Plasmodium vivax Reticulocyte Binding Proteins Are Key Targets of Naturally Acquired Immunity in Young Papua New Guinean Children
Identifieur interne : 000B88 ( Pmc/Checkpoint ); précédent : 000B87; suivant : 000B89Plasmodium vivax Reticulocyte Binding Proteins Are Key Targets of Naturally Acquired Immunity in Young Papua New Guinean Children
Auteurs : Camila T. França [Australie] ; Wen-Qiang He [Australie] ; Jakub Gruszczyk [Australie] ; Nicholas T. Y. Lim [Australie] ; Enmoore Lin [Papouasie-Nouvelle-Guinée] ; Benson Kiniboro [Papouasie-Nouvelle-Guinée] ; Peter M. Siba [Papouasie-Nouvelle-Guinée] ; Wai-Hong Tham [Australie] ; Ivo Mueller [Australie, France, Espagne]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2016.
Abstract
Major gaps in our understanding of
We assessed the binding specificity of five members of the PvRBP family (PvRBP1a, PvRBP1b, PvRBP2a, PvRBP2b, PvRBP2-P2 and a non-binding fragment of PvRBP2c) to normocytes or reticulocytes. PvRBP2b was identified as the only reticulocyte-specific binder (P<0.001), whereas the others preferentially bound to normocytes (PvRBP1a/b P≤0.034), or showed comparable binding to both (PvRBP2a/2-P2, P = 0.38). Furthermore, we measured levels of total and IgG subclasses 1, 2, 3 and 4 to the six PvRBPs in a cohort of young Papua New Guinean children, and assessed their relationship with prospective risk of
These results demonstrate a diversity of erythrocyte-binding phenotypes of PvRBPs, indicating binding to both reticulocyte-specific and normocyte-specific ligands. Our findings provide further insights into the naturally acquired immunity to
Url:
DOI: 10.1371/journal.pntd.0005014
PubMed: 27677183
PubMed Central: 5038947
Affiliations:
- Australie, Espagne, France, Papouasie-Nouvelle-Guinée
- Catalogne, Victoria (État), Île-de-France
- Barcelone, Melbourne, Paris
- Université de Melbourne
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França</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation></author><author><name sortKey="He, Wen Qiang" sort="He, Wen Qiang" uniqKey="He W" first="Wen-Qiang" last="He">Wen-Qiang He</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Gruszczyk, Jakub" sort="Gruszczyk, Jakub" uniqKey="Gruszczyk J" first="Jakub" last="Gruszczyk">Jakub Gruszczyk</name><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Lim, Nicholas T Y" sort="Lim, Nicholas T Y" uniqKey="Lim N" first="Nicholas T. 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Siba</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang, Papua New Guinea</addr-line></nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang</wicri:regionArea><wicri:noRegion>Madang</wicri:noRegion></affiliation></author><author><name sortKey="Tham, Wai Hong" sort="Tham, Wai Hong" uniqKey="Tham W" first="Wai-Hong" last="Tham">Wai-Hong Tham</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Malaria Parasites and Hosts Unit, Department of Parasites and Insect Vectors, Pasteur Institute, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Malaria Parasites and Hosts Unit, Department of Parasites and Insect Vectors, Pasteur Institute, 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><affiliation wicri:level="3"><nlm:aff id="aff006"><addr-line>Barcelona Institute of Global Health (ISGLOBAL), Barcelona, Spain</addr-line></nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona Institute of Global Health (ISGLOBAL), Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27677183</idno><idno type="pmc">5038947</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5038947</idno><idno type="RBID">PMC:5038947</idno><idno type="doi">10.1371/journal.pntd.0005014</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">002914</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002914</idno><idno type="wicri:Area/Pmc/Curation">002764</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002764</idno><idno type="wicri:Area/Pmc/Checkpoint">000B88</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000B88</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>Plasmodium vivax</italic> Reticulocyte Binding Proteins Are Key Targets of Naturally Acquired Immunity in Young Papua New Guinean Children</title><author><name sortKey="Franca, Camila T" sort="Franca, Camila T" uniqKey="Franca C" first="Camila T." last="França">Camila T. França</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation></author><author><name sortKey="He, Wen Qiang" sort="He, Wen Qiang" uniqKey="He W" first="Wen-Qiang" last="He">Wen-Qiang