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Histone hyperacetylation and DNA methylation interplay during murine spermatogenesis

Published online by Cambridge University Press:  15 August 2019

Liliana Burlibaşa Open the ORCID record for Liliana Burlibaşa [Opens in a new window] ,
Andreea Carmen Ionescu  and
Delia-Mihaela Dragusanu
Liliana Burlibaşa*
Affiliation:
University of Bucharest, Faculty of Biology, Genetics Department, Bucharest, Romania
Andreea Carmen Ionescu
Affiliation:
University of Bucharest, Faculty of Biology, Genetics Department, Bucharest, Romania
Delia-Mihaela Dragusanu
Affiliation:
University of Bucharest, Faculty of Biology, Genetics Department, Bucharest, Romania
*
Address for correspondence: Liliana Burlibaşa. Nos. 1–3 Aleea Portocalilor, Bucharest, Romania. Tel:/Fax: +40 213181565. E-mails: liliana_burlibasa@yahoo.com.au; liliana.burlibasa@bio.unibuc.ro
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Summary

Male germ cell development is a critical period during which epigenetic patterns are established and maintained. The progression from diploid spermatogonia to haploid spermatozoa involves the incorporation of testis-specific histone variants, mitotic and meiotic divisions, haploid gene expression, histone–protamine transitions and massive epigenetic reprogramming. Understanding the protein players and the epigenetic mark network involved in the setting of the epigenetic programme in spermatogenesis is an exciting new clue in the field of reproductive biology with translational outcomes. As information in the existing literature regarding cross-talk between DNA methylation and histone hyperacetylation in the advanced stages of murine spermatogenesis is still scarce and controversial we have investigated the effect of a DNA-methyltransferase inhibitor, 5-aza-2′-deoxycytidine, at the cytological and molecular level (by transmission electron microscopy, immunocytochemistry and immunoprecipitation methods). Our results revealed an important role for regulation of DNA methylation in controlling histone hyperacetylation and chromatin remodelling during spermatogenesis.

Keywords

5-Aza-2′-deoxycytidineDNA methylationEpigenetic marksH4 hyperacetylationSpermatogenesis
Type
Research Article
Information
Zygote , Volume 27 , Issue 5 , October 2019 , pp. 305 - 314
Copyright
© Cambridge University Press 2019 

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Footnotes

*

These authors made the same contribution to this work.

