{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,28]],"date-time":"2026-01-28T11:50:18Z","timestamp":1769601018739,"version":"3.49.0"},"reference-count":61,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T00:00:00Z","timestamp":1686873600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100017001","name":"Li Ka Shing Institute of Virology, University of Alberta","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100017001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000196","name":"Canada Foundation for Innovation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000196","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>During <jats:italic>Plasmodium falciparum<\/jats:italic> infection in pregnancy, VAR2CSA is expressed on the surface of infected erythrocytes (IEs) and mediates their sequestration in the placenta. As a result, antibodies to VAR2CSA are largely restricted to women who were infected during pregnancy. However, we discovered that VAR2CSA antibodies can also be elicited by <jats:italic>P. vivax<\/jats:italic> Duffy binding protein (PvDBP). We proposed that infection with <jats:italic>P. vivax<\/jats:italic> in non-pregnant individuals can generate antibodies that cross-react with VAR2CSA. To better understand the specificity of these antibodies, we took advantage of a mouse monoclonal antibody (3D10) raised against PvDBP that cross-reacts with VAR2CSA and identified the epitopes targeted by this antibody. We screened two peptide arrays that span the ectodomain of VAR2CSA from the FCR3 and NF54 alleles. Based on the top epitope recognized by 3D10, we designed a 34-amino acid synthetic peptide, which we call CRP1, that maps to a highly conserved region in DBL3X. Specific lysine residues are critical for 3D10 recognition, and these same amino acids are within a previously defined chondroitin sulfate A (CSA) binding site in DBL3X. We showed by isothermal titration calorimetry that the CRP1 peptide can bind directly to CSA, and antibodies to CRP1 raised in rats significantly blocked the binding of IEs to CSA <jats:italic>in vitro<\/jats:italic>. In our Colombian cohorts of pregnant and non-pregnant individuals, at least 45% were seroreactive to CRP1. Antibody reactivities to CRP1 and the 3D10 natural epitope in PvDBP region II, subdomain 1 (SD1), were strongly correlated in both cohorts. These findings suggest that antibodies arising from PvDBP may cross-react with VAR2CSA through the epitope in CRP1 and that CRP1 could be a potential vaccine candidate to target a distinct CSA binding site in VAR2CSA.<\/jats:p>","DOI":"10.3389\/fcimb.2023.1202276","type":"journal-article","created":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T05:44:20Z","timestamp":1686894260000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["A conserved epitope in VAR2CSA is targeted by a cross-reactive antibody originating from Plasmodium vivax Duffy binding protein"],"prefix":"10.3389","volume":"13","author":[{"given":"Uwa","family":"Iyamu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel Ferrer","family":"Vinals","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bernard","family":"Tornyigah","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eliana","family":"Arango","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rakesh","family":"Bhat","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Trixie Rae","family":"Adra","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simranjit","family":"Grewal","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kimberly","family":"Martin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amanda","family":"Maestre","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael","family":"Overduin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bart","family":"Hazes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stephanie K.","family":"Yanow","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,6,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0040042","article-title":"Structural insight into epitopes in the pregnancy-associated malaria protein VAR2CSA","volume":"4","author":"Andersen","year":"2008","journal-title":"PloS Pathog."