HPr prevents FruR-mediated facilitation of RNA polymerase binding to the fru promoter in Vibrio cholerae
Abstract Phosphorylation state-dependent interactions of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) components with transcription factors play a key role in carbon catabolite repression (CCR) by glucose in bacteria. Glucose inhibits the PTS-dependent transport of fruc...
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Veröffentlicht in: | Nucleic acids research 2023-06, Vol.51 (11), p.5432-5448 |
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creator | Yoon, Chang-Kyu Lee, Seung-Hwan Zhang, Jing Lee, Hye-Young Kim, Min-Kyu Seok, Yeong-Jae |
description | Abstract
Phosphorylation state-dependent interactions of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) components with transcription factors play a key role in carbon catabolite repression (CCR) by glucose in bacteria. Glucose inhibits the PTS-dependent transport of fructose and is preferred over fructose in Vibrio cholerae, but the mechanism is unknown. We have recently shown that, contrary to Escherichia coli, the fructose-dependent transcriptional regulator FruR acts as an activator of the fru operon in V. cholerae and binding of the FruR–fructose 1-phosphate (F1P) complex to an operator facilitates RNA polymerase (RNAP) binding to the fru promoter. Here we show that, in the presence of glucose, dephosphorylated HPr, a general PTS component, binds to FruR. Whereas HPr does not affect DNA-binding affinity of FruR, regardless of the presence of F1P, it prevents the FruR–F1P complex from facilitating the binding of RNAP to the fru promoter. Structural and biochemical analyses of the FruR–HPr complex identify key residues responsible for the V. cholerae-specific FruR–HPr interaction not observed in E. coli. Finally, we reveal how the dephosphorylated HPr interacts with FruR in V. cholerae, whereas the phosphorylated HPr binds to CcpA, which is a global regulator of CCR in Bacillus subtilis and shows structural similarity to FruR. |
doi_str_mv | 10.1093/nar/gkad220 |
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Phosphorylation state-dependent interactions of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) components with transcription factors play a key role in carbon catabolite repression (CCR) by glucose in bacteria. Glucose inhibits the PTS-dependent transport of fructose and is preferred over fructose in Vibrio cholerae, but the mechanism is unknown. We have recently shown that, contrary to Escherichia coli, the fructose-dependent transcriptional regulator FruR acts as an activator of the fru operon in V. cholerae and binding of the FruR–fructose 1-phosphate (F1P) complex to an operator facilitates RNA polymerase (RNAP) binding to the fru promoter. Here we show that, in the presence of glucose, dephosphorylated HPr, a general PTS component, binds to FruR. Whereas HPr does not affect DNA-binding affinity of FruR, regardless of the presence of F1P, it prevents the FruR–F1P complex from facilitating the binding of RNAP to the fru promoter. Structural and biochemical analyses of the FruR–HPr complex identify key residues responsible for the V. cholerae-specific FruR–HPr interaction not observed in E. coli. Finally, we reveal how the dephosphorylated HPr interacts with FruR in V. cholerae, whereas the phosphorylated HPr binds to CcpA, which is a global regulator of CCR in Bacillus subtilis and shows structural similarity to FruR.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkad220</identifier><identifier>PMID: 36987873</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Bacterial Proteins - metabolism ; DNA-Directed RNA Polymerases - metabolism ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Fructose - metabolism ; Gene Expression Regulation, Bacterial ; Gene regulation, Chromatin and Epigenetics ; Glucose ; Operon ; Phosphorylation ; Repressor Proteins - metabolism ; Vibrio cholerae - metabolism</subject><ispartof>Nucleic acids research, 2023-06, Vol.51 (11), p.5432-5448</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c371t-8e8d74c1df2ebb53c21fc31d613c61ef348dfea021dd95663e3d4e362f5165ee3</cites><orcidid>0000-0002-1546-9181 ; 0000-0001-9594-1396 ; 0000-0003-0379-3619</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/PMC10287919/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10287919/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1604,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36987873$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yoon, Chang-Kyu</creatorcontrib><creatorcontrib>Lee, Seung-Hwan</creatorcontrib><creatorcontrib>Zhang, Jing</creatorcontrib><creatorcontrib>Lee, Hye-Young</creatorcontrib><creatorcontrib>Kim, Min-Kyu</creatorcontrib><creatorcontrib>Seok, Yeong-Jae</creatorcontrib><title>HPr prevents FruR-mediated facilitation of RNA polymerase binding to the fru promoter in Vibrio cholerae</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Abstract
Phosphorylation state-dependent interactions of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) components with transcription factors play a key role in carbon catabolite repression (CCR) by glucose in bacteria. Glucose inhibits the PTS-dependent transport of fructose and is preferred over fructose in Vibrio cholerae, but the mechanism is unknown. We have recently shown that, contrary to Escherichia coli, the fructose-dependent transcriptional regulator FruR acts as an activator of the fru operon in V. cholerae and binding of the FruR–fructose 1-phosphate (F1P) complex to an operator facilitates RNA polymerase (RNAP) binding to the fru promoter. Here we show that, in the presence of glucose, dephosphorylated HPr, a general PTS component, binds to FruR. Whereas HPr does not affect DNA-binding affinity of FruR, regardless of the presence of F1P, it prevents the FruR–F1P complex from facilitating the binding of RNAP to the fru promoter. Structural and biochemical analyses of the FruR–HPr complex identify key residues responsible for the V. cholerae-specific FruR–HPr interaction not observed in E. coli. Finally, we reveal how the dephosphorylated HPr interacts with FruR in V. cholerae, whereas the phosphorylated HPr binds to CcpA, which is a global regulator of CCR in Bacillus subtilis and shows structural similarity to FruR.