{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T06:54:14Z","timestamp":1782370454065,"version":"3.54.5"},"reference-count":64,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2012,4,12]],"date-time":"2012-04-12T00:00:00Z","timestamp":1334188800000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1002451","type":"journal-article","created":{"date-parts":[[2012,4,12]],"date-time":"2012-04-12T21:03:51Z","timestamp":1334264631000},"page":"e1002451","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":40,"title":["Evolution of the Multi-Domain Structures of Virulence Genes in the Human Malaria Parasite, Plasmodium falciparum"],"prefix":"10.1371","volume":"8","author":[{"given":"Caroline O.","family":"Buckee","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Recker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2012,4,12]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"e1000290","DOI":"10.1371\/journal.pmed.1000290","article-title":"Estimating the global clinical burden of Plasmodium falciparum malaria in 2007.","volume":"7","author":"SI Hay","year":"2010","journal-title":"PLoS Med"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1038\/nature03342","article-title":"The global distribution of clinical episodes of Plasmodium falciparum malaria.","volume":"434","author":"RW Snow","year":"2005","journal-title":"Nature"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/S1473-3099(04)01043-6","article-title":"The global distribution and population at risk of malaria: past, present, and future.","volume":"4","author":"SI Hay","year":"2004","journal-title":"Lancet Infect Dis"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/nm0398-358","article-title":"Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria.","volume":"4","author":"PC Bull","year":"1998","journal-title":"Nat Med"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/S0966-842X(01)02278-8","article-title":"The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria.","volume":"10","author":"PC Bull","year":"2002","journal-title":"Trends Microbiol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1084\/jem.159.6.1567","article-title":"Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes.","volume":"159","author":"JH Leech","year":"1984","journal-title":"J Exp Med"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1172\/JCI114234","article-title":"A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes.","volume":"84","author":"JW Barnwell","year":"1989","journal-title":"J Clin Invest"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/341057a0","article-title":"Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum.","volume":"341","author":"AR Berendt","year":"1989","journal-title":"Nature"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1038\/318064a0","article-title":"Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence.","volume":"318","author":"DD Roberts","year":"1985","journal-title":"Nature"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1084\/jem.182.1.15","article-title":"Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes.","volume":"182","author":"SJ Rogerson","year":"1995","journal-title":"J Exp Med"},{"key":"ref11","first-page":"1057","article-title":"An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration.","volume":"145","author":"GD Turner","year":"1994","journal-title":"Am J Pathol"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1136\/bmj.311.7015.1273","article-title":"The incidence of malaria after splenectomy in Papua New Guinea.","volume":"311","author":"KE Boone","year":"1995","journal-title":"BMJ"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1097\/MOH.0b013e32832a1d4b","article-title":"Retention of erythrocytes in the spleen: a double-edged process in human malaria.","volume":"16","author":"PA Buffet","year":"2009","journal-title":"Curr Opin Hematol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1093\/infdis\/164.1.163","article-title":"Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1.","volume":"164","author":"CF Ockenhouse","year":"1991","journal-title":"J Infect Dis"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"168","DOI":"10.4269\/ajtmh.1991.44.168","article-title":"Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study.","volume":"44","author":"E Pongponratn","year":"1991","journal-title":"Am J Trop Med Hyg"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"5198","DOI":"10.1073\/pnas.96.9.5198","article-title":"The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1.","volume":"96","author":"JC Reeder","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1038\/357689a0","article-title":"Rapid switching to multiple antigenic and adhesive phenotypes in malaria.","volume":"357","author":"DJ Roberts","year":"1992","journal-title":"Nature"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/0092-8674(95)90056-X","article-title":"Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes.","volume":"82","author":"JD Smith","year":"1995","journal-title":"Cell"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"3904","DOI":"10.1128\/IAI.02073-05","article-title":"Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children.","volume":"74","author":"M Rottmann","year":"2006","journal-title":"Infect Immun"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.mib.2006.06.006","article-title":"A family affair: var genes, PfEMP1 binding, and malaria disease.","volume":"9","author":"SM Kraemer","year":"2006","journal-title":"Curr Opin Microbiol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1111\/j.1365-2958.2008.06248.x","article-title":"Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks.","volume":"68","author":"PC Bull","year":"2008","journal-title":"Mol Microbiol"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/S0166-6851(00)00286-3","article-title":"Var