Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4625-4633

  Osier, Faith H A ^a,b   Weedall, Gareth D ^b,e   Verra, Federica ^b   Murungi, Linda ^a   Tetteh, Kevin K A ^b   Bull, Pete ^a   Faber, Bart W ^c   Remarque, Ed ^c   Thomas, Alan ^c   Marsh, Kevin ^a   Conway, David J ^b,d  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^d MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; APICAL MEMBRANE ANTIGEN 1; NUCLEOTIDE;

ALLELE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; APICAL MEMBRANE; ARTICLE; CHILD; CLUSTER ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE FREQUENCY; GENETIC POLYMORPHISM; HAPLOTYPE; HUMAN; INFECTION; MAJOR CLINICAL STUDY; MALARIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD;

ADAPTIVE IMMUNITY; ALLELES; AMINO ACID SEQUENCE; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; GENE FREQUENCY; GENETIC VARIATION; HAPLOTYPES; HUMANS; INFANT; KENYA; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SEVERITY OF ILLNESS INDEX;

EID: 78049448429     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00576-10     Document Type: Article

References (54)

1. Alexander, D. L., S. Arastu-Kapur, J. F. Dubremetz, and J. C. Boothroyd. 2006. Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot. Cell 5:1169-1173.
2. Alexander, D. L., J. Mital, G. E. Ward, P. Bradley, and J. C. Boothroyd. 2005. Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog. 1:e17.
3. Anders, R. F., P. E. Crewther, S. Edwards, M. Margetts, M. L. Matthew, B. Pollock, and D. Pye. 1998. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine 16:240-247.
4. Babiker, H. A., J. Lines, W. G. Hill, and D. Walliker. 1997. Population structure of Plasmodium falciparum in villages with different malaria endemicity in east Africa. Am. J. Trop. Med. Hyg. 56:141-147.
5. Bai, T., M. Becker, A. Gupta, P. Strike, V. J. Murphy, R. F. Anders, and A. H. Batchelor. 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.
6. Bland, J. M., and D. G. Altman. 1995. Multiple significance tests: the Bonferroni method. BMJ 310:170.
7. Bull, P. C., B. S. Lowe, M. Kortok, C. S. Molyneux, C. I. Newbold, and K. Marsh. 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 4:358-360.
8. Cao, J., O. Kaneko, A. Thongkukiatkul, M. Tachibana, H. Otsuki, Q. Gao, T. Tsuboi, and M. Torii. 2009. Rhoptry neck protein RON2 forms a complex with microneme protein AMA1 in Plasmodium falciparum merozoites. Parasitol. Int. 58:29-35.
9. Coley, A. M., N. V. Campanale, J. L. Casey, A. N. Hodder, P. E. Crewther, R. F. Anders, L. M. Tilley, and M. Foley. 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.
10. Coley, A. M., A. Gupta, V. J. Murphy, T. Bai, H. Kim, R. F. Anders, M. Foley, and A. H. Batchelor. 2007. Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog. 3:1308-1319.
11. Coley, A. M., K. Parisi, R. Masciantonio, J. Hoeck, J. L. Casey, V. J. Murphy, K. S. Harris, A. H. Batchelor, R. F. Anders, and M. Foley. 2006. The most polymorphic residue on Plasmodium falciparum apical membrane antigen 1 determines binding of an invasion-inhibitory antibody. Infect. Immun. 74: 2628-2636.
12. Collins, C. R., C. Withers-Martinez, F. Hackett, and M. J. Blackman. 2009. An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog. 5:e1000273.
13. Conway, D. J., C. Roper, A. M. Oduola, D. E. Arnot, P. G. Kremsner, M. P. Grobusch, C. F. Curtis, and B. M. Greenwood. 1999. High recombination rate in natural populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 96:4506-4511.
14. Cortes, A., M. Mellombo, R. Masciantonio, V. J. Murphy, J. C. Reeder, and R. F. Anders. 2005. Allele specificity of naturally acquired antibody responses against Plasmodium falciparum apical membrane antigen 1. Infect. Immun. 73:422-430.
15. Cortes, A., M. Mellombo, I. Mueller, A. Benet, J. C. Reeder, and R. F. Anders. 2003. Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect. Immun. 71:1416-1426.
16. Crewther, P. E., M. L. Matthew, R. H. Flegg, and R. F. Anders. 1996. Protective immune responses to apical membrane antigen 1 of Plasmodium chabaudi involve recognition of strain-specific epitopes. Infect. Immun. 64: 3310-3317.