},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005831","article-title":"Placental sequestration of plasmodium falciparum malaria parasites is mediated by the interaction between VAR2CSA and chondroitin sulfate a on syndecan-1","volume":"12","author":"Ayres Pereira","year":"2016","journal-title":"PloS Pathogens"},{"key":"B3","doi-asserted-by":"publisher","first-page":"827","DOI":"10.1016\/j.chom.2019.04.003","article-title":"Influenza antigen engineering focuses immune responses to a subdominant but broadly protective viral epitope","volume":"25","author":"Bajic","year":"2019","journal-title":"Cell Host Microbe"},{"key":"B4","doi-asserted-by":"publisher","first-page":"3497","DOI":"10.1073\/pnas.93.8.3497","article-title":"Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1","volume":"93","author":"Baruch","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"B5","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1053\/j.semperi.2019.03.018","article-title":"An overview of malaria in pregnancy","volume":"43","author":"Bauserman","year":"2019","journal-title":"Semin. Perinatol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"18589","DOI":"10.1074\/jbc.RA120.014676","article-title":"Molecular architecture and domain arrangement of the placental malaria protein VAR2CSA suggests a model for carbohydrate binding","volume":"295","author":"Bewley","year":"2020","journal-title":"J. Biol. Chem."},{"key":"B7","doi-asserted-by":"publisher","first-page":"577","DOI":"10.18273\/revsal.v49n4-2017007","article-title":"La regi\u00f3n \u201cUrab\u00e1 antioque\u00f1o-cuencas altas de los r\u00edos sin\u00fa y San Jorge-bajo cauca antioque\u00f1o\u201d:\u201dguarida\u201d del paludismo colombiano","volume":"49","author":"Carmona-Fonseca","year":"2017","journal-title":"Rev. la Universidad Ind. Santander Salud"},{"key":"B8","doi-asserted-by":"publisher","first-page":"6277","DOI":"10.1073\/pnas.1600488113","article-title":"Broadly neutralizing epitopes in the plasmodium vivax vaccine candidate Duffy binding protein","volume":"113","author":"Chen","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"B9","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1038\/s41541-018-0064-6","article-title":"Down-selection of the VAR2CSA DBL1-2 expressed in e. coli as a lead antigen for placental malaria vaccine development","volume":"3","author":"Ch\u00eane","year":"2018","journal-title":"NPJ Vaccines"},{"key":"B10","doi-asserted-by":"publisher","first-page":"23332","DOI":"10.1074\/jbc.M112.348839","article-title":"Structural and functional insight into how the plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate a in placental malaria*","volume":"287","author":"Clausen","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1101\/gr.849004","article-title":"WebLogo: a sequence logo generator","volume":"14","author":"Crooks","year":"2004","journal-title":"Genome Res."},{"key":"B12","doi-asserted-by":"publisher","first-page":"15908","DOI":"10.1074\/jbc.M110.191510","article-title":"The chondroitin sulfate a-binding site of the VAR2CSA protein involves multiple n-terminal domains*","volume":"286","author":"Dahlb\u00e4ck","year":"2011","journal-title":"J. Biol. Chem."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0020124","article-title":"Epitope mapping and topographic analysis of VAR2CSA DBL3X involved in p. falciparum placental sequestration","volume":"2","author":"Dahlb\u00e4ck","year":"2006","journal-title":"PloS Pathogens"},{"key":"B14","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1038\/s42003-019-0704-z","article-title":"Placental malaria vaccine candidate antigen VAR2CSA displays atypical domain architecture in some plasmodium falciparum strains","volume":"2","author":"Doritchamou","year":"2019","journal-title":"Commun. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"774","DOI":"10.1111\/j.1365-2958.2005.04577.x","article-title":"Broad analysis reveals a consistent pattern of var gene transcription in plasmodium falciparum repeatedly selected for a defined adhesion phenotype","volume":"56","author":"Duffy","year":"2005","journal-title":"Mol. Microbiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1502","DOI":"10.1126\/science.272.5267.1502","article-title":"Adherence of plasmodium falciparum to chondroitin sulfate a in the human placenta","volume":"272","author":"Fried","year":"1996","journal-title":"Science"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a025551","article-title":"Malaria during pregnancy","volume":"7","author":"Fried","year":"2017","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.634508","article-title":"Progress and insights toward an effective placental malaria vaccine","volume":"12","author":"Gamain","year":"2021","journal-title":"Front. Immunol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1111\/j.1365-2958.2004.04145.x","article-title":"Identification of a 67-amino-acid region of the plasmodium falciparum variant surface antigen that binds chondroitin sulphate a and elicits antibodies reactive with the surface of placental isolates","volume":"53","author":"Gamain","year":"2004","journal-title":"Mol. Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1038\/nature01097","article-title":"Genome sequence of the human malaria parasite plasmodium falciparum","volume":"419","author":"Gardner","year":"2002","journal-title":"Nature"},{"key":"B21","doi-asserted-by":"publisher","first-page":"e00797","DOI":"10.1128\/IAI.00797-17","article-title":"Clinical outcomes of submicroscopic infections and correlates of protection of VAR2CSA antibodies in a longitudinal study of pregnant women in Colombia","volume":"86","author":"Gavina","year":"2018","journal-title":"Infect. Immun."},{"key":"B22","doi-asserted-by":"publisher","first-page":"2565","DOI":"10.1128\/IAI.01594-14","article-title":"Functional antibodies against VAR2CSA in nonpregnant populations from colombia exposed to plasmodium falciparum and plasmodium vivax","volume":"82","author":"Gnidehou","year":"2014","journal-title":"Infect. Immun."},{"key":"B23","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1093\/infdis\/jiy467","article-title":"Cross-species immune recognition between plasmodium vivax Duffy binding protein antibodies and the plasmodium falciparum surface antigen VAR2CSA","volume":"219","author":"Gnidehou","year":"2019","journal-title":"J. Infect. Diseases"},{"key":"B24","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.pt.2020.09.012","article-title":"VAR2CSA antibodies in non-pregnant populations","volume":"37","author":"Gnidehou","year":"2021","journal-title":"Trends Parasitol."},{"key":"B25","article-title":"Distribuci\u00f3n espacial de la malaria en el departamento de c\u00f3rdoba en el periodo 2015\u20132018","author":"Hel\u00edas Rodr\u00edguez","year":"2021"},{"key":"B26","doi-asserted-by":"publisher","first-page":"21842","DOI":"10.1074\/jbc.C800086200","article-title":"The structure of a chondroitin sulfate-binding domain important in placental malaria*","volume":"283","author":"Higgins","year":"2008","journal-title":"J. Biol. Chem."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.molbiopara.2006.03.004","article-title":"Disguising itself\u2013insights into plasmodium falciparum binding and immune evasion from the DBL crystal structure","volume":"148","author":"Howell","year":"2006","journal-title":"Mol. Biochem. Parasitol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/bs.apar.2015.02.004","article-title":"PfEMP1 - a parasite protein family of key importance in plasmodium falciparum malaria immunity and pathogenesis","volume":"88","author":"Hviid","year":"2015","journal-title":"Adv. Parasitol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1337","DOI":"10.1042\/BST0381337","article-title":"Structural insights into chondroitin sulfate binding in pregnancy-associated malaria","volume":"38","author":"Khunrae","year":"2010","journal-title":"Biochem. Soc. Trans."},{"key":"B30","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.jmb.2009.08.027","article-title":"Structural comparison of two CSPG-binding DBL domains from the VAR2CSA protein important in malaria during pregnancy","volume":"393","author":"Khunrae","year":"2009","journal-title":"J. Mol. Biol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1186\/s12859-018-2367-z","article-title":"Biotite: a unifying open source computational biology framework in Python","volume":"19","author":"Kunzmann","year":"2018","journal-title":"BMC Bioinf."},{"key":"B32","doi-asserted-by":"publisher","first-page":"4842","DOI":"10.1128\/IAI.02097-14","article-title":"Antigen reversal identifies targets of opsonizing IgGs against pregnancy-associated malaria","volume":"82","author":"Lambert","year":"2014","journal-title":"Infect. Immun."