Antibodies against PfEMP1, RIFIN, MSP3 and GLURP are acquired during controlled Plasmodium falciparum malaria infections in naïve volunteers

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Turner, Louise ^a   Wang, Christian W ^a   Lavstsen, Thomas ^a   Mwakalinga, Steven B ^a   Sauerwein, Robert W ^b   Hermsen, Cornelus C ^b   Theander, Thor G ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; ERYTHROCYTE MEMBRANE PROTEIN 1; ERYTHROCYTE MEMBRANE PROTEIN 1 ANTIBODY; GLUTAMATE RICH PROTEIN; GLUTAMATE RICH PROTEIN ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; MEMBRANE ANTIGEN; MEROZOITE SURFACE PROTEIN 3; MEROZOITE SURFACE PROTEIN 3 ANTIBODY; PARASITE ANTIBODY; RIFIN PROTEIN; RIFIN PROTEIN ANTIBODY; UNCLASSIFIED DRUG; GLUTAMATE RICH PROTEIN, PLASMODIUM; GLUTAMATE-RICH PROTEIN, PLASMODIUM; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 3, PLASMODIUM; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY; RIFIN PROTEIN, PLASMODIUM FALCIPARUM;

ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; HUMAN; HUMAN EXPERIMENT; IMMUNE RESPONSE; IMMUNOGENICITY; LIVER; MALARIA FALCIPARUM; MEROZOITE; NORMAL HUMAN; PARASITEMIA; ANIMAL; CHEMISTRY; CLINICAL TRIAL; GROWTH, DEVELOPMENT AND AGING; IMMUNIZATION; IMMUNOLOGY; LIFE CYCLE STAGE; PARASITOLOGY; PATHOLOGY; PLASMODIUM FALCIPARUM; PROTEIN TERTIARY STRUCTURE;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; HUMAN EXPERIMENTATION; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN G; LIFE CYCLE STAGES; LIVER; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; PLASMODIUM FALCIPARUM; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS;

EID: 83155183329     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029025     Document Type: Article

References (55)

