Current status of Plasmodium vivax vaccine

Human Vaccines

Volumn 6, Issue 1, 2010, Pages

  Arévalo Herrera, Myriam ^a,b   Chitnis, Chetan ^c   Herrera, Sócrates ^a,b  

^a Centro Internacional de Vacunas   (Colombia)

^b UNIVERSIDAD DEL VALLE   (Colombia)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Malaria antigens; Malaria clinical trial; Malaria vaccine; P. vivax; Plasmodium vaccines

Indexed keywords

APICAL MEMBRANE ANTIGEN 1; CHLOROQUINE; CIRCUMSPOROZOITE PROTEIN; DUFFY BINDING PROTEIN; MALARIA VACCINE; MEROZOITE SURFACE PROTEIN 1; PRIMAQUINE; RTS S VACCINE; SPOROZOITE SURFACE PROTEIN 2; THROMBOSPONDIN RELATED ADHESIVE PROTEIN; UNCLASSIFIED DRUG;

AFRICA; CLINICAL TRIAL; DISEASE TRANSMISSION; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MALARIA; NONHUMAN; PLASMODIUM VIVAX MALARIA; PROTEIN EXPRESSION; RECOMBINANT DNA TECHNOLOGY; REVIEW; VACCINE PRODUCTION; IMMUNOLOGY; PLASMODIUM VIVAX;

CLINICAL TRIALS AS TOPIC; HUMANS; MALARIA VACCINES; MALARIA, VIVAX; PLASMODIUM VIVAX;

EID: 85046915641     PISSN: 15548600     EISSN: 15548619     Source Type: Journal    
DOI: 10.4161/hv.6.1.9931     Document Type: Review

References (126)

1. Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW. The global distribution and population at risk of malaria: past, present and future. Lancet Infect Dis 2004; 4:327-36.
2. WHO. World Malaria Report. Geneva 2008.
3. Feachem R, Group TME. Shrinking the Malaria Map: A guide on Malaria Elimination for Policy Makers. The Global Health Group: University of California, San Francisco 2009; 85.
4. Gusmao R. Overview of malaria control in the Americas. Parassitologia 1999; 41:355-60.
5. Sina B. Focus on Plasmodium vivax. Trends Parasitol 2002; 18:287-9.
6. Kochar DK, Das A, Kochar SK, Saxena V, Sirohi P, Garg S, et al. Severe Plasmodium vivax malaria: a report on serial cases from Bikaner in northwestern India. Am J Trop Med Hyg 2009; 80:194-8.
7. Sharma A, Khanduri U. How benign is benign tertian malaria? J Vector Borne Dis 2009; 46:141-4.
8. Lacerda MV, Hipolito JR, Passos LN. Chronic Plasmodium vivax infection in a patient with splenomegaly and severe thrombocytopenia. Rev Soc Bras Med Trop 2008; 41:522-3.
9. Miller LH, Mason SJ, Clyde DF, McGinniss MH. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, Fy. N Engl J Med 1976; 295:302-4.
10. Langhi DM Jr, Bordin JO. Duffy blood group and malaria. Hematology 2006; 11:389-98.
11. Chitnis CE. Molecular insights into receptors used by malaria parasites for erythrocyte invasion. Curr Opin Hematol 2001; 8:85-91.
12. Mendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 2001; 64:97-106.
13. WHO. WHO Expert Commitee on Malaria-Twentieth Report. WHO technical No. 892, Geneva 2000; 2000:4-71.
14. Carme B. Substantial increase of malaria in inland areas of eastern French Guiana. Trop Med Int Health 2005; 10:154-9.
15. Yeom JS, Ryu SH, Oh S, Lee WJ, Kim TS, Kim KH, et al. Status of Plasmodium vivax malaria in the Republic of Korea during 2001-2003. Am J Trop Med Hyg 2005; 73:604-8.
