Molecular control of ovulation and luteinization in the primate follicle

Frontiers in Bioscience

Volumn 12, Issue 1, 2007, Pages 297-307

  Stouffer, Richard L ^a   Xu, Fuhua ^a   Duffy, Diane M ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

Angiopoietin; Granulosa cells; Luteinizing hormone; Oocyte; Ovary; Progesterone; Prostaglandin; Review; Rhesus monkey; Vascular endothelial growth factor

Indexed keywords

MACACA; MACACA MULATTA; PRIMATES;

EID: 34249799914     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2065     Document Type: Article

References (79)

1. Espey L. L., A. S. Bellinger, & J. A. Healy: Ovulation: An inflammatory cascade of gene expression. In: The Ovary. Eds: Leung PCK, Adashi EY, Elsevier Academic Press, San Diego, 145-165 (2004)
2. Richards J. S.: Ovulation: New factors that prepare the oocyte for fertilization. Mol Cell Endocrinol 234, 75-79 (2005)
3. Tsafriri A., X. Cao, H. Ashkenazi, S. Motola, M. Popliker, & S. H. Pomerantz: Resumption of oocyte meiosis in mammals: on models, meiosis activating sterols, steroids and EGF-like factors. Mol Cell Endocrinol 234, 37-45 (2005)
4. Richards J. S., D. L. Russell, S. Ochsner, M. Hsieh, K. H. Doyle, A. E. Falender, Y. K. Lo, & S. C. Sharma: Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 57, 195-220 (2002)
5. Richards J. S., I. Hernandez-Gonzalez, I. Gonzalez-Robayna, E. Teuling, Y. Lo, D. Boerboom, A. E. Falender, K. H. Doyle, R. G. LeBaron, V. Thompson, & J. D. Sandy: Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72, 1241-1255(2005)
6. Yacobi K., A. Wojtowicz, A. Tsafriri, & A. Gross: Gonadotropins enhance caspase-3 and -7 activity and apoptosis in the theca-interstitial cells of rat preovulatory follicles in culture. Endocinology 145, 1943-1951 (2004)
7. Shimada M., M. Nishibori, Y. Yamashita, J. Ito, M. Takahide, & J. S. Richards: Down-regulated expression of A disintegrin and metalloproteinase with thrombospondin-like repeats-1 by progesterone receptor antagonist is associated with impaired expansion of porcine cumulusoocyte complexes. Endocrinology 145, 4603-4614 (2004)
8. Brannstrom M. & A. Enskog: Leukocyte networks and ovulation. J Reprod Immunol 57, 47-60 (2002)
9. Murphy B. D.: Luteinization. In: The Ovary. Eds: Leung PCK, Adashi EY, Elsevier Academic Press, San Diego, 185-199 (2004)
10. Salustri A., C. Fulop, A. Camaioni, & V. C. Hascall: Oocyte-granulosa cell interactions. In: The Ovary. Eds: Leung PCK, Adashi EY, Elsevier Academic Press, San Diego, 131-143 (2004)
11. Hennebold J. D.: Characterization of the ovarian transcriptome through the use of differential analysis of gene expression methodologies. Hum Reprod Update 10, 227-239 (2004)
12. Richards J. S., D. L. Russell, S. Ochsner, & L. L. Espey: Ovulation: New dimensions and new regulators of the inflammatory-like response. Anna Rev Physiol 64, 69-92 (2002)
13. Sirois J., D. Boerboom, & K. Sayasith: Prostaglandin biosynthesis and action in the ovary. In: The Ovary. Eds: Leung PCK, Adashi EY, Elsevier Academic Press, San Diego, 233-247 (2004)
14. Matsumoto H., W. Ma, W. Smalley, J. Trzaskos, R. M. Breyer, & S. K. Dey: Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol Reprod 64, 1557-1565 (2001)
15. Sirois J. & M. Dore: The late induction of prostaglandin G/H synthase-2 in equine preovulatory follicles supports its role as a determinant of the ovulatory process. Endocrinology 138, 4427-4434 (1997)
16. Kobayashi T. & S. Narumiya: Function of prostanoid receptors: studies on knockout mice. Prostaglandins Other Lipid Mediat 68-69, 557-573 (2002)
17. Duffy D. M. & R. L. Stouffer: Prostaglandins modulate LH-stimulated periovulatory processes in primate granulosa cells in vitro. Endocrine 22, 249-256 (2003)
18. Duffy D. M. & R. L. Stouffer: The ovulatory gonadotropin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Mol Hum Reprod 7, 731-739 (2001)