</description><subject>Bacterial Proteins - metabolism</subject><subject>DNA-Directed RNA Polymerases - metabolism</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Fructose - metabolism</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene regulation, Chromatin and Epigenetics</subject><subject>Glucose</subject><subject>Operon</subject><subject>Phosphorylation</subject><subject>Repressor Proteins - metabolism</subject><subject>Vibrio cholerae - metabolism</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU1LHTEUhkOp6K115V6yKoUyNSeZz1UR0VoQFaluQyY5uTftzGSaZAT_vSn3VtpNV2eRhyfnPS8hx8A-A-vE6aTC6fqnMpyzN2QFouZF2dX8LVkxwaoCWNkekHcx_mAMSqjKfXIg6q5t2kasyObqLtA54BNOKdLLsNwXIxqnEhpqlXaDSyo5P1Fv6f3NGZ398DxiUBFp7ybjpjVNnqYNUhuWLPKjTxiom-ij64PzVG_8kHl8T_asGiIe7eYhebi8-H5-VVzffv12fnZdaNFAKlpsTVNqMJZj31dCc7BagKlB6BrQirI1FhXjYExX1bVAYUrMmW0FdYUoDsmXrXde-pxE51xBDXIOblThWXrl5L8vk9vItX-SwHjbdNBlw8edIfhfC8YkRxc1DoOa0C9R8qbj-cCdaDP6aYvq4GMMaF__ASZ_lyNzOXJXTqZP_l7tlf3TRgY-bAG_zP81vQAE85tV</recordid><startdate>20230623</startdate><enddate>20230623</enddate><creator>Yoon, Chang-Kyu</creator><creator>Lee, Seung-Hwan</creator><creator>Zhang, Jing</creator><creator>Lee, Hye-Young</creator><creator>Kim, Min-Kyu</creator><creator>Seok, Yeong-Jae</creator><general>Oxford University Press</general><scope>TOX</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1546-9181</orcidid><orcidid>https://orcid.org/0000-0001-9594-1396</orcidid><orcidid>https://orcid.org/0000-0003-0379-3619</orcidid></search><sort><creationdate>20230623</creationdate><title>HPr prevents FruR-mediated facilitation of RNA polymerase binding to the fru promoter in Vibrio cholerae</title><author>Yoon, Chang-Kyu ; Lee, Seung-Hwan ; Zhang, Jing ; Lee, Hye-Young ; Kim, Min-Kyu ; Seok, Yeong-Jae</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c371t-8e8d74c1df2ebb53c21fc31d613c61ef348dfea021dd95663e3d4e362f5165ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Bacterial Proteins - metabolism</topic><topic>DNA-Directed RNA Polymerases - metabolism</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Fructose - metabolism</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene regulation, Chromatin and Epigenetics</topic><topic>Glucose</topic><topic>Operon</topic><topic>Phosphorylation</topic><topic>Repressor Proteins - metabolism</topic><topic>Vibrio cholerae - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yoon, Chang-Kyu</creatorcontrib><creatorcontrib>Lee, Seung-Hwan</creatorcontrib><creatorcontrib>Zhang, Jing</creatorcontrib><creatorcontrib>Lee, Hye-Young</creatorcontrib><creatorcontrib>Kim, Min-Kyu</creatorcontrib><creatorcontrib>Seok, Yeong-Jae</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yoon, Chang-Kyu</au><au>Lee, Seung-Hwan</au><au>Zhang, Jing</au><au>Lee, Hye-Young</au><au>Kim, Min-Kyu</au><au>Seok, Yeong-Jae</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>HPr prevents FruR-mediated facilitation of RNA polymerase binding to the fru promoter in Vibrio cholerae</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2023-06-23</date><risdate>2023</risdate><volume>51</volume><issue>11</issue><spage>5432</spage><epage>5448</epage><pages>5432-5448</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Abstract
Phosphorylation state-dependent interactions of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) components with transcription factors play a key role in carbon catabolite repression (CCR) by glucose in bacteria. Glucose inhibits the PTS-dependent transport of fructose and is preferred over fructose in Vibrio cholerae, but the mechanism is unknown. We have recently shown that, contrary to Escherichia coli, the fructose-dependent transcriptional regulator FruR acts as an activator of the fru operon in V. cholerae and binding of the FruR–fructose 1-phosphate (F1P) complex to an operator facilitates RNA polymerase (RNAP) binding to the fru promoter. Here we show that, in the presence of glucose, dephosphorylated HPr, a general PTS component, binds to FruR. Whereas HPr does not affect DNA-binding affinity of FruR, regardless of the presence of F1P, it prevents the FruR–F1P complex from facilitating the binding of RNAP to the fru promoter. Structural and biochemical analyses of the FruR–HPr complex identify key residues responsible for the V. cholerae-specific FruR–HPr interaction not observed in E. coli. Finally, we reveal how the dephosphorylated HPr interacts with FruR in V. cholerae, whereas the phosphorylated HPr binds to CcpA, which is a global regulator of CCR in Bacillus subtilis and shows structural similarity to FruR.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>36987873</pmid><doi>10.1093/nar/gkad220</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-1546-9181</orcidid><orcidid>https://orcid.org/0000-0001-9594-1396</orcidid><orcidid>https://orcid.org/0000-0003-0379-3619</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacterial Proteins - metabolism DNA-Directed RNA Polymerases - metabolism Escherichia coli - genetics Escherichia coli - metabolism Fructose - metabolism Gene Expression Regulation, Bacterial Gene regulation, Chromatin and Epigenetics Glucose Operon Phosphorylation Repressor Proteins - metabolism Vibrio cholerae - metabolism |
title | HPr prevents FruR-mediated facilitation of RNA polymerase binding to the fru promoter in Vibrio cholerae |
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