primatol. 39, 170-176. https://doi.org/10.1111/j.1600-0684.2010.00409.x
  38. Moore, C. M., Hubbard, G. B., Leland, M. M., Dunn, B. G. and Best, R. G. (2003) Spontaneous ovarian tumors in twelve baboons: a review of ovarian neoplasms in non-human primates. J. Med. Primatol. 32, 48-56. https://doi.org/10.1034/j.1600-0684.2003.00002.x
  39. Swisher, E. (2003) Ovarian cancer associated with inherited mutations in BRCA1 or BRCA2. Curr. Womens Health Rep. 3, 27-32.
  40. Cline, J. M., Wood, C. E., Vidal, J. D., Tarara, R. P., Buse, E., Weinbauer, G. F., de Rijk, E. P. and van Esch, E. (2008) Selected background findings and interpretation of common lesions in the female reproductive system in macaques. Toxicol. Pathol. 36, 142s-163s. https://doi.org/10.1177/0192623308327117
  41. Rodriguez, G. C., Nagarsheth, N. P., Lee, K. L., Bentley, R. C., Walmer, D. K., Cline, M., Whitaker, R. S., Isner, P., Berchuck, A., Dodge, R. K. and Hughes, C. L. (2002) Progestin-induced apoptosis in the Macaque ovarian epithelium: differential regulation of transforming growth factor-beta. J. Natl. Cancer Inst. 94, 50-60. https://doi.org/10.1093/jnci/94.1.50
  42. Rodriguez, G. C., Walmer, D. K., Cline, M., Krigman, H., Lessey, B. A., Whitaker, R. S., Dodge, R. and Hughes, C. L. (1998) Effect of progestin on the ovarian epithelium of macaques: cancer prevention through apoptosis? J. Soc. Gynecol. Investig. 5, 271-276. https://doi.org/10.1016/S1071-5576(98)00017-3
  43. Lu, K. H., Yates, M. S. and Mok, S. C. (2009) The monkey, the hen, and the mouse: models to advance ovarian cancer chemoprevention. Cancer Prev. Res. (Phila Pa) 2, 773-775. https://doi.org/10.1158/1940-6207.CAPR-09-0156
  44. Barnes, M. N., Berry, W. D., Straughn, J. M., Kirby, T. O., Leath, C. A., Huh, W. K., Grizzle, W. E. and Partridge, E. E. (2002) A pilot study of ovarian cancer chemoprevention using medroxyprogesterone acetate in an avian model of spontaneous ovarian carcinogenesis. Gynecol. Oncol. 87, 57-63. https://doi.org/10.1006/gyno.2002.6806
  45. Fredrickson, T. N. (1987) Ovarian tumors of the hen. Environ. Health Perspect 73, 35-51. https://doi.org/10.1289/ehp.877335
  46. Barua, A., Bitterman, P., Abramowicz, J. S., Dirks, A. L., Bahr, J. M., Hales, D. B., Bradaric, M. J., Edassery, S. L., Rotmensch, J. and Luborsky, J. L. (2009) Histopathology of ovarian tumors in laying hens: a preclinical model of human ovarian cancer. Int. J. Gynecol. Cancer 19, 531-539. https://doi.org/10.1111/IGC.0b013e3181a41613
  47. Hakim, A. A., Barry, C. P., Barnes, H. J., Anderson, K. E., Petitte, J., Whitaker, R., Lancaster, J. M., Wenham, R. M., Carver, D. K., Turbov, J., Berchuck, A., Kopelovich, L. and Rodriguez, G. C. (2009) Ovarian adenocarcinomas in the laying hen and women share similar alterations in p53, ras, and HER-2/neu. Cancer Prev. Res. (Phila) 2, 114-121. https://doi.org/10.1158/1940-6207.CAPR-08-0065
