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High road, low road? Choices and challenges on the pathway to a malaria vaccine

Published online by Cambridge University Press:  02 February 2007

T. RICHIE
Affiliation:
Malaria Program, Naval Medical Research Center, 503 Robert Grant Avenue, Silver Spring, Maryland 20910-7500, USA

Abstract

Malaria causes much physical and economic hardship in endemic countries with billions of people at risk. A vaccine would clearly benefit these countries, reducing the requirement for hospital care and the economic impact of infection. Successful immunization with irradiated sporozoites and the fact that repeated exposure to malaria induces partial immunity to infection and high levels of protection against the clinical manifestations, suggest that a vaccine is feasible. Numerous candidate antigens have been identified but the vaccine, which has been promised to be ‘just round the corner’ for many years, remains elusive. The factors contributing to this frustratingly slow progress are discussed including gaps in the knowledge of host/parasite biology, methods to induce potent cell-mediated immune responses, the difficulties associated with defining immune correlates of protection and antigen production and delivery. Finally, the use of attenuated organism vaccines is discussed.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Adachi, K., Tsutsui, H., Kashiwamura, S., Seki, E., Nakano, H., Takeuchi, O., Takeda, K., Okumura, K., Van Kaer, L., Okamura, H., Akira, S. and Nakanishi, K. ( 2001). Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. Journal of Immunology 167, 59285934.CrossRefGoogle Scholar
Aguiar, J. C., LaBaer, J., Blair, P. L., Shamailova, V. Y., Koundinya, M., Russell, J. A., Huang, F., Mar, W., Anthony, R. M., Witney, A., Caruana, S. R., Brizuela, L., Sacci, J. B. Jr., Hoffman, S. L. and Carucci, D. J. ( 2004). High-throughput generation of P. falciparum functional molecules by recombinational cloning. Genome Research 14, 20762082.Google Scholar
Al-Olayan, E. M., Beetsma, A. L., Butcher, G. A., Sinden, R. E. and Hurd, H. ( 2002). Complete development of mosquito phases of the malaria parasite in vitro. Science 295, 677679.CrossRefGoogle Scholar
Alonso, P. L., Sacarlal, J., Aponte, J. J., Leach, A., Macete, E., Aide, P., Sigauque, B., Milman, J., Mandomando, I., Bassat, Q., Guinovart, C., Espasa, M., Corachan, S., Lievens, M., Navia, M. M., Dubois, M. C., Menendez, C., Dubovsky, F., Cohen, J., Thompson, R. and Ballou, W. R. ( 2005). Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet 366, 20122018.CrossRefGoogle Scholar
Alonso, P. L., Sacarlal, J., Aponte, J. J., Leach, A., Macete, E., Milman, J., Mandomando, I., Spiessens, B., Guinovart, C., Espasa, M., Bassat, Q., Aide, P., Ofori-Anyinam, O., Navia, M. M., Corachan, S., Ceuppens, M., Dubois, M. C., Demoitie, M. A., Dubovsky, F., Menendez, C., Tornieporth, N., Ballou, W. R., Thompson, R. and Cohen, J. ( 2004). Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364, 14111420.CrossRefGoogle Scholar
Anders, R. F., Brown, G. V., Coppel, R. L., Stahl, H. D., Bianco, A. E., Favaloro, J. M., Crewther, P. E., Culvenor, J. G. and Kemp, D. J. ( 1985). Potential vaccine antigens of the asexual blood-stages of Plasmodium falciparum. Developmental Biology Standards 62, 8189.Google Scholar
Arakawa, T., Komesu, A., Otsuki, H., Sattabongkot, J., Udomsangpetch, R., Matsumoto, Y., Tsuji, N., Wu, Y., Torii, M. and Tsuboi, T. ( 2005). Nasal immunization with a malaria transmission-blocking vaccine candidate, Pfs25, induces complete protective immunity in mice against field isolates of Plasmodium falciparum. Infection and Immunity 73, 73757380.CrossRefGoogle Scholar
Ardeshir, F., Flint, J. E. and Reese, R. T. ( 1985). Expression of Plasmodium falciparum surface antigens in Escherichia coli. Proceedings of the National Academy of Sciences, USA 82, 25182522.CrossRefGoogle Scholar
Arevalo-Herrera, M., Solarte, Y., Yasnot, M. F., Castellanos, A., Rincon, A., Saul, A., Mu, J., Long, C., Miller, L. and Herrera, S. ( 2005). Induction of transmission-blocking immunity in Aotus monkeys by vaccination with a Plasmodium vivax clinical grade PVS25 recombinant protein. American Journal of Tropical Medicine and Hygiene 73, 3237.CrossRefGoogle Scholar
Arevalo-Herrera M., Valencia, A. Z., Vergara, J., Bonelo, A., Fleischhauer, K., Gonzalez, J. M., Restrepo, J. C., Lopez, J. A., Valmori, D., Corradin, G. and Herrera, S. ( 2002). Identification of HLA-A2 restricted CD8(+) T-lymphocyte responses to Plasmodium vivax circumsporozoite protein in individuals naturally exposed to malaria. Parasite Immunology 24, 161169.CrossRefGoogle Scholar
Audran, R., Cachat, M., Lurati, F., Soe, S., Leroy, O., Corradin, G., Druilhe, P. and Spertini F. ( 2005). Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infection and Immunity 73, 80178026.CrossRefGoogle Scholar
Bai, T., Becker, M., Gupta, A., Strike, P., Murphy, V. J., Anders, R. F. and Batchelor, A. H. ( 2005). Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proceedings of the National Academy of Sciences, USA 102, 1273612741. Epub 2005 Aug 29.CrossRefGoogle Scholar
Baird, J. K. ( 1995). Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitology Today 11, 105111.CrossRefGoogle Scholar
Bahl, A., Brunk, B., Crabtree, J., Fraunholz, M. J., Gajria, B., Grant, G. R., Ginsburg, H., Gupta, D., Kissinger, J. C., Labo, P., Li, L., Mailman, M. D., Milgram, A. J., Pearson, D. S., Roos, D. S., Schug, J., Stoeckert, C. J. Jr. and Whetzel, P. ( 2003). PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Research 31, 212215.Google Scholar
Ballou, W. R., Arevalo-Herrera, M., Carucci, D., Richie, T. L., Corradin, G., Diggs, C., Druilhe, P., Giersing, B. K., Saul, A., Heppner, D. G., Kester, K. E., Lanar, D. E., Lyon, J., Hill, A. V., Pan, W. and Cohen, J. D. ( 2004). Update on the clinical development of candidate malaria vaccines. American Journal of Tropical Medicine and Hygiene 71, 239247.Google Scholar
Ballou, W. R., Hoffman, S. L., Sherwood, J. A., Hollingdale, M. R., Neva, F. A., Hockmeyer, W. T., Gordon, D. M., Schneider, I., Wirtz, R. A. and Young, J. F. ( 1987). Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet 8545, 12771281.CrossRefGoogle Scholar
Baum, J., Maier, A. G., Good, R. T., Simpson, K. M. and Cowman, A. F. ( 2005). Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathology 1, e37. Epub 2005 Dec 16.Google Scholar