16. Baird JK. Chloroquine resistance in Plasmodium vivax. Antimicrob Agents Chemother 2004; 48:4075-83.
17. Payne D. Spread of chloroquine resistance in Plasmodium falciparum. Parasitol Today 1987; 3:241-6.
18. Pukrittayakamee S, Chotivanich K, Chantra A, Clemens R, Looareesuwan S, White NJ. Activities of artesunate and primaquine against asexual- and sexual-stage parasites in falciparum malaria. Antimicrob Agents Chemother 2004; 48:1329-34.
19. Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, et al. Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 2008; 5:128.
20. Arias AE, Corredor A. Low response of Colombian strains of Plasmodium vivax to classical antimalarial therapy. Trop Med Parasitol 1989; 40:21-3.
21. Narasimhan V, Attaran A. Roll back malaria? The scarcity of international aid for malaria control. Malar J 2003; 2:8.
22. Roll Back Malaria. Global malaria action plan. Available at: http://wwwrbmwhoint/gmap/indexhtml 2008.
23. Grabowsky M. The billion-dollar malaria moment. Nature 2008; 451:1051-2.
24. Riley EM, Wahl S, Perkins DJ, Schofield L. Regulating immunity to malaria. Parasite Immunol 2006; 28:35-49.
25. Cucunuba ZM, Guerra AP, Rahirant SJ, Rivera JA, Cortes LJ, Nicholls RS. Asymptomatic Plasmodium spp. infection in Tierralta, Colombia. Mem Inst Oswaldo Cruz 2008; 103:668-73.
26. Clyde DF. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am J Trop Med Hyg 1975; 24:397-401.
27. Clyde DF. Immunity to falciparum and vivax malaria induced by irradiated sporozoites: a review of the University of Maryland studies, 1971-75. Bull World Health Organ 1990; 68:9-12.
28. Artavanis-Tsakonas K, Tongren JE, Riley EM. The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol 2003; 133:145-52.
29. Doolan DL, Dobano C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev 2009; 22:13-36.
30. McGregor IA. The Passive Transfer of Human Malarial Immunity. Am J Trop Med Hyg 1964; 13:237-9.
31. Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, Chantavanich P, et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg 1991; 45:297-308.
32. Hollingdale MR. Anti-sporozoite antibodies. Bull World Health Organ 1990; 68:47-51.
33. Holder A. Preventing the merozoite invasion of erythrocyte. In: Hoffman S, ed. Malaria Vaccine development A multi-immune response approach. Washington DC. ASM Press 1996; 77-104.
34. Tsuboi T, Tachibana M, Kaneko O, Torii M. Transmission-blocking vaccine of vivax malaria. Parasitol Int 2003; 52:1-11.
35. Naotunne TS, Karunaweera ND, Mendis KN, Carter R. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 1993; 78:555-62.
36. Carlton JM, Escalante AA, Neafsey D, Volkman SK. Comparative evolutionary genomics of human malaria parasites. Trends Parasitol 2008; 24:545-50.
37. Wang R, Arévalo-Herrera M, Gardner MJ, Bonelo A, Carlton JM, Gomez A, et al. Immune responses to Plasmodium vivax pre-erythrocytic stage antigens in naturally exposed Duffy-negative humans: a potential model for identification of liver-stage antigens. Eur J Immunol 2005; 35:1859-68.
38. Serruto D, Rappuoli R. Post-genomic vaccine development. FEBS Lett 2006; 580:2985-92.
39. List EO, Berryman DE, Bower B, Sackmann-Sala L, Gosney E, Ding J, et al. The use of proteomics to study infectious diseases. Infect Disord Drug Targets 2008; 8:31-45.
40. Nussenzweig R, Vanderberg J, Most H. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei IV. Dose response, specificity and humoral immunity. Mil Med 1969; 134:1176-82.
41. Rieckmann KH, Beaudoin RL, Cassells JS, Sell KW. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull World Health Organ 1979; 57:261-5.
