H4K5 Butyrylation Coexist with Acetylation during Human Spermiogenesis and Are Retained in the Mature Sperm Chromatin
Male germ cells experience a drastic chromatin remodeling through the nucleo-histone to nucleo-protamine (NH-NP) transition necessary for proper sperm functionality. Post-translational modifications (PTMs) of H4 Lys5, such as acetylation (H4K5ac), play a crucial role in epigenetic control of nucleos...
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| Veröffentlicht in: | International journal of molecular sciences 2022-10, Vol.23 (20), p.12398 |
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| creator | de la Iglesia, Alberto Jauregi, Paula Jodar, Meritxell Barrachina, Ferran Ded, Lukas Mallofré, Carme Rodríguez-Carunchio, Leonardo Corral, Juan Manuel Ballescà, Josep Lluís Komrskova, Katerina Castillo, Judit Oliva, Rafael |
| description | Male germ cells experience a drastic chromatin remodeling through the nucleo-histone to nucleo-protamine (NH-NP) transition necessary for proper sperm functionality. Post-translational modifications (PTMs) of H4 Lys5, such as acetylation (H4K5ac), play a crucial role in epigenetic control of nucleosome disassembly facilitating protamine incorporation into paternal DNA. It has been shown that butyrylation on the same residue (H4K5bu) participates in temporal regulation of NH-NP transition in mice, delaying the bromodomain testis specific protein (BRDT)-dependent nucleosome disassembly and potentially marking retained nucleosomes. However, no information was available so far on this modification in human sperm. Here, we report a dual behavior of H4K5bu and H4K5ac in human normal spermatogenesis, suggesting a specific role of H4K5bu during spermatid elongation, coexisting with H4K5ac although with different starting points. This pattern is stable under different testicular pathologies, suggesting a highly conserved function of these modifications. Despite a drastic decrease of both PTMs in condensed spermatids, they are retained in ejaculated sperm, with 30% of non-colocalizing nucleosome clusters, which could reflect differential paternal genome retention. Whereas no apparent effect of these PTMs was observed associated with sperm quality, their presence in mature sperm could entail a potential role in the zygote. |
| doi_str_mv | 10.3390/ijms232012398 |
| format | Article |
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Post-translational modifications (PTMs) of H4 Lys5, such as acetylation (H4K5ac), play a crucial role in epigenetic control of nucleosome disassembly facilitating protamine incorporation into paternal DNA. It has been shown that butyrylation on the same residue (H4K5bu) participates in temporal regulation of NH-NP transition in mice, delaying the bromodomain testis specific protein (BRDT)-dependent nucleosome disassembly and potentially marking retained nucleosomes. However, no information was available so far on this modification in human sperm. Here, we report a dual behavior of H4K5bu and H4K5ac in human normal spermatogenesis, suggesting a specific role of H4K5bu during spermatid elongation, coexisting with H4K5ac although with different starting points. This pattern is stable under different testicular pathologies, suggesting a highly conserved function of these modifications. Despite a drastic decrease of both PTMs in condensed spermatids, they are retained in ejaculated sperm, with 30% of non-colocalizing nucleosome clusters, which could reflect differential paternal genome retention. Whereas no apparent effect of these PTMs was observed associated with sperm quality, their presence in mature sperm could entail a potential role in the zygote.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms232012398</identifier><language>eng</language><publisher>Basel: MDPI AG</publisher><subject>Acetylation ; Chromatin remodeling ; Dismantling ; Elongation ; Epigenetics ; Genomes ; Germ cells ; Histones ; Nucleosomes ; Patients ; Post-translation ; Protamine ; Retention ; Sperm ; Spermatids ; Spermatogenesis ; Spermiogenesis ; Testicular cancer ; Zygotes</subject><ispartof>International journal of molecular sciences, 2022-10, Vol.23 (20), p.12398</ispartof><rights>2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). 