Passive immunoprotection of Plasmodium falciparum-infected mice designates the CyRPA as candidate malaria vaccine antigen

Journal of Immunology

Volumn 188, Issue 12, 2012, Pages 6225-6237

  Dreyer, Anita M ^a,b   Matile, Hugues ^c   Papastogiannidis, Petros ^a,b   Kamber, Jolanda ^a,b   Favuzza, Paola ^a,b   Voss, Till S ^a,b   Wittlin, Sergio ^a,b   Pluschke, Gerd ^a,b  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYRPA; CYSTEINE RICH PROTECTIVE ANTIGEN; MALARIA VACCINE; PFD 1130W; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; CELL INVASION; CONTROLLED STUDY; DOSE RESPONSE; ERYTHROCYTE; HUMAN; HUMAN CELL; IMMUNITY; IMMUNOFLUORESCENCE; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; INTRON; MALARIA FALCIPARUM; MEROZOITE; MOUSE; NONHUMAN; OPEN READING FRAME; PARASITE ISOLATION; PASSIVE IMMUNIZATION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTES; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HUMANS; MALARIA VACCINES; MALARIA, FALCIPARUM; MEROZOITES; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; SEQUENCE ALIGNMENT; SURFACE PLASMON RESONANCE; TRANSFECTION;

EID: 84862593601     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103177     Document Type: Article

References (97)

1. World Health Organization. 2010. World Malaria Report 2010. WHO, Geneva, Switzerland.
2. Doolan, D. L., and S. L. Hoffman. 1997. Multi-gene vaccination against malaria: a multistage, multi-immune response approach. Parasitol. Today 13: 171-178. (Pubitemid 27207488)
3. Patarroyo, M. E., and M. A. Patarroyo. 2008. Emerging rules for subunit-based, multiantigenic, multistage chemically synthesized vaccines. Acc. Chem. Res. 41: 377-386.
4. Marsh, K., and S. Kinyanjui. 2006. Immune effector mechanisms in malaria. Parasite Immunol. 28: 51-60.
5. Cohen, S., I. A. McGREGOR, and S. Carrington. 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192: 733-737.
6. McGregor, I. A. 1964. The passive transfer of human malarial immunity. Am. J. Trop. Med. Hyg. 13(Suppl): 237-239.
7. Sabchareon, A., T. Burnouf, D. Ouattara, P. Attanath, H. Bouharoun-Tayoun, P. Chantavanich, C. Foucault, T. Chongsuphajaisiddhi, and P. Druilhe. 1991. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am. J. Trop. Med. Hyg. 45: 297-308.
8. Genton, B., I. Betuela, I. Felger, F. Al-Yaman, R. F. Anders, A. Saul, L. Rare, M. Baisor, K. Lorry, G. V. Brown, et al. 2002. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J. Infect. Dis. 185: 820-827. (Pubitemid 34226210)
9. Mitchell, G. H., G. A. Butcher, A. Voller, and S. Cohen. 1976. The effect of human immune IgG on the in vitro development of Plasmodium falciparum. Parasitology 72: 149-162.
10. Ling, I. T., S. A. Ogun, P. Momin, R. L. Richards, N. Garçon, J. Cohen, W. R. Ballou, and A. A. Holder. 1997. Immunization against the murine malaria parasite Plasmodium yoelii using a recombinant protein with adjuvants developed for clinical use. Vaccine 15: 1562-1567. (Pubitemid 27402140)
11. Perera, K. L., S. M. Handunnetti, I. Holm, S. Longacre, and K. Mendis. 1998. Baculovirus merozoite surface protein 1 C-terminal recombinant antigens are highly protective in a natural primate model for human Plasmodium vivax malaria. Infect. Immun. 66: 1500-1506. (Pubitemid 128471510)
12. 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. (Pubitemid 26256181)
13. Collins, W. E., D. Pye, P. E. Crewther, K. L. Vandenberg, G. G. Galland, A. J. Sulzer, D. J. Kemp, S. J. Edwards, R. L. Coppel, J. S. Sullivan, et al. 1994. Protective immunity induced in squirrel monkeys with recombinant apical membrane antigen-1 of Plasmodium fragile. Am. J. Trop. Med. Hyg. 51: 711-719.
