Inhibin A inhibits follicle-stimulating hormone (FSH) action by suppressing its receptor expression in cultured rat granulosa cells

Molecular and Cellular Endocrinology

Volumn 298, Issue 1-2, 2009, Pages 48-56

  Lu, Cuiling ^a,b   Yang, Wei ^a   Chen, Min ^a   Liu, Tao ^a   Yang, Junling ^a   Tan, Ping ^a   Li, Lei ^a   Hu, Xiaoqian ^a   Fan, Cuihong ^a   Hu, Zhaoyuan ^a   Liu, Yixun ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

FSH; FSHR; Granulosa cells; Inhibin A

Indexed keywords

ANDROGEN RECEPTOR; CYCLIC AMP; FOLLITROPIN; FORSKOLIN; INHIBIN A; MESSENGER RNA; NUCLEAR RECEPTOR DAX 1; PROGESTERONE; STEROIDOGENIC FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GRANULOSA CELL; HORMONE ACTION; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; AROMATASE; CELLS, CULTURED; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; DNA-BINDING PROTEINS; FEMALE; FOLLICLE STIMULATING HORMONE; FORSKOLIN; GENE EXPRESSION; GRANULOSA CELLS; INHIBINS; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANDROGEN; RECEPTORS, FSH; RECEPTORS, RETINOIC ACID; REPRESSOR PROTEINS; STEROIDOGENIC FACTOR 1; STEROIDS;

EID: 57749207926     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.09.039     Document Type: Article

References (65)

