Discovery of a dual protease mechanism that promotes DNA damage checkpoint recovery
The DNA damage response is a signaling pathway found throughout biology. In many bacteria the DNA damage checkpoint is enforced by inducing expression of a small, membrane bound inhibitor that delays cell division providing time to repair damaged chromosomes. How cells promote checkpoint recovery af...
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description | The DNA damage response is a signaling pathway found throughout biology. In many bacteria the DNA damage checkpoint is enforced by inducing expression of a small, membrane bound inhibitor that delays cell division providing time to repair damaged chromosomes. How cells promote checkpoint recovery after sensing successful repair is unknown. By using a high-throughput, forward genetic screen, we identified two unrelated proteases, YlbL and CtpA, that promote DNA damage checkpoint recovery in Bacillus subtilis. Deletion of both proteases leads to accumulation of the checkpoint protein YneA. We show that DNA damage sensitivity and increased cell elongation in protease mutants depends on yneA. Further, expression of YneA in protease mutants was sufficient to inhibit cell proliferation. Finally, we show that both proteases interact with YneA and that one of the two proteases, CtpA, directly cleaves YneA in vitro. With these results, we report the mechanism for DNA damage checkpoint recovery in bacteria that use membrane bound cell division inhibitors. |
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In many bacteria the DNA damage checkpoint is enforced by inducing expression of a small, membrane bound inhibitor that delays cell division providing time to repair damaged chromosomes. How cells promote checkpoint recovery after sensing successful repair is unknown. By using a high-throughput, forward genetic screen, we identified two unrelated proteases, YlbL and CtpA, that promote DNA damage checkpoint recovery in Bacillus subtilis. Deletion of both proteases leads to accumulation of the checkpoint protein YneA. We show that DNA damage sensitivity and increased cell elongation in protease mutants depends on yneA. Further, expression of YneA in protease mutants was sufficient to inhibit cell proliferation. Finally, we show that both proteases interact with YneA and that one of the two proteases, CtpA, directly cleaves YneA in vitro. With these results, we report the mechanism for DNA damage checkpoint recovery in bacteria that use membrane bound cell division inhibitors.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1007512</identifier><identifier>PMID: 29979679</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacillus subtilis - physiology ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Biology and Life Sciences ; Cell cycle ; Cell Cycle Checkpoints - genetics ; Cell division ; Cell proliferation ; Chromosomes ; Clonal deletion ; Deoxyribonucleic acid ; Developmental biology ; DNA ; DNA damage ; DNA Damage - physiology ; DNA repair ; DNA Repair - physiology ; DNA Transposable Elements - genetics ; DNA, Bacterial - genetics ; E coli ; Endopeptidases - genetics ; Endopeptidases - metabolism ; Genes ; Genetic aspects ; Genetic research ; Genetic screening ; Genomes ; Kinases ; Medicine and Health Sciences ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Mutation ; Physiological aspects ; Proteases ; Proteinase ; Proteins ; Proteomics ; Research and Analysis Methods ; Signal transduction</subject><ispartof>PLoS genetics, 2018-07, Vol.14 (7), p.e1007512-e1007512</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Burby 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>2018 Burby et al 2018 Burby et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c585t-a2f9949452ebaf2280c842fa5662d2687d1e93bab25df36c8196dc53c9a58cd73</citedby><cites>FETCH-LOGICAL-c585t-a2f9949452ebaf2280c842fa5662d2687d1e93bab25df36c8196dc53c9a58cd73</cites><orcidid>0000-0001-6404-5652 ; 0000-0002-9600-7623</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/PMC6051672/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6051672/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29979679$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Burby, Peter E</creatorcontrib><creatorcontrib>Simmons, Zackary W</creatorcontrib><creatorcontrib>Schroeder, Jeremy