Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB
The Arc (anoxic redox control) two-component system of Escherichia coli, comprising ArcA as the response regulator and ArcB as the sensor histidine kinase, modulates the expression of numerous genes in response to respiratory growth conditions. Under reducing growth conditions, ArcB autophosphorylat...
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| Veröffentlicht in: | The Journal of biological chemistry 2018-08, Vol.293 (34), p.13214-13223 |
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| container_title | The Journal of biological chemistry |
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| creator | Teran-Melo, Juan L. Peña-Sandoval, Gabriela R. Silva-Jimenez, Hortencia Rodriguez, Claudia Alvarez, Adrián F. Georgellis, Dimitris |
| description | The Arc (anoxic redox control) two-component system of Escherichia coli, comprising ArcA as the response regulator and ArcB as the sensor histidine kinase, modulates the expression of numerous genes in response to respiratory growth conditions. Under reducing growth conditions, ArcB autophosphorylates at the expense of ATP, and transphosphorylates ArcA via a His292 → Asp576 → His717 → Asp54 phosphorelay, whereas under oxidizing growth conditions, ArcB catalyzes the dephosphorylation of ArcA-P by a reverse Asp54 → His717 → Asp576 → Pi phosphorelay. However, the exact phosphoryl group transfer routes and the molecular mechanisms determining their directions are unclear. Here, we show that, during signal propagation, the His292 → Asp576 and Asp576 → His717 phosphoryl group transfers within ArcB dimers occur intra- and intermolecularly, respectively. Moreover, we report that, during signal decay, the phosphoryl group transfer from His717 to Asp576 takes place intramolecularly. In conclusion, we present a mechanism that dictates the direction of the phosphoryl group transfer within ArcB dimers and that enables the discrimination of the kinase and phosphatase activities of ArcB. |
| doi_str_mv | 10.1074/jbc.RA118.003910 |
| format | Article |
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Under reducing growth conditions, ArcB autophosphorylates at the expense of ATP, and transphosphorylates ArcA via a His292 → Asp576 → His717 → Asp54 phosphorelay, whereas under oxidizing growth conditions, ArcB catalyzes the dephosphorylation of ArcA-P by a reverse Asp54 → His717 → Asp576 → Pi phosphorelay. However, the exact phosphoryl group transfer routes and the molecular mechanisms determining their directions are unclear. Here, we show that, during signal propagation, the His292 → Asp576 and Asp576 → His717 phosphoryl group transfers within ArcB dimers occur intra- and intermolecularly, respectively. Moreover, we report that, during signal decay, the phosphoryl group transfer from His717 to Asp576 takes place intramolecularly. In conclusion, we present a mechanism that dictates the direction of the phosphoryl group transfer within ArcB dimers and that enables the discrimination of the kinase and phosphatase activities of ArcB.</description><identifier>ISSN: 0021-9258</identifier><identifier>ISSN: 1083-351X</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.RA118.003910</identifier><identifier>PMID: 29945971</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>ArcB/A two-component system ; Aspartic Acid - chemistry ; Aspartic Acid - metabolism ; bacteria ; bacterial signal transduction ; conformation ; Escherichia coli - enzymology ; Escherichia coli Proteins - chemistry ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Histidine - chemistry ; Histidine - metabolism ; histidine kinase ; intermolecular phosphotransfer ; intramolecular phosphotransfer ; Membrane Proteins - chemistry ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Microbiology ; Mutation ; phosphorelay ; phosphoryl transfer ; Phosphorylation ; Protein Kinases - chemistry ; Protein Kinases - genetics ; Protein Kinases - metabolism ; sensor kinase ; Signal Transduction</subject><ispartof>The Journal of biological chemistry, 2018-08, Vol.293 (34), p.13214-13223</ispartof><rights>2018 © 2018 Teran-Melo et al.</rights><rights>2018 Teran-Melo et al.