1. Abel M.H., Wootton A.N., Wilkins V., Huhtaniemi I., Knight P.G., and Charlton H.M. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 141 (2000) 1795-1803
2. Agoulnik I.U., Krause W.C., Bingman III W.E., Rahman H.T., Amrikachi M., Ayala G.E., and Weigel N.L. Repressors of androgen and progesterone receptor action. J. Biol. Chem. 278 (2003) 31136-31148
3. Andersen C.Y., and Byskov A. Estradiol and regulation of anti-Mullerian hormone inhibin-A and inhibin-B secretion: analysis of small antral and preovulatory human follicles' fluid. J. Clin. Endocrinol. Metab. 91 (2006) 4064-4069
4. Baird D.T., and Smith K.B. Inhibin and related peptides in the regulation of reproduction. Oxf. Rev. Reprod. Biol. 15 (1993) 191-232
5. Bakke M., Zhao L., Hanley N.A., and Parker K.L. SF-1 a critical mediator of steroidogenesis. Mol. Cell. Endocrinol. 171 (2001) 5-7
6. Bernard D.J., Chapman S.C., and Woodruff T.K. Mechanisms of inhibin signal transduction. Recent Prog. Horm. Res. 56 (2001) 417-450
7. Burger H.G. Evidence for a negative feedback role of inhibin in follicle stimulating hormone regulation in women. Hum. Reprod. 8 Suppl. 2 (1993) 129-132
8. Campbell B.K., and Baird D.T. Inhibin A is a follicle stimulating hormone-responsive marker of granulosa cell differentiation, which has both autocrine and paracrine actions in sheep. J. Endocrinol. 169 (2001) 333-345
9. Chappel S.C., and Howles C. Reevaluation of the roles of luteinizing hormone and follicle-stimulating hormone in the ovulatory process. Hum. Reprod. (Oxford, England) 6 (1991) 1206-1212
10. Crawford P.A., Dorn C., Sadovsky Y., and Milbrandt J. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol. Cell. Biol. 18 (1998) 2949-2956
11. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gansmuller A., LeMeur M., and Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13612-13617
12. Dubey A.K., Zeleznik A.J., and Plant T.M. In the rhesus monkey (Macaca mulatta), the negative feedback regulation of follicle-stimulating hormone secretion by an action of testicular hormone directly at the level of the anterior pituitary gland cannot be accounted for by either testosterone or estradiol. Endocrinology 121 (1987) 2229-2237
13. Findlay J.K. An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol. Reprod. 48 (1993) 15-23
14. Goetz T.L., Lloyd T.L., and Griswold M.D. Role of E box and initiator region in the expression of the rat follicle-stimulating hormone receptor. J. Biol. Chem. 271 (1996) 33317-33324
15. Gudermann T., Nurnberg B., and Schultz G. Receptors and G proteins as primary components of transmembrane signal transduction. Part 1. G-protein-coupled receptors: structure and function. J. Mol. Med. (Berlin, Germany) 73 (1995) 51-63
16. Heckert L.L. Activation of the rat follicle-stimulating hormone receptor promoter by steroidogenic factor 1 is blocked by protein kinase a and requires upstream stimulatory factor binding to a proximal E box element. Mol. Endocrinol. 15 (2001) 704-715
17. Heckert L.L., Daley I.J., and Griswold M.D. Structural organization of the follicle-stimulating hormone receptor gene. Mol. Endocrinol. 6 (1992) 70-80
18. Heckert L.L., Sawadogo M., Daggett M.A., and Chen J.K. The USF proteins regulate transcription of the follicle-stimulating hormone receptor but are insufficient for cell-specific expression. Mol. Endocrinol. 14 (2000) 1836-1848
19. Heinlein C.A., and Chang C. Androgen receptor (AR) coregulators: an overview. Endocr. Rev. 23 (2002) 175-200
20. Herath C.B., Yamashita M., Watanabe G., Jin W., Tangtrongsup S., Kojima A., Groome N.P., Suzuki A.K., and Taya K. Regulation of follicle-stimulating hormone secretion by estradiol and dimeric inhibins in the infantile female rat. Biol. Reprod. 65 (2001) 1623-1633
21. Holter E., Kotaja N., Makela S., Strauss L., Kietz S., Janne O.A., Gustafsson J.A., Palvimo J.J., and Treuter E. Inhibition of androgen receptor (AR) function by the reproductive orphan nuclear receptor DAX-1. Mol. Endocrinol. 16 (2002) 515-528
22. Humaidan P., Bungum L., Bungum M., and Yding Andersen C. Rescue of corpus luteum function with peri-ovulatory HCG supplementation in IVF/ICSI GnRH antagonist cycles in which ovulation was triggered with a GnRH agonist: a pilot study. Reprod. Biomed. Online 13 (2006) 173-178
