PPARγ co-activator-1α co-activates steroidogenic factor 1 to stimulate the synthesis of luteinizing hormone and aldosterone

Biochemical Journal

Volumn 432, Issue 3, 2010, Pages 473-483

  Zhu, Liuluan ^a,b   Ke, Yaojun ^c   Shao, Di ^a   Cui, Ying ^a   Qiao, Aijun ^a   Liu, Xiaojun ^a   Fang, Fude ^a   Chang, Yongsheng ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c WUHAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Gene expression; Luteinizing hormone; Pituitary; Steroidogenesis; Transcription

Indexed keywords

ADRENAL GLAND; ALDOSTERONE SYNTHASE; BINDING ELEMENTS; CHROMATIN IMMUNOPRECIPITATION ASSAY; CO-ACTIVATION; CO-IMMUNOPRECIPITATION ASSAYS; GLUTATHIONE TRANSFERASE; HYDROXYLASES; IN-VITRO; IN-VIVO; LUTEINIZING HORMONE; NUCLEAR RECEPTORS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PITUITARY; PROMOTER REGION; SEX DIFFERENTIATION; SF-1 (STEROIDOGENIC FACTOR 1); SIDE-CHAIN; SMALL INTERFERING RNA; STEROIDOGENESIS;

CHEMICAL ACTIVATION; CYTOLOGY; ENZYME INHIBITION; GENES; MAMMALS; RNA;

TRANSCRIPTION;

ALDOSTERONE; ALDOSTERONE SYNTHASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); GLUTATHIONE TRANSFERASE; GLYCOPHORIN A; GONADOTROPIN; LUTEINIZING HORMONE BETA SUBUNIT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SMALL INTERFERING RNA; STEROID 11BETA MONOOXYGENASE; STEROIDOGENIC FACTOR 1;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; GONAD DEVELOPMENT; HORMONE SYNTHESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; SEX DIFFERENTIATION; STEROIDOGENESIS;

ADRENAL CORTEX; ALDOSTERONE; ALDOSTERONE SYNTHASE; ANIMALS; CELL LINE; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GENE EXPRESSION REGULATION; GENES, REPORTER; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; LUTEINIZING HORMONE; LUTEINIZING HORMONE, BETA SUBUNIT; MICE; PITUITARY GLAND; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, SMALL INTERFERING; STEROID 11-BETA-HYDROXYLASE; STEROIDOGENIC FACTOR 1; TRANS-ACTIVATORS;

MAMMALIA;

EID: 78649829460     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100460     Document Type: Article

References (45)

