Cargando…

Female Meiotic Sex Chromosome Inactivation in Chicken

During meiotic prophase in male mammals, the heterologous X and Y chromosomes remain largely unsynapsed, and meiotic sex chromosome inactivation (MSCI) leads to formation of the transcriptionally silenced XY body. In birds, the heterogametic sex is female, carrying Z and W chromosomes (ZW), whereas...

Descripción completa

Detalles Bibliográficos
Autores principales: Schoenmakers, Sam, Wassenaar, Evelyne, Hoogerbrugge, Jos W., Laven, Joop S. E., Grootegoed, J. Anton, Baarends, Willy M.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2678266/
https://www.ncbi.nlm.nih.gov/pubmed/19461881
http://dx.doi.org/10.1371/journal.pgen.1000466
_version_ 1782166839465345024
author Schoenmakers, Sam
Wassenaar, Evelyne
Hoogerbrugge, Jos W.
Laven, Joop S. E.
Grootegoed, J. Anton
Baarends, Willy M.
author_facet Schoenmakers, Sam
Wassenaar, Evelyne
Hoogerbrugge, Jos W.
Laven, Joop S. E.
Grootegoed, J. Anton
Baarends, Willy M.
author_sort Schoenmakers, Sam
collection PubMed
description During meiotic prophase in male mammals, the heterologous X and Y chromosomes remain largely unsynapsed, and meiotic sex chromosome inactivation (MSCI) leads to formation of the transcriptionally silenced XY body. In birds, the heterogametic sex is female, carrying Z and W chromosomes (ZW), whereas males have the homogametic ZZ constitution. During chicken oogenesis, the heterologous ZW pair reaches a state of complete heterologous synapsis, and this might enable maintenance of transcription of Z- and W chromosomal genes during meiotic prophase. Herein, we show that the ZW pair is transiently silenced, from early pachytene to early diplotene using immunocytochemistry and gene expression analyses. We propose that ZW inactivation is most likely achieved via spreading of heterochromatin from the W on the Z chromosome. Also, persistent meiotic DNA double-strand breaks (DSBs) may contribute to silencing of Z. Surprisingly, γH2AX, a marker of DSBs, and also the earliest histone modification that is associated with XY body formation in mammalian and marsupial spermatocytes, does not cover the ZW during the synapsed stage. However, when the ZW pair starts to desynapse, a second wave of γH2AX accumulates on the unsynapsed regions of Z, which also show a reappearance of the DSB repair protein RAD51. This indicates that repair of meiotic DSBs on the heterologous part of Z is postponed until late pachytene/diplotene, possibly to avoid recombination with regions on the heterologously synapsed W chromosome. Two days after entering diplotene, the Z looses γH2AX and shows reactivation. This is the first report of meiotic sex chromosome inactivation in a species with female heterogamety, providing evidence that this mechanism is not specific to spermatogenesis. It also indicates the presence of an evolutionary force that drives meiotic sex chromosome inactivation independent of the final achievement of synapsis.
format Text
id pubmed-2678266
institution National Center for Biotechnology Information
language English
publishDate 2009
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-26782662009-05-22 Female Meiotic Sex Chromosome Inactivation in Chicken Schoenmakers, Sam Wassenaar, Evelyne Hoogerbrugge, Jos W. Laven, Joop S. E. Grootegoed, J. Anton Baarends, Willy M. PLoS Genet Research Article During meiotic prophase in male mammals, the heterologous X and Y chromosomes remain largely unsynapsed, and meiotic sex chromosome inactivation (MSCI) leads to formation of the transcriptionally silenced XY body. In birds, the heterogametic sex is female, carrying Z and W chromosomes (ZW), whereas males have the homogametic ZZ constitution. During chicken oogenesis, the heterologous ZW pair reaches a state of complete heterologous synapsis, and this might enable maintenance of transcription of Z- and W chromosomal genes during meiotic prophase. Herein, we show that the ZW pair is transiently silenced, from early pachytene to early diplotene using immunocytochemistry and gene expression analyses. We propose that ZW inactivation is most likely achieved via spreading of heterochromatin from the W on the Z chromosome. Also, persistent meiotic DNA double-strand breaks (DSBs) may contribute to silencing of Z. Surprisingly, γH2AX, a marker of DSBs, and also the earliest histone modification that is associated with XY body formation in mammalian and marsupial spermatocytes, does not cover the ZW during the synapsed stage. However, when the ZW pair starts to desynapse, a second wave of γH2AX accumulates on the unsynapsed regions of Z, which also show a reappearance of the DSB repair protein RAD51. This indicates that repair of meiotic DSBs on the heterologous part of Z is postponed until late pachytene/diplotene, possibly to avoid recombination with regions on the heterologously synapsed W chromosome. Two days after entering diplotene, the Z looses γH2AX and shows reactivation. This is the first report of meiotic sex chromosome inactivation in a species with female heterogamety, providing evidence that this mechanism is not specific to spermatogenesis. It also indicates the presence of an evolutionary force that drives meiotic sex chromosome inactivation independent of the final achievement of synapsis. Public Library of Science 2009-05-22 /pmc/articles/PMC2678266/ /pubmed/19461881 http://dx.doi.org/10.1371/journal.pgen.1000466 Text en Schoenmakers et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Schoenmakers, Sam
Wassenaar, Evelyne
Hoogerbrugge, Jos W.
Laven, Joop S. E.
Grootegoed, J. Anton
Baarends, Willy M.
Female Meiotic Sex Chromosome Inactivation in Chicken
title Female Meiotic Sex Chromosome Inactivation in Chicken
title_full Female Meiotic Sex Chromosome Inactivation in Chicken
title_fullStr Female Meiotic Sex Chromosome Inactivation in Chicken
title_full_unstemmed Female Meiotic Sex Chromosome Inactivation in Chicken
title_short Female Meiotic Sex Chromosome Inactivation in Chicken
title_sort female meiotic sex chromosome inactivation in chicken
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2678266/
https://www.ncbi.nlm.nih.gov/pubmed/19461881
http://dx.doi.org/10.1371/journal.pgen.1000466
work_keys_str_mv AT schoenmakerssam femalemeioticsexchromosomeinactivationinchicken
AT wassenaarevelyne femalemeioticsexchromosomeinactivationinchicken
AT hoogerbruggejosw femalemeioticsexchromosomeinactivationinchicken
AT lavenjoopse femalemeioticsexchromosomeinactivationinchicken
AT grootegoedjanton femalemeioticsexchromosomeinactivationinchicken
AT baarendswillym femalemeioticsexchromosomeinactivationinchicken