23. Ito M., Yu R., and Jameson J.L. DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol. Cell. Biol. 17 (1997) 1476-1483
24. Iyer A.K., and McCabe E.R. Molecular mechanisms of DAX1 action. Mol. Genet. Metab. 83 (2004) 60-73
25. Jimenez-Krassel F., Winn M.E., Burns D., Ireland J.L., and Ireland J.J. Evidence for a negative intrafollicular role for inhibin in regulation of estradiol production by granulosa cells. Endocrinology 144 (2003) 1876-1886
26. Johnson P.A., Woodcock J.R., and Kent T.R. Effect of activin A and inhibin A on expression of the inhibin/activin beta-B-subunit and gonadotropin receptors in granulosa cells of the hen. Gen. Comp. Endocrinol. 147 (2006) 102-107
27. Jorgensen J.S., and Nilson J.H. AR suppresses transcription of the LHbeta subunit by interacting with steroidogenic factor-1. Mol. Endocrinol. 15 (2001) 1505-1516
28. Jouravel N., Sablin E., Arnold L.A., Guy R.K., and Fletterick R.J. Interaction between the androgen receptor and a segment of its corepressor SHP. Acta Crystallogr. D Biol. Crystallogr. 63 (2007) 1198-1200
29. Kumar T.R., Wang Y., Lu N., and Matzuk M.M. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15 (1997) 201-204
30. Lalli E., and Sassone-Corsi P. DAX-1, an unusual orphan receptor at the crossroads of steroidogenic function and sexual differentiation. Mol. Endocrinol. 17 (2003) 1445-1453
31. Lalli E., Melner M.H., Stocco D.M., and Sassone-Corsi P. DAX-1 blocks steroid production at multiple levels. Endocrinology 139 (1998) 4237-4243
32. Lanuza G.M., Groome N.P., Baranao J.L., and Campo S. Dimeric inhibin A and B production are differentially regulated by hormones and local factors in rat granulosa cells. Endocrinology 140 (1999) 2549-2554
33. Levallet J., Koskimies P., Rahman N., and Huhtaniemi I. The promoter of murine follicle-stimulating hormone receptor: functional characterization and regulation by transcription factor steroidogenic factor 1. Mol. Endocrinol. 15 (2001) 80-92
34. Lumpkin M.D., DePaolo L.V., and Negro-Vilar A. Pulsatile release of follicle-stimulating hormone in ovariectomized rats is inhibited by porcine follicular fluid (inhibin). Endocrinology 114 (1984) 201-206
35. Mann G.E., Campbell B.K., McNeilly A.S., and Baird D.T. The role of inhibin and oestradiol in the control of FSH secretion in the sheep. J. Endocrinol. 133 (1992) 381-391
36. Minegishi T., Hirakawa T., Kishi H., Abe K., Abe Y., Mizutani T., and Miyamoto K. A role of insulin-like growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol. Reprod. 62 (2000) 325-333
37. Molskness T.A., Woodruff T.K., Hess D.L., Dahl K.D., and Stouffer R.L. Recombinant human inhibin-A administered early in the menstrual cycle alters concurrent pituitary and follicular, plus subsequent luteal, function in rhesus monkeys. J. Clin. Endocrinol. Metab. 81 (1996) 4002-4006
38. Monaco L., Foulkes N.S., and Sassone-Corsi P. Pituitary follicle-stimulating hormone (FSH) induces CREM gene expression in Sertoli cells: involvement in long-term desensitization of the FSH receptor. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 10673-10677
39. Mukai T., Kusaka M., Kawabe K., Goto K., Nawata H., Fujieda K., and Morohashi K. Sexually dimorphic expression of Dax-1 in the adrenal cortex. Genes Cells 7 (2002) 717-729
40. Nakamura M., Minegishi T., Hasegawa Y., Nakamura K., Igarashi S., Ito I., Shinozaki H., Miyamoto K., Eto Y., and Ibuki Y. Effect of an activin A on follicle-stimulating hormone (FSH) receptor messenger ribonucleic acid levels and FSH receptor expressions in cultured rat granulosa cells. Endocrinology 133 (1993) 538-544
41. Orisaka M., Orisaka S., Jiang J.Y., Craig J., Wang Y., Kotsuji F., and Tsang B.K. Growth differentiation factor-9 is anti-apoptotic during follicular development from preantral to early antral stage. Mol. Endocrinol. (2006)
42. Ramaswamy S., Pohl C.R., McNeilly A.S., Winters S.J., and Plant T.M. The time course of follicle-stimulating hormone suppression by recombinant human inhibin A in the adult male rhesus monkey (Macaca mulatta). Endocrinology 139 (1998) 3409-3415
43. Schuiling G.A., Pols-Valkhof N., van der Schaaf-Verdonk G.C., de Jong F.H., and Koiter T.R. Decidua and the control of corpus luteum function, follicular development and pituitary LHRH-responsiveness in pseudopregnant and pregnant rats. Experientia 43 (1987) 895-898
