Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade
Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidativ...
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creator | Tossounian, Maria-Armineh Khanh Truong, Anh-Co Buts, Lieven Wahni, Khadija Mourenza, Álvaro Leermakers, Martine Vertommen, Didier Mateos, Luis Mariano Volkov, Alexander N. Messens, Joris |
description | Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidative stress. Although some aspects of the catalytic mechanism of the Msr enzymes have been reported, several details still await full elucidation. Here, we solved the solution structure of C. diphtheriae MsrB (Cd-MsrB) and unraveled its catalytic and oxidation-protection mechanisms. Cd-MsrB catalyzes methionine sulfoxide reduction involving three redox-active cysteines. Using NMR heteronuclear single-quantum coherence spectra, kinetics, biochemical assays, and MS analyses, we show that the conserved nucleophilic residue Cys-122 is S-sulfenylated after substrate reduction, which is then resolved by a conserved cysteine, Cys-66, or by the nonconserved residue Cys-127. We noted that the overall structural changes during the disulfide cascade expose the Cys-122–Cys-66 disulfide to recycling through thioredoxin. In the presence of hydrogen peroxide, Cd-MsrB formed reversible intra- and intermolecular disulfides without losing its Cys-coordinated Zn2+, and only the nonconserved Cys-127 reacted with the low-molecular-weight (LMW) thiol mycothiol, protecting it from overoxidation. In summary, our structure-function analyses reveal critical details of the Cd-MsrB catalytic mechanism, including a major structural rearrangement that primes the Cys-122–Cys-66 disulfide for thioredoxin reduction and a reversible protection against excessive oxidation of the catalytic cysteines in Cd-MsrB through intra- and intermolecular disulfide formation and S-mycothiolation. |
doi_str_mv | 10.1074/jbc.RA119.012438 |
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In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidative stress. Although some aspects of the catalytic mechanism of the Msr enzymes have been reported, several details still await full elucidation. Here, we solved the solution structure of C. diphtheriae MsrB (Cd-MsrB) and unraveled its catalytic and oxidation-protection mechanisms. Cd-MsrB catalyzes methionine sulfoxide reduction involving three redox-active cysteines. Using NMR heteronuclear single-quantum coherence spectra, kinetics, biochemical assays, and MS analyses, we show that the conserved nucleophilic residue Cys-122 is S-sulfenylated after substrate reduction, which is then resolved by a conserved cysteine, Cys-66, or by the nonconserved residue Cys-127. We noted that the overall structural changes during the disulfide cascade expose the Cys-122–Cys-66 disulfide to recycling through thioredoxin. In the presence of hydrogen peroxide, Cd-MsrB formed reversible intra- and intermolecular disulfides without losing its Cys-coordinated Zn2+, and only the nonconserved Cys-127 reacted with the low-molecular-weight (LMW) thiol mycothiol, protecting it from overoxidation. In summary, our structure-function analyses reveal critical details of the Cd-MsrB catalytic mechanism, including a major structural rearrangement that primes the Cys-122–Cys-66 disulfide for thioredoxin reduction and a reversible protection against excessive oxidation of the catalytic cysteines in Cd-MsrB through intra- and intermolecular disulfide formation and S-mycothiolation.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.RA119.012438</identifier><identifier>PMID: 31992594</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Biocatalysis ; biochemistry ; Catalytic Domain ; Conserved Sequence ; Corynebacterium diphtheriae - enzymology ; Cysteine - metabolism ; Disulfides - metabolism ; enzyme mechanism ; enzyme structure ; Enzymology ; Glycopeptides - metabolism ; hydrogen peroxide ; Inositol - metabolism ; kinetics ; Magnetic Resonance Spectroscopy ; methionine sulfoxide ; Methionine Sulfoxide Reductases - chemistry ; Methionine Sulfoxide Reductases - metabolism ; Models, Molecular ; nuclear magnetic resonance (NMR) ; Oxidation-Reduction ; redox regulation ; Safrole - analogs & derivatives ; Safrole - metabolism ; Substrate Specificity ; Sulfenic Acids - metabolism ; Thioredoxin-Disulfide Reductase - metabolism ; Thioredoxins - metabolism ; Zinc - metabolism</subject><ispartof>The Journal of biological chemistry, 2020-03, Vol.295 (11), p.3664-3677</ispartof><rights>2020 © 2020 Tossounian et al.</rights><rights>2020 Tossounian et al.