17. Dicko, A., D. J. Diemert, I. Sagara, M. Sogoba, M. B. Niambele, M. H. Assadou, O. Guindo, B. Kamate, M. Baby, M. Sissoko, E. M. Malkin, M. P. Fay, M. A. Thera, K. Miura, A. Dolo, D. A. Diallo, G. E. Mullen, C. A. Long, A. Saul, O. Doumbo, and L. H. Miller. 2007. Impact of a Plasmodium falciparum AMA1 vaccine on antibody responses in adult Malians. PLoS One 2:e1045.
18. Dutta, S., S. Y. Lee, A. H. Batchelor, and D. E. Lanar. 2007. Structural basis of antigenic escape of a malaria vaccine candidate. Proc. Natl. Acad. Sci. U. S. A. 104:12488-12493.
19. Fu, Y. X., and W. H. Li. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
20. Garg, S., M. T. Alam, M. K. Das, V. Dev, A. Kumar, A. P. Dash, and Y. D. Sharma. 2007. Sequence diversity and natural selection at domain I of the apical membrane antigen 1 among Indian Plasmodium falciparum populations. Malar. J. 6:154.
21. Healer, J., V. Murphy, A. N. Hodder, R. Masciantonio, A. W. Gemmill, R. F. Anders, A. F. Cowman, and A. Batchelor. 2004. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum. Mol. Microbiol. 52:159-168.
22. Hill, W. G., and A. Robertson. 1968. The effects of inbreeding at loci with heterozygote advantage. Genetics 60:615-628.
23. Hodder, A. N., P. E. Crewther, M. L. Matthew, G. E. Reid, R. L. Moritz, R. J. Simpson, and R. F. Anders. 1996. The disulfide bond structure of Plasmodium apical membrane antigen-1. J. Biol. Chem. 271:29446-29452.
24. Hoffmann, E. H., L. A. da Silveira, R. Tonhosolo, F. J. Pereira, W. L. Ribeiro, A. P. Tonon, F. Kawamoto, and M. U. Ferreira. 2001. Geographical patterns of allelic diversity in the Plasmodium falciparum malaria-vaccine candidate, merozoite surface protein-2. Ann. Trop. Med. Parasitol. 95:117-132.
25. Hudson, R. R. 1987. Estimating the recombination parameter of a finite population model without selection. Genet. Res. 50:245-250.
26. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
27. Kennedy, M. C., J. Wang, Y. Zhang, A. P. Miles, F. Chitsaz, A. Saul, C. A. Long, L. H. Miller, and A. W. Stowers. 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.
28. Kocken, C. H., D. L. Narum, A. Massougbodji, B. Ayivi, M. A. Dubbeld, A. van der Wel, D. J. Conway, A. Sanni, and A. W. Thomas. 2000. Molecular characterisation of Plasmodium reichenowi apical membrane antigen-1 (AMA-1), comparison with P. falciparum AMA-1, and antibody-mediated inhibition of red cell invasion. Mol. Biochem. Parasitol. 109:147-156.
29. Kocken, C. H., C. Withers-Martinez, M. A. Dubbeld, A. van der Wel, F. Hackett, A. Valderrama, M. J. Blackman, and A. W. Thomas. 2002. Highlevel 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.
30. Kusi, K. A., B. W. Faber, A. W. Thomas, and E. J. Remarque. 2009. Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS One 4:e8110.
31. Lal, A. A., M. A. Hughes, D. A. Oliveira, C. Nelson, P. B. Bloland, A. J. Oloo, W. E. Hawley, A. W. Hightower, B. L. Nahlen, and V. Udhayakumar. 1996. Identification of T-cell determinants in natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in an adult population exposed to malaria. Infect. Immun. 64:1054-1059.
32. Lalitha, P. V., L. A. Ware, A. Barbosa, S. Dutta, J. K. Moch, J. D. Haynes, B. B. Fileta, C. E. White, and D. E. Lanar. 2004. Production of the subdomains of the Plasmodium falciparum apical membrane antigen 1 ectodomain and analysis of the immune response. Infect. Immun. 72:4464-4470.
33. Lewontin, R. C. 1964. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49:49-67.
34. Mbogo, C. M., J. M. Mwangangi, J. Nzovu, W. Gu, G. Yan, J. T. Gunter, C. Swalm, J. Keating, J. L. Regens, J. I. Shililu, J. I. Githure, and J. C. Beier. 2003. Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am. J. Trop. Med. Hyg. 68:734-742.
35. Mbogo, C. N., R. W. Snow, E. W. Kabiru, J. H. Ouma, J. I. Githure, K. Marsh, and J. C. Beier. 1993. Low-level Plasmodium falciparum transmission and the incidence of severe malaria infections on the Kenyan coast. Am. J. Trop. Med. Hyg. 49:245-253.
36. Morahan, B. J., G. B. Sallmann, R. Huestis, V. Dubljevic, and K. L. Waller. 2009. Plasmodium falciparum: genetic and immunogenic characterisation of the rhoptry neck protein PfRON4. Exp. Parasitol. 122:280-288.
37. Mu, J., P. Awadalla, J. Duan, K. M. McGee, D. A. Joy, G. A. McVean, and X. Z. Su. 2005. Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 3:e335.
