Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein

The discovery that Africans were resistant to infection by ( ) led to the conclusion that invasion relied on the Duffy Binding Protein (PvDBP) interacting with the Duffy Antigen Receptor for Chemokines (DARC) expressed on erythrocytes. However, the recent reporting of infections in DARC-negative Afr...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2024-01, Vol.121 (5), p.e2316304121
Hauptverfasser: Lee, Seong-Kyun, Crosnier, Cécile, Valenzuela-Leon, Paola Carolina, Dizon, Brian L P, Atkinson, John P, Mu, Jianbing, Wright, Gavin J, Calvo, Eric, Gunalan, Karthigayan, Miller, Louis H
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 5
container_start_page e2316304121
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 121
creator Lee, Seong-Kyun
Crosnier, Cécile
Valenzuela-Leon, Paola Carolina
Dizon, Brian L P
Atkinson, John P
Mu, Jianbing
Wright, Gavin J
Calvo, Eric
Gunalan, Karthigayan
Miller, Louis H
description The discovery that Africans were resistant to infection by ( ) led to the conclusion that invasion relied on the Duffy Binding Protein (PvDBP) interacting with the Duffy Antigen Receptor for Chemokines (DARC) expressed on erythrocytes. However, the recent reporting of infections in DARC-negative Africans suggests that the parasite might use an alternate invasion pathway to infect DARC-negative reticulocytes. To identify the parasite ligands and erythrocyte receptors that enable invasion of both DARC-positive and -negative erythrocytes, we expressed region II containing the Duffy Binding-Like (DBL) domain of erythrocyte binding protein (PvEBP-RII) and verified that the DBL domain binds to both DARC-positive and -negative erythrocytes. Furthermore, an AVidity-based EXtracelluar Interaction Screening (AVEXIS) was used to identify the receptor for PvEBP among over 750 human cell surface receptor proteins, and this approach identified only Complement Receptor 1 (CR1, CD35, or C3b/C4b receptor) as a PvEBP receptor. CR1 is a well-known receptor for Reticulocyte binding protein Homology 4 (PfRh4) and is present on the surfaces of both reticulocytes and normocytes, but its expression decreases as erythrocytes age. Indeed, PvEBP-RII bound to a subpopulation of both reticulocytes and normocytes, and this binding was blocked by the addition of soluble CR1 recombinant protein, indicating that CR1 is the receptor of PvEBP. In addition, we found that the Long Homology Repeat A (LHR-A) subdomain of CR1 is the only subdomain responsible for mediating the interaction with PvEBP-RII.
doi_str_mv 10.1073/pnas.2316304121
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10835065</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2918198754</sourcerecordid><originalsourceid>FETCH-LOGICAL-c422t-cca5901c0356c47ea4bdbdefecb3a9b5573cbca92739684427a68b61ac8c54433</originalsourceid><addsrcrecordid>eNpdkU1v1DAQhi0EokvhzA1F4sIlrcdfsU8IrfiSKpVDe7YcZ7ZxldjBTlbsvyerlpb2YM3Bz7yaVw8h74GeAW34-RRdOWMcFKcCGLwgG6AGaiUMfUk2lLKm1oKJE_KmlFtKqZGaviYnXDMFCpoN6bdpnAYcMc5VRo_TnHIFVSjV3GPVL6OLFebD3OfkDzM-Mrv1_RpcGVMXlrHah73784RsQ-xCvKmmnGYM8S15tXNDwXf385Rcf_t6tf1RX1x-_7n9clF7wdhce--koeApl8qLBp1ou7bDHfqWO9NK2XDfemdYw43SQrDGKd0qcF57KQTnp-TzXe60tCN2fi2W3WCnHEaXDza5YJ_-xNDbm7S3QDWXVMk14dN9Qk6_FyyzHUPxOAwuYlqKZQY0GN1IsaIfn6G3aclx7bdSDMAoIY7U-R3lcyol4-7hGqD2qNEeNdpHjevGh_9LPPD_vPG_BbicAQ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2921196444</pqid></control><display><type>article</type><title>Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein</title><source>MEDLINE</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Lee, Seong-Kyun ; Crosnier, Cécile ; Valenzuela-Leon, Paola Carolina ; Dizon, Brian L P ; Atkinson, John P ; Mu, Jianbing ; Wright, Gavin J ; Calvo, Eric ; Gunalan, Karthigayan ; Miller, Louis H</creator><creatorcontrib>Lee, Seong-Kyun ; Crosnier, Cécile ; Valenzuela-Leon, Paola Carolina ; Dizon, Brian L P ; Atkinson, John P ; Mu, Jianbing ; Wright, Gavin J ; Calvo, Eric ; Gunalan, Karthigayan ; Miller, Louis H</creatorcontrib><description>The discovery that Africans were resistant to infection by ( ) led to the conclusion that invasion relied on the Duffy Binding Protein (PvDBP) interacting with the Duffy Antigen Receptor for Chemokines (DARC) expressed on erythrocytes. However, the recent reporting of infections in DARC-negative Africans suggests that the parasite might use an alternate invasion pathway to infect DARC-negative reticulocytes. To identify the parasite ligands and erythrocyte receptors that enable invasion of both DARC-positive and -negative erythrocytes, we expressed region II containing the Duffy Binding-Like (DBL) domain of erythrocyte binding protein (PvEBP-RII) and verified that the DBL domain binds to both DARC-positive and -negative erythrocytes. Furthermore, an AVidity-based EXtracelluar Interaction Screening (AVEXIS) was used to identify the receptor for PvEBP among over 750 human cell surface receptor proteins, and this approach identified only Complement Receptor 1 (CR1, CD35, or C3b/C4b receptor) as a PvEBP receptor. CR1 is a well-known receptor for Reticulocyte binding protein Homology 4 (PfRh4) and is present on the surfaces of both reticulocytes and normocytes, but its expression decreases as erythrocytes age. Indeed, PvEBP-RII bound to a subpopulation of both reticulocytes and normocytes, and this binding was blocked by the addition of soluble CR1 recombinant protein, indicating that CR1 is the receptor of PvEBP. In addition, we found that the Long Homology Repeat A (LHR-A) subdomain of CR1 is the only subdomain responsible for mediating the interaction with PvEBP-RII.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2316304121</identifier><identifier>PMID: 38261617</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Avidity ; Biological Sciences ; CD2 Antigens ; Cell Adhesion Molecules ; Cell surface ; Cell surface receptors ; Chemokines ; Complement receptor 1 ; Duffy antigen ; Erythrocytes ; Homology ; Humans ; Malaria, Falciparum ; Parasites ; Plasmodium vivax ; Proteins ; Receptors ; Receptors, Cell Surface ; Reticulocytes</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2024-01, Vol.121 (5), p.e2316304121</ispartof><rights>Copyright National Academy of Sciences Jan 30, 2024</rights><rights>Copyright © 2024 the Author(s). Published by PNAS. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c422t-cca5901c0356c47ea4bdbdefecb3a9b5573cbca92739684427a68b61ac8c54433</citedby><cites>FETCH-LOGICAL-c422t-cca5901c0356c47ea4bdbdefecb3a9b5573cbca92739684427a68b61ac8c54433</cites><orcidid>0000-0002-5740-5178 ; 0000-0001-7880-2730 ; 0000-0002-2514-3441</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10835065/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10835065/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38261617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Seong-Kyun</creatorcontrib><creatorcontrib>Crosnier, Cécile</creatorcontrib><creatorcontrib>Valenzuela-Leon, Paola Carolina</creatorcontrib><creatorcontrib>Dizon, Brian L P</creatorcontrib><creatorcontrib>Atkinson, John P</creatorcontrib><creatorcontrib>Mu, Jianbing</creatorcontrib><creatorcontrib>Wright, Gavin J</creatorcontrib><creatorcontrib>Calvo, Eric</creatorcontrib><creatorcontrib>Gunalan, Karthigayan</creatorcontrib><creatorcontrib>Miller, Louis H</creatorcontrib><title>Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The discovery that Africans were resistant to infection by ( ) led to the conclusion that invasion relied on the Duffy Binding Protein (PvDBP) interacting with the Duffy Antigen Receptor for Chemokines (DARC) expressed on erythrocytes. However, the recent reporting of infections in DARC-negative Africans suggests that the parasite might use an alternate invasion pathway to infect DARC-negative reticulocytes. To identify the parasite ligands and erythrocyte receptors that enable invasion of both DARC-positive and -negative erythrocytes, we expressed region II containing the Duffy Binding-Like (DBL) domain of