Beier, J. C., Davis, J. R., Vaughan, J. A., Noden, B. H. and Beier, M. S. ( 1991 b). Quantitation of Plasmodium falciparum sporozoites transmitted in vitro by experimentally infected Anopheles gambiae and Anopheles stephensi. American Journal of Tropical Medicine and Hygiene 44, 564570.Google Scholar
Beier, J. C., Onyango, F. K., Koros, J. K., Ramadhan, M., Ogwang, R., Wirtz, R. A., Koech, D. K. and Roberts, C. R. ( 1991 a). Quantitation of malaria sporozoites transmitted in vitro during salivation by wild Afrotropical Anopheles. Medical and Veterinary Entomology 5, 7179.Google Scholar
Bejon, P., Andrews, L., Andersen, R. F., Dunachie, S., Webster, D., Walther, M., Gilbert, S. C., Peto, T. and Hill, A. V. ( 2005). Calculation of liver-to-blood inocula, parasite growth rates, and preerythrocytic vaccine efficacy, from serial quantitative polymerase chain reaction studies of volunteers challenged with malaria sporozoites. Journal of Infectious Diseases 191, 619626.CrossRefGoogle Scholar
Belyakov, I. M., Earl, P., Dzutsev, A., Kuznetsov, V. A., Lemon, M., Wyatt, L. S., Snyder, J. T., Ahlers, J. D., Franchini, G., Moss, B. and Berzofsky, J. A. ( 2003). Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proceedings of the National Academy of Sciences, USA 100, 94589463.CrossRefGoogle Scholar
Ben Mohamed, L., Thomas, A. and Druilhe, P. ( 2004). Long-term multiepitopic cytotoxic-T-lymphocyte responses induced in chimpanzees by combinations of Plasmodium falciparum liver-stage peptides and lipopeptides. Infection and Immunity 72, 43764384.Google Scholar
Bennison, B. E. and Coatney, G. R. ( 1949). Effects of X-irradiation on Plasmodium gallinaceum and Plasmodium lophurae infections in young chicks. Journal of the National Malaria Society 8, 280289.Google Scholar
BOSTON CONSULTING GROUP ( 2005). Market Assessment for Malaria Vaccines, January 19, 2005. http://www.malariavaccine.org/down-factsheets.htm
Bruna-Romero, O., Gonzalez-Aseguinolaza, G., Hafalla, J. C., Tsuji, M. and Nussenzweig, R. S. ( 2001). Complete, long-lasting protection against malaria of mice primed and boosted with two distinct viral vectors expressing the same plasmodial antigen. Proceedings of the National Academy of Sciences, USA 98, 1149111496.CrossRefGoogle Scholar
Bruna-Romero, O., Rocha, C. D., Tsuji, M. and Gazzinelli, R. T. ( 2004). Enhanced protective immunity against malaria by vaccination with a recombinant adenovirus encoding the circumsporozoite protein of Plasmodium lacking the GPI-anchoring motif. Vaccine 22, 35753584.CrossRefGoogle Scholar
Cai, Q. L., Wei, F., Lin, Y. H., Shao, D. D. and Wang, H. ( 2004). Immunogenicity of polyepitope libraries assembled by epitope shuffling: an approach to the development of chimeric gene vaccination against malaria. Vaccine 23, 267277.CrossRefGoogle Scholar
Campbell, C. C., Collins, W. E., Nguyen-Dinh, P., Barber, A. and Broderson, J. R. ( 1982). Plasmodium falciparum gametocytes from culture in vitro develop to sporozoites that are infectious to primates. Science 217, 10481050.CrossRefGoogle Scholar
Chatterjee, S., Ngonseu, E., Van Overmeir, C., Correwyn, A., Druilhe, P. and Wery, M. ( 2001). Rodent malaria in the natural host–irradiated sporozoites of Plasmodium berghei induce liver-stage specific immune responses in the natural host Grammomys surdaster and protect immunized Grammomys against P. berghei sporozoite challenge. African Journal of Medicine and Medical Sciences 30 (Suppl), 2533.Google Scholar
Cheng, Q., Lawrence, G., Reed, C., Stowers, A., Ranford-Cartwright, L., Creasey, A., Carter, R. and Saul, A. ( 1997). Measurement of Plasmodium falciparum growth rates in vivo: a test of malaria vaccines. American Journal of Tropical Medicine and Hygiene 57, 495500.CrossRefGoogle Scholar
Church, L. W., Le, T. P., Bryan, J. P., Gordon, D. M., Edelman, R., Fries, L., Davis, J. R., Herrington, D. A., Clyde, D. F., Shmuklarsky, M. J., Schneider, I., McGovern, T. W., Chulay, J. D., Ballou, W. R. and Hoffman, S. L. ( 1997). Clinical manifestations of Plasmodium falciparum malaria experimentally induced by mosquito challenge. Journal of Infectious Disease 175, 915920.CrossRefGoogle Scholar
Clyde, D. F., Most, H., McCarthy, V. C. and Vanderberg, J. P. ( 1973). Immunization of man against sporozoite-induced falciparum malaria. American Journal of the Medical Sciences 266, 169177.CrossRefGoogle Scholar
Coban, C., Philipp, M. T., Purcell, J. E., Keister, D. B., Okulate, M., Martin, D. S. and Kumar, N. ( 2004). Induction of Plasmodium falciparum transmission-blocking antibodies in nonhuman primates by a combination of DNA and protein immunizations. Infection and Immunity 72, 253259.CrossRefGoogle Scholar
Cohen, P. ( 2006). Immunity's yin and yang. A successful vaccine must first avoid being eliminated by pre-existing immunity before it can promote a protective immune response. IAVI Report 10, 15.Google Scholar
Cohen, S., McGregoria, D. and Carrington, S. ( 1961). Gamma-globulin and acquired immunity to human malaria. Nature 192, 733737.CrossRefGoogle Scholar
Collins, W. E. and Contacos, P. G. ( 1972). Immunization of monkeys against Plasmodium cynomolgi by X-irradiated sporozoites. Nature New Biology 236, 176177.CrossRefGoogle Scholar
Collins, W. E., Barnwell, J. W., Sullivan, J. S., Nace, D., Williams, T., Bounngaseng, A., Roberts, J., Strobert, E., McClure, H., Saul, A. and Long, C. A. ( 2006). Assessment of transmission-blocking activity of candidate Pvs25 vaccine using gametocytes from chimpanzees. American Journal of Tropical Medicine and Hygiene 74, 215221.Google Scholar
Collins, W. E., Galland, G. G., Barnwell, J. W., Udhayakumar, V., Sullivan, J. S., Nace, D., Tongren, J. E., Williams, T., Roberts, J., Shi, Y. P. and Lal, A. A. ( 2005). Preliminary observations on the efficacy of a recombinant multistage Plasmodium falciparum vaccine in Aotus nancymai monkeys. American Journal of Tropical Medicine and Hygiene 73, 686693.Google Scholar
Cowman, A. F. and Crabb, B. S. ( 2006). Invasion of red blood cells by malaria parasites. Cell 124, 755766.CrossRefGoogle Scholar
Crabb, B. S. and Beeson, J. G. ( 2005). Promising functional readouts of immunity in a blood-stage malaria vaccine trial. PLoS Medicine 2(): e380. Epub 2005 Nov 8.Google Scholar
Dame, J. B., Williams, J. L., McCutchan, T. F., Weber, J. L., Wirtz, R. A., Hockmeyer, W. T., Maloy, W. L., Haynes, J. D., Schneider, I. and Roberts, D. ( 1984). Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225, 593599.CrossRefGoogle Scholar
Desowitz, R. S. ( 1991). The Malaria Capers (More Tales of Parasites and People, Research and Reality). W.W. Norton & Company, New York.