38. Mueller, M. S., A. Renard, F. Boato, D. Vogel, M. Naegeli, R. Zurbriggen, J. A. Robinson, and G. Pluschke. 2003. Induction of parasite growth-inhibitory antibodies by a virosomal formulation of a peptidomimetic of loop I from domain III of Plasmodium falciparum apical membrane antigen 1. Infect. Immun. 71:4749-4758.
39. Mwangi, T. W., A. Ross, R. W. Snow, and K. Marsh. 2005. Case definitions of clinical malaria under different transmission conditions in Kilifi District, Kenya. J. Infect. Dis. 191:1932-1939.
40. Nair, M., M. G. Hinds, A. M. Coley, A. N. Hodder, M. Foley, R. F. Anders, and R. S. Norton. 2002. Structure of domain III of the blood-stage malaria vaccine candidate, Plasmodium falciparum apical membrane antigen 1 (AMA1). J. Mol. Biol. 322:741-753.
41. Neafsey, D. E., S. F. Schaffner, S. K. Volkman, D. Park, P. Montgomery, D. A. Milner, Jr., A. Lukens, D. Rosen, R. Daniels, N. Houde, J. F. Cortese, E. Tyndall, C. Gates, N. Stange-Thomann, O. Sarr, D. Ndiaye, O. Ndir, S. Mboup, M. U. Ferreira, S. L. Moraes, A. P. Dash, C. E. Chitnis, R. C. Wiegand, D. L. Hartl, B. W. Birren, E. S. Lander, P. C. Sabeti, and D. F. Wirth. 2008. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol. 9:R171.
42. Osier, F. H., G. Fegan, S. D. Polley, L. Murungi, F. Verra, K. K. Tetteh, B. Lowe, T. Mwangi, P. C. Bull, A. W. Thomas, D. R. Cavanagh, J. S. McBride, D. E. Lanar, M. J. Mackinnon, D. J. Conway, and K. Marsh. 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.
43. Osier, F. H., S. D. Polley, T. Mwangi, B. Lowe, D. J. Conway, and K. Marsh. 2007. Naturally acquired antibodies to polymorphic and conserved epitopes of Plasmodium falciparum merozoite surface protein 3. Parasite Immunol. 29:387-394.
44. Polley, S. D., W. Chokejindachai, and D. J. Conway. 2003. Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics 165:555-561.
45. Polley, S. D., and D. J. Conway. 2001. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158:1505-1512.
46. Polley, S. D., D. J. Conway, D. R. Cavanagh, J. S. McBride, B. S. Lowe, T. N. Williams, T. W. Mwangi, and K. Marsh. 2006. High levels of serum antibodies to merozoite surface protein 2 of Plasmodium falciparum are associated with reduced risk of clinical malaria in coastal Kenya. Vaccine 24:4233-4246.
47. Polley, S. D., T. Mwangi, C. H. Kocken, A. W. Thomas, S. Dutta, D. E. Lanar, E. Remarque, A. Ross, T. N. Williams, G. Mwambingu, B. Lowe, D. J. Conway, and K. Marsh. 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.
48. Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497. (Pubitemid 38016658)
49. Schoepflin, S., F. Valsangiacomo, E. Lin, B. Kiniboro, I. Mueller, and I. Felger. 2009. Comparison of Plasmodium falciparum allelic frequency distribution in different endemic settings by high-resolution genotyping. Malar. J. 8:250.
50. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
51. Takala, S. L., D. Coulibaly, M. A. Thera, A. H. Batchelor, M. P. Cummings, A. A. Escalante, A. Ouattara, K. Traore, A. Niangaly, A. A. Djimde, O. K. Doumbo, and C. V. Plowe. 2009. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci. Transl. Med. 1:2ra5.
52. Thera, M. A., O. K. Doumbo, B. Coulibaly, M. B. Laurens, A. Kone, A. Guindo, D. Diallo, T. K. B. Kouriba, I. Diarra, A. Dolo, A. Niangaly, M. Daou, M. Sissoko, D. Traore, K. E. Lyke, S. Takala, O. Godeaux, J. Thonnard, J. Cohen, D. E. Lanar, C. Diggs, L. Soisson, D. G. Heppner, and C. V. Plowe. 2009. Randomized, controlled, phase 2B clinical trial to evaluate the safety, immunogenicity and efficacy of WRAIR's AMA-1 malaria vaccine (FMP2.1) adjuvanted in GSK Biologicals' AS02A vs. rabies vaccine in 1-6 year old children in Bandiagara, Mali. Abstr. Am. Soc. Trop. Med. Hyg. 58th Annu. Meet., Washington, DC.
53. Udhayakumar, V., S. Kariuki, M. Kolczack, M. Girma, J. M. Roberts, A. J. Oloo, B. L. Nahlen, and A. A. Lal. 2001. Longitudinal study of natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in a holoendemic region of malaria in western Kenya: Asembo Bay Cohort Project VIII. Am. J. Trop. Med. Hyg. 65:100-107.
54. Walliker, D., I. A. Quakyi, T. E. Wellems, T. F. McCutchan, A. Szarfman, W. T. London, L. M. Corcoran, T. R. Burkot, and R. Carter. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236:1661-1666.