Imprinted X chromosome inactivation in marsupials

Milton, Ashley M.|||0000-0002-2847-2777; Marin Gual, Laia|||0000-0003-1480-0976; Lister, Nicholas|||0000-0002-6597-4784; McIntyre, Kim L.; Grady, Patrick G. S.; Laird, Melanie K.; Bond, Donna M.; Hore, Timothy A.|||0000-0002-6735-225X; O'Neill, Rachel J.; Pask, Andrew J.|||0000-0002-1900-2263; Renfree, Marilyn B.|||0000-0002-4589-0436; Ruiz Herrera Moreno, Aurora|||0000-0003-3868-6151; Waters, Paul D.|||0000-0002-4689-8747

Imprinted X chromosome inactivation in marsupials

This research examines the contrasting mechanisms of eutherian and marsupial X chromosome inactivation (XCI) by investigating one of the key differences: paternal imprinting in marsupials. Analysis of DNA methylation patterns on the marsupial X chromosome during spermatogenesis revealed that genes o...

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Autores:	Milton, Ashley M.\|\|\|0000-0002-2847-2777, Marin Gual, Laia\|\|\|0000-0003-1480-0976, Lister, Nicholas\|\|\|0000-0002-6597-4784, McIntyre, Kim L., Grady, Patrick G. S., Laird, Melanie K., Bond, Donna M., Hore, Timothy A.\|\|\|0000-0002-6735-225X, O'Neill, Rachel J., Pask, Andrew J.\|\|\|0000-0002-1900-2263, Renfree, Marilyn B.\|\|\|0000-0002-4589-0436, Ruiz Herrera Moreno, Aurora\|\|\|0000-0003-3868-6151, Waters, Paul D.\|\|\|0000-0002-4689-8747
Tipo de recurso:	artículo
Fecha de publicación:	2024
País:	España
Institución:	Universitat Autònoma de Barcelona
Repositorio:	Dipòsit Digital de Documents de la UAB
Idioma:	inglés
OAI Identifier:	oai:ddd.uab.cat:317822
Acceso en línea:	https://ddd.uab.cat/record/317822 https://dx.doi.org/urn:doi:10.1073/pnas.2412185121
Access Level:	acceso abierto
Palabra clave:	DNA methylation Marsupial Imprinting X chromosome inactivation Spermatogenesis

