Dynamics of the primate ovarian surface epithelium during the ovulatory menstrual cycle

Human Reproduction

Volumn 26, Issue 6, 2011, Pages 1408-1421

  Wright, Jay W ^a,b   Jurevic, Leigh ^a   Stouffer, Richard L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

cadherin; epithelial ovarian cancer; menstrual cycle; non human primate; ovarian surface epithelium

Indexed keywords

DNA; STEROID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DEATH; CELL PROLIFERATION; CELL STRUCTURE; COLUMNAR EPITHELIUM; CONTROLLED STUDY; DNA REPAIR; EPITHELIUM; FEMALE; HISTOLOGY; MACACA; MENSTRUAL CYCLE; NONHUMAN; OVARIAN SURFACE EPITHELIUM; OVARY; OVARY CELL; OVARY CYCLE; OVULATION; PROTEIN EXPRESSION; SQUAMOUS CELL;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 79957455973     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der057     Document Type: Article

References (66)

1. Auersperg N, Woo MM, Gilks CB. The origin of ovarian carcinomas: A developmental view. Gynecol Oncol 2008;110:452-454.
2. 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. (Pubitemid 32164666)
3. Bellino FL, Wise PM. Nonhuman primate models of menopause workshop. Biol Reprod 2003;68:10-18. (Pubitemid 36076312)
4. Bogan RL, Murphy MJ, Stouffer RL, Hennebold JD. Systematic determination of differential gene expression in the primate corpus luteum during the luteal phase of the menstrual cycle. Mol Endocrinol 2008;22:1260-1273. (Pubitemid 351629624)
5. Bowen NJ, Walker LD, Matyunina LV, Logani S, Totten KA, Benigno BB, McDonald JF. 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 2009;2:71.
6. Burdette JE, Kurley SJ, Kilen SM, Mayo KE, Woodruff TK. Gonadotropin-induced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 2006;147:2338-2345.
7. Burdette JE, Oliver RM, Ulyanov V, Kilen SM, Mayo KE, Woodruff TK. Ovarian epithelial inclusion cysts in chronically superovulated CD1 and Smad2 dominant-negative mice. Endocrinology 2007;148: 3595-3604. (Pubitemid 47105830)
8. Chaffin CL, Stouffer RL, Duffy DM. Gonadotropin and steroid regulation of steroid receptor and aryl hydrocarbon receptor messenger ribonucleic acid in macaque granulosa cells during the periovulatory interval. Endocrinology 1999;140:4753-4760. (Pubitemid 30666144)
9. Colgin DC, Murdoch WJ. 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 1997; 47:197-204. (Pubitemid 27362925)
10. 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. (Pubitemid 29273895)
11. Doyle LK, Donadeu FX. Regulation of the proliferative activity of ovarian surface epithelial cells by follicular fluid. Anim Reprod Sci 2009; 114:443-448.
12. Fathalla MF. Incessant ovulation-a factor in ovarian neoplasia?. Lancet 1971;2:163.
13. Fegan KS, Rae MT, Critchley HO, Hillier SG. Anti-inflammatory steroid signalling in the human peritoneum. J Endocrinol 2008;196:369-376. (Pubitemid 351298522)
14. Folkins AK, Saleemuddin A, Garrett LA, Garber JE, Muto MG, Tworoger SS, Crum CP. Epidemiologic correlates of ovarian cortical inclusion cysts (CICs) support a dual precursor pathway to pelvic epithelial cancer. Gynecol Oncol 2009;115:108-111.
15. Fong MY, Kakar SS. Ovarian cancer mouse models: A summary of current models and their limitations. J Ovarian Res 2009;2:12.
16. Fredrickson TN. Ovarian tumors of the hen. Environ Health Perspect 1987; 73:35-51.