19. Seachord C. L., C. A. VandeVoort, & D. M. Duffy: Adipose differentiation-related protein: a gonadotropin- and prostaglandin-regulated protein in primate periovulatory follicles. Biol Reprod 72, 1305-1314 (2005)
20. Duffy D. M., C. L. Seachord, & B. L. Dozier: An ovulatory gonadotropin stimulus increases cytosolic phospholipase A2 (cPLA2) expression and activity in granulosa cells of primate periovulatory follicles. J Clin Endocrinol Metab doi:10.1210/jc.2005-0980, (2005)
21. Kurusu S., S. Motegi, M. Kawaminami, & I. Hashimoto: Expression and cellular distribution of cytosolic phospholipase A2 in the rat ovary. Prostaglandins Leukot Essent Fatty Acids 58, 399-404 (1998)
22. Kurusu S., M. Iwao, M. Kawaminami, & I. Hashimoto: Involvement of cytosolic phospholipase A2 in the ovulatory process in gonadotropin-primed immature rats. Prostaglandins Leukot Essent Fatty Acids 58, 405-411 (1998)
23. Homaidan F. R., I. Chakroun, H. A. Haidar, & M. E. El-Sabban: Protein regulators of eicosanoid synthesis: role in inflammation. Curr Protein Pept Sci 3,467-484 (2002)
24. Roman R. J.: P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 82, 131-185 (2002)
25. Kroetz D. L. & D. C. Zeldin: Cytochrome P450 pathways of arachidonic acid metabolism. Curr Opin Lipidol 13, 273-283 (2002)
26. Mikuni M, M. Yoshida, P. Hellberg, C. A. Peterson, S. S. Edwin, M. Brännström, & C. M. Peterson: The lipoxygenase inhibitor, nordihydroguaiaretic acid, inhibits ovulation and reduces leukotriene and prostaglandin levels in the rat ovary. Biol Reprod 58, 1211-1216 (1998)
27. 4 receptor antagonist. Mol Hum Reprod 7, 35-42 (2001)
28. Ichikawa F., Y. Yoshimura, & T. Oda: The effects of lipoxygenase products on progesterone and prostaglandin production by human corpora lutea. J Clin Endocrinol Metab 70, 849-(1990)
29. Duffy D. M., C. L. Seachord, & B. L. Dozier: Microsomal prostaglandin E synthase-1 (mPGES-1) is the primary form of PGES expressed by the primate periovulatory follicle. Hum Reprod 20, 1485-1492 (2005)
30. Patwardhan V. V. & A. Lanthier: Prostaglandins PGE and PGF in human ovarian follicles: endogenous contents and in vitro formation by theca and granulosa cells. Acta Endocrinol (Copenh) 97, 543-550 (1981)
31. Duffy D. M., B. L. Dozier, & C. L. Seachord: Prostaglandin dehydrogenase and prostaglandin levels in periovulatory follicles: implications for control of primate ovulation by prostaglandin E2. J Clin Endocrinol Metab 90, 1021-1027 (2005)
32. Wallach E. E., A. de la Cruz, J. Hunt, K. H. Wright, & V. C. Stevens: The effect of indomethacin on hMG-hCG induced ovulation in the rhesus monkey. Prostaglandins 9, 645-658 (1975)
33. Killick S. & M. Elstein: Pharmacologic production of luteinized unruptured follicles by prostaglandin synthetase inhibitors. Fertil Steril 47, 773-777 (1987)
34. Norman R. J.: Reproductive consequences of COX-2 inhibition. The Lancet 358, 1287-1288 (2001)
35. Duffy D. M. & R. L. Stouffer: Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Hum Reprod 17, 2825-2831 (2002)
36. Harris T. E., P. E. Squires, A. E. Michael, A. L. Bernai, & D. R. Abayasekara: Human granulosa-lutein cells express functional EP1 and EP2 prostaglandin receptors. Biochem Biophys Res Commun 285, 1089-1094 (2001)
37. Narko K., K. Saukkonen, I. Ketola, R. Butzow, M. Heikinheimo, & A. Ristimaki: Regulated expression of prostaglandin E2 receptors EP2 and EP4 in human ovarian granulosa-luteal cells. J Clin Endocrinol Metab 86,1765-1768 (2001)
38. Rothchild I.: The regulation of the mammalian corpus luteum. Rec Prog Harm Res 37, 183-298 (1981)
39. Stouffer R. L.: Progesterone as a mediator of gonadotropin action in the primate corpus luteum: beyond steroidogenesis. Hum Reprod Update 9, 99-117 (2003)
40. A receptor-like features. Biol Reprod 58, 1131-1137 (1998)
41. Peluso J. J., A. Pappalardo, G. Fernandez, & C. A. Wu: Involvement of an unnamed protein, RDA288, in the mechanism through which progesterone mediates its antiapoptotic action in spontaneously immortalized granulosa cells. Endocrinology 145, 3014-3022 (2004)