He</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Gruszczyk, Jakub" sort="Gruszczyk, Jakub" uniqKey="Gruszczyk J" first="Jakub" last="Gruszczyk">Jakub Gruszczyk</name><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Lim, Nicholas T Y" sort="Lim, Nicholas T Y" uniqKey="Lim N" first="Nicholas T. Y." last="Lim">Nicholas T. Y. Lim</name><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Lin, Enmoore" sort="Lin, Enmoore" uniqKey="Lin E" first="Enmoore" last="Lin">Enmoore Lin</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang, Papua New Guinea</addr-line></nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang</wicri:regionArea><wicri:noRegion>Madang</wicri:noRegion></affiliation></author><author><name sortKey="Kiniboro, Benson" sort="Kiniboro, Benson" uniqKey="Kiniboro B" first="Benson" last="Kiniboro">Benson Kiniboro</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang, Papua New Guinea</addr-line></nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang</wicri:regionArea><wicri:noRegion>Madang</wicri:noRegion></affiliation></author><author><name sortKey="Siba, Peter M" sort="Siba, Peter M" uniqKey="Siba P" first="Peter M." last="Siba">Peter M. Siba</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang, Papua New Guinea</addr-line></nlm:aff><country xml:lang="fr">Papouasie-Nouvelle-Guinée</country><wicri:regionArea>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang</wicri:regionArea><wicri:noRegion>Madang</wicri:noRegion></affiliation></author><author><name sortKey="Tham, Wai Hong" sort="Tham, Wai Hong" uniqKey="Tham W" first="Wai-Hong" last="Tham">Wai-Hong Tham</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Medical Biology, University of Melbourne, Melbourne</wicri:regionArea><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region><settlement type="city">Melbourne</settlement></placeName><orgName type="university">Université de Melbourne</orgName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Malaria Parasites and Hosts Unit, Department of Parasites and Insect Vectors, Pasteur Institute, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Malaria Parasites and Hosts Unit, Department of Parasites and Insect Vectors, Pasteur Institute, 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><affiliation wicri:level="3"><nlm:aff id="aff006"><addr-line>Barcelona Institute of Global Health (ISGLOBAL), Barcelona, Spain</addr-line></nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona Institute of Global Health (ISGLOBAL), Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Background</title><p>Major gaps in our understanding of <italic>Plasmodium vivax</italic> biology and the acquisition of immunity to this parasite hinder vaccine development. <italic>P</italic>. <italic>vivax</italic> merozoites exclusively invade reticulocytes, making parasite proteins that mediate reticulocyte binding and/or invasion potential key vaccine or drug targets. While protein interactions that mediate invasion are still poorly understood, the <italic>P</italic>. <italic>vivax</italic> Reticulocyte-Binding Protein family (PvRBP) is thought to be involved in <italic>P</italic>. <italic>vivax</italic> restricted host-cell selectivity.</p></sec><sec id="sec002"><title>Methodology/Principal findings</title><p>We assessed the binding specificity of five members of the PvRBP family (PvRBP1a, PvRBP1b, PvRBP2a, PvRBP2b, PvRBP2-P2 and a non-binding fragment of PvRBP2c) to normocytes or reticulocytes. PvRBP2b was identified as the only reticulocyte-specific binder (P<0.001), whereas the others preferentially bound to normocytes (PvRBP1a/b P≤0.034), or showed comparable binding to both (PvRBP2a/2-P2, P = 0.38). Furthermore, we measured levels of total and IgG subclasses 1, 2, 3 and 4 to the six PvRBPs in a cohort of young Papua New Guinean children, and assessed their relationship with prospective risk of <italic>P</italic>. <italic>vivax</italic> malaria. Children had substantial, highly correlated (rho = 0.49–0.82, P<0.001) antibody levels to all six PvRBPs, with dominant IgG1 and IgG3 subclasses. Both total IgG (Incidence Rate Ratio [IRR] 0.63–0.73, P = 0.008–0.041) and IgG1 (IRR 0.56–0.69, P = 0.001–0.035) to PvRBP2b and PvRBP1a were strongly associated with reduced risk of vivax-malaria, independently of age and exposure.