  48. Nofech-Mozes, S., Khalifa, M. A., Ismiil, N., Saad, R. S., Hanna, W. M., Covens, A. and Ghorab, Z. (2008) Immunophenotyping of serous carcinoma of the female genital tract. Mod. Pathol. 21, 1147-1155. https://doi.org/10.1038/modpathol.2008.108
  49. Nowee, M. E., Dorsman, J. C., Piek, J. M., Kosma, V. M., Hamalainen, K., Verheijen, R. H. and van Diest, P. J. (2007) HER-2/neu and p27Kip1 in progression of Fallopian tube carcinoma: an immunohistochemical and array comparative genomic hybridization study. Histopathology 51, 666-673. https://doi.org/10.1111/j.1365-2559.2007.02850.x
  50. Trevino, L. S., Giles, J. R., Wang, W., Urick, M. E. and Johnson, P. A. (2010) Gene Expression Profiling Reveals Differentially Expressed Genes in Ovarian Cancer of the Hen: Support for Oviductal Origin? Hormones and Cancer 1, 177-186. https://doi.org/10.1007/s12672-010-0024-8
  51. Greenacre, C. B. (2004) Spontaneous tumors of small mammals. Vet. Clin. North. Am. Exot. Anim. Pract. 7, 627- 651, vi. https://doi.org/10.1016/j.cvex.2004.04.009
  52. Gregson, R. L., Lewis, D. J. and Abbott, D. P. (1984) Spontaneous ovarian neoplasms of the laboratory rat. Vet. Pathol. 21, 292-299. https://doi.org/10.1177/030098588402100305
  53. Sharrow, A. C., Ronnett, B. M., Thoburn, C. J., Barber, J. P., Giuntoli, R. L., 2nd, Armstrong, D. K., Jones, R. J. and Hess, A. D. (2010) Identification and characterization of a spontaneous ovarian carcinoma in Lewis rats. J. Ovarian Res. 3, 9. https://doi.org/10.1186/1757-2215-3-9
  54. Komatsu, M. and Fujita, H. (1978) Electron-microscopic studies on the development and aging of the oviduct epithelium of mice. Anat. Embryol. (Berl) 152, 243-259. https://doi.org/10.1007/BF00350523
  55. Critoph, F. N. and Dennis, K. J. (1977) The cellular composition of the human oviduct epithelium. Br. J. Obstet. Gynaecol. 84, 219-221. https://doi.org/10.1111/j.1471-0528.1977.tb12559.x
  56. Baird, D. T., Baker, T. G., McNatty, K. P. and Neal, P. (1975) Relationship between the secretion of the corpus luteum and the length of the follicular phase of the ovarian cycle. J. Reprod. Fertil. 45, 611-619. https://doi.org/10.1530/jrf.0.0450611
  57. Maronpot, R. R. (1987) Ovarian toxicity and carcinogenicity in eight recent National Toxicology Program studies. Environ. Health Perspect 73, 125-130. https://doi.org/10.1289/ehp.8773125
  58. Bai, W., Oliveros-Saunders, B., Wang, Q., Acevedo- Duncan, M. E. and Nicosia, S. V. (2000) Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev. Biol. Anim. 36, 657-666. https://doi.org/10.1290/1071-2690(2000)036<0657:ESOOSE>2.0.CO;2
  59. Umezu, T., Hanazono, M., Aizawa, S. and Tomooka, Y. (2003) Characterization of newly established clonal oviductal cell lines and differential hormonal regulation of gene expression. In Vitro Cell Dev. Biol. Anim. 39, 146-156.
