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Acetylation and methylation profiles of H3K27 in porcine embryos cultured in vitro

Published online by Cambridge University Press:  11 July 2017

Luciana Simões Rafagnin Marinho ,
Vitor Braga Rissi ,
Andressa Guidugli Lindquist ,
Marcelo Marcondes Seneda  and
Vilceu Bordignon
Luciana Simões Rafagnin Marinho
Affiliation:
Laboratory of Animal Reproduction, State University of Londrina (UEL), Rodovia Celso Garcia Cid, Km 380, s/n – Campus Universitário, CEP 86057–970, Londrina, PR, Brazil
Vitor Braga Rissi
Affiliation:
Laboratory of Biotechnology and Animal Reproduction – BioRep, Veterinary Hospital, Federal University of Santa Maria, Av. Roraima, 1000 – Camobi, CEP 97105–900, Santa Maria, RS, Brazil
Andressa Guidugli Lindquist
Affiliation:
Laboratory of Animal Reproduction, State University of Londrina (UEL), Rodovia Celso Garcia Cid, Km 380, s/n – Campus Universitário, CEP 86057–970, Londrina, PR, Brazil
Marcelo Marcondes Seneda*
Affiliation:
Laboratory of Animal Reproduction, State University of Londrina (UEL), Rodovia Celso Garcia Cid, Km 380, s/n – Campus Universitário, CEP 86057–970, Londrina, PR, Brazil.
Vilceu Bordignon
Affiliation:
Department of Animal Science, McGill University, 21111 Lakeshore Road, Sainte Anne de Bellevue, Quebec H9X 3V9, Canada
*
All correspondence to: Marcelo Marcondes Seneda. Laboratory of Animal Reproduction, State University of Londrina (UEL), Rodovia Celso Garcia Cid, Km 380, s/n – Campus Universitário, CEP 86057–970, Londrina, PR, Brazil. E-mail: [email protected]
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Summary

Methylation and acetylation of histone H3 at lysine 27 (H3K27) regulate chromatin structure and gene expression during early embryo development. While H3K27 acetylation (H3K27ac) is associated with active gene expression, H3K27 methylation (H3K27me) is linked to transcriptional repression. The aim of this study was to assess the profile of H3K27 acetylation and methylation (mono-, di- and trimethyl) during oocyte maturation and early development in vitro of porcine embryos. Oocytes/embryos were fixed at different developmental stages from germinal vesicle to day 8 blastocysts and submitted to an immunocytochemistry protocol to identify the presence and quantify the immunofluorescence intensity of H3K27ac, H3K27me1, H3K27me2 and H3K27me3. A strong fluorescent signal for H3K27ac was observed in all developmental stages. H3K27me1 and H3K27me2 were detected in oocytes, but the fluorescent signal decreased through the cleavage stages and rose again at the blastocyst stage. H3K27me3 was detected in oocytes, in only one pronucleus in zygotes, cleaved-stage embryos and blastocysts. The nuclear fluorescence signal for H3K27me3 increased from the 2-cell stage to 4-cell stage embryos, decreased at the 8-cell and morula stages and increased again in blastocysts. Different patterns of the H3K27me3 mark were observed at the blastocyst stage. Our results suggest that changes in the H3K27 methylation status regulate early porcine embryo development as previously shown in other species.

Keywords

Embryo developmentGene expressionH3K27 acetylationH3K27 methylationSwine
Type
Research Article
Information
Zygote , Volume 25 , Issue 5 , October 2017 , pp. 575 - 582
Copyright
Copyright © Cambridge University Press 2017 

