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Evolution from XIST-Independent to XIST-Controlled X-Chromosome Inactivation: Epigenetic Modifications in Distantly Related Mammals

Chaumeil, Julie; Waters, Paul D.; Koina, Edda; Gilbert, Clément; Robinson, Terence J.; Marshall Graves, Jennifer A.

Description

X chromosome inactivation (XCI) is the transcriptional silencing of one X in female mammals, balancing expression of X genes between females (XX) and males (XY). In placental mammals non-coding XIST RNA triggers silencing of one X (Xi) and recruits a characteristic suite of epigenetic modifications, including the histone mark H3K27me3. In marsupials, where XIST is missing, H3K27me3 association seems to have different degrees of stability, depending on cell-types and species. However, the...[Show more]

dc.contributor.authorChaumeil, Julie
dc.contributor.authorWaters, Paul D.
dc.contributor.authorKoina, Edda
dc.contributor.authorGilbert, Clément
dc.contributor.authorRobinson, Terence J.
dc.contributor.authorMarshall Graves, Jennifer A.
dc.date.accessioned2015-11-29T23:03:05Z
dc.date.available2015-11-29T23:03:05Z
dc.identifier.issn1932-6203
dc.identifier.urihttp://hdl.handle.net/1885/16899
dc.description.abstractX chromosome inactivation (XCI) is the transcriptional silencing of one X in female mammals, balancing expression of X genes between females (XX) and males (XY). In placental mammals non-coding XIST RNA triggers silencing of one X (Xi) and recruits a characteristic suite of epigenetic modifications, including the histone mark H3K27me3. In marsupials, where XIST is missing, H3K27me3 association seems to have different degrees of stability, depending on cell-types and species. However, the complete suite of histone marks associated with the Xi and their stability throughout cell cycle remain a mystery, as does the evolution of an ancient mammal XCI system. Our extensive immunofluorescence analysis (using antibodies against specific histone modifications) in nuclei of mammals distantly related to human and mouse, revealed a general absence from the mammalian Xi territory of transcription machinery and histone modifications associated with active chromatin. Specific repressive modifications associated with XCI in human and mouse were also observed in elephant (a distantly related placental mammal), as was accumulation of XIST RNA. However, in two marsupial species the Xi either lacked these modifications (H4K20me1), or they were restricted to specific windows of the cell cycle (H3K27me3, H3K9me2). Surprisingly, the marsupial Xi was stably enriched for modifications associated with constitutive heterochromatin in all eukaryotes (H4K20me3, H3K9me3). We propose that marsupial XCI is comparable to a system that evolved in the common therian (marsupial and placental) ancestor. Silent chromatin of the early inactive X was exapted from neighbouring constitutive heterochromatin and, in early placental evolution, was augmented by the rise of XIST and the stable recruitment of specific histone modifications now classically associated with XCI.
dc.description.sponsorshipJulie Chaumeil was supported by the Association pour la Recherche sur le Cancer (France). PDW is supported by an Australian Research Fellowship (DP0987091) awarded by the Australian Research Council. The project was supported by institutional funding from the Research School of Biology, The Australian National University; and Australian Research Council discovery projects (DP0987091 and DP1094868). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
dc.publisherPublic Library of Science
dc.rights© 2011 Chaumeil et al. 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 credited.
dc.sourcePLoS ONE
dc.source.urihttp://journals.plos.org/plosone/article?id=10.1371/journal.pone.0019040
dc.subjectanimals
dc.subjectfemale
dc.subjectfluorescent antibody technique
dc.subjectheterochromatin
dc.subjecthistones
dc.subjecthumans
dc.subjectlysine
dc.subjectmale
dc.subjectmammals
dc.subjectmarsupialia
dc.subjectmethylation
dc.subjectmice
dc.subjectmodels, genetic
dc.subjectrna, long noncoding
dc.subjectrna, untranslated
dc.subjecttranscription, genetic
dc.subjectx chromosome
dc.subjectx chromosome inactivation
dc.subjectepigenesis, genetic
dc.subjectevolution, molecular
dc.subjectphylogeny
dc.titleEvolution from XIST-Independent to XIST-Controlled X-Chromosome Inactivation: Epigenetic Modifications in Distantly Related Mammals
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume6
dc.date.issued2011-04-25
local.identifier.absfor060399
local.identifier.absfor060404
local.identifier.absfor060407
local.identifier.ariespublicationf2965xPUB1879
local.publisher.urlhttp://journals.plos.org/
local.type.statusPublished Version
local.contributor.affiliationChaumeil, Julie, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
local.contributor.affiliationWaters, Paul, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
local.contributor.affiliationKoina, Edda, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
local.contributor.affiliationGilbert, Clement, University of Stellenbosch, South Africa
local.contributor.affiliationRobinson, Terence J, University of Stellenbosch, South Africa
local.contributor.affiliationGraves, Jennifer, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
dc.relationhttp://purl.org/au-research/grants/arc/DP0987091
dc.relationhttp://purl.org/au-research/grants/arc/DP1094868
local.identifier.essn1932-6203
local.bibliographicCitation.issue4
local.bibliographicCitation.startpagee19040
local.bibliographicCitation.lastpage11
local.identifier.doi10.1371/journal.pone.0019040
local.identifier.absseo970106
dc.date.updated2015-12-10T11:21:45Z
local.identifier.scopusID2-s2.0-79955567395
local.identifier.thomsonID000290016800032
CollectionsANU Research Publications

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