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Post-translational modifications (PTMs) of H4 Lys5, such as acetylation (H4K5ac), play a crucial role in epigenetic control of nucleosome disassembly facilitating protamine incorporation into paternal DNA. It has been shown that butyrylation on the same residue (H4K5bu) participates in temporal regulation of NH-NP transition in mice, delaying the bromodomain testis specific protein (BRDT)-dependent nucleosome disassembly and potentially marking retained nucleosomes. However, no information was available so far on this modification in human sperm. Here, we report a dual behavior of H4K5bu and H4K5ac in human normal spermatogenesis, suggesting a specific role of H4K5bu during spermatid elongation, coexisting with H4K5ac although with different starting points. This pattern is stable under different testicular pathologies, suggesting a highly conserved function of these modifications. Despite a drastic decrease of both PTMs in condensed spermatids, they are retained in ejaculated sperm, with 30% of non-colocalizing nucleosome clusters, which could reflect differential paternal genome retention. Whereas no apparent effect of these PTMs was observed associated with sperm quality, their presence in mature sperm could entail a potential role in the zygote.</description><subject>Acetylation</subject><subject>Chromatin remodeling</subject><subject>Dismantling</subject><subject>Elongation</subject><subject>Epigenetics</subject><subject>Genomes</subject><subject>Germ cells</subject><subject>Histones</subject><subject>Nucleosomes</subject><subject>Patients</subject><subject>Post-translation</subject><subject>Protamine</subject><subject>Retention</subject><subject>Sperm</subject><subject>Spermatids</subject><subject>Spermatogenesis</subject><subject>Spermiogenesis</subject><subject>Testicular cancer</subject><subject>Zygotes</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkUtLxDAUhYsoqKNL9wE3bqppHk2zEcZBHVERfKxDbG9nMrTJmIc6_976RF3dyz0fh3M5WbZX4ENKJT4yiz4QSnBBqKzWsq2CEZJjXIr1X_tmth3CAuMB5HIrS1N2ydFJiiu_6nQ0zqKJg1cTInoxcY7GNcRvoUne2Bmapl5bdLcE3xs3AwvBBKRtg8Ye0C1EbSw0yFgU54CudUzD-YNGk7l3_eBld7KNVncBdr_mKHs4O72fTPOrm_OLyfgqr6kkMeeyFKXUrGkob4e4lYACeNU-liWrpeA1MA1lxUE3wFpR0bYusIBWay1kCZyOsuNP32V67KGpwUavO7X0ptd-pZw26q9izVzN3LOSJWa8qAaDgy8D754ShKh6E2roOm3BpaCIIJITLqQc0P1_6MIlb4f33qmKSSIrNlD5J1V7F4KH9idMgdV7i-pPi_QNG86Sxg</recordid><startdate>20221017</startdate><enddate>20221017</enddate><creator>de la Iglesia, Alberto</creator><creator>Jauregi, Paula</creator><creator>Jodar, Meritxell</creator><creator>Barrachina, Ferran</creator><creator>Ded, Lukas</creator><creator>Mallofré, Carme</creator><creator>Rodríguez-Carunchio, Leonardo</creator><creator>Corral, Juan Manuel</creator><creator>Ballescà, Josep Lluís</creator><creator>Komrskova, Katerina</creator><creator>Castillo, Judit</creator><creator>Oliva, Rafael</creator><general>MDPI AG</general><general>MDPI</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4876-2410</orcidid><orcidid>https://orcid.org/0000-0002-9407-2675</orcidid><orcidid>https://orcid.org/0000-0003-1053-4025</orcidid><orcidid>https://orcid.org/0000-0002-6837-2148</orcidid><orcidid>https://orcid.org/0000-0002-3272-0163</orcidid><orcidid>https://orcid.org/0000-0003-3475-2086</orcidid><orcidid>https://orcid.org/0000-0003-3138-4142</orcidid></search><sort><creationdate>20221017</creationdate><title>H4K5 Butyrylation Coexist with Acetylation during Human Spermiogenesis and Are Retained in the Mature Sperm Chromatin</title><author>de la Iglesia, Alberto ; 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| subjects | Acetylation Chromatin remodeling Dismantling Elongation Epigenetics Genomes Germ cells Histones Nucleosomes Patients Post-translation Protamine Retention Sperm Spermatids Spermatogenesis Spermiogenesis Testicular cancer Zygotes |
| title | H4K5 Butyrylation Coexist with Acetylation during Human Spermiogenesis and Are Retained in the Mature Sperm Chromatin |
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