Progestin signaling through mPRαin atlantic croaker granulosa/theca cell cocultures and its involvement in progestin inhibition of apoptosis

Endocrinology

Volumn 151, Issue 12, 2010, Pages 5916-5926

  Dressing, Gwen E ^a,b   Pang, Yefei ^a   Dong, Jing ^c   Thomas, Peter ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

17,20BETA,21 TRIHYDROXY 4 PREGNEN 3 ONE; CYCLIC AMP; GESTAGEN; GUANINE NUCLEOTIDE BINDING PROTEIN; PERTUSSIS TOXIN; PROGESTERONE RECEPTOR; PROMEGESTONE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL CULTURE; CELL MEMBRANE; CELLULAR DISTRIBUTION; FEMALE; FISH; GRANULOSA CELL; MOLECULAR MECHANICS; NONHUMAN; OVARY FOLLICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THECA CELL;

ANIMALS; APOPTOSIS; CELL DEATH; CELLS, CULTURED; COCULTURE TECHNIQUES; CORTODOXONE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GRANULOSA CELLS; PERCIFORMES; PROGESTINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, PROGESTERONE; RNA, SMALL INTERFERING; THECA CELLS;

EID: 78649831918     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0165     Document Type: Article

References (55)

1. Masui Y, Markert CL 1971 Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129-145
2. Thomas P, Zhu Y, Pace M 2002 Progestin membrane receptors involved in the meiotic maturation of teleost oocytes: a review with some new findings. Steroids 67:511-517
3. Patiño R, Thomas P 1990 Characterization of membrane receptor activity for 17α,20β,21-tryhydroxy-4-pregnen-3-one in ovaries of spotted seatrout (Cynoscion nebulosus). Gen Comp Endocrinol 78:204-217
4. Pinter J, Thomas P 1997 The ovarian progestogen receptor in the spotted seatrout, Cynoscion nebulosus, demonstrates steroid specificity different from the progesterone receptors in other vertebrates. J Steroid Biochem Mol Biol 60:113-119
5. Pinter J, Thomas P 1995 Characterization of a progestogen receptor in the ovary of the spotted sea-trout, Cynoscion Nebulosus. Biol Reprod 52:667-675
6. Zhu Y, Rice CD, Pang Y, Pace M, Thomas P 2003 Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 100:2231-2236
7. Thomas P, Pang Y, Dong J, Groenen P, Kelder J, de Vlieg J, Zhu Y, Tubbs C 2007 Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor α subtypes and their evolutionary origins. Endocrinology 148:705-718
8. Tang YT, Hu T, Arterburn M, Boyle B, Bright JM, Emtage PC, Funk WD 2005 PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol 61:372-380
9. Lyons TJ, Villa NY, Regalla LM, Kupchak BR, Vagstad A, Eide DJ 2004 Metalloregulation of yeast membrane steroid receptor homologs. Proc Natl Acad Sci USA 101:5506-5511
10. Tubbs C, Pace M, Thomas P 2010 Expression and gonadotropin regulation of membrane progestin receptor α in Atlantic croaker (Micropogonias undulatus) gonads: role in gamete maturation. Gen Comp Endocrinol 165:144-154
11. Hanna R, Pang Y, Thomas P, Zhu Y 2006 Cell-surface expression, progestin binding, and rapid nongenomic signaling of zebrafish membrane progestin receptors α and β in transfected cells. J Endocrinol 190:247-260
12. Tokumoto M, Nagahama Y, Thomas P, Tokumoto T 2006 Cloning and identification of a membrane progestin receptor in goldfish ovaries and evidence it is an intermediary in oocyte meiotic maturation. Gen Comp Endocrinol 145:101-108
13. Josefsberg Ben-Yehoshua L, Lewellyn AL, Thomas P, Maller Jl 2007 The role of Xenopus membrane progesterone receptor β in mediating the effect of progesterone on oocyte maturation. Mol Endocrinol 21:664-673
14. Kazeto Y, Goto-Kazeto R, Trant JM 2005 Membrane-bound progestin receptors in channel catfish and zebrafish ovary: changes in gene expression associated with the reproductive cycles and hormonal reagents. Gen Comp Endocrinol 142:204-211
