Induction of strain-transcending antibodies against group A PfEMP1 surface antigens from virulent malaria parasites

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Ghumra, Ashfaq ^a   Semblat, Jean Philippe ^a   Ataide, Ricardo ^a   Kifude, Carolyne ^a,b   Adams, Yvonne ^a   Claessens, Antoine ^a   Anong, Damian N ^c   Bull, Peter C ^b   Fennell, Clare ^a   Arman, Monica ^a   Amambua Ngwa, Alfred ^d   Walther, Michael ^d   Conway, David J ^d   Kassambara, Lalla ^e   Doumbo, Ogobara K ^e   Raza, Ahmed ^a   Rowe, J Alexandra ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^c UNIVERSITY OF BUEA   (Cameroon)

^d MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^e UNIVERSITY OF BAMAKO   (Mali)

Author keywords

[No Author keywords available]

Indexed keywords

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

ARTICLE; CELL ADHESION; CONTROLLED STUDY; CROSS REACTION; ERYTHROCYTE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; MALARIA FALCIPARUM; NONHUMAN; PARASITE ISOLATION; PARASITE VIRULENCE; PHAGOCYTOSIS; PHENOTYPE; PLASMODIUM FALCIPARUM; ROSETTE FORMATION; SPECIES DIVERSITY; AFRICA SOUTH OF THE SAHARA; ANIMAL; CLINICAL TRIAL; FEMALE; IMMUNOLOGY; MALE; MULTICENTER STUDY; PARASITOLOGY; PROTEIN TERTIARY STRUCTURE; RABBIT;

ORYCTOLAGUS CUNICULUS; PLASMODIUM FALCIPARUM;

AFRICA SOUTH OF THE SAHARA; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ERYTHROCYTES; FEMALE; HUMANS; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RABBITS;

EID: 84861220382     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002665     Document Type: Article

References (88)