  60. Ziecik, A. J., Kaczmarek, M. M., Blitek, A., Kowalczyk, A. E., Li, X. and Rahman, N. A. (2007) Novel biological and possible applicable roles of LH/hCG receptor. Mol. Cell. Endocrinol. 269, 51-60. https://doi.org/10.1016/j.mce.2006.08.016
  61. Tunca, J. C., Erturk, E. and Bryan, G. T. (1985) Chemical induction of ovarian tumors in rats. Gynecol. Oncol. 21, 54-64. https://doi.org/10.1016/0090-8258(85)90232-X
  62. Stewart, S. L., Querec, T. D., Ochman, A. R., Gruver, B. N., Bao, R., Babb, J. S., Wong, T. S., Koutroukides, T., Pinnola, A. D., Klein-Szanto, A., Hamilton, T. C. and Patriotis, C. (2004) Characterization of a carcinogenesis rat model of ovarian preneoplasia and neoplasia. Cancer Res. 64, 8177-8183. https://doi.org/10.1158/0008-5472.CAN-04-1702
  63. Crist, K. A., Zhang, Z., You, M., Gunning, W. T., Conran, P. B., Steele, V. E. and Lubet, R. A. (2005) Characterization of rat ovarian adenocarcinomas developed in response to direct instillation of 7,12-dimethylbenz[a]anthracene (DMBA) coated suture. Carcinogenesis 26, 951-957. https://doi.org/10.1093/carcin/bgi039
  64. Wang, Y., Zhang, Z., Lu, Y., Yao, R., Jia, D., Wen, W., LaRegina, M., Crist, K., Lubet, R. and You, M. (2008) Enhanced susceptibility to chemical induction of ovarian tumors in mice with a germ line p53 mutation. Mol. Cancer Res. 6, 99-109. https://doi.org/10.1158/1541-7786.MCR-07-0216
  65. Jarboe, E. A., Pizer, E. S., Miron, A., Monte, N., Mutter, G. L. and Crum, C. P. (2009) Evidence for a latent precursor (p53 signature) that may precede serous endometrial intraepithelial carcinoma. Mod. Pathol. 22, 345-350. https://doi.org/10.1038/modpathol.2008.197
  66. Corney, D. C., Flesken-Nikitin, A., Choi, J. and Nikitin, A. Y. (2008) Role of p53 and Rb in ovarian cancer. Adv. Exp. Med. Biol. 622, 99-117. https://doi.org/10.1007/978-0-387-68969-2_9
  67. Gowen, L. C., Johnson, B. L., Latour, A. M., Sulik, K. K. and Koller, B. H. (1996) Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat. Genet. 12, 191-194. https://doi.org/10.1038/ng0296-191
  68. Garson, K., Shaw, T. J., Clark, K. V., Yao, D. S. and Vanderhyden, B. C. (2005) Models of ovarian cancer--are we there yet? Mol. Cell Endocrinol. 239, 15-26. https://doi.org/10.1016/j.mce.2005.03.019
  69. Boyd, J. (2005) Mouse models of gynecologic pathology. N. Engl. J. Med. 352, 2240-2242. https://doi.org/10.1056/NEJMcibr051024
  70. Buller, R. E., Lallas, T. A., Shahin, M. S., Sood, A. K., Hatterman-Zogg, M., Anderson, B., Sorosky, J. I. and Kirby, P. A. (2001) The p53 mutational spectrum associated with BRCA1 mutant ovarian cancer. Clin Cancer Res. 7, 831-838.
  71. Clark-Knowles, K. V., Senterman, M. K., Collins, O. and Vanderhyden, B. C. (2009) Conditional inactivation of Brca1, p53 and Rb in mouse ovaries results in the development of leiomyosarcomas. PLoS One 4, e8534. https://doi.org/10.1371/journal.pone.0008534
  72. Clark-Knowles, K. V., Garson, K., Jonkers, J. and Vanderhyden, B. C. (2007) Conditional inactivation of Brca1 in the mouse ovarian surface epithelium results in an increase in preneoplastic changes. Exp. Cell Res. 313, 133-145. https://doi.org/10.1016/j.yexcr.2006.09.026
  73. Quinn, B. A., Brake, T., Hua, X., Baxter-Jones, K., Litwin, S., Ellenson, L. H. and Connolly, D. C. (2009) Induction of ovarian leiomyosarcomas in mice by conditional inactivation of Brca1 and p53. PLoS One 4, e8404. https://doi.org/10.1371/journal.pone.0008404
  74. Flesken-Nikitin, A., Choi, K. C., Eng, J. P., Shmidt, E. N. and Nikitin, A. Y. (2003) Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res. 63, 3459-3463.
