Antibodies to Polymorphic Invasion-Inhibitory and Non-Inhibitory Epitopes of Plasmodium falciparum Apical Membrane Antigen 1 in Human Malaria

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Mugyenyi, Cleopatra K ^a   Elliott, Salenna R ^b   McCallum, Fiona J ^c   Anders, Robin F ^d   Marsh, Kevin ^a   Beeson, James G ^b,c,e  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b BURNET INSTITUTE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

^e MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL MEMBRANE ANTIGEN 1; EPITOPE; IMMUNOGLOBULIN G1;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; BINDING SITE; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; HAZARD ASSESSMENT; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MEROZOITE; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; RISK FACTOR; SCHOOL CHILD;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; EPITOPES; HUMANS; IMMUNOGLOBULIN G; INFANT; MALARIA; MEMBRANE PROTEINS; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; YOUNG ADULT;

PLASMODIUM FALCIPARUM;

EID: 84879813551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068304     Document Type: Article

References (55)

1. Doolan DL, Dobano C, Baird JK, (2009) Acquired immunity to malaria. Clin Microbiol Rev 22: 13-36.
2. Richards JS, Beeson JG, (2009) The future for blood-stage vaccines against malaria. Immunol Cell Biol 87: 377-390.
3. Beeson JG, Osier FH, Engwerda CR, (2008) Recent insights into humoral and cellular immune responses against malaria. Trends Parasitol 24: 578-584.
4. Fowkes FJ, Richards JS, Simpson JA, Beeson JG, (2010) The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med 7: e1000218.
5. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, et al. (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38: 706-718.
6. Richard D, MacRaild CA, Riglar DT, Chan JA, Foley M, et al. (2010) Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. J Biol Chem 285: 14815-14822.
7. Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, et al. (2011) Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci U S A 108: 13275-13280.
8. Lamarque M, Besteiro S, Papoin J, Roques M, Vulliez-Le Normand B, et al. (2011) The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathog 7: e1001276.
9. Hodder AN, Crewther PE, Anders RF, (2001) Specificity of the protective antibody response to apical membrane antigen 1. Infection and Immunity 69: 3286-3294.
10. Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, et al. (2002) High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun 70: 4471-4476.
11. Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, et al. (2002) In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun 70: 6948-6960.
12. Healer J, Murphy V, Hodder AN, Masciantonio R, Gemmill AW, et al. (2004) Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum. Mol Microbiol 52: 159-168.
13. Kusi KA, Faber BW, Thomas AW, Remarque EJ, (2009) Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS One 4: e8110.
14. Crewther PE, Matthew MLSM, Flegg RH, Anders RF, (1996) Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect Immun 64: 3310-3317.
15. Remarque EJ, Faber BW, Kocken CH, Thomas AW, (2008) Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol 24: 74-84.
16. Thomas AW, Trape JF, Rogier C, Goncalves A, Rosario VE, et al. (1994) High prevalence of natural antibodies against Plasmodium falciparum 83- kilodalton apical membrane antigen (PF83/AMA-1) as detected by capture- enzyme-linked immunosorbent assay using full-length baculovirus recombinant PF83/AMA-1. Am J Trop Med Hyg 51: 730-740.
17. Polley SD, Mwangi T, Kocken CH, Thomas AW, Dutta S, et al. (2004) Human antibodies to recombinant protein constructs of Plasmodium falciparum Apical Membrane Antigen 1 (AMA1) and their associations with protection from malaria. Vaccine 23: 718-728.
18. Johnson AH, Leke RG, Mendell NR, Shon D, Suh YJ, et al. (2004) Human leukocyte antigen class II alleles influence levels of antibodies to the Plasmodium falciparum asexual-stage apical membrane antigen 1 but not to merozoite surface antigen 2 and merozoite surface protein 1. Infect Immun 72: 2762-2771.
19. Cortes A, Mellombo M, Masciantonio R, Murphy VJ, Reeder JC, et al. (2005) Allele specificity of naturally acquired antibody responses against Plasmodium falciparum apical membrane antigen 1. Infect Immun 73: 422-430.
20. Chelimo K, Ofulla AV, Narum DL, Kazura JW, Lanar DE, et al. (2005) Antibodies to Plasmodium falciparum antigens vary by age and antigen in children in a malaria-holoendemic area of Kenya. Pediatr Infect Dis J 24: 680-684.
21. Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, et al. (2009) Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect Immun 77: 1165-1174.
22. Gray JC, Corran PH, Mangia E, Gaunt MW, Li Q, et al. (2007) Profiling the antibody immune response against blood stage malaria vaccine candidates. Clin Chem 53: 1244-1253.
23. Osier FH, Fegan G, Polley SD, Murungi L, Verra F, et al. (2008) Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun 76: 2240-2248.
24. Roussilhon C, Oeuvray C, Muller-Graf C, Tall A, Rogier C, et al. (2007) Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS Med 4: e320.
