DNA methylation and histone modifications are associated with repression of the inhibin α promoter in the rat corpus luteum

Endocrinology

Volumn 153, Issue 10, 2012, Pages 4905-4917

  Meldi, Kristen M ^a   Gaconnet, Georgia A ^a   Mayo, Kelly E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; DNA METHYLTRANSFERASE 3A; HISTONE; HISTONE H3; INHIBIN; INHIBIN ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CORPUS LUTEUM; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE SILENCING; HISTONE MODIFICATION; LUTEAL CELL; LUTEINIZATION; NONHUMAN; OVARY; OVULATION; PRIORITY JOURNAL; PROMOTER REGION; RAT;

ANIMALS; CORPUS LUTEUM; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GRANULOSA CELLS; HISTONES; INHIBINS; OVARY; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84866769672     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1292     Document Type: Article

References (75)

1. McRae RS, Johnston HM, Mihm M, O'Shaughnessy PJ 2005 Changes in mouse granulosa cell gene expression during early luteinization. Endocrinology 146:309-317 (Pubitemid 40063541)
2. Gilbert I, Robert C, Dieleman S, Blondin P, Sirard MA 2011 Transcriptional effect of the LH surge in bovine granulosa cells during the peri-ovulation period. Reproduction 141:193-205
3. Rao JU, Shah KB, Puttaiah J, Rudraiah M 2011 Gene expression profiling of preovulatory follicle in the buffalo cow: effects of increased IGF-I concentration on periovulatory events. PLoS ONE 6:e20754
4. Agca C, Ries JE, Kolath SJ, Kim JH, Forrester LJ, Antoniou E, Whitworth KM, Mathialagan N, Springer GK, Prather RS, Lucy MC 2006 Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132: 133-145 (Pubitemid 44123390)
5. Woodruff TK, D'Agostino J, Schwartz NB, Mayo KE 1989 Decreased inhibin gene expression in preovulatory follicles requires primary gonadotropin surges. Endocrinology 124:2193-2199 (Pubitemid 19132017)
6. Woodruff TK, D'Agostino J, Schwartz N, Mayo K 1988 Dynamic changes in inhibin messenger RNAs in rat ovarian follicles during the reproductive cycle. Science 239:1296-1299
7. Ling N, Ying SY, Ueno N, Esch F, Denoroy L, Guillemin R 1985 Isolation and partial characterization of a Mr 32,000 protein with inhibin activity from porcine follicular fluid. Proc Natl Acad Sci USA 82:7217-7221 (Pubitemid 16193713)
8. Robertson DM, Foulds LM, Leversha L, Morgan FJ, Hearn MT, Burger HG, Wettenhall RE, de Kretser DM 1985 Isolation of inhibin from bovine follicular fluid. Biochem Biophys Res Commun 126:220-226 (Pubitemid 15126611)
9. Miyamoto K, Hasegawa Y, Fukuda M, Nomura M, Igarashi M, Kangawa K, Matsuo H 1985 Isolation of porcine follicular fluid inhibin of 32K daltons. Biochem Biophys Res Commun 129:396-403 (Pubitemid 15008410)
10. Rivier J, Spiess J, McClintock R, Vaughan J, Vale W 1985 Purification and partial characterization of inhibin from porcine follicular fluid. Biochem Biophys Res Commun 133:120-127 (Pubitemid 16155336)
11. Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, Karr D, Spiess J 1986 Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321:776-779 (Pubitemid 16077904)
12. Ling N, Ying SY, Ueno N, Shimasaki S, Esch F, Hotta M, Guillemin R 1986 Pituitary FSH is released by a heterodimer of the β-subunits from the two forms of inhibin. Nature 321:779-782 (Pubitemid 16077905)
13. Schwartz NB, Channing CP 1977 Evidence for ovarian "inhibin": suppression of the secondary rise in serum follicle stimulating hormone levels in proestrous rats by injection of porcine follicular fluid. Proc Natl Acad Sci USA 74:5721-5724
14. Meunier H, Cajander SB, Roberts VJ, Rivier C, Sawchenko PE, Hsueh AJ, Vale W 1988 Rapid changes in the expression of inhibin α-, β A-, and β B-subunits in ovarian cell types during the rat estrous cycle. Mol Endocrinol 2:1352-1363 (Pubitemid 19005948)