1. Rappuoli R, Aderem A, (2011) A 2020 vision for vaccines against HIV, tuberculosis and malaria. Nature 473: 463-469.
2. Hviid L, (2010) The role of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Hum Vaccin 6: 84-89.
3. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, et al. (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022.
4. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, et al. (2007) Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45.
5. Barry AE, Leliwa-Sytek A, Tavul L, Imrie H, Migot-Nabias F, et al. (2007) Population genomics of the immune evasion (var) genes of Plasmodium falciparum. PLoS Pathog 3: e34.
6. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T, (2010) Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. PLoS Comput Biol 6: e1000933.
7. Kyes S, Horrocks P, Newbold C, (2001) Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 55: 673-707.
8. Chen DS, Barry AE, Leliwa-Sytek A, Smith TA, Peterson I, et al. (2011) A molecular epidemiological study of var gene diversity to characterize the reservoir of Plasmodium falciparum in humans in Africa. PLoS One 6: e16629.
9. Good MF, Doolan DL, (2010) Malaria vaccine design: immunological considerations. Immunity 33: 555-566.
10. Pierce SK, Miller LH, (2009) World Malaria Day 2009: what malaria knows about the immune system that immunologists still do not. J Immunol 182: 5171-5177.
11. Newbold CI, Pinches R, Roberts DJ, Marsh K, (1992) Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Exp Parasitol 75: 281-292.
12. Vigan-Womas I, Guillotte M, Juillerat A, Vallieres C, Lewit-Bentley A, et al. (2011) Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS One 6: e16544.
13. Ghumra A, Khunrae P, Ataide R, Raza A, Rogerson SJ, et al. (2011) Immunisation with recombinant PfEMP1 domains elicits functional rosette-inhibiting and phagocytosis-inducing antibodies to Plasmodium falciparum. PLoS One 6: e16414.
14. Langhorne J, Ndungu FM, Sponaas AM, Marsh K, (2008) Immunity to malaria: more questions than answers. Nat Immunol 9: 725-732.
15. Marsh K, Howard RJ, (1986) Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 231: 150-153.
16. Bull PC, Kortok M, Kai O, Ndungu F, Ross A, et al. (2000) Plasmodium falciparum-IEs: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. J Infect Dis 182: 252-259.
17. Nielsen MA, Staalsoe T, Kurtzhals JA, Goka BQ, Dodoo D, et al. (2002) Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. J Immunol 168: 3444-3450.
18. Kraemer SM, Smith JD, (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9: 374-380.
19. Rowe JA, Claessens A, Corrigan RA, Arman M, (2009) Adhesion of Plasmodium falciparum-IEs to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 11: e16.
20. Robinson BA, Welch TL, Smith JD, (2003) Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol 47: 1265-1278.
21. Janes JH, Wang CP, Levin-Edens E, Vigan-Womas I, Guillotte M, et al. (2011) Investigating the Host Binding Signature on the Plasmodium falciparum PfEMP1 Protein Family. PLoS Pathog 7: e1002032.
22. Rowe JA, Moulds JM, Newbold CI, Miller LH, (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
23. Vigan-Womas I, Guillotte M, Le Scanf C, Igonet S, Petres S, et al. (2008) 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. Infect Immun 76: 5565-5580.
24. Udomsangpetch R, Wahlin B, Carlson J, Berzins K, Torii M, et al. (1989) Plasmodium falciparum-IEs form spontaneous erythrocyte rosettes. J Exp Med 169: 1835-1840.
25. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, et al. (1992) Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357: 689-692.
26. Kirchgatter K, Portillo Hdel A, (2002) Association of severe noncerebral Plasmodium falciparum malaria in Brazil with expressed PfEMP1 DBL1 alpha sequences lacking cysteine residues. Mol Med 8: 16-23.
27. Kyriacou HM, Stone GN, Challis RJ, Raza A, Lyke KE, et al. (2006) Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Mol Biochem Parasitol 150: 211-218.
28. Rottmann M, Lavstsen T, Mugasa JP, Kaestli M, Jensen AT, et al. (2006) Differential Expression of var Gene Groups Is Associated with Morbidity Caused by Plasmodium falciparum Infection in Tanzanian Children. Infect Immun 74: 3904-3911.
29. Warimwe GM, Keane TM, Fegan G, Musyoki JN, Newton CR, et al. (2009) Plasmodium falciparum var gene expression is modified by host immunity. Proc Natl Acad Sci U S A 106: 21801-21806.
30. 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: 1179-1190.
31. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, et al. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336: 1457-1460.
32. Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, et al. (1992) Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg 46: 503-510.
33. Rowe A, Obeiro J, Newbold CI, Marsh K, (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63: 2323-2326.
