Overcoming allelic specificity by immunization with five allelic forms of Plasmodium falciparum apical membrane antigen 1

Infection and Immunity

Volumn 81, Issue 5, 2013, Pages 1491-1501

  Miura, Kazutoyo ^a   Herrera, Raul ^a   Diouf, Ababacar ^a   Zhou, Hong ^a,b   Mu, Jianbing ^a   Hu, Zonghui ^a   MacDonald, Nicholas J ^a   Reiter, Karine ^a   Nguyen, Vu ^a   Shimp, Richard L ^a   Singh, Kavita ^a   Narum, David L ^a   Long, Carole A ^a   Miller, Louis H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; IMMUNOGLOBULIN G; MALARIA VACCINE; RECOMBINANT APICAL MEMBRANE ANTIGEN 1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANTIMALARIAL ACTIVITY; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; GROWTH INHIBITION; IMMUNIZATION; MALARIA FALCIPARUM; MICROBIAL POPULATION DYNAMICS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

EID: 84877804342     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01414-12     Document Type: Article

References (39)

1. Cibulskis RE, Aregawi M, Williams R, Otten M, Dye C. 2011. Worldwide incidence of malaria in 2009: estimates, time trends, and a critique of methods. PLoS Med. 8:e1001142. doi:10.1371/journal.pmed.1001142.
2. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, Methogo BG, Doucka Y, Flamen A, Mordmuller B, Issifou S, Kremsner PG, Sacarlal J, Aide P, Lanaspa M, Aponte JJ, Nhamuave A, Quelhas D, Bassat Q, Mandjate S, Macete E, Alonso P, Abdulla S, Salim N, Juma O, Shomari M, Shubis K, Machera F, Hamad AS, Minja R, Mtoro A, Sykes A, Ahmed S, Urassa AM, Ali AM, Mwangoka G, Tanner M, Tinto H, D'Alessandro U, Sorgho H, Valea I, Tahita MC, Kabore W, Ouedraogo S, Sandrine Y, Guiguemde RT, Ouedraogo JB, Hamel MJ, Kariuki S, Odero C, et al. 2011. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N. Engl. J. Med. 365:1863-1875.
3. Cohen S, McGregor IA, Carrington S. 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192:733-737.
4. Hodder AN, Crewther PE, Matthew ML, Reid GE, Moritz RL, Simpson RJ, Anders RF. 1996. The disulfide bond structure of Plasmodium apical membrane antigen-1. J. Biol. Chem. 271:29446-29452.
5. Pizarro JC, Normand BV, Chesne-Seck ML, Collins CR, Withers- Martinez C, Hackett F, Blackman MJ, Faber BW, Remarque EJ, Kocken CH, Thomas AW, Bentley GA. 2005. Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science 308:408-411.
6. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, Crabb BS, Cowman AF. 2000. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol. Microbiol. 38:706-718.
7. Polley SD, Conway DJ. 2001. Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158:1505-1512.
8. Cortes A, Mellombo M, Mueller I, Benet A, Reeder JC, Anders RF. 2003. Geographical structure of diversity and differences between symptomatic and asymptomatic infections for Plasmodium falciparum vaccine candidate AMA1. Infect. Immun. 71:1416-1426.
9. 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.
10. Osier FH, Weedall GD, Verra F, Murungi L, Tetteh KK, Bull P, Faber BW, Remarque E, Thomas A, Marsh K, Conway DJ. 2010. Allelic diversity and naturally acquired allele-specific antibody responses to Plasmodium falciparum apical membrane antigen 1 in Kenya. Infect. Immun. 78:46254633.
11. Mullen GE, Ellis RD, Miura K, Malkin E, Nolan C, Hay M, Fay MP, Saul A, Zhu D, Rausch K, Moretz S, Zhou H, Long CA, Miller LH, Treanor J. 2008. Phase 1 trial of AMA1-C1/Alhydrogel plus CPG 7909: an asexual blood-stage vaccine for Plasmodium falciparum malaria. PLoS One 3:e2940. doi:10.1371/journal.pone.0002940.
12. Polhemus ME, Magill AJ, Cummings JF, Kester KE, Ockenhouse CF, Lanar DE, Dutta S, Barbosa A, Soisson L, Diggs CL, Robinson SA, Haynes JD, Stewart VA, Ware LA, Brando C, Krzych U, Bowden RA, Cohen JD, Dubois MC, Ofori-Anyinam O, De-Kock E, Ballou WR, Heppner DG, Jr. 2007. Phase I dose escalation safety and immunogenicity trial of Plasmodium falciparum apical membrane protein (AMA-1) FMP2.1, adjuvanted with AS02A, in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 25:4203-4212.
