CREB coactivator CRTC2/TORC2 and its regulator calcineurin crucially mediate follicle-stimulating hormone and transforming growth factor β1 upregulation of steroidogenesis

Journal of Cellular Physiology

Volumn 227, Issue 6, 2012, Pages 2430-2440

  Fang, Wei Ling ^a   Lee, Ming Ting ^b   Wu, Leang Shin ^c   Chen, Yun Ju ^a,e   Mason, Jian ^d   Ke, Ferng Chun ^c   Hwang, Jiuan Jiuan ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e I SHOU UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CALCINEURIN; CRTC2 PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; FOLLITROPIN; GONADOTROPIN; PROTEIN; TORC2 PROTEIN; TRANSFORMING GROWTH FACTOR ALPHA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; GRANULOSA CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; RAT; STEROIDOGENESIS; UPREGULATION;

RATTUS;

EID: 84863170593     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22978     Document Type: Article

References (43)

1. Brown KA, McInnes KJ, Hunger NI, Oakhill JS, Steinberg GR, Simpson ER. 2009. Subcellular localization of cyclic AMP-responsive element binding protein-regulated transcription coactivator 2 provides a link between obesity and breast cancer in postmenopausal women. Cancer Res 69: 5392-5399.
2. Carnegie JA, Tsang BK. 1984. The calcium-calmodulin system: Participation in the regulation of steroidogenesis at different stages of granulosa cell differentiation. Biol Reprod 30: 515-522.
3. Chen YJ, Hsiao PW, Lee MT, Mason JI, Ke FC, Hwang JJ. 2007. Interplay of PI3K and cAMP/PKA signaling, and rapamycin-hypersensitivity in TGFbeta1 enhancement of FSH-stimulated steroidogenesis in rat ovarian granulosa cells. J Endocrinol 192: 405-419.
4. Chen YJ, Lee MT, Yao HC, Hsiao PW, Ke FC, Hwang JJ. 2008. Crucial role of estrogen receptor-alpha interaction with transcription coregulators in follicle-stimulating hormone and transforming growth factor beta1 up-regulation of steroidogenesis in rat ovarian granulosa cells. Endocrinology 149: 4658-4668.
5. Clem BF, Hudson EA, Clark BJ. 2005. Cyclic adenosine 3', 5'-monophosphate (cAMP) enhances cAMP-responsive element binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory protein gene promoter. Endocrinology 146: 1348-1356.
6. Conkright MD, Canettieri G, Screaton R, Guzman E, Miraglia L, Hogenesch JB, Montminy M. 2003. TORCs: Transducers of regulated CREB activity. Mol Cell 12: 413-423.
7. Dentin R, Liu Y, Koo SH, Hedrick S, Vargas T, Heredia J, Yates J III, Montminy M. 2007. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature 449: 366-369.
8. Dodson WC, Schomberg DW. 1987. The effect of transforming growth factor-beta on follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells. Endocrinology 120: 512-516.
9. Escamilla-Hernandez R, Little-Ihrig L, Orwig KE, Yue J, Chandran U, Zeleznik AJ. 2008. Constitutively active protein kinase A qualitatively mimics the effects of follicle-stimulating hormone on granulosa cell differentiation. Mol Endocrinol 22: 1842-1852.
10. Flores JA, Veldhuis JD, Leong DA. 1990. Follicle-stimulating hormone evokes an increase in intracellular free calcium ion concentrations in single ovarian (granulosa) cells. Endocrinology 27: 3172-3179.
11. Gitay-Goren H, Kim IC, Miggans ST, Schomberg DW. 1993. Transforming growth factor beta modulates gonadotropin receptor expression in porcine and rat granulosa cells differently. Biol Reprod 48: 1284-1289.
12. Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL, Richards JS. 2002. Follicle-Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-lnduced kinase (Sgk): Evidence for A kinase-independent signaling by FSH in granulosa cells. Mol Endocrinol 14: 1283-1300.
13. Gooch JL, Gorin Y, Zhang BX, Abboud HE. 2004. Involvement of calcineurin in transforming growth factor-beta-mediated regulation of extracellular matrix accumulation. J Biol Chem 279: 15561-15570.
14. Guo IC, Huang CY, Wang CK, Chung BC. 2007. Activating protein-1 cooperates with steroidogenic factor-1 to regulate 3', 5'-cyclic adenosine 5'-monophosphate-dependent human CYP11A1 transcription in vitro and in vivo. Endocrinology 148: 1804-1812.
15. Ingman WV, Robker RL, Woittiez K, Robertson SA. 2006. Null mutation in transforming growth factor beta1 disrupts ovarian function and causes oocyte incompetence and early embryo arrest. Endocrinology 147: 835-845.
16. Iourgenko V, Zhang W, Mickanin C, Daly I, Jiang C, Hexham JM, Orth AP, Miraglia L, Meltzer J, Garza D, Chirn GW, McWhinnie E, Cohen D, Skelton J, Terry R, Yu Y, Bodian D, Buxton FP, Zhu J, Song C, Labow MA. 2003. Identification of a family of cAMP response element-binding protein coactivators by genome-scale functional analysis in mammalian cells. Proc Natl Acad Sci USA 100: 12147-12152.
17. Jayes FC, Day RN, Garmey JC, Urban RJ, Zhang G, Veldhuis JD. 2000. Calcium ions positively modulate follicle-stimulating hormone- and exogenous cyclic 3', 5'-adenosine monophosphate-driven transcription of the P450(scc) gene in porcine granulosa cells. Endocrinology 141: 2377-2384.
