Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T23:31:41.215Z Has data issue: false hasContentIssue false

DNA methyltransferase inhibitors modulate histone methylation: epigenetic crosstalk between H3K4me3 and DNA methylation during sperm differentiation

Published online by Cambridge University Press:  08 January 2021

Liliana Burlibaşa*
Affiliation:
Genetics Department, University of Bucharest, Faculty of Biology, Romania
Alina-Teodora Nicu
Affiliation:
Genetics Department, University of Bucharest, Faculty of Biology, Romania
Carmen Domnariu
Affiliation:
‘Lucian Blaga’ University, Faculty of Medicine, Sibiu, Romania
*
Author for correspondence: Liliana Burlibaşa. Genetics Department, University of Bucharest, Nos. 1–3 Aleea Portocalilor, Bucharest, 060101, Romania. Tel: +40 213181565. E-mail: [email protected]

Summary

The process of cytodifferentiation in spermatogenesis is governed by a unique genetic and molecular programme. In this context, accurate ‘tuning’ of the regulatory mechanisms involved in germ cells differentiation is required, as any error could have dramatic consequences on species survival and maintenance. To study the processes that govern the spatial–temporal expression of genes, as well as analyse transmission of epigenetic information to descendants, an integrated approach of genetics, biochemistry and cytology data is necessary. As information in the literature on interplay between DNA methylation and histone H3 lysine 4 trimethylation (H3K4me3) in the advanced stages of murine spermatogenesis is still scarce, we investigated the effect of a DNA methyltransferase inhibitor, 5-aza-2′-deoxycytidine, at the cytological level using immunocytochemistry methodology. Our results revealed a particular distribution of H3K4me3 during sperm cell differentiation and highlighted an important role for regulation of DNA methylation in controlling histone methylation and chromatin remodelling during spermatogenesis.

Type
Short Communication
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bartke, T, Vermeulen, M, Xhemalce, B, Robson, SC, Mann, M and Kouzarides, T (2010). Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143, 470–84.CrossRefGoogle ScholarPubMed
Burlibaşa, L and Zarnescu, O (2013). In vivo effects of trichostatin A – a histone deacetylase inhibitor – on chromatin remodeling during Triturus cristatus spermatogenesis. Anim Reprod Sci 142(1–2), 8999.CrossRefGoogle ScholarPubMed
Burlibaşa, L, Zarnescu, O, Cucu, N and Gavrilă, L (2008). Chromatin dynamics in Triturus cristatus oogenesis: an epigenetic approach. Zygote 16, 315–26.CrossRefGoogle ScholarPubMed
Burlibaşa, L, Ionescu, AC and Dragusanu, DM (2019). Histone hyperacetylation and DNA methylation interplay during murine spermatogenesis. Zygote 27, 305–14.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, 8792.CrossRefGoogle ScholarPubMed
Godmann, M, Auger, V, Ferraroni-Aguiar, V, Di Sauro, A, Sette, C, Behr, R and Kimmins, S (2007). Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol Rep 77, 754–64.CrossRefGoogle ScholarPubMed
Greer, EL and Shi, Y (2012). Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13, 343–57.CrossRefGoogle ScholarPubMed
Guccione, E, Bassi, C, Casadio, F, Martinato, F, Cesaroni, M, Schuchlautz, H, Lüscher, B and Amati, B (2007). Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449, 933–7.CrossRefGoogle ScholarPubMed
Jenuwein, T and Allis, CD (2001). Translating the histone code. Science 293, 1074–80.CrossRefGoogle ScholarPubMed
Kirmizis, A, Santos-Rosa, H, Penkett, CJ, Singer, MA, Vermeulen, M, Mann, M, Bähler, J, Green, RD and Kouzarides, T (2007). Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449, 928–32.CrossRefGoogle ScholarPubMed
Kouzarides, T (2007). Chromatin modifications and their function. Cell 128, 693705.CrossRefGoogle ScholarPubMed
Lee, DY, Teyssier, C and Strahl, BD (2005). Role of protein methylation in regulation of transcription. Endocr Rev 26, 147–70.CrossRefGoogle ScholarPubMed
Lee, MG, Wynder, C, Bochar, DA, Hakimi, MA, Cooch, N and Shickhattar, R (2006). Functional interplay between histone demethylase and deacetylase enzymes. Mol Cell Biol 26, 6395–402.CrossRefGoogle ScholarPubMed
Li, H, Ilin, S, Wang, W, Duncan, EM, Wysocka, J, Allis, CD and Patel, DJ (2006). Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442, 91–5.CrossRefGoogle ScholarPubMed
Martin, C and Zhang, Y (2005). The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6, 838–49.CrossRefGoogle ScholarPubMed
Mizukami, H, Kim, JD, Tabara, S, Lu, W, Kwon, C., Nakashima, M and Fukamizu, A (2019). KDM5D-mediated H3K4 demethylation is required for sexually dimorphic gene expression in mouse embryonic fibroblasts. J Biochem 165, 335–42.CrossRefGoogle ScholarPubMed
Rea, S, Eisenhaber, F, O’Carroll, D, Strahl, BD, Sun, ZW, Schmid, M, Opravil, S, Mechthel, K, Ponting, CP, Allis, CD and Jenuwein, T (2000). Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406(6796), 593–9.CrossRefGoogle ScholarPubMed
Roosen-Runge, EC (1962). The process of spermatogenesis in mammals. Biol Rev Camb Philos Soc 37, 343–77.CrossRefGoogle ScholarPubMed
Shi, X, Lan, F, Matson, C, Mulligan, P, Whetstine, JR, Cole, PA, Casero, RA and Shi, Y (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–53.CrossRefGoogle ScholarPubMed
Sims, RJ, Chen, CF, Santos-Rosa, H, Kouzarides, T, Patel, SS and Reinberg, D (2006). Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 51, 41789–92.Google Scholar
Song, N, Liu, J, An, S, Nishino, T, Hishikawa, Y and Koji, T (2011). Immunohistochemical analysis of histone H3 modifications in germ cells during mouse spermatogenesis. Acta Histochem Cytochem 44, 183–90.CrossRefGoogle ScholarPubMed
Štiavnická, M, García-Álvarez, O, Ulčová-Gallová, Z, Sutovsky, P, Abril-Parreño, L, Dolejšová, M and Nevoral, J (2020). H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment. Syst Biol Rep Med 66, 311.CrossRefGoogle ScholarPubMed
Taverna, SD, Li, H, Ruthenburg, AJ, Allis, CD and Patel, DJ (2007). How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14, 1025–40.CrossRefGoogle ScholarPubMed
van Leeuwen, F, Gafken, PR and Gottschling, DE (2002). Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745–56.CrossRefGoogle ScholarPubMed
Zhang, Y and Reinberg, D (2001). Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tail. Genes Dev 15, 2343–60.CrossRefGoogle Scholar