15. Ling N, Ying SY, Ueno N, Shimasaki S, Esch F, Hotta M, Guillemin R 1986 A homodimer of the β-subunits of inhibin A stimulates the secretion of pituitary follicle stimulating hormone. Biochem Biophys Res Commun 138:1129-1137 (Pubitemid 16028517)
16. Cho BN, McMullen ML, Pei L, Yates CJ, Mayo KE 2001 Reproductive deficiencies in transgenic mice expressing the rat inhibin α-subunit gene. Endocrinology 142:4994-5004 (Pubitemid 33022376)
17. McMullen ML, Cho BN, Yates CJ, Mayo KE 2001 Gonadal pathologies in transgenic mice expressing the rat inhibin α-subunit. Endocrinology 142:5005-5014 (Pubitemid 33022377)
18. Woodruff TK, Ackland J, Rahal JO, Schwartz NB, Mayo KE 1991 Expression of ovarian inhibin during pregnancy in the rat. Endocrinology 128:1647-1654
19. Rodgers RJ, Stuchbery SJ, Findlay JK 1989 Inhibin mRNAs in ovine and bovine ovarian follicles and corpora lutea throughout the estrous cycle and gestation. Mol Cell Endocrinol 62:95-101 (Pubitemid 19070498)
20. Bramley TA, Menzies GS, Baxter G, Webb R, McNeilly AS 1992 Apparent α-inhibin subunit immunoactivity in porcine and ovine luteal extracts is due to interference by cytosolic proteases in the assay. J Endocrinol 134:341-352
21. Weck J, Mayo KE 2006 Switching of NR5A proteins associated with the inhibin α-subunit gene promoter after activation of the gene in granulosa cells. Mol Endocrinol 20:1090-1103
22. Ito M, Park Y, Weck J, Mayo KE, Jameson JL 2000 Synergistic activation of the inhibin α-promoter by steroidogenic factor-1 and cyclic adenosine 3′,5′-monophosphate. Mol Endocrinol 14:66-81 (Pubitemid 32260328)
23. Pei L, Dodson R, Schoderbek WE, Maurer RA, Mayo KE 1991 Regulation of the α inhibin gene by cyclic adenosine 3′,5′-monophosphate after transfection into rat granulosa cells. Mol Endocrinol 5:521-534
24. Mukherjee A, Park-Sarge OK, Mayo KE 1996 Gonadotropins induce rapid phosphorylation of the 3′,5′-cyclic adenosine monophosphate response element binding protein in ovarian granulosa cells. Endocrinology 137:3234-3245 (Pubitemid 26250169)
25. Mukherjee A, Urban J, Sassone-Corsi P, Mayo KE 1998 Gonadotropins regulate inducible cyclic adenosine 3′,5′-monophosphate early repressor in the rat ovary: implications for inhibin α subunit gene expression. Mol Endocrinol 12:785-800 (Pubitemid 30659052)
26. Burkart AD, Mukherjee A, Mayo KE 2006 Mechanism of repression of the inhibin α-subunit gene by inducible 3′,5′-cyclic adenosine monophosphate early repressor. Mol Endocrinol 20:584-597 (Pubitemid 43291210)
27. Burkart A, Mukherjee A, Sterneck E, Johnson P, Mayo K 2005 Repression of the inhibin α subunit gene by the transcription factor CCAAT/enhancer binding protein β (C/EBPβ). Endocrinology 146:1909-1921 (Pubitemid 40396900)
28. Jones PA, Gonzalgo ML 1997 Altered DNA methylation and genome instability: a new pathway to cancer? Proc Natl Acad Sci USA 94:2103-2105 (Pubitemid 27136834)
29. Li E, Bestor TH, Jaenisch R 1992 Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926
30. Li E, Beard C, Jaenisch R 1993 Role for DNA methylation in genomic imprinting. Nature 366:362-365 (Pubitemid 23349366)
31. Kim MS, Kondo T, Takada I, Youn MY, Yamamoto Y, Takahashi S, Matsumoto T, Fujiyama S, Shirode Y, Yamaoka I, Kitagawa H, Takeyama K, Shibuya H, Ohtake F, Kato S 2009 DNA demethylation in hormone-induced transcriptional derepression. Nature 461:1007-1012
32. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE 2003 DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302:890-893 (Pubitemid 37339633)
33. Barrès R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, Caidahl K, Krook A, O'Gorman DJ, Zierath JR 2012 Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 15:405-411
34. Balanathan P, Ball EM, Wang H, Harris SE, Shelling AN, Risbridger GP 2004 Epigenetic regulation of inhibin α-subunit gene in prostate cancer cell lines. J Mol Endocrinol 32:55-67 (Pubitemid 38312621)
35. Schmitt JF, Millar DS, Pedersen JS, Clark SL, Venter DJ, Frydenberg M, Molloy PL, Risbridger GP 2002 Hypermethylation of the inhibin α-subunit gene in prostate carcinoma. Mol Endocrinol 16:213-220 (Pubitemid 34131220)