17. Garson K, Shaw TJ, Clark KV, Yao DS, Vanderhyden BC. Models of ovarian cancer-are we there yet?. Mol Cell Endocrinol 2005;239:15-26. (Pubitemid 40848725)
18. Gaytan M, Sanchez MA, Morales C, Bellido C, Millan Y, Martin de Las Mulas J, Sanchez-Criado JE, Gaytan F. Cyclic changes of the ovarian surface epithelium in the rat. Reproduction 2005;129:311-321. (Pubitemid 40425641)
19. Giles JR, Olson LM, Johnson PA. Characterization of ovarian surface epithelial cells from the hen: A unique model for ovarian cancer. Exp Biol Med (Maywood) 2006;231:1718-1725. (Pubitemid 44865989)
20. Gillett WR, James C, Jetha N, McComb PF. Removal of the ovarian surface epithelium from the rabbit ovary-a cause of adhesions following a standard injury. Hum Reprod 1994;9:497-500. (Pubitemid 24096406)
21. Gubbay O, Guo W, Rae MT, Niven D, Howie AF, McNeilly AS, Xu L, Hillier SG. Anti-inflammatory and proliferative responses in human and ovine ovarian surface epithelial cells. Reproduction 2004; 128:607-614. (Pubitemid 40124291)
22. Gubbay O, Guo W, Rae MT, Niven D, Langdon SP, Hillier SG. Inflammation-associated gene expression is altered between normal human ovarian surface epithelial cells and cell lines derived from ovarian adenocarcinomas. Br J Cancer 2005;92:1927-1933. (Pubitemid 40826143)
23. Heller DS, Hameed M, Baergen R. Lack of proliferative activity of surface epithelial inclusion cysts of the ovary. Int J Gynecol Cancer 2003; 13:303-307. (Pubitemid 38222578)
24. Heller DS, Murphy P, Westhoff C. Are germinal inclusion cysts markers of ovulation? Gynecol Oncol 2005;96:496-499. (Pubitemid 40127154)
25. Isola J, Korte JM, Tuohimaa P. Immunocytochemical localization of progesterone receptor in the chick ovary. Endocrinology 1987; 121:1034-1040. (Pubitemid 17139156)
26. Ivarsson K, Sundfeldt K, Brannstrom M, Hellberg P, Janson PO. Diverse effects of FSH and LH on proliferation of human ovarian surface epithelial cells. Hum Reprod 2001;16:18-23. (Pubitemid 32058573)
27. Johnson KA. The standard of perfection: Thoughts about the laying hen model of ovarian cancer. Cancer Prev Res (Phila) 2009;2:97-99.
28. Keith Bechtel M, Bonavida B. Inhibitory effects of 17beta-estradiol and progesterone on ovarian carcinoma cell proliferation: A potential role for inducible nitric oxide synthase. Gynecol Oncol 2001; 82:127-138. (Pubitemid 32634965)
29. Lane MA, Black A, Handy AM, Shapses SA, Tilmont EM, Kiefer TL, Ingram DK, Roth GS. Energy restriction does not alter bone mineral metabolism or reproductive cycling and hormones in female rhesus monkeys. J Nutr 2001;131:820-827. (Pubitemid 32199151)
30. Lynch HT, Casey MJ, Snyder CL, Bewtra C, Lynch JF, Butts M, Godwin AK. Hereditary ovarian carcinoma: Heterogeneity, molecular genetics, pathology, and management. Mol Oncol 2009;3:97-137.
31. Marquez RT, Baggerly KA, Patterson AP, Liu J, Broaddus R, Frumovitz M, Atkinson EN, Smith DI, Hartmann L, Fishman D et al. Patterns of gene expression in different histotypes of epithelial ovarian cancer correlate with those in normal fallopian tube, endometrium, and colon. Clin Cancer Res 2005;11:6116-6126. (Pubitemid 41262937)
32. Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 2006;30:230-236. (Pubitemid 43740193)
