The Caenorhabditis elegans Protein FIC-1 Is an AMPylase That Covalently Modifies Heat-Shock 70 Family Proteins, Translation Elongation Factors and Histones
Protein AMPylation by Fic domain-containing proteins (Fic proteins) is an ancient and conserved post-translational modification of mostly unexplored significance. Here we characterize the Caenorhabditis elegans Fic protein FIC-1 in vitro and in vivo. FIC-1 is an AMPylase that localizes to the nuclea...
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| creator | Truttmann, Matthias C Cruz, Victor E Guo, Xuanzong Engert, Christoph Schwartz, Thomas U Ploegh, Hidde L |
| description | Protein AMPylation by Fic domain-containing proteins (Fic proteins) is an ancient and conserved post-translational modification of mostly unexplored significance. Here we characterize the Caenorhabditis elegans Fic protein FIC-1 in vitro and in vivo. FIC-1 is an AMPylase that localizes to the nuclear surface and modifies core histones H2 and H3 as well as heat shock protein 70 family members and translation elongation factors. The three-dimensional structure of FIC-1 is similar to that of its human ortholog, HYPE, with 38% sequence identity. We identify a link between FIC-1-mediated AMPylation and susceptibility to the pathogen Pseudomonas aeruginosa, establishing a connection between AMPylation and innate immunity in C. elegans. |
| doi_str_mv | 10.1371/journal.pgen.1006023 |
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Here we characterize the Caenorhabditis elegans Fic protein FIC-1 in vitro and in vivo. FIC-1 is an AMPylase that localizes to the nuclear surface and modifies core histones H2 and H3 as well as heat shock protein 70 family members and translation elongation factors. The three-dimensional structure of FIC-1 is similar to that of its human ortholog, HYPE, with 38% sequence identity. We identify a link between FIC-1-mediated AMPylation and susceptibility to the pathogen Pseudomonas aeruginosa, establishing a connection between AMPylation and innate immunity in C. elegans.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006023</identifier><identifier>PMID: 27138431</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; autoradiography ; BASIC BIOLOGICAL SCIENCES ; Biology and Life Sciences ; Caenorhabditis elegans ; Caenorhabditis elegans - chemistry ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - microbiology ; Caenorhabditis elegans Proteins - genetics ; Carrier Proteins - chemistry ; Carrier Proteins - genetics ; Crystallography, X-Ray ; Data collection ; DNA-binding proteins ; DNA-Binding Proteins - chemistry ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; elongation factors ; Genes ; Genetic aspects ; Heat shock proteins ; heat shock response ; Heat-Shock Response - genetics ; histones ; Histones - genetics ; Histones - metabolism ; HSP70 Heat-Shock Proteins - chemistry ; HSP70 Heat-Shock Proteins - genetics ; HSP70 Heat-Shock Proteins - metabolism ; Humans ; Immunity, Innate - genetics ; Insects ; Mass spectrometry ; Medicine and Health Sciences ; Membrane Proteins - chemistry ; Membrane Proteins - genetics ; Nematodes ; Nucleotidyltransferases - genetics ; Observations ; Peptide Chain Elongation, Translational ; Physiological aspects ; Protein Conformation ; protein translation ; Proteins ; Pseudomonas aeruginosa ; Pseudomonas aeruginosa - genetics ; Pseudomonas aeruginosa - pathogenicity ; Recombinant Proteins - chemistry ; Recombinant Proteins - genetics ; Recombinant Proteins - metabolism ; Research and Analysis Methods ; Scientific imaging ; Studies ; Translation (Genetics)</subject><ispartof>PLoS genetics, 2016-05, Vol.12 (5), p.e1006023-e1006023</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. 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: Protein FIC-1 Is an AMPylase That Covalently Modifies Heat-Shock 70 Family Proteins, Translation Elongation Factors and Histones. PLoS Genet 12(5): e1006023. doi:10.1371/journal.pgen.1006023</rights><rights>2016 Truttmann et al 2016 Truttmann et al</rights><rights>2016 Public Library of Science. 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: Protein FIC-1 Is an AMPylase That Covalently Modifies Heat-Shock 70 Family Proteins, Translation Elongation Factors and Histones. 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Here we characterize the Caenorhabditis elegans Fic protein FIC-1 in vitro and in vivo. FIC-1 is an AMPylase that localizes to the nuclear surface and modifies core histones H2 and H3 as well as heat shock protein 70 family members and translation elongation factors. The three-dimensional structure of FIC-1 is similar to that of its human ortholog, HYPE, with 38% sequence identity. We identify a link between FIC-1-mediated AMPylation and susceptibility to the pathogen Pseudomonas aeruginosa, establishing a connection between AMPylation and innate immunity in C. elegans.