Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium
Summary Indirect readout mechanisms of transcription control rely on the recognition of DNA shape by transcription factors (TFs). TFs may also employ a direct readout mechanism that involves the reading of the base sequence in the DNA major groove at the binding site. TFs with winged helix–turn–heli...
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Indirect readout mechanisms of transcription control rely on the recognition of DNA shape by transcription factors (TFs). TFs may also employ a direct readout mechanism that involves the reading of the base sequence in the DNA major groove at the binding site. TFs with winged helix–turn–helix (wHTH) motifs use an alpha helix to read the base sequence in the major groove while inserting a beta sheet ‘wing’ into the adjacent minor groove. Such wHTH proteins are important regulators of virulence gene transcription in many pathogens; they also control housekeeping genes. This article considers the cases of the non‐invasive Gram‐negative pathogen Vibrio cholerae and the invasive pathogen Salmonella enterica serovar Typhimurium. Both possess clusters of A + T‐rich horizontally acquired virulence genes that are silenced by the nucleoid‐associated protein H‐NS and regulated positively or negatively by wHTH TFs: for example, ToxR and LeuO in V. cholerae; HilA, LeuO, SlyA and OmpR in S. Typhimurium. Because of their relatively relaxed base sequence requirements for target recognition, indirect readout mechanisms have the potential to engage regulatory proteins with many more targets than might be the case using direct readout, making indirect readout an important, yet often ignored, contributor to the expression of pathogenic phenotypes. |
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Indirect readout mechanisms of transcription control rely on the recognition of DNA shape by transcription factors (TFs). TFs may also employ a direct readout mechanism that involves the reading of the base sequence in the DNA major groove at the binding site. TFs with winged helix–turn–helix (wHTH) motifs use an alpha helix to read the base sequence in the major groove while inserting a beta sheet ‘wing’ into the adjacent minor groove. Such wHTH proteins are important regulators of virulence gene transcription in many pathogens; they also control housekeeping genes. This article considers the cases of the non‐invasive Gram‐negative pathogen Vibrio cholerae and the invasive pathogen Salmonella enterica serovar Typhimurium. Both possess clusters of A + T‐rich horizontally acquired virulence genes that are silenced by the nucleoid‐associated protein H‐NS and regulated positively or negatively by wHTH TFs: for example, ToxR and LeuO in V. cholerae; HilA, LeuO, SlyA and OmpR in S. Typhimurium. Because of their relatively relaxed base sequence requirements for target recognition, indirect readout mechanisms have the potential to engage regulatory proteins with many more targets than might be the case using direct readout, making indirect readout an important, yet often ignored, contributor to the expression of pathogenic phenotypes.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.13838</identifier><identifier>PMID: 28631437</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Animals ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Base Composition - genetics ; Base Sequence ; Binding sites ; Binding Sites - genetics ; Deoxyribonucleic acid ; DNA ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; essential genes ; Gene Expression Regulation, Bacterial ; Gene silencing ; Genes ; H protein ; Humans ; Minireview ; Minireviews ; Nucleotide sequence ; nucleotide sequences ; Pathogens ; phenotype ; Protein structure ; Proteins ; Regulators ; Regulatory proteins ; Salmonella ; Salmonella Typhimurium ; Salmonella typhimurium - genetics ; Salmonella typhimurium - pathogenicity ; Shape recognition ; Target recognition ; Trans-Activators - genetics ; Trans-Activators - metabolism ; transcription (genetics) ; Transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic - genetics ; Vibrio cholerae ; Vibrio cholerae - genetics ; Vibrio cholerae - pathogenicity ; Virulence ; Virulence - genetics ; Waterborne diseases</subject><ispartof>Environmental microbiology, 2017-10, Vol.19 (10), p.3834-3845</ispartof><rights>2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2017 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5008-c868d7bf26cb5e3185d694e879d3796a326f61d6736054e17a42647446ecb3693</citedby><cites>FETCH-LOGICAL-c5008-c868d7bf26cb5e3185d694e879d3796a326f61d6736054e17a42647446ecb3693</cites><orcidid>0000-0001-7064-6163</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.13838$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.13838$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28631437$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dorman, Charles J.