1. Day KP, Marsh K, (1991) Naturally acquired immunity to Plasmodium falciparum. In: Ash C, Gallagher RB, eds. Immunol Today 12: A68-A71.
2. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C, (1995) Immunity to noncerebral severe malaria is acquired after one or two infections. Nat Med 5: 340-343.
3. Marsh K, Howard RJ, (1986) Antigens induced on erythrocytes by P. falciparum, expression of diverse and conserved determinants. Science 231: 150-153.
4. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, et al. (1998) Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nature Med 4: 358-360.
5. 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.
6. Giha HA, Staalsoe T, Dodoo D, Elhassan IM, Roper C, et al. (2000) Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immunol Lett 71: 117-126.
7. Sirima SB, Nebie I, Ouedraogo A, Tiono AB, Konate AT, et al. (2007) A Safety and immunogenicity of the Plasmodium falciparum merozoite surface protein-3 long synthetic peptide (MSP3-LSP) malaria vaccine in healthy, semi-immune adult males in Burkina Faso, West Africa. Vaccine 25: 2723-2732.
8. Jacobsen PH, Heegaard PMH, Koch C, Wasniowska K, Lemnge MM, et al. (1998) Identification of an Erythrocyte Binding Peptide from the Erythrocyte Binding Antigen, EBA-175, Which Blocks Parasite Multiplication and Induces Peptide-Blocking Antibodies. Infect Immun 66: 4203-4207.
9. Borre MB, Dziegiel M, Hogh B, Petersen E, Rieneck K, et al. (1991) Primary structure and localization of a conserved immunogenic Plasmodium falciparum glutamate rich protein (GLURP) expressed in both the preerythrocytic and erythrocytic stages of the vertebrate life cycle. Mol Biochem Parasitol 49: 119-132.
10. Baruch DI, Pasloske BL, Singh HB, Bi XH, Ma XC, et al. (1995) Cloning the Plasmodium falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82: 77-87.
11. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, et al. (1995) Switches in Expression of Plasmodium falciparum var Genes Correlate with Changes in Antigenic and Cytoadherent Phenotypes of Infected Erythrocytes. Cell 82: 101-110.
12. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, 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.
13. Salanti A, Dahlbäck 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.
14. Bachmann A, Esser C, Petter M, Predehl S, von Kalckreuth V, et al. (2009) Absence of erythrocyte sequestration and lack of multicopy gene family expression in Plasmodium falciparum from a splenectomized malaria patient. PLoS One 4: e7459.
15. Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G, et al. (1998) Stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol 97: 161-176.
16. Abdel-Latif MS, Khattab A, Lindenthal C, Kremsner PG, Klinkert MQ, (2002) Recognition of variant Rifin antigens by human antibodies induced during natural Plasmodium falciparum infections. Infect Immun 70: 7013-7021.
17. Dzikowski R, Frank M, Deitch K, (2006) Mutually Exclusive Expression of Virulence Genes by Malaria Parasites Is Regulated Independently of Antigen Production. PLoS Pathog 2: e22.
18. Voss TS, Healer J, Marty AJ, Duffy MF, Thompson JK, et al. (2006) A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439: 1004-1008.
19. Joergensen L, Bengtsson DC, Bengtsson A, Ronander E, Berger SS, et al. (2010) Surface co-expression of two different PfEMP1 antigens on single plasmodium falciparum-infected erythrocytes facilitates binding to ICAM1 and PECAM1. PLoS Pathog 6: e1001083.
20. 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 Biol 6: e1000933.
21. Kraemer SM, Smith JD, (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol Microbiol 50: 1527-1538.
22. 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.
23. Bull PC, Kortok M, Kai O, Ndungu F, Ross A, et al. (2000) Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. J Infect Dis 182: 252-259.
24. 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 Immun 168: 3444-3450.
25. Bull PC, Berriman M, Kyes S, Quail MA, Hall N, et al. (2005) Plasmodium falciparum variant surface antigen expression patterns during malaria. PLoS Pathog 1: e26.
26. Cham GKK, Turner L, Lusingu J, Vestergaard L, Mmbando BP, et al. (2009) Sequential, ordered acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 domains. J Immun 183: 3356-3363.
27. 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.
28. Rottmann M, Lavstsen T, Mugasa JP, Kaestli M, Jensen ATR, et al. (2006) Differential expression of var gene groups is associated with morbidity caused by P. falciparum infection in Tanzanian children. Infect. Immun 74: 3904-3911.
29. Lusingu JP, Jensen AT, Vestergaard LS, Minja DT, Dalgaard MB, et al. (2006) Levels of plasma immunoglobulin G with specificity against the cysteine-rich interdomain regions of a semiconserved Plasmodium falciparum erythrocyte membrane protein 1, VAR4, predict protection against malarial anemia and febrile episodes. Infect Immun 74: 2867-2875.