</rights><rights>2018 Teran-Melo et al. 2018 Teran-Melo et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c447t-c9add3754a1cd77a73fc762c639de45a13f32a5b3a359c0b04b3d675507d17e53</citedby><cites>FETCH-LOGICAL-c447t-c9add3754a1cd77a73fc762c639de45a13f32a5b3a359c0b04b3d675507d17e53</cites><orcidid>0000-0002-6114-795X</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/PMC6109937/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6109937/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29945971$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Teran-Melo, Juan L.</creatorcontrib><creatorcontrib>Peña-Sandoval, Gabriela R.</creatorcontrib><creatorcontrib>Silva-Jimenez, Hortencia</creatorcontrib><creatorcontrib>Rodriguez, Claudia</creatorcontrib><creatorcontrib>Alvarez, Adrián F.</creatorcontrib><creatorcontrib>Georgellis, Dimitris</creatorcontrib><title>Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>The Arc (anoxic redox control) two-component system of Escherichia coli, comprising ArcA as the response regulator and ArcB as the sensor histidine kinase, modulates the expression of numerous genes in response to respiratory growth conditions. Under reducing growth conditions, ArcB autophosphorylates at the expense of ATP, and transphosphorylates ArcA via a His292 → Asp576 → His717 → Asp54 phosphorelay, whereas under oxidizing growth conditions, ArcB catalyzes the dephosphorylation of ArcA-P by a reverse Asp54 → His717 → Asp576 → Pi phosphorelay. However, the exact phosphoryl group transfer routes and the molecular mechanisms determining their directions are unclear. Here, we show that, during signal propagation, the His292 → Asp576 and Asp576 → His717 phosphoryl group transfers within ArcB dimers occur intra- and intermolecularly, respectively. Moreover, we report that, during signal decay, the phosphoryl group transfer from His717 to Asp576 takes place intramolecularly. In conclusion, we present a mechanism that dictates the direction of the phosphoryl group transfer within ArcB dimers and that enables the discrimination of the kinase and phosphatase activities of ArcB.</description><subject>ArcB/A two-component system</subject><subject>Aspartic Acid - chemistry</subject><subject>Aspartic Acid - metabolism</subject><subject>bacteria</subject><subject>bacterial signal transduction</subject><subject>conformation</subject><subject>Escherichia coli - enzymology</subject><subject>Escherichia coli Proteins - chemistry</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Histidine - chemistry</subject><subject>Histidine - metabolism</subject><subject>histidine kinase</subject><subject>intermolecular phosphotransfer</subject><subject>intramolecular phosphotransfer</subject><subject>Membrane Proteins - chemistry</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Microbiology</subject><subject>Mutation</subject><subject>phosphorelay</subject><subject>phosphoryl transfer</subject><subject>Phosphorylation</subject><subject>Protein Kinases - chemistry</subject><subject>Protein Kinases - genetics</subject><subject>Protein Kinases - metabolism</subject><subject>sensor kinase</subject><subject>Signal Transduction</subject><issn>0021-9258</issn><issn>1083-351X</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kd9rFDEQx4Mo9qy--yR59GXPZLPZbHwQzuKPQqFQFHwL2WT2bupecia7haP_vKnbFn0wMAQm3_lOZj6EvOZszZlq3l33bn214bxbMyY0Z0_IirNOVELyH0_JirGaV7qW3Ql5kfM1K6fR_Dk5qbVupFZ8RW6v4jxBpnGgh13MJdJxpNsU5wOdkg15gET9nDBsacZtsOOS3mPOGAO1wT_kPTh7pBjotAPqcQ8JHc0Qckx0h3lCjwHoTww2A90k9_EleTbYMcOr-_uUfP_86dvZ1-ri8sv52eaick2jpspp671QsrHceaWsEoNTbe1aoT000nIxiNrKXlghtWM9a3rhWyUlU54rkOKUfFh8D3O_B-8glBFGc0i4t-lookXz70vAndnGG9NyprVQxeDtvUGKv2bIkynjOxhHGyDO2dSsZV3bdaorUrZIXYo5Jxge23Bm7piZwsz8YWYWZqXkzd_feyx4gFQE7xcBlCXdICSTHUJw4DGBm4yP-H_33w5GqhI</recordid><startdate>20180824</startdate><enddate>20180824</enddate><creator>Teran-Melo, Juan L.</creator><creator>Peña-Sandoval, Gabriela R.</creator><creator>Silva-Jimenez, Hortencia</creator><creator>Rodriguez, Claudia</creator><creator>Alvarez, Adrián F.