Expression pattern and role of a 60-kilodalton progesterone binding protein in regulating granulosa cell apoptosis: Involvement of the mitogen-activated protein kinase cascade

Biology of Reproduction

Volumn 68, Issue 1, 2003, Pages 122-128

  Peluso, J J ^a   Bremner, T ^a,b   Fernandez, G ^a   Pappalardo, A ^a   White, B A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b Fertility Physicians of Northern California   (United States)

Author keywords

Apoptosis; Granulosa cells; Progesterone; Progesterone receptor; Signal transduction

Indexed keywords

MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROGESTERONE; PROGESTERONE BINDING PROTEIN; PROGESTERONE RECEPTOR;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GRANULOSA CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; ENZYME INHIBITORS; FEMALE; FLAVONOIDS; GRANULOSA CELLS; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR WEIGHT; PROGESTERONE; PROGESTERONE-BINDING GLOBULIN; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RATS; RATS, WISTAR;

ANIMALIA;

EID: 0037235460     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.007542     Document Type: Article

References (41)

1. Monniaux D, Huet C, Besnard N, Clement F, Bosc M, Pisselet C, Monget P, Mariana JC. Follicular growth and ovarian dynamics in mammals. J Reprod Fertil Suppl 1997; 51:3-23.
2. Fujii T, Hoover DJ, Channing CP. Changes in inhibin activity, and progesterone, oestrogen and androstenedione concentrations, in rat follicular fluid throughout the oestrous cycle. J Reprod Fertil 1983; 69:307-314.
3. Roy SK, Greenwald GS. In vitro steroidogenesis by primary to antral follicles in the hamster during the periovulatory period: Effects of follicle-stimulating hormone, luteinizing hormone, and prolactin. Biol Reprod 1987; 37:39-46.
4. Curry TE Jr, Nothnick WB. Mifepristone and ovarian function. Clin Obstet Gynecol 1996; 39:486-497.
5. Robker RL, Russell DL, Yoshioka S, Sharma SC, Lydon JP, O'Malley BW, Espey LL, Richards JS. Ovulation: A multi-gene, multi-step process. Steroids 2000; 65:559-570.
6. Natraj U, Richards JS. Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 1993; 133:761-769.
7. Park OK, Mayo KE. Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 1991; 5:967-978.
8. Pall M, Mikuni M, Mitsube K, Brannstrom M. Time-dependent ovulation inhibition of a selective progesterone-receptor antagonist (Org 31710) and effects on ovulatory mediators in the in vitro perfused rat ovary. Biol Reprod 2000; 63:1642-1647.
9. Svensson EC, Markström E, Andersson M, Billig H. Progesterone receptor-mediated inhibition of apoptosis in granulosa cells isolated from rats treated with human chorionic gonadotropin. Biol Reprod 2000; 63:1457-1464.
10. Schreiber JR, Nakamura K, Erickson GF. Progestins inhibit FSH-stimulated steroidogenesis in cultured rat granulosa cells. Mol Cell Endocrinol 1980; 19:165-173.
11. Schreiber JR, Nakamura K, Erickson GF. Progestins inhibit FSH-stimulated granulosa estrogen production at a post-cAMP site. Mol Cell Endocrinol 1981; 21:161-170.
12. Peluso JJ, Pappalardo A. Progesterone mediates its anti-mitogenic and anti-apoptotic actions in rat granulosa cells through a progesterone-binding protein with gamma aminobutyric acid A receptor-like features. Biol Reprod 1998; 58:1131-1137.
13. Luciano AM, Peluso JJ. Effect of in vivo gonadotropin treatment on the ability of progesterone, estrogen, and cyclic adenosine 5′-monophosphate to inhibit insulin-dependent granulosa cell mitosis in vitro. Biol Reprod 1995; 53:664-669.
14. Peluso JJ, Fernandez G, Pappalardo A, White BA. Characterization of a putative membrane receptor for progesterone in rat granulosa cells. Biol Reprod 2001; 65:94-101.
15. Peluso JJ, Fernandez G, Pappalardo A, White BA. Membrane-initiated events account for progesterone's ability to regulate intracellular free calcium and inhibit rat granulosa cell mitosis. Biol Reprod 2002; (in press).
16. Schreiber JR, Hsueh AJW. Progesterone "receptor" in rat ovary. Endocrinology 1979; 105:915-925.
17. Schreiber JR, Erickson GF. Progesterone receptor in the rat ovary: Further characterization and localization in the granulosa cell. Steroids 1979; 34:459-469.
