Membrane-Wrapping Contributions to Malaria Parasite Invasion of the Human Erythrocyte
Identifieur interne : 003724 ( Main/Exploration ); précédent : 003723; suivant : 003725Membrane-Wrapping Contributions to Malaria Parasite Invasion of the Human Erythrocyte
Auteurs : Sabyasachi Dasgupta [Allemagne] ; Thorsten Auth [Allemagne] ; Nir S. Gov [Israël, France] ; Timothy J. Satchwell [Royaume-Uni] ; Eric Hanssen [Australie] ; Elizabeth S. Zuccala [Australie] ; David T. Riglar [Australie] ; Ashley M. Toye [Royaume-Uni] ; Timo Betz [France] ; Jake Baum [Australie, Royaume-Uni] ; Gerhard Gompper [Allemagne]Source :
- Biophysical Journal [ 0006-3495 ] ; 2014.
Descripteurs français
- KwdFr :
- MESH :
- métabolisme : Cytosquelette, Membrane cellulaire.
- parasitologie : Membrane cellulaire, Érythrocytes.
- pathogénicité : Plasmodium falciparum.
- physiologie : Mérozoïtes.
- Humains, Interactions hôte-parasite.
English descriptors
- KwdEn :
- MESH :
- metabolism : Cell Membrane, Cytoskeleton.
- parasitology : Cell Membrane, Erythrocytes.
- pathogenicity : Plasmodium falciparum.
- physiology : Merozoites.
- Host-Parasite Interactions, Humans.
Abstract
The blood stage malaria parasite, the merozoite, has a small window of opportunity during which it must successfully target and invade a human erythrocyte. The process of invasion is nonetheless remarkably rapid. To date, mechanistic models of invasion have focused predominantly on the parasite actomyosin motor contribution to the energetics of entry. Here, we have conducted a numerical analysis using dimensions for an archetypal merozoite to predict the respective contributions of the host-parasite interactions to invasion, in particular the role of membrane wrapping. Our theoretical modeling demonstrates that erythrocyte membrane wrapping alone, as a function of merozoite adhesive and shape properties, is sufficient to entirely account for the first key step of the invasion process, that of merozoite reorientation to its apex and tight adhesive linkage between the two cells. Next, parasite-induced reorganization of the erythrocyte cytoskeleton and release of parasite-derived membrane can also account for a considerable energetic portion of actual invasion itself, through membrane wrapping. Thus, contrary to the prevailing dogma, wrapping by the erythrocyte combined with parasite-derived membrane release can markedly reduce the expected contributions of the merozoite actomyosin motor to invasion. We therefore propose that invasion is a balance between parasite and host cell contributions, evolved toward maximal efficient use of biophysical forces between the two cells.
Url:
DOI: 10.1016/j.bpj.2014.05.024
PubMed: 24988340
PubMed Central: 4184798
Affiliations:
- Allemagne, Australie, France, Israël, Royaume-Uni
- Angleterre, District de Cologne, Grand Londres, Rhénanie-du-Nord-Westphalie, Victoria (État), Île-de-France
- Juliers, Londres, Melbourne, Paris
- Université de Melbourne
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Le document en format XML
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type="city">Juliers</settlement></placeName></affiliation></author><author><name sortKey="Auth, Thorsten" sort="Auth, Thorsten" uniqKey="Auth T" first="Thorsten" last="Auth">Thorsten Auth</name><affiliation wicri:level="3"><nlm:aff id="aff1">Institute of Complex Systems and Institute for Advanced Simulation, Forschungszentrum Jülich, Jülich, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Complex Systems and Institute for Advanced Simulation, Forschungszentrum Jülich, Jülich</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">Juliers</settlement></placeName></affiliation></author><author><name sortKey="Gov, Nir S" sort="Gov, Nir S" uniqKey="Gov N" first="Nir S." last="Gov">Nir S. Gov</name><affiliation wicri:level="1"><nlm:aff id="aff2">Department of Chemical Physics, Weizmann Institute of Science, Rehovot, Israel</nlm:aff><country xml:lang="fr">Israël</country><wicri:regionArea>Department of Chemical Physics, Weizmann Institute of Science, Rehovot</wicri:regionArea><wicri:noRegion>Rehovot</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:aff id="aff3">Centre de Recherche, Institut Curie, Paris, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre de Recherche, Institut Curie, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Satchwell, Timothy J" sort="Satchwell, Timothy J" uniqKey="Satchwell T" first="Timothy J." last="Satchwell">Timothy J. Satchwell</name><affiliation wicri:level="1"><nlm:aff id="aff4">School of Biochemistry, University of Bristol, Bristol, United Kingdom</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Biochemistry, University of Bristol, Bristol</wicri:regionArea><wicri:noRegion>Bristol</wicri:noRegion></affiliation></author><author><name