Ovary and fimbrial stem cells: Biology, niche and cancer origins

Nature Reviews Molecular Cell Biology

Volumn 16, Issue 10, 2015, Pages 625-638

  Ng, Annie ^a   Barker, Nick ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; G PROTEIN COUPLED RECEPTOR; LEU RICH REPEAT CONTAINING G PROTEIN COUPLED RECEPTOR 5; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN;

CANCER GROWTH; CELL COMPONENT; CYTOLOGY; EPITHELIUM; FEMALE; FIMBRIAL STEM CELL; GERMLINE STEM CELL; GRANULOSA CELL; GRANULOSA STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; META ANALYSIS (TOPIC); NONHUMAN; OVARIAN CANCER CELL LINE; OVARIAN SURFACE EPITHELIUM; OVARIAN SURFACE EPITHELIUM STEM CELL; OVARY CARCINOMA; OVARY STEM CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL NICHE; THECA CELL; THECA STEM CELL; TISSUE STRUCTURE; ANIMAL; METABOLISM; OVARY; OVARY TUMOR; OVULATION; PATHOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; FEMALE; HUMANS; OVARIAN NEOPLASMS; OVARY; OVULATION; STEM CELL NICHE; STEM CELLS; TUMOR MICROENVIRONMENT;

EID: 84942297491     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm4056     Document Type: Review

References (179)

1. Auersperg, N., Wong, A. S., Choi, K. C., Kang, S. K., & Leung, P. C. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr. Rev. 22, 255-288 (2001
2. Tan, O. L., & Fleming, J. S. Proliferating cell nuclear antigen immunoreactivity in the ovarian surface epithelium of mice of varying ages and total lifetime ovulation number following ovulation. Biol. Reprod. 71, 1501-1507 (2004
3. Wright, J. W., Jurevic, L., & Stouffer, R. L. Dynamics of the primate ovarian surface epithelium during the ovulatory menstrual cycle. Hum. Reprod. 26, 1408-1421 (2011
4. Burdette, J. E., Kurley, S. J., Kilen, S. M., Mayo, K. E., & Woodruff, T. K. Gonadotropin-induced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 147, 2338-2345 (2006
5. Lau, A., et al. Altered expression of inflammation-Associated genes in oviductal cells following follicular fluid exposure: implications for ovarian carcinogenesis. Exp. Biol. Med. 239, 24-32 (2014
6. Bahar-Shany, K., et al. Exposure of fallopian tube epithelium to follicular fluid mimics carcinogenic changes in precursor lesions of serous papillary carcinoma. Gynecol. Oncol. 132, 322-327 (2014
7. Emori, M. M., & Drapkin, R. The hormonal composition of follicular fluid and its implications for ovarian cancer pathogenesis. Reprod. Biol. Endocrinol. 12, 60 (2014
8. Barker, N., et al Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007
9. Barker, N., et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6, 25-36 (2010
10. Van Keymeulen, A., et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 479, 189-193 (2011
11. van Amerongen, R., Bowman, A. N., & Nusse, R. Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 11, 387-400 (2012
12. Ousset, M., et al. Multipotent and unipotent progenitors contribute to prostate postnatal development. Nat. Cell Biol. 14, 1131-1138 (2012
13. DeWard, A. D., Cramer, J., & Lagasse, E. Cellular heterogeneity in the mouse esophagus implicates the presence of a nonquiescent epithelial stem cell population. Cell Rep. 9, 701-711 (2014
14. Doupe, D. P., et al. A single progenitor population switches behavior to maintain and repair esophageal epithelium. Science 337, 1091-1093 (2012
15. Clayton, E., et al. A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189 (2007
16. Jaks, V., et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 40, 1291-1299 (2008
17. Mascre, G., et al. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489, 257-262 (2012
18. Trempus, C. S., et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 120, 501-511 (2003
19. Tumbar, T., et al. Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004
20. Lim, X., et al. Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling. Science 342, 1226-1230 (2013
21. Reya, T., Morrison, S. J., Clarke, M. F., & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001
22. Goodell, M. A., Nguyen, H., & Shroyer, N. Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments. Nat. Rev. Mol. Cell Biol. 16, 299-309 (2015