14. Ogutu, B. R., O. J. Apollo, D. McKinney, W. Okoth, J. Siangla, F. Dubovsky, K. Tucker, J. N. Waitumbi, C. Diggs, J. Wittes, et al; MSP-1 Malaria Vaccine Working Group. 2009. Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS ONE 4: e4708.
15. Esen, M., P. G. Kremsner, R. Schleucher, M. Gässler, E. B. Imoukhuede, N. Imbault, O. Leroy, S. Jepsen, B. W. Knudsen, M. Schumm, et al. 2009. Safety and immunogenicity of GMZ2 - a MSP3-GLURP fusion protein malaria vaccine candidate. Vaccine 27: 6862-6868.
16. Audran, R., M. Cachat, F. Lurati, S. Soe, O. Leroy, G. Corradin, P. Druilhe, and F. Spertini. 2005. Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infect. Immun. 73: 8017-8026. (Pubitemid 41740288)
17. Sirima, S. B., A. B. Tiono, A. Ouédraogo, A. Diarra, A. L. Ouédraogo, J. B. Yaro, E. Ouédraogo, A. Gansané, E. C. Bougouma, A. T. Konaté, et al. 2009. Safety and immunogenicity of the malaria vaccine candidate MSP3 long synthetic peptide in 12-24 months-old Burkinabe children. PLoS ONE 4: e7549.
18. Druilhe, P., F. Spertini, D. Soesoe, G. Corradin, P. Mejia, S. Singh, R. Audran, A. Bouzidi, C. Oeuvray, and C. Roussilhon. 2005. A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS Med. 2: e344.
19. Sagara, I., R. D. Ellis, A. Dicko, M. B. Niambele, B. Kamate, O. Guindo, M. S. Sissoko, M. P. Fay, M. A. Guindo, O. Kante, et al. 2009. A randomized and controlled phase 1 study of the safety and immunogenicity of the AMA1-C1/Alhydrogel + CPG 7909 vaccine for Plasmodium falciparum malaria in semiimmune Malian adults. Vaccine 27: 7292-7298.
20. El Sahly, H. M., S. M. Patel, R. L. Atmar, T. A. Lanford, T. Dube, D. Thompson, B. K. L. Sim, C. Long, and W. A. Keitel. 2010. Safety and immunogenicity of a recombinant nonglycosylated erythrocyte binding antigen 175 Region II malaria vaccine in healthy adults living in an area where malaria is not endemic. Clin. Vaccine Immunol. 17: 1552-1559.
21. Hermsen, C. C., D. F. Verhage, D. S. C. Telgt, K. Teelen, J. T. Bousema, M. Roestenberg, A. Bolad, K. Berzins, G. Corradin, O. Leroy, et al. 2007. Glutamate-rich protein (GLURP) induces antibodies that inhibit in vitro growth of Plasmodium falciparum in a phase 1 malaria vaccine trial. Vaccine 25: 2930-2940. (Pubitemid 46412561)
22. Horii, T., H. Shirai, L. Jie, K. J. Ishii, N. Q. Palacpac, T. Tougan, M. Hato, N. Ohta, A. Bobogare, N. Arakaki, et al. 2010. Evidences of protection against blood-stage infection of Plasmodium falciparum by the novel protein vaccine SE36. Parasitol. Int. 59: 380-386.
23. Dvorak, J. A., L. H. Miller, W. C. Whitehouse, and T. Shiroishi. 1975. Invasion of erythrocytes by malaria merozoites. Science 187: 748-750.
24. Gilson, P. R., and B. S. Crabb. 2009. Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int. J. Parasitol. 39: 91-96.
25. Persson, K. E. M. 2010. Erythrocyte invasion and functionally inhibitory antibodies in Plasmodium falciparum malaria. Acta Trop. 114: 138-143.