1. Finck, B. N. and Kelly, D. P. (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116, 615-622
2. Puigserver, P. and Spiegelman, B. M. (2003) Peroxisome proliferator-activated receptor-γ coactivator 1 α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90
3. Schreiber, S. N., Knutti, D., Brogli, K., Uhlmann, T. and Kralli, A. (2003) The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor α (ERRα). J. Biol. Chem. 278, 9013-9018 (Pubitemid 36800379)
4. Huss, J. M., Kopp, R. P. and Kelly, D. P. (2002) Peroxisome proliferator-activated receptor coactivator-1α (PGC-1α) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and -γ . Identification of novel leucine-rich interaction motif within PGC-1α. J. Biol. Chem. 277, 40265-40274
5. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M. and Spiegelman, B. M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839
6. Vega, R. B., Huss, J. M. and Kelly, D. P. (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20, 1868-1876
7. Puigserver, P., Rhee, J., Donovan, J., Walkey, C. J., Yoon, J. C., Oriente, F., Kitamura, Y., Altomonte, J., Dong, H., Accili, D. and Spiegelman, B. M. (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423, 550-555
8. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C. and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124
9. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C. Y., Mootha, V. K., Jager, S., Vianna, C. R., Reznick, R. M. et al. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119, 121-135
10. Leone, T. C., Lehman, J. J., Finck, B. N., Schaeffer, P. J., Wende, A. R., Boudina, S., Courtois, M., Wozniak, D. F., Sambandam, N., Bernal-Mizrachi, C. et al. (2005) PGC-1α deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101
11. Lin, J., Handschin, C. and Spiegelman, B. M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370
12. Hoivik, E. A., Lewis, A. E., Aumo, L. and Bakke, M. (2010) Molecular aspects of steroidogenic factor 1 (SF-1). Mol. Cell. Endocrinol. 315, 27-39
13. Parker, K. L. and Schimmer, B. P. (1997) Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18, 361-377
14. Jorgensen, J. S., Quirk, C. C. and Nilson, J. H. (2004) Multiple and overlapping combinatorial codes orchestrate hormonal responsiveness and dictate cell-specific expression of the genes encoding luteinizing hormone. Endocr. Rev. 25, 521-542
15. Halvorson, L. M., Kaiser, U. B. and Chin, W. W. (1996) Stimulation of luteinizing hormone β gene promoter activity by the orphan nuclear receptor, steroidogenic factor-1. J. Biol. Chem. 271, 6645-6650
16. Keri, R. A. and Nilson, J. H. (1996) A steroidogenic factor-1 binding site is required for activity of the luteinizing hormone β subunit promoter in gonadotropes of transgenic mice. J. Biol. Chem. 271, 10782-10785
17. Ingraham, H. A., Lala, D. S., Ikeda, Y., Luo, X., Shen, W. H., Nachtigal, M. W., Abbud, R., Nilson, J. H. and Parker, K. L. (1994) The nuclear receptor steroidogenic factor 1 acts at multiple levels of the reproductive axis. Genes Dev. 8, 2302-2312
18. Sadovsky, Y. and Dorn, C. (2000) Function of steroidogenic factor 1 during development and differentiation of the reproductive system. Rev. Reprod. 5, 136-142
19. Mornet, E., Dupont, J., Vitek, A. and White, P. C. (1989) Characterization of two genes encoding human steroid 11β-hydroxylase [P-450(11)β]. J. Biol. Chem. 264, 20961-20967
20. Clyne, C. D., Zhang, Y., Slutsker, L., Mathis, J. M., White, P. C. and Rainey, W. E. (1997) Angiotensin II and potassium regulate human CYP11B2 transcription through common cis-elements. Mol. Endocrinol. 11, 638-649
21. Sadovsky, Y., Crawford, P. A., Woodson, K. G., Polish, J. A., Clements, M. A., Tourtellotte, L. M., Simburger, K. and Milbrandt, J. (1995) Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 side-chain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc. Natl. Acad. Sci. U.S.A. 92, 10939-10943
22. Crawford, P. A., Polish, J. A., Ganpule, G. and Sadovsky, Y. (1997) The activation function-2 hexamer of steroidogenic factor-1 is required, but not sufficient for potentiation by SRC-1. Mol. Endocrinol. 11, 1626-1635
23. Ito, M., Yu, R. N. and Jameson, J. L. (1998) Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol. Endocrinol. 12, 290-301
24. Gizard, F., Lavallee, B., DeWitte, F., Teissier, E., Staels, B. and Hum, D. W. (2002) The transcriptional regulating protein of 132 kDa (TReP-132) enhances P450scc gene transcription through interaction with steroidogenic factor-1 in human adrenal cells. J. Biol. Chem. 277, 39144-39155
25. Grasfeder, L. L., Gaillard, S., Hammes, S. R., Ilkayeva, O., Newgard, C. B., Hochberg, R. B., Dwyer, M. A., Chang, C. Y. and McDonnell, D. P. (2009) Fasting-induced hepatic production of DHEA is regulated by PGC-1α, ERRα, and HNF4α. Mol. Endocrinol. 23, 1171-1182