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spelling	Imprinted X chromosome inactivation in marsupialsThe paternal X arrives at the egg with a silent DNA methylation profileMilton, Ashley M.\|\|\|0000-0002-2847-2777Marin Gual, Laia\|\|\|0000-0003-1480-0976Lister, Nicholas\|\|\|0000-0002-6597-4784McIntyre, Kim L.Grady, Patrick G. S.Laird, Melanie K.Bond, Donna M.Hore, Timothy A.\|\|\|0000-0002-6735-225XO'Neill, Rachel J.Pask, Andrew J.\|\|\|0000-0002-1900-2263Renfree, Marilyn B.\|\|\|0000-0002-4589-0436Ruiz Herrera Moreno, Aurora\|\|\|0000-0003-3868-6151Waters, Paul D.\|\|\|0000-0002-4689-8747DNA methylationMarsupialImprintingX chromosome inactivationSpermatogenesisThis research examines the contrasting mechanisms of eutherian and marsupial X chromosome inactivation (XCI) by investigating one of the key differences: paternal imprinting in marsupials. Analysis of DNA methylation patterns on the marsupial X chromosome during spermatogenesis revealed that genes on the paternal X chromosome exhibit a DNA methylation profile akin to the "silent" profile of genes on inactive X chromosomes in female somatic cells. This observation suggests a preexisting, silent DNA methylation landscape on the paternal X chromosome upon fertilization, which we hypothesize is the long sought-after imprint governing paternal XCI in marsupials. X chromosome inactivation (XCI) is an epigenetic process that results in the transcriptional silencing of one X chromosome in the somatic cells of females. This phenomenon is common to both eutherian and marsupial mammals, but there are fundamental differences. In eutherians, the X chosen for silencing is random. DNA methylation on the eutherian inactive X is high at transcription start sites (TSSs) and their flanking regions, resulting in universally high DNA methylation. This contrasts XCI in marsupials where the paternally derived X is always silenced, and in which DNA methylation is low at TSSs and flanking regions. Here, we examined the DNA methylation status of the tammar wallaby X chromosome during spermatogenesis to determine the DNA methylation profile of the paternal X prior to and at fertilization. Whole genome enzymatic methylation sequencing was carried out on enriched flow-sorted populations of premeiotic, meiotic, and postmeiotic cells. We observed that the X displayed a pattern of DNA methylation from spermatogonia to mature sperm that reflected the inactive X in female somatic tissue. Therefore, the paternal X chromosome arrives at the egg with a DNA methylation profile that reflects the transcriptionally silent X in adult female somatic tissue. We present this epigenetic signature as a candidate for the long sought-after imprint for paternal XCI in marsupials. 22024-01-0120242024-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/317822https://dx.doi.org/urn:doi:10.1073/pnas.2412185121reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengAgencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2020-112557GB-I00Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2021/SGR-00122open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, i la comunicació pública de l'obra, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original. No es permet la creació d'obres derivades.https://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:3178222026-06-06T12:50:31Z
dc.title.none.fl_str_mv	Imprinted X chromosome inactivation in marsupials The paternal X arrives at the egg with a silent DNA methylation profile
title	Imprinted X chromosome inactivation in marsupials
spellingShingle	Imprinted X chromosome inactivation in marsupials Milton, Ashley M.\|\|\|0000-0002-2847-2777 DNA methylation Marsupial Imprinting X chromosome inactivation Spermatogenesis
title_short	Imprinted X chromosome inactivation in marsupials
title_full	Imprinted X chromosome inactivation in marsupials
title_fullStr	Imprinted X chromosome inactivation in marsupials
title_full_unstemmed	Imprinted X chromosome inactivation in marsupials
title_sort	Imprinted X chromosome inactivation in marsupials
dc.creator.none.fl_str_mv	Milton, Ashley M.\|\|\|0000-0002-2847-2777 Marin Gual, Laia\|\|\|0000-0003-1480-0976 Lister, Nicholas\|\|\|0000-0002-6597-4784 McIntyre, Kim L. Grady, Patrick G. S. Laird, Melanie K. Bond, Donna M. Hore, Timothy A.\|\|\|0000-0002-6735-225X O'Neill, Rachel J. Pask, Andrew J.\|\|\|0000-0002-1900-2263 Renfree, Marilyn B.\|\|\|0000-0002-4589-0436 Ruiz Herrera Moreno, Aurora\|\|\|0000-0003-3868-6151 Waters, Paul D.\|\|\|0000-0002-4689-8747
author	Milton, Ashley M.\|\|\|0000-0002-2847-2777