Doolan, D. L., Aguiar, J. C., Weiss, W. R., Sette, A., Felgner, P. L., Regis, D. P., Quinones-Casas, P., Yates, J. R. 3rd, Blair, P. L., Richie, T. L., Hoffman, S. L. and Carucci, D. J. ( 2003 b). Utilization of genomic sequence information to develop malaria vaccines. Journal of Experimental Biology 206, 37893792.Google Scholar
Doolan, D. L. and Hoffman, S. L. ( 2000). The complexity of protective immunity against liver-stage malaria. Journal of Immunology 165, 14531462.CrossRefGoogle Scholar
Doolan, D. L. and Hoffman, S. L. ( 2001). DNA-based vaccines against malaria: status and promise of the Multi-Stage Malaria DNA Vaccine Operation. International Journal for Parasitology 31, 753762.CrossRefGoogle Scholar
Doolan, D. L., Hoffman, S. L., Southwood, S., Wentworth, P. A., Sidney, J., Chesnut, R. W., Keogh, E., Appella, E., Nutman, T. B., Lal, A. A., Gordon, D. M., Oloo, A. and Sette, A. ( 1997). Degenerate cytotoxic T cell epitopes from P. falciparum restricted by multiple HLA-A and HLA-B supertype alleles. Immunity 7, 97112.Google Scholar
Doolan, D. L. and Martinez-Alier, N. ( 2006). Immune response to pre-erythrocytic stages of malaria parasites. Current Molecular Medicine 6, 169185.CrossRefGoogle Scholar
Doolan, D. L., Sedegah, M., Hedstrom, R. C., Hobart, P., Charoenvit, Y. and Hoffman, S. L. ( 1996). Circumventing genetic restriction of protection against malaria with multigene DNA immunization: CD8+ cell-, interferon gamma-, and nitric oxide-dependent immunity. Journal of Experimental Medicine 183, 17391746.CrossRefGoogle Scholar
Doolan, D. L., Southwood, S., Freilich, D. A., Sidney, J., Graber, N. L., Shatney, L., Bebris, L., Florens, L., Dobano, C., Witney, A. A., Appella, E., Hoffman, S. L., Yates, J. R. 3rd, Carucci, D. J. and Sette, A. ( 2003 a). Identification of Plasmodium falciparum antigens by antigenic analysis of genomic and proteomic data. Proceedings of the National Academy of Sciences, USA 100, 99529957.Google Scholar
Druilhe, P., Spertini, F., Soesoe, D., Corradin, G., Mejia, P., Singh, S., Audran, R., Bouzidi, A., Oeuvray, C. and Roussilhon, C. ( 2005). A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS Medicine 2, e344. Epub 2005 Nov 8.CrossRefGoogle Scholar
Duffy, P. E., Krzych, U., Francis, S. and Fried, M. ( 2005). Malaria vaccines: using models of immunity and functional genomics tools to accelerate the development of vaccines against Plasmodium falciparum. Vaccine 23, 22352242.CrossRefGoogle Scholar
Dunachie, S. J. and Hill, A. V. ( 2003). Prime-boost strategies for malaria vaccine development. Journal of Experimental Biology 206, 37713779.CrossRefGoogle Scholar
Dunachie, S. J., Walther, M., Epstein, J. E., Keating, S., Berthoud, T., Andrews, L., Andersen, R. F., Bejon, P., Goonetilleke, N., Poulton, I., Webster, D. P., Butcher, G., Watkins, K., Sinden, R. E., Levine, G. L., Richie, T. L., Schneider, J., Kaslow, D., Gilbert, S. C., Carucci, D. J. and Hill, A. V. ( 2006). A DNA prime-MVA boost vaccine encoding TRAP but not circumsporozoite protein partially protects healthy malaria-naïve adults against P. falciparum sporozoite challenge. Infection and Immunity 74, 59335942.CrossRefGoogle Scholar
Dupuis, M., Denis-Mize, K., Woo, C., Goldbeck, C., Selby, M. J., Chen, M., Otten, G. R., Ulmer, J. B., Donnelly, J. J., Ott, G. and McDonald, D. M. ( 2000). Distribution of DNA vaccines determines their immunogenicity after intramuscular injection in mice. Journal of Immunology 165, 28502858.CrossRefGoogle Scholar
Egan, J. E., Weber, J. L., Ballou, W. R., Hollingdale, M. R., Majarian, W. R., Gordon, D. M., Maloy, W. L., Hoffman, S. L., Wirtz, R. A. and Schneider, I. ( 1987). Efficacy of murine malaria sporozoite vaccines: implications for human vaccine development. Science 236, 453456.CrossRefGoogle Scholar
Ellis, J., Ozaki, L. S., Gwadz, R. W., Cochrane, A. H., Nussenzweig, V., Nussenzweig, R. S. and Godson, G. N. ( 1983). Cloning and expression in E. coli of the malarial sporozoite surface antigen gene from Plasmodium knowlesi. Nature 302, 536538.Google Scholar
Engwerda, C. R. and Good, M. F. ( 2005). Interactions between malaria parasites and the host immune system. Current Opinions in Immunology 17, 381387.CrossRefGoogle Scholar
Ferreira, A., Schofield, L., Enea, V., Schellekens, H., van der Meide, P., Collins, W. E., Nussenzweig, R. S. and Nussenzweig, V. ( 1986). Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon. Science 232, 881884.CrossRefGoogle Scholar
Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M., Grainger, M., Haynes, J. D., Moch, J. K., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y., Gardner, M. J., Holder, A. A., Sinden, R. E., Yates, J. R. and Carucci, D. J. ( 2002). A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520526.CrossRefGoogle Scholar
Franke, E. D., Corradin, G. and Hoffman, S. L. ( 1997). Induction of protective CTL responses against the Plasmodium yoelii circumsporozoite protein by immunization with peptides. Journal of Immunology 159, 34243433.Google Scholar
