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The DnaK Chaperone Uses Different Mechanisms To Promote and Inhibit Replication of Vibrio cholerae Chromosome 2

Identifieur interne : 000703 ( Pmc/Checkpoint ); précédent : 000702; suivant : 000704

The DnaK Chaperone Uses Different Mechanisms To Promote and Inhibit Replication of Vibrio cholerae Chromosome 2

Auteurs : Jyoti K. Jha [États-Unis] ; Mi Li [États-Unis] ; Rodolfo Ghirlando [États-Unis] ; Lisa M. Miller Jenkins [États-Unis] ; Alexander Wlodawer [États-Unis] ; Dhruba Chattoraj [États-Unis]

Source :

RBID : PMC:5395669

Abstract

ABSTRACT

Replication of Vibrio cholerae chromosome 2 (Chr2) depends on molecular chaperone DnaK to facilitate binding of the initiator (RctB) to the replication origin. The binding occurs at two kinds of site, 12-mers and 39-mers, which promote and inhibit replication, respectively. Here we show that DnaK employs different mechanisms to enhance the two kinds of binding. We found that mutations in rctB that reduce DnaK binding also reduce 12-mer binding and initiation. The initiation defect is suppressed by second-site mutations that increase 12-mer binding only marginally. Instead, they reduce replication inhibitory mechanisms: RctB dimerization and 39-mer binding. One suppressing change was in a dimerization domain which is folded similarly to the initiator of an iteron plasmid—the presumed progenitor of Chr2. In plasmids, DnaK promotes initiation by reducing dimerization. A different mutation was in the 39-mer binding domain of RctB and inactivated it, indicating an alternative suppression mechanism. Paradoxically, although DnaK increases 39-mer binding, the increase was also achieved by inactivating the DnaK binding site of RctB. This result suggests that the site inhibits the 39-mer binding domain (via autoinhibition) when prevented from binding DnaK. Taken together, our results reveal an important feature of the transition from plasmid to chromosome: the Chr2 initiator retains the plasmid-like dimerization domain and its control by chaperones but uses the chaperones in an unprecedented way to control the inhibitory 39-mer binding.


Url:
DOI: 10.1128/mBio.00427-17
PubMed: 28420739
PubMed Central: 5395669


Affiliations:


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PMC:5395669

Le document en format XML

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chromosome 2 (Chr2) depends on molecular chaperone DnaK to facilitate binding of the initiator (RctB) to the replication origin. The binding occurs at two kinds of site, 12-mers and 39-mers, which promote and inhibit replication, respectively. Here we show that DnaK employs different mechanisms to enhance the two kinds of binding. We found that mutations in
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">mBio</journal-id>
<journal-id journal-id-type="iso-abbrev">MBio</journal-id>
<journal-id journal-id-type="hwp">mbio</journal-id>
<journal-id journal-id-type="pmc">mbio</journal-id>
<journal-id journal-id-type="publisher-id">mBio</journal-id>
<journal-title-group>
<journal-title>mBio</journal-title>
</journal-title-group>
<issn pub-type="epub">2150-7511</issn>
<publisher>
<publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
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</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">28420739</article-id>
<article-id pub-id-type="pmc">5395669</article-id>
<article-id pub-id-type="publisher-id">mBio00427-17</article-id>
<article-id pub-id-type="doi">10.1128/mBio.00427-17</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>The DnaK Chaperone Uses Different Mechanisms To Promote and Inhibit Replication of
<italic>Vibrio cholerae</italic>
Chromosome 2</article-title>
<alt-title alt-title-type="running-head">DnaK and Replication of
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Chr2</alt-title>
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<xref ref-type="aff" rid="aff1">
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<surname>Li</surname>
<given-names>Mi</given-names>
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<xref ref-type="aff" rid="aff2">
<sup>b</sup>
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<given-names>Rodolfo</given-names>
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<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Miller Jenkins</surname>
<given-names>Lisa M.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wlodawer</surname>
<given-names>Alexander</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Chattoraj</surname>
<given-names>Dhruba</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<aff id="aff1">
<label>a</label>
<addr-line>Laboratory of Biochemistry and Molecular Biology, CCR, NCI, NIH, Bethesda, Maryland, USA</addr-line>
</aff>
<aff id="aff2">
<label>b</label>
<addr-line>Macromolecular Crystallography Laboratory, NCI, Frederick, Maryland, USA</addr-line>
</aff>
<aff id="aff3">
<label>c</label>
<addr-line>Basic Science Program, Leidos Biomedical Research, Frederick National Laboratory for Cancer Research, Frederick, Maryland, USA</addr-line>
</aff>
<aff id="aff4">
<label>d</label>
<addr-line>Laboratory of Molecular Biology, NIDDK, NIH, Bethesda, Maryland, USA</addr-line>
</aff>
<aff id="aff5">
<label>e</label>
<addr-line>Laboratory of Cell Biology, CCR, NCI, NIH, Bethesda, Maryland, USA</addr-line>
</aff>
</contrib-group>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Dunny</surname>
<given-names>Gary M.</given-names>
</name>
<role>Editor</role>
<aff>University of Minnesota Medical School</aff>
</contrib>
</contrib-group>
<author-notes>
<corresp id="cor1">Address correspondence to Dhruba Chattoraj,
<email>chattoraj@nih.gov</email>
.</corresp>
<fn fn-type="other">
<p>This article is a direct contribution from a Fellow of the American Academy of Microbiology. External solicited reviewers: Didier Mazel, Institut Pasteur; Rafael Giraldo, CIB-CSIC.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>18</day>
<month>4</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<season>Mar-Apr</season>
<year>2017</year>
</pub-date>
<volume>8</volume>
<issue>2</issue>
<elocation-id>e00427-17</elocation-id>
<history>
<date date-type="received">
<day>16</day>
<month>3</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>20</day>
<month>3</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2017 Jha et al.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Jha et al.</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open-access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="mbo002173276001.pdf"></self-uri>
<abstract>
<title>ABSTRACT</title>
<p>Replication of
<italic>Vibrio cholerae</italic>
chromosome 2 (Chr2) depends on molecular chaperone DnaK to facilitate binding of the initiator (RctB) to the replication origin. The binding occurs at two kinds of site, 12-mers and 39-mers, which promote and inhibit replication, respectively. Here we show that DnaK employs different mechanisms to enhance the two kinds of binding. We found that mutations in
<italic>rctB</italic>
that reduce DnaK binding also reduce 12-mer binding and initiation. The initiation defect is suppressed by second-site mutations that increase 12-mer binding only marginally. Instead, they reduce replication inhibitory mechanisms: RctB dimerization and 39-mer binding. One suppressing change was in a dimerization domain which is folded similarly to the initiator of an iteron plasmid—the presumed progenitor of Chr2. In plasmids, DnaK promotes initiation by reducing dimerization. A different mutation was in the 39-mer binding domain of RctB and inactivated it, indicating an alternative suppression mechanism. Paradoxically, although DnaK increases 39-mer binding, the increase was also achieved by inactivating the DnaK binding site of RctB. This result suggests that the site inhibits the 39-mer binding domain (via autoinhibition) when prevented from binding DnaK. Taken together, our results reveal an important feature of the transition from plasmid to chromosome: the Chr2 initiator retains the plasmid-like dimerization domain and its control by chaperones but uses the chaperones in an unprecedented way to control the inhibitory 39-mer binding.</p>
</abstract>
<abstract abstract-type="executive-summary">
<title>IMPORTANCE</title>
<p>The capacity of proteins to undergo remodeling provides opportunities to control their function. However, remodeling remains a poorly understood aspect of the structure-function paradigm due to its dynamic nature. Here we have studied remodeling of the initiator of replication of
<italic>Vibrio cholerae</italic>
Chr2 by the molecular chaperone, DnaK. We show that DnaK binds to a site on the Chr2 initiator (RctB) that promotes initiation by reducing the initiator’s propensity to dimerize. Dimerization of the initiator of the putative plasmid progenitor of Chr2 is also reduced by DnaK, which promotes initiation. Paradoxically, the DnaK binding also promotes replication inhibition by reducing an autoinhibitory activity of RctB. In the plasmid-to-chromosome transition, it appears that the initiator has acquired an autoinhibitory activity and along with it a new chaperone activity that apparently helps to control replication inhibition independently of replication promotion.</p>
</abstract>
<kwd-group>
<title>KEYWORDS</title>
<kwd>chromosome replication</kwd>
<kwd>DNA-protein interactions</kwd>
<kwd>DnaK chaperone</kwd>
<kwd>initiator remodeling</kwd>
<kwd>initiator structure</kwd>
<kwd>
<italic>Vibrio cholerae</italic>
</kwd>
</kwd-group>
<funding-group>
<award-group id="award1">
<funding-source>Intramural Research Program, CCR, NCI, NIH</funding-source>
<principal-award-recipient>Dhruba Chattoraj</principal-award-recipient>
<principal-award-recipient>Mi Li</principal-award-recipient>
<principal-award-recipient>Lisa M. Miller Jenkins</principal-award-recipient>
<principal-award-recipient>Alexander Wlodawer</principal-award-recipient>
<principal-award-recipient>Jyoti K. Jha</principal-award-recipient>
</award-group>
<award-group id="award2">
<funding-source>Intramural Research Program, NIDDK, NIH</funding-source>
<principal-award-recipient>Rodolfo Ghirlando</principal-award-recipient>
</award-group>
</funding-group>
<counts>
<count count="9" count-type="supplementary-material"></count>
<fig-count count="8"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="64"></ref-count>
<page-count count="20"></page-count>
<word-count count="13184"></word-count>
</counts>
<custom-meta-group>
<custom-meta>
<meta-name>cover-date</meta-name>
<meta-value>March/April 2017</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Maryland</li>
</region>
</list>
<tree>
<country name="États-Unis">
<region name="Maryland">
<name sortKey="Jha, Jyoti K" sort="Jha, Jyoti K" uniqKey="Jha J" first="Jyoti K." last="Jha">Jyoti K. Jha</name>
</region>
<name sortKey="Chattoraj, Dhruba" sort="Chattoraj, Dhruba" uniqKey="Chattoraj D" first="Dhruba" last="Chattoraj">Dhruba Chattoraj</name>
<name sortKey="Ghirlando, Rodolfo" sort="Ghirlando, Rodolfo" uniqKey="Ghirlando R" first="Rodolfo" last="Ghirlando">Rodolfo Ghirlando</name>
<name sortKey="Li, Mi" sort="Li, Mi" uniqKey="Li M" first="Mi" last="Li">Mi Li</name>
<name sortKey="Li, Mi" sort="Li, Mi" uniqKey="Li M" first="Mi" last="Li">Mi Li</name>
<name sortKey="Miller Jenkins, Lisa M" sort="Miller Jenkins, Lisa M" uniqKey="Miller Jenkins L" first="Lisa M." last="Miller Jenkins">Lisa M. Miller Jenkins</name>
<name sortKey="Wlodawer, Alexander" sort="Wlodawer, Alexander" uniqKey="Wlodawer A" first="Alexander" last="Wlodawer">Alexander Wlodawer</name>
</country>
</tree>
</affiliations>
</record>

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