33. Moore CM, Hubbard GB, Leland MM, Dunn BG, Best RG. Spontaneous ovarian tumors in twelve baboons: A review of ovarian neoplasms in non-human primates. J Med Primatol 2003;32:48-56. (Pubitemid 36621658)
34. Mukherjee K, Syed V, Ho SM. Estrogen-induced loss of progesterone receptor expression in normal and malignant ovarian surface epithelial cells. Oncogene 2005;24:4388-4400. (Pubitemid 40961762)
35. Murdoch WJ. Carcinogenic potential of ovulatory genotoxicity. Biol Reprod 2005;73:586-590. (Pubitemid 41356115)
36. Murdoch WJ, Martinchick JF. Oxidative damage to DNA of ovarian surface epithelial cells affected by ovulation: Carcinogenic implication and chemoprevention. Exp Biol Med (Maywood) 2004;229:546-552. (Pubitemid 38736324)
37. Murdoch WJ, McDonnel AC. Roles of the ovarian surface epithelium in ovulation and carcinogenesis. Reproduction 2002;123:743-750. (Pubitemid 34662050)
38. Murdoch WJ, Townsend RS, McDonnel AC. Ovulation-induced DNA damage in ovarian surface epithelial cells of ewes: Prospective regulatory mechanisms of repair/survival and apoptosis. Biol Reprod 2001;65:1417-1424. (Pubitemid 33031499)
39. NRC. Guide for the Care and Use of Laboratory Animals. Washington DC, USA, 1996.
40. Nichols SM, Bavister BD, Brenner CA, Didier PJ, Harrison RM, Kubisch HM. Ovarian senescence in the rhesus monkey (Macaca mulatta). Hum Reprod 2005;20:79-83.
41. Osterholzer HO, Johnson JH, Nicosia SV. An autoradiographic study of rabbit ovarian surface epithelium before and after ovulation. Biol Reprod 1985;33:729-738. (Pubitemid 15247604)
42. Parrott JA, Doraiswamy V, Kim G, Mosher R, Skinner MK. 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 2001;172:213-222. (Pubitemid 32098413)
43. Pejovic T, Yates JE, Liu HY, Hays LE, Akkari Y, Torimaru Y, Keeble W, Rathbun RK, Rodgers WH, Bale AE et al. Cytogenetic instability in ovarian epithelial cells from women at risk of ovarian cancer. Cancer Res 2006;66:9017-9025. (Pubitemid 44521120)
44. Piek JM, Verheijen RH, Menko FH, Jongsma AP, Weegenaar J, Gille JJ, Pals G, Kenemans P, van Diest PJ. Expression of differentiation and proliferation related proteins in epithelium of prophylactically removed ovaries from women with a hereditary female adnexal cancer predisposition. Histopathology 2003;43:26-32. (Pubitemid 36836584)
45. Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, Bogomolniy F, Olvera N, Lin O, Soslow RA et al. Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS ONE 2010;5:e10358.
46. Rae MT, Hillier SG. Steroid signalling in the ovarian surface epithelium. Trends Endocrinol Metab 2005;16:327-333. (Pubitemid 41213290)
47. Rae MT, Niven D, Critchley HO, Harlow CR, Hillier SG. Antiinflammatory steroid action in human ovarian surface epithelial cells. J Clin Endocrinol Metab 2004;89:4538-4544. (Pubitemid 39244466)
48. Resko JA, Goy RW, Robinson JA, Norman RL. The pubescent rhesus monkey: Some characteristics of the menstrual cycle. Biol Reprod 1982;27:354-361. (Pubitemid 13230810)
49. Rodriguez GC, Nagarsheth NP, Lee KL, Bentley RC, Walmer DK, Cline M, Whitaker RS, Isner P, Berchuck A, Dodge RK et al. Progestin-induced apoptosis in the Macaque ovarian epithelium: Differential regulation of transforming growth factor-beta. J Natl Cancer Inst 2002;94:50-60. (Pubitemid 34082843)
