Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression

Autores
Nardelli, Sheila C.; Silmon de Monerri, Natalie C.; Vanagas, Laura; Wang, Xiaonan; Tampaki, Zoi; Sullivan, William J.; Ángel, Sergio Oscar; Kim, Kami
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Toxoplasma gondii is a protozoan parasite that differentiates from acute tachyzoite stages to latent bradyzoite forms in response to environmental cues that modify the epigenome. We studied the distribution of the histone variants CenH3, H3.3, H2A.X, H2A.Z and H2B.Z, by genome-wide chromatin immunoprecipitation to understand the role of variant histones in developmental transitions of T. gondii parasites. Results: H3.3 and H2A.X were detected in telomere and telomere associated sequences, whereas H3.3, H2A.X and CenH3 were enriched in centromeres. Histones H2A.Z and H2B.Z colocalize with the transcriptional activation mark H3K4me3 in promoter regions surrounding the nucleosome-free region upstream of the transcription start site. The H2B.Z/H2A.Z histone pair also localizes to the gene bodies of genes that are silent but poised for activation, including bradyzoite stage-specific genes. The majority of H2A.X and H2A.Z/H2B.Z loci do not overlap, consistent with variant histones demarcating specific functional regions of chromatin. The extent of enrichment of H2A.Z/H2B.Z (and H3.3 and H2A.X) within the entire gene (5’UTR and gene body) reflects the timing of gene expression during the cell cycle, suggesting that dynamic turnover of H2B.Z/H2A.Z occurs during the tachyzoite cell cycle. Thus, the distribution of the variant histone H2A.Z/H2B.Z dimer defines active and developmentally silenced regions of the T. gondii epigenome including genes that are poised for expression. Conclusions: Histone variants mark functional regions of parasite genomes with the dynamic placement of the H2A.Z/H2B.Z dimer implicated as an evolutionarily conserved regulator of parasite and eukaryotic differentiation.
Fil: Nardelli, Sheila C.. Albert Einstein College Of Medicine; Estados Unidos
Fil: Silmon de Monerri, Natalie C.. Albert Einstein College Of Medicine; Estados Unidos
Fil: Vanagas, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Wang, Xiaonan. University of Cambridge; Reino Unido
Fil: Tampaki, Zoi. Albert Einstein College Of Medicine; Estados Unidos
Fil: Sullivan, William J.. Indiana University; Estados Unidos
Fil: Ángel, Sergio Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Kim, Kami. Albert Einstein College Of Medicine; Estados Unidos
Materia
APICOMPLEXA
CHIP-SEQ
EPIGENETIC
HISTONES
PARASITES
TOXOPLASMA
TRANSCRIPTIONAL REGULATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/215159

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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expressionNardelli, Sheila C.Silmon de Monerri, Natalie C.Vanagas, LauraWang, XiaonanTampaki, ZoiSullivan, William J.Ángel, Sergio OscarKim, KamiAPICOMPLEXACHIP-SEQEPIGENETICHISTONESPARASITESTOXOPLASMATRANSCRIPTIONAL REGULATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background: Toxoplasma gondii is a protozoan parasite that differentiates from acute tachyzoite stages to latent bradyzoite forms in response to environmental cues that modify the epigenome. We studied the distribution of the histone variants CenH3, H3.3, H2A.X, H2A.Z and H2B.Z, by genome-wide chromatin immunoprecipitation to understand the role of variant histones in developmental transitions of T. gondii parasites. Results: H3.3 and H2A.X were detected in telomere and telomere associated sequences, whereas H3.3, H2A.X and CenH3 were enriched in centromeres. Histones H2A.Z and H2B.Z colocalize with the transcriptional activation mark H3K4me3 in promoter regions surrounding the nucleosome-free region upstream of the transcription start site. The H2B.Z/H2A.Z histone pair also localizes to the gene bodies of genes that are silent but poised for activation, including bradyzoite stage-specific genes. The majority of H2A.X and H2A.Z/H2B.Z loci do not overlap, consistent with variant histones demarcating specific functional regions of chromatin. The extent of enrichment of H2A.Z/H2B.Z (and H3.3 and H2A.X) within the entire gene (5’UTR and gene body) reflects the timing of gene expression during the cell cycle, suggesting that dynamic turnover of H2B.Z/H2A.Z occurs during the tachyzoite cell cycle. Thus, the distribution of the variant histone H2A.Z/H2B.Z dimer defines active and developmentally silenced regions of the T. gondii epigenome