23. Garson, K., & Vanderhyden, B. C. Epithelial ovarian cancer stem cells: underlying complexity of a simple paradigm. Reproduction 149, R59-R70 (2015
24. Barker, N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol. 15, 19-33 (2014
25. Tata, P. R., et al. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503, 218-223 (2013
26. Mannik, J., Alzayady, K., & Ghazizadeh, S. Regeneration of multilineage skin epithelia by differentiated keratinocytes. J. Invest. Dermatol. 130, 388-397 (2010
27. Ahmed, N., Abubaker, K., & Findlay, J. K. Ovarian cancer stem cells: molecular concepts and relevance as therapeutic targets. Mol. Aspects Med. 39, 110-125 (2014
28. Flesken-Nikitin, A., Odai-Afotey, A. A., & Nikitin, A. Y. Role of the stem cell niche in the pathogenesis of epithelial ovarian cancers. Mol. Cell. Oncol. 1, e963435 (2014
29. Szotek, P. P., et al. Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc. Natl Acad. Sci. USA 105, 12469-12473 (2008
30. Wang, Y., et al. Identification of quiescent, stem-like cells in the distal female reproductive tract. PLoS ONE 7, e40691 (2012
31. Paik, D. Y., et al. Stem-like epithelial cells are concentrated in the distal end of the fallopian tube: a site for injury and serous cancer initiation. Stem Cells 30, 2487-2497 (2012
32. Gamwell, L. F., Collins, O., & Vanderhyden, B. C. The mouse ovarian surface epithelium contains a population of LY6A (SCA 1) expressing progenitor cells that are regulated by ovulation-Associated factors. Biol. Reprod. 87, 80 (2012
33. Patterson, A. L., & Pru, J. K. Long-Term label retaining cells localize to distinct regions within the female reproductive epithelium. Cell Cycle 12, 2888-2898 (2013
34. Ng, A., et al. Lgr5 marks stem/progenitor cells in ovary and tubal epithelia. Nat. Cell Biol. 16, 745-757 (2014
35. Flesken-Nikitin, A., et al. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature 495, 241-245 (2013
36. Auersperg, N. The origin of ovarian cancers-hypotheses and controversies. Front. Biosci. 5, 709-719 (2013
37. Auersperg, N. The origin of ovarian carcinomas: a unifying hypothesis. Int. J. Gynecol. Pathol. 30, 12-21 (2011
38. Dubeau, L., & Drapkin, R. Coming into focus: the nonovarian origins of ovarian cancer. Ann. Oncol. 24 (Suppl. 8), 28-35 (2013
39. Yang-Hartwich, Y., et al. Ovulation and extra-ovarian origin of ovarian cancer. Sci. Rep. 4, 6116 (2014
40. Auersperg, N., Woo, M. M., & Gilks, C. B. The origin of ovarian carcinomas: a developmental view. Gynecol. Oncol. 110, 452-454 (2008
41. Shih, leM., & Kurman, R. J. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol. 164, 1511-1518 (2004
42. Scully, R. E. Early de novo ovarian cancer and cancer developing in benign ovarian lesions. Int. J. Gynaecol. Obstetr. 49, S9-S15 (1995
43. Crum, C. P., et al. The distal fallopian tube: a new model for pelvic serous carcinogenesis. Curr. Opin. Obstetr. Gynecol. 19, 3-9 (2007
44. Piek, J. M., et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J. Pathol. 195, 451-456 (2001
45. Kobayashi, A., & Behringer, R. R. Developmental genetics of the female reproductive tract in mammals. Nat. Rev. Genet. 4, 969-980 (2003
46. Wright, J. W., et al. Ovarian surface epitheliectomy in the non-human primate: continued cyclic ovarian function and limited epithelial replacement. Hum. Reprod. 26, 1422-1430 (2011
47. Kabawat, S. E., et al. Tissue distribution of a coelomic-epithelium-related antigen recognized by the monoclonal antibody OC125. Int. J. Gynecol. Pathol. 2, 275-285 (1983
48. Sherman-Baust, C. A., et al. A genetically engineered ovarian cancer mouse model based on fallopian tube transformation mimics human high-grade serous carcinoma development. J. Pathol. 233, 228-237 (2014
49. King, S. M., et al. The impact of ovulation on fallopian tube epithelial cells: evaluating three hypotheses connecting ovulation and serous ovarian cancer. Endocr. Relat. Cancer 18, 627-642 (2011
50. Zou, K., et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat. Cell Biol. 11, 631-636 (2009