</p></sec><sec id="sec003"><title>Conclusion/Significance</title><p>These results demonstrate a diversity of erythrocyte-binding phenotypes of PvRBPs, indicating binding to both reticulocyte-specific and normocyte-specific ligands. Our findings provide further insights into the naturally acquired immunity to <italic>P</italic>. <italic>vivax</italic> and highlight the importance of PvRBP proteins as targets of naturally acquired humoral immunity. In-depth studies of the role of PvRBPs in <italic>P</italic>. <italic>vivax</italic> invasion and functional validation of the role of anti-PvRBP antibodies in clinical immunity against <italic>P</italic>. <italic>vivax</italic> are now required to confirm the potential of the reticulocyte-binding PvRBP2b and PvRBP1a as vaccine candidate antigens.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Mueller, I" uniqKey="Mueller I">I Mueller</name></author><author><name sortKey="Galinski, Mr" uniqKey="Galinski M">MR Galinski</name></author><author><name sortKey="Baird, Jk" uniqKey="Baird J">JK Baird</name></author><author><name sortKey="Carlton, Jm" uniqKey="Carlton J">JM Carlton</name></author><author><name sortKey="Kochar, Dk" uniqKey="Kochar D">DK Kochar</name></author><author><name sortKey="Alonso, Pl" uniqKey="Alonso P">PL Alonso</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cowman, Af" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosntds</journal-id><journal-title-group><journal-title>PLoS Neglected Tropical Diseases</journal-title></journal-title-group><issn pub-type="ppub">1935-2727</issn><issn pub-type="epub">1935-2735</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27677183</article-id><article-id pub-id-type="pmc">5038947</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0005014</article-id><article-id pub-id-type="publisher-id">PNTD-D-16-00772</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Parasitology</subject><subj-group><subject>Parasite Groups</subject><subj-group><subject>Apicomplexa</subject><subj-group><subject>Plasmodium</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Immune System Proteins</subject><subj-group><subject>Antibodies</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Types</subject><subj-group><subject>Animal Cells</subject><subj-group><subject>Bone Marrow Cells</subject><subj-group><subject>Reticulocytes</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Types</subject><subj-group><subject>Animal Cells</subject><subj-group><subject>Blood Cells</subject><subj-group><subject>Red Blood Cells</subject><subj-group><subject>Reticulocytes</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Immunologic Techniques</subject><subj-group><subject>Immunoassays</subject><subj-group><subject>Enzyme-Linked Immunoassays</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Parasitic Diseases</subject><subj-group><subject>Malaria</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Tropical Diseases</subject><subj-group><subject>Malaria</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject><subj-group><subject>Population Groupings</subject><subj-group><subject>Age Groups</subject><subj-group><subject>Children</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject><subj-group><subject>Population Groupings</subject><subj-group><subject>Families</subject><subj-group><subject>Children</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immunity</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immunity</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and places</subject><subj-group><subject>Geographical locations</subject><subj-group><subject>Oceania</subject><subj-group><subject>Papua New Guinea</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title><italic>Plasmodium vivax</italic> Reticulocyte Binding Proteins Are Key Targets of Naturally Acquired Immunity in Young Papua New Guinean Children</article-title><alt-title alt-title-type="running-head">IgG Responses to PvRBPs and Protection against <italic>P</italic>. <italic>vivax</italic> Malaria</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>França</surname><given-names>Camila T.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>He</surname><given-names>Wen-Qiang</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gruszczyk</surname><given-names>Jakub</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lim</surname><given-names>Nicholas T. Y.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Enmoore</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kiniboro</surname><given-names>Benson</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Siba</surname><given-names>Peter M.