42. Engers HD, Godal T. Malaria vaccine development: current status. Parasitol Today 1998; 14:56-64.
43. Tediosi F, Maire N, Penny M, Studer A, Smith TA. Simulation of the cost-effectiveness of malaria vaccines. Malar J 2009; 8:127.
44. WHO/IVR. Portafolio of candidates malaria vaccines currently in development. http://wwwcolumbiaedu/ itc /hs /medical /pathophys /id/2005/ LarussaMalariaTablepdf 2005; 2005.
45. Sharma S, Pathak S. Malaria vaccine: a current perspective. J Vector Borne Dis 2008; 45:1-20.
46. Nussenzweig V, Nussenzweig RS. Rationale for the development of an engineered sporozoite malaria vaccine. Adv Immunol 1989; 45:283-334.
47. Stoute JA, Kester KE, Krzych U, Wellde BT, Hall T, White K, et al. Long-term efficacy and immune responses following immunization with the RTS,S malaria vaccine. J Infect Dis 1998; 178:1139-44.
48. Bojang KA, Milligan PJ, Pinder M, Vigneron L, Alloueche A, Kester KE, et al. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 2001; 358:1927-34.
49. Alonso PL, Sacarlal J, Aponte JJ, Leach A, Macete E, Milman J, et al. Efficacy of the RTS, S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomized controlled trial. Lancet 2004; 364:1411-20.
50. Moorthy VS, Reed Z, Smith PG. MALVAC 2008: Measures of efficacy of malaria vaccines in phase 2b and phase 3 trials-scientific, regulatory and public health perspectives. Vaccine 2009; 27:624-8.
51. Abdulla S, Oberholzer R, Juma O, Kubhoja S, Machera F, Membi C, et al. Safety and immunogenicity of RTS,S/AS02D malaria vaccine in infants. N Engl J Med 2008; 359:2533-44.
52. Greenwood BM. Control to elimination: implications for malaria research. Trends Parasitol 2008; 24:449-54.
53. Herrera S, Bonelo A, Perlaza BL, Fernandez OL, Victoria L, Lenis AM, et al. Safety and elicitation of humoral and cellular responses in Colombian malarianaive volunteers by a Plasmodium vivax circumsporozoite protein-derived synthetic vaccine. Am J Trop Med Hyg 2005; 73:3-9.
54. Malkin EM, Durbin AP, Diemert DJ, Sattabongkot J, Wu Y, Miura K, et al. Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine 2005; 23:3131-8.
55. Wu Y, Ellis RD, Shaffer D, Fontes E, Malkin EM, Mahanty S, et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with Montanide ISA 51. PLoS ONE 2008; 3:2636.
56. Galinski MR, Barnwell JW. Plasmodium vivax: who cares? Malar J 2008; 7:9.
57. Herrera S, Corradin G, Arévalo-Herrera M. An update on the search for a Plasmodium vivax vaccine. Trends Parasitol 2007; 23:122-8.
58. Arévalo-Herrera M, Herrera S. Plasmodium vivax malaria vaccine development. Mol Immunol 2001; 38:443-55.
59. Herrera S, Perlaza BL, Bonelo A, Arévalo-Herrera M. Aotus monkeys: their great value for anti-malaria vaccines and drug testing. Int J Parasitol 2002; 32:1625-35.
60. Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. J Immunol 1984; 132:909-13.
61. Doolan DL, Hoffman SL. The complexity of protective immunity against liver-stage malaria. J Immunol 2000; 165:1453-62.
62. Kain KC, Brown AE, Webster HK, Wirtz RA, Keystone JS, Rodriguez MH, et al. Circumsporozoite genotyping of global isolates of Plasmodium vivax from dried blood specimens. J Clin Microbiol 1992; 30:1863-6.
