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Histone H3 acetylation of StAR and decrease in DAX-1 is involved in the luteinization of bovine granulosa cells during in vitro culture

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Abstract

We investigated the expression of genes and transcription factors associated with steroidogenesis during the luteinization of granulosa cells isolated from bovine small follicles. Granulosa cells produced progesterone when cultivated in a culture medium including serum and attached to the substrate and began to display an elongated or fibroblastic aspect within 24 h of culture. We observed an increase in the number of granulosa cells at the same time. P450arom expression in the cultured granulosa cells had decreased at 24 h compared with 0 h of culture, and afterward was maintained at a low level. This expression was consistent with the decline of E2 concentration in the medium. Expression of StAR and P450scc mRNAs in the cultured granulosa cells was significantly increased at 72 h compared with 0 h of culture. Although the expression of Ad4BP/SF-1 mRNA began to increase during period between 48 and 72 h of culture, protein expression of Ad4BP/SF-1 remained at a constant level throughout the culture period. DAX-1 mRNA expression had decreased at 24 h of culture and remained at a low level. In parallel with this expression, the protein expression of DAX-1 began to decrease between 24 and 48 h of culture and then remained at a low level. Histone H3 acetylation of the StAR promoter region was observed at 72 h of culture period. Our data suggested that the decrease of Dax-1 transcription factor and the increase in histone H3 acetylation may play important roles in progesterone synthesis in luteinizing granulosa cells.

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References

  1. Channing CP, Ledwitz-Rigby F (1975) Methods fro assessing hormone-mediated differentiation of ovarian cells in culture and in short-term incubations. Methods Enzymol 39:183–230. doi:10.1016/S0076-6879(75)39020-4

    Article  PubMed  CAS  Google Scholar 

  2. Niswender GD (2002) Molecular control of luteal secretion of progesterone. Reproduction 123:333–339. doi:10.1530/rep.0.1230333

    Article  PubMed  CAS  Google Scholar 

  3. Stocco DM (2001) StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 63:193–213. doi:10.1146/annurev.physiol.63.1.193

    Article  PubMed  CAS  Google Scholar 

  4. Fortune JE (1986) Bovine theca and granulosa cells interact to promote androgen production. Biol Reprod 35:292–299. doi:10.1095/biolreprod35.2.292

    Article  PubMed  CAS  Google Scholar 

  5. Espey LL, Richards JS (2002) Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod 67:1662–1670. doi:10.1095/biolreprod.102.005173

    Article  PubMed  CAS  Google Scholar 

  6. Orly J, Stocco DM (1999) The role of the steroidogenic acute regulatory (StAR) protein in female reproductive tissues. Horm Metab Res 31:389–398. doi:10.1055/s-2007-978761

    Article  PubMed  CAS  Google Scholar 

  7. Pescador N, Stocco DM, Murphy DB (1999) Growth factor modulation of steroidogenic acute regulatory protein and luteinization in the pig ovary. Biol Reprod 60:1453–1461. doi:10.1095/biolreprod60.6.1453

    Article  PubMed  CAS  Google Scholar 

  8. Zanaria E, Muscatelli F, Bardoni B, Strom TM, Guioli S, Guo W, Lalli E, Moser C, Walker AP, McCabe ER, Meitinger T, Monaco AP, Sassone-Corsi P, Camerino G (1994) An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 372:635–641. doi:10.1038/372635a0

    Article  PubMed  CAS  Google Scholar 

  9. Muscatelli F, Strom TM, Walker AP, Zanaria E, Recan D, Meindl A, Bardoni B, Guioli S, Zehetner G, Rabl W, Schwarz HP, Kaplan JC, Camerino G, Meitinger T, Monaco AP (1994) Mutations in the DAX-1 gene give rise to both X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism. Nature 372:672–676. doi:10.1038/372672a0

    Article  PubMed  CAS  Google Scholar 

  10. Ikeda Y, Shen W, Ingraham HA, Parker KL (1994) Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 8:654–662. doi:10.1210/me.8.5.654

    Article  PubMed  CAS  Google Scholar 

  11. Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K (1994) Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 120:2787–2797

    PubMed  CAS  Google Scholar 

  12. Shibata H, Kurihara I, Kobayashi S, Yokota K, Suda N, Saito I, Saruta T (2003) Regulation of differential COUP-TF-coregulator interactions in adrenal cortical steroidogenesis. J Steroid Biochem Mol Biol 85:449–456. doi:10.1016/S0960-0760(03)00217-6

    Article  PubMed  CAS  Google Scholar 

  13. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349–352. doi:10.1038/38664

    Article  PubMed  CAS  Google Scholar 

  14. Kadonaga JT (1998) Eukaryotic transcription: an interlaced network of transcription factors and chromatin-modifying machines. Cell 92:307–313. doi:10.1016/S0092-8674(00)80924-1