</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tham</surname><given-names>Wai-Hong</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="author-notes" rid="econtrib001"><sup>‡</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff005"><sup>5</sup></xref><xref ref-type="aff" rid="aff006"><sup>6</sup></xref><xref ref-type="author-notes" rid="econtrib001"><sup>‡</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Medical Biology, University of Melbourne, Melbourne, Australia</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Infection and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Malaria Immuno-Epidemiology Unit, PNG Institute of Medical Research, Madang, Papua New Guinea</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Malaria Parasites and Hosts Unit, Department of Parasites and Insect Vectors, Pasteur Institute, Paris, France</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Barcelona Institute of Global Health (ISGLOBAL), Barcelona, Spain</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Schallig</surname><given-names>Henk D. F. H.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Academic Medical Centre, NETHERLANDS</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceived and designed the experiments:</bold> IM WHT.</p></list-item><list-item><p><bold>Performed the experiments:</bold> CTF WQH JG NTYL.</p></list-item><list-item><p><bold>Analyzed the data:</bold> CTF WQH WHT IM.</p></list-item><list-item><p><bold>Contributed reagents/materials/analysis tools:</bold> EL BK PMS.</p></list-item><list-item><p><bold>Wrote the paper:</bold> CTF WQH JG WHT IM.</p></list-item></list></p></fn><fn fn-type="other" id="econtrib001"><p>‡ These authors are joint senior authors on this work.</p></fn><corresp id="cor001">* E-mail: <email>ivomueller@fastmail.fm</email></corresp></author-notes><pub-date pub-type="epub"><day>27</day><month>9</month><year>2016</year></pub-date><pub-date pub-type="collection"><month>9</month><year>2016</year></pub-date><volume>10</volume><issue>9</issue><elocation-id>e0005014</elocation-id><history><date date-type="received"><day>27</day><month>4</month><year>2016</year></date><date date-type="accepted"><day>30</day><month>8</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 França et al</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>França et al</copyright-holder><license 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 License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pntd.0005014.pdf"></self-uri><abstract><sec id="sec001"><title>Background</title><p>Major gaps in our understanding of <italic>Plasmodium vivax</italic> biology and the acquisition of immunity to this parasite hinder vaccine development. <italic>P</italic>. <italic>vivax</italic> merozoites exclusively invade reticulocytes, making parasite proteins that mediate reticulocyte binding and/or invasion potential key vaccine or drug targets. While protein interactions that mediate invasion are still poorly understood, the <italic>P</italic>. <italic>vivax</italic> Reticulocyte-Binding Protein family (PvRBP) is thought to be involved in <italic>P</italic>. <italic>vivax</italic> restricted host-cell selectivity.</p></sec><sec id="sec002"><title>Methodology/Principal findings</title><p>We assessed the binding specificity of five members of the PvRBP family (PvRBP1a, PvRBP1b, PvRBP2a, PvRBP2b, PvRBP2-P2 and a non-binding fragment of PvRBP2c) to normocytes or reticulocytes. PvRBP2b was identified as the only reticulocyte-specific binder (P<0.001), whereas the others preferentially bound to normocytes (PvRBP1a/b P≤0.034), or showed comparable binding to both (PvRBP2a/2-P2, P = 0.38). Furthermore, we measured levels of total and IgG subclasses 1, 2, 3 and 4 to the six PvRBPs in a cohort of young Papua New Guinean children, and assessed their relationship with prospective risk of <italic>P</italic>. <italic>vivax</italic> malaria. Children had substantial, highly correlated (rho = 0.49–0.82, P<0.001) antibody levels to all six PvRBPs, with dominant IgG1 and IgG3 subclasses. Both total IgG (Incidence Rate Ratio [IRR] 0.63–0.73, P = 0.008–0.041) and IgG1 (IRR 0.56–0.69, P = 0.001–0.035) to PvRBP2b and PvRBP1a were strongly associated with reduced risk of vivax-malaria, independently of age and exposure.