63. Gonzalez JM, Hurtado S, Arévalo-Herrera M, Herrera S. Variants of the Plasmodium vivax circumsporozoite protein (VK210 and VK247) in Colombian isolates. Mem Inst Oswaldo Cruz 2001; 96:709-12.
64. Tewari R, Spaccapelo R, Bistoni F, Holder AA, Crisanti A. Function of region I and II adhesive motifs of Plasmodium falciparum circumsporozoite protein in sporozoite motility and infectivity. J Biol Chem 2002; 277:47613-8.
65. Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 2005; 201:27-33.
66. Yuda M, Ishino T. Liver invasion by malarial parasites-how do malarial parasites break through the host barrier? Cell Microbiol 2004; 6:1119-25.
67. Herrington DA, Nardin EH, Losonsky G, Bathurst IC, Barr PJ, Hollingdale MR, et al. Safety and immunogenicity of a recombinant sporozoite malaria vaccine against Plasmodium vivax. Am J Trop Med Hyg 1991; 45:695-701.
68. Fries LF, Gordon DM, Schneider I, Beier JC, Long GW, Gross M, et al. Safety, immunogenicity, and efficacy of a Plasmodium falciparum vaccine comprising a circumsporozoite protein repeat region peptide conjugated to Pseudomonas aeruginosa toxin A. Infect Immun 1992; 60:1834-9.
69. Bell BA, Wood JF, Bansal R, Ragab H, Cargo J, 3rd, Washington MA, et al. Process development for the production of an E. coli produced clinical grade recombinant malaria vaccine for Plasmodium vivax. Vaccine 2009; 27:1448-53.
70. Arévalo-Herrera M, Roggero MA, Gonzalez JM, Vergara J, Corradin G, Lopez JA, et al. Mapping and comparison of the B-cell epitopes recognized on the Plasmodium vivax circumsporozoite protein by immune Colombians and immunized Aotus monkeys. Ann Trop Med Parasitol 1998; 92:539-51.
71. Herrera S, Escobar P, de Plata C, Avila GI, Corradin G, Herrera MA. Human recognition of T cell epitopes on the Plasmodium vivax circumsporozoite protein. J Immunol 1992; 148:3986-90.
72. Arévalo-Herrera M, Valencia AZ, Vergara J, Bonelo A, Fleischhauer K, Gonzalez JM, et al. Identification of HLA-A2 restricted CD8(+) T-lymphocyte responses to Plasmodium vivax circumsporozoite protein in individuals naturally exposed to malaria. Parasite Immunol 2002; 24:161-9.
73. Herrera S, Bonelo A, Perlaza BL, Valencia AZ, Cifuentes C, Hurtado S, et al. Use of long synthetic peptides to study the antigenicity and immunogenicity of the P. vivax circumsporozoite protein. International Journal for Parasitology 2004; 34:1535-46.
74. Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 1993; 177:1287-98.
75. Rogers WO, Gowda K, Hoffman SL. Construction and immunogenicity of DNA vaccine plasmids encoding four Plasmodium vivax candidate vaccine antigens. Vaccine 1999; 17:3136-44.
76. Castellanos A, Arévalo-Herrera M, Restrepo N, Gulloso L, Corradin G, Herrera S. Plasmodium vivax thrombospondin related adhesion protein: immunogenicity and protective efficacy in rodents and Aotus monkeys. Mem Inst Oswaldo Cruz 2007; 102:411-6.
77. Karunaweera ND, Wijesekera SK, Wanasekera D, Mendis KN, Carter R. The paroxysm of Plasmodium vivax malaria. Trends Parasitol 2003; 19:188-93.
78. Herrera MA, Rosero F, Herrera S, Caspers P, Rotmann D, Sinigaglia F, et al. Protection against malaria in Aotus monkeys immunized with a recombinant blood-stage antigen fused to a universal T-cell epitope: correlation of serum gamma interferon levels with protection. Infect Immun 1992; 60:154-8.
