Characterization of the roles of NikR, a nickel‐responsive pleiotropic autoregulator of Helicobacter pylori
Summary The Helicobacter pylori genome contains a gene (hp1338 or nikR) that encodes a nickel‐dependent regulator that is homologous to the Escherichia coli nickel‐responsive regulator, NikR. The H. pylori nikR product acts as a pleiotropic metal‐dependent regulator. We constructed a non‐polar isoge...
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| Veröffentlicht in: | Molecular microbiology 2003-08, Vol.49 (4), p.947-963 |
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| creator | Contreras, Monica Thiberge, Jean‐Michel Mandrand‐Berthelot, Marie‐Andrée Labigne, Agnès |
| description | Summary
The Helicobacter pylori genome contains a gene (hp1338 or nikR) that encodes a nickel‐dependent regulator that is homologous to the Escherichia coli nickel‐responsive regulator, NikR. The H. pylori nikR product acts as a pleiotropic metal‐dependent regulator. We constructed a non‐polar isogenic mutant deleted for the nikR gene. NikR was essential for the survival of H. pylori in the presence of high nickel and cobalt ion concentrations in vitro. We screened a DNA macroarray for genes that were differentially expressed in parental and nikR‐deficient H. pylori strains grown in the presence of excess nickel. We found that H. pylori NikR mediates the expression of nickel‐activated and ‐repressed genes. In the presence of excess nickel, NikR activated the transcription of ureA‐ureB (hp72–73), nixA (hp1077 ), copA2 (hp1072), hpn (hp1427 ) and hpn‐like (hp1432) genes and repressed the expression of genes encoding proteins involved in ferric iron uptake and storage [pfr (hp0653), fur (hp1027 ), frpB4 (hp1512), exbB/exbD (hp1339–1340), ceuE (hp1561)], motility [cheV (hp616), flaA (hp0601), flaB (hp0115 )], stress responses [hrcA‐grpE‐dnaK (hp111–110–109)] and encoding outer‐membrane proteins [omp11(hp0472), omp31 (hp1469), omp32 (hp1501)]. Slot blot DNA/RNA hybridization experiments using RNA from three independent bacterial cultures confirmed the transcriptome data for 10 selected genes. The results of gel shift experiments using purified native NikR, β‐galactosidase assays with the region between nikR and the exbB/exbD divergent operon, and the study of exbB gene expression using a gentamicin/apramycin reporter gene in H. pylori indicated that NikR is an autorepressor that binds to this intergenic region and also controls the expression of the exbB/exbD/tonB operon, which provides energy for ferric iron uptake. Thus, as previously suggested for Fur in H. pylori, NikR appears to be a global regulator of the metabolism of some divalent cations within a highly complex regulated network. |
| doi_str_mv | 10.1046/j.1365-2958.2003.03621.x |
| format | Article |
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The Helicobacter pylori genome contains a gene (hp1338 or nikR) that encodes a nickel‐dependent regulator that is homologous to the Escherichia coli nickel‐responsive regulator, NikR. The H. pylori nikR product acts as a pleiotropic metal‐dependent regulator. We constructed a non‐polar isogenic mutant deleted for the nikR gene. NikR was essential for the survival of H. pylori in the presence of high nickel and cobalt ion concentrations in vitro. We screened a DNA macroarray for genes that were differentially expressed in parental and nikR‐deficient H. pylori strains grown in the presence of excess nickel. We found that H. pylori NikR mediates the expression of nickel‐activated and ‐repressed genes. In the presence of excess nickel, NikR activated the transcription of ureA‐ureB (hp72–73), nixA (hp1077 ), copA2 (hp1072), hpn (hp1427 ) and hpn‐like (hp1432) genes and repressed the expression of genes encoding proteins involved in ferric iron uptake and storage [pfr (hp0653), fur (hp1027 ), frpB4 (hp1512), exbB/exbD (hp1339–1340), ceuE (hp1561)], motility [cheV (hp616), flaA (hp0601), flaB (hp0115 )], stress responses [hrcA‐grpE‐dnaK (hp111–110–109)] and encoding outer‐membrane proteins [omp11(hp0472), omp31 (hp1469), omp32 (hp1501)]. Slot blot DNA/RNA hybridization experiments using RNA from three independent bacterial cultures confirmed the transcriptome data for 10 selected genes. The results of gel shift experiments using purified native NikR, β‐galactosidase assays with the region between nikR and the exbB/exbD divergent operon, and the study of exbB gene expression using a gentamicin/apramycin reporter gene in H. pylori indicated that NikR is an autorepressor that binds to this intergenic region and also controls the expression of the exbB/exbD/tonB operon, which provides energy for ferric iron uptake. Thus, as previously suggested for Fur in H. pylori, NikR appears to be a global regulator of the metabolism of some divalent cations within a highly complex regulated network.