26. Blackman, M. J., T. J. Scott-Finnigan, S. Shai, and A. A. Holder. 1994. Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J. Exp. Med. 180: 389-393. (Pubitemid 24181090)
27. Epstein, N., L. H. Miller, D. C. Kaushel, I. J. Udeinya, J. Rener, R. J. Howard, R. Asofsky, M. Aikawa, and R. L. Hess. 1981. Monoclonal antibodies against a specific surface determinant on malarial (Plasmodium knowlesi) merozoites block erythrocyte invasion. J. Immunol. 127: 212-217. (Pubitemid 11075480)
28. Collins, C. R., C. Withers-Martinez, G. A. Bentley, A. H. Batchelor, A. W. Thomas, and M. J. Blackman. 2007. Fine mapping of an epitope recognized by an invasion-inhibitory monoclonal antibody on the malaria vaccine candidate apical membrane antigen 1. J. Biol. Chem. 282: 7431-7441. (Pubitemid 47093640)
29. Druilhe, P., and S. Khusmith. 1987. Epidemiological correlation between levels of antibodies promoting merozoite phagocytosis of Plasmodium falciparum and malaria-immune status. Infect. Immun. 55: 888-891. (Pubitemid 17035422)
30. Kumaratilake, L. M., and A. Ferrante. 2000. Opsonization and phagocytosis of Plasmodium falciparum merozoites measured by flow cytometry. Clin. Diagn. Lab. Immunol. 7: 9-13. (Pubitemid 30051453)
31. Ramasamy, R., and R. Rajakaruna. 1997. Association of malaria with inactivation of [alpha]1,3-galactosyl transferase in catarrhines. Biochim. Biophys. Acta Mol. Basis Dis. 1360: 241-246. (Pubitemid 27226997)
32. Joos, C., L. Marrama, H. E. J. Polson, S. Corre, A.-M. Diatta, B. Diouf, J.-F. Trape, A. Tall, S. Longacre, and R. Perraut. 2010. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS ONE 5: e9871.
33. Crompton, P. D., S. K. Pierce, and L. H. Miller. 2010. Advances and challenges in malaria vaccine development. J. Clin. Invest. 120: 4168-4178.
34. Sagara, I., A. Dicko, R. D. Ellis, M. P. Fay, S. I. Diawara, M. H. Assadou, M. S. Sissoko, M. Kone, A. I. Diallo, R. Saye, et al. 2009. A randomized controlled phase 2 trial of the blood stage AMA1-C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 27: 3090-3098.
35. Spring, M. D., J. F. Cummings, C. F. Ockenhouse, S. Dutta, R. Reidler, E. Angov, E. Bergmann-Leitner, V. A. Stewart, S. Bittner, L. Juompan, et al. 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.
36. Cech, P. G., T. Aebi, M. S. Abdallah, M. Mpina, E. B. Machunda, N. Westerfeld, S. A. Stoffel, R. Zurbriggen, G. Pluschke, M. Tanner, et al. 2011. Virosome-formulated Plasmodium falciparum AMA-1 & CSP derived peptides as malaria vaccine: randomized phase 1b trial in semi-immune adults & children. PLoS ONE 6: e22273.
37. Takala, S. L., and C. V. Plowe. 2009. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming 'vaccine resistant malaria'. Parasite Immunol. 31: 560-573.
38. 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.
39. Miller, L. H., T. Roberts, M. Shahabuddin, and T. F. McCutchan. 1993. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Mol. Biochem. Parasitol. 59: 1-14.
40. Smythe, J. A., M. G. Peterson, R. L. Coppel, A. J. Saul, D. J. Kemp, and R. F. Anders. 1990. Structural diversity in the 45-kilodalton merozoite surface antigen of Plasmodium falciparum. Mol. Biochem. Parasitol. 39: 227-234. (Pubitemid 20073136)
41. Volkman, S. K., D. L. Hartl, D. F. Wirth, K. M. Nielsen, M. Choi, S. Batalov, Y. Zhou, D. Plouffe, K. G. Le Roch, R. Abagyan, and E. A. Winzeler. 2002. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298: 216-218.
42. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
43. Rappuoli, R. 2000. Reverse vaccinology. Curr. Opin. Microbiol. 3: 445-450.
44. Chaudhuri, R., S. Ahmed, F. A. Ansari, H. V. Singh, and S. Ramachandran. 2008. MalVac: database of malarial vaccine candidates. Malar. J. 7: 184.
45. Doolan, D. L., Y. Mu, B. Unal, S. Sundaresh, S. Hirst, C. Valdez, A. Randall, D. Molina, X. Liang, D. A. Freilich, et al. 2008. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics 8: 4680-4694.
46. Le Roch, K. G., Y. Zhou, P. L. Blair, M. Grainger, J. K. Moch, J. D. Haynes, P. De La Vega, A. A. Holder, S. Batalov, D. J. Carucci, and E. A. Winzeler. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508. (Pubitemid 37128535)
47. Bozdech, Z., M. Llinás, B. L. Pulliam, E. D. Wong, J. Zhu, and J. L. DeRisi. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1: E5.
