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Plasmodium Merozoite TRAP Family Protein Is Essential for Vacuole Membrane Disruption and Gamete Egress from Erythrocytes

Identifieur interne : 002505 ( Main/Curation ); précédent : 002504; suivant : 002506

Plasmodium Merozoite TRAP Family Protein Is Essential for Vacuole Membrane Disruption and Gamete Egress from Erythrocytes

Auteurs : Daniel Y. Bargieri [France, Brésil] ; Sabine Thiberge [France] ; Chwen L. Tay [Royaume-Uni] ; Alison F. Carey [France, États-Unis] ; Alice Rantz [France] ; Florian Hischen [Allemagne] ; Audrey Lorthiois [France] ; Ursula Straschil [Royaume-Uni] ; Pallavi Singh [France] ; Shailja Singh [France] ; Tony Triglia [Australie] ; Takafumi Tsuboi [Japon] ; Alan Cowman [Australie] ; Chetan Chitnis [France] ; Pietro Alano [Italie] ; Jake Baum [Royaume-Uni] ; Gabriele Pradel [Allemagne] ; Catherine Lavazec [France] ; Robert Ménard [France]

Source :

RBID : PMC:5104695

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English descriptors

Abstract

Summary

Surface-associated TRAP (thrombospondin-related anonymous protein) family proteins are conserved across the phylum of apicomplexan parasites. TRAP proteins are thought to play an integral role in parasite motility and cell invasion by linking the extracellular environment with the parasite submembrane actomyosin motor. Blood stage forms of the malaria parasite Plasmodium express a TRAP family protein called merozoite-TRAP (MTRAP) that has been implicated in erythrocyte invasion. Using MTRAP-deficient mutants of the rodent-infecting P. berghei and human-infecting P. falciparum parasites, we show that MTRAP is dispensable for erythrocyte invasion. Instead, MTRAP is essential for gamete egress from erythrocytes, where it is necessary for the disruption of the gamete-containing parasitophorous vacuole membrane, and thus for parasite transmission to mosquitoes. This indicates that motor-binding TRAP family members function not just in parasite motility and cell invasion but also in membrane disruption and cell egress.