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1046/j.1365-2958.2003.03621.x</identifier><identifier>PMID: 12890020</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>Amino Acid Sequence ; Base Sequence ; Chromosomes, Bacterial ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial ; Genetic Vectors ; Helicobacter pylori - genetics ; Helicobacter pylori - metabolism ; Molecular Sequence Data ; Nickel - metabolism ; Oligonucleotide Array Sequence Analysis ; Open Reading Frames ; Operon ; Recombinant Proteins - genetics ; Recombinant Proteins - metabolism ; Repressor Proteins - genetics ; Repressor Proteins - metabolism</subject><ispartof>Molecular microbiology, 2003-08, Vol.49 (4), p.947-963</ispartof><rights>Copyright Blackwell Scientific Publications Ltd. Aug 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5391-9173b4e3e5c80253c06f8a122b6d525685619a27d566dbc1b15543efff841d913</citedby><cites>FETCH-LOGICAL-c5391-9173b4e3e5c80253c06f8a122b6d525685619a27d566dbc1b15543efff841d913</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1046%2Fj.1365-2958.2003.03621.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1046%2Fj.1365-2958.2003.03621.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12890020$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Contreras, Monica</creatorcontrib><creatorcontrib>Thiberge, Jean‐Michel</creatorcontrib><creatorcontrib>Mandrand‐Berthelot, Marie‐Andrée</creatorcontrib><creatorcontrib>Labigne, Agnès</creatorcontrib><title>Characterization of the roles of NikR, a nickel‐responsive pleiotropic autoregulator of Helicobacter pylori</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
The Helicobacter pylori genome contains a gene (hp1338 or nikR) that encodes a nickel‐dependent regulator that is homologous to the Escherichia coli nickel‐responsive regulator, NikR. The H. pylori nikR product acts as a pleiotropic metal‐dependent regulator. We constructed a non‐polar isogenic mutant deleted for the nikR gene. NikR was essential for the survival of H. pylori in the presence of high nickel and cobalt ion concentrations in vitro. We screened a DNA macroarray for genes that were differentially expressed in parental and nikR‐deficient H. pylori strains grown in the presence of excess nickel. We found that H. pylori NikR mediates the expression of nickel‐activated and ‐repressed genes. In the presence of excess nickel, NikR activated the transcription of ureA‐ureB (hp72–73), nixA (hp1077 ), copA2 (hp1072), hpn (hp1427 ) and hpn‐like (hp1432) genes and repressed the expression of genes encoding proteins involved in ferric iron uptake and storage [pfr (hp0653), fur (hp1027 ), frpB4 (hp1512), exbB/exbD (hp1339–1340), ceuE (hp1561)], motility [cheV (hp616), flaA (hp0601), flaB (hp0115 )], stress responses [hrcA‐grpE‐dnaK (hp111–110–109)] and encoding outer‐membrane proteins [omp11(hp0472), omp31 (hp1469), omp32 (hp1501)]. Slot blot DNA/RNA hybridization experiments using RNA from three independent bacterial cultures confirmed the transcriptome data for 10 selected genes. The results of gel shift experiments using purified native NikR, β‐galactosidase assays with the region between nikR and the exbB/exbD divergent operon, and the study of exbB gene expression using a gentamicin/apramycin reporter gene in H. pylori indicated that NikR is an autorepressor that binds to this intergenic region and also controls the expression of the exbB/exbD/tonB operon, which provides energy for ferric iron uptake. Thus, as previously suggested for Fur in H. pylori, NikR appears to be a global regulator of the metabolism of some divalent cations within a highly complex regulated network.</description><subject>Amino Acid Sequence</subject><subject>Base Sequence</subject><subject>Chromosomes, Bacterial</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genetic Vectors</subject><subject>Helicobacter pylori - genetics</subject><subject>Helicobacter pylori - metabolism</subject><subject>Molecular Sequence Data</subject><subject>Nickel - metabolism</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Open Reading Frames</subject><subject>Operon</subject><subject>Recombinant Proteins - genetics</subject><subject>Recombinant Proteins - metabolism</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1u1DAURi0EotPCKyCLBSuS-if22AsWaFTaSi2VEEjsLMe5oZ564mAn0GHFI_CMPEmTzohKbGB1bfl835V1EMKUlJRU8nhdUi5FwbRQJSOEl4RLRsvbR2jx5-ExWhAtSMEV-3yADnNeE0I5kfwpOqBMaUIYWaDN6tom6wZI_ocdfOxwbPFwDTjFAHm-vPc3H15jizvvbiD8_vkrQe5jl_03wH0AH4cUe--wHYeY4MsY7DTn4BkE72J9X477bYjJP0NPWhsyPN_PI_Tp3cnH1VlxcXV6vnp7UTjBNS00XfK6Ag7CKcIEd0S2ylLGatkIJqQSkmrLlo2QsqkdrakQFYe2bVVFG035EXq16-1T_DpCHszGZwch2A7imM2SCzotYf8EqVJMqEpM4Mu_wHUcUzd9wlAtBVGaLSdI7SCXYs4JWtMnv7FpaygxszizNrMfM_sxszhzL87cTtEX-_6x3kDzENybmoA3O-C7D7D972JzeXk-n_gdZUCn4A</recordid><startdate>200308</startdate><enddate>200308</enddate><creator>Contreras, Monica</creator><creator>Thiberge, Jean‐Michel</creator><creator>Mandrand‐Berthelot, Marie‐Andrée</creator><creator>Labigne, Agnès</creator><general>Blackwell