30. Magistrado PA, Lusingu J, Vestergaard LS, Lemnge M, Lavstsen T, et al. (2007) Immunoglobulin G antibody reactivity to a Group A Plasmodium falciparum erythrocyte membrane protein 1 and protection from P. falciparum malaria. Infect Immun 75: 2415-2420.
31. Falk N, Kaestli M, Qi W, Ott M, Baea K, et al. (2009) Analysis of Plasmodium falciparum var genes expressed in children from Papua New Guinea. J Infect Dis 200: 347-356.
32. Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, et al. (2009) The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int 58: 478-480.
33. Hermsen CC, Telgt DS, Linders EH, van de Locht LA, Eling WM, et al. (2001) Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol 118: 247-251.
34. Hermsen CC, de Vlas SJ, van Gemert GA, Telgt DSC, Verhage DF, et al. (2004) Testing vaccines in human experimental malaria: statistical analysis of parasitemia measured by a quantitative real-time polymerase chain reaction. Am J Trop Med Hyg 71: 196-201.
35. Verhage DF, Telgt DS, Bousema JT, Hermsen CC, van Gemert GJ, et al. (2005) Clinical outcome of experimental human malaria induced by Plasmodium falciparum infected mosquitoes. Neth J Med 63: 52-58.
36. McCall MB, Netea MG, Hermsen CC, Jansen T, Jacobs L, et al. (2007) Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. RWJ Immunol 179: 162-171.
37. Roestenberg M, McCall M, Hopman J, Wiersma J, Luty AJF, et al. (2009) Protection against a Malaria Challenge by Sporozoite Inoculation. N Engl J Med 361: 468-477.
38. Roestenberg M, Teirlinck AC, McCall M, Teelen K, Makamdop KN, et al. (2011) Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377: 1770-1776.
39. Heegaard ED, Qvortrup K, Christensen J, (2002) Baculovirus expression of erythrovirus V9 capsids and screening by ELISA: serologic cross-reactivity with erythrovirus B19. J Med Virol 66: 246-252.
40. Theisen M, Soe S, Brunstedt K, Follmann F, Bredmose L, et al. (2004) A Plasmodium falciparum GLURP-MSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine 22: 1188-1198.
41. Theisen M, Vuust J, Gottschau A, Jepsen S, Høgh B, (1995) Antigenicity and Immunogenicity of Recombinant Glutamate-Rich Protein of Plasmodium falciparum Expressed in Escherichia coli. Clin Diagn Lab Immunol 2: 30-34.
42. Salanti A, Resende M, Ditlev SB, Pinto VV, Dahlback M, et al. (2010) Several domains from VAR2CSA can induce Plasmodium falciparum adhesion-blocking antibodies. Malar J 9: 11.
43. Cham GKK, Kurtis J, Lusingu J, Theander TG, Jensen ATR, et al. (2008) A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malar J 7: 108.
44. Nielsen MA, Pinto VV, Resende M, Dahlback M, Ditlev SB, et al. (2009) Induction of adhesion-inhibitory antibodies against placental Plasmodium falciparum parasites by using single domains of VAR2CSA. Infect Immun 77: 2482-2487.
45. Wang CW, Magistrado PA, Nielsen MA, Theander TG, Lavstsen T, (2009) Preferential transcription of conserved rif genes in two phenotypically distinct Plasmodium falciparum parasite lines. Int J Parasitol 39: 655-664.
46. Lavstsen T, Magistrado P, Hermsen CC, Salanti A, Jensen AT, et al. (2005) Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar J 4: 21.
47. 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 naïve adults. Am J Trop Med Hyg 76: 860-864.
48. Joergensen L, Turner L, Magistrado P, Dahlbäck MA, Vestergaard LS, et al. (2006) Limited cross-reactivity among domains of the Plasmodium falciparum clone 3D7 erythrocyte membrane protein 1 family. Infect Immun 74: 6778-6784.
49. 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: 4653-4659.
50. Recker M, Nee S, Bull PC, Kinyanjui S, Marsh K, et al. (2004) Transient cross-reactive immune responses can orchestrate antigenic variation in malaria. Nature 429: 555-558.
51. Theisen M, Dodoo D, Toure-Balde A, Soe S, Corradin G, et al. (2001) Selection of glutamate-rich protein long synthetic peptides for vaccine development: antigenicity and relationship with clinical protection and immunogenicity. Infect Immun 69: 5223-5229.
52. Ong CS, Zhang KY, Eida SJ, Graves PM, Dow C, et al. (1990) The primary antibody response of malaria patients to Plasmodium falciparum sexual stage antigens which are potential transmission blocking vaccine candidates. Parasite Immunol 12: 447-456.
53. Felger I, Steiger S, Hatz C, Smith T, Beck HP, (2003) Antigenic cross-reactivity between different alleles of the Plasmodium falciparum merozoite surface protein 2. Parasite Immunol 25: 531-543.
54. Eisen DP, Wang L, Jouin H, Murhandarwati EEH, Black CG, et al. (2007) Antibodies elicited in adults by aprimary Plasmodium falciparum blood-stage infection recognize different epitopes compared with immune individuals. Malar J 6: 86.
55. Ambrosino E, Dumoulin C, Orlandi-Pradines E, Remoue F, Toure-Baldé A, et al. (2010) A multiplex assay for the simultaneous detection of antibodies against 15 Plasmodium falciparum and Anopheles gambiae saliva antigens. Malar J 9: 317.