</creatorcontrib><creatorcontrib>Dorman, Matthew J.</creatorcontrib><title>Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Indirect readout mechanisms of transcription control rely on the recognition of DNA shape by transcription factors (TFs). TFs may also employ a direct readout mechanism that involves the reading of the base sequence in the DNA major groove at the binding site. TFs with winged helix–turn–helix (wHTH) motifs use an alpha helix to read the base sequence in the major groove while inserting a beta sheet ‘wing’ into the adjacent minor groove. Such wHTH proteins are important regulators of virulence gene transcription in many pathogens; they also control housekeeping genes. This article considers the cases of the non‐invasive Gram‐negative pathogen Vibrio cholerae and the invasive pathogen Salmonella enterica serovar Typhimurium. Both possess clusters of A + T‐rich horizontally acquired virulence genes that are silenced by the nucleoid‐associated protein H‐NS and regulated positively or negatively by wHTH TFs: for example, ToxR and LeuO in V. cholerae; HilA, LeuO, SlyA and OmpR in S. Typhimurium. Because of their relatively relaxed base sequence requirements for target recognition, indirect readout mechanisms have the potential to engage regulatory proteins with many more targets than might be the case using direct readout, making indirect readout an important, yet often ignored, contributor to the expression of pathogenic phenotypes.</description><subject>Animals</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Base Composition - genetics</subject><subject>Base Sequence</subject><subject>Binding sites</subject><subject>Binding Sites - genetics</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>essential genes</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene silencing</subject><subject>Genes</subject><subject>H protein</subject><subject>Humans</subject><subject>Minireview</subject><subject>Minireviews</subject><subject>Nucleotide sequence</subject><subject>nucleotide sequences</subject><subject>Pathogens</subject><subject>phenotype</subject><subject>Protein structure</subject><subject>Proteins</subject><subject>Regulators</subject><subject>Regulatory proteins</subject><subject>Salmonella</subject><subject>Salmonella Typhimurium</subject><subject>Salmonella typhimurium - genetics</subject><subject>Salmonella typhimurium - pathogenicity</subject><subject>Shape recognition</subject><subject>Target recognition</subject><subject>Trans-Activators - genetics</subject><subject>Trans-Activators - metabolism</subject><subject>transcription (genetics)</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic - genetics</subject><subject>Vibrio cholerae</subject><subject>Vibrio cholerae - genetics</subject><subject>Vibrio cholerae - pathogenicity</subject><subject>Virulence</subject><subject>Virulence - genetics</subject><subject>Waterborne diseases</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhiMEoqVw5oYsceGy1N9OLkhoVaBSqx5auFqOM-m6SuxlnGy1_Hq8bFlRLvXF9viZVzN-p6reMvqRlXXKpOYL3vByFbWon1XHh8jzw5nxo-pVzneUMiMMfVkd8VoLJoU5rn4tU5wwDST1ZBNwHiB6ILcQgUzoYvYY1lNIkbRbEmIXEPxEEFyX5qkEyI_QYkjEr9IA6IC42JFrN4wpwjA4AnECDN6RDJg2DsnNdr0K44xhHl9XL3o3ZHjzsJ9U37-c3Sy_LS6uvp4vP18svKK0Xvha151pe659q0CwWnW6kVCbphOm0U5w3WvWaSM0VRKYcZJraaTU4FuhG3FSfdrrrud2hM6XmtANdo1hdLi1yQX7-CWGlb1NG6u0Ug1TReDDgwCmnzPkyY4h-11_EdKcLaeUKs2NeBplDWOGFkdkQd__h96lGWP5iUIpThWVrC7U6Z7ymHJG6A91M2p3I2B3Jtud4fbPCJSMd_-2e-D_el4AtQfuwwDbp_Ts2eX5Xvg3U3y8Og</recordid><startdate>201710</startdate><enddate>201710</enddate><creator>Dorman, Charles J.</creator><creator>Dorman, Matthew J.