W</creatorcontrib><creatorcontrib>Simmons, Lyle A</creatorcontrib><title>Discovery of a dual protease mechanism that promotes DNA damage checkpoint recovery</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The DNA damage response is a signaling pathway found throughout biology. In many bacteria the DNA damage checkpoint is enforced by inducing expression of a small, membrane bound inhibitor that delays cell division providing time to repair damaged chromosomes. How cells promote checkpoint recovery after sensing successful repair is unknown. By using a high-throughput, forward genetic screen, we identified two unrelated proteases, YlbL and CtpA, that promote DNA damage checkpoint recovery in Bacillus subtilis. Deletion of both proteases leads to accumulation of the checkpoint protein YneA. We show that DNA damage sensitivity and increased cell elongation in protease mutants depends on yneA. Further, expression of YneA in protease mutants was sufficient to inhibit cell proliferation. Finally, we show that both proteases interact with YneA and that one of the two proteases, CtpA, directly cleaves YneA in vitro. With these results, we report the mechanism for DNA damage checkpoint recovery in bacteria that use membrane bound cell division inhibitors.</description><subject>Bacillus subtilis - physiology</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biology and Life Sciences</subject><subject>Cell cycle</subject><subject>Cell Cycle Checkpoints - genetics</subject><subject>Cell division</subject><subject>Cell proliferation</subject><subject>Chromosomes</subject><subject>Clonal deletion</subject><subject>Deoxyribonucleic acid</subject><subject>Developmental biology</subject><subject>DNA</subject><subject>DNA damage</subject><subject>DNA Damage - physiology</subject><subject>DNA repair</subject><subject>DNA Repair - physiology</subject><subject>DNA Transposable Elements - genetics</subject><subject>DNA, Bacterial - genetics</subject><subject>E coli</subject><subject>Endopeptidases - genetics</subject><subject>Endopeptidases - metabolism</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Genetic screening</subject><subject>Genomes</subject><subject>Kinases</subject><subject>Medicine and Health Sciences</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Mutation</subject><subject>Physiological aspects</subject><subject>Proteases</subject><subject>Proteinase</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Research and Analysis Methods</subject><subject>Signal transduction</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUttu1DAQjRCIlsIfILCEhHjZxXF8fUFatVwqVfAAPFsTx7ksSRxsp1L_HodNq13Ek62ZM2fOHJ0se5njbV6I_P3ezX6Efjs1dtzmGAuWk0fZec5YsREU08dH_7PsWQh7jAsmlXianRGlhOJCnWffr7pg3K31d8jVCFA1Q48m76KFYNFgTQtjFwYUW4hLfUidgK6-7lAFAzQWmdaaX5Prxoi8PTA9z57U0Af7Yn0vsp-fPv64_LK5-fb5-nJ3szFMsrgBUitFFWXEllATIrGRlNTAOCcV4VJUuVVFCSVhVV1wI3PFK8MKo4BJU4niInt94J16F_TqR9CEMMwZF4QmxPUBUTnY68l3A_g77aDTfwvONxp87ExvNS4VpyJpgKQi8QPBBNK2kjEmlCSJ68O6bS4HWxk7Rg_9CelpZ-xa3bhbzTHLk5pE8G4l8O73bEPUQ_Le9j2M1s1JN-acSiYxT9A3_0D_f92KaiAd0I21S3vNQqp3jEpeYCwXl94eoVoLfWyD6-fYuTGcAukBaLwLwdv64bYc6yVy9yL0Ejm9Ri6NvTr25WHoPmPFH2Ya0kw</recordid><startdate>20180701</startdate><enddate>20180701</enddate><creator>Burby, Peter E</creator><creator>Simmons, Zackary W</creator><creator>Schroeder, Jeremy W</creator><creator>Simmons, Lyle A</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>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>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6404-5652</orcidid><orcidid>https://orcid.org/0000-0002-9600-7623</orcidid></search><sort><creationdate>20180701</creationdate><title>Discovery of a dual protease mechanism that promotes DNA damage checkpoint recovery</title><author>Burby, Peter E ; Simmons, Zackary W ; Schroeder, Jeremy W ; Simmons, Lyle A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c585t-a2f9949452ebaf2280c842fa5662d2687d1e93bab25df36c8196dc53c9a58cd73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Bacillus subtilis - physiology</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biology and Life Sciences</topic><topic>Cell cycle</topic><topic>Cell Cycle Checkpoints - genetics</topic><topic>Cell division</topic><topic>Cell proliferation</topic><topic>Chromosomes</topic><topic>Clonal deletion</topic><topic>Deoxyribonucleic