51. Virant-Klun, I., et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 76, 843-856 (2008
52. Pacchiarotti, J., et al. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation 79, 159-170 (2010
53. Virant-Klun, I., et al. Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 18, 137-149 (2009
54. White, Y. A., et al. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-Age women. Nat. Med. 18, 413-421 (2012
55. Johnson, J., Canning, J., Kaneko, T., Pru, J. K., & Tilly, J. L. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145-150 (2004
56. Zhang, H., et al. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc. Natl Acad. Sci. USA 109, 12580-12585 (2012
57. Byskov, A. G., et al. No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum. Reprod. 26, 2129-2139 (2011
58. Kerr, J. B., et al. The primordial follicle reserve is not renewed after chemical or gamma-irradiation mediated depletion. Reproduction 143, 469-476 (2012
59. Lei, L., & Spradling, A. C. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc. Natl Acad. Sci. USA 110, 8585-8590 (2013
60. Lavranos, T. C., Rodgers, H. F., Bertoncello, I., & Rodgers, R. J. Anchorage-independent culture of bovine granulosa cells: the effects of basic fibroblast growth factor and dibutyryl cAMP on cell division and differentiation. Exp. Cell Res. 211, 245-251 (1994
61. Rastetter, R. H., et al. Marker genes identify three somatic cell types in the fetal mouse ovary. Dev. Biol. 394, 242-252 (2014
62. Mork, L., et al. Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice. Biol. Reprod. 86, 37 (2012
63. Honda, A., et al. Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells. Proc. Natl Acad. Sci. USA 104, 12389-12394 (2007
64. Bowen, N. J., et al. Gene expression profiling supports the hypothesis that human ovarian surface epithelia are multipotent and capable of serving as ovarian cancer initiating cells. BMC Med. Genomics 2, 71 (2009
65. Auersperg, N. The stem-cell profile of ovarian surface epithelium is reproduced in the oviductal fimbriae, with increased stem-cell marker density in distal parts of the fimbriae. Int. J. Gynecol. Pathol. 32, 444-453 (2013
66. Moreb, J. S. Aldehyde dehydrogenase as a marker for stem cells. Curr. Stem Cell Res. Ther. 3, 237-246 (2008
67. Barker, N., et al. Very long-Term self-renewal of small intestine, colon, and hair follicles from cycling Lgr5+ve stem cells. Cold Spring Harb. Symp. Quant. Biol. 73, 351-356 (2008
68. de Visser, K. E., et al. Developmental stage-specific contribution of LGR5+ cells to basal and luminal epithelial lineages in the postnatal mammary gland. J. Pathol. 228, 300-309 (2012
69. Barker, N., et al. Lgr5+ve stem/progenitor cells contribute to nephron formation during kidney development. Cell Rep. 2, 540-552 (2012
70. Jameson, S. A., et al. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet. 8, e1002575 (2012
71. Gat, U., DasGupta, R., Degenstein, L., & Fuchs, E. De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell 95, 605-614 (1998
72. Badders, N. M., et al. The Wnt receptor, Lrp5, is expressed by mouse mammary stem cells and is required to maintain the basal lineage. PLoS ONE 4, e6594 (2009
73. Reynolds, A., et al. Canonical Wnt signals combined with suppressed TGFβ/BMP pathways promote renewal of the native human colonic epithelium. Gut 63, 610-621 (2014
74. Korinek, V., et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf 4. Nat. Genet. 19, 379-383 (1998
75. Sato, T., et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011
76. Fafilek, B., et al. Troy, a tumor necrosis factor receptor family member, interacts with Lgr5 to inhibit Wnt signaling in intestinal stem cells. Gastroenterology 144, 381-391 (2013
77. Stange, D. E., et al. Differentiated Troy+ chief cells act as reserve stem cells to generate all lineages of the stomach epithelium. Cell 155, 357-368 (2013
78. Vainio, S., Heikkila, M., Kispert, A., Chin, N., & McMahon, A. P. Female development in mammals is regulated by Wnt 4 signalling. Nature 397, 405-409 (1999
79. Chassot, A. A., et al. Activation of β-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum. Mol. Genet. 17, 1264-1277 (2008