    Article  PubMed  CAS  Google Scholar 

  15. Braunstein M, Rose AB, Holmes SG, Allis CD, Broach JR (1993) Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev 7:592–604. doi:10.1101/gad.7.4.592

    Article  PubMed  CAS  Google Scholar 

  16. Orlando V, Strutt H, Paro R (1997) Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205–214. doi:10.1006/meth.1996.0407

    Article  PubMed  CAS  Google Scholar 

  17. Rust W, Stedronsky K, Tillmann G, Morley S, Walther N, Ivell R (1998) The role of SF-1/Ad4BP in the control of the bovine gene for the steroidogenic acute regulatory (StAR) protein. J Mol Endocrinol 21:189–200. doi:10.1677/jme.0.0210189

    Article  PubMed  CAS  Google Scholar 

  18. Miyamoto A, Okuda K, Schweigert FJ, Schams D (1992) Effects of basic fibroblast growth factor, transforming growth factor-beta and nerve growth factor on the secretory function of the bovine corpus luteum in vitro. J Endocrinol 135:103–114. doi:10.1677/joe.0.1350103

    Article  PubMed  CAS  Google Scholar 

  19. Acosta TJ, Miyamoto A, Ozawa T, Wijayagunawardane MP, Sato K (1998) Local release of steroid hormones, prostaglandin E2, and endothelin-1 from bovine mature follicles In vitro: effects of luteinizing hormone, endothelin-1, and cytokines. Biol Reprod 59:437–443. doi:10.1095/biolreprod59.2.437

    Article  PubMed  CAS  Google Scholar 

  20. Murphy BD (2000) Model of luteinization. Biol Reprod 63:2–11. doi:10.1095/biolreprod63.1.2

    Article  PubMed  CAS  Google Scholar 

  21. Shimasaki S, Zachow RJ, Li D, Kim H, Iemura S, Ueno N, Sampath K, Chang RJ, Erickson GF (1999) A functional bone morphogenetic protein system in the ovary. Proc Natl Acad Sci USA 96:7282–7287. doi:10.1073/pnas.96.13.7282

    Article  PubMed  CAS  Google Scholar 

  22. Pierre A, Pisselet C, Dupont J, Mandon-Pepin B, Monniaux D, Monget P, Fabre S (2004) Molecular basis of bone morphogenetic protein-4 inhibitory action on progesterone secretion by ovine granulosa cells. J Mol Endocrinol 33:805–817. doi:10.1677/jme.1.01545

    Article  PubMed  CAS  Google Scholar 

  23. Zazopoulos E, Lalli E, Stocco DM, Sassone-Corsi P (1997) DNA binding and transcriptional repression by DAX1 blocks steroidogenesis. Nature 390:311–315. doi:10.1038/36899

    Article  PubMed  CAS  Google Scholar 

  24. Ito M, Yu R, Jameson JL (1997) DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenital. Mol Cell Biol 17:1476–1483

    PubMed  CAS  Google Scholar 

  25. Suzuki T, Kasahara M, Yoshioka H, Morohashi K, Umesono K (2003) LXXLL-related motifs in Dax-1 have target specificity for the orphan nuclear receptors Ad4BP/SF-1 and LRH-1. Mol Cell Biol 23:238–249. doi:10.1128/MCB.23.1.238-249.2003

    Article  PubMed  CAS  Google Scholar 

  26. Sugawara T, Kiriakidou M, McAllister JM, Kallen CB, Strauss JFIII (1997) 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 36:7249–7255. doi:10.1021/bi9628984

    Article  PubMed  CAS  Google Scholar 

  27. Wooton-Kee CR, Clark BJ (2000) Steroidogenic factor-1 influences protein-deoxyribonucleic acid interactions within the cyclic adenosine 3,5-monophosphate-responsive regions of the murine steroidogenic acute regulatory protein gene. Endocrinology 141:1345–1355. doi:10.1210/en.141.4.1345

    Article  PubMed  CAS  Google Scholar 

  28. Christenson LK, Stouffer R, Strauss JFIII (2001) Quantitative analysis of the hormone-induced hyperacetylation of histone H3 associated with the steroidogenesis acute regulatory protein gene promoter. J Biol Chem 276:27392–27399. doi:10.1074/jbc.M101650200

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

The authors thank Dr. K. Okuda, Okayama University, Japan, for progesterone antibodies. This study was supported by a grant-in-aid for scientific research from the Japan Society for the Promotion of Science (JSPS), Japan. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.

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Correspondence to Takashi Shimizu.

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Shimizu, T., Sudo, N., Yamashita, H. et al. Histone H3 acetylation of StAR and decrease in DAX-1 is involved in the luteinization of bovine granulosa cells during in vitro culture. Mol Cell Biochem 328, 41–47 (2009). https://doi.org/10.1007/s11010-009-0072-y

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  • DOI: https://doi.org/10.1007/s11010-009-0072-y

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