sortKey="Hanssen, Eric" sort="Hanssen, Eric" uniqKey="Hanssen E" first="Eric" last="Hanssen">Eric Hanssen</name><affiliation wicri:level="4"><nlm:aff id="aff5">Advanced Microscopy Facility, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Advanced Microscopy Facility, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria</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="Zuccala, Elizabeth S" sort="Zuccala, Elizabeth S" uniqKey="Zuccala E" first="Elizabeth S." last="Zuccala">Elizabeth S. Zuccala</name><affiliation wicri:level="1"><nlm:aff id="aff6">Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff7">Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Parkville, Victoria</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="Riglar, David T" sort="Riglar, David T" uniqKey="Riglar D" first="David T." last="Riglar">David T. Riglar</name><affiliation wicri:level="1"><nlm:aff id="aff6">Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff7">Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Parkville, Victoria</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="Toye, Ashley M" sort="Toye, Ashley M" uniqKey="Toye A" first="Ashley M." last="Toye">Ashley M. Toye</name><affiliation wicri:level="1"><nlm:aff id="aff4">School of Biochemistry, University of Bristol, Bristol, United Kingdom</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Biochemistry, University of Bristol, Bristol</wicri:regionArea><wicri:noRegion>Bristol</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff8">Bristol Institute for Transfusion Sciences, NHS Blood and Transplant, Bristol, United Kingdom</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Bristol Institute for Transfusion Sciences, NHS Blood and Transplant, Bristol</wicri:regionArea><wicri:noRegion>Bristol</wicri:noRegion></affiliation></author><author><name sortKey="Betz, Timo" sort="Betz, Timo" uniqKey="Betz T" first="Timo" last="Betz">Timo Betz</name><affiliation wicri:level="3"><nlm:aff id="aff3">Centre de Recherche, Institut Curie, Paris, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre de Recherche, Institut Curie, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></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="aff6">Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff7">Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Parkville, Victoria</wicri:regionArea><orgName type="university">Université de Melbourne</orgName><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff9">Department of Life Sciences, Imperial College London, South Kensington, London, United Kingdom</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Life Sciences, Imperial College London, South Kensington, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Gompper, Gerhard" sort="Gompper, Gerhard" uniqKey="Gompper G" first="Gerhard" last="Gompper">Gerhard Gompper</name><affiliation wicri:level="3"><nlm:aff id="aff1">Institute of Complex Systems and Institute for Advanced Simulation, Forschungszentrum Jülich, Jülich, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Complex Systems and Institute for Advanced Simulation, Forschungszentrum Jülich, Jülich</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">Juliers</settlement></placeName></affiliation></author></analytic><series><title level="j">Biophysical Journal</title><idno type="ISSN">0006-3495</idno><idno type="eISSN">1542-0086</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cell Membrane (metabolism)</term><term>Cell Membrane (parasitology)</term><term>Cytoskeleton (metabolism)</term><term>Erythrocytes (parasitology)</term><term>Host-Parasite Interactions</term><term>Humans</term><term>Merozoites (physiology)</term><term>Plasmodium falciparum (pathogenicity)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Cytosquelette (métabolisme)</term><term>Humains</term><term>Interactions hôte-parasite</term><term>Membrane cellulaire (métabolisme)</term><term>Membrane cellulaire (parasitologie)</term><term>Mérozoïtes (physiologie)</term><term>Plasmodium falciparum (pathogénicité)</term><term>Érythrocytes (parasitologie)</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Membrane</term><term>Cytoskeleton</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Cytosquelette</term><term>Membrane cellulaire</term></keywords><keywords scheme="MESH" qualifier="parasitologie" xml:lang="fr"><term>Membrane cellulaire</term><term>Érythrocytes</term></keywords><keywords scheme="MESH" qualifier="parasitology" xml:lang="en"><term>Cell Membrane</term><term>Erythrocytes</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Plasmodium falciparum</term></keywords><keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Plasmodium