15. Ashley RL, Clay CM, Farmerie TA, Niswender GD, Nett TM 2006 Cloning and characterization of an ovine intracellular seven transmembrane receptor for progesterone that mediates calcium mobilization. Endocrinology 147:4151-4159
16. Zhu Y, Bond J, Thomas P 2003 Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci USA 100:2237-2242
17. Cai Z, Stocco CO 2005 Expression and regulation of progestin membrane receptors in the rat corpus luteum. Endocrinology 146:5522-5532
18. Telleria CM, Stocco CO, Stati AO, Deis RP 1999 Progesterone receptor is not required for progesterone action in the rat corpus luteum of pregnancy. Steroids 64:760-766
19. Engmann L, Losel R, Wehling M, Peluso JJ 2006 Progesterone regulation of human granulosa/luteal cell viability by an RU486-independent mechanism. J Clin Endocrinol Metab 91:4962-4968
20. Peluso JJ, Pappalardo A, Losel R, Wehling M 2006 Progesterone membrane receptor component 1 expression in the immature rat ovary and its role in mediating progesterone's antiapoptotic action. Endocrinology 147:3133-3140
21. Chaffin CL, Stouffer RL 2000 Role of gonadotrophins and progesterone in the regulation of morphological remodelling and atresia in the monkey peri-ovulatory follicle. Hum Reprod 15:2489-2495
22. Mussche S, D'Herde K 2001 Contribution of progesterone, follicle stimulating hormone and glucocorticoids in survival of serum-free cultured granulosa cell explants. J Endocrinol 169:321-331
23. Quirk SM, Cowan RG, Harman RM 2004 Progesterone receptor and the cell cycle modulate apoptosis in granulosa cells. Endocrinology 145:5033-5043
24. Rueda BR, Hendry IR, Hendry III W, Stormshak F, Slayden OD, Davis JS 2000 Decreased progesterone levels and progesterone receptor antagonists promote apoptotic cell death in bovine luteal cells. Biol Reprod 62:269-276
25. Svensson EC, Markström E, Andersson M, Billig H 2000 Progesterone receptor-mediated inhibition of apoptosis in granulosa cells isolated from rats treated with human chorionic gonadotropin. Biol Reprod 63:1457-1464
26. Benninghoff AD, Thomas P 2006 Gonadotropin regulation of testosterone production by primary cultured theca and granulosa cells of Atlantic croaker: I. Novel role of CaMKs and interactions between calcium- and adenylyl cyclase-dependent pathways. Gen Comp Endocrinol 147:276-287
27. Karteris E, Zervou S, Pang Y, Dong J, Hillhouse EW, Randeva HS, Thomas P 2006 Progesterone signaling in human myometrium through two novel membrane G protein coupled receptors: potential role in functional progesterone withdrawal at term. Mol Endocrinol 20:1519-1534
28. Dressing GE, Thomas P 2007 Identification of membrane progestin receptors in human breast cancer cell lines and biopsies and their potential involvement in breast cancer. Steroids 72:111-116
29. Kelder J, Azevedo R, Pang Y, de Vlieg J, Dong J, Thomas P 2010 Comparison between steroid binding to the human progestin membrane receptor α subtype and to the human progestin nuclear receptor: correlations with physiochemical properties assessed by comparative molecular field analysis. Steroids 75:314-322
30. Scott AP, Sheldrick EL, Flint APF 1982 Measurement of 17α,20β- dihydroxy-4-pregnen-3-one in plasma of trout (Salmo gairdneri Richardson): seasonal changes and response to salmon pituitary extract. Gen Comp Endocrinol 46:444-451
31. Kaslow HR, Lim LK, Moss J, Lesikar DD 1987 Structure-activity analysis of the activation of pertussis toxin. Biochemistry 26:123-127
32. Moore MR, Spence JB, Kiningham KK, Dillon JL 2006 Progestin inhibition of cell death in human breast cancer cell lines. J Steroid Biochem Mol Biol 98:218-227
33. Freshney RI 1994 Culture of animal cells: a manual of basic technique. 4th ed. New York: Wiley-Liss