80. Tomizuka, K., et al. R-spondin 1 plays an essential role in ovarian development through positively regulating Wnt 4 signaling. Hum. Mol. Genet. 17, 1278-1291 (2008
81. Hashimoto, T., Schlessinger, D., & Cui, C. Y. Troy binding to lymphotoxin-α activates NF?B mediated transcription. Cell Cycle 7, 106-111 (2008
82. Pispa, J., Pummila, M., Barker, P. A., Thesleff, I., & Mikkola, M. L. Edar and Troy signalling pathways act redundantly to regulate initiation of hair follicle development. Hum. Mol. Genet. 17, 3380-3391 (2008
83. Mohamed, O. A., et al. Uterine Wnt/β-catenin signaling is required for implantation. Proc. Natl Acad. Sci. USA 102, 8579-8584 (2005
84. Kessler, M., et al. Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling. Am. J. Pathol. 180, 186-198 (2012
85. Carroll, T. J., Park, J. S., Hayashi, S., Majumdar, A., & McMahon, A. P. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev. Cell 9, 283-292 (2005
86. Parr, B A., & McMahon, A. P. Sexually dimorphic development of the mammalian reproductive tract requires Wnt 7a. Nature 395, 707-710 (1998
87. Hsu, Y. C., & Fuchs, E. A family business: stem cell progeny join the niche to regulate homeostasis. Nat. Rev. Mol. Cell Biol. 13, 103-114 (2012
88. Clevers, H., Loh, K. M., & Nusse, R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 1248012 (2014
89. Sato, T., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009
90. Gregorieff, A., et al. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 129, 626-638 (2005
91. Farin, H. F., Van Es, J. H., & Clevers, H. Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143, 1518-1529.e7 (2012
92. He, X. C., et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-β-catenin signaling. Nat. Genet. 36, 1117-1121 (2004
93. Haramis, A. P., et al. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303, 1684-1686 (2004
94. Liu, Y., Lyle, S., Yang, Z., & Cotsarelis, G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Invest. Dermatol. 121, 963-968 (2003
95. Watt, F. M. Mammalian skin cell biology: at the interface between laboratory and clinic. Science 346, 937-940 (2014
96. Hsu, Y. C., Li, L., & Fuchs, E. Emerging interactions between skin stem cells and their niches. Nat. Med. 20, 847-856 (2014
97. Boyer, A., Goff, A. K., & Boerboom, D. WNT signaling in ovarian follicle biology and tumorigenesis. Trends Endocrinol. Metab. 21, 25-32 (2010
98. Hsieh, M., Johnson, M. A., Greenberg, N. M., & Richards, J. S. Regulated expression of Wnts and Frizzleds at specific stages of follicular development in the rodent ovary. Endocrinology 143, 898-908 (2002
99. Ricken, A., Lochhead, P., Kontogiannea, M., & Farookhi, R. Wnt signaling in the ovary: identification and compartmentalized expression of wnt 2, wnt 2b, and Frizzled 4 mRNAs. Endocrinology 143, 2741-2749 (2002
100. Hsieh, M., Mulders, S. M., Friis, R. R., Dharmarajan, A., & Richards, J. S. Expression and localization of secreted Frizzled-related protein 4 in the rodent ovary: evidence for selective up regulation in luteinized granulosa cells. Endocrinology 144, 4597-4606 (2003
101. Usongo, M., & Farookhi, R. β-catenin/Tcf-signaling appears to establish the murine ovarian surface epithelium (OSE) and remains active in selected postnatal OSE cells. BMC Dev. Biol. 12, 17 (2012
102. Monkley, S. J., Delaney, S. J., Pennisi, D. J., Christiansen, J. H., & Wainwright, B. J. Targeted disruption of the Wnt2 gene results in placentation defects. Development 122, 3343-3353 (1996
103. Sakaki-Yumoto, M., Katsuno, Y., & Derynck, R. TGF-β family signaling in stem cells. Biochim. Biophys. Acta 1830, 2280-2296 (2013
104. Mani, S. A., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008
105. Ahmed, N., et al. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am. J. Physiol. Cell Physiol. 290, C1532-C1542 (2006
106. Zhu, Y., Nilsson, M., & Sundfeldt, K. Phenotypic plasticity of the ovarian surface epithelium: TGF β1 induction of epithelial to mesenchymal transition (EMT) in vitro. Endocrinology 151, 5497-5505 (2010