26. Kong, X., Fan, H., Liu, X., Wang, R., Liang, J., Gupta, N., Chen, Y., Fang, F. and Chang, Y. (2009) Peroxisome proliferator-activated receptor γ coactivator-1α enhances antiproliferative activity of 5′-deoxy-5-fluorouridine in cancer cells through induction of uridine phosphorylase. Mol. Pharmacol. 76, 854-860
27. Rui, X., Tsao, J., Scheys, J. O., Hammer, G. D. and Schimmer, B. P. (2008) Contributions of specificity protein-1 and steroidogenic factor 1 to Adcy4 expression in Y1 mouse adrenal cells. Endocrinology 149, 3668-3678
28. Gao, X., Pan, W. S., Dai, H., Zhang, Y., Wu, N. H. and Shen, Y. F. (2010) CARM1 activates myogenin gene via PCAF in the early differentiation of TPA-induced rhabdomyosarcoma-derived cells. J. Cell. Biochem. 110, 162-170
29. Mouillet, J. F., Sonnenberg-Hirche, C., Yan, X. and Sadovsky, Y. (2004) p300 regulates the synergy of steroidogenic factor-1 and early growth response-1 in activating luteinizing hormone-β subunit gene. J. Biol. Chem. 279, 7832-7839
30. Jameson, L., Chin, W. W., Hollenberg, A. N., Chang, A. S. and Habener, J. F. (1984) The gene encoding the beta-subunit of rat luteinizing hormone. Analysis of gene structure and evolution of nucleotide sequence. J. Biol. Chem. 259, 15474-15480
31. Talmadge, K., Vamvakopoulos, N. C. and Fiddes, J. C. (1984) Evolution of the genes for the β subunits of human chorionic gonadotropin and luteinizing hormone. Nature 307, 37-40
32. Virgin, J. B., Silver, B. J., Thomason, A. R. and Nilson, J. H. (1985) The gene for the β subunit of bovine luteinizing hormone encodes a gonadotropin mRNA with an unusually short 5′-untranslated region. J. Biol. Chem. 260, 7072-7077
33. Kanaya, E., Shiraki, T. and Jingami, H. (2004) The nuclear bile acid receptor FXR is activated by PGC-1α in a ligand-dependent manner. Biochem. J. 382, 913-921
34. Tcherepanova, I., Puigserver, P., Norris, J. D., Spiegelman, B. M. and McDonnell, D. P. (2000) Modulation of estrogen receptor-α transcriptional activity by the coactivator PGC-1. J. Biol. Chem. 275, 16302-16308
35. Liu, Z. and Simpson, E. R. (1997) Steroidogenic factor 1 (SF-1) and SP1 are required for regulation of bovine CYP11A gene expression in bovine luteal cells and adrenal Y1 cells. Mol. Endocrinol. 11, 127-137
36. Wang, X. L., Bassett, M., Zhang, Y., Yin, S., Clyne, C., White, P. C. and Rainey, W. E. (2000) Transcriptional regulation of human 11β-hydroxylase (hCYP11B1). Endocrinology 141, 3587-3594
37. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., St Pierre, J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N. et al. (2004) Erra and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U.S.A. 101, 6570-6575
38. Salisbury, T. B., Binder, A. K., Grammer, J. C. and Nilson, J. H. (2007) Maximal activity of the luteinizing hormone β-subunit gene requires β-catenin. Mol. Endocrinol. 21, 963-971
39. Delerive, P., Wu, Y., Burris, T. P., Chin, W. W. and Suen, C. S. (2002) PGC-1 functions as a transcriptional coactivator for the retinoid X receptors. J. Biol. Chem. 277, 3913-3917
40. Knutti, D., Kaul, A. and Kralli, A. (2000) A tissue-specific coactivator of steroid receptors, identified in a functional genetic screen. Mol. Cell. Biol. 20, 2411-2422
41. Forrest, M. J., Bloomfield, D., Briscoe, R. J., Brown, P. N., Cumiskey, A. M., Ehrhart, J., Hershey, J. C., Keller, W. J., Ma, X., McPherson, H. E. et al. (2008) Torcetrapib-induced blood pressure elevation is independent of CETP inhibition and is accompanied by incresed circulating levels of aldosterone. Br. J. Pharmacol. 154, 1465-1473
42. Laganiere, J., Tremblay, G. B., Dufour, C. R., Giroux, S., Rousseau, F. and Giguere, V. (2004) A polymorphic autoregulatory hormone response element in the human estrogen-related receptor α (ERRα) promoter dictates peroxisome proliferator-activated receptor γ coactivator-1α control of ERRα expression. J. Biol. Chem. 279, 18504-18510
43. Shen, J. H. and Ingraham, H. A. (2002) Regulation of the orphan nuclear receptor steroidogenic factor 1 by Sox proteins. Mol. Endocrinol. 16, 529-540
44. Kawakami, Y., Tsuda, M., Takahashi, S., Taniguchi, N., Esteban, C. R., Zemmyo, M., Furumatsu, T., Lotz, M., Belmonte, J. C. and Asahara, H. (2005) Transcriptional coactivator PGC-1α regulates chondrogenesis via association with Sox9. Proc. Natl. Acad. Sci. U.S.A. 102, 2414-2419
45. Yazawa, T., Inaoka, Y., Okada, R., Mizutani, T., Yamazaki, Y., Usami, Y., Kuribayashi, M., Orisaka, M., Umezawa, A. and Miyamoto, K. (2010) PPAR-γ coactivator-1α regulates progesterone production in ovarian granulosa cells with SF-1 and LRH-1. Mol. Endocrinol. 24, 485-496