18. Ke FC, Chuang LC, Lee MT, Chen YJ, Lin SW, Wang PS, Stocco DM, Hwang JJ. 2004. The modulatory role of transforming growth factor beta1 and androstenedione on follicle-stimulating hormone-induced gelatinase secretion and steroidogenesis in rat granulosa cells. Biol Reprod 70: 1292-1298.
19. Ke FC, Fang SH, Lee MT, Sheu SY, Lai SY, Chen YJ, Huang FL, Wang PS, Stocco DM, Hwang JJ. 2005. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor beta1-induced connexin43 gap junction formation and steroidogenesis in rat granulosa cells. J Endocrinol 184: 555-566.
20. Kidder GM, Mhawi AA. 2002. Gap junctions and ovarian folliculogenesis. Reproduction 123: 613-620.
21. Kuo SW, Ke FC, Chang GD, Lee MT, Hwang JJ. 2011. Potential role of follicle-stimulating hormone (FSH) and transforming growth factor (TGFβ1) in the regulation of ovarian angiogenesis. J Cell Physiol 226: 1608-1619.
22. 2+ channels in rat sertoli cells. Endocrinology 149: 1031-1037.
23. Manna PR, Dyson MT, Eubank DW, Clark BJ, Lalli E, Sassone-Corsi P, Zeleznik AJ, Stocco DM. 2002. Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol Endocrinol 16: 184-199.
24. Manna PR, Dyson MT, Stocco DM. 2009. Role of basic leucine zipper proteins in transcriptional regulation of the steroidogenic acute regulatory protein gene. Mol Cell Endocrinol 302: 1-11.
25. Mariana JC. 1997. Follicular growth and ovarian dynamics in mammals. J Reprod Fertil Suppl 51: 3-23.
26. Mayr B, Montminy M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2: 599-609.
27. McGee EA, Hsueh AJ. 2000. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21: 200-214.
28. Richards JS. 2001. Perspective: The ovarian follicle-A perspective in 2001. Endocrinology 142: 2184-2193.
29. Rosairo D, Kuyznierewicz I, Findlay J, Drummond A. 2008. Transforming growth factor-beta: Its role in ovarian follicle development. Reproduction 136: 799-809.
30. Screaton RA, Conkright MD, Katoh Y, Best JL, Canettieri G, Jeffries S, Guzman E, Niessen S, Yates JR III, Takemori H, Okamoto M, Montminy M. 2004. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119: 61-74.
31. Sher N, Yivgi-Ohana N, Orly J. 2007. Transcriptional regulation of the cholesterol side chain cleavage cytochrome P450 gene (CYP11A1) revisited: Binding of GATA, cyclic adenosine 3', 5'-monophosphate response element-binding protein and activating protein (AP)-1 proteins to a distal novel cluster of cis-regulatory elements potentiates AP-2 and steroidogenic factor-1-dependent gene expression in the rodent placenta and ovary. Mol Endocrinol 21: 948-962.
32. Spiga F, Liu Y, Aguilera G, Lightman SL. 2011. Temporal effect of adrenocorticotrophic hormone on adrenal glucocorticoid steroidogenesis: Involvement of the transducer of regulated cyclic AMP-response element-binding protein activity. J Neuroendocrinol 23: 136-142.
33. Takemori H, Kanematsu M, Kajimura J, Hatano O, Katoh Y, Lin XZ, Min L, Yamazaki T, Doi J, Okamoto M. 2007. Dephosphorylation of TORC initiates expression of the StAR gene. Mol Cell Endocrinol 265-266: 196-204.
34. Tamanini C, De Ambrogi M. 2004. Angiogenesis in developing follicle and corpus luteum. Reprod Domest Anim 39: 206-216.
35. Tsang BK, Carnegie JA. 1983. Calcium requirement in the gonadotropic regulation of rat granulosa cell progesterone production. Endocrinology 113: 763-769.
36. Tsang BK, Mattice DF, Li M, Asem EK. 1989. Influence of A23187 and dibutyryl cyclic AMP on progestagen production by rat granulosa cells in vitro. J Reprod Fertil 86: 373-381.
37. Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM. 2006. Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: Insights from basic science and clinical studies. Endocr Rev 27: 575-605.
38. Welsh TH, Jr, Zhuang LZ, Hsueh AJ. 1983. Estrogen augmentation of gonadotropin-stimulated progestin biosynthesis in cultured rat granulosa cells. Endocrinology 112: 1916-1924.
39. Wu Z, Huang X, Feng Y, Handschin C, Feng Y, Gullicksen PS, Bare O, Labow M, Spiegelman B, Stevenson SC. 2006. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc Natl Acad Sci USA 103: 14379-14384.
40. Yivgi-Ohana N, Sher N, Melamed-Book N, Eimerl S, Koler M, Manna PR, Stocco DM, Orly J. 2009. Transcription of steroidogenic acute regulatory protein in the rodent ovary and placenta: Alternative modes of cyclic adenosine 3', 5'-monophosphate dependent and independent regulation. Endocrinology 150: 977-989.
41. Zeleznik AJ, Saxena D, Little-Ihrig L. 2003. Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 144: 3985-3994.
42. Zhang ZW, Findlay JK, Carson RS, Herington AC, Burger HG. 1988. Transforming growth factor beta enhances basal and FSH-stimulated inhibin production by rat granulosa cells in vitro. Mol Cell Endocrinol 58: 161-166.
43. Zheng X, Price CA, Tremblay Y, Lussier JG, Carrière PD. 2008. Role of transforming growth factor-beta1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cells. Reproduction 136: 447-457.