gene diversity in Plasmodium falciparum is generated by frequent recombination events.","volume":"110","author":"HM Taylor","year":"2000","journal-title":"Mol Biochem Parasitol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/1475-2875-2-27","article-title":"Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions.","volume":"2","author":"T Lavstsen","year":"2003","journal-title":"Malar J"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.molbiopara.2007.03.011","article-title":"An approach to classifying sequence tags sampled from Plasmodium falciparum var genes.","volume":"154","author":"PC Bull","year":"2007","journal-title":"Mol Biochem Parasitol"},{"key":"ref25","article-title":"Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes\u2013divide and conquer.","volume":"6","author":"TS Rask","year":"2010","journal-title":"PLoS Comput Biol"},{"key":"ref26","doi-asserted-by":"crossref","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":"A Salanti","year":"2003","journal-title":"Mol Microbiol"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1086\/430933","article-title":"High level of var2csa transcription by Plasmodium falciparum isolated from the placenta.","volume":"192","author":"NG Tuikue Ndam","year":"2005","journal-title":"J Infect Dis"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"1837","DOI":"10.1128\/IAI.00480-07","article-title":"The C-terminal segment of the cysteine-rich interdomain of Plasmodium falciparum erythrocyte membrane protein 1 determines CD36 binding and elicits antibodies that inhibit adhesion of parasite-infected erythrocytes.","volume":"76","author":"M Mo","year":"2008","journal-title":"Infect Immun"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"3766","DOI":"10.1182\/blood.V90.9.3766","article-title":"Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence.","volume":"90","author":"DI Baruch","year":"1997","journal-title":"Blood"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"e26","DOI":"10.1371\/journal.ppat.0010026","article-title":"Plasmodium falciparum variant surface antigen expression patterns during malaria.","volume":"1","author":"PC Bull","year":"2005","journal-title":"PLoS Pathog"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"15835","DOI":"10.1073\/pnas.0610485104","article-title":"PfEMP1-DBL1alpha amino acid motifs in severe disease states of Plasmodium falciparum malaria.","volume":"104","author":"J Normark","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"2323","DOI":"10.1128\/IAI.63.6.2323-2326.1995","article-title":"Plasmodium falciparum rosetting is associated with malaria severity in Kenya.","volume":"63","author":"A Rowe","year":"1995","journal-title":"Infect Immun"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/nm0496-437","article-title":"The maintenance of strain structure in populations of recombining infectious agents.","volume":"2","author":"S Gupta","year":"1996","journal-title":"Nat Med"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"17209","DOI":"10.1073\/pnas.252512799","article-title":"Dynamics and selection of many-strain pathogens.","volume":"99","author":"JR Gog","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1098\/rsif.2008.0333","article-title":"Improving the realism of deterministic multi-strain models: implications for modelling influenza A.","volume":"6","author":"P Minayev","year":"2009","journal-title":"J R Soc Interface"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1126\/science.280.5365.912","article-title":"Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents.","volume":"280","author":"S Gupta","year":"1998","journal-title":"Science"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1086\/381186","article-title":"Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets.","volume":"189","author":"JG Beeson","year":"2004","journal-title":"J Infect Dis"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1128\/IAI.00749-06","article-title":"Generation of cross-protective antibodies against Plasmodium falciparum sequestration by immunization with an erythrocyte membrane protein 1-duffy binding-like 1 alpha domain.","volume":"75","author":"K Moll","year":"2007","journal-title":"Infect Immun"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.4049\/jimmunol.165.6.3309","article-title":"Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A.","volume":"165","author":"CH Ricke","year":"2000","journal-title":"J Immunol"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"1766","DOI":"10.1073\/pnas.040545897","article-title":"Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria.","volume":"97","author":"JD Smith","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"5565","DOI":"10.1128\/IAI.00901-08","article-title":"An in vivo and in vitro model of Plasmodium falciparum rosetting and autoagglutination mediated by varO, a group A var gene encoding a frequent serotype.","volume":"76","author":"I Vigan-Womas","year":"2008","journal-title":"Infect Immun"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"2701","DOI":"10.1016\/j.vaccine.2004.02.015","article-title":"Immunization with PfEMP1-DBL1alpha generates antibodies that disrupt rosettes and protect against the sequestration of Plasmodium falciparum-infected erythrocytes.","volume":"22","author":"Q Chen","year":"2004","journal-title":"Vaccine"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/0169-4758(93)90121-U","article-title":"Protection, pathogenesis and phenotypic plasticity in Plasmodium falciparum malaria.","volume":"9","author":"DJ Roberts","year":"1993","journal-title":"Parasitol Today"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"e1001306","DOI":"10.1371\/journal.ppat.1001306","article-title":"Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern.","volume":"7","author":"M