13. Remarque EJ, Roestenberg M, Younis S, Walraven V, van der Werff N, Faber BW, Leroy O, Sauerwein R, Kocken CH, Thomas AW. 2012. Humoral immune responses to a single allele PfAMA1 vaccine in healthy malaria-naive adults. PLoS One 7:e38898. doi:10.1371/journal.pone .0038898.
14. Spring MD, Cummings JF, Ockenhouse CF, Dutta S, Reidler R, Angov E, Bergmann-Leitner E, Stewart VA, Bittner S, Juompan L, Kortepeter MG, Nielsen R, Krzych U, Tierney E, Ware LA, Dowler M, Hermsen CC, Sauerwein RW, de Vlas SJ, Ofori-Anyinam O, Lanar DE, Williams JL, Kester KE, Tucker K, Shi M, Malkin E, Long C, Diggs CL, Soisson L, Dubois MC, Ballou WR, Cohen J, Heppner DG, Jr. 2009. Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS One 4:e5254. doi:10.1371/journal.pone.0005254.
15. Sagara I, Dicko A, Ellis RD, Fay MP, Diawara SI, Assadou MH, Sissoko MS, Kone M, Diallo AI, Saye R, Guindo MA, Kante O, Niambele MB, Miura K, Mullen GE, Pierce M, Martin LB, Dolo A, Diallo DA, Doumbo OK, Miller LH, Saul A. 2009. A randomized controlled phase 2 trial of the blood stage AMA1-C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 27:3090-3098.
16. Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, Kone AK, Guindo AB, Traore K, Traore I, Kouriba B, Diallo DA, Diarra I, Daou M, Dolo A, Tolo Y, Sissoko MS, Niangaly A, Sissoko M, Takala- Harrison S, Lyke KE, Wu Y, Blackwelder WC, Godeaux O, Vekemans J, Dubois MC, Ballou WR, Cohen J, Thompson D, Dube T, Soisson L, Diggs CL, House B, Lanar DE, Dutta S, Heppner DG, Jr, Plowe CV. 2011. A field trial to assess a blood-stage malaria vaccine. N. Engl. J. Med. 365:1004-1013.
17. 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.
18. Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, Saye R, Tolo Y, Dutta S, Heppner DG, Soisson L, Diggs CL, Vekemans J, Cohen J, Blackwelder WC, Dube T, Laurens MB, Doumbo OK, Plowe CV. 2012. Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J. Infect. Dis. 207:511-519.
19. Drew DR, Hodder AN, Wilson DW, Foley M, Mueller I, Siba PM, Dent AE, Cowman AF, Beeson JG. 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. doi:10.1371 /journal.pone.0051023.
20. Duan J, Mu J, Thera MA, Joy D, Kosakovsky Pond SL, Diemert D, Long C, Zhou H, Miura K, Ouattara A, Dolo A, Doumbo O, Su XZ, Miller L. 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.
21. Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, Saul A, Long CA, Miller LH, Stowers AW. 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.
22. Giersing B, Miura K, Shimp R, Wang J, Zhou H, Orcutt A, Stowers A, Saul A, Miller LH, Long C, Singh S. 2005. Posttranslational modification of recombinant Plasmodium falciparum apical membrane antigen 1: impact on functional immune responses to a malaria vaccine candidate. Infect. Immun. 73:3963-3970.
23. Plassmeyer ML, Reiter K, Shimp RL, Kotova S, Smith PD, Hurt DE, House B, Zou X, Zhang Y, Hickman M, Uchime O, Herrera R, Nguyen V, Glen J, Lebowitz J, Jin AJ, Miller LH, Macdonald NJ, Wu Y, Narum DL. 2009. The structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate. J. Biol. Chem. 284:26951-26963.
24. Uchime O, Herrera R, Reiter K, Kotova S, Shimp RL, Jr, Miura K, Jones D, Lebowitz J, Ambroggio X, Hurt DE, Jin AJ, Long C, Miller LH, Narum DL. 2012. Analysis of the conformation and function of the Plasmodium falciparum merozoite proteins MTRAP and PTRAMP. Eukaryot. Cell 11:615-625.
25. Kocken CH, van der Wel AM, Dubbeld MA, Narum DL, van de Rijke FM, van Gemert GJ, van der Linde X, Bannister LH, Janse C, Waters AP, Thomas AW. 1998. Precise timing of expression of a Plasmodium falciparum-derived transgene in Plasmodium berghei is a critical determinant of subsequent subcellular localization. J. Biol. Chem. 273:15119-15124.