References

Banu, M, Simion, M, Ratiu, AC, Popescu, M, Romanitan, C, Danila, M, Radoi, A, Ecovoiu, A and Kusko, M (2015) Enhance nucleotide mismatch detection based on 3D silicon nanowire microarray. RSC Adv 5, 74506–14.CrossRefGoogle Scholar
Bellvé, AR (1993) Purification, culture and fractioning of spermatogenic cells. Methods Enzymol 225, 84–113.CrossRefGoogle Scholar
Berger, SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12, 142–8.CrossRefGoogle ScholarPubMed
Bestor, T, Laudano, A, Mattaliano, R and Ingram, V (1988) Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxy-terminal domain of the mammalian enzyme is related to bacterial restriction methyltransferases. Mol Biol 203, 971–83.CrossRefGoogle Scholar
Burlibaşa, L and Gavrilă, L (2005) Molecular and ultrastructural studies of the sperm chromatin from Triturus cristatus . Zygote 13, 197–205.CrossRefGoogle ScholarPubMed
Burlibaşa, L, Zărnescu, O, Cucu, N and Gavrilă, L (2008) Chromatin dynamics in Triturus cristatus oogenesis: an epigenetic approach. Zygote 16, 315–26.CrossRefGoogle ScholarPubMed
Burlibaşa, L and Gavrilă, L (2011) Developmental epigenetics: roles in embryonic development. In: Niculescu, M and Haggarty, P (eds). Nutrition in Epigenetics. Wiley-Blackwell, pp. 107–26.Google Scholar
Burlibaşa, L and Zărnescu, O (2013) In vivo effects of trichostatin A – a histone deacetylase inhibitor, on chromatin remodeling during Triturus cristatus spermatogenesis. Anim Reprod Sci 142, 89–99.CrossRefGoogle ScholarPubMed
Burlibaşa, L and Suciu, I (2015) Investigation of histone H4 hyperacetylation dynamics in the 5S rRNA genes family by chromatin immunoprecipitation assay. Zygote 23, 951–4.CrossRefGoogle ScholarPubMed
Caron, C, Govin, J, Rousseaux, S and Khochbin, S (2005) How to pack the genome for a safe trip. In: Jeanteur, P (eds), Epigenetics and Chromatin. Progress in Molecular and Subcellular Biology, vol 38. Springer, Berlin, Heidelberg.Google Scholar
Christensen, ME, Rattner, JB and Dixon, GH (1984) Hyperacetylation of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acids Res 12, 4575–92.CrossRefGoogle ScholarPubMed
Doerksen, T, Benoit, G and Trasler, JM (2000) Deoxyribonucleic acid hypomethylation of male germ cells by mitotic and meiotic exposure to 5-azacytidine is associated with altered testicular histology. Endocrinology 141, 3235–44.CrossRefGoogle ScholarPubMed
Eckhardt, F, Lewin, J, Cortese, R, Rakyan, VK and Attwood, J (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38, 1378–85.CrossRefGoogle ScholarPubMed
Eden, S, Hashimshony, T, Keshet, I, Cedar, H and Thorne, AW (1998) DNA methylation models histone acetylation. Nature 394, 842–3.CrossRefGoogle ScholarPubMed
Fenic, I, Sonnack, V, Failing, K, Bergman, M and Steger, K (2004) In vivo effects of histone-deacetylase inhibitor trichostatin-A on murine spermatogenesis. J Androl 25, 811–8.CrossRefGoogle ScholarPubMed
Gabbara, S and Bhagwat, AS (1995) The mechanism of inhibition of DNA (cytosine-5)-methyltransferases by 5-azacytosine is likely to involve methyl transfer to the inhibitor. Biochem J 307, 87–92.CrossRefGoogle ScholarPubMed
Gavrilă, L and Mircea, L (2001) Chromatin and chromosomal fine structure in spermatogenesis of some species of amphibians. Zygote 9, 183–92.CrossRefGoogle ScholarPubMed
Gavrilă, L, Burlibaşa, L, Usurelu, MD, Radu, I, Magdalena, LM, Ardelean, A and Carabas, M (2008) Chromosomal rearrangements in Chironomus sp. as genosensors for monitoring environmental pollution. Rom Biotech Lett 13, 3962–9.Google Scholar
Goldman, DC, Bailey, AS, Pfaffle, DL, Al Masri, A, Christian, JL and Fleming, WH (2009) BMP4 regulates the hematopoetic stem cell niche. Blood 114, 4393–401.CrossRefGoogle Scholar
Govin, J, Caron, C, Lestrat, C, Rousseaux, S and Khochbin, S (2004) The role of histones in chromatin remodelling during mammalian spermiogenesis. Eur J Biochem 271, 3459–69.CrossRefGoogle ScholarPubMed
Hajkova, P, Erhardt, S, Lane, N, Haaf, T and El-Maarri, O (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117, 15–23.CrossRefGoogle ScholarPubMed