</p></sec><sec id="sec003"><title>Conclusion/Significance</title><p>These results demonstrate a diversity of erythrocyte-binding phenotypes of PvRBPs, indicating binding to both reticulocyte-specific and normocyte-specific ligands. Our findings provide further insights into the naturally acquired immunity to <italic>P</italic>. <italic>vivax</italic> and highlight the importance of PvRBP proteins as targets of naturally acquired humoral immunity. In-depth studies of the role of PvRBPs in <italic>P</italic>. <italic>vivax</italic> invasion and functional validation of the role of anti-PvRBP antibodies in clinical immunity against <italic>P</italic>. <italic>vivax</italic> are now required to confirm the potential of the reticulocyte-binding PvRBP2b and PvRBP1a as vaccine candidate antigens.</p></sec></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>In parallel with the tremendous reduction in malaria burden, <italic>Plasmodium vivax (Pv)</italic> is now the predominant malaria species in the Asia-Pacific and Americas. <italic>Pv</italic> can only invade young erythrocytes (reticulocytes) and this restriction is thought to involve the Reticulocyte-Binding Protein family (PvRBP). Given their predicted role, PvRBPs are potentially interesting vaccine targets. However, the acquisition of immunity to <italic>Pv</italic> in general (PvRBPs in particular) is poorly understood, hindering vaccine development. Here, we show that out of five PvRBPs, only one (PvRBP2b) binds exclusively to reticulocytes. Furthermore, we measured antibody levels to all six PvRBPs in a cohort of young Papua New Guinean children, assessing the relationship between antibodies to PvRBPs and risk of malaria disease. Both total and specific antibody subclass levels (IgG1 and IgG3) to the reticulocyte-specific binder PvRBP2b, and the non-specific binder PvRBP1a were strongly associated with lower risk of clinical disease. Our findings indicate a diversity of roles of PvRBPs in erythrocyte invasion and highlight their importance as targets of the naturally acquired immunity to <italic>Pv</italic>. Functional studies of the role of PvRBPs in reticulocyte invasion will be required to fully understand the potential of PvRBP1a and PvRBP2b as vaccine candidates.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000060</institution-id><institution>National Institute of Allergy and Infectious Diseases</institution></institution-wrap></funding-source><award-id>U19AI089686</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000060</institution-id><institution>National Institute of Allergy and Infectious Diseases</institution></institution-wrap></funding-source><award-id>AI063135</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000925</institution-id><institution>National Health and Medical Research Council</institution></institution-wrap></funding-source><award-id>1021544</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000925</institution-id><institution>National Health and Medical Research Council</institution></institution-wrap></funding-source><award-id>1084717</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award005"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000925</institution-id><institution>National Health and Medical Research Council</institution></institution-wrap></funding-source><award-id>1043345</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award006"><funding-source><institution>Malaria Elimination Science Alliance (MESA)</institution></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6554-6889</contrib-id><name><surname>Mueller</surname><given-names>Ivo</given-names></name></principal-award-recipient></award-group><award-group id="award007"><funding-source><institution>Victorian State Government Operational 397 Infrastructure Support and Australian Government NHMRC IRIISS</institution></funding-source></award-group><award-group id="award008"><funding-source><institution>Melbourne International Postgraduate Scholarship (MIPS)</institution></funding-source><principal-award-recipient><name><surname>França</surname><given-names>Camila T</given-names></name></principal-award-recipient></award-group><award-group id="award009"><funding-source><institution>Melbourne International Research Scholarship</institution></funding-source><principal-award-recipient><name><surname>He</surname><given-names>Wen-Qiang</given-names></name></principal-award-recipient></award-group><award-group id="award010"><funding-source><institution>Melbourne International Postgraduate Scholarship (MIPS)</institution></funding-source><principal-award-recipient><name><surname>He</surname><given-names>Wen-Qiang</given-names></name></principal-award-recipient></award-group><award-group id="award011"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000923</institution-id><institution>Australian Research Council</institution></institution-wrap></funding-source><award-id>Future Fellowship.