},{"key":"B33","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1038\/s41564-020-00858-9","article-title":"Structural basis for placental malaria mediated by plasmodium falciparum VAR2CSA","volume":"6","author":"Ma","year":"2021","journal-title":"Nat. Microbiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"W276","DOI":"10.1093\/nar\/gkac240","article-title":"Search and sequence analysis tools services from EMBL-EBI in 2022","volume":"50","author":"Madeira","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.644563","article-title":"High antibodies to VAR2CSA in response to malaria infection are associated with improved birthweight in a longitudinal study of pregnant women","volume":"12","author":"McLean","year":"2021","journal-title":"Front. Immunol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"2883","DOI":"10.1080\/21645515.2017.1347740","article-title":"Epitope mapping of Ebola virus dominant and subdominant glycoprotein epitopes facilitates construction of an epitope-based DNA vaccine able to focus the antibody response in mice","volume":"13","author":"Mitchell","year":"2017","journal-title":"Hum. Vaccin. Immunother."},{"key":"B37","doi-asserted-by":"publisher","first-page":"392","DOI":"10.3390\/vaccines8030392","article-title":"Generation of a peptide vaccine candidate against falciparum placental malaria based on a discontinuous epitope","volume":"8","author":"Mitran","year":"2020","journal-title":"Vaccines (Basel)"},{"key":"B38","doi-asserted-by":"publisher","first-page":"e02343","DOI":"10.1128\/mBio.02343-19","article-title":"Antibodies to cryptic epitopes in distant homologues underpin a mechanism of heterologous immunity between plasmodium vivax PvDBP and plasmodium falciparum VAR2CSA","volume":"10","author":"Mitran","year":"2019","journal-title":"mBio"},{"key":"B39","doi-asserted-by":"publisher","first-page":"1509","DOI":"10.1093\/cid\/ciy1140","article-title":"First-in-human, randomized, double-blind clinical trial of differentially adjuvanted PAMVAC, a vaccine candidate to prevent pregnancy-associated malaria","volume":"69","author":"Mordm\u00fcller","year":"2019","journal-title":"Clin. Infect. Dis."},{"key":"B40","doi-asserted-by":"publisher","first-page":"2013","DOI":"10.1016\/S0002-9440(10)63761-3","article-title":"Plasmodium falciparum-infected erythrocytes adhere both in the intervillous space and on the villous surface of human placenta by binding to the low-sulfated chondroitin sulfate proteoglycan receptor","volume":"164","author":"Muthusamy","year":"2004","journal-title":"Am. J. Pathology"},{"key":"B41","doi-asserted-by":"publisher","first-page":"2482","DOI":"10.1128\/IAI.00159-09","article-title":"Induction of adhesion-inhibitory antibodies against placental plasmodium falciparum parasites by using single domains of VAR2CSA","volume":"77","author":"Nielsen","year":"2009","journal-title":"Infect. Immun."},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0135406","article-title":"The influence of Sub-unit composition and expression system on the functional antibody response in the development of a VAR2CSA based plasmodium falciparum placental malaria vaccine","volume":"10","author":"Nielsen","year":"2015","journal-title":"PloS One"},{"key":"B43","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1128\/CVI.00638-12","article-title":"Identification of VAR2CSA domain-specific inhibitory antibodies of the plasmodium falciparum erythrocyte membrane protein 1 using a novel flow cytometry assay","volume":"20","author":"Obiakor","year":"2013","journal-title":"Clin. Vaccine Immunol."},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0247811","article-title":"Malaria risk stratification in Colombia 2010 to 2019","volume":"16","author":"Padilla-Rodr\u00edguez","year":"2021","journal-title":"PloS One"},{"key":"B45","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1038\/s41541-018-0053-9","article-title":"Skin infection boosts memory b-cells specific for a cryptic vaccine epitope of group a streptococcus and broadens the immune response to enhance vaccine efficacy","volume":"3","author":"Pandey","year":"2018","journal-title":"NPJ Vaccines"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1084\/jem.20041579","article-title":"Evidence for the involvement of VAR2CSA in pregnancy-associated malaria","volume":"200","author":"Salanti","year":"2004","journal-title":"J. Exp. Med."},{"key":"B47","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/1475-2875-9-11","article-title":"Several domains from VAR2CSA can induce plasmodium falciparum adhesion-blocking antibodies","volume":"9","author":"Salanti","year":"2010","journal-title":"Malar J."