erythrocyte binding protein (PvEBP-RII) and verified that the DBL domain binds to both DARC-positive and -negative erythrocytes. Furthermore, an AVidity-based EXtracelluar Interaction Screening (AVEXIS) was used to identify the receptor for PvEBP among over 750 human cell surface receptor proteins, and this approach identified only Complement Receptor 1 (CR1, CD35, or C3b/C4b receptor) as a PvEBP receptor. CR1 is a well-known receptor for Reticulocyte binding protein Homology 4 (PfRh4) and is present on the surfaces of both reticulocytes and normocytes, but its expression decreases as erythrocytes age. Indeed, PvEBP-RII bound to a subpopulation of both reticulocytes and normocytes, and this binding was blocked by the addition of soluble CR1 recombinant protein, indicating that CR1 is the receptor of PvEBP. In addition, we found that the Long Homology Repeat A (LHR-A) subdomain of CR1 is the only subdomain responsible for mediating the interaction with PvEBP-RII.</description><subject>Avidity</subject><subject>Biological Sciences</subject><subject>CD2 Antigens</subject><subject>Cell Adhesion Molecules</subject><subject>Cell surface</subject><subject>Cell surface receptors</subject><subject>Chemokines</subject><subject>Complement receptor 1</subject><subject>Duffy antigen</subject><subject>Erythrocytes</subject><subject>Homology</subject><subject>Humans</subject><subject>Malaria, Falciparum</subject><subject>Parasites</subject><subject>Plasmodium vivax</subject><subject>Proteins</subject><subject>Receptors</subject><subject>Receptors, Cell Surface</subject><subject>Reticulocytes</subject><issn>0027-8424</issn><issn>1091-6490</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1v1DAQhi0EokvhzA1F4sIlrcdfsU8IrfiSKpVDe7YcZ7ZxldjBTlbsvyerlpb2YM3Bz7yaVw8h74GeAW34-RRdOWMcFKcCGLwgG6AGaiUMfUk2lLKm1oKJE_KmlFtKqZGaviYnXDMFCpoN6bdpnAYcMc5VRo_TnHIFVSjV3GPVL6OLFebD3OfkDzM-Mrv1_RpcGVMXlrHah73784RsQ-xCvKmmnGYM8S15tXNDwXf385Rcf_t6tf1RX1x-_7n9clF7wdhce--koeApl8qLBp1ou7bDHfqWO9NK2XDfemdYw43SQrDGKd0qcF57KQTnp-TzXe60tCN2fi2W3WCnHEaXDza5YJ_-xNDbm7S3QDWXVMk14dN9Qk6_FyyzHUPxOAwuYlqKZQY0GN1IsaIfn6G3aclx7bdSDMAoIY7U-R3lcyol4-7hGqD2qNEeNdpHjevGh_9LPPD_vPG_BbicAQ</recordid><startdate>20240130</startdate><enddate>20240130</enddate><creator>Lee, Seong-Kyun</creator><creator>Crosnier, Cécile</creator><creator>Valenzuela-Leon, Paola Carolina</creator><creator>Dizon, Brian L P</creator><creator>Atkinson, John P</creator><creator>Mu, Jianbing</creator><creator>Wright, Gavin J</creator><creator>Calvo, Eric</creator><creator>Gunalan, Karthigayan</creator><creator>Miller, Louis H</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5740-5178</orcidid><orcidid>https://orcid.org/0000-0001-7880-2730</orcidid><orcidid>https://orcid.org/0000-0002-2514-3441</orcidid></search><sort><creationdate>20240130</creationdate><title>Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein</title><author>Lee, Seong-Kyun ; Crosnier, Cécile ; Valenzuela-Leon, Paola Carolina ; Dizon, Brian L P ; Atkinson, John P ; Mu, Jianbing ; Wright, Gavin J ; Calvo, Eric ; Gunalan, Karthigayan ; Miller, Louis H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c422t-cca5901c0356c47ea4bdbdefecb3a9b5573cbca92739684427a68b61ac8c54433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Avidity</topic><topic>Biological Sciences</topic><topic>CD2 Antigens</topic><topic>Cell Adhesion Molecules</topic><topic>Cell surface</topic><topic>Cell surface receptors</topic><topic>Chemokines</topic><topic>Complement receptor 1</topic><topic>Duffy antigen</topic><topic>Erythrocytes</topic><topic>Homology</topic><topic>Humans</topic><topic>Malaria, Falciparum</topic><topic>Parasites</topic><topic>Plasmodium vivax</topic><topic>Proteins</topic><topic>Receptors</topic><topic>Receptors, Cell Surface</topic><topic>Reticulocytes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Seong-Kyun</creatorcontrib><creatorcontrib>Crosnier, Cécile</creatorcontrib><creatorcontrib>Valenzuela-Leon, Paola Carolina</creatorcontrib><creatorcontrib>Dizon, Brian L