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Immunolocalization of BRG1–SWI/SNF protein during folliculogenesis in the porcine ovary

Published online by Cambridge University Press:  15 April 2011

Livia Aires Lisboa ,
Vilceu Bordignon  and
Marcelo Marcondes Seneda
Livia Aires Lisboa
Affiliation:
Laboratory of Animal Reproduction, Londrina State University, Parana 86051990, Brazil.
Vilceu Bordignon
Affiliation:
Department of Animal Science, McGill University, 21111 Lakeshore Road, Ste-Anne-de-Bellevue, Québec, H9X3V9, Canada.
Marcelo Marcondes Seneda*
Affiliation:
Laboratory of Animal Reproduction, Veterinary Hospital, Londrina State University, Parana 86051990, Brazil.
*
All correspondence to: Marcelo Marcondes Seneda. Laboratory of Animal Reproduction, Veterinary Hospital, Londrina State University, Parana 86051990, Brazil. Tel: +55 43 3371 4064. Fax: +55 43 33714063. e-mail: [email protected]
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Summary

Dynamic changes in chromatin structure and gene expression occur during follicular and oocyte growth. Epigenetic mechanisms regulate these changes through biochemical reactions that modify the nucleosome structure, and consequently affect transcription. Chromatin remodellers that alter DNA–histone interactions can influence transcriptional activity by facilitating or repressing DNA access. The SWItch/Sucrose NonFermentable (SWI/SNF) complex represents an important chromatin remodelling family, which comprises many protein subunits including the BRG1 (brahma-related gene 1). Our aim in this study was to analyse BRG1 expression patterns in different stages of follicular development. Ovaries (n = 10) were collected from prepubertal gilts and then rinsed in phosphate-buffered saline (PBS). Ovarian fragments of 8 × 8 × 8 mm were cut and placed into a 4% paraformaldehyde solution. For immunofluorescence analysis, samples were incubated with primary antibodies: polyclonal rabbit anti-BRG1 (1/200) or control rabbit IgG at the same concentration, overnight at 4°C. Primary antibodies were detected using Alexa Fluor 594-anti-rabbit 1/1000 diluted secondary antibody. Cells were counterstained with 4′,6-diamidino-2-phenylindole (DAPI). Positive fluorescence signal for BRG1 was detected in all analysed samples. In primary follicles, the protein was detected only in the oocyte nucleus. However, in growing follicles, BRG1 was identified in granulosa and theca cells in a well defined pattern, according to the proximity of the cells from the oocyte. These results suggest an important role for BRG1 in the regulation of follicular growth, probably modulating granulosa and theca cell proliferation, as well as oocyte growth and maturation.

Keywords

BRG1FolliculogenesisOocytePorcineSWI/SNF complex
Type
Research Article
Information
Zygote , Volume 20 , Issue 3 , August 2012 , pp. 243 - 248
Copyright
Copyright © Cambridge University Press 2011