42. Lydon J. P., F. J. DeMayo, C. R. Funk, S. K. Mani, A. R. Hughes, C. A. Montgomery, Jr., G. Shyamala, O. M. Conneely, & B. W. O'Malley: Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9, 2266-2278 (1995)
43. Mulac-Jericevic B. & O. M. Conneely: Reproductive tissue selective actions of progesterone receptors. Reproduction 128, 139-146 (2004)
44. Hibbert M. L., R. L. Stouffer, D. P. Wolf, & M. F. Zelinski-Wooten: Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Nail Acad Sci USA 93, 1897-1901 (1996)
45. Borman S. M., C. L. Chaffin, K. M. Schwinof, R. L. Stouffer, & M. B. Zelinski-Wooten: Progesterone promotes oocyte maturation, but not ovulation, in primate follicles without a gonadotropin surge. Biol Reprod 71, 366-373 (2004)
46. Hammes S. R.: Steroids and oocyte maturation - a new look at an old story. Mol Endocrinol 18, 769-775 (2004)
47. Shimada M. & T. Terada: FSH and LH induce progesterone production and progesterone receptor synthesis in cumulus cells: a requirement for meiotic resumption in porcine oocytes. Mol Hum Reprod 8, 612-618(2002)
48. Robker R. L., D. L. Russell, L. L. Espey, J. P. Lydon, B. W. O'Malley, & J. S. Richards: Progesterone-regulated genes in the ovulation process: AD AMTS-1 and cathepsin L proteases. Proc Natl Acad Sci 97, 4689-4694 (2000)
49. Chaffin C. L., D. L. Hess, & R. L. Stouffer: Dynamics of periovulatory steroidogenesis in the rhesus monkey follicle after ovarian stimulation. Hum Reprod 14, 642-649 (1999)
50. Chaffin C. L., G. A. Dissen, & R. L. Stouffer: Hormonal regulation of steroidogenic enzyme expression in granulosa cells during the periovulatory interval in monkeys. Mol Hum Reprod 6, 11-18 (2000)
51. 2α during ovulation in the gonadotropin-primed immature rat. Endocrinology 127, 259-263 (1990)
52. Tanaka N., J. Iwamasa, K. Matsuura, & H. Okamura: Effects of progesterone and anti-progesterone RU486 on ovarian 3ß-hydroxysteroid dehydrogenase activity during ovulation in the gonadotrophin-primed immature rat. J Reprod Fertil 97, 167-172 (1993)
53. Lui K., Q. Feng, & H. J. Gao: Expression and regulation of plasminogen activators (PA), plasminogen activator inhibitor type-1 (PAI-1) and steroidogenic acute regulatory protein (StAR) in rhesus monkey corpus luteum. Endocrinology 144, 3611-3617 (2003)
54. Chaffin C. L., K. M. Schwinof, & R. L. Stouffer: Gonadotropin and steroid control of granulosa cell proliferation during the periovulatory interval in monkeys. Biol Reprod 65, 755-762 (2001)
55. Robker R. L. & J. S. Richards: Hormone control of the cell cycle in ovarian cells: proliferation versus differentiation. Biol Reprod 59, 476-482 (1996)
56. Chaffin C. L., R. S. Brogan, R. L. Stouffer, & C. A. VandeVoort: Dynamics of Myc/Max/Mad expression during luteinization of primate granulosa cells in vitro: association with periovulatory proliferation. Endocinology 144, 1249-1256 (2003)
57. Chaffin C. L. & R. L. Stouffer: Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation. Biol Reprod 61, 14-21 (1999)
58. Young K. A., J. D. Hennebold, & R. L. Stouffer: 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 8, 833-840 (2002)
59. Chen X. L., H. J. Gao, F. Gao, P. Wei, Z. Y. Hu, & Y. X. Liu: Temporal and spatial expression of MMP-2, -9, 14 and their inhibitors TIMP-1, -2, -3 in the corpus luteum of the cycling rhesus monkey. Front Biosci in press, (2005)
60. Curry T. E., Jr. & K. G. Osteen: The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocrine Rev 24, 428-465 (2003)
61. Liu Y.-X., K. Liu, Q. Feng, Z.-Y. Hu, H.-Z. Liu, G.-Q. Fu, Y.-C. Li, R.-J. Zou, & T. Ny: Tissue-type plasminogen activator and its inhibitor plasminogen activator type 1 are coordinately expressed during ovulation in the rhesus monkey. Endocrinology 145, 1767-1775 (2004)
