Yersinia remodels epigenetic histone modifications in human macrophages
Various pathogens systematically reprogram gene expression in macrophages, but the underlying mechanisms are largely unknown. We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin im...
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| creator | Bekere, Indra Huang, Jiabin Schnapp, Marie Rudolph, Maren Berneking, Laura Ruckdeschel, Klaus Grundhoff, Adam Günther, Thomas Fischer, Nicole Aepfelbacher, Martin |
| description | Various pathogens systematically reprogram gene expression in macrophages, but the underlying mechanisms are largely unknown. We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin immunoprecipitation (ChIP) seq analyses showed that pathogen-associated molecular patterns (PAMPs) induced up- or down-regulation of histone modifications (HMod) at approximately 14500 loci in promoters and enhancers. Effectors of Y. enterocolitica reorganized about half of these dynamic HMod, with the effector YopP being responsible for about half of these modulatory activities. The reorganized HMod were associated with genes involved in immune response and metabolism. Remarkably, the altered HMod also associated with 61% of all 534 known Rho GTPase pathway genes, revealing a new level in Rho GTPase regulation and a new aspect of bacterial pathogenicity. Changes in HMod were associated to varying degrees with corresponding gene expression, e. g. depending on chromatin localization and cooperation of the HMod. In summary, infection with Y. enterocolitica remodels HMod in human macrophages to modulate key gene expression programs of the innate immune response. |
| doi_str_mv | 10.1371/journal.ppat.1010074 |
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We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin immunoprecipitation (ChIP) seq analyses showed that pathogen-associated molecular patterns (PAMPs) induced up- or down-regulation of histone modifications (HMod) at approximately 14500 loci in promoters and enhancers. Effectors of Y. enterocolitica reorganized about half of these dynamic HMod, with the effector YopP being responsible for about half of these modulatory activities. The reorganized HMod were associated with genes involved in immune response and metabolism. Remarkably, the altered HMod also associated with 61% of all 534 known Rho GTPase pathway genes, revealing a new level in Rho GTPase regulation and a new aspect of bacterial pathogenicity. Changes in HMod were associated to varying degrees with corresponding gene expression, e. g. depending on chromatin localization and cooperation of the HMod. In summary, infection with Y. enterocolitica remodels HMod in human macrophages to modulate key gene expression programs of the innate immune response.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1010074</identifier><identifier>PMID: 34793580</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Bacteria ; Bacterial infections ; Biology and Life Sciences ; Care and treatment ; Chromatin ; Cytokines ; Diagnosis ; DNA methylation ; Enhancers ; Epigenesis, Genetic ; Epigenetics ; Gene expression ; Genes ; Genomes ; Health aspects ; Histone Code ; Histones ; Humans ; Immune response ; Immune system ; Immunity, Innate ; Immunoprecipitation ; Infections ; Innate immunity ; Kinases ; Localization ; Macrophages ; Macrophages - immunology ; Macrophages - metabolism ; Macrophages - microbiology ; Medicine and Health Sciences ; Metabolism ; Metabolites ; Observations ; Pathogenicity ; Pathogens ; Proteins ; rho GTP-Binding Proteins - genetics ; rho GTP-Binding Proteins - metabolism ; Risk factors ; Transcription factors ; Virulence ; Yersinia enterocolitica - pathogenicity ; Yersinia infections ; Yersinia Infections - genetics ; Yersinia Infections - immunology ; Yersinia Infections - metabolism ; Yersinia Infections - microbiology</subject><ispartof>PLoS pathogens, 2021-11, Vol.17 (11), p.e1010074-e1010074</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Bekere et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Bekere et al 2021 Bekere et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c661t-c4d4b1141673f638c80620ee7472fa181fb4ca12f7db70b416b4b4e03ced535b3</citedby><cites>FETCH-LOGICAL-c661t-c4d4b1141673f638c80620ee7472fa181fb4ca12f7db70b416b4b4e03ced535b3</cites><orcidid>0000-0001-5156-2909 ; 0000-0001-9650-0218 ; 0000-0001-9166-2533 ; 0000-0002-3480-7115 ; 0000-0002-0164-9085</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8639070/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8639070/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23867,27925,27926,53792,53794</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34793580$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Monack, Denise M.