Comprehensive Histone Phosphorylation Analysis and Identification of Pf14-3-3 Protein as a Histone H3 Phosphorylation Reader in Malaria Parasites
Identifieur interne : 002908 ( Pmc/Curation ); précédent : 002907; suivant : 002909Comprehensive Histone Phosphorylation Analysis and Identification of Pf14-3-3 Protein as a Histone H3 Phosphorylation Reader in Malaria Parasites
Auteurs : Eeshita G. Dastidar [France] ; Kristina Dzeyk [Allemagne] ; Jeroen Krijgsveld [Allemagne] ; Nicholas A. Malmquist [France] ; Christian Doerig [Australie] ; Artur Scherf [France] ; Jose-Juan Lopez-Rubio [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2013.
Abstract
The important role of histone posttranslational modifications, particularly methylation and acetylation, in
Url:
DOI: 10.1371/journal.pone.0053179
PubMed: 23308157
PubMed Central: 3538786
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Comprehensive Histone Phosphorylation Analysis and Identification of Pf14-3-3 Protein as a Histone H3 Phosphorylation Reader in Malaria Parasites</title><author><name sortKey="Dastidar, Eeshita G" sort="Dastidar, Eeshita G" uniqKey="Dastidar E" first="Eeshita G." last="Dastidar">Eeshita G. Dastidar</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Dzeyk, Kristina" sort="Dzeyk, Kristina" uniqKey="Dzeyk K" first="Kristina" last="Dzeyk">Kristina Dzeyk</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Krijgsveld, Jeroen" sort="Krijgsveld, Jeroen" uniqKey="Krijgsveld J" first="Jeroen" last="Krijgsveld">Jeroen Krijgsveld</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Malmquist, Nicholas A" sort="Malmquist, Nicholas A" uniqKey="Malmquist N" first="Nicholas A." last="Malmquist">Nicholas A. Malmquist</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Doerig, Christian" sort="Doerig, Christian" uniqKey="Doerig C" first="Christian" last="Doerig">Christian Doerig</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Microbiology, Monash University, Clayton, Victoria</wicri:regionArea></affiliation></author><author><name sortKey="Scherf, Artur" sort="Scherf, Artur" uniqKey="Scherf A" first="Artur" last="Scherf">Artur Scherf</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Lopez Rubio, Jose Juan" sort="Lopez Rubio, Jose Juan" uniqKey="Lopez Rubio J" first="Jose-Juan" last="Lopez-Rubio">Jose-Juan Lopez-Rubio</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23308157</idno><idno type="pmc">3538786</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3538786</idno><idno type="RBID">PMC:3538786</idno><idno type="doi">10.1371/journal.pone.0053179</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">002A58</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002A58</idno><idno type="wicri:Area/Pmc/Curation">002908</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002908</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Comprehensive Histone Phosphorylation Analysis and Identification of Pf14-3-3 Protein as a Histone H3 Phosphorylation Reader in Malaria Parasites</title><author><name sortKey="Dastidar, Eeshita G" sort="Dastidar, Eeshita G" uniqKey="Dastidar E" first="Eeshita G." last="Dastidar">Eeshita G. Dastidar</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Dzeyk, Kristina" sort="Dzeyk, Kristina" uniqKey="Dzeyk K" first="Kristina" last="Dzeyk">Kristina Dzeyk</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Krijgsveld, Jeroen" sort="Krijgsveld, Jeroen" uniqKey="Krijgsveld J" first="Jeroen" last="Krijgsveld">Jeroen Krijgsveld</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg</wicri:regionArea></affiliation></author><author><name sortKey="Malmquist, Nicholas A" sort="Malmquist, Nicholas A" uniqKey="Malmquist N" first="Nicholas A." last="Malmquist">Nicholas A. Malmquist</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Doerig, Christian" sort="Doerig, Christian" uniqKey="Doerig C" first="Christian" last="Doerig">Christian Doerig</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Microbiology, Monash University, Clayton, Victoria</wicri:regionArea></affiliation></author><author><name sortKey="Scherf, Artur" sort="Scherf, Artur" uniqKey="Scherf A" first="Artur" last="Scherf">Artur Scherf</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Lopez Rubio, Jose Juan" sort="Lopez Rubio, Jose Juan" uniqKey="Lopez Rubio J" first="Jose-Juan" last="Lopez-Rubio">Jose-Juan Lopez-Rubio</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The important role of histone posttranslational modifications, particularly methylation and acetylation, in <italic>Plasmodium falciparum</italic> gene regulation has been established. However, the role of histone phosphorylation remains understudied. Here, we investigate histone phosphorylation utilizing liquid chromatography and tandem mass spectrometry to analyze histones extracted from asexual blood stages using two improved protocols to enhance preservation of PTMs. Enrichment for phosphopeptides lead to the detection of 14 histone phospho-modifications in <italic>P. falciparum</italic>. The majority of phosphorylation sites were observed at the N-terminal regions of various histones and were frequently observed adjacent to acetylated lysines. We also report the identification of one novel member of the <italic>P. falciparum</italic> histone phosphosite binding protein repertoire, Pf14-3-3I. Recombinant Pf14-3-3I protein bound to purified parasite histones. <italic>In silico</italic> structural analysis of Pf14-3-3 proteins revealed that residues responsible for binding to histone H3 S10ph and/or S28ph are conserved at the primary and the tertiary structure levels. Using a battery of H3 specific phosphopeptides, we demonstrate that Pf14-3-3I preferentially binds to H3S28ph over H3S10ph, independent of modification of neighbouring residues like H3S10phK14ac and H3S28phS32ph. Our data provide key insight into histone phosphorylation sites. The identification of a second member of the histone modification reading machinery suggests a widespread use of histone phosphorylation in the control of various nuclear processes in malaria parasites.