107. Shepherd, T. G., & Nachtigal, M. W. Identification of a putative autocrine bone morphogenetic protein-signaling pathway in human ovarian surface epithelium and ovarian cancer cells. Endocrinology 144, 3306-3314 (2003
108. Nilsson, E., Doraiswamy, V., Parrott, J. A., & Skinner, M. K. Expression and action of transforming growth factor beta (TGFβ1, TGFβ2, TGFβ3) in normal bovine ovarian surface epithelium and implications for human ovarian cancer. Mol. Cell. Endocrinol. 182, 145-155 (2001
109. Henriksen, R., et al. Expression and prognostic significance of TGF-β isotypes, latent TGF-β 1 binding protein, TGF-β type I and type II receptors, and endoglin in normal ovary and ovarian neoplasms. Lab. Invest. 73, 213-220 (1995
110. Shimasaki, S., et al. A functional bone morphogenetic protein system in the ovary. Proc. Natl Acad. Sci. USA 96, 7282-7287 (1999
111. Symonds, D., Tomic, D., Borgeest, C., McGee, E., & Flaws, J. A. Smad 3 regulates proliferation of the mouse ovarian surface epithelium. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 273, 681-686 (2003
112. Erickson, G. F., & Shimasaki, S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol. 1, 9 (2003
113. Maruo, T., et al. Expression of epidermal growth factor and its receptor in the human ovary during follicular growth and regression. Endocrinology 132, 924-931 (1993
114. Doraiswamy, V., Parrott, J. A., & Skinner, M. K. Expression and action of transforming growth factor alpha in normal ovarian surface epithelium and ovarian cancer. Biol. Reprod. 63, 789-796 (2000
115. Jindal, S. K., Snoey, D. M., Lobb, D. K., & Dorrington, J. H. Transforming growth factor α localization and role in surface epithelium of normal human ovaries and in ovarian carcinoma cells. Gynecol. Oncol. 53, 17-23 (1994
116. Parrott, J. A., Mosher, R., Kim, G., & Skinner, M. K. Autocrine interactions of keratinocyte growth factor, hepatocyte growth factor, and kit-ligand in the regulation of normal ovarian surface epithelial cells. Endocrinology 141, 2532-2539 (2000
117. Hess, S., Gulati, R., & Peluso, J. J. Hepatocyte growth factor induces rat ovarian surface epithelial cell mitosis or apoptosis depending on the presence or absence of an extracellular matrix. Endocrinology 140, 2908-2916 (1999
118. Parrott, J. A., Kim, G., Mosher, R., & Skinner, M. K. Expression and action of keratinocyte growth factor (KGF) in normal ovarian surface epithelium and ovarian cancer. Mol. Cell. Endocrinol. 167, 77-87 (2000
119. Karlan, B. Y., Jones, J., Greenwald, M., & Lagasse, L. D. Steroid hormone effects on the proliferation of human ovarian surface epithelium in vitro. Am. J. Obstetr. Gynecol. 173, 97-104 (1995
120. Stewart, S. L., et al. Gonadotropin and steroid hormones stimulate proliferation of the rat ovarian surface epithelium. J. Cell. Physiol. 198, 119-124 (2004
121. Davies, B. R., Finnigan, D. S., Smith, S. K., & Ponder, B. A. Administration of gonadotropins stimulates proliferation of normal mouse ovarian surface epithelium. Gynecol. Endocrinol. 13, 75-81 (1999
122. Donnez, J., Casanas-Roux, F., Caprasse, J., Ferin, J., & Thomas, K. Cyclic changes in ciliation, cell height, and mitotic activity in human tubal epithelium during reproductive life. Fertil. Steril. 43, 554-559 (1985
123. Saddick, S. Y. In vitro regulation of sheep ovarian surface epithelium (OSE) proliferation by local ovarian factors. Saudi J. Biol. Sci. 19, 285-290 (2012
124. Press, M. F., Nousek-Goebl, N. A., Bur, M., & Greene, G. L. Estrogen receptor localization in the female genital tract. Am. J. Pathol. 123, 280-292 (1986
125. Amso, N. N., Crow, J., & Shaw, R. W. Comparative immunohistochemical study of oestrogen and progesterone receptors in the fallopian tube and uterus at different stages of the menstrual cycle and the menopause. Hum. Reprod. 9, 1027-1037 (1994
126. King, S. M., Modi, D. A., Eddie, S. L., & Burdette, J. E. Insulin and insulin-like growth factor signaling increases proliferation and hyperplasia of the ovarian surface epithelium and decreases follicular integrity through upregulation of the PI3 kinase pathway. J. Ovarian Res. 6, 12 (2013