</rights><rights>2020 Tossounian et al. 2020 Tossounian et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c447t-da84fdd836e01ee65b2495b81d25b984f5c39de412880f037edda39c8202b7ea3</citedby><cites>FETCH-LOGICAL-c447t-da84fdd836e01ee65b2495b81d25b984f5c39de412880f037edda39c8202b7ea3</cites><orcidid>0000-0003-3679-7376 ; 0000-0002-2128-8264</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/PMC7076214/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076214/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31992594$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tossounian, Maria-Armineh</creatorcontrib><creatorcontrib>Khanh Truong, Anh-Co</creatorcontrib><creatorcontrib>Buts, Lieven</creatorcontrib><creatorcontrib>Wahni, Khadija</creatorcontrib><creatorcontrib>Mourenza, Álvaro</creatorcontrib><creatorcontrib>Leermakers, Martine</creatorcontrib><creatorcontrib>Vertommen, Didier</creatorcontrib><creatorcontrib>Mateos, Luis Mariano</creatorcontrib><creatorcontrib>Volkov, Alexander N.</creatorcontrib><creatorcontrib>Messens, Joris</creatorcontrib><title>Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidative stress. Although some aspects of the catalytic mechanism of the Msr enzymes have been reported, several details still await full elucidation. Here, we solved the solution structure of C. diphtheriae MsrB (Cd-MsrB) and unraveled its catalytic and oxidation-protection mechanisms. Cd-MsrB catalyzes methionine sulfoxide reduction involving three redox-active cysteines. Using NMR heteronuclear single-quantum coherence spectra, kinetics, biochemical assays, and MS analyses, we show that the conserved nucleophilic residue Cys-122 is S-sulfenylated after substrate reduction, which is then resolved by a conserved cysteine, Cys-66, or by the nonconserved residue Cys-127. We noted that the overall structural changes during the disulfide cascade expose the Cys-122–Cys-66 disulfide to recycling through thioredoxin. In the presence of hydrogen peroxide, Cd-MsrB formed reversible intra- and intermolecular disulfides without losing its Cys-coordinated Zn2+, and only the nonconserved Cys-127 reacted with the low-molecular-weight (LMW) thiol mycothiol, protecting it from overoxidation. In summary, our structure-function analyses reveal critical details of the Cd-MsrB catalytic mechanism, including a major structural rearrangement that primes the Cys-122–Cys-66 disulfide for thioredoxin reduction and a reversible protection against excessive oxidation of the catalytic cysteines in Cd-MsrB through intra- and intermolecular disulfide formation and S-mycothiolation.</description><subject>Biocatalysis</subject><subject>biochemistry</subject><subject>Catalytic Domain</subject><subject>Conserved Sequence</subject><subject>Corynebacterium diphtheriae - enzymology</subject><subject>Cysteine - metabolism</subject><subject>Disulfides - metabolism</subject><subject>enzyme mechanism</subject><subject>enzyme structure</subject><subject>Enzymology</subject><subject>Glycopeptides - metabolism</subject><subject>hydrogen peroxide</subject><subject>Inositol - metabolism</subject><subject>kinetics</subject><subject>Magnetic Resonance Spectroscopy</subject><subject>methionine sulfoxide</subject><subject>Methionine Sulfoxide Reductases - chemistry</subject><subject>Methionine Sulfoxide Reductases - metabolism</subject><subject>Models, Molecular</subject><subject>nuclear magnetic resonance (NMR)</subject><subject>Oxidation-Reduction</subject><subject>redox regulation</subject><subject>Safrole - analogs & derivatives</subject><subject>Safrole - metabolism</subject><subject>Substrate Specificity</subject><subject>Sulfenic Acids - metabolism</subject><subject>Thioredoxin-Disulfide Reductase - metabolism</subject><subject>Thioredoxins - metabolism</subject><subject>Zinc - metabolism</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU2LFDEQhoMo7rh69yQ5eukxXz2deBDWwY-FXQRR8Baqk2onS3dnTLoHxz_g3zazs7sosrkkpJ56UuQl5DlnS84a9eqqdcvPZ5ybJeNCSf2ALDjTspI1__aQLBgTvDKi1ifkSc5XrCxl-GNyIrkp10YtyO9LnDYhjmFEmue-iz-DR5rQz26CjPQt7VIc6Dqm_YgtuAlTmAfqw3YzbcoZkDqYoN__wvyfoHjpLgCFkYZxSjDEHt3cQyr9B_ZAOsgOPD4ljzroMz672U_J1_fvvqw_VhefPpyvzy4qp1QzVR606rzXcoWMI67qVihTt5p7Ubem1GonjUfFhdasY7JB70EapwUTbYMgT8mbo3c7twN6h4e5ertNYYC0txGC_bcyho39Hne2Yc1KcFUEL28EKf6YMU92CNlh38OIcc5WSKWFYPoaZUfUpZhzwu7uGc7sIT9b8rPX-dljfqXlxd_j3TXcBlaA10cAyyftAiabXcDRoQ8J3WR9DPfb_wASBq_P</recordid><startdate>20200313</startdate><enddate>20200313</enddate><creator>Tossounian, Maria-Armineh</creator><creator>Khanh Truong, Anh-Co</creator><creator>Buts, Lieven</creator><creator>Wahni, Khadija</creator><creator>Mourenza, Álvaro</creator><creator>Leermakers, Martine</creator><creator>Vertommen, Didier</creator><creator>Mateos, Luis Mariano</creator><creator>Volkov, Alexander N.