Hypervariable antigen genes in malaria have ancient roots

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Zilversmit, Martine M ^a,b,c,d   Chase, Ella K ^c   Chen, Donald S ^b   Awadalla, Philip ^d   Day, Karen P ^b   McVean, Gil ^c,e  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF MONTREAL   (Canada)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Balancing selection; Gene family evolution; Hidden Markov model; Malaria; Non allelic homologous recombination; PfEMP1; var genes

Indexed keywords

CONSERVATION GENETICS; GENE EXPRESSION; GENETIC DIFFERENTIATION; HOST-PARASITE INTERACTION; IMMUNE SYSTEM; MALARIA; PATHOLOGY; PROTEIN; RECOMBINATION; ROOT; VIRULENCE;

PLASMODIUM FALCIPARUM; PLASMODIUM REICHENOWI; PRIMATES;

ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANTIGENIC VARIATION; ARTICLE; CHEMISTRY; CLASSIFICATION; GENETIC VARIABILITY; GENETICS; HUMAN; IMMUNOLOGY; MALARIA; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; PLASMODIUM; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANTIGENIC VARIATION; ANTIGENS, PROTOZOAN; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; MALARIA; MEMBRANE PROTEINS; PHYLOGENY; PLASMODIUM; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT;

EID: 84878364260     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-110     Document Type: Article

References (35)

