The antigenic switching network of Plasmodium falciparum and its implications for the immuno-epidemiology of malaria

eLife

Volumn 2013, Issue 2, 2013, Pages

  Noble, Robert ^a   Christodoulou, Zóe ^b   Kyes, Sue ^b   Pinches, Robert ^b   Newbold, Chris I ^b   Recker, Mario ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA;

ALGORITHM; ANTIGENIC VARIATION; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE CONVERSION; GENE EXPRESSION; GENE SWITCHING; GENETIC TRANSCRIPTION; GROWTH RATE; MALARIA; MODEL; NONHUMAN; NORTHERN BLOTTING; PLASMODIUM FALCIPARUM; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SIGNAL NOISE RATIO; SIMULATION; VALIDATION PROCESS; ANIMAL; CHROMOSOME MAP; GENETICS; HUMAN; IMMUNOLOGY; MALARIA, FALCIPARUM; PROMOTER REGION;

ANIMALS; ANTIGENIC VARIATION; CHROMOSOME MAPPING; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84884685300     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01074     Document Type: Article

References (61)

1. Avril M, Tripathi AK, Brazier AJ, Andisi C, Janes JH, Soma VL, et al. 2012. A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells. Proc Natl Acad Sci USA 109:E1782-90. doi: 10.1073/pnas.1120534109.
2. Blomqvist K, Normark J, Nilsson D, Ribacke U, Orikiriza J, Trillkott P, et al. 2010. var gene transcription dynamics in Plasmodium falciparum patient isolates. Mol Biochem Parasitol 170:74-83. doi: 10.1016/j.molbiopara.2009.12.002.
3. Boone KE, Watters DA. 1995. The incidence of malaria after splenectomy in Papua New Guinea. BMJ 311:1273. doi: 10.1136/bmj.311.7015.1273.
4. Buckee CO, Recker M. 2012. Evolution of the multi-domain structures of virulence genes in the human malaria parasite, Plasmodium falciparum. PLOS Comput Biol 8:e1002451. doi: 10.1371/journal.pcbi.1002451.
5. Buckee CO, Bull PC, Gupta S. 2009. Inferring malaria parasite population structure from serological networks. Proc Biol Sci 276:477-85. doi: 10.1098/rspb.2008.1122.
6. Buffet PA, Safeukui I, Milon G, Mercereau-Puijalon O, David PH. 2009. Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr Opin Hematol 16:157-64. doi: 10.1097/MOH.0b013e32832a1d4b.
7. Bull PC, Berriman M, Kyes S, Quail MA, Hall N, Kortok MM, et al. 2005. Plasmodium falciparum variant surface antigen expression patterns during malaria. PLOS Pathog 1:202-13. doi: 10.1371/journal.ppat.0010026.
8. Bull PC, Buckee CO, Kyes S, Kortok MM, Thathy V, Guyah B, et al. 2008. Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks. Mol Microbiol 68:1519-34. doi: 10.1111/j.1365-2958.2008.06248.x.
9. Cham GK, Turner L, Kurtis JD, Mutabingwa T, Fried M, et al. 2010. Hierarchical, domain type-specific acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 in Tanzanian children. Infect Immun 78:4653-9. doi: 10.1128/IAI.00593-10.
10. Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, Andisi C, et al. 2012. A subset of group a-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci USA 109:E1772-81. doi: 10.1073/pnas.1120461109.
11. Deitsch KW, del Pinal A, Wellems TE. 1999. Intra-cluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum. Mol Biochem Parasitol 101:107-16. doi: 10.1016/S0166-6851(99)00062-6.
12. Dzikowski R, Frank M, Deitsch K. 2006. Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLOS Pathog 2:e22. doi: 10.1371/journal.ppat.0020022.
13. Enderes C, Kombila D, Dal-Bianco M, Dzikowski R, Kremsner P, Frank M. 2011. Var gene promoter activation in clonal Plasmodium falciparum isolates follows a hierarchy and suggests a conserved switching program that is independent of genetic background. J Infect Dis 204:1620-31. doi: 10.1093/infdis/jir594.
14. Fastman Y, Noble R, Recker M, Dzikowski R. 2012. Erasing the epigenetic memory and beginning to switch-the onset of antigenic switching of var genes in Plasmodium falciparum. PLOS ONE 7:e34168. doi: 10.1371/journal.pone.0034168.
15. Frank M, Dzikowski R, Amulic B, Deitsch K. 2007. Variable switching rates of malaria virulence genes are associated with chromosomal position. Mol Microbiol 64:1486-98. doi: 10.1111/j.1365-2958.2007.05736.x.