62. Tanaka N., L. L. Espey, S. Stacy, & H. Okamura: Epostane and indomethacin actions on ovarian kallikrein and plasminogen activator activites during ovulation in the gonadotropin-primed immature rat. Biol Reprod 46, 665-670 (1992)
63. Young K. A., B. Bumlinson, & R. L. Stouffer: ADAMTS-l/METH-1 and TIMP-3 expression in the primate corpus luteum: divergent patterns and stage-dependent regulation during the natural menstrual cycle. Mol Hum Reprod 10, 559-565 (2004)
64. Hazzard T. M. & R. L. Stouffer: Angiogenesis in ovarian follicular and luteal development. In: Clinical Obstetrics & Gynaecology. Angiogenesis in the Female Reproductive Tract. Eds: Arulkumaran S, Bailliere Tindall, London, 883-900 (2000)
65. Fraser H. M. & C. Wulff: Angiogenesis in the corpus luteum. Reprod Biol Endocrinol 1, 88-(2003)
66. Xu F., T. M. Hazzard, A. Evans, S. Charnock-Jones, S. Smith, & R. L. Stouffer: Intraovarian actions of anti- angiogenic agents disrupt periovulatory events during the menstrual cycle in monkeys. Contraception 71, 239-248 (2005)
67. Hanahan D.: Signaling vascular morphogenesis and maintenance. Science 277, 48-50 (1997)
68. Christenson L. K. & R. L. Stouffer: Folliclestimulating hormone and luteinizing hormone/chorionic gonadotropin stimulation of vascular endothelial growth factor production by macaque granulosa cells from pre- and periovulatory follicles. J Clin Endocrinol Metab 82, 2135-2142 (1997)
69. Martinez-Chequer J. C., R. L. Stouffer, T. M. Hazzard, P. E. Patton, & T. A. Molskness: Insulin-like growth factor (IGF) -1 and -2, but not hypoxia, synergize with gonadotropin hormone to promote vascular endothelial growth factor (VEGF) -A secretion by monkey granulosa cells from preovulatory follicles. Biol Reprod 68, 1112-1118 (2003)
70. Friedman C. I., D. R. Danforth, C. Herbosa-Encarnacion, L. Arbogast, B. M. Alak, & D. B. Seifer: Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction. Fertil Steril 68,607-612 (1997)
71. Tesone M., R. L. Stouffer, S. M. Borman, J. D. Hennebold, & T. A. Molskness: Vascular endothelial growth factor (VEGF) production by the monkey corpus luteum during the menstrual cycle: isoform-selective mRNA expression in vivo and hypoxia regulated protein secretion in vitro. Biol Reprod 73, 927-934 (2005)
72. Hazzard T. M., T. A. Molskness, C. L. Chaffin, & R. L. Stouffer: Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval. Mol Hum Reprod 5, 1115-1121 (1999)
73. Maisonpierre P. C., C. Suri, P. F. Jones, S. Bartunkova, S. J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T. H. Aldrich, N. Papadopoulos, T. J. Daly, S. Davis, T. N. Sato, & G. D. Yancopoulos: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277, 55-60 (1997)
74. Hazzard T. M., F. Xu, & R. L. Stouffer: Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol Reprod 67, 1305-1312 (2002)
75. Xu F. & R. L. Stouffer: Local delivery of angiopoietin-2 into the preovulatory follicle terminates the menstrual cycle in rhesus monkeys. Biol Reprod 72, 1352-1358 (2005)
76. LeCouter J., J. Kowalski, J. Foster, P. Hass, Z. Zhang, L. Dillard-Telm, G. Frantz, L. Rangell, L. DeGuzman, G. A. Keller, F. Peale, A. Gurney, K. J. Hillan, & N. Ferrara: Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877-884 (2001)
77. Fraser H. M., J. Bell, H. Wilson, P. D. Taylor, K. Morgan, R. A. Anderson, & W. C. Duncan: Localization and quantification of cyclic changes in the expression of endocrine gland vascular endothelial growth factor in the human corpus luteum. J Clin Endocrinol Metab in press, (2004)
78. Kisliouk T., H. Podlovni, K. Spanel-Borowski, O. Ovadia, Q.-Y. Zhou, & R. Meidan: Prokineticins (endocrine gland-derived vascular endothelial growth factor and BV8) in the bovine ovary: expression and role as mitogens and survival factors for corpus luteum-derived endothelial cells. Endocrinology 146, 3950-3958 (2005)
79. Xu J., R. L. Stouffer, & J. D. Hennebold: Discovery of luteinizing hormone (LH)-regulated genes in the primate corpus luteum. Mol Hum Reprod 11, 151-159 (2005)