P</creatorcontrib><creatorcontrib>Atkinson, John P</creatorcontrib><creatorcontrib>Mu, Jianbing</creatorcontrib><creatorcontrib>Wright, Gavin J</creatorcontrib><creatorcontrib>Calvo, Eric</creatorcontrib><creatorcontrib>Gunalan, Karthigayan</creatorcontrib><creatorcontrib>Miller, Louis H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Seong-Kyun</au><au>Crosnier, Cécile</au><au>Valenzuela-Leon, Paola Carolina</au><au>Dizon, Brian L P</au><au>Atkinson, John P</au><au>Mu, Jianbing</au><au>Wright, Gavin J</au><au>Calvo, Eric</au><au>Gunalan, Karthigayan</au><au>Miller, Louis H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2024-01-30</date><risdate>2024</risdate><volume>121</volume><issue>5</issue><spage>e2316304121</spage><pages>e2316304121-</pages><issn>0027-8424</issn><issn>1091-6490</issn><eissn>1091-6490</eissn><abstract>The discovery that Africans were resistant to infection by ( ) led to the conclusion that invasion relied on the Duffy Binding Protein (PvDBP) interacting with the Duffy Antigen Receptor for Chemokines (DARC) expressed on erythrocytes. However, the recent reporting of infections in DARC-negative Africans suggests that the parasite might use an alternate invasion pathway to infect DARC-negative reticulocytes. To identify the parasite ligands and erythrocyte receptors that enable invasion of both DARC-positive and -negative erythrocytes, we expressed region II containing the Duffy Binding-Like (DBL) domain of erythrocyte binding protein (PvEBP-RII) and verified that the DBL domain binds to both DARC-positive and -negative erythrocytes. Furthermore, an AVidity-based EXtracelluar Interaction Screening (AVEXIS) was used to identify the receptor for PvEBP among over 750 human cell surface receptor proteins, and this approach identified only Complement Receptor 1 (CR1, CD35, or C3b/C4b receptor) as a PvEBP receptor. CR1 is a well-known receptor for Reticulocyte binding protein Homology 4 (PfRh4) and is present on the surfaces of both reticulocytes and normocytes, but its expression decreases as erythrocytes age. Indeed, PvEBP-RII bound to a subpopulation of both reticulocytes and normocytes, and this binding was blocked by the addition of soluble CR1 recombinant protein, indicating that CR1 is the receptor of PvEBP. In addition, we found that the Long Homology Repeat A (LHR-A) subdomain of CR1 is the only subdomain responsible for mediating the interaction with PvEBP-RII.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>38261617</pmid><doi>10.1073/pnas.2316304121</doi><orcidid>https://orcid.org/0000-0002-5740-5178</orcidid><orcidid>https://orcid.org/0000-0001-7880-2730</orcidid><orcidid>https://orcid.org/0000-0002-2514-3441</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0027-8424
ispartof Proceedings of the National Academy of Sciences - PNAS, 2024-01, Vol.121 (5), p.e2316304121
issn 0027-8424
1091-6490
1091-6490
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10835065
source MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects Avidity
Biological Sciences
CD2 Antigens
Cell Adhesion Molecules
Cell surface
Cell surface receptors
Chemokines
Complement receptor 1
Duffy antigen
Erythrocytes
Homology
Humans
Malaria, Falciparum
Parasites
Plasmodium vivax
Proteins
Receptors
Receptors, Cell Surface
Reticulocytes
title Complement receptor 1 is the human erythrocyte receptor for Plasmodium vivax erythrocyte binding protein
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-20T12%3A23%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Complement%20receptor%201%20is%20the%20human%20erythrocyte%20receptor%20for%20Plasmodium%20vivax%20erythrocyte%20binding%20protein&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Lee,%20Seong-Kyun&rft.date=2024-01-30&rft.volume=121&rft.issue=5&rft.spage=e2316304121&rft.pages=e2316304121-&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.2316304121&rft_dat=%3Cproquest_pubme%3E2918198754%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2921196444&rft_id=info:pmid/38261617&rfr_iscdi=true