falciparum</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Mérozoïtes</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Merozoites</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Host-Parasite Interactions</term><term>Humans</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Humains</term><term>Interactions hôte-parasite</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The blood stage malaria parasite, the merozoite, has a small window of opportunity during which it must successfully target and invade a human erythrocyte. The process of invasion is nonetheless remarkably rapid. To date, mechanistic models of invasion have focused predominantly on the parasite actomyosin motor contribution to the energetics of entry. Here, we have conducted a numerical analysis using dimensions for an archetypal merozoite to predict the respective contributions of the host-parasite interactions to invasion, in particular the role of membrane wrapping. Our theoretical modeling demonstrates that erythrocyte membrane wrapping alone, as a function of merozoite adhesive and shape properties, is sufficient to entirely account for the first key step of the invasion process, that of merozoite reorientation to its apex and tight adhesive linkage between the two cells. Next, parasite-induced reorganization of the erythrocyte cytoskeleton and release of parasite-derived membrane can also account for a considerable energetic portion of actual invasion itself, through membrane wrapping. Thus, contrary to the prevailing dogma, wrapping by the erythrocyte combined with parasite-derived membrane release can markedly reduce the expected contributions of the merozoite actomyosin motor to invasion. We therefore propose that invasion is a balance between parasite and host cell contributions, evolved toward maximal efficient use of biophysical forces between the two cells.</p></div></front></TEI><affiliations><list><country><li>Allemagne</li><li>Australie</li><li>France</li><li>Israël</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>District de Cologne</li><li>Grand Londres</li><li>Rhénanie-du-Nord-Westphalie</li><li>Victoria (État)</li><li>Île-de-France</li></region><settlement><li>Juliers</li><li>Londres</li><li>Melbourne</li><li>Paris</li></settlement><orgName><li>Université de Melbourne</li></orgName></list><tree><country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Dasgupta, Sabyasachi" sort="Dasgupta, Sabyasachi" uniqKey="Dasgupta S" first="Sabyasachi" last="Dasgupta">Sabyasachi Dasgupta</name></region><name sortKey="Auth, Thorsten" sort="Auth, Thorsten" uniqKey="Auth T" first="Thorsten" last="Auth">Thorsten Auth</name><name sortKey="Gompper, Gerhard" sort="Gompper, Gerhard" uniqKey="Gompper G" first="Gerhard" last="Gompper">Gerhard Gompper</name></country><country name="Israël"><noRegion><name sortKey="Gov, Nir S" sort="Gov, Nir S" uniqKey="Gov N" first="Nir S." last="Gov">Nir S. Gov</name></noRegion></country><country name="France"><region name="Île-de-France"><name sortKey="Gov, Nir S" sort="Gov, Nir S" uniqKey="Gov N" first="Nir S." last="Gov">Nir S. Gov</name></region><name sortKey="Betz, Timo" sort="Betz, Timo" uniqKey="Betz T" first="Timo" last="Betz">Timo Betz</name></country><country name="Royaume-Uni"><noRegion><name sortKey="Satchwell, Timothy J" sort="Satchwell, Timothy J" uniqKey="Satchwell T" first="Timothy J." last="Satchwell">Timothy J. Satchwell</name></noRegion><name sortKey="Baum, Jake" sort="Baum, Jake" uniqKey="Baum J" first="Jake" last="Baum">Jake Baum</name><name sortKey="Toye, Ashley M" sort="Toye, Ashley M" uniqKey="Toye A" first="Ashley M." last="Toye">Ashley M. Toye</name><name sortKey="Toye, Ashley M" sort="Toye, Ashley M" uniqKey="Toye A" first="Ashley M." last="Toye">Ashley M. Toye</name></country><country name="Australie"><region name="Victoria (État)"><name sortKey="Hanssen, Eric" sort="Hanssen, Eric" uniqKey="Hanssen E" first="Eric" last="Hanssen">Eric Hanssen</name></region><name sortKey="Baum, Jake" sort="Baum, Jake" uniqKey="Baum J" first="Jake" last="Baum">Jake Baum</name><name sortKey="Baum, Jake" sort="Baum, Jake" uniqKey="Baum J" first="Jake" last="Baum">Jake Baum</name><name sortKey="Riglar, David T" sort="Riglar, David T" uniqKey="Riglar D" first="David T." last="Riglar">David T. Riglar</name><name sortKey="Riglar, David T" sort="Riglar, David T" uniqKey="Riglar D" first="David T." last="Riglar">David T. Riglar</name><name sortKey="Zuccala, Elizabeth S" sort="Zuccala, Elizabeth S" uniqKey="Zuccala E" first="Elizabeth S." last="Zuccala">Elizabeth S. Zuccala</name><name sortKey="Zuccala, Elizabeth S" sort="Zuccala, Elizabeth S" uniqKey="Zuccala E" first="Elizabeth S." last="Zuccala">Elizabeth S. Zuccala</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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