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References

Albert, M. & Peters, A.H.F.M. (2009). Genetic and epigenetic control of early mouse development. Curr. Opin. Gen. Dev. 19, 113–21.CrossRefGoogle ScholarPubMed
Bultman, S., Gebuhr, T., Yee, D., La Mantia, C., Nicholson, J., Gilliam, A., Randazzo, F., Metzger, D., Chambon, P. & Crabtree, G. (2000). A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287–95.CrossRefGoogle ScholarPubMed
Bultman, S., Gebuhr, T.C., Pan, H., Svoboda, T., Schultz, R.M. & Magnuson, T. (2006). Maternal BRG1 regulates zygote genome activation in the mouse. Genes Dev. 20, 1744–54.CrossRefGoogle ScholarPubMed
Carabatsos, M.J., Elvin, J., Matzuk, M.M. & Albertini, D.F. (1998). Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 204, 373–84.CrossRefGoogle ScholarPubMed
De La Fuente, R. (2006). Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 292, 1–12.CrossRefGoogle ScholarPubMed
Di Stefano, L., Ji, J.Y., Monn, N.S., Herr, A. & Dyson, N. (2007). Mutation of Drosophila LSD1 disrupts H3-K4 methylation, resulting in tissue-specific defects during development. Curr. Biol. 17, 808–12.CrossRefGoogle ScholarPubMed
Driancourt, M.A. (1991). Follicular dynamics in sheep and cattle. Theriogenology 33, 55–73.CrossRefGoogle Scholar
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–16.CrossRefGoogle ScholarPubMed
Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H. & Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–83.CrossRefGoogle Scholar
Godmann, M., Auger, V., Ferraroni-Aguiar, V., Di Sauro, A., Sette, C., Behr, R. & Kimmins, S. (2007). Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol. Reprod. 77, 754–64.CrossRefGoogle ScholarPubMed
Gutierrez, C.G., Ralph, J.H., Telfer, E.E. & Wilmut, I., Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–8.CrossRefGoogle ScholarPubMed
Hans, F. & Dimitrov, S. (2001). Histone H3 phosphorylation and cell division. Nature 20, 3021–7.Google ScholarPubMed
Hasegawa, A., Kumamoto, K., Mochida, N., Komori, S. & Koyama, K. (2009). Gene expression profile during ovarian folliculogenesis. J. Reprod. Immunol. 83, 40–4.CrossRefGoogle ScholarPubMed
Ichinose, H., Garnier, J.M., Chambon, P. & Losson, R. (1997). Ligand dependent interaction between the estrogen receptor and the human homologues of SWI2/SNF2. Gene 188, 95–100.CrossRefGoogle ScholarPubMed
Inayoshi, Y., Kaneoka, H., Machida, Y., Terajima, M., Dohda, T., Miyake, K. & Iijima, S. (2005). Repression of GR-mediated expression of the tryptophan oxygenase gene by the SWI/SNF complex during liver development. J. Biochem. 138, 457–65.CrossRefGoogle ScholarPubMed
Itoh, T., Miyake, K. & Lijima, S. (2008). Differentiation-specific expression of chromatin remodeling factor BRM. Biochem. Biophys. Res. Commun. 366, 827–33.CrossRefGoogle ScholarPubMed
Juengel, J.L., Hudson, N.L., Heath, D.A., Smith, P., Reader, K.L., Lawrence, S.B., O'Connell, A.R., Laitinen, M.P., Cranfield, M., Groome, N.P., Ritvos, O. & McNatty, K.P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 68, 1777–89.CrossRefGoogle Scholar
Knight, P.G. & Glister, C. (2003). Local roles of TGF-β superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165–83.CrossRefGoogle ScholarPubMed
Knott, J.G., Palmer, S. & De Matos, D.G. (2006). P-226: search for epigenetic markers of oocyte and embryo quality: Elucidation of role of BRG1 (brahma-related gene 1) in embryo development in mouse. Fertil. Steril. 86 (Suppl. 1), S217–8.CrossRefGoogle Scholar
Martens, J.A. & Winston, F. (2003). Recent advances in understanding chromatin remodeling by SWI/SNF complexes. Curr. Opin. Gen. Dev. 13, 136–42.CrossRefGoogle ScholarPubMed
Morbeck, D.E., Esbenshade, K.L., Flowers, W.L. & Britt, J.H. (1992). Kinetics of follicle growth in the prepubertal gilt. Biol. Reprod. 47, 485–91.CrossRefGoogle ScholarPubMed
Narlikar, G.J., Fan, H.Y. & Kingston, R.E. (2002). Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475–87.CrossRefGoogle ScholarPubMed
Nilsson, E., Parrot, J.A. & Skinner, M.K. (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol. 175, 123–30.CrossRefGoogle ScholarPubMed
Nilsson, E., Kezele, P. & Skinner, M.K. (2002). Leukemia inhibiting factor (LIF) promotes primordial to primary follicle transition in rat ovaries. Mol. Cell. Endocrinol. 188, 65–73.CrossRefGoogle Scholar
Pangas, S.A. & Matzuk, M.M. (2004). Genetic models for transforming growth factor beta superfamily signaling in ovarian follicle development. Mol. Cell Endocrinol. 225, 83–91.CrossRefGoogle ScholarPubMed
Parrot, J.A. & Skinner, M.K. (1999). Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262–71.CrossRefGoogle Scholar
Pan, H., O'Brien, M.J., Wigglesworth, K., Eppig, J.J. & Schultz, R.M. (2005). Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 286, 493–506.CrossRefGoogle ScholarPubMed
Peterson, C.L. & Workman, J.L. (2000). Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr. Opin. Genet. Dev. 10, 187–92.CrossRefGoogle ScholarPubMed
Reisman, D.N., Sciarrotta, J., Boudin, T.W., Weissman, B.E. & Funkhouser, W.K. (2005). The expression of the SWI/SNF ATPase subunits BRG1 and BRM in normal human tissues. App. Immunohistochem. Mol. Morphol. 13, 66–74.CrossRefGoogle ScholarPubMed
Ruiz-Cortés, Z.T., Kimmins, S., Monaco, L., Burns, K.H., Sassone-Corsi, P. & Murphy, B.D. (2005). Estrogen mediates phosphorylation of histone H3 in ovarian follicle and mammary epithelial tumor cells via the mitotic kinase, aurora B. Mol. Endocrinol. 19, 2991–3000.CrossRefGoogle ScholarPubMed
Seneda, M.M., Godmann, M., Murphy, B.D., Kimmins, S. & Bordignon, V. (2008). Developmental regulation of histone H3 methylation at lysine 1 in the porcine ovary. Reproduction 135, 829–38.CrossRefGoogle ScholarPubMed
Sirard, M. & Coenen, K. (1994). The effect of hormones during in vitro meiotic inhibition with cycloheximide on subsequent development of bovine oocytes. Biol. Reprod. 50, 361.Google Scholar
Tang, L., Nogales, E. & Ciferri, C. (2010). Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription. Prog. Biophys. Mol. Biol. 102, 122–8.CrossRefGoogle ScholarPubMed
Trotter, K.W. & Archer, T.K. (2007). Nuclear receptors and chromatin remodeling machinery. Mol. Cell. Endocrinol. 265–266, 162–7.CrossRefGoogle ScholarPubMed
Van Den Hurk, R., Abir, R., Telfer, E.E. & Bevers, M.M. (2000). Primate and bovine immature oocytes and follicles as sources of fertilizable oocytes. Hum. Reprod. Update 6, 457–74.CrossRefGoogle ScholarPubMed
Vitt, U.A., McGee, E.A., Hayashi, M. & Hsuch, A.J. (2000). In vivo treatment with GDF9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141, 3814–20.CrossRefGoogle ScholarPubMed
Zhao, J., Taverne, M.A.M., Van Der Weijden, G.C., Bevers, M.M. & Van Den Hurk, R. (2001). Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol. Reprod. 65, 967–77.CrossRefGoogle ScholarPubMed