16. Frank M, Kirkman L, Costantini D, Sanyal S, Lavazec C, Templeton TJ, et al. 2008. Frequent recombination events generate diversity within the multi-copy variant antigen gene families of Plasmodium falciparum. Int J Parasitol 38:1099-109. doi: 10.1016/j.ijpara.2008.01.010.
17. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, et al. 2000. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407:1018-22. doi: 10.1038/35039531.
18. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511. doi: 10.1038/nature01097.
19. Gottipati P, Helleday T. 2009. Transcription-associated recombination in eukaryotes: link between transcription, replication and recombination. Mutagenesis 24:203-10. doi: 10.1093/mutage/gen072.
20. Greenwood BM, Bradley AK, Greenwood AM, Byass P, Jammeh K, Marsh K, et al. 1987. Mortality and morbidity from malaria among children in a rural area of the Gambia, West Africa. Trans R Soc Trop Med Hyg 81:478-86. doi: 10.1016/0035-9203(87)90170-2.
21. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C. 1999. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5:340-3. doi: 10.1038/6560.
22. Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI. 2004. Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci USA 101:11129-34. doi: 10.1073/pnas.0402347101.
23. Jensen AT, Magistrado P, Sharp S, Joergensen L, Lavstsen T, et al. 2004. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group a var genes. J Exp Med 199:1179-90. doi: 10.1084/jem.20040274.
24. Kaestli M, Cockburn IA, Cortes A, Baea K, Rowe JA, Beck HP. 2006. Virulence of malaria is associated with differential expression of Plasmodium falciparum var gene subgroups in a case-control study. J Infect Dis 193:1567-74. doi: 10.1086/503776.
25. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, Christodoulou Z, et al. 2007. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8:45. doi: 10.1186/1471-2164-8-45.
26. Kraemer SM, Smith JD. 2006. A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9:374-80. doi: 10.1016/j.mib.2006.06.006.
27. Kyes S, Christodoulou Z, Pinches R, Kriek N, Horrocks P, Newbold C. 2007. Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. Mol Microbiol 63:1237-47. doi: 10.1111/j.1365-2958.2007.05587.x.
28. Kyes S, Pinches R, Newbold C. 2000. A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol Biochem parasitol 105:311-5. doi: 10.1016/S0166-6851(99)00193-0.
29. Kyriacou HM, Stone GN, Challis RJ, Raza A, Lyke KE, Thera MA, et al. 2006. Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Mol Biochem Parasitol 150:211-8. doi: 10.1016/j.molbiopara.2006.08.005.
30. Lambros C, Vanderberg JP. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:418-20. doi: 10.2307/3280287.
31. Lavstsen T, Magistrado P, Hermsen CC, Salanti A, Jensen AT, Sauerwein R, et al. 2005. Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar J 4:21. doi: 10.1186/1475-2875-4-21.
32. Lavstsen T, Salanti A, Jensen ATR, Arnot DE, Theander TG. 2003. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2:27. doi: 10.1186/1475-2875-2-27.
33. Lavstsen T, Turner L, Saguti F, Magistrado P, Rask TS, Jespersen JS, et al. 2012. Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children. Proc Natl Acad Sci USA 109:E1791-800. doi: 10.1073/pnas.1120455109.
34. Marsh K. 1992. Malaria-a neglected disease? Parasitology 104(Suppl):S53-69. doi: 10.1017/S0031182000075247.
35. Marsh K, Snow RW. 1997. Host-parasite interaction and morbidity in malaria endemic areas. Philos Trans R Soc Lond B Biol Sci 352:1385-94. doi: 10.1098/rstb.1997.0124.
36. Newman MEJ. 2001. Scientific collaboration networks. II. shortest paths, weighted networks, and centrality. Phys Rev E Stat Nonlin Soft Matter Phys 64:016132. doi: 10.1103/PhysRevE.64.016132.
37. Noble R, Recker M. 2012. A statistically rigorous method for determining antigenic switching networks. PLOS ONE 7:e39335. doi: 10.1371/journal.pone.0039335.
38. Ockenhouse CF, Ho M, Tandon NN, Vanseventer GA, Shaw S, White NJ, et al. 1991. Molecular-basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria-differential adhesion of infected erythrocytes to CD36 and ICAM-1. J Infect Dis 164:163-169. doi: 10.1093/infdis/164.1.163.