</description><subject>Animals</subject><subject>autoradiography</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biology and Life Sciences</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - chemistry</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - microbiology</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Carrier Proteins - chemistry</subject><subject>Carrier Proteins - genetics</subject><subject>Crystallography, X-Ray</subject><subject>Data collection</subject><subject>DNA-binding proteins</subject><subject>DNA-Binding Proteins - chemistry</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>elongation factors</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Heat shock proteins</subject><subject>heat shock response</subject><subject>Heat-Shock Response - genetics</subject><subject>histones</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>HSP70 Heat-Shock Proteins - chemistry</subject><subject>HSP70 Heat-Shock Proteins - genetics</subject><subject>HSP70 Heat-Shock Proteins - metabolism</subject><subject>Humans</subject><subject>Immunity, Innate - genetics</subject><subject>Insects</subject><subject>Mass spectrometry</subject><subject>Medicine and Health Sciences</subject><subject>Membrane Proteins - chemistry</subject><subject>Membrane Proteins - genetics</subject><subject>Nematodes</subject><subject>Nucleotidyltransferases - genetics</subject><subject>Observations</subject><subject>Peptide Chain Elongation, Translational</subject><subject>Physiological aspects</subject><subject>Protein Conformation</subject><subject>protein translation</subject><subject>Proteins</subject><subject>Pseudomonas aeruginosa</subject><subject>Pseudomonas aeruginosa - genetics</subject><subject>Pseudomonas aeruginosa - pathogenicity</subject><subject>Recombinant Proteins - chemistry</subject><subject>Recombinant Proteins - genetics</subject><subject>Recombinant Proteins - metabolism</subject><subject>Research and Analysis Methods</subject><subject>Scientific imaging</subject><subject>Studies</subject><subject>Translation (Genetics)</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk99u0zAUxiMEYmPwBggskBBItPhfYucGaapWVmljEyvcWieO03i48YjdiT0LL4u7ZtOKJgHKRSz7d77j8_mcLHtO8JgwQT6c-1XfgRtfLEw3JhgXmLIH2S7JczYSHPOHd9Y72ZMQzjFmuSzF42yHCsIkZ2Q3-zVvDZqA6XzfQlXbaAMyziygC-i099HYDk1nkxFBs4CgQ_vHp1cOgkHzFiKa-EtwpovuCh372jbWBHRoII7OWq-_I4HRFJY2nQ5S4T2a90naQbS-QwfOd4vNcgo6-n6dokaHNkTfmfA0e9SAC-bZ8N_Lvk4P5pPD0dHJp9lk_2ikhSziiIuayLIUGmQuGJXc1AzAiLqhOVS6kAZXpSGFKJmhsiIMU64pF7LCJasA2F72cqN74XxQg69BEVGKHOeS80TMNkTt4Vxd9HYJ_ZXyYNX1hu8XCvpotTOqSS_RQCkorSteaSI5FVAWBCjmFNId9rKPQ7ZVtTS1Tvb14LZEt08626qFv1Rc5pzJPAm82gj4EK0K2kajW-27zuioCKcFFThBb4csvf-xMiGqpQ3aOAed8atUnMSy4IxL8XdUSIFLml_78PoP9H63BmqRmkPZrvGpDr0WVftclDktSrYuY3wPlb7aLG0qxzQ27W8FvNsKSEw0P-MCViGo2dmX_2A__zt78m2bfXOHbQ242AbvVuseDtsg34C69yH0prl9YILVen5vnFPr-VXD_KawF3eb4zboZmDZb7V3PWk</recordid><startdate>20160503</startdate><enddate>20160503</enddate><creator>Truttmann, Matthias C</creator><creator>Cruz, Victor E</creator><creator>Guo, Xuanzong</creator><creator>Engert, Christoph</creator><creator>Schwartz, Thomas U</creator><creator>Ploegh, Hidde L</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5338-0973</orcidid><orcidid>https://orcid.org/0000000153380973</orcidid></search><sort><creationdate>20160503</creationdate><title>The Caenorhabditis elegans Protein FIC-1 Is an AMPylase That Covalently Modifies Heat-Shock 70 Family Proteins, Translation Elongation Factors and Histones</title><author>Truttmann, Matthias C ; Cruz, Victor E ; Guo, Xuanzong ; Engert, Christoph ; Schwartz, Thomas U ; Ploegh, Hidde L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c786t-47d18997ca8573284ed3aae7df25abc68e0b9e16793e28b13024c2478b093baa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>autoradiography</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biology and Life Sciences</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - chemistry</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - microbiology</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Carrier Proteins - chemistry</topic><topic>Carrier Proteins - genetics</topic><topic>Crystallography, X-Ray</topic><topic>Data collection</topic><topic>DNA-binding proteins</topic><topic>DNA-Binding Proteins - chemistry</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>elongation factors</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Heat shock proteins</topic><topic>heat shock response</topic><topic>Heat-Shock Response - genetics</topic><topic>histones</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>HSP70 Heat-Shock Proteins - chemistry</topic><topic>HSP70 Heat-Shock Proteins - genetics</topic><topic>HSP70 Heat-Shock Proteins - metabolism</topic><topic>Humans</topic><topic>Immunity, Innate - genetics</topic><topic>Insects</topic><topic>Mass spectrometry</topic><topic>Medicine and Health Sciences</topic><topic>Membrane Proteins - chemistry</topic><topic>Membrane Proteins - genetics</topic><topic>Nematodes</topic><topic>Nucleotidyltransferases - genetics</topic><topic>Observations</topic><topic>Peptide Chain Elongation, Translational</topic><topic>Physiological aspects</topic><topic>Protein Conformation</topic><topic>protein translation</topic><topic>Proteins</topic><topic>Pseudomonas aeruginosa</topic><topic>Pseudomonas aeruginosa - genetics</topic><topic>Pseudomonas aeruginosa - pathogenicity</topic><topic>Recombinant Proteins - chemistry</topic><topic>Recombinant Proteins - genetics</topic><topic>Recombinant Proteins - metabolism</topic><topic>Research and Analysis Methods</topic><topic>Scientific imaging</topic><topic>Studies</topic><topic>Translation (Genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Truttmann, Matthias C</creatorcontrib><creatorcontrib>Cruz, Victor E</creatorcontrib><creatorcontrib>Guo, Xuanzong</creatorcontrib><creatorcontrib>Engert, Christoph</creatorcontrib><creatorcontrib>Schwartz, Thomas U</creatorcontrib><creatorcontrib>Ploegh, Hidde L</creatorcontrib><creatorcontrib>Argonne National Laboratory (ANL), Argonne, IL (United States)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - 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Here we characterize the Caenorhabditis elegans Fic protein FIC-1 in vitro and in vivo. FIC-1 is an AMPylase that localizes to the nuclear surface and modifies core histones H2 and H3 as well as heat shock protein 70 family members and translation elongation factors. The three-dimensional structure of FIC-1 is similar to that of its human ortholog, HYPE, with 38% sequence identity. We identify a link between FIC-1-mediated AMPylation and susceptibility to the pathogen Pseudomonas aeruginosa, establishing a connection between AMPylation and innate immunity in C. elegans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27138431</pmid><doi>10.1371/journal.pgen.1006023</doi><orcidid>https://orcid.org/0000-0001-5338-0973</orcidid><orcidid>https://orcid.org/0000000153380973</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central |
| subjects | Animals autoradiography BASIC BIOLOGICAL SCIENCES Biology and Life Sciences Caenorhabditis elegans Caenorhabditis elegans - chemistry Caenorhabditis elegans - genetics Caenorhabditis elegans - microbiology Caenorhabditis elegans Proteins - genetics Carrier Proteins - chemistry Carrier Proteins - genetics Crystallography, X-Ray Data collection DNA-binding proteins DNA-Binding Proteins - chemistry DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism elongation factors Genes Genetic aspects Heat shock proteins heat shock response Heat-Shock Response - genetics histones Histones - genetics Histones - metabolism HSP70 Heat-Shock Proteins - chemistry HSP70 Heat-Shock Proteins - genetics HSP70 Heat-Shock Proteins - metabolism Humans Immunity, Innate - genetics Insects Mass spectrometry Medicine and Health Sciences Membrane Proteins - chemistry Membrane Proteins - genetics Nematodes Nucleotidyltransferases - genetics Observations Peptide Chain Elongation, Translational Physiological aspects Protein Conformation protein translation Proteins Pseudomonas aeruginosa Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - pathogenicity Recombinant Proteins - chemistry Recombinant Proteins - genetics Recombinant Proteins - metabolism Research and Analysis Methods Scientific imaging Studies Translation (Genetics) |
| title | The Caenorhabditis elegans Protein FIC-1 Is an AMPylase That Covalently Modifies Heat-Shock 70 Family Proteins, Translation Elongation Factors and Histones |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-11T09%3A27%3A44IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20Caenorhabditis%20elegans%20Protein%20FIC-1%20Is%20an%20AMPylase%20That%20Covalently%20Modifies%20Heat-Shock%2070%20Family%20Proteins,%20Translation%20Elongation%20Factors%20and%20Histones&rft.jtitle=PLoS%20genetics&rft.au=Truttmann,%20Matthias%20C&rft.aucorp=Argonne%20National%20Laboratory%20(ANL),%20Argonne,%20IL%20(United%20States)&rft.date=2016-05-03&rft.volume=12&rft.issue=5&rft.spage=e1006023&rft.epage=e1006023&rft.pages=e1006023-e1006023&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1006023&rft_dat=%3Cgale_plos_%3EA479526935%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1797505844&rft_id=info:pmid/27138431&rft_galeid=A479526935&rft_doaj_id=oai_doaj_org_article_f006fa9722db4bc18427a961a2042a79&rfr_iscdi=true |