34. Thomas P, Harris C, Pang Y 2008 The roles of different types of progestin receptors in oocyte maturation of zebrafish. Biol Reprod (Sp Iss SI) 705:220 (Abstract)
35. Song G, Ouyang G, Bao S 2005 The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9:59-71
36. Sleiter N, Pang Y, Park C, Horton TH, Dong J, Thomas P, Levine JE 2009 Progesterone receptor A (PRA) and PRB-independent effects of progesterone on gonadotropin-releasing hormone release. Endocrinology 150:3833-3844
37. Foster H, Reynolds A, Stenbeck G, Dong J, Thomas P, Karteris E 2009 Internalization of membrane progesterone receptor α (mPRα) after treatment with progesterone: potential involvement of a clathrin- dependent pathway. Mol Med Report 3:27-35
38. Petaja-Repo UE, Hogue M, Laperriere A, Walker P, Bouvier M 2000 Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human δ opioid receptor. J Biol Chem 275:13727-13736
39. Rae MT, Menzies GS, Bramley TA 1998 Bovine ovarian nongenomic progesterone binding sites: presence in follicular and luteal cell membranes. J Endocrinol 159:413-427
40. Meyer C, Schmid R, Scriba PC, Wehling M 1996 Purification and partial sequencing of high-affinity progesterone-binding site(s) from porcine liver membranes. Eur J Biochem 239:726-731
41. Peluso JJ, Fernandez G, Pappalardo A, White BA 2001 Characterization of a putative membrane receptor for progesterone in rat granulosa cells. Biol Reprod 65:94-101
42. Cahill MA 2007 Progesterone receptor membrane component 1: an integrative review. J Ster Biochem Mol Biol 105:16-36
43. Thomas P 2008 Characteristics of membrane progestin receptor α (mPRα) and progesterone membrane receptor component one (PGRMC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol 29:292-312
44. West Jr RE, Moss J, Vaughn M, Lui T, Lui TY 1985 Pertussis toxin catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADPribose acceptor site. J Biol Chem 260:14428-14430
45. Pace MC, Thomas P 2005 Activation of a pertussis toxin-sensitive, inhibitory G-protein is necessary for steroid-mediated oocyte maturation in spotted seatrout. Dev Biol 285:70-79
46. Drummond CD, Bazzoli N, Rizzo E, Sato Y 2000 Postovulatory follicle: a model for experimental studies of programmed cell death or apoptosis in teleosts. J Exp Zool 287:176-182
47. Johnson AL 2003 Intracellular mechanisms regulating cell survival in ovarian follicles. Anim Reprod Sci 78:185-201
48. Pace MC, Thomas P 2005 Steroid-induced oocyte maturation in Atlantic croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Biol Reprod 73:988-996
49. Lin H, Chen C, Li X, Chen BD 2002 Activation of the MEK/MAPK pathway is involved in bryostatin 1-induced monocytic differentiation and up-regulation of X-linked inhibitor of apoptosis protein. Exp Cell Res 272:192-198
50. She QB, Ma WY, Zhong S, Dong Z 2002 Activation of JNK1, RSK2, and MSK1 is involved in serine 112 phosphorylation of Bad by ultraviolet B radiation. J Biol Chem 277:24039-24048
51. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME 1997 Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241
52. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC 1998 Regulation of cell death protease caspase-9 by phosphorylation. Science 282:1318-1321
53. Bertelsen EL, Endresen PC, Orbo A, Sager G 2004 Non-genomic cell growth inhibition by progesterone. cell cycle retardation and induction of cell death. Anticancer Res 24:3749-3755
54. Friberg PA, Larsson DG, Billig H 2009 Dominant role of nuclear progesterone receptor in the control of rat periovulatory granulosa cell apoptosis. Biol Reprod 80:1160-1167
55. Friberg PA, Larsson DG, Rung E, Billig H 2007 Apoptotic effects of a progesterone receptor antagonist on rat granulosa cells are not mediated via reduced protein isoprenylation. Mol Reprod Dev 74: 1317-1326