34. Rowe JA, Obiero J, Marsh K, Raza A, (2002) Positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am J Trop Med Hyg 66: 458-460.
35. Doumbo OK, Thera MA, Kone AK, Raza A, Tempest LJ, et al. (2009) High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am J Trop Med Hyg 81: 987-993.
36. Le Scanf C, Vigan-Womas I, Contamin H, Guillotte M, Bischoff E, et al. (2008) Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey. Microbes Infect 10: 447-451.
37. Kaul DK, Roth EFJ, Nagel RL, Howard RJ, Handunnetti SM, (1991) Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78: 812-819.
38. Cockburn IA, Mackinnon MJ, O'Donnell A, Allen SJ, Moulds JM, et al. (2004) A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc Natl Acad Sci U S A 101: 272-277.
39. Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, et al. (2007) Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci U S A 104: 17471-17476.
40. Scholander C, Treutiger CJ, Hultenby K, Wahlgren M, (1996) Novel fibrillar structure confers adhesive property to malaria-IEs. Nat Med 2: 204-208.
41. Rowe JA, Shafi J, Kai OK, Marsh K, Raza A, (2002) Nonimmune IgM, but not IgG binds to the surface of Plasmodium falciparum-IEs and correlates with rosetting and severe malaria. Am J Trop Med Hyg 66: 692-699.
42. Clough B, Abiola Atilola F, Black J, Pasvol G, (1998) Plasmodium falciparum: The Importance of IgM in the Rosetting of Parasite-IEs. Exp Parasitol 89: 129-132.
43. Somner EA, Black J, Pasvol G, (2000) Multiple human serum components act as bridging molecules in rosette formation by Plasmodium falciparum-IEs. Blood 95: 674-682.
44. Barfod L, Dalgaard MB, Pleman ST, Ofori MF, Pleass RJ, et al. (2011) Evasion of immunity to Plasmodium falciparum malaria by IgM masking of protective IgG epitopes in IE surface-exposed PfEMP1. Proc Natl Acad Sci U S A 108: 12485-12490.
45. Claessens A, Ghumra A, Gupta AP, Mok S, Bozdech Z, et al. (2011) Design of a variant surface antigen-supplemented microarray chip for whole transcriptome analysis of multiple Plasmodium falciparum cytoadherent strains, and identification of strain-transcendent rif and stevor genes. Malar J 10: 180.
46. Creasey AM, Staalsoe T, Raza A, Arnot DE, Rowe JA, (2003) Nonspecific immunoglobulin M binding and chondroitin sulfate A binding are linked phenotypes of Plasmodium falciparum isolates implicated in malaria during pregnancy. Infect Immun 71: 4767-4771.
47. Fried M, Duffy PE, (1996) Adherence of Plasmodium falciparum to chondroitin sulphate A in the human placenta. Science 272: 1502-1504.
48. Handunnetti SM, Gilladoga AD, van Schravendijk MR, Nakamura K, Aikawa M, et al. (1992) Purification and in vitro selection of rosette-positive (R+) and rosette-negative (R-) phenotypes of knob-positive Plasmodium falciparum parasites. Am J Trop Med Hyg 46: 371-381.
49. Semblat JP, Raza A, Kyes SA, Rowe JA, (2006) Identification of Plasmodium falciparum var1CSA and var2CSA domains that bind IgM natural antibodies. Mol Biochem Parasitol 146: 192-197.
50. Ghumra A, Semblat JP, McIntosh RS, Raza A, Rasmussen IB, et al. (2008) Identification of residues in the Cmu4 domain of polymeric IgM essential for interaction with Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1). J Immunol 181: 1988-2000.
51. Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH, (2000) Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 110: 293-310.
52. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, et al. (1995) Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitised human erythrocytes. Cell 82: 77-87.
53. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, et al. (2004) Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200: 1197-1203.
54. Magistrado P, Salanti A, Tuikue Ndam NG, Mwakalinga SB, Resende M, et al. (2008) VAR2CSA expression on the surface of placenta-derived Plasmodium falciparum-IEs. J Infect Dis 198: 1071-1074.
55. Leech JH, Barnwell JW, Miller LH, Howard RJ, (1984) Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum IEs. J Exp Med 159: 1567-1575.
56. Barragan A, Kremsner PG, Weiss W, Wahlgren M, Carlson J, (1998) Age-related buildup of humoral immunity against epitopes for rosette formation and agglutination in African areas of malaria endemicity. Infect Immun 66: 4783-4787.
57. Avril M, Kulasekara BR, Gose SO, Rowe C, Dahlback M, et al. (2008) Evidence for globally shared, cross-reacting polymorphic epitopes in the pregnancy-associated malaria vaccine candidate VAR2CSA. Infect Immun 76: 1791-1800.
58. Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F, et al. (2010) Chondroitin sulfate A-adhering Plasmodium falciparum-IEs express functionally important antibody epitopes shared by multiple variants. J Immunol 185: 7553-7561.
59. Trimnell AR, Kraemer SM, Mukherjee S, Phippard DJ, Janes JH, et al. (2006) Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria. Mol Biochem Parasitol 148: 169-180.