25. Nebie I, Diarra A, Ouedraogo A, Soulama I, Bougouma EC, et al. (2008) Humoral responses to Plasmodium falciparum blood-stage antigens and association with incidence of clinical malaria in children living in an area of seasonal malaria transmission in Burkina Faso, West Africa. Infect Immun 76: 759-766.
26. Dodoo D, Aikins A, Kusi KA, Lamptey H, Remarque E, et al. (2008) Cohort study of the association of antibody levels to AMA1, MSP119, MSP3 and GLURP with protection from clinical malaria in Ghanaian children. Malar J 7: 142.
27. Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, et al. (2011) A field trial to assess a blood-stage malaria vaccine. N Engl J Med 365: 1004-1013.
28. Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, et al. (2013) Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J Infect Dis 207: 511-519.
29. Bai T, Becker M, Gupta A, Strike P, Murphy VJ, et al. (2005) Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci U S A 102: 12736-12741.
30. Collins CR, Withers-Martinez C, Hackett F, Blackman MJ, (2009) An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog 5: e1000273.
31. Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, et al. (2003) Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect Immun 71: 1416-1426.
32. Polley SD, Chokejindachai W, Conway DJ, (2003) Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics 165: 555-561.
33. Drew DR, Hodder AN, Wilson DW, Foley M, Mueller I, et al. (2012) Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. PLoS One 7: e51023.
34. Duan J, Mu J, Thera MA, Joy D, Kosakovsky Pond SL, et al. (2008) Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: implications for vaccine design. Proc Natl Acad Sci U S A 105: 7857-7862.
35. Barry AE, Schultz L, Buckee CO, Reeder JC, (2009) Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. PLoS One 4: e8497.
36. Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, et al. (2009) Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med 1: 2ra5.
37. Coley AM, Campanale NV, Casey JL, Hodder AN, Crewther PE, et al. (2001) Rapid and precise epitope mapping of monoclonal antibodies against Plasmodium falciparum AMA1 by combined phage display of fragments and random peptides. Protein Eng 14: 691-698.
38. Coley AM, Parisi K, Masciantonio R, Hoeck J, Casey JL, et al. (2006) The most polymorphic residue on Plasmodium falciparum apical membrane antigen 1 determines binding of an invasion-inhibitory antibody. Infect Immun 74: 2628-2636.
39. Coley AM, Gupta A, Murphy VJ, Bai T, Kim H, et al. (2007) Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog 3: 1308-1319.
40. Dutta S, Lee SY, Batchelor AH, Lanar DE, (2007) Structural basis of antigenic escape of a malaria vaccine candidate. Proc Natl Acad Sci U S A 104: 12488-12493.
41. Mwangi TW, Ross A, Snow RW, Marsh K, (2005) Case definitions of clinical malaria under different transmission conditions in Kilifi District, Kenya. J Infect Dis 191: 1932-1939.
42. Mbogo CN, Snow RW, Khamala CP, Kabiru EW, Ouma JH, et al. (1995) Relationships between Plasmodium falciparum transmission by vector populations and the incidence of severe disease at nine sites on the Kenyan coast. Am J Trop Med Hyg 52: 201-206.
43. Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, et al. (2003) Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg 68: 734-742.
44. Mackintosh CL, Mwangi T, Kinyanjui SM, Mosobo M, Pinches R, et al. (2008) Failure to respond to the surface of Plasmodium falciparum infected erythrocytes predicts susceptibility to clinical malaria amongst African children. Int J Parasitol 38: 1445-1454.
45. McCallum FJ, Persson KE, Mugyenyi CK, Fowkes FJ, Simpson JA, et al. (2008) Acquisition of growth-inhibitory antibodies against blood-stage Plasmodium falciparum. PLoS One 3: e3571.
46. Persson KE, McCallum FJ, Reiling L, Lister NA, Stubbs J, et al. (2008) Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 118: 342-351.
47. Ndungu FM, Bull PC, Ross A, Lowe BS, Kabiru E, et al. (2002) Naturally acquired immunoglobulin (Ig)G subclass antibodies to crude asexual Plasmodium falciparum lysates: evidence for association with protection for IgG1 and disease for IgG2. Parasite Immunol 24: 77-82.
48. Richards JS, Stanisic DI, Fowkes FJ, Tavul L, Dabod E, et al. (2010) Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis 51: e50-60.
49. Persson KE, Lee CT, Marsh K, Beeson JG, (2006) Development and optimization of high-throughput methods to measure Plasmodium falciparum-specific growth inhibitory antibodies. J Clin Microbiol 44: 1665-1673.
50. Boyle MJ, Wilson DW, Richards JS, Riglar DT, Tetteh KK,et al. Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci U S A 107: 14378-14383.
51. Wilson S, Booth M, Jones FM, Mwatha JK, Kimani G, et al. (2007) Age-adjusted Plasmodium falciparum antibody levels in school-aged children are a stable marker of microgeographical variations in exposure to Plasmodium infection. BMC Infect Dis 7: 67.
52. Tonkin ML, Roques M, Lamarque MH, Pugniere M, Douguet D, et al. (2011) Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333: 463-467.
53. Marsh K, Kinyanjui S, (2006) Immune effector mechanisms in malaria. Parasite Immunol 28: 51-60.
54. Siegrist CA, Aspinall R, (2009) B-cell responses to vaccination at the extremes of age. Nat Rev Immunol 9: 185-194.
55. Reddy SB, Anders RF, Beeson JG, Farnert A, Kironde F, et al. (2012) High affinity antibodies to Plasmodium falciparum merozoite antigens are associated with protection from malaria. PLoS One 7: e32242.