48. Hu, G., A. Cabrera, M. Kono, S. Mok, B. K. Chaal, S. Haase, K. Engelberg, S. Cheemadan, T. Spielmann, P. R. Preiser, et al. 2010. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat. Biotechnol. 28: 91-98.
49. Florens, L., M. P. Washburn, J. D. Raine, R. M. Anthony, M. Grainger, J. D. Haynes, J. K. Moch, N. Muster, J. B. Sacci, D. L. Tabb, et al. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
50. Lasonder, E., Y. Ishihama, J. S. Andersen, A. M. W. Vermunt, A. Pain, R. W. Sauerwein, W. M. C. Eling, N. Hall, A. P. Waters, H. G. Stunnenberg, and M. Mann. 2002. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419: 537-542.
51. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783-795. (Pubitemid 38829638)
52. Gaur, D., S. Singh, S. Singh, L. Jiang, A. Diouf, and L. H. Miller. 2007. Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc. Natl. Acad. Sci. USA 104: 17789-17794. (Pubitemid 350210913)
53. Baum, J., L. Chen, J. Healer, S. Lopaticki, M. Boyle, T. Triglia, F. Ehlgen, S. A. Ralph, J. G. Beeson, and A. F. Cowman. 2009. Reticulocyte-binding protein homologue 5 - an essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum. Int. J. Parasitol. 39: 371-380.
54. Winter, G., S. Kawai, M. Haeggström, O. Kaneko, A. von Euler, S. Kawazu, D. Palm, V. Fernandez, and M. Wahlgren. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J. Exp. Med. 201: 1853-1863. (Pubitemid 41002903)
55. Bullen, H. E., C. J. Tonkin, R. A. O'Donnell, W.-H. Tham, A. T. Papenfuss, S. Gould, A. F. Cowman, B. S. Crabb, and P. R. Gilson. 2009. A novel family of Apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. J. Biol. Chem. 284: 25353-25363.
56. Dreyer, A.M., J. Beauchamp, H. Matile, and G. Pluschke. 2010. An efficient system to generate monoclonal antibodies against membrane-associated proteins by immunisation with antigen-expressing mammalian cells. BMC Biotechnol. 10: 87.
57. Matile, H., and J. R. Pink. 1990. Plasmodium falciparum malaria parasite cultures and their use in immunology. In Immunological Methods. Volume IV. I. Lefkovits, and B. Pernis, eds. Academic Press, San Diego, CA, p. 221-234.
58. Dorn, A., R. Stoffel, H. Matile, A. Bubendorf, and R. G. Ridley. 1995. Malarial haemozoin/beta-haematin supports haem polymerization in the absence of protein. Nature 374: 269-271.
59. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65: 418-420. (Pubitemid 10222999)
60. 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. (Pubitemid 36919944)
61. Moreno, R., F. Pöltl-Frank, D. Stüber, H. Matile, M. Mutz, N. A. Weiss, and G. Pluschke. 2001. Rhoptry-associated protein 1-binding monoclonal antibody raised against a heterologous peptide sequence inhibits Plasmodium falciparum growth in vitro. Infect. Immun. 69: 2558-2568. (Pubitemid 32239730)
62. Daubenberger, C. A., E. J. Tisdale, M. Curcic, D. Diaz, O. Silvie, D. Mazier, W. Eling, B. Bohrmann, H. Matile, and G. Pluschke. 2003. The N′-terminal domain of glyceraldehyde-3-phosphate dehydrogenase of the apicomplexan Plasmodium falciparum mediates GTPase Rab2-dependent recruitment to membranes. Biol. Chem. 384: 1227-1237. (Pubitemid 37121194)
63. Wang, L., C. G. Black, V. M. Marshall, and R. L. Coppel. 1999. Structural and antigenic properties of merozoite surface protein 4 of Plasmodium falciparum. Infect. Immun. 67: 2193-2200. (Pubitemid 29200472)
64. Marshall, V. M., W. Tieqiao, and R. L. Coppel. 1998. Close linkage of three merozoite surface protein genes on chromosome 2 of Plasmodium falciparum. Mol. Biochem. Parasitol. 94: 13-25. (Pubitemid 28345145)
65. Jiménez-Díaz, M.B., T. Mulet, S. Viera, V. Gómez, H. Garuti, J. Ibáñez, A. Alvarez-Doval, L. D. Shultz, A. Martínez, D. Gargallo-Viola, and I. Angulo-Barturen. 2009. Improved murine model of malaria using Plasmodium falciparum competent strains and non-myelodepleted NOD-scid IL2Rgammanull mice engrafted with human erythrocytes. Antimicrob. Agents Chemother. 53: 4533-4536.
