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Porin self-association enables cell-to-cell contact in Providencia stuartii floating communities

Identifieur interne : 000017 ( Hal/Corpus ); précédent : 000016; suivant : 000018

Porin self-association enables cell-to-cell contact in Providencia stuartii floating communities

Auteurs : Mariam El Khatib ; Chady Nasrallah ; Julie Lopes ; Que-Tien Tran ; Guillaume Tetreau ; Hind Basbous ; Daphna Fenel ; Benoit Gallet ; Mathilde Lethier ; Jean-Michel Bolla ; Jean-Marie Pagès ; Michel Vivaudou ; Martin Weik ; Mathias Winterhalter ; Jacques-Philippe Colletier

Source :

RBID : Hal:hal-01894519

English descriptors

Abstract

The gram-negative pathogen Providencia stuartii forms floating communities within which adjacent cells are in apparent contact, before depositing as canonical surface-attached biofilms. Because porins are the most abundant proteins in the outer membrane of gram-negative bacteria, we hypothesized that they could be involved in cell-to-cell contact and undertook a structure-function relationship study on the two porins of P. stuartii, Omp-Pst1 and Omp-Pst2. Our crystal structures reveal that these porins can self-associate through their extracellular loops, forming dimers of tri-mers (DOTs) that could enable cell-to-cell contact within floating communities. Support for this hypothesis was obtained by studying the porin-dependent aggregation of liposomes and model cells. The observation that facing channels are open in the two porin structures suggests that DOTs could not only promote cell-to-cell contact but also contribute to intercellular communication. biofilms | porins | intercellular communication | cell adhesion | steric zippers