1. WHO, World Health Organization World Malaria Report 2011 http://www.who.int/malaria/world-malaria-report-2011/en/
2. A theoretical framework for the immunoepidemiology of Plasmodium falciparum malaria. Gupta S, Day KP, Parasite Immunol 1994 16 7 361 370 10.1111/j.1365-3024.1994.tb00361.x 7970875 (Pubitemid 24251685)
3. Molecular Aspects of Severe Malaria. Chen Q, Schlichtherle M, Wahlgren M, Clin Microbiol Rev 2000 13 3 439 450 10.1128/CMR.13.3.439-450.2000 10885986 (Pubitemid 30452616)
4. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, Christodoulou Z, Smith LM, Wang W, Levin E, Newbold CI, BMC Genomics 2007 8 45 10.1186/1471-2164-8-45 17286864 (Pubitemid 46358101)
5. Population Genomics of the Immune Evasion (var) Genes of Plasmodium falciparum. Barry AE, Leliwa-Sytek A, Tavul L, Imrie H, Migot-Nabias F, Brown SM, McVean GAV, Day KP, PLoS Pathog 2007 3 3 34 10.1371/journal.ppat.0030034 17367208 (Pubitemid 46535808)
6. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, Scherf A, Nature 2000 407 6807 1018 1022 10.1038/35039531 11069183
7. Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks. Bull PC, Buckee CO, Kyes S, Kortok MM, Thathy V, Guyah B, Stoute JA, Newbold CI, Marsh K, Mol Microbiol 2008 68 6 1519 1534 10.1111/j.1365-2958.2008.06248.x 18433451 (Pubitemid 351725260)
8. Origins and evolution of antigenic diversity in malaria parasites. Ferreira MU, Zilversmit M, Wunderlich G, Curr Mol Med 2007 7 6 588 602 10.2174/156652407781695756 17896995 (Pubitemid 47618055)
9. Evolution of allelic dimorphism in malarial surface antigens. Roy SW, Ferreira MU, Hartl DL, Heredity 2006 100 2 103 110 17021615 (Pubitemid 351156863)
10. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Lavstsen T, Salanti A, Jensen ATR, Theander TG, Copenhagen D, Malar J 2003 2 27 10.1186/1475-2875-2-27 14565852
11. Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria. Trimnell AR, Kraemer SM, Mukherjee S, Phippard DJ, Janes JH, Flamoe E, Su XZ, Awadalla P, Smith JD, Mol Biochem Parasitol 2006 148 2 169 180 10.1016/j.molbiopara.2006.03.012 16697476 (Pubitemid 43946513)
12. Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA. Bockhorst J, Lu F, Janes JH, Keebler J, Gamain B, Awadalla P, Su X-z, Samudrala R, Jojic N, Smith JD, Mol Biochem Parasitol 2007 155 2 103 112 10.1016/j.molbiopara.2007.06.007 17669514 (Pubitemid 47238448)
13. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Salanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, Arnot DE, Hviid L, Theander TG, Mol Microbiol 2003 49 1 179 191 10.1046/j.1365-2958.2003.03570.x 12823820 (Pubitemid 36792013)
14. A molecular epidemiological study of var gene diversity to characterize the reservoir of Plasmodium falciparum in humans in Africa. Chen DS, Barry AE, Leliwa-Sytek A, Smith TA, Peterson I, Brown SM, Migot-Nabias F, Deloron P, Kortok MM, Marsh K, PLoS One 2011 6 2 16629 10.1371/journal.pone.0016629 21347415
15. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Su X, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE, Cell 1995 82 1 89 100 10.1016/0092-8674(95)90055-1 7606788
16. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango J-BN, Sanz CM, Morgan DB, Locatelli S, Nature 2010 467 7314 420 425 10.1038/nature09442 20864995
17. Modeling Linkage Disequilibrium and Identifying Recombination Hotspots Using Single-Nucleotide Polymorphism Data. Li N, Stephens M, Genetics 2003 165 2213 2233 14704198 (Pubitemid 38040302)
18. Durbin R, Eddy SR, Krogh A, Michison G, Biological sequence analysis: probabilistic models of proteins and nucleic acids Cambridge, UK: Cambridge University Press 1998
19. On the abundance, amino acid composition, and evolutionary dynamics of low-complexity regions in proteins. DePristo MA, Zilversmit MM, Hartl DL, Gene 2006 378 19 30 16806741 (Pubitemid 44108462)
20. Duplication, gene conversion, and genetic diversity in the species-specific acyl-CoA synthetase gene family of Plasmodium falciparum. Bethke LL, Zilversmit M, Nielsen K, Daily J, Volkman SK, Ndiaye D, Lozovsky ER, Hartl DL, Wirth DF, Mol Biochem Parasitol 2006 150 1 10 10.1016/j.molbiopara. 2006.06.004 16860410 (Pubitemid 44332573)
21. var genes, PfEMP1 and the human host. Flick K, Chen Q, Mol Biochem Parasitol 2004 134 1 3 9 10.1016/j.molbiopara.2003.09.010 14747137 (Pubitemid 38121512)
22. Early origin and recent expansion of Plasmodium falciparum. Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Science 2003 300 5617 318 321 10.1126/science.1081449 12690197 (Pubitemid 36433721)
23. Plasmodium falciparum Erythrocyte Membrane Protein 1 Diversity in Seven Genomes: Divide and Conquer. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T, PLoS Comput Biol 2010 6 9 1000933 10.1371/journal.pcbi.1000933 20862303
24. Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Zilversmit MM, Volkman SK, DePristo MA, Wirth DF, Awadalla P, Hartl DL, Mol Biol Evol 2010 27 9 2198 2209 10.1093/molbev/ msq108 20427419
25. Hartl DL, Clark AG, Principles of Population Genetics, 4th Edition Sunderland, MA: Sinauer Associates, Inc. 4 2007
26. Population Biology of Antigen Presentation by MHC Class I Molecules. Parham P, Ohta T, Science 1996 272 5258 67 10.1126/science.272.5258.67 8600539
27. Association of Malaria Parasite Population Structure, HLA, and Immunological Antagonism. Gilbert SC, Plebanski M, Gupta S, Morris J, Cox M, Aidoo M, Kwiatkowski D, Greenwood BM, Whittle HC, Hill AVS, Science 1998 279 5354 1173 1177 10.1126/science.279.5354.1173 9469800 (Pubitemid 28164361)
28. A New Malaria Agent in African Hominids. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, Leroy E, Renaud F, PLoS Pathog 2009 5 5 1000446 10.1371/journal.ppat.1000446 19478877
29. The Importance of the Natural History of Malaria (E-Letter). Zilversmit MM, Awadalla P, Science 2011 vol. http://www.sciencemag.org/content/329/5999/ 1586/reply
30. Maddison DR, Maddison WP, MacClade 4: Analysis of Phylogeny and Character Evolution MA, USA: Sinauer Associates, Sunderland 2000
31. Clustal W and Clustal X version 2.0. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Bioinformatics 2007 23 21 2947 10.1093/bioinformatics/btm404 17846036 (Pubitemid 350162903)
32. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Edgar RC, Nucleic Acids Res 2004 32 5 1792 1797 10.1093/nar/gkh340 15034147 (Pubitemid 38832724)
33. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, Syst Biol 2010 59 3 307 321 10.1093/sysbio/syq010 20525638
34. An improved general amino acid replacement matrix. Le SQ, Gascuel O, Mol Biol Evol 2008 25 7 1307 1320 10.1093/molbev/msn067 18367465 (Pubitemid 351882003)
35. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Smith SA, Dunn CW, Bioinformatics 2008 24 5 715 716 10.1093/ bioinformatics/btm619 18227120 (Pubitemid 351321218)