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References

Ambrosi, C., Manzo, M. & Baubec, T. (2017). Dynamics and context-dependent roles of DNA methylation. J. Mol. Biol. 429, 1459–75.CrossRefGoogle ScholarPubMed
Ancelin, K., Syx, L., Borensztein, M., Ranisavljevic, N., Vassilev, I., Briseno-Roa, L., Liu, T., Metzger, E., Servant, N., Barillot, E., et al. (2016). Maternal LSD1/KDM1A is an essential regulator of chromatin and transcription landscapes during zygotic genome activation. Elife 5, pii: e08851.Google Scholar
Beaujean, N. (2014). Histone post-translational modifications in preimplantation mouse embryos and their role in nuclear architecture. Mol. Reprod. Dev. 81, 100–12.Google Scholar
Boland, M.J., Nazor, K.L. & Loring, J.F. (2014). Epigenetic regulation of pluripotency and differentiation. Circ. Res. 115, 311–324.Google Scholar
Boyer, L.A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L.A., Lee, T.I., Levine, S.S., Wernig, M., Tajonar, A., Ray, M.K., et al. (2006). Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349–53.Google Scholar
Breton, A., LE Bourhis, D., Audouard, C., Vignon, X. & Lelièvre, J.-M. (2010). Nuclear profiles of H3 histones trimethylated on Lys27 in bovine (Bos taurus) embryos obtained after in vitro fertilization or somatic cell nuclear transfer. J. Reprod. Dev. 56, 379–88.Google Scholar
Cao, Z., Li, Y., Chen, Z., Wang, H., Zhang, M., Zhou, N., Wu, R., Ling, Y., Fang, F., Li, N., et al. (2015). Genome-wide dynamic profiling of histone methylation during nuclear transfer-mediated porcine somatic cell reprogramming. PLoS One 10, e0144897.Google Scholar
Chen, J. & Pei, D. (2016). Epigenetic landmarks during somatic reprogramming. IUBMB Life 68, 854–7.Google Scholar
Ciarapica, R., Carcarino, E., Adesso, L., De Salvo, M., Bracaglia, G., Leoncini, P.P., Dall'agnese, A., Verginelli, F., Milano, G.M., Boldrini, R., et al. (2014). Pharmacological inhibition of EZH2 as a promising differentiation therapy in embryonal RMS. BMC Cancer 14, 139.Google Scholar
Cook, M.S. & Blelloch, R. (2013). Small RNAs in germline development. Curr. Top. Dev. Biol. 102, 159–205.CrossRefGoogle ScholarPubMed
Creyghton, M.P., Cheng, A.W., Welstead, G.G., Kooistra, T., Carey, B.W., Steine, E.J., Hanna, J., Lodato, M. a, Frampton, G.M., Sharp, P.A., et al. (2010). Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 107, 21931–6.Google Scholar
Dallaire, A. & Simard, M.J. (2016). The implication of microRNAs and endo-siRNAs in animal germline and early development. Dev. Biol. 416, 18–25.Google Scholar
Erhardt, S., Su, I.-H., Schneider, R., Barton, S., Bannister, A.J., Perez-Burgos, L., Jenuwein, T., Kouzarides, T., Tarakhovsky, A. & Surani, M.A. (2003). Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130, 4235–48.Google Scholar
Fraser, R. & Lin, C.-J. (2016). Epigenetic reprogramming of the zygote in mice and men: on your marks, get set, go! Reproduction 152, R211–22.Google Scholar
Gannon, O.M., De Long, L.M., Endo-Munoz, L., Hazar-Rethinam, M. & Saunders, N.A. (2013). Dysregulation of the repressive H3K27 trimethylation mark in head and neck squamous cell carcinoma contributes to dysregulated squamous differentiation. Clin. Cancer Res. 19, 428– 41.CrossRefGoogle ScholarPubMed
Gao, Y., Hyttel, P. & Hall, V.J. (2010). Regulation of H3K27me3 and H3K4me3 during early porcine embryonic development. Mol. Reprod. Dev. 77, 540–9.CrossRefGoogle ScholarPubMed
Hales, B.F., Grenier, L., Lalancette, C. & Robaire, B. (2011). Epigenetic programming: From gametes to blastocyst. Birth Defects Res. Part A - Clin. Mol. Teratol. 91, 652– 65.CrossRefGoogle ScholarPubMed
Hasan, S. & Hottiger, M.O. (2002). Histone acetyl transferases: a role in DNA repair and DNA replication. J. Mol. Med. 80, 463–74.Google Scholar
Huang, Y., Yuan, L., Li, T., Wang, A., Li, Z., Pang, D., Wang, B. & Ouyang, H. (2015). Valproic acid improves porcine parthenogenetic embryo development through transient remodeling of histone modifiers. Cell. Physiol. Biochem. 37, 1463–73.Google Scholar
