Epidermal growth factor-mediated inhibition of follicle-stimulating hormone-stimulated StAR gene expression in porcine granulosa cells is associated with reduced histone H3 acetylation

Biology of Reproduction

Volumn 72, Issue 4, 2005, Pages 862-871

  Rusovici, Raluca ^a   Hui, Yvonne Y ^a   LaVoie, Holly A ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Follicle stimulating hormone; Granulosa cells; Growth factors; Steroid hormones

Indexed keywords

EPIDERMAL GROWTH FACTOR; FOLLITROPIN; HISTONE H3; MESSENGER RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASE PAIRING; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GRANULOSA CELL; IMMUNOPRECIPITATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; RNA STABILITY; STEROIDOGENESIS; SWINE;

ACETYLATION; ANIMALS; CELLS, CULTURED; DRUG INTERACTIONS; EPIDERMAL GROWTH FACTOR; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GRANULOSA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HISTONE DEACETYLASES; HISTONES; PHOSPHOPROTEINS; SWINE; TRANSCRIPTION, GENETIC;

SUIDAE;

EID: 15544364247     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.034298     Document Type: Article

References (61)

1. Gore-Langton RE, Armstrong DT. Follicular steroidogenesis. In: Knobil E, Neill JD (eds.). The Physiology of Reproduction, 2nd ed. New York: Raven Press, Ltd.; 1994:571-627.
2. Grummer RR, Carroll DJ. A review of lipoprotein cholesterol metabolism: importance to ovarian function. J Anim Sci 1988; 66:3160-3173.
3. Kiriakidou M, McAllister JM, Sugawara T, Strauss JF III. Expression of steroidogenic acute regulatory protein (StAR) in the human ovary. J Clin Endo Metab 1996; 81:4122-4128.
4. Farkash Y, Timberg R, Orly J. Preparation of antiserum to rat cytochrome P-450 cholesterol side chain cleavage, and its use for ultrastructural localization of the immunoreactive enzyme by protein A-gold technique. Endocrinology 1986; 118:1353-1365.
5. Oonk RB, Krasnow JS, Beattie WG, Richards JS. Cyclic AMP-dependent and -independent regulation of cholesterol side chain cleavage cytochrome P-450 (P-450scc) in rat ovarian granulosa cells and corpora lutea. cDNA and deduced amino acid sequence of rat P-450scc. J Biol Chem 1989; 264:21934-21942.
6. La Voie HA, Benoit AM, Garmey JC, Dailey RA, Wright DJ, Veldhuis JD. Coordinate developmental expression of genes regulating sterol economy and cholesterol side-chain cleavage in the porcine ovary. Biol Reprod 1997; 57:402-407.
7. Pescador N, Houde A, Stocco DM, Murphy BD. Follicle-stimulating hormone and intracellular second messengers regulate steroidogenic acute regulatory protein messenger ribonucleic acid in luteinized porcine granulosa cells. Biol Reprod 1997; 57:660-668.
8. Balasubramanian K, LaVoie HA, Garmey JC, Stocco DM, Veldhuis JD. Regulation of porcine granulosa cell steroidogenic acute regulatory protein (StAR) by insulin-like growth factor I: synergism with follicle-stimulating hormone or protein kinase A agonist. Endocrinology 1997; 138:433-439.
9. Stocco DM. Tracking the role of a StAR in the sky of the new millennium. Mol Endocrinol 2001; 15:1245-1254.
10. Christenson LK, Johnson PF, McAllister JM, Strauss JF. CCAAT/enhancer-binding proteins regulate expression of the human steroidogenic acute regulatory protein (StAR) gene. J Biol Chem 1999; 274: 26591-26598.
11. Silverman E, Eimerl S, Orly J. CCAAT enhancer-binding protein beta and GATA-4 binding regions within the promoter of the steroidogenic acute regulatory protein (StAR) gene are required for transcription in rat ovarian cells. J Biol Chem 1999; 274:17987-17996.
12. LaVoie HA, Singh D, Hui YY. Concerted regulation of the porcine StAR gene promoter activity by FSH and IGF-I in granulosa cells involves GATA-4 and CCAAT/enhancer binding protein beta. Endocrinology 2004; 145:3122-3134.
13. Sugawara T, Kiriakidou M, McAllister JM, Kallen CB, Strauss JF III. Multiple steroidogenic factor 1 binding elements in the human steroidogenic acute regulatory protein gene 5′-flanking region are required for maximal promoter activity and cyclic AMP responsiveness. Biochemistry 1997; 36:7249-7255.
14. Hiroi H, Christenson LK, Chang L, Sammel MD, Berger SL, Strauss JF III. Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (StAR) locus associated with StAR transcription. Mol Endocrinol 2004; 18:791-806.