127. King, S. M., Quartuccio, S., Hilliard, T. S., Inoue, K., & Burdette, J. E. Alginate hydrogels for three-dimensional organ culture of ovaries and oviducts. J. Vis. Exp. 20, 2084 (2011
128. Jackson, K. S., Inoue, K., Davis, D. A., Hilliard, T. S., & Burdette, J. E. Three-dimensional ovarian organ culture as a tool to study normal ovarian surface epithelial wound repair. Endocrinology 150, 3921-3926 (2009
129. Lawrenson, K., et al. In vitro three-dimensional modeling of fallopian tube secretory epithelial cells. BMC Cell Biol. 14, 43 (2013
130. Lawrenson, K., et al. In vitro three-dimensional modelling of human ovarian surface epithelial cells. Cell Prolif. 42, 385-393 (2009
131. Jung, P., et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 17, 1225-1227 (2011
132. Sato, T., et al. Long-Term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-1772 (2011
133. Zeng, Y. A., & Nusse, R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-Term expansion in culture. Cell Stem Cell 6, 568-577 (2010
134. Cancer Genome Atlas Research Network et al. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615 (2011
135. Levanon, K., Crum, C., & Drapkin, R. New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J. Clin. Oncol. 26, 5284-5293 (2008
136. Orsulic, S., et al. Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell 1, 53-62 (2002
137. Connolly, D. C., et al. 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 (2003
138. Flesken-Nikitin, A., Choi, K. C., Eng, J. P., Shmidt, E. N., & Nikitin, A. Y. Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res. 63, 3459-3463 (2003
139. Laviolette, L. A., et al. 17β estradiol accelerates tumor onset and decreases survival in a transgenic mouse model of ovarian cancer. Endocrinology 151, 929-938 (2010
140. Mullany, L. K., et al. Molecular and functional characteristics of ovarian surface epithelial cells transformed by KrasG12D and loss of Pten in a mouse model in vivo. Oncogene 30, 3522-3536 (2011
141. Vanderhyden, B. C., Shaw, T. J., & Ethier, J. F. Animal models of ovarian cancer. Reprod. Biol. Endocrinol. 1, 67 (2003
142. Clark-Knowles, K. V., Garson, K., Jonkers, J., & Vanderhyden, B. C. Conditional inactivation of Brca1 in the mouse ovarian surface epithelium results in an increase in preneoplastic changes. Exp. Cell Res. 313, 133-145 (2007
143. Dinulescu, D. M., et al. Role of K ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat. Med. 11, 63-70 (2005
144. Wu, R., et al. Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/β-catenin and PI3K/Pten signaling pathways. Cancer Cell 11, 321-333 (2007
145. Szabova, L., et al. Perturbation of Rb, 53, and Brca1 or Brca2 cooperate in inducing metastatic serous epithelial ovarian cancer. Cancer Res. 72, 4141-4153 (2012
146. Perets, R., et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell 24, 751-765 (2013
147. Kim, J., et al. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc. Natl Acad. Sci. USA 109, 3921-3926 (2012
148. van der Horst, P. H., et al. A mouse model for endometrioid ovarian cancer arising from the distal oviduct. J. Int. Cancer 135, 1028-1037 (2014
149. Barker, N., et al. Crypt stem cells as the cells of origin of intestinal cancer. Nature 457, 608-611 (2009
150. Zhu, L., et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457, 603-607 (2009
151. Sangiorgi, E., & Capecchi, M. R. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40, 915-920 (2008
152. Tan, T. Z., et al. Functional genomics identifies five distinct molecular subtypes with clinical relevance and pathways for growth control in epithelial ovarian cancer. EMBO Mol. Med. 5, 983-998 (2013
153. Asad, M., et al. FZD7 drives in vitro aggressiveness in Stem A subtype of ovarian cancer via regulation of non-canonical Wnt/PCP pathway. Cell Death Dis. 5, e1346 (2014
154. Herfs, M., et al. A discrete population of squamocolumnar junction cells implicated in the pathogenesis of cervical cancer. Proc. Natl Acad. Sci. USA 109, 10516-10521 (2012
155. Wang, X., et al. Residual embryonic cells as precursors of a Barrett's like metaplasia. Cell 145, 1023-1035 (2011