Lu, F. & Zhang, Y. (2015). Cell totipotency: molecular features, induction, and maintenance. Natl. Sci. Rev. 2, 217–25.Google Scholar
Morris, K. (2009). Non-coding RNAs, epigenetic memory and the passage of information to progeny. RNA Biol. 6, 242–7.Google Scholar
Novina, C.D. & Sharp, P.A. (2004). The RNAi revolution. Nature 430, 161–4.Google Scholar
O'Meara, M.M. & Simon, J.A. (2012). Inner workings and regulatory inputs that control Polycomb repressive complex 2. Chromosoma 121, 221–34.Google Scholar
Park, K.E., Magnani, L. & Cabot, R.A. (2009). Differential remodeling of mono- and trimethylated H3K27 during porcine embryo development. Mol. Reprod. Dev. 76, 1033–42.Google Scholar
Pasini, D., Malatesta, M., Jung, H.R., Walfridsson, J., Willer, A., Olsson, L., Skotte, J., Wutz, A., Porse, B., Jensen, O.N., et al. (2010). Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 38, 4958–69.CrossRefGoogle ScholarPubMed
Patel, T., Tursun, B., Rahe, D.P. & Hobert, O. (2012). Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types. Cell Rep. 2, 1178–86.CrossRefGoogle ScholarPubMed
Rodriguez-Sanz, H., Moreno-Romero, J., Solis, M.-T., Kohler, C., Risueno, M.C. & Testillano, P.S. (2014). Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with Bn HKMT and Bn HAT expression and are associated with cell totipotency, proliferation & differentiation in Brassica napus . Cytogenet. Genome Res. 143, 209–18.Google Scholar
Ross, P.J., Ragina, N.P., Rodriguez, R.M., Iager, A.E., Siripattarapravat, K., Lopez-Corrales, N. & Cibelli, J.B. (2008). Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction 136, 777–85.Google Scholar
Santos, F., Peters, A.H., Otte, A.P., Reik, W. & Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225–236.Google Scholar
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–5.Google Scholar
Schwartz, Y.B. & Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9–22.Google Scholar
Schwartz, Y.B., Kahn, T.G., Stenberg, P., Ohno, K., Bourgon, R. & Pirrotta, V. (2010). Alternative epigenetic chromatin states of Polycomb target genes. PLoS Genet. 6, e1000805.Google Scholar
Shpargel, K.B., Starmer, J., Yee, D., Pohlers, M. & Magnuson, T. (2014). KDM6 demethylase independent loss of histone H3 lysine 27 trimethylation during early embryonic development. PLoS Genet. 10, e1004507.Google Scholar
Surface, L.E., Thornton, S.R. & Boyer, L.A. (2010). Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 7, 288–98.Google Scholar
Tie, F., Banerjee, R., Stratton, C. a, Prasad-Sinha, J., Stepanik, V., Zlobin, A., Diaz, M.O., Scacheri, P.C. & Harte, P.J. (2009). CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136, 3131–41.Google Scholar
Van Der Heijden, G.W., Dieker, J.W., Derijck, A.A.H.A., Muller, S., Berden, J.H.M., Braat, D.D.M., Van Der Vlag, J. & De Boer, P. (2005). Asymmetry in Histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 122, 1008–22.Google Scholar
Wang, F., Kou, Z., Zhang, Y. & Gao, S. (2007). Dynamic reprogramming of histone acetylation and methylation in the first cell cycle of cloned mouse embryos. Biol. Reprod. 77, 1007–16.Google Scholar
Williams, K., Christensen, J., Rappsilber, J., Nielsen, A.L., Johansen, J.V. & Helin, K. (2014). The histone lysine demethylase JMJD3/KDM6B is recruited to p53 bound promoters and enhancer elements in a p53 dependent manner. PLoS One 9, e96545.Google Scholar
Xie, B., Zhang, H., Wei, R., Li, Q., Weng, X., Kong, Q. & Liu, Z. (2016). Histone H3 lysine 27 trimethylation acts as an epigenetic barrier in porcine nuclear reprogramming. Reproduction 151, 9–16.Google Scholar
Young, S.J., Yeo, S., Jung, S.P., Lee, K.K. & Kang, Y.K. (2007). Gradual development of a genome-wide H3-K9 trimethylation pattern in paternally derived pig pronucleus. Dev. Dyn. 236, 1509–16.Google Scholar
Zhou, N., Cao, Z., Wu, R., Liu, X., Tao, J., Chen, Z., Song, D., Han, F., Li, Y., Fang, F., et al. (2014). Dynamic changes of histone H3 lysine 27 acetylation in pre-implantational pig embryos derived from somatic cell nuclear transfer. Anim. Reprod. Sci. 148, 153–63.Google Scholar