50. Shaw PA, Rouzbahman M, Pizer ES, Pintilie M, Begley H. Candidate serous cancer precursors in fallopian tube epithelium of BRCA1/2 mutation carriers. Mod Pathol 2009;22:1133-1138.
51. Slot KA, de Boer-Brouwer M, Voorendt M, Sie-Go DM, Ghahremani M, Dorrington JH, Teerds KJ. Irregularly shaped inclusion cysts display increased expression of Ki67, Fas, Fas ligand, and procaspase-3 but relatively little active caspase-3. Int J Gynecol Cancer 2006; 16:231-239.
52. Sueblinvong T, Carney ME. Current understanding of risk factors for ovarian cancer. Curr Treat Options Oncol 2009;10:67-81.
53. Syed V, Ulinski G, Mok SC, Yiu GK, Ho SM. Expression of gonadotropin receptor and growth responses to key reproductive hormones in normal and malignant human ovarian surface epithelial cells. Cancer Res 2001;61:6768-6776. (Pubitemid 32896499)
54. Symonds D, Tomic D, Borgeest C, McGee E, Flaws JA. Smad 3 regulates proliferation of the mouse ovarian surface epithelium. Anat Rec A Discov Mol Cell Evol Biol 2003;273:681-686. (Pubitemid 37238389)
55. Tan OL, Fleming JS. Proliferating cell nuclear antigen immunoreactivity in the ovarian surface epithelium of mice of varying ages and total lifetime ovulation number following ovulation. Biol Reprod 2004; 71:1501-1507. (Pubitemid 39403244)
56. Tan OL, Hurst PR, Fleming JS. Location of inclusion cysts in mouse ovaries in relation to age, pregnancy, and total ovulation number: Implications for ovarian cancer? J Pathol 2005;205:483-490. (Pubitemid 40361337)
57. Walker ML, Herndon JG. Menopause in nonhuman primates? Biol Reprod 2008;79:398-406.
58. Werness BA, Afify AM, Eltabbakh GH, Huelsman K, Piver MS, Paterson JM. p53, c-erbB, and Ki-67 expression in ovaries removed prophylactically from women with a family history of ovarian cancer. Int J Gynecol Pathol 1999;18:338-343. (Pubitemid 29489055)
59. Westhoff C, Murphy P, Heller D, Halim A. Is ovarian cancer associated with an increased frequency of germinal inclusion cysts? Am J Epidemiol 1993;138:90-93. (Pubitemid 23227924)
60. Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: The technique and its applications. Mol Reprod Dev 1990;27:261-280. (Pubitemid 20369549)
61. Wong AS, Auersperg N. Ovarian surface epithelium: Family history and early events in ovarian cancer. Reprod Biol Endocrinol 2003; 1:70.
62. Wright JW, Stouffer RL, Rodland KD. High-dose estrogen and clinical selective estrogen receptor modulators induce growth arrest, p21, and p53 in primate ovarian surface epithelial cells. J Clin Endocrinol Metab 2005;90:3688-3695. (Pubitemid 41014344)
63. Wright JW, Pejovic T, Fanton J, Stouffer RL. Induction of proliferation in the primate ovarian surface epithelium in vivo. Hum Reprod 2008; 23:129-138. (Pubitemid 351767319)
64. Wright JW, Pejovic T, Lawson M, Jurevic L, Hobbs T, Stouffer RL. Ovulation in the absence of the ovarian surface epithelium in the primate. Biol Reprod 2010;82:599-605.
65. Young KA, Hennebold JD, Stouffer RL. Dynamic expression of mRNAs and proteins for matrix metalloproteinases and their tissue inhibitors in the primate corpus luteum during the menstrual cycle. Mol Hum Reprod 2002;8:833-840. (Pubitemid 35012471)
66. Young KA, Chaffin CL, Molskness TA, Stouffer RL. Controlled ovulation of the dominant follicle: A critical role for LH in the late follicular phase of the menstrual cycle. Hum Reprod 2003; 18:2257-2263. (Pubitemid 37427800)