79. Valderrama-Aguirre A, Quintero G, Gomez A, Castellanos A, Perez Y, Mendez F, et al. Antigenicity, immunogenicity and protective efficacy of Plasmodium vivax MSP1 PV200l: a potential malaria vaccine subunit. Am J Trop Med Hyg 2005; 73:16-24.
80. Perera KL, Handunnetti SM, Holm I, Longacre S, Mendis K. Baculovirus merozoite surface protein 1 C-terminal recombinant antigens are highly protective in a natural primate model for human Plasmodium vivax malaria. Infect Immun 1998; 66:1500-6.
81. Yazdani SS, Shakri AR, Mukherjee P, Baniwal SK, Chitnis CE. Evaluation of immune responses elicited in mice against a recombinant malaria vaccine based on Plasmodium vivax Duffy binding protein. Vaccine 2004; 22:3727-37.
82. Arévalo-Herrera M, Castellanos A, Yazdani SS, Shakri AR, Chitnis CE, Dominik R, et al. Immunogenicity and protective efficacy of recombinant vaccine based on the receptor-binding domain of the Plasmodium vivax Duffy binding protein in Aotus monkeys. Am J Trop Med Hyg 2005; 73:25-31.
83. Barnwell JW, Galinski MR, DeSimone SG, Perler F, Ingravallo P. Plasmodium vivax, P. cynomolgi and P. knowlesi: identification of homologue proteins associated with the surface of merozoites. Exp Parasitol 1999; 91:238-49.
84. Oliveira-Ferreira J, Vargas-Serrato E, Barnwell JW, Moreno A, Galinski MR. Immunogenicity of Plasmodium vivax merozoite surface protein-9 recombinant proteins expressed in E. coli. Vaccine 2004; 22:2023-30.
85. Galinski MR, Ingravallo P, Corredor-Medina C, Al-Khedery B, Povoa M, Barnwell JW. Plasmodium vivax merozoite surface proteins-3beta and-3gamma share structural similarities with P. vivax merozoite surface protein-3alpha and define a new gene family. Mol Biochem Parasitol 2001; 115:41-53.
86. Galinski MR, Corredor-Medina C, Povoa M, Crosby J, Ingravallo P, Barnwell JW. Plasmodium vivax merozoite surface protein-3 contains coiled-coil motifs in an alanine-rich central domain. Mol Biochem Parasitol 1999; 101:131-47.
87. Black CG, Barnwell JW, Huber CS, Galinski MR, Coppel RL. The Plasmodium vivax homologues of merozoite surface proteins 4 and 5 from Plasmodium falciparum are expressed at different locations in the merozoite. Mol Biochem Parasitol 2002; 120:215-24.
88. Galinski MR, Xu M, Barnwell JW. Plasmodium vivax reticulocyte binding protein-2 (PvRBP-2) shares structural features with PvRBP-1 and the Plasmodium yoelii 235 kDa rhoptry protein family. Mol Biochem Parasitol 2000; 108:257-62.
89. Adams JH, Hudson DE, Torii M, Ward GE, Wellems TE, Aikawa M, et al. The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 1990; 63:141-53.
90. Cole-Tobian J, King CL. Diversity and natural selection in Plasmodium vivax Duffy binding protein gene. Mol Biochem Parasitol 2003; 127:121-32.
91. Singh SK, Hora R, Belrhali H, Chitnis CE, Sharma A. Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature 2006; 439:741-4.
92. Chitnis CE, Miller LH. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J Exp Med 1994; 180:497-506.
93. Ranjan A, Chitnis CE. Mapping regions containing binding residues within functional domains of Plasmodium vivax and Plasmodium knowlesi erythrocyte-binding proteins. Proc Natl Acad Sci USA 1999; 96:14067-72.
94. Singh SK, Singh AP, Pandey S, Yazdani SS, Chitnis CE, Sharma A. Definition of structural elements in Plasmodium vivax and P. knowlesi Duffy-binding domains necessary for erythrocyte invasion. Biochem J 2003; 374:193-8.