Frevert, U. ( 2004). Sneaking in through the back entrance: the biology of malaria liver stages. Trends in Parasitology 20, 417424.CrossRefGoogle Scholar
Gallup, J. L. and Sachs, J. D. ( 2001). The economic burden of malaria. American Journal of Tropical Medicine and Hygiene 64, 8596.CrossRefGoogle Scholar
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. ( 2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498511.CrossRefGoogle Scholar
Genton, B., Betuela, I., Felger, I., Al-Yaman, F., Anders, R. F., Saul, A., Rare, L., Baisor, M., Lorry, K., Brown, G. V., Pye, D., Irving, D. O., Smith, T. A., Beck, H. P. and Alpers, M. P. ( 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. Journal of Infectious Disease 185, 820827.CrossRefGoogle Scholar
Giersing, B. K., Dubovsky, F., Saul, A., Denamur, F., Minor, P. and Meade, B. ( 2006). Potency assay design for adjuvanted recombinant proteins as malaria vaccines. Vaccine 24, 42644270.CrossRefGoogle Scholar
Gilbert, S. C., Moorthy, V. S., Andrews, L., Pathan, A. A., McConkey, S. J., Vuola, J. M., Keating, S. M., Berthoud, T., Webster, D., McShane, H. and Hill, A. V. ( 2006). Synergistic DNA-MVA prime-boost vaccination regimes for malaria and tuberculosis. Vaccine 24, 45544561.CrossRefGoogle Scholar
Gilbert, S. C., Schneider, J., Hannan, C. M., Hu, J. T., Plebanski, M., Sinden, R. and Hill, A. V. ( 2002). Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime-boost immunisation regimes. Vaccine 20, 10391045.CrossRefGoogle Scholar
Good, M. F. ( 2005 a). Vaccine-induced immunity to malaria parasites and the need for novel strategies. Trends in Parasitology 21, 2934.Google Scholar
Good, M. F. ( 2005 b). Genetically modified Plasmodium highlights the potential of whole parasite vaccine strategies. Trends in Immunology 26, 295297.Google Scholar
Good, M. F., Xu, H., Wykes, M. and Engwerda, C. R. ( 2005). Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annual Reviews of Immunology 23, 6999.CrossRefGoogle Scholar
Gordon, D. M., McGovern, T. W., Krzych, U., Cohen, J. C., Schneider, I., LaChance, R., Heppner, D. G., Yuan, G., Hollingdale, M. and Slaoui, M. ( 1995). Safety, immunogenicity, and efficacy of a recombinantly produced Plasmodium falciparum circumsporozoite protein-hepatitis B surface antigen subunit vaccine. Journal of Infectious Diseases 171, 15761585.CrossRefGoogle Scholar
Graves, P. M. ( 1998). Comparison of the cost-effectiveness of vaccines and insecticide impregnation of mosquito nets for the prevention of malaria. Annals of Tropical Medicine and Parasitology 92, 399410.CrossRefGoogle Scholar
Graves, P. and Gelband, H. ( 2006). Vaccines for preventing malaria (SPf66). Cochrane Database of Systematic Reviews 19, CD005966.CrossRefGoogle Scholar
Greenwood, B. ( 2005). Malaria vaccines. Evaluation and implementation. Acta Tropica 95, 298304.CrossRefGoogle Scholar
Grüner, A. C., Snounou, G., Brahimi, K., Letourneur, F., Rénia, L. and Druilhe, P. ( 2003). Pre-erythrocytic antigens of Plasmodium falciparum: from rags to riches? Trends in Parasitology 19, 7478.Google Scholar
Guerra, C. A., Snow, R. W. and Hay, S. I. ( 2005). Mapping the global extent of malaria in 2005. Trends in Parasitology 22, 353358.Google Scholar
Guerra-Neira, A., Rubio, J. M., Royo, J. R., Ortega, J. C., Aunon, A. S., Diaz, P. B. and Llanes, A. B. ( 2006). Plasmodium diversity in non-malaria individuals from the Bioko Island in Equatorial Guinea (West Central-Africa). International Journal for Health Geography 5, 27.CrossRefGoogle Scholar
Guinovart, C., Navia, M. M., Tanner, M. and Alonso, P. L. ( 2006). Malaria: burden of disease. Current Molecular Medicine 6, 137140.CrossRefGoogle Scholar
Gysin, J., Barnwell, J., Schlesinger, D. H., Nussenzweig, V. and Nussenzweig, R. S. ( 1984). Neutralization of the infectivity of sporozoites of Plasmodium knowlesi by antibodies to a synthetic peptide. Journal of Experimental Medicine 160, 935940.CrossRefGoogle Scholar
Hafalla, J. C., Rai, U., Morrot, A., Bernal-Rubio, D., Zavala, F. and Rodriguez, A. ( 2006). Priming of CD8+ T cell responses following immunization with heat-killed Plasmodium sporozoites. European Journal of Immunology 36, 11791186.CrossRefGoogle Scholar
Henning, L., Schellenberg, D., Smith, T., Henning, D., Alonso, P., Tanner, M., Mshinda, H., Beck, H. P. and Felger, I. ( 2004). A prospective study of Plasmodium falciparum multiplicity of infection and morbidity in Tanzanian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 687694.CrossRefGoogle Scholar
Heppner, D. G., Cummings, J. F., Cohen, J. D., Ballou, W. R., Ockenhouse, C. F. and Kester, K. E. ( 2004). Adjuvented RTS,S and other protein-based pre-erythrocytic stage malaria vaccines. In New Generation Vaccines ( ed. Levine, M. M., Kaper, J. B., Rappuoli, R., Liu, M. A. and Good, M. F.), pp. 851860. Marcel Dekker, New York.