39. Opsahl T. 2009. Structure and evolution of weighted networks. p. 104-122 [Online]. Available: http://toreopsahl.com/publications/thesis/.
40. Peters J, Fowler E, Gatton M, Chen N, Saul A, Cheng Q. 2002. High diversity and rapid changeover of expressed var genes during the acute phase of Plasmodium falciparum infections in human volunteers. Proc Natl Acad Sci USA 99:10 689-94. doi: 10.1073/pnas.162349899.
41. Peters JM, Fowler EV, Krause DR, Cheng Q, Gatton ML. 2007. Differential changes in Plasmodium falciparum var transcription during adaptation to culture. J Infect Dis 195:748-55. doi: 10.1086/511436.
42. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. doi: 10.1093/nar/29.9.e45.
43. Pongponratn E, Riganti M, Punpoowong B, Aikawa M. 1991. Microvascular sequestration of parasitized erythrocytes in human falciparum-malaria-a pathological study. Am J Trop Med Hyg 44:168-75.
44. Prado F, Aguilera A. 2005. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J 24:1267-76. doi: 10.1038/sj.emboj.7600602.
45. Rask TS, Hansen DA, Theander TG, Pedersen AG, Lavstsen T. 2010. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. Plos Comput Biology 6:e1000933. doi: 10.1371/journal.pcbi.1000933.
46. Recker M, Buckee CO, Serazin A, Kyes S, Pinches R, Christodoulou Z, et al. 2011. Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. Plos Pathog 7:e1001306. doi: 10.1371/journal.ppat.1001306.
47. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, Marsh K, et al. 1992. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357:689-92. doi: 10.1038/357689a0.
48. Rottmann M, Lavstsen T, Mugasa JP, Kaestli M, Jensen AT, Muller D, et al. 2006. Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children. Infect Immun 74:3904-11. doi: 10.1128/IAI.02073-05.
49. Rowe JA, Claessens A, Corrigan RA, Arman M. 2009. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 11:e16. doi: 10.1017/S1462399409001082.
50. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, Magistrado P, et al. 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200:1197-203. doi: 10.1084/jem.20041579.
51. Salanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, Arnot DE, et al. 2003. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49:179-191. doi: 10.1046/j.1365-2958.2003.03570.x.
52. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, et al. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101-10. doi: 10.1016/0092-8674(95)90056-X.
53. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, et al. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82:89-100. doi: 10.1016/0092-8674(95)90055-1.
54. Taylor HM, Kyes SA, Newbold CI. 2000. Var gene diversity in Plasmodium falciparum is generated by frequent recombination events. Mol Biochem Parasitol 110:391-7. doi: 10.1016/S0166-6851(00)00286-3.
55. Trager W, Jensen JB. 1976. Human malaria parasites in continuous culture. Science 193:673-675. doi: 10.1126/science.781840.
56. Tran TM, Li S, Doumbo S, Doumtabe D, Huang CY, Dia S, et al. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 57:40-7. doi: 10.1093/cid/cit174.
57. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71-4. doi: 10.1093/nar/gkm306.
58. Ward CP, Clottey GT, Dorris M, Ji DD, Arnot DE. 1999. Analysis of Plasmodium falciparum PfEMP-1/var genes suggests that recombination rearranges constrained sequences. Mol Biochem Parasitol 102:167-77. doi: 10.1016/S0166-6851(99)00106-1.
59. Warimwe GM, Keane TM, Fegan G, Musyoki JN, Newton CR, Pain A, et al. 2009. Plasmodium falciparum var gene expression is modified by host immunity. Proc Natl Acad Sci USA 106:21 801-6. doi: 10.1073/pnas.0907590106.
60. Wunderlich G, Alves FP, Golnitz U, Tada MS, Camargo EF, Pereira-da Silva LH. 2005. Rapid turnover of Plasmodium falciparum var gene transcripts and genotypes during natural non-symptomatic infections. Rev Inst Med Trop Sao Paulo 47:195-201. doi: 10.1590/S0036-46652005000400004.
61. Zhang Q, Zhang Y, Huang Y, Xue X, Yan H, Sun X, et al. 2011. From in vivo to in vitro: dynamic analysis of Plasmodium falciparum var gene expression patterns of patient isolates during adaptation to culture. PLOS ONE 6:e20591. doi: 10.1371/journal.pone.0020591.