15. Christenson LK, Stouffer RL, Strauss JF III. Quantitative analysis of the hormone-induced hyperacetylation of histone H3 associated with the steroidogenic acute regulatory protein gene promoter. J Biol Chem 2001; 276:27392-27399.
16. Cardenas H, Pope WF. Androgen receptor and follicle-stimulating hormone receptor in the pig ovary during the follicular phase of the estrous cycle. Mol Reprod Dev 2002; 62:92-98.
17. Guthrie HD, Barber JA, Leighton JK, Hammond JM. Steroidogenic cytochrome P450 enzyme messenger ribonucleic acids and follicular fluid steroids in individual follicles during preovulatory maturation in the pig. Biol Reprod 1994; 51:465-471.
18. Conley AJ, Howard HJ, Slanger WD, Ford JJ. Steroidogenesis in the preovulatory porcine follicle. Biol Reprod 1994; 51:655-661.
19. Urban RJ, Veldhuis JD. Endocrine control of steroidogenesis in granulosa cells. Oxf Rev Reprod Biol 1992; 14:225-262.
20. Singh B, Rutledge JM, Armstrong DT. Epidermal growth factor and its receptor gene expression and peptide localization in porcine ovarian follicles. Mol Reprod Dev 1995; 40:391-399.
21. Fujinaga H, Yamoto M, Nakano R, Shima K. Epidermal growth factor binding sites in porcine granulosa cells and their regulation by follicle-stimulating hormone. Biol Reprod 1992; 46:705-709.
22. Gospodarowicz D, Bialecki H. Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology 1979; 104:757-764.
23. Endo K, Atlas SJ, Rone JD, Zanagnolo VL, Kuo TC, Dharmarajan AM, Wallach EE. Epidermal growth factor inhibits follicular response to human chorionic gonadotropin: possible role of cell to cell communication in the response to gonadotropin. Endocrinology 1992; 130:186-192.
24. Pescador N, Stocco DM, Murphy BD. Growth factor modulation of steroidogenic acute regulatory protein and luteinization in the pig ovary. Biol Reprod 1999; 60:1453-1461.
25. Steinkampf MP, Mendelson CR, Simpson ER. Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells. Mol Cell Endocrinol 1988; 59:93-99.
26. Mondschein JS, Schomberg DW. Growth factors modulate gonadotropin receptor induction in granulosa cell cultures. Science 1981; 211: 1179-1180.
27. Knecht M, Catt K. Epidermal growth factor and gonadotropin-releasing hormone inhibit cyclic AMP-dependent luteinizing hormone receptor formation in ovarian granulosa cells. J Cell Biochem 1983; 21: 209-217.
28. Garmey JC, Day RN, Day KH, Veldhuis JD. Mechanisms of regulation of ovarian sterol metabolism by insulin-like growth factor type II (IGF-II): in vitro studies with swine granulosa cells. Endocrinology 1993; 133:800-808.
29. LaVoie HA, Garmey JC, Veldhuis JD. Mechanisms of insulin-like growth factor I augmentation of FSH-induced porcine steroidogenic acute regulatory protein gene promoter activity in granulosa cells. Endocrinology 1999; 140:146-153.
30. Zhang G, Garmey JC, Veldhuis JD. Interactive stimulation by luteinizing hormone and insulin of the steroidogenic acute regulatory (StAR) protein and 17alpha-hydroxylase/17,20-lyase (CYP17) genes in porcine theca cells. Endocrinology 2000; 141:2735-2742.
31. LaVoie HA, DeSimone DC, Gillio-Meina C, Hui YY. Cloning and characterization of porcine ovarian estrogen receptor beta isoforms. Biol Reprod 2002; 66:616-623.
32. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45.
33. LaVoie HA, Garmey JC, Day RN, Veldhuis JD. Concerted regulation of the low density lipoprotein receptor gene expression by FSH and IGF-I in porcine granulosa cells: promoter activation, mRNA stability, and sterol feedback. Endocrinology 1999; 140:178-186.
34. Urban RJ, Shupnik MA, Bodenburg YH. Insulin-like growth factor-I increases expression of the porcine P-450 cholesterol side chain cleavage gene through a GC-rich domain. J Biol Chem 1994; 269:25761-25769.
35. Hunzicker-Dunn M. Selective activation of rabbit ovarian protein kinase isozymes in rabbit ovarian follicles and corpora lutea. J Biol Chem 1981; 256:12185-12193.
36. Westergaard LG, Yding AC, Byskov AG. Epidermal growth factor in small antral ovarian follicles of pregnant women. J Endocrinol 1990; 127:363-367.
37. Eden JA, Jones J, Carter GD, Alaghband-Zadeh J. Follicular fluid concentrations of insulin-like growth factor 1, epidermal growth factor, transforming growth factor-alpha and sex-steroids in volume matched normal and polycystic human follicles. Clin Endocrinol (Oxf) 1990; 32:395-405.
38. Johnson AL, Bridgham JT. Regulation of steroidogenic acute regulatory protein and luteinizing hormone receptor messenger ribonucleic acid in hen granulosa cells. Endocrinology 2001; 142:3116-3124.