Science Ltd</general><general>Blackwell Publishing Ltd</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>200308</creationdate><title>Characterization of the roles of NikR, a nickel‐responsive pleiotropic autoregulator of Helicobacter pylori</title><author>Contreras, Monica ; Thiberge, Jean‐Michel ; Mandrand‐Berthelot, Marie‐Andrée ; Labigne, Agnès</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5391-9173b4e3e5c80253c06f8a122b6d525685619a27d566dbc1b15543efff841d913</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Amino Acid Sequence</topic><topic>Base Sequence</topic><topic>Chromosomes, Bacterial</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genetic Vectors</topic><topic>Helicobacter pylori - genetics</topic><topic>Helicobacter pylori - metabolism</topic><topic>Molecular Sequence Data</topic><topic>Nickel - metabolism</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Open Reading Frames</topic><topic>Operon</topic><topic>Recombinant Proteins - genetics</topic><topic>Recombinant Proteins - metabolism</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Contreras, Monica</creatorcontrib><creatorcontrib>Thiberge, Jean‐Michel</creatorcontrib><creatorcontrib>Mandrand‐Berthelot, Marie‐Andrée</creatorcontrib><creatorcontrib>Labigne, Agnès</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Contreras, Monica</au><au>Thiberge, Jean‐Michel</au><au>Mandrand‐Berthelot, Marie‐Andrée</au><au>Labigne, Agnès</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of the roles of NikR, a nickel‐responsive pleiotropic autoregulator of Helicobacter pylori</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2003-08</date><risdate>2003</risdate><volume>49</volume><issue>4</issue><spage>947</spage><epage>963</epage><pages>947-963</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
The Helicobacter pylori genome contains a gene (hp1338 or nikR) that encodes a nickel‐dependent regulator that is homologous to the Escherichia coli nickel‐responsive regulator, NikR. The H. pylori nikR product acts as a pleiotropic metal‐dependent regulator. We constructed a non‐polar isogenic mutant deleted for the nikR gene. NikR was essential for the survival of H. pylori in the presence of high nickel and cobalt ion concentrations in vitro. We screened a DNA macroarray for genes that were differentially expressed in parental and nikR‐deficient H. pylori strains grown in the presence of excess nickel. We found that H. pylori NikR mediates the expression of nickel‐activated and ‐repressed genes. In the presence of excess nickel, NikR activated the transcription of ureA‐ureB (hp72–73), nixA (hp1077 ), copA2 (hp1072), hpn (hp1427 ) and hpn‐like (hp1432) genes and repressed the expression of genes encoding proteins involved in ferric iron uptake and storage [pfr (hp0653), fur (hp1027 ), frpB4 (hp1512), exbB/exbD (hp1339–1340), ceuE (hp1561)], motility [cheV (hp616), flaA (hp0601), flaB (hp0115 )], stress responses [hrcA‐grpE‐dnaK (hp111–110–109)] and encoding outer‐membrane proteins [omp11(hp0472), omp31 (hp1469), omp32 (hp1501)]. Slot blot DNA/RNA hybridization experiments using RNA from three independent bacterial cultures confirmed the transcriptome data for 10 selected genes. The results of gel shift experiments using purified native NikR, β‐galactosidase assays with the region between nikR and the exbB/exbD divergent operon, and the study of exbB gene expression using a gentamicin/apramycin reporter gene in H. pylori indicated that NikR is an autorepressor that binds to this intergenic region and also controls the expression of the exbB/exbD/tonB operon, which provides energy for ferric iron uptake. Thus, as previously suggested for Fur in H. pylori, NikR appears to be a global regulator of the metabolism of some divalent cations within a highly complex regulated network.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>12890020</pmid><doi>10.1046/j.1365-2958.2003.03621.x</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Sequence Base Sequence Chromosomes, Bacterial Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Gene Expression Profiling Gene Expression Regulation, Bacterial Genetic Vectors Helicobacter pylori - genetics Helicobacter pylori - metabolism Molecular Sequence Data Nickel - metabolism Oligonucleotide Array Sequence Analysis Open Reading Frames Operon Recombinant Proteins - genetics Recombinant Proteins - metabolism Repressor Proteins - genetics Repressor Proteins - metabolism |
| title | Characterization of the roles of NikR, a nickel‐responsive pleiotropic autoregulator of Helicobacter pylori |
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