95. Hans D, Pattnaik P, Bhattacharyya A, Shakri AR, Yazdani SS, Sharma M, et al. Mapping binding residues in the Plasmodium vivax domain that binds Duffy antigen during red cell invasion. Mol Microbiol 2005; 55:1423-34.
96. VanBuskirk KM, Sevova E, Adams JH. Conserved residues in the Plasmodium vivax Duffy-binding protein ligand domain are critical for erythrocyte receptor recognition. Proc Natl Acad Sci USA 2004; 101:15754-9.
97. King CL, Michon P, Shakri AR, Marcotty A, Stanisic D, Zimmerman PA, et al. Naturally acquired Duffybinding protein-specific binding inhibitory antibodies confer protection from blood-stage Plasmodium vivax infection. Proc Natl Acad Sci USA 2008; 105:8363-8.
98. Michon P, Fraser T, Adams JH. Naturally acquired and vaccine-elicited antibodies block erythrocyte cytoadherence of the Plasmodium vivax Duffy binding protein. Infect Immun 2000; 68:3164-71.
99. Ceravolo IP, Sanchez BA, Sousa TN, Guerra BM, Soares IS, Braga EM, et al. Naturally acquired inhibitory antibodies to Plasmodium vivax Duffy binding protein are short-lived and allele-specific following a single malaria infection. Clin Exp Immunol 2009; 156:502-10.
100. Cole-Tobian JL, Michon P, Biasor M, Richards JS, Beeson JG, Mueller I, et al. Strain-Specific Duffy Binding Protein Antibodies Correlate with Protection Against Infection with Homologous Compared to Heterologous Plasmodium vivax Strains in Papua New Guinean Children. Infect Immun 2009.
101. Yazdani SS, Shakri AR, Chitnis CE. A high cell density fermentation strategy to produce recombinant malarial antigen in E. coli. Biotechnol Lett 2004; 26:1891-5.
102. Yazdani SS, Shakri AR, Pattnaik P, Rizvi MM, Chitnis CE. Improvement in Yield and Purity of a Recombinant Malaria Vaccine Candidate Based on the Receptor-Binding Domain of Plasmodium vivax Duffy Binding Protein by Codon Optimization. Biotechnol Lett 2006; 28:1109-14.
103. Riley EM, Allen SJ, Wheeler JG, Blackman MJ, Bennett S, Takacs B, et al. Naturally acquired cellular and humoral immune responses to the major merozoite surface antigen (PfMSP1) of Plasmodium falciparum are associated with reduced malaria morbidity. Parasite Immunol 1992; 14:321-37.
104. Siddiqui WA, Tam LQ, Kramer KJ, Hui GS, Case SE, Yamaga KM, et al. Merozoite surface coat precursor protein completely protects Aotus monkeys against Plasmodium falciparum malaria. Proc Natl Acad Sci USA 1987; 84:3014-8.
105. Daly TM, Long CA. A recombinant 15-kilodalton carboxyl-terminal fragment of Plasmodium yoelii yoelii 17XL merozoite surface protein 1 induces a protective immune response in mice. Infect Immun 1993; 61:2462-7.
106. Lyon JA, Angov E, Fay MP, Sullivan JS, Girourd AS, Robinson SJ, et al. Protection induced by Plasmodium falciparum MSP1(42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS One 2008; 3:2830.
107. Singh S, Miura K, Zhou H, Muratova O, Keegan B, Miles A, et al. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasiteinhibitory activity. Infect Immun 2006; 74:4573-80.
108. Koussis K, Withers-Martinez C, Yeoh S, Child M, Hackett F, Knuepfer E, et al. A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J 2009; 28:725-35.
109. Graves P, Gelband H. Vaccines for preventing malaria (blood-stage). Cochrane Database Syst Rev 2006; 006199.
110. del Portillo HA, Longacre S, Khouri E, David PH. Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA 1991; 88:4030-4.