39. Minegishi T, Tsuchiya M, Hirakawa T, Abe K, Inoue K, Mizutani T, Miyamoto K. Expression of steroidogenic acute regulatory protein (StAR) in rat granulosa cells. Life Sci 2000; 67:1015-1024.
40. Elferink CJ, Reiners JJ Jr. Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 1996; 20:470-477.
41. Smith CL, Hager GL. Transcriptional regulation of mammalian genes in vivo. A tale of two templates. J Biol Chem 1997; 272:27493-27496.
42. Goffin J, Eisenhauer E. DNA methyltransferase inhibitors-state of the art. Ann Oncol 2002; 13:1699-1716.
43. Urban RJ, Garmey JC, Shupnik MA, Veldhuis JD. Insulin-like growth factor type I increases concentrations of messenger ribonucleic acid encoding cytochrome P450 cholesterol side-chain cleavage enzyme in primary cultures of porcine granulosa cells. Endocrinology 1990; 127: 2481-2488.
44. Manna PR, Huhtaniemi IT, Wang XJ, Eubank DW, Stocco DM. Mechanisms of epidermal growth factor signaling: regulation of steroid biosynthesis and the steroidogenic acute regulatory protein in mouse Leydig tumor cells. Biol Reprod 2002; 67:1393-1404.
45. Galway AB, Oikawa M, Ny T, Hsueh AJ. Epidermal growth factor stimulates tissue plasminogen activator activity and messenger ribonucleic acid levels in cultured rat granulosa cells: mediation by pathways independent of protein kinases-A and -C. Endocrinology 1989; 125:126-135.
46. Makarevich AV, Sirotkin AV, Chrenek P, Bulla J. Effect of epidermal growth factor (EGF) on steroid and cyclic nucleotide secretion, proliferation and ERK-related MAP-kinase in cultured rabbit granulosa cells. Exp Clin Endocrinol Diabetes 2002; 110:124-129.
47. Knecht M, Catt KJ. Modulation of cAMP-mediated differentiation in ovarian granulosa cells by epidermal growth factor and platelet-derived growth factor. J Biol Chem 1983; 258:2789-2794.
48. Tilly JL, Lapolt PS, Hsueh AJ. Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 1992; 130:1296-1302.
49. 125I]iodo-follicle-stimulating hormone binding by cultured porcine granulosa cells. Endocrinology 1987; 120:2413-2420.
50. Clark BJ, Combs R, Hales KH, Hales DB, Stocco DM. Inhibition of transcription affects synthesis of steroidogenic acute regulatory protein and steroidogenesis in MA-10 mouse Leydig tumor cells. Endocrinology 1997; 138:4893-4901.
51. Stocco DM, Clark BJ, Reinhart AJ, Williams SC, Dyson M, Dassi B, Walsh LP, Manna PR, Wang XJ, Zeleznik AJ, Orly J. Elements involved in the regulation of the StAR gene. Mol Cell Endocrinol 2001; 177:55-59.
52. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074-1080.
53. Kuo MH, Allis CD. In vivo cross-linking and immunoprecipitation for studying dynamic protein:DNA associations in a chromatin environment. Methods 1999; 19:425-433.
54. Flores JA, Garmey JC, Nestler JE, Veldhuis JD. Sites of inhibition of steroidogenesis by activation of protein kinase-C in swine ovarian (granulosa) cells. Endocrinology 1993; 132:1983-1990.
55. Tsubaki J, Choi WK, Ingermann AR, Twigg SM, Kim HS, Rosenfeld RG, Oh Y. Effects of sodium butyrate on expression of members of the IGF-binding protein superfamily in human mammary epithelial cells. J Endocrinol 2001; 169:97-110.
56. Antos CL, McKinsey TA, Dreitz M, Hollingsworth LM, Zhang CL, Schreiber K, Rindt H, Gorczynski RJ, Olson EN. Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem 2003; 278:28930-28937.
57. Salvador LM, Park Y, Cottom J, Maizels ET, Jones JC, Schillace RV, Carr DW, Cheung P, Allis CD, Jameson JL, Hunzicker-Dunn M. Follicle-stimulating hormone stimulates protein kinase A-mediated histone H3 phosphorylation and acetylation leading to select gene activation in ovarian granulosa cells. J Biol Chem 2001; 276:40146-40155.
58. Bendell JJ, Dorrington JH. Epidermal growth factor influences growth and differentiation of rat granulosa cells. Endocrinology 1990; 127: 533-540.
59. Hsueh AJ, Welsh TH, Jones PB. Inhibition of ovarian and testicular steroidogenesis by epidermal growth factor. Endocrinology 1981; 108: 2002-2004.
60. Dorrington JH, Bendell JJ, Lobb DK. Aromatase activity in granulosa cells: regulation by growth factors. Steroids 1987; 50:411-421.
61. Keel BA, Davis JS. Epidermal growth factor activates extracellular signal-regulated protein kinases (ERK) in freshly isolated porcine granulosa cells. Steroids 1999; 64:654-658.