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Llinas, M" uniqKey="Llinas M">M Llinas</name></author><author><name sortKey="Deitsch, Kw" uniqKey="Deitsch K">KW Deitsch</name></author><author><name sortKey="Voss, Ts" uniqKey="Voss T">TS Voss</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bartfai, R" uniqKey="Bartfai R">R Bartfai</name></author><author><name sortKey="Hoeijmakers, Wa" uniqKey="Hoeijmakers W">WA Hoeijmakers</name></author><author><name sortKey="Salcedo Amaya, Am" uniqKey="Salcedo Amaya A">AM Salcedo-Amaya</name></author><author><name sortKey="Smits, Ah" uniqKey="Smits A">AH Smits</name></author><author><name sortKey="Janssen Megens, E" uniqKey="Janssen Megens E">E 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23308157</article-id><article-id pub-id-type="pmc">3538786</article-id><article-id pub-id-type="publisher-id">PONE-D-12-24776</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0053179</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Genetics</subject><subj-group><subject>Epigenetics</subject><subj-group><subject>Histone Modification</subject><subject>Chromatin</subject></subj-group></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Protozoology</subject><subj-group><subject>Parastic Protozoans</subject><subj-group><subject>Plasmodium Falciparum</subject></subj-group></subj-group></subj-group><subj-group><subject>Pathogenesis</subject></subj-group></subj-group><subj-group><subject>Molecular Cell Biology</subject><subj-group><subject>Gene Expression</subject><subj-group><subject>Histone Modification</subject></subj-group></subj-group></subj-group><subj-group><subject>Proteomics</subject><subj-group><subject>Peptide Mapping</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Parasitic Diseases</subject><subj-group><subject>Malaria</subject></subj-group></subj-group><subj-group><subject>Tropical Diseases (Non-Neglected)</subject><subj-group><subject>Malaria</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Comprehensive Histone Phosphorylation Analysis and Identification of Pf14-3-3 Protein as a Histone H3 Phosphorylation Reader in Malaria Parasites</article-title><alt-title alt-title-type="running-head">Histone Phosphorylation in <italic>P. falciparum</italic></alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Dastidar</surname><given-names>Eeshita G.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dzeyk</surname><given-names>Kristina</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Krijgsveld</surname><given-names>Jeroen</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Malmquist</surname><given-names>Nicholas A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Doerig</surname><given-names>Christian</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Scherf</surname><given-names>Artur</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lopez-Rubio</surname><given-names>Jose-Juan</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Centre National de la Recherche Scientifique, Unité de Recherche Associé 2581, Paris, France</addr-line></aff><aff id="aff3"><label>3</label><addr-line>European Molecular Biology Laboratory, Proteomics Core Facility, Heidelberg, Germany</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Department of Microbiology, Monash University, Clayton, Victoria, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Spielmann</surname><given-names>Tobias</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Bernhard Nocht Institute for Tropical Medicine, Germany</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>artur.scherf@pasteur.fr</email> (AS); <email>jjlopez@pasteur.fr</email> (JJLR)</corresp><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: JJLR AS CD NM. Performed the experiments: EGD JK KD NM. Analyzed the data: JJLR EGD AS CD NM KD JK. Contributed reagents/materials/analysis tools: JJLR EGD AS CD NM KD JK. Wrote the paper: EGD JJLR AS CD NM.</p></fn></author-notes><pub-date pub-type="collection"><year>2013</year></pub-date><pub-date pub-type="epub"><day>7</day><month>1</month><year>2013</year></pub-date><volume>8</volume><issue>1</issue><elocation-id>e53179</elocation-id><history><date date-type="received"><day>9</day><month>8</month><year>2012</year></date><date date-type="accepted"><day>26</day><month>11</month><year>2012</year></date></history><permissions><copyright-year>2013</copyright-year><copyright-holder>Dastidar et al</copyright-holder><license><license-p>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.</license-p></license></permissions><abstract><p>The important role of histone posttranslational modifications, particularly methylation and acetylation, in <italic>Plasmodium falciparum</italic> gene regulation has been established. However, the role of histone phosphorylation remains understudied. Here, we investigate histone phosphorylation utilizing liquid chromatography and tandem mass spectrometry to analyze histones extracted from asexual blood stages using two improved protocols to enhance preservation of PTMs. Enrichment for phosphopeptides lead to the detection of 14 histone phospho-modifications in <italic>P. falciparum</italic>. The majority of phosphorylation sites were observed at the N-terminal regions of various histones and were frequently observed adjacent to acetylated lysines. We also report the identification of one novel member of the <italic>P. falciparum</italic> histone phosphosite binding protein repertoire, Pf14-3-3I. Recombinant Pf14-3-3I protein bound to purified parasite histones. <italic>In silico</italic> structural analysis of Pf14-3-3 proteins revealed that residues responsible for binding to histone H3 S10ph and/or S28ph are conserved at the primary and the tertiary structure levels. Using a battery of H3 specific phosphopeptides, we demonstrate that Pf14-3-3I preferentially binds to H3S28ph over H3S10ph, independent of modification of neighbouring residues like H3S10phK14ac and H3S28phS32ph. Our data provide key insight into histone phosphorylation sites. The identification of a second member of the histone modification reading machinery suggests a widespread use of histone phosphorylation in the control of various nuclear processes in malaria parasites.</p></abstract><funding-group><funding-statement>EGD benefits from a PhD fellowship funded by the European Union Framework Program 7 Marie Curie Initial Training Network “Intervention strategies against malaria (InterMalTraining)”, contract number 215281. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="12"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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