156. Murdoch, W. J., & McDonnel, A. C. Roles of the ovarian surface epithelium in ovulation and carcinogenesis. Reproduction 123, 743-750 (2002
157. Bjersing, L., & Cajander, S. Ovulation and the role of the ovarian surface epithelium. Experientia 31, 605-608 (1975
158. Colgin, D. C., & Murdoch, W. J. Evidence for a role of the ovarian surface epithelium in the ovulatory mechanism of the sheep: secretion of urokinase-Type plasminogen activator. Anim. Reprod. Sci. 47, 197-204 (1997
159. Kruk, P. A., Uitto, V. J., Firth, J. D., Dedhar, S., & Auersperg, N. Reciprocal interactions between human ovarian surface epithelial cells and adjacent extracellular matrix. Exp. Cell Res. 215, 97-108 (1994
160. Gaytan, F., Bellido, C., Gaytan, M., Morales, C., & Sanchez-Criado, J. E. Differential effects of RU486 and indomethacin on follicle rupture during the ovulatory process in the rat. Biol. Reprod. 69, 99-105 (2003
161. Singavarapu, R., Buchinsky, N., Cheon, D. J., & Orsulic, S. Whole ovary immunohistochemistry for monitoring cell proliferation and ovulatory wound repair in the mouse. Reprod. Biol. Endocrinol. 8, 98 (2010
162. Wright, J. W., et al. Ovulation in the absence of the ovarian surface epithelium in the primate. Biol. Reprod. 82, 599-605 (2010
163. Wright, J. W., Pejovic, T., Fanton, J., & Stouffer, R. L. Induction of proliferation in the primate ovarian surface epithelium in vivo. Hum. Reprod. 23, 129-138 (2008
164. Auersperg, N., Maclaren, I. A., & Kruk, P. A. Ovarian surface epithelium: autonomous production of connective tissue-Type extracellular matrix. Biol. Reprod. 44, 717-724 (1991
165. George, S. H., Milea, A., & Shaw, P. A. Proliferation in the normal FTE is a hallmark of the follicular phase, not BRCA mutation status. Clin. Cancer Res. 18, 6199-6207 (2012
166. Crow, J., Amso, N. N., Lewin, J., & Shaw, R. W. Morphology and ultrastructure of fallopian tube epithelium at different stages of the menstrual cycle and menopause. Hum. Reprod. 9, 2224-2233 (1994
167. Beller, U., Haimovitch, R., & Ben-Sasson, S. Periovulatory multifocal mesothelial proliferation: a possible association with malignant transformation. Int. J. Gynecol. Cancer 5, 306-309 (1995
168. Gaytan, M., et al. Cyclic changes of the ovarian surface epithelium in the rat. Reproduction 129, 311-321 (2005
169. Fleming, J. S., McQuillan, H. J., Millier, M. J., Beaugie, C. R., & Livingstone, V. E cadherin expression and bromodeoxyuridine incorporation during development of ovarian inclusion cysts in age-matched breeder and incessantly ovulated CD 1 mice. Reprod. Biol. Endocrinol. 5, 14 (2007
170. Fathalla, M. F. Incessant ovulation-A factor in ovarian neoplasia? Lancet 2, 163 (1971
171. Auersperg, N. Ovarian surface epithelium as a source of ovarian cancers: unwarranted speculation or evidence-based hypothesis? Gynecol. Oncol. 130, 246-251 (2013
172. Cheng, W., Liu, J., Yoshida, H., Rosen, D., & Naora, H. Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract. Nat. Med. 11, 531-537 (2005
173. Kindelberger, D. W., et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am. J. Surg. Pathol. 31, 161-169 (2007
174. Medeiros, F., et al. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am. J. Surg. Pathol. 30, 230-236 (2006
175. Seidman, J. D., Zhao, P., & Yemelyanova, A. Primary peritoneal high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecol. Oncol. 120, 470-473 (2011
176. Mehrad, M., Ning, G., Chen, E. Y., Mehra, K. K., & Crum, C. P. A pathologist's road map to benign, precancerous, and malignant intraepithelial proliferations in the fallopian tube. Adv. Anatom. Pathol. 17, 293-302 (2010
177. Kuhn, E., et al. TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma-evidence supporting the clonal relationship of the two lesions. J. Pathol. 226, 421-426 (2012
178. Levanon, K., et al. Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29, 1103-1113 (2010
179. Przybycin, C. G., Kurman, R. J., Ronnett, B. M., Shih, I. M., & Vang, R. Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am. J. Surg. Pathol. 34, 1407-1416 (2010