</creator><creator>Messens, Joris</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/0000-0003-3679-7376</orcidid><orcidid>https://orcid.org/0000-0002-2128-8264</orcidid></search><sort><creationdate>20200313</creationdate><title>Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade</title><author>Tossounian, Maria-Armineh ; Khanh Truong, Anh-Co ; Buts, Lieven ; Wahni, Khadija ; Mourenza, Álvaro ; Leermakers, Martine ; Vertommen, Didier ; Mateos, Luis Mariano ; Volkov, Alexander N. ; Messens, Joris</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c447t-da84fdd836e01ee65b2495b81d25b984f5c39de412880f037edda39c8202b7ea3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Biocatalysis</topic><topic>biochemistry</topic><topic>Catalytic Domain</topic><topic>Conserved Sequence</topic><topic>Corynebacterium diphtheriae - enzymology</topic><topic>Cysteine - metabolism</topic><topic>Disulfides - metabolism</topic><topic>enzyme mechanism</topic><topic>enzyme structure</topic><topic>Enzymology</topic><topic>Glycopeptides - metabolism</topic><topic>hydrogen peroxide</topic><topic>Inositol - metabolism</topic><topic>kinetics</topic><topic>Magnetic Resonance Spectroscopy</topic><topic>methionine sulfoxide</topic><topic>Methionine Sulfoxide Reductases - chemistry</topic><topic>Methionine Sulfoxide Reductases - metabolism</topic><topic>Models, Molecular</topic><topic>nuclear magnetic resonance (NMR)</topic><topic>Oxidation-Reduction</topic><topic>redox regulation</topic><topic>Safrole - analogs & derivatives</topic><topic>Safrole - metabolism</topic><topic>Substrate Specificity</topic><topic>Sulfenic Acids - metabolism</topic><topic>Thioredoxin-Disulfide Reductase - metabolism</topic><topic>Thioredoxins - metabolism</topic><topic>Zinc - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tossounian, Maria-Armineh</creatorcontrib><creatorcontrib>Khanh Truong, Anh-Co</creatorcontrib><creatorcontrib>Buts, Lieven</creatorcontrib><creatorcontrib>Wahni, Khadija</creatorcontrib><creatorcontrib>Mourenza, Álvaro</creatorcontrib><creatorcontrib>Leermakers, Martine</creatorcontrib><creatorcontrib>Vertommen, Didier</creatorcontrib><creatorcontrib>Mateos, Luis Mariano</creatorcontrib><creatorcontrib>Volkov, Alexander N.</creatorcontrib><creatorcontrib>Messens, Joris</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>Tossounian, Maria-Armineh</au><au>Khanh Truong, Anh-Co</au><au>Buts, Lieven</au><au>Wahni, Khadija</au><au>Mourenza, Álvaro</au><au>Leermakers, Martine</au><au>Vertommen, Didier</au><au>Mateos, Luis Mariano</au><au>Volkov, Alexander N.</au><au>Messens, Joris</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2020-03-13</date><risdate>2020</risdate><volume>295</volume><issue>11</issue><spage>3664</spage><epage>3677</epage><pages>3664-3677</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidative stress. Although some aspects of the catalytic mechanism of the Msr enzymes have been reported, several details still await full elucidation. Here, we solved the solution structure of C. diphtheriae MsrB (Cd-MsrB) and unraveled its catalytic and oxidation-protection mechanisms. Cd-MsrB catalyzes methionine sulfoxide reduction involving three redox-active cysteines. Using NMR heteronuclear single-quantum coherence spectra, kinetics, biochemical assays, and MS analyses, we show that the conserved nucleophilic residue Cys-122 is S-sulfenylated after substrate reduction, which is then resolved by a conserved cysteine, Cys-66, or by the nonconserved residue Cys-127. We noted that the overall structural changes during the disulfide cascade expose the Cys-122–Cys-66 disulfide to recycling through thioredoxin. In the presence of hydrogen peroxide, Cd-MsrB formed reversible intra- and intermolecular disulfides without losing its Cys-coordinated Zn2+, and only the nonconserved Cys-127 reacted with the low-molecular-weight (LMW) thiol mycothiol, protecting it from overoxidation. In summary, our structure-function analyses reveal critical details of the Cd-MsrB catalytic mechanism, including a major structural rearrangement that primes the Cys-122–Cys-66 disulfide for thioredoxin reduction and a reversible protection against excessive oxidation of the catalytic cysteines in Cd-MsrB through intra- and intermolecular disulfide formation and S-mycothiolation.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31992594</pmid><doi>10.1074/jbc.RA119.012438</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3679-7376</orcidid><orcidid>https://orcid.org/0000-0002-2128-8264</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biocatalysis biochemistry Catalytic Domain Conserved Sequence Corynebacterium diphtheriae - enzymology Cysteine - metabolism Disulfides - metabolism enzyme mechanism enzyme structure Enzymology Glycopeptides - metabolism hydrogen peroxide Inositol - metabolism kinetics Magnetic Resonance Spectroscopy methionine sulfoxide Methionine Sulfoxide Reductases - chemistry Methionine Sulfoxide Reductases - metabolism Models, Molecular nuclear magnetic resonance (NMR) Oxidation-Reduction redox regulation Safrole - analogs & derivatives Safrole - metabolism Substrate Specificity Sulfenic Acids - metabolism Thioredoxin-Disulfide Reductase - metabolism Thioredoxins - metabolism Zinc - metabolism |
title | Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade |
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