</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7064-6163</orcidid></search><sort><creationdate>201710</creationdate><title>Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium</title><author>Dorman, Charles J. ; Dorman, Matthew J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5008-c868d7bf26cb5e3185d694e879d3796a326f61d6736054e17a42647446ecb3693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Base Composition - genetics</topic><topic>Base Sequence</topic><topic>Binding sites</topic><topic>Binding Sites - genetics</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>essential genes</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene silencing</topic><topic>Genes</topic><topic>H protein</topic><topic>Humans</topic><topic>Minireview</topic><topic>Minireviews</topic><topic>Nucleotide sequence</topic><topic>nucleotide sequences</topic><topic>Pathogens</topic><topic>phenotype</topic><topic>Protein structure</topic><topic>Proteins</topic><topic>Regulators</topic><topic>Regulatory proteins</topic><topic>Salmonella</topic><topic>Salmonella Typhimurium</topic><topic>Salmonella typhimurium - genetics</topic><topic>Salmonella typhimurium - pathogenicity</topic><topic>Shape recognition</topic><topic>Target recognition</topic><topic>Trans-Activators - genetics</topic><topic>Trans-Activators - metabolism</topic><topic>transcription (genetics)</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription, Genetic - genetics</topic><topic>Vibrio cholerae</topic><topic>Vibrio cholerae - genetics</topic><topic>Vibrio cholerae - pathogenicity</topic><topic>Virulence</topic><topic>Virulence - genetics</topic><topic>Waterborne diseases</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dorman, Charles J.</creatorcontrib><creatorcontrib>Dorman, Matthew J.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dorman, Charles J.</au><au>Dorman, Matthew J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2017-10</date><risdate>2017</risdate><volume>19</volume><issue>10</issue><spage>3834</spage><epage>3845</epage><pages>3834-3845</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Indirect readout mechanisms of transcription control rely on the recognition of DNA shape by transcription factors (TFs). TFs may also employ a direct readout mechanism that involves the reading of the base sequence in the DNA major groove at the binding site. TFs with winged helix–turn–helix (wHTH) motifs use an alpha helix to read the base sequence in the major groove while inserting a beta sheet ‘wing’ into the adjacent minor groove. Such wHTH proteins are important regulators of virulence gene transcription in many pathogens; they also control housekeeping genes. This article considers the cases of the non‐invasive Gram‐negative pathogen Vibrio cholerae and the invasive pathogen Salmonella enterica serovar Typhimurium. Both possess clusters of A + T‐rich horizontally acquired virulence genes that are silenced by the nucleoid‐associated protein H‐NS and regulated positively or negatively by wHTH TFs: for example, ToxR and LeuO in V. cholerae; HilA, LeuO, SlyA and OmpR in S. Typhimurium. Because of their relatively relaxed base sequence requirements for target recognition, indirect readout mechanisms have the potential to engage regulatory proteins with many more targets than might be the case using direct readout, making indirect readout an important, yet often ignored, contributor to the expression of pathogenic phenotypes.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28631437</pmid><doi>10.1111/1462-2920.13838</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7064-6163</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bacterial Proteins - genetics Bacterial Proteins - metabolism Base Composition - genetics Base Sequence Binding sites Binding Sites - genetics Deoxyribonucleic acid DNA DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism essential genes Gene Expression Regulation, Bacterial Gene silencing Genes H protein Humans Minireview Minireviews Nucleotide sequence nucleotide sequences Pathogens phenotype Protein structure Proteins Regulators Regulatory proteins Salmonella Salmonella Typhimurium Salmonella typhimurium - genetics Salmonella typhimurium - pathogenicity Shape recognition Target recognition Trans-Activators - genetics Trans-Activators - metabolism transcription (genetics) Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic - genetics Vibrio cholerae Vibrio cholerae - genetics Vibrio cholerae - pathogenicity Virulence Virulence - genetics Waterborne diseases |
title | Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium |
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