</award-id><principal-award-recipient><name><surname>Tham</surname><given-names>Wai-Hong</given-names></name></principal-award-recipient></award-group><funding-statement>This study was funded in part by the Southwest Pacific International Centre of Excellence in Malaria Research (NIH grant U19AI089686) “Research to control and eliminate malaria in the Southwest Pacific”), the National Institutes of Health (AI063135), the National Health & Medical Research Council (1021544 & 1084717), the Malaria Elimination Science Alliance (MESA). This work was made possible through Victorian State Government Operational Infrastructure Support and Australian Government NHMRC IRIISS. IM is supported by an NHMRC Senior Research Fellowship 1043345), CTF is supported by the University of Melbourne—Melbourne International Postgraduate Scholarship (MIPS), WQH is supported by both Melbourne International Research Scholarship and MIPS and WHT is supported by an Australian Research Council Future Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="4"></fig-count><table-count count="1"></table-count><page-count count="17"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>Data cannot be made publicly available because it would compromise participant privacy and violates the ethical agreement in the informed consent forms. Data is available upon reasonable request by contacting the PNG Medical Research Advisory Committee and the PNG Institute of Medical Research IRB. The contact is Dr. William Pomat, secretary PNG IMR IRB: <email>William.Pomat@pngimr.org.pg</email>.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>Data cannot be made publicly available because it would compromise participant privacy and violates the ethical agreement in the informed consent forms. Data is available upon reasonable request by contacting the PNG Medical Research Advisory Committee and the PNG Institute of Medical Research IRB. The contact is Dr. William Pomat, secretary PNG IMR IRB: <email>William.Pomat@pngimr.org.pg</email>.</p></notes></front></pmc><affiliations><list><country><li>Australie</li><li>Espagne</li><li>France</li><li>Papouasie-Nouvelle-Guinée</li></country><region><li>Catalogne</li><li>Victoria (État)</li><li>Île-de-France</li></region><settlement><li>Barcelone</li><li>Melbourne</li><li>Paris</li></settlement><orgName><li>Université de Melbourne</li></orgName></list><tree><country name="Australie"><region name="Victoria (État)"><name sortKey="Franca, Camila T" sort="Franca, Camila T" uniqKey="Franca C" first="Camila T." last="França">Camila T. França</name></region><name sortKey="Franca, Camila T" sort="Franca, Camila T" uniqKey="Franca C" first="Camila T." last="França">Camila T. França</name><name sortKey="Gruszczyk, Jakub" sort="Gruszczyk, Jakub" uniqKey="Gruszczyk J" first="Jakub" last="Gruszczyk">Jakub Gruszczyk</name><name sortKey="He, Wen Qiang" sort="He, Wen Qiang" uniqKey="He W" first="Wen-Qiang" last="He">Wen-Qiang He</name><name sortKey="He, Wen Qiang" sort="He, Wen Qiang" uniqKey="He W" first="Wen-Qiang" last="He">Wen-Qiang He</name><name sortKey="Lim, Nicholas T Y" sort="Lim, Nicholas T Y" uniqKey="Lim N" first="Nicholas T. Y." last="Lim">Nicholas T. Y. Lim</name><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name><name sortKey="Tham, Wai Hong" sort="Tham, Wai Hong" uniqKey="Tham W" first="Wai-Hong" last="Tham">Wai-Hong Tham</name><name sortKey="Tham, Wai Hong" sort="Tham, Wai Hong" uniqKey="Tham W" first="Wai-Hong" last="Tham">Wai-Hong Tham</name></country><country name="Papouasie-Nouvelle-Guinée"><noRegion><name sortKey="Lin, Enmoore" sort="Lin, Enmoore" uniqKey="Lin E" first="Enmoore" last="Lin">Enmoore Lin</name></noRegion><name sortKey="Kiniboro, Benson" sort="Kiniboro, Benson" uniqKey="Kiniboro B" first="Benson" last="Kiniboro">Benson Kiniboro</name><name sortKey="Siba, Peter M" sort="Siba, Peter M" uniqKey="Siba P" first="Peter M." last="Siba">Peter M. Siba</name></country><country name="France"><region name="Île-de-France"><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name></region></country><country name="Espagne"><region name="Catalogne"><name sortKey="Mueller, Ivo" sort="Mueller, Ivo" uniqKey="Mueller I" first="Ivo" last="Mueller">Ivo Mueller</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|texte= Plasmodium vivax Reticulocyte Binding Proteins Are Key Targets of Naturally Acquired Immunity in Young Papua New Guinean Children
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