including genes that are poised for expression. Conclusions: Histone variants mark functional regions of parasite genomes with the dynamic placement of the H2A.Z/H2B.Z dimer implicated as an evolutionarily conserved regulator of parasite and eukaryotic differentiation.Fil: Nardelli, Sheila C.. Albert Einstein College Of Medicine; Estados UnidosFil: Silmon de Monerri, Natalie C.. Albert Einstein College Of Medicine; Estados UnidosFil: Vanagas, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); ArgentinaFil: Wang, Xiaonan. University of Cambridge; Reino UnidoFil: Tampaki, Zoi. Albert Einstein College Of Medicine; Estados UnidosFil: Sullivan, William J.. Indiana University; Estados UnidosFil: Ángel, Sergio Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); ArgentinaFil: Kim, Kami. Albert Einstein College Of Medicine; Estados UnidosBioMed Central2022-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/215159Nardelli, Sheila C.; Silmon de Monerri, Natalie C.; Vanagas, Laura; Wang, Xiaonan; Tampaki, Zoi; et al.; Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression; BioMed Central; BMC Genomics; 23; 1; 2-2022; 1-171471-2164CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1186/s12864-022-08338-6info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:54:15Zoai:ri.conicet.gov.ar:11336/215159instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:54:15.42CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
title Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
spellingShingle Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
Nardelli, Sheila C.
APICOMPLEXA
CHIP-SEQ
EPIGENETIC
HISTONES
PARASITES
TOXOPLASMA
TRANSCRIPTIONAL REGULATION
title_short Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
title_full Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
title_fullStr Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
title_full_unstemmed Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
title_sort Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression
dc.creator.none.fl_str_mv Nardelli, Sheila C.
Silmon de Monerri, Natalie C.
Vanagas, Laura
Wang, Xiaonan
Tampaki, Zoi
Sullivan, William J.
Ángel, Sergio Oscar
Kim, Kami
author Nardelli, Sheila C.
author_facet Nardelli, Sheila C.
Silmon de Monerri, Natalie C.
Vanagas, Laura
Wang, Xiaonan
Tampaki, Zoi
Sullivan, William J.
Ángel, Sergio Oscar
Kim, Kami
author_role author
author2 Silmon de Monerri, Natalie C.
Vanagas, Laura
Wang, Xiaonan
Tampaki, Zoi
Sullivan, William J.
Ángel, Sergio Oscar
Kim, Kami
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv APICOMPLEXA
CHIP-SEQ
EPIGENETIC
HISTONES
PARASITES
TOXOPLASMA
TRANSCRIPTIONAL REGULATION
topic APICOMPLEXA
CHIP-SEQ
EPIGENETIC
HISTONES
PARASITES
TOXOPLASMA
TRANSCRIPTIONAL REGULATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background: Toxoplasma gondii is a protozoan parasite that differentiates from acute tachyzoite stages to latent bradyzoite forms in response to environmental cues that modify the epigenome. We studied the distribution of the histone variants CenH3, H3.3, H2A.X, H2A.Z and H2B.Z, by genome-wide chromatin immunoprecipitation to understand the role of variant histones in developmental transitions of T. gondii parasites. Results: H3.3 and H2A.X were detected in telomere and telomere associated sequences, whereas H3.3, H2A.X and CenH3 were enriched in centromeres. Histones H2A.Z and H2B.Z colocalize with the transcriptional activation mark H3K4me3 in promoter regions surrounding the nucleosome-free region upstream of the transcription start site. The H2B.Z/H2A.Z histone pair also localizes to the gene bodies of genes that are silent but poised for activation, including bradyzoite stage-specific genes. The majority of H2A.X and H2A.Z/H2B.Z loci do not overlap, consistent with variant histones demarcating specific functional regions of chromatin. The extent of enrichment of H2A.Z/H2B.Z (and H3.3 and H2A.X) within the entire gene (5’UTR and gene body) reflects the timing of gene expression during the cell cycle, suggesting that dynamic turnover of H2B.Z/H2A.Z occurs during the tachyzoite cell cycle. Thus, the distribution of the variant histone H2A.Z/H2B.Z dimer defines active and developmentally silenced regions of the T. gondii epigenome including genes that are poised for expression. Conclusions: Histone variants mark functional regions of parasite genomes with the dynamic placement of the H2A.Z/H2B.Z dimer implicated as an evolutionarily conserved regulator of parasite and eukaryotic differentiation.