Url:
DOI: 10.1073/pnas.1714582115

Links to Exploration step

Hal:hal-01894519

Le document en format XML

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<idno type="DOI">10.1073/pnas.1714582115</idno>
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<title level="j">Proceedings of the National Academy of Sciences of the United States of America </title>
<idno type="ISSN">0027-8424</idno>
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<date type="datePub">2018</date>
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<keywords scheme="mix" xml:lang="en">
<term>biofilms</term>
<term>cell adhesion</term>
<term>intercellular communication</term>
<term>porins</term>
<term>steric zippers</term>
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<p>The gram-negative pathogen Providencia stuartii forms floating communities within which adjacent cells are in apparent contact, before depositing as canonical surface-attached biofilms. Because porins are the most abundant proteins in the outer membrane of gram-negative bacteria, we hypothesized that they could be involved in cell-to-cell contact and undertook a structure-function relationship study on the two porins of P. stuartii, Omp-Pst1 and Omp-Pst2. Our crystal structures reveal that these porins can self-associate through their extracellular loops, forming dimers of tri-mers (DOTs) that could enable cell-to-cell contact within floating communities. Support for this hypothesis was obtained by studying the porin-dependent aggregation of liposomes and model cells. The observation that facing channels are open in the two porin structures suggests that DOTs could not only promote cell-to-cell contact but also contribute to intercellular communication. biofilms | porins | intercellular communication | cell adhesion | steric zippers</p>
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<title xml:lang="en">Porin self-association enables cell-to-cell contact in Providencia stuartii floating communities</title>
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<forename type="first">Mariam</forename>
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<author role="aut">
<persName>
<forename type="first">Martin</forename>
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</author>
<author role="aut">
<persName>
<forename type="first">Jacques-Philippe</forename>
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<forename>emmanuelle</forename>
<surname>rosa</surname>
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<email type="md5">52b1c011c447ef75a2c97ca12ce69932</email>
<email type="domain">univ-amu.fr</email>
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<funder ref="#projanr-38043"></funder>
<funder>We thank E. Kandiah, D. Cascio, M. R. Sawaya, I. Silman, and J. Zaccaï for critically reading the manuscript; C. Breyton and D. Levy for suggesting on-column delipidation of porins and sucrose gradient experiments, respectively; and A. Martel, A. Le Roy, A. Flayhan, A. Laganowsky, A. Davin-Regli, E. Moiseeva, M. Zhao, G. Schoehn, and T. Vernet for stimulating discussions. We are indebted to I. Snigireva for scanning electron micrographs and to J.-P. Kleman and F. Lacroix for technical support and advice during epifluorescence microscopy experiments. This work used the platforms of the Grenoble Instruct Center [Integrated Structural Biology Grenoble: Unité mixte de service 3518 CNRS–CEA–UGA–European Molecular Biology Laboratory (EMBL)], with support from the French Infrastructure for Integrated Structural Biology (Grant ANR-10-INSB-05-02) and the Grenoble Alliance for Integrated Structural Cell Biology (GRAL) (Grant ANR-10-LABX-49-01) within the Grenoble Partnership for Structural Biology. The electron microscopy facility is supported by the Rhône-Alpes Region, the Fondation de la Recherche Medicale, the Fonds Européen de Développement Régional, the CNRS, the CEA, the UGA, the EMBL, and the Groupement d’Intérêt Scientifique-Infrastrutures en Biologie, Santé et Agronomie. We are grateful to the ESRF for beam time under the long-term projects MX722, MX1464, and MX1583 (IBS beamtime allocation group). We acknowledge financial support from the CEA, the CNRS, the UGA, Agence Nationale de la Recherche Grant ANR-15-CE18-0005-02 (to J.-P.C.), GRAL Grant C7H-LXG11A20-COLLETIER (to J.-P.C.), Laboratory of Excellence “Ion Channel Science and Therapeutics” Grant ANR-11-LABX-0015-01 (to M.V.), and Aix-Marseille University and the Service de Santé des Armées (J.-M.P.). M.E.-K. is supported by a joint CEA-GRAL doctoral fellowship (Grant C7H-LXG11A20-DYNAMOP).</funder>
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<date type="whenSubmitted">2018-10-12 15:05:30</date>
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<idno type="stamp" n="UNIV-GRENOBLE1" corresp="UGA">Université Joseph Fourier - Grenoble I</idno>
<idno type="stamp" n="CEA">CEA - Commissariat à l'énergie atomique</idno>
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<idno type="stamp" n="CEA-DRF" corresp="CEA">Direction de Recherche Fondamentale</idno>
<idno type="stamp" n="UNIV-AMU">Aix Marseille Université</idno>
<idno type="stamp" n="UGA">HAL Grenoble Alpes</idno>
<idno type="stamp" n="INSERM">INSERM - Institut national de la santé et de la recherche médicale</idno>
<idno type="stamp" n="IBS" corresp="CEA">Institut de Biologie Structurale</idno>
<idno type="stamp" n="IBS-CAN" corresp="IBS">Groupe Canaux / Channels Group (IBS-CHANNELS)</idno>