111. Soares IS, Levitus G, Souza JM, Portillo HAd, Rodrigues MM. Acquired immune responses to the Nand C-terminal regions of Plasmodium vivax merozoite surface protein 1 in individuals exposed to malaria. Infection & Immunity 1997; 65:1606-14.
112. Yeom JS, Kim ES, Lim KJ, Oh JH, Sohn MJ, Yoo SB, et al. Naturally acquired IgM antibody response to the C-terminal region of the merozoite surface protein 1 of Plasmodium vivax in Korea: use for serodiagnosis of vivax malaria. J Parasitol 2008; 94:1410-4.
113. Stowers AW, Cioce V, Shimp RL, Lawson M, Hui G, Muratova O, et al. Efficacy of two alternate vaccines based on Plasmodium falciparum merozoite surface protein 1 in an Aotus challenge trial. Infect Immun 2001; 69:1536-46.
114. Collins WE, Kaslow DC, Sullivan JS, Morris CL, Galland GG, Yang C, et al. Testing the efficacy of a recombinant merozoite surface protein MSP-1(19) of Plasmodium vivax in Saimiri boliviensis monkeys. Am J Trop Med Hyg 1999; 60:350-6.
115. Genton B, Al-Yaman F, Anders R, Saul A, Brown G, Pye D, et al. Safety and immunogenicity of a threecomponent blood-stage malaria vaccine in adults living in an endemic area of Papua New Guinea. Vaccine 2000; 18:2504-11.
116. Mitchell GH, Thomas AW, Margos G, Dluzewski AR, Bannister LH. Apical membrane antigen 1, a major malaria vaccine candidate, mediates the close attachment of invasive merozoites to host red blood cells. Infect Immun 2004; 72:154-8.
117. Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A, Bodescot M, et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 2004; 279:9490-6.
118. Rodrigues MH, Rodrigues KM, Oliveira TR, Comodo AN, Rodrigues MM, Kocken CH, et al. Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Int J Parasitol 2005; 35:185-92.
119. Kocken CH, Dubbeld MA, Van Der Wel A, Pronk JT, Waters AP, Langermans JA, et al. High-level expression of Plasmodium vivax apical membrane antigen 1 (AMA-1) in Pichia pastoris: strong immunogenicity in Macaca mulatta immunized with P. vivax AMA-1 and adjuvant SBAS2. Infect Immun 1999; 67:43-9.
120. Bueno LL, Fujiwara RT, Soares IS, Braga EM. Direct effect of Plasmodium vivax recombinant vaccine candidates AMA-1 and MSP-119 on the innate immune response. Vaccine 2008; 26:1204-13.
121. Tsuboi T, Kaslow DC, Gozar MM, Tachibana M, Cao YM, Torii M. Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates. Mol Med 1998; 4:772-82.
122. Zakeri S, Raeisi A, Afsharpad M, Kakar Q, Ghasemi F, Atta H, et al. Molecular characterization of Plasmodium vivax clinical isolates in Pakistan and Iran using pvmsp-1, pvmsp-3alpha and pvcsp genes as molecular markers. Parasitol Int 2009.
123. Kaslow DC, Quakyi IA, Syin C, Raum MG, Keister DB, Coligan JE, et al. A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 1988; 333:74-6.
124. Hisaeda H, Stowers AW, Tsuboi T, Collins WE, Sattabongkot JS, Suwanabun N, et al. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 2000; 68:6618-23.
125. Arévalo-Herrera M, Solarte Y, Yasnot MF, Castellanos A, Rincon A, Saul A, et al. Induction of transmissionblocking immunity in Aotus monkeys by vaccination with a Plasmodium vivax clinical grade PVS25 recombinant protein. Am J Trop Med Hyg 2005; 73:32-7.
126. Luke TC, Hoffman SL. Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. J Exp Biol 2003; 206:3803-8.