Fil: Nardelli, Sheila C.. Albert Einstein College Of Medicine; Estados Unidos
Fil: Silmon de Monerri, Natalie C.. Albert Einstein College Of Medicine; Estados Unidos
Fil: Vanagas, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Wang, Xiaonan. University of Cambridge; Reino Unido
Fil: Tampaki, Zoi. Albert Einstein College Of Medicine; Estados Unidos
Fil: Sullivan, William J.. Indiana University; Estados Unidos
Fil: Ángel, Sergio Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Kim, Kami. Albert Einstein College Of Medicine; Estados Unidos
description Background: Toxoplasma gondii is a protozoan parasite that differentiates from acute tachyzoite stages to latent bradyzoite forms in response to environmental cues that modify the epigenome. We studied the distribution of the histone variants CenH3, H3.3, H2A.X, H2A.Z and H2B.Z, by genome-wide chromatin immunoprecipitation to understand the role of variant histones in developmental transitions of T. gondii parasites. Results: H3.3 and H2A.X were detected in telomere and telomere associated sequences, whereas H3.3, H2A.X and CenH3 were enriched in centromeres. Histones H2A.Z and H2B.Z colocalize with the transcriptional activation mark H3K4me3 in promoter regions surrounding the nucleosome-free region upstream of the transcription start site. The H2B.Z/H2A.Z histone pair also localizes to the gene bodies of genes that are silent but poised for activation, including bradyzoite stage-specific genes. The majority of H2A.X and H2A.Z/H2B.Z loci do not overlap, consistent with variant histones demarcating specific functional regions of chromatin. The extent of enrichment of H2A.Z/H2B.Z (and H3.3 and H2A.X) within the entire gene (5’UTR and gene body) reflects the timing of gene expression during the cell cycle, suggesting that dynamic turnover of H2B.Z/H2A.Z occurs during the tachyzoite cell cycle. Thus, the distribution of the variant histone H2A.Z/H2B.Z dimer defines active and developmentally silenced regions of the T. gondii epigenome including genes that are poised for expression. Conclusions: Histone variants mark functional regions of parasite genomes with the dynamic placement of the H2A.Z/H2B.Z dimer implicated as an evolutionarily conserved regulator of parasite and eukaryotic differentiation.
publishDate 2022
dc.date.none.fl_str_mv 2022-02
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/215159
Nardelli, Sheila C.; Silmon de Monerri, Natalie C.; Vanagas, Laura; Wang, Xiaonan; Tampaki, Zoi; et al.; Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression; BioMed Central; BMC Genomics; 23; 1; 2-2022; 1-17
1471-2164
CONICET Digital
CONICET
url http://hdl.handle.net/11336/215159
identifier_str_mv Nardelli, Sheila C.; Silmon de Monerri, Natalie C.; Vanagas, Laura; Wang, Xiaonan; Tampaki, Zoi; et al.; Genome-wide localization of histone variants in Toxoplasma gondii implicates variant exchange in stage-specific gene expression; BioMed Central; BMC Genomics; 23; 1; 2-2022; 1-17
1471-2164
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1186/s12864-022-08338-6
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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