18. Naess O. Characterization of cytoplasmic progesterone receptors in rat granulosa cells. Evidence for nuclear translocation. Acta Endocrinol 1981; 98:288-294.
19. Blackmore PF, Im WB, Bleasdale JE. The cell surface progesterone receptor which stimulates calcium influx in human sperm is unlike the A ring reduced steroid site on the GABAA receptor/chloride channel. Mol Cell Endocrinol 1994; 104:237-243.
20. - ion channels modulated by multiple drug-binding sites. TIPS 1992; 131:446-450.
21. Schreiber JR, Nakamura K, Erickson GF. Rat ovary glucocorticoid receptor: Identification and characterization. Steroids 1982; 39:569-584.
22. Tetsuka M, Milne M, Simpson GE, Hillier SG. Expression of 11beta-hydroxysteroid dehydrogenase, glucocorticoid receptor, and mineralocorticoid receptor genes in rat ovary. Biol Reprod 1999; 60:330-335.
23. Peluso JJ, Pappalardo A. Progesterone maintains large rat granulosa cell viability indirectly by stimulating small granulosa cells to synthesize basic fibroblast growth factor. Biol Reprod 1999; 50:290-296.
24. Peluso JJ, Pappalardo A, Fernandez G. E-cadherin-mediated cell contact prevents apoptosis of spontaneously immortalized granulosa cells by regulating Akt kinase activity. Biol Reprod 2001; 64:1183-1190.
25. Stein LS, Stein DWJ, Echols J, Burghardt RC. Concomitant alterations of desmosomes, adhesiveness, and diffusion through gap junction channels in a rat ovarian transformation model system. Exp Cell Res 1993; 207:19-32.
26. Lynch K, Fernandez G, Pappalardo A, Peluso JJ. Basic fibroblast growth factor inhibits apoptosis of spontaneously immortalized granulosa cells by regulating intracellular free calcium levels through a protein kinase C delta-dependent pathway. Endocrinology 2000; 141:4209-4217.
27. Lederer KJ, Luciano AM, Pappalardo A, Peluso JJ. Proliferative and steroidogenic capabilities of rat granulosa cells of different sizes. J Reprod Fertil 1995; 103:47-54.
28. Rao IM, Mills TM, Anderson E, Mahesh VB. Heterogeneity in granulosa cells of developing rat follicles. Anat Rec 1991; 229:177-185.
29. Sanbuissho A, Lee GY, Anderson E. Functional and ultrastructural characteristics of two types of rat granulosa cell cultured in the presence of FSH or transforming growth factor alpha (TGF-alpha). J Reprod Fertil 1993; 98:367-376.
30. Hsueh AJW, McGee EA, Hayashi M, Hsu SY. Hormonal regulation of early follicle development in the rat ovary. Mol Cell Endocrinol 2000; 163:95-100.
31. Orly J. Molecular Events Defining Follicular Development and Steroidogenesis in the Ovary. Totowa, NJ: Human Press; 2000.
32. Hirshfield A. Development of follicles in the mammalian ovary. Int Rev Cytol 1991; 124:43-101.
33. Boone DL, Yan W, Tsang BK. Identification of a deoxyribonuclease I-like endonuclease in rat granulosa and luteal cell nuclei. Biol Reprod 1995; 53:1057-1065.
34. Peluso JJ. Placing progesterone in the apoptotic pathway. TEM 1997; 8:267-271.
35. Makrigiannakis A, Coukos G, Christofidou-Solomidou M, Montas S, Coutifaris C. Progesterone is an autocrine/paracrine regulator of human granulosa cell survival in vitro. Ann N Y Acad Sci 2000; 900:16-25.
36. Ballif BA, Blenis J. Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ 2001; 12:397-408.
37. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev 2001; 22:153-183.
38. Oliver RH, Khan SM, Leung BS, Yeh J. Induction of apoptosis in luteinized granulosa cells by the MAP kinase (MEK) inhibitor PD98059. Biochem Biophys Res Commun 1999; 263:143-148.
39. Gebauer G, Peter AT, Onesime D, Dhanasekaran N. Apoptosis of ovarian granulosa cells: Correlation with the reduced activity of ERK-signaling module. J Cell Biochem 1999; 75:547-554.
40. Bacus SS, Gudkov AV, Lowe M, Lyass L, Yung Y, Komarov AP, Keyomarsi K, Yarden Y, Seger R. Taxol-induced apoptosis depends on MAP kinase pathways (ERK and p38) and is independent of p53. Oncogene 2001; 20:147-155.
41. Zugasti O, Rul W, Roux P, Peyssonnaux C, Eychene A, Franke TF, Fort P, Hibner U. Raf-MEK-Erk cascade in anoikis is controlled by Racl and Cdc42 via Akt. Mol Cell Biol 2001; 21:6706-6717.