Heppner, D. G. Jr., Kester, K. E., Ockenhouse, C. F., Tornieporth, N., Ofori, O., Lyon, J. A., Stewart, V. A., Dubois, P., Lanar, D. E., Krzych, U., Moris, P., Angov, E., Cummings, J. F., Leach, A., Hall, B. T., Dutta, S., Schwenk, R., Hillier, C., Barbosa, A., Ware, L. A., Nair, L., Darko, C. A., Withers, M. R., Ogutu, B., Polhemus, M. E., Fukuda, M., Pichyangkul, S., Gettyacamin, M., Diggs, C., Soisson, L., Milman, J., Dubois, M. C., Garcon, N., Tucker, K., Wittes, J., Plowe, C. V., Thera, M. A., Duombo, O. K., Pau, M. G., Goudsmit, J., Ballou, W. R. and Cohen, J. ( 2005). Towards an RTS,S-based, multi-stage, multi-antigen vaccine against falciparum malaria: progress at the Walter Reed Army Institute of Research. Vaccine 23, 22432250.CrossRefGoogle Scholar
Hermsen, C. C., de Vlas, S. J., van Gemert, G. J., Telgt, D. S., Verhage, D. F. and Sauerwein, R. W. ( 2004). Testing vaccines in human experimental malaria: statistical analysis of parasitemia measured by a quantitative real-time polymerase chain reaction. American Journal of Tropical Medicine and Hygiene 71, 196201.Google Scholar
Herrera, S., Bonelo, A., Perlaza, B. L., Fernandez, O. L., Victoria, L., Lenis, A. M., Soto, L., Hurtado, H., Acuna, L. M., Velez, J. D., Palacios, R., Chen-Mok, M., Corradin, G. and Arevalo-Herrera, M. ( 2005). Safety and elicitation of humoral and cellular responses in colombian malaria-naive volunteers by a Plasmodium vivax circumsporozoite protein-derived synthetic vaccine. American Journal of Tropical Medicine and Hygiene 73 (5 Suppl), 39.CrossRefGoogle Scholar
Hill, A. V. ( 1999). The immunogenetics of resistance to malaria. Proceedings of the Association of American Physicians 111, 272277.CrossRefGoogle Scholar
Hill, A. V. ( 2006). Pre-erythrocytic malaria vaccines: towards greater efficacy. Nature Reviews Immunology 6, 2132.CrossRefGoogle Scholar
Hill, A. V., Elvin, J., Willis, A. C., Aidoo, M., Allsopp, C. E., Gotch, F. M., Gao, X. M., Takiguchi, M., Greenwood, B. M. and Townsend, A. R. ( 1992). Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature 360, 434439.CrossRefGoogle Scholar
Hirunpetcharat, C., Wipasa, J., Sakkhachornphop, S., Nitkumhan, T., Zheng, Y. Z., Pichyangkul, S., Krieg, A. M., Walsh, D. S., Heppner, D. G. and Good, M. F. ( 2003). CpG oligodeoxynucleotide enhances immunity against blood-stage malaria infection in mice parenterally immunized with a yeast-expressed 19 kDa carboxyl-terminal fragment of Plasmodium yoelii merozoite surface protein-1 (MSP1(19)) formulated in oil-based Montanides. Vaccine 21, 29232932.CrossRefGoogle Scholar
Hisaeda, H., Yasutomo, K. and Himeno, K. ( 2005). Malaria: immune evasion by parasites. International Journal of Biochemistry and Cell Biology 37, 700706.CrossRefGoogle Scholar
Hoffman, S. L., Goh, L. M., Luke, T. C., Schneider, I., Le, T. P., Doolan, D. L., Sacci, J., de la Vega, P., Dowler, M., Paul, C., Gordon, D. M., Stoute, J. A., Church, L. W., Sedegah, M., Heppner, D. G., Ballou, W. R. and Richie, T. L. ( 2002). Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. Journal of Infectious Diseases 185, 11551164.CrossRefGoogle Scholar
Hoffman, S. L., Oster, C. N., Plowe, C. V., Woollett, G. R., Beier, J. C., Chulay, J. D., Wirtz, R. A., Hollingdale, M. R. and Mugambi, M. ( 1987). Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237, 639642.CrossRefGoogle Scholar
Hollingdale, M. R., Nardin, E. H., Tharavanij, S., Schwartz, A. L. and Nussenzweig, R. S. ( 1984). Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. Journal of Immunology 132, 909913.Google Scholar
Jafari-Guemouri, S., Boudin, C., Fievet, N., Ndiaye, P. and Deloron, P. ( 2006). Plasmodium falciparum genotype population dynamics in asymptomatic children from Senegal. Microbes and Infection Apr 19; [Epub ahead of print].CrossRefGoogle Scholar
Jafari-Guemouri, S., Ndam, N. T., Bertin, G., Renart, E., Sow, S., Le Hesran, J. Y. and Deloron, P. ( 2005). Demonstration of a high level of parasite population homology by quantification of Plasmodium falciparum alleles in matched peripheral, placental, and umbilical cord blood samples. Journal of Clinical Microbiology 43, 29802983.CrossRefGoogle Scholar
Jones, T. R. ( 1997). Quantitative aspects of the relationship between the sickle-cell gene and malaria. Parasitology Today 13, 107111.CrossRefGoogle Scholar
Kaiser, K., Matuschewski, K., Camargo, N., Ross, J. and Kappe, S. H. ( 2004). Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Molecular Microbiology 51, 12211232.CrossRefGoogle Scholar
Kaslow, D. C. ( 2002). Transmission-blocking vaccines. In Malaria Immunology ( ed. Perlmann, P. and Troye-Blomberg, M). Chemical Immunology 80, 287307.CrossRef
Keating, S. M., Bejon, P., Berthoud, T., Vuola, J. M., Todryk, S., Webster, D. P., Dunachie, S. J., Moorthy, V. S., McConkey, S. J., Gilbert, S. C. and Hill, A. V. ( 2005). Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. Journal of Immunology 175, 56755680.CrossRefGoogle Scholar
Kemp, D. J., Coppel, R. L., Cowman, A. F., Saint, R. B., Brown, G. V. and Anders, R. F. ( 1983). Expression of Plasmodium falciparum blood-stage antigens in Escherichia coli: detection with antibodies from immune humans. Proceedings of the National Academy of Sciences, USA 80, 37873791.CrossRefGoogle Scholar
Kester, K. E., McKinney, D. A., Tornieporth, N., Ockenhouse, C. F., Heppner, D. G., Hall, T., Krzych, U., Delchambre, M., Voss, G., Dowler, M. G., Palensky, J., Wittes, J., Cohen, J. and Ballou, W. R. ( 2001). RTS,S Malaria Vaccine Evaluation Group. Efficacy of recombinant circumsporozoite protein vaccine regimens against experimental Plasmodium falciparum malaria. Journal of Infectious Disease 183, 640647.Google Scholar
Kochar, D. K., Saxena, V., Singh, N., Kochar, S. K., Kumar, S. V. and Das, A. ( 2005). Plasmodium vivax malaria. Emerging Infectious Diseases 11, 132134.CrossRefGoogle Scholar
Koh, K. H., Chew, P. H. and Kiyu, A. ( 2004). A retrospective study of malaria infections in an intensive care unit of a general hospital in Malaysia. Singapore Medical Journal 45, 2836.Google Scholar
Krzych, U. and Schwenk, J. ( 2005). The dissection of CD8 T cells during liver-stage infection. Current Topics in Microbiology and Immunology 297, 124.CrossRefGoogle Scholar
Kumar, S., Epstein, J. and Richie, T. L. ( 2002 b). Vaccines against asexual stage malaria parasites. In Malaria Immunology ( ed. Perlmann, P. and Troye-Blomberg, M.), Chemical Immunology, Basel, Karger, vol 80, 262286.