  75. Laviolette, L. A., Garson, K., Macdonald, E. A., Senterman, M. K., Courville, K., Crane, C. A. and Vanderhyden, B. C. (2010) 17beta-estradiol accelerates tumor onset and decreases survival in a transgenic mouse model of ovarian cancer. Endocrinology 151, 929-938. https://doi.org/10.1210/en.2009-0602
  76. Tanyi, J. L., Lapushin, R., Eder, A., Auersperg, N., Tabassam, F. H., Roth, J. A., Gu, J., Fang, B., Mills, G. B. and Wolf, J. (2002) Identification of tissue- and cancer-selective promoters for the introduction of genes into human ovarian cancer cells. Gynecol. Oncol. 85, 451-458. https://doi.org/10.1006/gyno.2002.6644
  77. Zhang, Y., Huang, G., Shornick, L. P., Roswit, W. T., Shipley, J. M., Brody, S. L. and Holtzman, M. J. (2007) A transgenic FOXJ1-Cre system for gene inactivation in ciliated epithelial cells. Am. J. Respir. Cell Mol. Biol. 36, 515-519. https://doi.org/10.1165/rcmb.2006-0475RC
  78. Miyoshi, I., Takahashi, K., Kon, Y., Okamura, T., Mototani, Y., Araki, Y. and Kasai, N. (2002) Mouse transgenic for murine oviduct-specific glycoprotein promoter-driven Simian Virus 40 large T-antigen: tumor formation and its hormonal regulation. Mol. Reprod. Dev. 63, 168-176. https://doi.org/10.1002/mrd.10175
  79. Connolly, D. C., Bao, R., Nikitin, A. Y., Stephens, K. C., Poole, T. W., Hua, X., Harris, S. S., Vanderhyden, B. C. and Hamilton, T. C. (2003) Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 63, 1389-1397.
  80. Quinn, B. A., Xiao, F., Bickel, L., Martin, L., Hua, X., Klein-Szanto, A. and Connolly, D. C. (2010) Development of a syngeneic mouse model of epithelial ovarian cancer. J. Ovarian Res. 3, 24. https://doi.org/10.1186/1757-2215-3-24
  81. Karst, A. M., Levanon, K. and Drapkin, R. (2011) Modeling high-grade serous ovarian carcinogenesis from the fallopian tube. Proc. Natl. Acad. Sci. U.S.A. 108, 7547- 7552. https://doi.org/10.1073/pnas.1017300108
  82. Chodankar, R., Kwang, S., Sangiorgi, F., Hong, H., Yen, H. Y., Deng, C., Pike, M. C., Shuler, C. F., Maxson, R. and Dubeau, L. (2005) Cell-nonautonomous induction of ovarian and uterine serous cystadenomas in mice lacking a functional Brca1 in ovarian granulosa cells. Curr. Biol. 15, 561-565. https://doi.org/10.1016/j.cub.2005.01.052
  83. Zheng, W., Magid, M. S., Kramer, E. E. and Chen, Y. T. (1996) Follicle-stimulating hormone receptor is expressed in human ovarian surface epithelium and fallopian tube. Am. J. Pathol. 148, 47-53.
  84. Mishina, Y., Whitworth, D. J., Racine, C. and Behringer, R. R. (1999) High specificity of Mullerian-inhibiting substance signaling in vivo. Endocrinology 140, 2084-2088. https://doi.org/10.1210/en.140.5.2084
  85. Bristol-Gould, S. K., Hutten, C. G., Sturgis, C., Kilen, S. M., Mayo, K. E. and Woodruff, T. K. (2005) The development of a mouse model of ovarian endosalpingiosis. Endocrinology 146, 5228-5236. https://doi.org/10.1210/en.2005-0697
  86. Liang, S., Yang, N., Pan, Y., Deng, S., Lin, X., Yang, X., Katsaros, D., Roby, K. F., Hamilton, T. C., Connolly, D. C., Coukos, G. and Zhang, L. (2009) Expression of activated PIK3CA in ovarian surface epithelium results in hyperplasia but not tumor formation. PLoS One 4, e4295. https://doi.org/10.1371/journal.pone.0004295
  87. Mullany, L. K., Fan, H. Y., Liu, Z., White, L. D., Marshall, A., Gunaratne, P., Anderson, M. L., Creighton, C. J., Xin, L., Deavers, M., Wong, K. K. and Richards, J. S. (2011) Molecular and functional characteristics of ovarian surface epithelial cells transformed by KrasG12D and loss of Pten in a mouse model in vivo. Oncogene.
  88. Shayesteh, L., Lu, Y., Kuo, W. L., Baldocchi, R., Godfrey, T., Collins, C., Pinkel, D., Powell, B., Mills, G. B. and Gray, J. W. (1999) PIK3CA is implicated as an oncogene in ovarian cancer. Nat. Genet. 21, 99-102. https://doi.org/10.1038/5042
  89. Dinulescu, D. M., Ince, T. A., Quade, B. J., Shafer, S. A., Crowley, D. and Jacks, T. (2005) Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat. Med. 11, 63-70. https://doi.org/10.1038/nm1173

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