36. Kim YI, Shim J, Kim BH, Lee SJ, Lee HK, Cho C, Cho BN 2012 Transcriptional silencing of the inhibin-α gene in human gastric carcinoma cells. Int J Oncol 41:690-700
37. Salvador LM, Park Y, Cottom J, Maizels ET, Jones JC, Schillace RV, Carr DW, Cheung P, Allis CD, Jameson JL, Hunzicker-Dunn M 2001 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 276:40146-40155
38. Gonzalez-Robayna IJ, Alliston TN, Buse P, Firestone GL, Richards JS 1999 Functional and subcellular changes in the A-kinase-signaling pathway: relation to aromatase and Sgk expression during the transition of granulosa cells to luteal cells. Mol Endocrinol 13:1318-1337 (Pubitemid 30645289)
39. Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL, Richards JS 2000 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 (Pubitemid 32260488)
40. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K 2007 High-resolution profiling of histone methylations in the human genome. Cell 129:823-837 (Pubitemid 46802390)
41. Li BZ, Huang Z, Cui QY, Song XH, Du L, Jeltsch A, Chen P, Li G, Li E, Xu GL 2011 Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res 21:1172-1181
42. Myers M, Middlebrook BS, Matzuk MM, Pangas SA 2009 Loss of inhibin α uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis. Dev Biol 334:458-467
43. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A 1992 α-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313-319 (Pubitemid 23000668)
44. Seok OS, Ahn JM, Mayo KE, ChoBN2004 Developmental changes in inhibin-α gene expression in the mouse testis. Mol Cells 17:67-72 (Pubitemid 39137047)
45. Vanselow J, Spitschak M, Nimz M, Fürbass R 2010 DNA methylation is not involved in preovulatory down-regulation of CYP11A1, HSD3B1, and CYP19A1 in bovine follicles but may have a role in permanent silencing of CYP19A1 in large granulosa lutein cells. Biol Reprod 82:289-298
46. Stocco C, Kwintkiewicz J, Cai Z 2007 Identification of regulatory elements in the Cyp19 proximal promoter in rat luteal cells. J Mol Endocrinol 39:211-221 (Pubitemid 350047643)
47. Spitschak M, Vanselow J 2012 Bovine large luteal cells show increasing de novo DNA methylation of the main ovarian CYP19A1 promoter P2. Gen Comp Endocrinol 178:37-45
48. Monga R, Ghai S, Datta TK, Singh D 2011 Tissue-specific promoter methylation and histone modifications regulate CYP19 gene expression during folliculogenesis and luteinization in buffalo ovary. Gen Comp Endocrinol 173:205-215
49. Fürbass R, Selimyan R, Vanselow J 2008 DNA methylation and chromatin accessibility of the proximal Cyp 19 promoter region 1.5/2 correlate with expression levels in sheep placentomes. Mol Reprod Dev 75:1-7 (Pubitemid 350223984)
50. Demura M, Bulun SE 2008 CpG dinucleotide methylation of the CYP19 I. 3/II promoter modulates cAMP-stimulated aromatase activity. Mol Cell Endocrinol 283:127-132
51. Ghai S, Monga R, Mohanty TK, Chauhan MS, Singh D 2010 Tissue-specific promoter methylation coincides with Cyp19 gene expression in buffalo (Bubalus bubalis) placenta of different stages of gestation. Gen Comp Endocrinol 169:182-189
52. Zhang X, Ho SM 2011 Epigenetics meets endocrinology. J Mol Endocrinol 46:R11-R32
53. Kangaspeska S, Stride B, Métivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G 2008 Transient cyclical methylation of promoter DNA. Nature 452:112-115 (Pubitemid 351355094)
54. Inoue H, Sakamoto Y, Kangawa N, Kimura C, Ogata T, Fujieda K, Qian ZR, Sano T, Itakura M 2011 Analysis of expression and structure of the rat GH-secretagogue/ghrelin receptor (Ghsr) gene: roles of epigenetic modifications in transcriptional regulation. Mol Cell Endocrinol 345:1-15
55. Missaghian E, Kempná P, Dick B, Hirsch A, Alikhani-Koupaei R, Jégou B, Mullis PE, Frey BM, Flück CE 2009 Role of DNA methylation in the tissue-specific expression of the CYP17A1 gene for steroidogenesis in rodents. J Endocrinol 202:99-109