Kumar, S., Epstein, J. E., Richie, T. L., Nkrumah, F. K., Soisson, L., Carucci, D. J. and Hoffman, S. L. ( 2002 a). A multilateral effort to develop DNA vaccines against falciparum malaria. Trends in Parasitology 18, 129135.Google Scholar
Kumar, S., Jones, T. R., Oakley, M. S., Zheng, H., Kuppusamy, S. P., Taye, A., Krieg, A. M., Stowers, A. W., Kaslow, D. C. and Hoffman, S. L. ( 2004). CpG oligodeoxynucleotide and Montanide ISA 51 adjuvant combination enhanced the protective efficacy of a subunit malaria vaccine. Infection and Immunity 72, 949957.CrossRefGoogle Scholar
Kyes, S., Horrocks, P. and Newbold, C. ( 2001). Antigenic variation at the infected red cell surface in malaria. Annual Review of Microbiology 55, 673707.CrossRefGoogle Scholar
Lalvani, A., Hurt, N., Aidoo, M., Kibatala, P., Tanner, M. and Hill, A. V. ( 1996). Cytotoxic T lymphocytes to Plasmodium falciparum epitopes in an area of intense and perennial transmission in Tanzania. European Journal of Immunology 26, 773779.CrossRefGoogle Scholar
Lalvani, A., Moris, P., Voss, G., Pathan, A. A., Kester, K. E., Brookes, R., Lee, E., Koutsoukos, M., Plebanski, M., Delchambre, M., Flanagan, K. L., Carton, C., Slaoui, M., Van Hoecke, C., Ballou, W. R., Hill, A. V. and Cohen, J. ( 1999). Potent induction of focused Th1-type cellular and humoral immune responses by RTS,S/SBAS2, a recombinant Plasmodium falciparum malaria vaccine. Journal of Infectious Diseases 180, 16561664.CrossRefGoogle Scholar
Lasonder, E., Ishihama, Y., Andersen, J. S., Vermunt, A. M., Pain, A., Sauerwein, R. W., Eling, W. M., Hall, N., Waters, A. P., Stunnenberg, H. G. and Mann, M. ( 2002). Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419, 537542.CrossRefGoogle Scholar
Le Roch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., De La Vega, P., Holder, A. A., Batalov, S., Carucci, D. J. and Winzeler, E. A. ( 2003). Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 15031508.CrossRefGoogle Scholar
Lomar, A. V., Vidal, J. E., Lomar, F. P., Barbas, C. V., Matos, G. J. and Boulos, M. ( 2006). Acute respiratory distress syndrome due to vivax malaria: case report and literature review. Brazilian Journal of Infectious Disease 9, 425430.Google Scholar
Lopez, J. A., Weilenman, C., Audran, R., Roggero, M. A., Bonelo, A., Tiercy, J. M., Spertini, F. and Corradin, G. ( 2001). A synthetic malaria vaccine elicits a potent CD8(+) and CD4(+) T lymphocyte immune response in humans. Implications for vaccination strategies. European Journal of Immunology 31, 19891998. (Erratum in: European Journal of Immunology (2001) 31, 2839.)Google Scholar
Luke, T. C. and Hoffman, S. L. ( 2003). Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. Journal of Experimental Biology 206, 38033808.CrossRefGoogle Scholar
Maeda, K., West, K., Hayasaka, D., Ennis, F. A. and Terajima, M. ( 2005). Recombinant adenovirus vector vaccine induces stronger cytotoxic T-cell responses than recombinant vaccinia virus vector, plasmid DNA, or a combination of these. Viral Immunology 18, 657667.CrossRefGoogle Scholar
Mahajan, R. C., Farooq, U., Dubey, M. L. and Malla, N. ( 2005). Genetic polymorphism in Plasmodium falciparum vaccine candidate antigens. Indian Journal of Pathology and Microbiology 48, 429438.Google Scholar
Mahanty, S., Saul, A. and Miller, L. H. ( 2003). Progress in the development of recombinant and synthetic blood-stage malaria vaccines. Journal of Experimental Biology 206, 37813788.CrossRefGoogle Scholar
MALARIA VACCINE TECHNOLOGY ROADMAP ( 2005). http://www.malariavaccineroadmap.net/
Malkin, E. M., Diemert, D. J., McArthur, J. H., Perreault, J. R., Miles, A. P., Giersing, B. K., Mullen, G. E., Orcutt, A., Muratova, O., Awkal, M., Zhou, H., Wang, J., Stowers, A., Long, C. A., Mahanty, S., Miller, L. H., Saul, A. and Durbin, A. P. ( 2005 b). Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. Infection and Immunity 73, 36773685.Google Scholar
Malkin, E. M., Durbin, A. P., Diemert, D. J., Sattabongkot, J., Wu, Y., Miura, K., Long, C. A., Lambert, L., Miles, A. P., Wang, J., Stowers, A., Miller, L. H. and Saul, A. ( 2005 a). Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine 23, 31313138.Google Scholar
Marsh, K. and Kinyanjui, S. ( 2006). Immune effector mechanisms in malaria. Parasite Immunology 28, 5160.CrossRefGoogle Scholar
Matuschewski, K., Ross, J., Brown, S. M., Kaiser, K., Nussenzweig, V. and Kappe, S. H. ( 2002). Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. Journal of Biological Chemistry 277, 4194841953.CrossRefGoogle Scholar
McCarthy, V. C. and Clyde, D. F. ( 1977). Plasmodium vivax: correlation of circumsporozoite precipitation (CSP) reaction with sporozoite-induced protective immunity in man. Experimental Parasitology 41, 167171.CrossRefGoogle Scholar
McConkey, S. J., Reece, W. H., Moorthy, V. S., Webster, D., Dunachie, S., Butcher, G., Vuola, J. M., Blanchard, T. J., Gothard, P., Watkins, K., Hannan, C. M., Everaere, S., Brown, K., Kester, K. E., Cummings, J., Williams, J., Heppner, D. G., Pathan, A., Flanagan, K., Arulanantham, N., Roberts, M. T., Roy, M., Smith, G. L., Schneider, J., Peto, T., Sinden, R. E., Gilbert, S. C. and Hill, A. V. ( 2003). Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nature Medicine 9, 729735.CrossRefGoogle Scholar