Url:
DOI: 10.1016/j.chom.2016.10.015
PubMed: 27832590
PubMed Central: 5104695

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PMC:5104695

Le document en format XML

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Merozoite TRAP Family Protein Is Essential for Vacuole Membrane Disruption and Gamete Egress from Erythrocytes</title>
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<name sortKey="Singh, Pallavi" sort="Singh, Pallavi" uniqKey="Singh P" first="Pallavi" last="Singh">Pallavi Singh</name>
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<name sortKey="Cowman, Alan" sort="Cowman, Alan" uniqKey="Cowman A" first="Alan" last="Cowman">Alan Cowman</name>
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<name sortKey="Menard, Robert" sort="Menard, Robert" uniqKey="Menard R" first="Robert" last="Ménard">Robert Ménard</name>
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Merozoite TRAP Family Protein Is Essential for Vacuole Membrane Disruption and Gamete Egress from Erythrocytes</title>
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<name sortKey="Hischen, Florian" sort="Hischen, Florian" uniqKey="Hischen F" first="Florian" last="Hischen">Florian Hischen</name>
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<name sortKey="Lorthiois, Audrey" sort="Lorthiois, Audrey" uniqKey="Lorthiois A" first="Audrey" last="Lorthiois">Audrey Lorthiois</name>
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<name sortKey="Straschil, Ursula" sort="Straschil, Ursula" uniqKey="Straschil U" first="Ursula" last="Straschil">Ursula Straschil</name>
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<nlm:aff id="aff3">Department of Life Sciences, Imperial College London, South Kensington, London SW7 2AZ, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Life Sciences, Imperial College London, South Kensington, London SW7 2AZ</wicri:regionArea>
<wicri:noRegion>London SW7 2AZ</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Singh, Pallavi" sort="Singh, Pallavi" uniqKey="Singh P" first="Pallavi" last="Singh">Pallavi Singh</name>
<affiliation wicri:level="1">
<nlm:aff id="aff7">Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015</wicri:regionArea>
<wicri:noRegion>75015</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Singh, Shailja" sort="Singh, Shailja" uniqKey="Singh S" first="Shailja" last="Singh">Shailja Singh</name>
<affiliation wicri:level="1">
<nlm:aff id="aff7">Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015</wicri:regionArea>
<wicri:noRegion>75015</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Triglia, Tony" sort="Triglia, Tony" uniqKey="Triglia T" first="Tony" last="Triglia">Tony Triglia</name>
<affiliation wicri:level="1">
<nlm:aff id="aff8">The Walter and Eliza Hall Institute of Medical Research, Parkville 3052, VIC, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>The Walter and Eliza Hall Institute of Medical Research, Parkville 3052, VIC</wicri:regionArea>
<wicri:noRegion>VIC</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Tsuboi, Takafumi" sort="Tsuboi, Takafumi" uniqKey="Tsuboi T" first="Takafumi" last="Tsuboi">Takafumi Tsuboi</name>
<affiliation wicri:level="1">
<nlm:aff id="aff10">Division of Malaria Research, Proteo-Science Center, Ehime University, Matsuyama, Ehime 790-8577, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Division of Malaria Research, Proteo-Science Center, Ehime University, Matsuyama, Ehime 790-8577</wicri:regionArea>
<wicri:noRegion>Ehime 790-8577</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Cowman, Alan" sort="Cowman, Alan" uniqKey="Cowman A" first="Alan" last="Cowman">Alan Cowman</name>
<affiliation wicri:level="1">
<nlm:aff id="aff8">The Walter and Eliza Hall Institute of Medical Research, Parkville 3052, VIC, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>The Walter and Eliza Hall Institute of Medical Research, Parkville 3052, VIC</wicri:regionArea>
<wicri:noRegion>VIC</wicri:noRegion>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="aff9">Department of Medical Biology, University of Melbourne, Parkville 3052, VIC, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Department of Medical Biology, University of Melbourne, Parkville 3052, VIC</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Chitnis, Chetan" sort="Chitnis, Chetan" uniqKey="Chitnis C" first="Chetan" last="Chitnis">Chetan Chitnis</name>
<affiliation wicri:level="1">
<nlm:aff id="aff7">Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Malaria Parasite Biology and Vaccines Unit, Pasteur Institute, Paris 75015</wicri:regionArea>
<wicri:noRegion>75015</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Alano, Pietro" sort="Alano, Pietro" uniqKey="Alano P" first="Pietro" last="Alano">Pietro Alano</name>
<affiliation wicri:level="1">
<nlm:aff id="aff11">Dipartimento di Malattie Infettive, Parassitarie ed Immunomediate, Istituto Superiore di Sanità, Rome 00161, Italy</nlm:aff>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Dipartimento di Malattie Infettive, Parassitarie ed Immunomediate, Istituto Superiore di Sanità, Rome 00161</wicri:regionArea>
<placeName>
<settlement type="city">Rome</settlement>