},{"key":"B48","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1046\/j.1365-2958.2003.03570.x","article-title":"Selective upregulation of a single distinctly structured var gene in chondroitin sulphate a-adhering plasmodium falciparum involved in pregnancy-associated malaria","volume":"49","author":"Salanti","year":"2003","journal-title":"Mol. Microbiol."},{"key":"B49","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-0716-1036-7_1","article-title":"The clustal omega multiple alignment package","volume-title":"Multiple sequence alignment: methods and protocols","author":"Sievers","year":"2021"},{"key":"B50","doi-asserted-by":"publisher","first-page":"24855","DOI":"10.1074\/jbc.M110.118612","article-title":"Subdomain 3 of plasmodium falciparum VAR2CSA DBL3x is identified as a minimal chondroitin sulfate a-binding region","volume":"285","author":"Singh","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B51","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1038\/nsmb.1479","article-title":"Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate a","volume":"15","author":"Singh","year":"2008","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1016\/S1473-3099(19)30739-X","article-title":"PRIMVAC vaccine adjuvanted with alhydrogel or GLA-SE to prevent placental malaria: a first-in-human, randomised, double-blind, placebo-controlled study","volume":"20","author":"Sirima","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"B53","doi-asserted-by":"publisher","first-page":"e20270","DOI":"10.1371\/journal.pone.0020270","article-title":"Var2CSA minimal CSA binding region is located within the n-terminal region","volume":"6","author":"Srivastava","year":"2011","journal-title":"PloS One"},{"key":"B54","doi-asserted-by":"publisher","first-page":"4884","DOI":"10.1073\/pnas.1000951107","article-title":"Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA","volume":"107","author":"Srivastava","year":"2010","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B55","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1016\/j.pt.2013.10.001","article-title":"Escaping the immune system: how the malaria parasite makes vaccine development a challenge","volume":"29","author":"Stanisic","year":"2013","journal-title":"Trends Parasitology"},{"key":"B56","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1002\/jmr.846","article-title":"Functional reconstruction and synthetic mimicry of a conformational epitope using CLIPS technology","volume":"20","author":"Timmerman","year":"2007","journal-title":"J. Mol. Recognit."},{"key":"B57","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1126\/science.781840","article-title":"Human malaria parasites in continuous culture","volume":"193","author":"Trager","year":"1976","journal-title":"Science"},{"key":"B58","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1086\/430933","article-title":"High level of var2csa transcription by plasmodium falciparum isolated from the placenta","volume":"192","author":"Tuikue Ndam","year":"2005","journal-title":"J. Infect. Diseases"},{"key":"B59","doi-asserted-by":"publisher","first-page":"2956","DOI":"10.1038\/s41467-021-23254-1","article-title":"Cryo-EM reveals the architecture of placental malaria VAR2CSA and provides molecular insight into chondroitin sulfate binding","volume":"12","author":"Wang","year":"2021","journal-title":"Nat. Commun."},{"key":"B60","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1038\/s41421-021-00324-8","article-title":"The molecular mechanism of cytoadherence to placental or tumor cells through VAR2CSA from plasmodium falciparum","volume":"7","author":"Wang","year":"2021","journal-title":"Cell Discovery"},{"key":"B61","volume-title":"World malaria report 2022","year":"2022"}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2023.1202276\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T05:44:29Z","timestamp":1686894269000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2023.1202276\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,16]]},"references-count":61,"alternative-id":["10.3389\/fcimb.2023.1202276"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2023.1202276","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,16]]},"article-number":"1202276"}}