Recker","year":"2011","journal-title":"PLoS Pathog"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1017\/S0031182005007481","article-title":"A mathematical model for a new mechanism of phenotypic variation in malaria.","volume":"131","author":"M Recker","year":"2005","journal-title":"Parasitology"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/nature02486","article-title":"Transient cross-reactive immune responses can orchestrate antigenic variation in malaria.","volume":"429","author":"M Recker","year":"2004","journal-title":"Nature"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1017\/S0031182001007533","article-title":"Plasmodium falciparum parasitaemia described by a new mathematical model.","volume":"122","author":"L Molineaux","year":"2001","journal-title":"Parasitology"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1111\/j.1365-3024.1994.tb00361.x","article-title":"A theoretical framework for the immunoepidemiology of Plasmodium falciparum malaria.","volume":"16","author":"S Gupta","year":"1994","journal-title":"Parasite Immunol"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1016\/0169-4758(94)90160-0","article-title":"A strain theory of malaria transmission.","volume":"10","author":"S Gupta","year":"1994","journal-title":"Parasitol Today"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"3715","DOI":"10.1073\/pnas.91.9.3715","article-title":"Parasite virulence and disease patterns in Plasmodium falciparum malaria.","volume":"91","author":"S Gupta","year":"1994","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1126\/science.8310293","article-title":"Antigenic diversity and the transmission dynamics of Plasmodium falciparum.","volume":"263","author":"S Gupta","year":"1994","journal-title":"Science"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/S0166-6851(99)00106-1","article-title":"Analysis of Plasmodium falciparum PfEMP-1\/var genes suggests that recombination rearranges constrained sequences.","volume":"102","author":"CP Ward","year":"1999","journal-title":"Mol Biochem Parasitol"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1086\/315652","article-title":"Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age.","volume":"182","author":"PC Bull","year":"2000","journal-title":"J Infect Dis"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1128\/IAI.67.2.733-739.1999","article-title":"Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants.","volume":"67","author":"PC Bull","year":"1999","journal-title":"Infect Immun"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"e1002032","DOI":"10.1371\/journal.ppat.1002032","article-title":"Investigating the Host Binding Signature on the Plasmodium falciparum PfEMP1 Protein Family.","volume":"7","author":"JH Janes","year":"2011","journal-title":"PLoS Pathog"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.molbiopara.2006.08.005","article-title":"Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia.","volume":"150","author":"HM Kyriacou","year":"2006","journal-title":"Mol Biochem Parasitol"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1084\/jem.20040274","article-title":"Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes.","volume":"199","author":"AT Jensen","year":"2004","journal-title":"J Exp Med"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1086\/503776","article-title":"Virulence of malaria is associated with differential expression of Plasmodium falciparum var gene subgroups in a case-control study.","volume":"193","author":"M Kaestli","year":"2006","journal-title":"J Infect Dis"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"21801","DOI":"10.1073\/pnas.0907590106","article-title":"Plasmodium falciparum var gene expression is modified by host immunity.","volume":"106","author":"GM Warimwe","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1186\/1471-2148-7-229","article-title":"Barriers to antigenic escape by pathogens: trade-off between reproductive rate and antigenic mutability.","volume":"7","author":"SA Frank","year":"2007","journal-title":"BMC Evol Biol"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"4842","DOI":"10.1016\/j.vaccine.2010.04.042","article-title":"Re-emergence of the type 1 pilus among Streptococcus pneumoniae isolates in Massachusetts, USA.","volume":"28","author":"G Regev-Yochay","year":"2010","journal-title":"Vaccine"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"e11276","DOI":"10.1371\/journal.pone.0011276","article-title":"Towards the rational design of a candidate vaccine against pregnancy associated malaria: conserved sequences of the DBL6epsilon domain of VAR2CSA.","volume":"5","author":"C Badaut","year":"2010","journal-title":"PLoS One"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1051\/parasite\/2008153515","article-title":"Towards a vaccine against pregnancy-associated malaria.","volume":"15","author":"N Tuikue Ndam","year":"2008","journal-title":"Parasite"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.ijpara.2006.11.011","article-title":"Pregnancy-associated malaria: parasite binding, natural immunity and vaccine development.","volume":"37","author":"B Gamain","year":"2007","journal-title":"Int J Parasitol"}],"container-title":["PLoS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1002451","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,7,5]],"date-time":"2020-07-05T20:39:13Z","timestamp":1593981553000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1002451"}},"subtitle":[],"editor":[{"given":"Rustom","family":"Antia","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2012,4,12]]},"references-count":64,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2012,4,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1002451","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,4,12]]}}}