author_facet	Milton, Ashley M.\|\|\|0000-0002-2847-2777 Marin Gual, Laia\|\|\|0000-0003-1480-0976 Lister, Nicholas\|\|\|0000-0002-6597-4784 McIntyre, Kim L. Grady, Patrick G. S. Laird, Melanie K. Bond, Donna M. Hore, Timothy A.\|\|\|0000-0002-6735-225X O'Neill, Rachel J. Pask, Andrew J.\|\|\|0000-0002-1900-2263 Renfree, Marilyn B.\|\|\|0000-0002-4589-0436 Ruiz Herrera Moreno, Aurora\|\|\|0000-0003-3868-6151 Waters, Paul D.\|\|\|0000-0002-4689-8747
author_role	author
author2	Marin Gual, Laia\|\|\|0000-0003-1480-0976 Lister, Nicholas\|\|\|0000-0002-6597-4784 McIntyre, Kim L. Grady, Patrick G. S. Laird, Melanie K. Bond, Donna M. Hore, Timothy A.\|\|\|0000-0002-6735-225X O'Neill, Rachel J. Pask, Andrew J.\|\|\|0000-0002-1900-2263 Renfree, Marilyn B.\|\|\|0000-0002-4589-0436 Ruiz Herrera Moreno, Aurora\|\|\|0000-0003-3868-6151 Waters, Paul D.\|\|\|0000-0002-4689-8747
author2_role	author author author author author author author author author author author author
dc.subject.none.fl_str_mv	DNA methylation Marsupial Imprinting X chromosome inactivation Spermatogenesis
topic	DNA methylation Marsupial Imprinting X chromosome inactivation Spermatogenesis
description	This research examines the contrasting mechanisms of eutherian and marsupial X chromosome inactivation (XCI) by investigating one of the key differences: paternal imprinting in marsupials. Analysis of DNA methylation patterns on the marsupial X chromosome during spermatogenesis revealed that genes on the paternal X chromosome exhibit a DNA methylation profile akin to the "silent" profile of genes on inactive X chromosomes in female somatic cells. This observation suggests a preexisting, silent DNA methylation landscape on the paternal X chromosome upon fertilization, which we hypothesize is the long sought-after imprint governing paternal XCI in marsupials. X chromosome inactivation (XCI) is an epigenetic process that results in the transcriptional silencing of one X chromosome in the somatic cells of females. This phenomenon is common to both eutherian and marsupial mammals, but there are fundamental differences. In eutherians, the X chosen for silencing is random. DNA methylation on the eutherian inactive X is high at transcription start sites (TSSs) and their flanking regions, resulting in universally high DNA methylation. This contrasts XCI in marsupials where the paternally derived X is always silenced, and in which DNA methylation is low at TSSs and flanking regions. Here, we examined the DNA methylation status of the tammar wallaby X chromosome during spermatogenesis to determine the DNA methylation profile of the paternal X prior to and at fertilization. Whole genome enzymatic methylation sequencing was carried out on enriched flow-sorted populations of premeiotic, meiotic, and postmeiotic cells. We observed that the X displayed a pattern of DNA methylation from spermatogonia to mature sperm that reflected the inactive X in female somatic tissue. Therefore, the paternal X chromosome arrives at the egg with a DNA methylation profile that reflects the transcriptionally silent X in adult female somatic tissue. We present this epigenetic signature as a candidate for the long sought-after imprint for paternal XCI in marsupials.
publishDate	2024
dc.date.none.fl_str_mv	2 2024-01-01 2024 2024-01-01
dc.type.none.fl_str_mv	Article http://purl.org/coar/resource_type/c_6501 VoR http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv	info:eu-repo/semantics/article
format	article
dc.identifier.none.fl_str_mv	https://ddd.uab.cat/record/317822 https://dx.doi.org/urn:doi:10.1073/pnas.2412185121
url	https://ddd.uab.cat/record/317822 https://dx.doi.org/urn:doi:10.1073/pnas.2412185121
dc.language.none.fl_str_mv	Inglés eng
language_invalid_str_mv	Inglés
language	eng
dc.relation.none.fl_str_mv	Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2020-112557GB-I00 Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2021/SGR-00122
dc.rights.none.fl_str_mv	open access http://purl.org/coar/access_right/c_abf2 https://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv	info:eu-repo/semantics/openAccess
rights_invalid_str_mv	open access http://purl.org/coar/access_right/c_abf2 https://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv	openAccess
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dc.source.none.fl_str_mv	reponame:Dipòsit Digital de Documents de la UAB instname:Universitat Autònoma de Barcelona
instname_str	Universitat Autònoma de Barcelona
reponame_str	Dipòsit Digital de Documents de la UAB
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Imprinted X chromosome inactivation in marsupials

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