Hazzouri, M, Rousseaux, S, Mongelard, F, Usson, Y, Pelletier, R, Faure, AK, Vourc’h, C and Sele, B (2000) Genome organization in the human sperm nucleus studied by FISH and confocal microscopy. Mol Reprod Dev 55, 307–15.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Jenuwein, T and Allis, CD (2001) Translating the histone code. Science 293(5532), 1074–80.CrossRefGoogle ScholarPubMed
Jones, PL, Veenstra, GJC, Wade, PA, Vermaak, D, Kass, SU, Landsberg, N, Strouboulis, J and Wolffe, AP (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19, 187–91.CrossRefGoogle ScholarPubMed
Kaneda, M, Okano, M, Hata, K, Sado, T, Tsujimoto, N, Li, E and Sasaki, H (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900–3.CrossRefGoogle Scholar
Kelly, TLJ Li, E and Trasler, JM (2003) 5-Aza-2-deoxycytidine induces alterations in murine spermatogenesis and pregnancy outcome. J Androl 24, 822–30.CrossRefGoogle ScholarPubMed
Khalil, AM and Wahlested, C (2008) Epigenetic mechanisms of gene regulation during mammalian spermatogenesis. Epigenetics 3, 21–7.CrossRefGoogle ScholarPubMed
La Salle, S and Trasler, J (2006) Epigenetic patterning in male germ cells: importance of DNA methylation to progeny outcome. In: De Jonge, C and Barratt, C (eds), The Sperm Cell: Production Maturation Fertilization Regeneration. Cambridge: Cambridge University Press, pp. 279–322.CrossRefGoogle Scholar
Liu, Y and Zhang, D (2015) HP1a/KDM4A is involved in the autoregulatory loop of the oncogene gene c-Jun. Epigenetics 10, 453–9.CrossRefGoogle ScholarPubMed
Maatouk, DK, Kellam, LD, Mann, MRW, Lei, H and Li, E (2006) DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133, 3411–8.CrossRefGoogle ScholarPubMed
Nan, X, Ng, H-H, Johnson, CA, Laherty, CD, Turner, BM, Eisenman, RN and Bird, A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386–9.CrossRefGoogle ScholarPubMed
Natsume-Kitatani, Y, Shiga, M and Mamitsuka, H (2011) Genome-wide integration on transcription factors, histone acetylation and gene expression reveals genes co-regulated by histone modification patterns. PLoS One 6, e22281.CrossRefGoogle ScholarPubMed
Niedenberger, BA, Busada, JT and Geyer, CB (2015) Marker expression reveals heterogeneity of spermatogonia in the neonatal mouse testis. Reproduction 149, 329–38.CrossRefGoogle ScholarPubMed
Oakes, CC, La Salle, S, Smiraglia, DJ, Robaire, B and Trasler, JM (2007a) A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci USA 104, 228–33.CrossRefGoogle ScholarPubMed
Oakes, CO, Kelly, TLJ, Robaire, B and Trasler, JM (2007b) Adverse effects of 5-aza-2-deoxycytidine on spermatogenesis include reduced sperm function and selective inhibition of the novo DNA methylation. J Pharmacol Exp Ther 322, 1171–80.CrossRefGoogle ScholarPubMed
Okano, M, Xie, S and Li, E (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19, 219–20.CrossRefGoogle ScholarPubMed
Oliva, R and Mazquita, C (1982) Histone H4 hyperacetylation and rapid turnover of its acetyl groups in transcriptionally inactive rooster testis spermatids. Nucleic Acids Res 10, 8049–59.CrossRefGoogle ScholarPubMed
Reik, W, Dean, W and Walter, J (2001) Epigenetic reprogramming in mammalian development. Science 293, 1089–93.CrossRefGoogle ScholarPubMed
Shiota, K, Kogo, Y, Ohgane, J, Imamura, T and Urano, A (2002) Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 7, 961–9.CrossRefGoogle ScholarPubMed
Strahl, BD and Allis, CD (2000) The language of covalent histone modifications. Nature 403(6765), 41–5.CrossRefGoogle ScholarPubMed
Workman, JL (2006) Nucleosome displacement in transcription. Genes Dev 20, 2009–17.CrossRefGoogle ScholarPubMed
Zhao, J, Herrera-Diaz, J and Gross, DS (2005) Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol 25, 8985–99.CrossRefGoogle Scholar
Zhu, WG, Lakshmanan, RR, Beal, DM and Otterson, GA (2001) DNA methyltransferase inhibition enhances apoptosis induced by histone deacetylase inhibitors. Cancer Res 61, 1327–33.Google ScholarPubMed