McGuire, W., Hill, A. V., Allsopp, C. E., Greenwood, B. M. and Kwiatkowski, D. ( 1994). Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria. Nature 371, 508510.CrossRefGoogle Scholar
Mendis, K., Sina, B. J., Marchesini, P. and Carter, R. ( 2001). The neglected burden of Plasmodium vivax malaria. American Journal of Tropical Medicine and Hygiene 64, 97106.CrossRefGoogle Scholar
Miller, L. H., Baruch, D. I., Marsh, K. and Doumbo, O. K. ( 2002). The pathogenic basis of malaria. Nature 415, 673679.CrossRefGoogle Scholar
Mockenhaupt, F. P., Cramer, J. P., Hamann, L., Stegemann, M. S., Eckert, J., Oh, N. R., Otchwemah, R. N., Dietz, E., Ehrhardt, S., Schroder, N. W., Bienzle, U. and Schumann, R. R. ( 2006). Toll-like receptor (TLR) polymorphisms in African children: Common TLR-4 variants predispose to severe malaria. Proceedings of the National Academy of Sciences, USA 103, 177182.CrossRefGoogle Scholar
Morgan, W. D., Lock, M. J., Frenkiel, T. A., Grainger, M. and Holder, A. A. ( 2004). Malaria parasite-inhibitory antibody epitopes on Plasmodium falciparum merozoite surface protein-1(19) mapped by TROSY NMR. Molecular and Biochemical Parasitology 138, 2936.CrossRefGoogle Scholar
Moorthy, V. S., Good, M. F. and Hill, A. V. ( 2004 a). Malaria vaccine developments. Lancet 363, 150156.Google Scholar
Moorthy, V. S., Imoukhuede, E. B., Milligan, P., Bojang, K., Keating, S., Kaye, P., Pinder, M., Gilbert, S. C., Walraven, G., Greenwood, B. M. and Hill, A. S. ( 2004 b). A randomised, double-blind, controlled vaccine efficacy trial of DNA/MVA ME-TRAP against malaria infection in Gambian adults. PLoS Medicine 1, e33. Epub 2004 Oct 26.Google Scholar
Morosan, S., Hez-Deroubaix, S., Lunel, F., Renia, L., Giannini, C., Van Rooijen, N., Battaglia, S., Blanc, C., Eling, W., Sauerwein, R., Hannoun, L., Belghiti, J., Brechot, C., Kremsdorf, D. and Druilhe, P. ( 2006). Liver-stage development of Plasmodium falciparum, in a humanized mouse model. Journal of Infectious Disease 193, 9961004.CrossRefGoogle Scholar
Mueller, A. K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K. and Kappe, S. H. ( 2005 b). Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proceedings of the National Academy of Sciences, USA 102, 30223037.Google Scholar
Mueller, A. K., Labaied, M., Kappe, S. H. and Matuschewski, K. ( 2005 a). Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433, 164167.Google Scholar
Mullen, G. E., Giersing, B. K., Ajose-Popoola, O., Davis, H. L., Kothe, C., Zhou, H., Aebig, J., Dobrescu, G., Saul, A. and Long, C. A. ( 2006). Enhancement of functional antibody responses to AMA1-C1/Alhydrogel, a Plasmodium falciparum malaria vaccine, with CpG oligodeoxynucleotide. Vaccine 24, 24972505.CrossRefGoogle Scholar
Mwangi, J. M., Omar, S. A. and Ranford-Cartwright, L. C. ( 2006). Comparison of microsatellite and antigen-coding loci for differentiating recrudescing Plasmodium falciparum infections from reinfections in Kenya. International Journal for Parasitology 36, 329336.CrossRefGoogle Scholar
Nussenzweig, R. S., Vanderberg, J., Most, H. and Orton, C. ( 1967). Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216, 160162.CrossRefGoogle Scholar
Nussenzweig, R. S., Vanderberg, J. P., Most, H. and Orton, C. ( 1969). Specificity of protective immunity produced by x-irradiated Plasmodium berghei sporozoites. Nature 222, 488489.CrossRefGoogle Scholar
Ockenhouse, C. F., Sun, P. F., Lanar, D. E., Wellde, B. T., Hall, B. T., Kester, K., Stoute, J. A., Magill, A., Krzych, U., Farley, L., Wirtz, R. A., Sadoff, J. C., Kaslow, D. C., Kumar, S., Church, L. W., Crutcher, J. M., Wizel, B., Hoffman, S., Lalvani, A., Hill, A. V., Tine, J. A., Guito, K. P., de Taisne, C., Anders, R., Ballou, W. R., et al. ( 1998). Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. Journal of Infectious Diseases 177, 16641673.CrossRefGoogle Scholar
Oeuvray, C., Theisen, M., Rogier, C., Trape, J. F., Jepsen, S. and Druilhe, P. ( 2000). Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infection and Immunity 68, 26172620.CrossRefGoogle Scholar
Okech, B. A., Corran, P. H., Todd, J., Joynson-Hicks, A., Uthaipibull, C., Egwang, T. G., Holder, A. A. and Riley, E. M. ( 2004). Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia. Infection and Immunity 72, 15571567.CrossRefGoogle Scholar
Orjih, A. U. and Nussenzweig, R. S. ( 1980). Immunization against rodent malaria with cryopreserved irradiated sporozoites of Plasmodium berghei. American Journal of Tropical Medicine and Hygiene 29, 343347.CrossRefGoogle Scholar
Orlandi, P. A., Klotz, F. W. and Haynes, J. D. ( 1992). A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha 2–3) Gal- sequences of glycophorin A. Journal of Cell Biology 116, 901909.CrossRefGoogle Scholar
Ophorst, O. J., Radosevic, K., Havenga, M. J., Pau, M. G., Holterman, L., Berkhout, B., Goudsmit, J. and Tsuji, M. ( 2006). Immunogenicity and protection of a recombinant human adenovirus serotype 35-based malaria vaccine against Plasmodium yoelii in mice. Infection and Immunity 74, 313320.CrossRefGoogle Scholar
Oseroff, C., Kos, F., Bui, H. H., Peters, B., Pasquetto, V., Glenn, J., Palmore, T., Sidney, J., Tscharke, D. C., Bennink, J. R., Southwood, S., Grey, H. M., Yewdell, J. W. and Sette, A. ( 2005). HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proceedings of the National Academy of Sciences, USA 102, 1398013985.CrossRefGoogle Scholar