</creator><creator>Georgellis, Dimitris</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</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/0000-0002-6114-795X</orcidid></search><sort><creationdate>20180824</creationdate><title>Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB</title><author>Teran-Melo, Juan L. ; Peña-Sandoval, Gabriela R. ; Silva-Jimenez, Hortencia ; Rodriguez, Claudia ; Alvarez, Adrián F. ; Georgellis, Dimitris</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c447t-c9add3754a1cd77a73fc762c639de45a13f32a5b3a359c0b04b3d675507d17e53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>ArcB/A two-component system</topic><topic>Aspartic Acid - chemistry</topic><topic>Aspartic Acid - metabolism</topic><topic>bacteria</topic><topic>bacterial signal transduction</topic><topic>conformation</topic><topic>Escherichia coli - enzymology</topic><topic>Escherichia coli Proteins - chemistry</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Histidine - chemistry</topic><topic>Histidine - metabolism</topic><topic>histidine kinase</topic><topic>intermolecular phosphotransfer</topic><topic>intramolecular phosphotransfer</topic><topic>Membrane Proteins - chemistry</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Microbiology</topic><topic>Mutation</topic><topic>phosphorelay</topic><topic>phosphoryl transfer</topic><topic>Phosphorylation</topic><topic>Protein Kinases - chemistry</topic><topic>Protein Kinases - genetics</topic><topic>Protein Kinases - metabolism</topic><topic>sensor kinase</topic><topic>Signal Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Teran-Melo, Juan L.</creatorcontrib><creatorcontrib>Peña-Sandoval, Gabriela R.</creatorcontrib><creatorcontrib>Silva-Jimenez, Hortencia</creatorcontrib><creatorcontrib>Rodriguez, Claudia</creatorcontrib><creatorcontrib>Alvarez, Adrián F.</creatorcontrib><creatorcontrib>Georgellis, Dimitris</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Teran-Melo, Juan L.</au><au>Peña-Sandoval, Gabriela R.</au><au>Silva-Jimenez, Hortencia</au><au>Rodriguez, Claudia</au><au>Alvarez, Adrián F.</au><au>Georgellis, Dimitris</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2018-08-24</date><risdate>2018</risdate><volume>293</volume><issue>34</issue><spage>13214</spage><epage>13223</epage><pages>13214-13223</pages><issn>0021-9258</issn><issn>1083-351X</issn><eissn>1083-351X</eissn><abstract>The Arc (anoxic redox control) two-component system of Escherichia coli, comprising ArcA as the response regulator and ArcB as the sensor histidine kinase, modulates the expression of numerous genes in response to respiratory growth conditions. Under reducing growth conditions, ArcB autophosphorylates at the expense of ATP, and transphosphorylates ArcA via a His292 → Asp576 → His717 → Asp54 phosphorelay, whereas under oxidizing growth conditions, ArcB catalyzes the dephosphorylation of ArcA-P by a reverse Asp54 → His717 → Asp576 → Pi phosphorelay. However, the exact phosphoryl group transfer routes and the molecular mechanisms determining their directions are unclear. Here, we show that, during signal propagation, the His292 → Asp576 and Asp576 → His717 phosphoryl group transfers within ArcB dimers occur intra- and intermolecularly, respectively. Moreover, we report that, during signal decay, the phosphoryl group transfer from His717 to Asp576 takes place intramolecularly. In conclusion, we present a mechanism that dictates the direction of the phosphoryl group transfer within ArcB dimers and that enables the discrimination of the kinase and phosphatase activities of ArcB.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>29945971</pmid><doi>10.1074/jbc.RA118.003910</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-6114-795X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | ArcB/A two-component system Aspartic Acid - chemistry Aspartic Acid - metabolism bacteria bacterial signal transduction conformation Escherichia coli - enzymology Escherichia coli Proteins - chemistry Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Histidine - chemistry Histidine - metabolism histidine kinase intermolecular phosphotransfer intramolecular phosphotransfer Membrane Proteins - chemistry Membrane Proteins - genetics Membrane Proteins - metabolism Microbiology Mutation phosphorelay phosphoryl transfer Phosphorylation Protein Kinases - chemistry Protein Kinases - genetics Protein Kinases - metabolism sensor kinase Signal Transduction |
| title | Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB |
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