<idno type="stamp" n="IBS-DYC" corresp="IBS">Groupe Dynamique et Cinétique des processus moléculaires / Dynamics and Kinetics of Molecular Processes Group (IBS-DYNAMOP)</idno>
<idno type="stamp" n="IRIG" corresp="CEA">Institut de Recherche Interdisciplinaire de Grenoble</idno>
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<idno type="stamp" n="UNIV-TLSE3">Université Paul Sabatier - Toulouse III</idno>
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<title xml:lang="en">Porin self-association enables cell-to-cell contact in Providencia stuartii floating communities</title>
<author role="aut">
<persName>
<forename type="first">Mariam</forename>
<surname>El Khatib</surname>
</persName>
<idno type="halauthorid">1300734</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Chady</forename>
<surname>Nasrallah</surname>
</persName>
<idno type="halauthorid">1175848</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Julie</forename>
<surname>Lopes</surname>
</persName>
<idno type="halauthorid">1558428</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Que-Tien</forename>
<surname>Tran</surname>
</persName>
<idno type="halauthorid">1558427</idno>
<affiliation ref="#struct-264916"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Guillaume</forename>
<surname>Tetreau</surname>
</persName>
<idno type="halauthorid">663638</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Hind</forename>
<surname>Basbous</surname>
</persName>
<idno type="halauthorid">1258065</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Daphna</forename>
<surname>Fenel</surname>
</persName>
<idno type="halauthorid">1163763</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Benoit</forename>
<surname>Gallet</surname>
</persName>
<idno type="halauthorid">232678</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Mathilde</forename>
<surname>Lethier</surname>
</persName>
<idno type="halauthorid">1192198</idno>
<affiliation ref="#struct-325850"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Jean-Michel</forename>
<surname>Bolla</surname>
</persName>
<idno type="halauthorid">202126</idno>
<affiliation ref="#struct-527037"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Jean-Marie</forename>
<surname>Pagès</surname>
</persName>
<idno type="halauthorid">418085</idno>
<affiliation ref="#struct-527037"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Michel</forename>
<surname>Vivaudou</surname>
</persName>
<idno type="halauthorid">402307</idno>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Martin</forename>
<surname>Weik</surname>
</persName>
<idno type="halauthorid">1190680</idno>
<orgName ref="#struct-576"></orgName>
<affiliation ref="#struct-576"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Mathias</forename>
<surname>Winterhalter</surname>
</persName>
<idno type="halauthorid">122117</idno>
<affiliation ref="#struct-583"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Jacques-Philippe</forename>
<surname>Colletier</surname>
</persName>
<idno type="halauthorid">1178434</idno>
<orgName ref="#struct-576"></orgName>
<affiliation ref="#struct-576"></affiliation>
</author>
</analytic>
<monogr>
<idno type="halJournalId" status="VALID">7969</idno>
<idno type="issn">0027-8424</idno>
<idno type="eissn">1091-6490</idno>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America </title>
<imprint>
<publisher>National Academy of Sciences</publisher>
<biblScope unit="volume">115</biblScope>
<biblScope unit="issue">10</biblScope>
<biblScope unit="pp">E2220-E2228</biblScope>
<date type="datePub">2018</date>
<date type="dateEpub">2018-02-23</date>
</imprint>
</monogr>
<idno type="doi">10.1073/pnas.1714582115</idno>
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</sourceDesc>
<profileDesc>
<langUsage>
<language ident="en">English</language>
</langUsage>
<textClass>
<keywords scheme="author">
<term xml:lang="en">porins</term>
<term xml:lang="en">intercellular communication</term>
<term xml:lang="en">biofilms</term>
<term xml:lang="en">cell adhesion</term>
<term xml:lang="en">steric zippers</term>
</keywords>
<classCode scheme="halDomain" n="sdv.bbm.bs">Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biomolecules [q-bio.BM]</classCode>
<classCode scheme="halDomain" n="sdv.mp.bac">Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology</classCode>
<classCode scheme="halTypology" n="ART">Journal articles</classCode>
</textClass>
<abstract xml:lang="en">
<p>The gram-negative pathogen Providencia stuartii forms floating communities within which adjacent cells are in apparent contact, before depositing as canonical surface-attached biofilms. Because porins are the most abundant proteins in the outer membrane of gram-negative bacteria, we hypothesized that they could be involved in cell-to-cell contact and undertook a structure-function relationship study on the two porins of P. stuartii, Omp-Pst1 and Omp-Pst2. Our crystal structures reveal that these porins can self-associate through their extracellular loops, forming dimers of tri-mers (DOTs) that could enable cell-to-cell contact within floating communities. Support for this hypothesis was obtained by studying the porin-dependent aggregation of liposomes and model cells. The observation that facing channels are open in the two porin structures suggests that DOTs could not only promote cell-to-cell contact but also contribute to intercellular communication. biofilms | porins | intercellular communication | cell adhesion | steric zippers</p>
</abstract>
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</hal>
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