<region nuts="2">Latium</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Baum, Jake" sort="Baum, Jake" uniqKey="Baum J" first="Jake" last="Baum">Jake Baum</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">Department of Life Sciences, Imperial College London, South Kensington, London SW7 2AZ, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Life Sciences, Imperial College London, South Kensington, London SW7 2AZ</wicri:regionArea>
<wicri:noRegion>London SW7 2AZ</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Pradel, Gabriele" sort="Pradel, Gabriele" uniqKey="Pradel G" first="Gabriele" last="Pradel">Gabriele Pradel</name>
<affiliation wicri:level="3">
<nlm:aff id="aff5">Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, Aachen 52074, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, Aachen 52074</wicri:regionArea>
<placeName>
<region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
<region type="district" nuts="2">District de Cologne</region>
<settlement type="city">Aix-la-Chapelle</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Lavazec, Catherine" sort="Lavazec, Catherine" uniqKey="Lavazec C" first="Catherine" last="Lavazec">Catherine Lavazec</name>
<affiliation wicri:level="4">
<nlm:aff id="aff6">Inserm U1016, CNRS UMR 8104, Université Paris Descartes, Institut Cochin, Paris 75014, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Inserm U1016, CNRS UMR 8104, Université Paris Descartes, Institut Cochin, Paris 75014</wicri:regionArea>
<wicri:noRegion>75014</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
<orgName type="university">Université Paris-Descartes</orgName>
</affiliation>
</author>
<author>
<name sortKey="Menard, Robert" sort="Menard, Robert" uniqKey="Menard R" first="Robert" last="Ménard">Robert Ménard</name>
<affiliation wicri:level="1">
<nlm:aff id="aff1">Malaria Biology and Genetics Unit, Pasteur Institute, Paris 75015, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Malaria Biology and Genetics Unit, Pasteur Institute, Paris 75015</wicri:regionArea>
<wicri:noRegion>75015</wicri:noRegion>
<placeName>
<settlement type="city">Paris</settlement>
<region type="région" nuts="2">Île-de-France</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Cell Host & Microbe</title>
<idno type="ISSN">1931-3128</idno>
<idno type="eISSN">1934-6069</idno>
<imprint>
<date when="2016">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Animals</term>
<term>Culicidae</term>
<term>Erythrocytes (parasitology)</term>
<term>Exocytosis</term>
<term>Humans</term>
<term>Membranes (metabolism)</term>
<term>Merozoites (physiology)</term>
<term>Mice</term>
<term>Plasmodium berghei (physiology)</term>
<term>Plasmodium falciparum (physiology)</term>
<term>Protozoan Proteins (metabolism)</term>
<term>Vacuoles (parasitology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux</term>
<term>Culicidae</term>
<term>Exocytose</term>
<term>Humains</term>
<term>Membranes (métabolisme)</term>
<term>Mérozoïtes (physiologie)</term>
<term>Plasmodium berghei (physiologie)</term>
<term>Plasmodium falciparum (physiologie)</term>
<term>Protéines de protozoaire (métabolisme)</term>
<term>Souris</term>
<term>Vacuoles (parasitologie)</term>
<term>Érythrocytes (parasitologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Protozoan Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Membranes</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Membranes</term>
<term>Protéines de protozoaire</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitologie" xml:lang="fr">
<term>Vacuoles</term>
<term>Érythrocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitology" xml:lang="en">
<term>Erythrocytes</term>
<term>Vacuoles</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Mérozoïtes</term>
<term>Plasmodium berghei</term>
<term>Plasmodium falciparum</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Merozoites</term>
<term>Plasmodium berghei</term>
<term>Plasmodium falciparum</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Culicidae</term>
<term>Exocytosis</term>
<term>Humans</term>
<term>Mice</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Culicidae</term>
<term>Exocytose</term>
<term>Humains</term>
<term>Souris</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<title>Summary</title>
<p>Surface-associated TRAP (thrombospondin-related anonymous protein) family proteins are conserved across the phylum of apicomplexan parasites. TRAP proteins are thought to play an integral role in parasite motility and cell invasion by linking the extracellular environment with the parasite submembrane actomyosin motor. Blood stage forms of the malaria parasite
<italic>Plasmodium</italic>
express a TRAP family protein called merozoite-TRAP (MTRAP) that has been implicated in erythrocyte invasion. Using MTRAP-deficient mutants of the rodent-infecting
<italic>P. berghei</italic>
and human-infecting
<italic>P. falciparum</italic>
parasites, we show that MTRAP is dispensable for erythrocyte invasion. Instead, MTRAP is essential for gamete egress from erythrocytes, where it is necessary for the disruption of the gamete-containing parasitophorous vacuole membrane, and thus for parasite transmission to mosquitoes. This indicates that motor-binding TRAP family members function not just in parasite motility and cell invasion but also in membrane disruption and cell egress.</p>
</div>
</front>
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