</contributor><creatorcontrib>Bekere, Indra</creatorcontrib><creatorcontrib>Huang, Jiabin</creatorcontrib><creatorcontrib>Schnapp, Marie</creatorcontrib><creatorcontrib>Rudolph, Maren</creatorcontrib><creatorcontrib>Berneking, Laura</creatorcontrib><creatorcontrib>Ruckdeschel, Klaus</creatorcontrib><creatorcontrib>Grundhoff, Adam</creatorcontrib><creatorcontrib>Günther, Thomas</creatorcontrib><creatorcontrib>Fischer, Nicole</creatorcontrib><creatorcontrib>Aepfelbacher, Martin</creatorcontrib><title>Yersinia remodels epigenetic histone modifications in human macrophages</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Various pathogens systematically reprogram gene expression in macrophages, but the underlying mechanisms are largely unknown. We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin immunoprecipitation (ChIP) seq analyses showed that pathogen-associated molecular patterns (PAMPs) induced up- or down-regulation of histone modifications (HMod) at approximately 14500 loci in promoters and enhancers. Effectors of Y. enterocolitica reorganized about half of these dynamic HMod, with the effector YopP being responsible for about half of these modulatory activities. The reorganized HMod were associated with genes involved in immune response and metabolism. Remarkably, the altered HMod also associated with 61% of all 534 known Rho GTPase pathway genes, revealing a new level in Rho GTPase regulation and a new aspect of bacterial pathogenicity. Changes in HMod were associated to varying degrees with corresponding gene expression, e. g. depending on chromatin localization and cooperation of the HMod. In summary, infection with Y. enterocolitica remodels HMod in human macrophages to modulate key gene expression programs of the innate immune response.</description><subject>Analysis</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Biology and Life Sciences</subject><subject>Care and treatment</subject><subject>Chromatin</subject><subject>Cytokines</subject><subject>Diagnosis</subject><subject>DNA methylation</subject><subject>Enhancers</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Histone Code</subject><subject>Histones</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Innate</subject><subject>Immunoprecipitation</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Kinases</subject><subject>Localization</subject><subject>Macrophages</subject><subject>Macrophages - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bekere, Indra</au><au>Huang, Jiabin</au><au>Schnapp, Marie</au><au>Rudolph, Maren</au><au>Berneking, Laura</au><au>Ruckdeschel, Klaus</au><au>Grundhoff, Adam</au><au>Günther, Thomas</au><au>Fischer, Nicole</au><au>Aepfelbacher, Martin</au><au>Monack, Denise M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Yersinia remodels epigenetic histone modifications in human macrophages</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>17</volume><issue>11</issue><spage>e1010074</spage><epage>e1010074</epage><pages>e1010074-e1010074</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Various pathogens systematically reprogram gene expression in macrophages, but the underlying mechanisms are largely unknown. We investigated whether the enteropathogen Yersinia enterocolitica alters chromatin states to reprogram gene expression in primary human macrophages. Genome-wide chromatin immunoprecipitation (ChIP) seq analyses showed that pathogen-associated molecular patterns (PAMPs) induced up- or down-regulation of histone modifications (HMod) at approximately 14500 loci in promoters and enhancers. Effectors of Y. enterocolitica reorganized about half of these dynamic HMod, with the effector YopP being responsible for about half of these modulatory activities. The reorganized HMod were associated with genes involved in immune response and metabolism. Remarkably, the altered HMod also associated with 61% of all 534 known Rho GTPase pathway genes, revealing a new level in Rho GTPase regulation and a new aspect of bacterial pathogenicity. Changes in HMod were associated to varying degrees with corresponding gene expression, e. g. depending on chromatin localization and cooperation of the HMod. In summary, infection with Y. enterocolitica remodels HMod in human macrophages to modulate key gene expression programs of the innate immune response.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34793580</pmid><doi>10.1371/journal.ppat.1010074</doi><orcidid>https://orcid.org/0000-0001-5156-2909</orcidid><orcidid>https://orcid.org/0000-0001-9650-0218</orcidid><orcidid>https://orcid.org/0000-0001-9166-2533</orcidid><orcidid>https://orcid.org/0000-0002-3480-7115</orcidid><orcidid>https://orcid.org/0000-0002-0164-9085</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Bacteria Bacterial infections Biology and Life Sciences Care and treatment Chromatin Cytokines Diagnosis DNA methylation Enhancers Epigenesis, Genetic Epigenetics Gene expression Genes Genomes Health aspects Histone Code Histones Humans Immune response Immune system Immunity, Innate Immunoprecipitation Infections Innate immunity Kinases Localization Macrophages Macrophages - immunology Macrophages - metabolism Macrophages - microbiology Medicine and Health Sciences Metabolism Metabolites Observations Pathogenicity Pathogens Proteins rho GTP-Binding Proteins - genetics rho GTP-Binding Proteins - metabolism Risk factors Transcription factors Virulence Yersinia enterocolitica - pathogenicity Yersinia infections Yersinia Infections - genetics Yersinia Infections - immunology Yersinia Infections - metabolism Yersinia Infections - microbiology |
| title | Yersinia remodels epigenetic histone modifications in human macrophages |
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