66. Genton, B., G. Pluschke, L. Degen, A. R. Kammer, N. Westerfeld, S. L. Okitsu, S. Schroller, P. Vounatsou, M. M. Mueller, M. Tanner, and R. Zurbriggen. 2007. A randomized placebo-controlled phase Ia malaria vaccine trial of two virosome-formulated synthetic peptides in healthy adult volunteers. PLoS ONE 2: e1018.
67. Appawu, M., S. Owusu-Agyei, S. Dadzie, V. Asoala, F. Anto, K. Koram, W. Rogers, F. Nkrumah, S. L. Hoffman, and D. J. Fryauff. 2004. Malaria transmission dynamics at a site in northern Ghana proposed for testing malaria vaccines. Trop. Med. Int. Health 9: 164-170. (Pubitemid 38178026)
68. Müller, H. M., K. Früh, A. von Brunn, F. Esposito, S. Lombardi, A. Crisanti, and H. Bujard. 1989. Development of the human immune response against the major surface protein (gp190) of Plasmodium falciparum. Infect. Immun. 57: 3765-3769. (Pubitemid 20001245)
69. Ecker, A., E. S. C. Bushell, R. Tewari, and R. E. Sinden. 2008. Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol. Microbiol. 70: 209-220.
70. Gerloff, D. L., A. Creasey, S. Maslau, and R. Carter. 2005. Structural models for the protein family characterized by gamete surface protein Pfs230 of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 102: 13598-13603. (Pubitemid 41420894)
71. Llinás, M., Z. Bozdech, E. D. Wong, A. T. Adai, and J. L. DeRisi. 2006. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 34: 1166-1173.
72. Bowyer, P. W., G. M. Simon, B. F. Cravatt, and M. Bogyo. 2011. Global profiling of proteolysis during rupture of Plasmodium falciparum from the host erythrocyte. Mol. Cell. Proteomics 10: M110.001636.
73. Healer, J., S. Crawford, S. Ralph, G. McFadden, and A. F. Cowman. 2002. Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect. Immun. 70: 5751-5758.
74. Howard, R. F., D. L. Narum, M. Blackman, and J. Thurman. 1998. Analysis of the processing of Plasmodium falciparum rhoptry-associated protein 1 and localization of Pr86 to schizont rhoptries and p67 to free merozoites. Mol. Biochem. Parasitol. 92: 111-122.
75. Pirson, P. J., and M. E. Perkins. 1985. Characterization with monoclonal antibodies of a surface antigen of Plasmodium falciparum merozoites. J. Immunol. 134: 1946-1951. (Pubitemid 15128966)
76. Bouharoun-Tayoun, H., C. Oeuvray, F. Lunel, and P. Druilhe. 1995. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182: 409-418.
77. Tippett, E., L. A. Fernandes, S. J. Rogerson, and A. Jaworowski. 2007. A novel flow cytometric phagocytosis assay of malaria-infected erythrocytes. J. Immunol. Methods 325: 42-50. (Pubitemid 47238288)
78. Bouharoun-Tayoun, H., P. Attanath, A. Sabchareon, T. Chongsuphajaisiddhi, and P. Druilhe. 1990. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J. Exp. Med. 172: 1633-1641.
79. Badell, E., C. Oeuvray, A. Moreno, S. Soe, N. van Rooijen, A. Bouzidi, and P. Druilhe. 2000. Human malaria in immunocompromised mice: an in vivo model to study defense mechanisms against Plasmodium falciparum. J. Exp. Med. 192: 1653-1660.
80. Arnold, L., R. K. Tyagi, P. Meija, C. Swetman, J. Gleeson, J.-L. Pérignon, and P. Druilhe. 2011. Further improvements of the P. falciparum humanized mouse model. PLoS ONE 6: e18045.
81. Treutiger, C. J., I. Hedlund, H. Helmby, J. Carlson, A. Jepson, P. Twumasi, D. Kwiatkowski, B. M. Greenwood, and M. Wahlgren. 1992. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am. J. Trop. Med. Hyg. 46: 503-510.