44. Shapiro D.B., Pappalardo A., White B.A., and Peluso J.J. Steroidogenic factor-1 as a positive regulator of rat granulosa cell differentiation and a negative regulator of mitosis. Endocrinology 137 (1996) 1187-1195
45. Shukovski L., and Findlay J.K. Activin-A inhibits oxytocin and progesterone production by preovulatory bovine granulosa cells in vitro. Endocrinology 126 (1990) 2222-2224
46. Simoni M., Gromoll J., and Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18 (1997) 739-773
47. Smyth C.D., Gosden R.G., McNeilly A.S., and Hillier S.G. Effect of inhibin immunoneutralization on steroidogenesis in rat ovarian follicles in vitro. J. Endocrinol. 140 (1994) 437-443
48. Su Y.Q., Wigglesworth K., Pendola F.L., O'Brien M.J., and Eppig J.J. Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143 (2002) 2221-2232
49. Tai C.J., Kang S.K., Tzeng C.R., and Leung P.C. Adenosine triphosphate activates mitogen-activated protein kinase in human granulose-luteal cells. Endocrinology 142 (2001) 1554-1560
50. Tajima K., Dantes A., Yao Z., Sorokina K., Kotsuji F., Seger R., and Amsterdam A. Down-regulation of steroidogenic response to gonadotropins in human and rat preovulatory granulosa cells involves mitogen-activated protein kinase activation and modulation of DAX-1 and steroidogenic factor-1. J. Clin. Endocrinol. Metab. 88 (2003) 2288-2299
51. Tano M., Minegishi T., Nakamura K., Karino S., Ibuki Y., and Miyamoto K. Transcriptional and post-transcriptional regulation of FSH receptor in rat granulosa cells by cyclic AMP and activin. J. Endocrinol. 153 (1997) 465-473
52. Tetsuka M., and Hillier S.G. Androgen receptor gene expression in rat granulosa cells: the role of follicle-stimulating hormone and steroid hormones. Endocrinology 137 (1996) 4392-4397
53. Tetsuka M., Whitelaw P.F., Bremner W.J., Millar M.R., Smyth C.D., and Hillier S.G. Developmental regulation of androgen receptor in rat ovary. J. Endocrinol. 145 (1995) 535-543
54. Tilly J.L., LaPolt P.S., and Hsueh A.J. Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 130 (1992) 1296-1302
55. Ulloa-Aguirre A., Midgley Jr. A.R., Beitins I.Z., and Padmanabhan V. Follicle-stimulating isohormones: characterization and physiological relevance. Endocr. Rev. 16 (1995) 765-787
56. von Bubnoff A., and Cho K.W. Intracellular BMP signaling regulation in vertebrates: pathway or network?. Dev. Biol. 239 (2001) 1-14
57. Wang H., Andoh K., Hagiwara H., Xiaowei L., Kikuchi N., Abe Y., Yamada K., Fatima R., and Mizunuma H. Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice. Endocrinology 142 (2001) 4930-4936
58. Weil S., Vendola K., Zhou J., and Bondy C.A. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J. Clin. Endocrinol. Metab. 84 (1999) 2951-2956
59. Woodruff T.K., and Mather J.P. Inhibin, activin and the female reproductive axis. Annu. Rev. Physiol. 57 (1995) 219-244
60. Wrathall J.H., and Knight P.G. Effects of inhibin-related peptides and oestradiol on androstenedione and progesterone secretion by bovine theca cells in vitro. J. Endocrinol. 145 (1995) 491-500
61. Xiao S., Robertson D.M., and Findlay J.K. Effects of activin and follicle-stimulating hormone (FSH)-suppressing protein/follistatin on FSH receptors and differentiation of cultured rat granulosa cells. Endocrinology 131 (1992) 1009-1016
62. Yazawa T., Mizutani T., Yamada K., Kawata H., Sekiguchi T., Yoshino M., Kajitani T., Shou Z., and Miyamoto K. Involvement of cyclic adenosine 5′-monophosphate response element-binding protein, steroidogenic factor 1, and Dax-1 in the regulation of gonadotropin-inducible ovarian transcription factor 1 gene expression by follicle-stimulating hormone in ovarian granulosa cells. Endocrinology 144 (2003) 1920-1930
63. Ying S.Y., Czvik J., Becker A., Ling N., Ueno N., and Guillemin R. Secretion of follicle-stimulating hormone and production of inhibin are reciprocally related. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 4631-4635
64. Yu F.Q., Han C.S., Yang W., Jin X., Hu Z.Y., and Liu Y.X. Activation of the p38 MAPK pathway by follicle-stimulating hormone regulates steroidogenesis in granulosa cells differentially. J. Endocrinol. 186 (2005) 85-96
65. Zazopoulos E., Lalli E., Stocco D.M., and Sassone-Corsi P. DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature 390 (1997) 311-315