60. Krause DR, Gatton ML, Frankland S, Eisen DP, Good MF, et al. (2007) Characterization of the antibody response against Plasmodium falciparum erythrocyte membrane protein 1 in human volunteers. Infect Immun 75: 5967-5973.
61. Bull PC, Lowe BS, Kortok M, Marsh K, (1999) Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect Immun 67: 733-739.
62. Chattopadhyay R, Sharma A, Srivastava VK, Pati SS, Sharma SK, et al. (2003) Plasmodium falciparum infection elicits both variant-specific and cross-reactive antibodies against variant surface antigens. Infect Immun 71: 597-604.
63. Elliott SR, Payne PD, Duffy MF, Byrne TJ, Tham WH, et al. (2007) Antibody recognition of heterologous variant surface antigens after a single Plasmodium falciparum infection in previously naive adults. Am J Trop Med Hyg 76: 860-864.
64. 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: 340-343.
65. 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: 748-755.
66. Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, et al. (2001) Platelet-mediated clumping of Plasmodium falciparum-IEs is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci U S A 98: 1805-1810.
67. Mayor A, Hafiz A, Bassat Q, Rovira-Vallbona E, Sanz S, et al. (2011) Association of severe malaria outcomes with platelet-mediated clumping and adhesion to a novel host receptor. PLoS One 6: e19422.
68. Ochola LB, Siddondo BR, Ocholla H, Nkya S, Kimani EN, et al. (2011) Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS One 6: e14741.
69. Arman M, Raza A, Tempest LJ, Lyke KE, Thera MA, et al. (2007) Platelet-Mediated Clumping of Plasmodium falciparum IEs Is Associated with High Parasitemia but Not Severe Clinical Manifestations of Malaria in African Children. Am J Trop Med Hyg 77: 943-946.
70. Arman M, Rowe JA, (2008) Experimental conditions affect the outcome of Plasmodium falciparum platelet-mediated clumping assays. Malar J 7: 243.
71. Rogerson SJ, Tembenu R, Dobano C, Plitt S, Taylor TE, et al. (1999) Cytoadherence characteristics of Plasmodium falciparum-IEs from Malawian children with severe and uncomplicated malaria. Am J Trop Med Hyg 61: 467-472.
72. Fry AE, Auburn S, Diakite M, Green A, Richardson A, et al. (2008) Variation in the ICAM1 gene is not associated with severe malaria phenotypes. Genes Immun 9: 462-469.
73. Carlson J, Wahlgren M, (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176: 1311-1317.
74. Fry AE, Griffiths MJ, Auburn S, Diakite M, Forton JT, et al. (2008) Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 17: 567-576.
75. Czajkowsky DM, Salanti A, Ditlev SB, Shao Z, Ghumra A, et al. (2010) IgM, Fc mu Rs, and malarial immune evasion. J Immunol 184: 4597-4603.
76. Flick K, Scholander C, Chen Q, Fernandez V, Pouvelle B, et al. (2001) Role of nonimmune IgG bound to PfEMP1 in placental malaria. Science 293: 2098-2100.
77. Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI, (2004) Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci U S A 101: 11129-11134.
78. Albrecht L, Moll K, Blomqvist K, Normark J, Chen Q, et al. (2011) var gene transcription and PfEMP1 expression in the rosetting and cytoadhesive Plasmodium falciparum clone FCR3S1.2. Malar J 10: 17.
79. Corrigan RA, Rowe JA, (2010) Strain variation in early innate cytokine induction by Plasmodium falciparum. Parasite Immunol 32: 512-527.
80. Deans AM, Lyke KE, Thera MA, Plowe CV, Kone A, et al. (2006) Low multiplication rates of African Plasmodium falciparum isolates and lack of association of multiplication rate and red blood cell selectivity with malaria virulence. Am J Trop Med Hyg 74: 554-563.
81. Rowe JA, Scragg IG, Kwiatkowski D, Ferguson DJP, Carucci DJ, et al. (1998) Implications of mycoplasma contamination in Plasmodium falciparum cultures and methods for its detection and eradication. Mol Biochem Parasitol 92: 177-180.
82. Farnert A, Arez AP, Babiker HA, Beck HP, Benito A, et al. (2001) Genotyping of Plasmodium falciparum infections by PCR: a comparative multicentre study. Trans R Soc Trop Med Hyg 95: 225-232.
83. Claessens A, Rowe JA, (2012) Selection of Plasmodium falciparum Parasites for Cytoadhesion to Human Brain Endothelial Cells. J Vis Exp 59: e3122.
84. Newbold C, Warn P, Black G, Berendt A, Craig A, et al. (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57: 389-398.
85. Bull PC, Buckee CO, Kyes S, Kortok MM, Thathy V, et al. (2008) Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks. Mol Microbiol 68: 1519-1534.
86. Kraemer SM, Gupta L, Smith JD, (2003) New tools to identify var sequence tags and clone full-length genes using type-specific primers to Duffy binding-like domains. Mol Biochem Parasitol 129: 91-102.
87. Heddini A, Treutiger CJ, Wahlgren M, (1998) Enrichment of immunoglobulin binding Plasmodium falciparum-IEs using anti-immunoglobulin-coated magnetic beads. Am J Trop Med Hyg 59: 663-666.
88. Mu J, Awadalla P, Duan J, McGee KM, Joy DA, et al. (2005) Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol 3: e335.