82. Udeinya, I. J., L. H. Miller, I. A. McGregor, and J. B. Jensen. 1983. Plasmodium falciparum strain-specific antibody blocks binding of infected erythrocytes to amelanotic melanoma cells. Nature 303: 429-431. (Pubitemid 13094881)
83. Sugamura, K., H. Asao, M. Kondo, N. Tanaka, N. Ishii, K. Ohbo, M. Nakamura, and T. Takeshita. 1996. The interleukin-2 receptor gamma chain: its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu. Rev. Immunol. 14: 179-205. (Pubitemid 26130182)
84. Cao, X., E. W. Shores, J. Hu-Li, M. R. Anver, B. L. Kelsall, S. M. Russell, J. Drago, M. Noguchi, A. Grinberg, E. T. Bloom, et al. 1995. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 2: 223-238.
85. Kester, K. E., D. A. McKinney, N. Tornieporth, C. F. Ockenhouse, D. G. Heppner, Jr., T. Hall, B. T. Wellde, K. White, P. Sun, R. Schwenk, et al; RTS,S Malaria Vaccine Evaluation Group. 2007. A phase I/IIa safety, immunogenicity, and efficacy bridging randomized study of a two-dose regimen of liquid and lyophilized formulations of the candidate malaria vaccine RTS,S/AS02A in malaria-naïve adults. Vaccine 25: 5359-5366. (Pubitemid 46977534)
86. Persson, K. E. M., F. J. McCallum, L. Reiling, N. A. Lister, J. Stubbs, A. F. Cowman, K. Marsh, and J. G. Beeson. 2008. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J. Clin. Invest. 118: 342-351.
87. Nwuba, R. I., O. Sodeinde, C. I. Anumudu, Y. O. Omosun, A. B. Odaibo, A. A. Holder, and M. Nwagwu. 2002. The human immune response to Plasmodium falciparum includes both antibodies that inhibit merozoite surface protein 1 secondary processing and blocking antibodies. Infect. Immun. 70: 5328-5331.
88. Li, C., R. Wang, Y. Wu, D. Zhang, Z. He, and W. Pan. 2010. Epitope mapping of PfCP-2.9, an asexual blood-stage vaccine candidate of Plasmodium falciparum. Malar. J. 9: 94.
89. Kedzierski, L., C. G. Black, and R. L. Coppel. 2000. Immunization with recombinant Plasmodium yoelii merozoite surface protein 4/5 protects mice against lethal challenge. Infect. Immun. 68: 6034-6037.
90. Bracho, G., C. Zayas, L. Wang, R. Coppel, O. Pérez, and N. Petrovsky. 2009. AFCo1, a meningococcal B-derived cochleate adjuvant, strongly enhances antibody and T-cell immunity against Plasmodium falciparum merozoite surface protein 4 and 5. Malar. J. 8: 35.
91. Wu, T., C. G. Black, L. Wang, A. R. Hibbs, and R. L. Coppel. 1999. Lack of sequence diversity in the gene encoding merozoite surface protein 5 of Plasmodium falciparum. Mol. Biochem. Parasitol. 103: 243-250. (Pubitemid 29469776)
92. Kidgell, C., S. K. Volkman, J. Daily, J. O. Borevitz, D. Plouffe, Y. Zhou, J. R. Johnson, K. Le Roch, O. Sarr, O. Ndir, et al. 2006. A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog. 2: e57.
93. Polley, S. D., K. K. A. Tetteh, J. M. Lloyd, O. J. Akpogheneta, B. M. Greenwood, K. A. Bojang, and D. J. Conway. 2007. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J. Infect. Dis. 195: 279-287. (Pubitemid 46080060)
94. Hodder, A. N., P. E. Crewther, and R. F. Anders. 2001. Specificity of the protective antibody response to apical membrane antigen 1. Infect. Immun. 69: 3286-3294. (Pubitemid 32332227)
95. 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. (Pubitemid 35387930)
96. Kocken, C. H. M., C. Withers-Martinez, M. A. Dubbeld, A. van der Wel, F. Hackett, A. Valderrama, M. J. Blackman, and A.W. Thomas. 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. (Pubitemid 34790958)
97. Richards, J. S., and J. G. Beeson. 2009. The future for blood-stage vaccines against malaria. Immunol. Cell Biol. 87: 377-390.