acid</topic><topic>Developmental biology</topic><topic>DNA</topic><topic>DNA damage</topic><topic>DNA Damage - physiology</topic><topic>DNA repair</topic><topic>DNA Repair - physiology</topic><topic>DNA Transposable Elements - genetics</topic><topic>DNA, Bacterial - genetics</topic><topic>E coli</topic><topic>Endopeptidases - genetics</topic><topic>Endopeptidases - metabolism</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic research</topic><topic>Genetic screening</topic><topic>Genomes</topic><topic>Kinases</topic><topic>Medicine and Health Sciences</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Mutation</topic><topic>Physiological aspects</topic><topic>Proteases</topic><topic>Proteinase</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Research and Analysis Methods</topic><topic>Signal transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Burby, Peter E</creatorcontrib><creatorcontrib>Simmons, Zackary W</creatorcontrib><creatorcontrib>Schroeder, Jeremy W</creatorcontrib><creatorcontrib>Simmons, Lyle A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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</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>ProQuest Central (New)</collection><collection>ProQuest One Academic (New)</collection><collection>Publicly Available Content Database</collection><collection>ProQuest Health & Medical Research Collection</collection><collection>ProQuest One Academic Middle East (New)</collection><collection>ProQuest One Health & Nursing</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Applied & Life Sciences</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Burby, Peter E</au><au>Simmons, Zackary W</au><au>Schroeder, Jeremy W</au><au>Simmons, Lyle A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Discovery of a dual protease mechanism that promotes DNA damage checkpoint recovery</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2018-07-01</date><risdate>2018</risdate><volume>14</volume><issue>7</issue><spage>e1007512</spage><epage>e1007512</epage><pages>e1007512-e1007512</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The DNA damage response is a signaling pathway found throughout biology. In many bacteria the DNA damage checkpoint is enforced by inducing expression of a small, membrane bound inhibitor that delays cell division providing time to repair damaged chromosomes. How cells promote checkpoint recovery after sensing successful repair is unknown. By using a high-throughput, forward genetic screen, we identified two unrelated proteases, YlbL and CtpA, that promote DNA damage checkpoint recovery in Bacillus subtilis. Deletion of both proteases leads to accumulation of the checkpoint protein YneA. We show that DNA damage sensitivity and increased cell elongation in protease mutants depends on yneA. Further, expression of YneA in protease mutants was sufficient to inhibit cell proliferation. Finally, we show that both proteases interact with YneA and that one of the two proteases, CtpA, directly cleaves YneA in vitro. With these results, we report the mechanism for DNA damage checkpoint recovery in bacteria that use membrane bound cell division inhibitors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29979679</pmid><doi>10.1371/journal.pgen.1007512</doi><orcidid>https://orcid.org/0000-0001-6404-5652</orcidid><orcidid>https://orcid.org/0000-0002-9600-7623</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacillus subtilis - physiology Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biology and Life Sciences Cell cycle Cell Cycle Checkpoints - genetics Cell division Cell proliferation Chromosomes Clonal deletion Deoxyribonucleic acid Developmental biology DNA DNA damage DNA Damage - physiology DNA repair DNA Repair - physiology DNA Transposable Elements - genetics DNA, Bacterial - genetics E coli Endopeptidases - genetics Endopeptidases - metabolism Genes Genetic aspects Genetic research Genetic screening Genomes Kinases Medicine and Health Sciences Membrane Proteins - genetics Membrane Proteins - metabolism Mutation Physiological aspects Proteases Proteinase Proteins Proteomics Research and Analysis Methods Signal transduction |
title | Discovery of a dual protease mechanism that promotes DNA damage checkpoint recovery |
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