56. Hoivik EA, Bjanesoy TE, Mai O, Okamoto S, Minokoshi Y, Shima Y, Morohashi K, Boehm U, Bakke M 2011 DNA methylation of intronic enhancers directs tissue-specific expression of steroidogenic factor 1/adrenal 4 binding protein (SF-1/Ad4BP). Endocrinology 152:2100-2112
57. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D 2007 Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466 (Pubitemid 46514772)
58. Song F, Smith JF, Kimura MT, Morrow AD, Matsuyama T, Nagase H, Held WA 2005 Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. Proc Natl Acad Sci USA 102:3336-3341 (Pubitemid 40328046)
59. De Bustos C, Ramos E, Young JM, Tran RK, Menzel U, Langford CF, Eichler EE, Hsu L, Henikoff S, Dumanski JP, Trask BJ 2009 Tissue-specific variation in DNA methylation levels along human chromosome 1. Epigenetics Chromatin 2:7
60. DiNardo DN, Butcher DT, Robinson DP, Archer TK, Rodenhiser DI 2001 Functional analysis of CpG methylation in the BRCA1 promoter region. Oncogene 20:5331-5340 (Pubitemid 32844064)
61. Kuroda A, Rauch TA, Todorov I, Ku HT, Al-Abdullah IH, Kandeel F, Mullen Y, Pfeifer GP, Ferreri K 2009 Insulin gene expression is regulated by DNA methylation. PLoS ONE 4:e6953
62. Mancini DN, Singh SM, Archer TK, Rodenhiser DI 1999 Site-specific DNA methylation in the neurofibromatosis (NF1) promoter interferes with binding of CREB and SP1 transcription factors. Oncogene 18:4108-4119 (Pubitemid 29363918)
63. Derreumaux S, Chaoui M, Tevanian G, Fermandjian S 2001 Impact of CpG methylation on structure, dynamics and solvation of cAMP DNA responsive element. Nucleic Acids Res 29:2314-2326 (Pubitemid 32514934)
64. Sriraman V, Sinha M, Richards JS 2010 Progesterone receptor-induced gene expression in primary mouse granulosa cell cultures. Biol Reprod 82:402-412
65. Park OK, Mayo KE 1991 Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 5:967-978
66. Camp TA, Rahal JO, Mayo KE 1991 Cellular localization and hormonal regulation of follicle-stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary. Mol Endocrinol 5:1405-1417
67. Ronen-Fuhrmann T, Timberg R, King SR, Hales KH, Hales DB, Stocco DM, Orly J 1998 Spatio-temporal expression patterns of steroidogenic acute regulatory protein (StAR) during follicular development in the rat ovary. Endocrinology 139:303-315 (Pubitemid 28166323)
68. Hickey GJ, Chen SA, Besman MJ, Shively JE, Hall PF, Gaddy-Kurten D, Richards JS 1988 Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis. Endocrinology 122:1426-1436 (Pubitemid 18091973)
69. Hiroi H, Christenson LK, Chang L, Sammel MD, Berger SL, Strauss III JF 2004 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 18:791-806 (Pubitemid 38429473)
70. Zhang Y, Fatima N, Dufau ML 2005 Coordinated changes in DNA methylation and histone modifications regulate silencing/depression of luteinizing hormone receptor gene transcription. Mol Cell Biol 25:7929-7939 (Pubitemid 41262988)
71. Zhang Y, Dufau ML 2002 Silencing of transcription of the human luteinizing hormone receptor gene by histone deacetylase-mSin3A complex. J Biol Chem 277:33431-33438 (Pubitemid 34984866)
72. Smiraglia DJ, Rush LJ, Frühwald MC, Dai Z, Held WA, Costello JF, Lang JC, Eng C, Li B, Wright FA, Caligiuri MA, Plass C 2001 Excessive CpG island hypermethylation in cancer cell lines versus primary human malignancies. Hum Mol Genet 10:1413-1419 (Pubitemid 32640670)
73. Antequera F, Boyes J, Bird A 1990 High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 62:503-514
74. Di-Poï N, Desvergne B, Michalik L, Wahli W 2005 Transcriptional repression of peroxisome proliferator-activated receptor β/δ in murine keratinocytes by CCAAT/enhancer-binding proteins. J Biol Chem 280:38700-38710 (Pubitemid 43853773)
75. Kowenz-Leutz E, Pless O, Dittmar G, Knoblich M, Leutz A 2010 Crosstalk between C/EBPβ phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. EMBO J 29:1105-1115