26. Miura K, Orcutt AC, Muratova OV, Miller LH, Saul A, Long CA. 2008. Development and characterization of a standardized ELISA including a reference serum on each plate to detect antibodies induced by experimental malaria vaccines. Vaccine 26:193-200.
27. Miura K, Zhou H, Muratova OV, Orcutt AC, Giersing B, Miller LH, Long CA. 2007. In immunization with Plasmodium falciparum apical membrane antigen 1, the specificity of antibodies depends on the species immunized. Infect. Immun. 75:5827-5836.
28. Bai T, Becker M, Gupta A, Strike P, Murphy VJ, Anders RF, Batchelor AH. 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.
29. Howell SA, Withers-Martinez C, Kocken CH, Thomas AW, Blackman MJ. 2001. Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J. Biol. Chem. 276: 31311-31320.
30. 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. doi:10.1371/journal.pone .0008110.
31. Remarque EJ, Faber BW, Kocken CH, Thomas AW. 2008. A diversitycovering approach to immunization with Plasmodium falciparum apical membrane antigen 1 induces broader allelic recognition and growth inhibition responses in rabbits. Infect. Immun. 76:2660-2670.
32. Kusi KA, Faber BW, Riasat V, Thomas AW, Kocken CH, Remarque EJ. 2010. Generation of humoral immune responses to multi-allele PfAMA1 vaccines; effect of adjuvant and number of component alleles on the breadth of response. PLoS One 5:e15391. doi:10.1371/journal.pone .0015391.
33. Kusi KA, Remarque EJ, Riasat V, Walraven V, Thomas AW, Faber BW, Kocken CH. 2011. Safety and immunogenicity of multi-antigen AMA1-based vaccines formulated with CoVaccine HTTM and Montanide ISA 51 in rhesus macaques. Malar. J. 10:182. doi:10.1186/1475 -2875-10-182.
34. Coley AM, Gupta A, Murphy VJ, Bai T, Kim H, Anders RF, Foley M, Batchelor AH. 2007. Structure of the malaria antigen AMA1 in complex with a growth-inhibitory antibody. PLoS Pathog. 3:1308-1319.
35. Crompton PD, Miura K, Traore B, Kayentao K, Ongoiba A, Weiss G, Doumbo S, Doumtabe D, Kone Y, Huang CY, Doumbo OK, Miller LH, Long CA, Pierce SK. 2010. In vitro growth-inhibitory activity and malaria risk in a cohort study in Mali. Infect. Immun. 78:737-745.
36. Dent AE, Bergmann-Leitner ES, Wilson DW, Tisch DJ, Kimmel R, Vulule J, Sumba PO, Beeson JG, Angov E, Moormann AM, Kazura JW. 2008. Antibody-mediated growth inhibition of Plasmodium fal-ciparum: relationship to age and protection from parasitemia in Kenyan children and adults. PLoS One 3:e3557. doi:10.1371/journal.pone .0003557.
37. Perraut R, Marrama L, Diouf B, Sokhna C, Tall A, Nabeth P, Trape JF, Longacre S, Mercereau-Puijalon O. 2005. Antibodies to the conserved C-terminal domain of the Plasmodium falciparum merozoite surface protein 1 and to the merozoite extract and their relationship with in vitro inhibitory antibodies and protection against clinical malaria in a Senegalese village. J. Infect. Dis. 191:264-271.
38. Dutta S, Sullivan JS, Grady KK, Haynes JD, Komisar J, Batchelor AH, Soisson L, Diggs CL, Heppner DG, Lanar DE, Collins WE, Barnwell JW. 2009. High antibody titer against apical membrane antigen-1 is required to protect against malaria in the Aotus model. PLoS One 4:e8138. doi:10 .1371/journal.pone.0008138.
39. Duncan CJ, Sheehy SH, Ewer KJ, Douglas AD, Collins KA, Halstead FD, Elias SC, Lillie PJ, Rausch K, Aebig J, Miura K, Edwards NJ, Poulton ID, Hunt-Cooke A, Porter DW, Thompson FM, Rowland R, Draper SJ, Gilbert SC, Fay MP, Long CA, Zhu D, Wu Y, Martin LB, Anderson CF, Lawrie AM, Hill AV, Ellis RD. 2011. Impact on malaria parasite multiplication rates in infected volunteers of the protein-inadjuvant vaccine AMA1-C1/Alhydrogel+CPG 7909. PLoS One 6:e22271. doi:10.1371/journal.pone.0022271.