Ozaki, L. S., Vec, P., Nussenzweig, R. S., Nussenzweig, V. and Godson, G. N. ( 1983). Structure of the Plasmodium knowlesi gene coding for the circumsporozoite protein. Cell 34, 815822.CrossRefGoogle Scholar
Patarroyo, M. E., Amador, R., Clavijo, P., Moreno, A., Guzman, F., Romero, P., Tascon, R., Franco, A., Murillo, L. A., Ponton, G. and Trujillo, G. ( 1988). A synthetic vaccine protects humans against challenge with asexual blood stages of Plasmodium falciparum malaria. Nature 332, 158161.CrossRefGoogle Scholar
Pichyangkul, S., Gettayacamin, M., Miller, R. S., Lyon, J. A., Angov, E., Tongtawe, P., Ruble, D. L., Heppner, D. G. Jr., Kester, K. E., Ballou, W. R., Diggs, C. L., Voss, G., Cohen, J. D. and Walsh, D. S. ( 2004). Pre-clinical evaluation of the malaria vaccine candidate P. falciparum MSP1(42) formulated with novel adjuvants or with alum. Vaccine 22, 38313840.Google Scholar
Polley, S. D., McRobert, L. and Sutherland, C. J. ( 2004). Vaccination for vivax malaria: targeting the invaders. Trends in Parasitology 20, 99102.CrossRefGoogle Scholar
Pombo, D. J., Lawrence, G., Hirunpetcharat, C., Rzepczyk, C., Bryden, M., Cloonan, N., Anderson, K., Mahakunkijcharoen, Y., Martin, L. B., Wilson, D., Elliott, S., Elliott, S., Eisen, D. P., Weinberg, J. B., Saul, A. and Good, M. F. ( 2002). Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 360, 610617.CrossRefGoogle Scholar
Reece, W. H., Pinder, M., Gothard, P. K., Milligan, P., Bojang, K., Doherty, T., Plebanski, M., Akinwunmi, P., Everaere, S., Watkins, K. R., Voss, G., Tornieporth, N., Alloueche, A., Greenwood, B. M., Kester, K. E., McAdam, K. P., Cohen, J. and Hill, A. V. ( 2004). A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nature Medicine 10, 406410.CrossRefGoogle Scholar
Reed, Z. H., Friede, M. and Kieny, M. P. ( 2006). Malaria vaccine development: progress and challenges. Current Molecular Medicine 6, 231245.CrossRefGoogle Scholar
Richie, T. L. ( 2004). Malaria vaccine for travelers. Travel Medicine and Infectious Diseases 2, 193210.CrossRefGoogle Scholar
Richie, T. L. and Saul, A. ( 2002). Progress and challenges for malaria vaccines. Nature 415, 694701.CrossRefGoogle Scholar
Roberts, D. M., Nanda, A., Havenga, M. J., Abbink, P., Lynch, D. M., Ewald, B. A., Liu, J., Thorner, A. R., Swanson, P. E., Gorgone, D. A., Lifton, M. A., Lemckert, A. A., Holterman, L., Chen, B., Dilraj, A., Carville, A., Mansfield, K. G., Goudsmit, J. and Barouch, D. H. ( 2006). Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441, 239243.CrossRefGoogle Scholar
Rodriguez-Morales, A. J., Sanchez, E., Vargas, M., Piccolo, C., Colina, R. and Arria, M. ( 2006). Anemia and thrombocytopenia in children with Plasmodium vivax malaria. Journal of Tropical Pediatrics 52, 4951.CrossRefGoogle Scholar
Rogers, W. O., Weiss, W. R., Kumar, A., Aguiar, J. C., Tine, J. A., Gwadz, R., Harre, J. G., Gowda, K., Rathore, D., Kumar, S. and Hoffman, S. L. ( 2002). Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. Infection and Immunity 70, 43294335.CrossRefGoogle Scholar
Sabchareon, A., Burnouf, T., Ouattara, D., Attanath, P., Bouharoun-Tayoun, H., Chantavanich, P., Foucault, C., Chongsuphajaisiddhi, T. and Druilhe, P. ( 1991). Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. American Journal of Tropical Medicine and Hygiene 45, 297308.CrossRefGoogle Scholar
Sacci, J. B. Jr., Alam, U., Douglas, D., Lewis, J., Tyrrell, D. L., Azad, A. F. and Kneteman, N. M. ( 2006). Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. International Journal for Parasitology 36, 353360.CrossRefGoogle Scholar
Sama, W., Killeen, G. and Smith, T. ( 2004). Estimating the duration of Plasmodium falciparum infection from trials of indoor residual spraying. American Journal of Tropical Medicine and Hygiene 70, 625634.Google Scholar
Sanders, P. R., Kats, L. M., Drew, D. R., O'Donnell, R. A., O'Neill, M., Maier, A. G., Coppel, R. L. and Crabb, B. S. ( 2006). A set of glycosylphosphatidyl inositol-anchored membrane proteins of Plasmodium falciparum is refractory to genetic deletion. Infection and Immunity 74, 43304338.CrossRefGoogle Scholar
Sattabongkot, J., Maneechai, N., Phunkitchar, V., Eikarat, N., Khuntirat, B., Sirichaisinthop, J., Burge, R. and Coleman, R. E. ( 2003). Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. American Journal of Tropical Medicine and Hygiene 69, 529535.Google Scholar
Saul, A. ( 1999). The role of variant surface antigens on malaria-infected red blood cells. Parasitology Today 15, 455457.CrossRefGoogle Scholar
Saul, A., Lawrence, G., Smillie, A., Rzepczyk, C. M., Reed, C., Taylor, D., Anderson, K., Stowers, A., Kemp, R., Allworth, A., Anders, R. F., Brown, G. V., Pye, D., Schoofs, P., Irving, D. O., Dyer, S. L., Woodrow, G. C., Briggs, W. R., Reber, R. and Sturchler, D. ( 1999). Human phase I vaccine trials of 3 recombinant asexual stage malaria antigens with Montanide ISA720 adjuvant. Vaccine 17, 31453159.CrossRefGoogle Scholar
Scheller, L. F. and Azad, A. F. ( 1995). Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites. Proceedings of the National Academy of Sciences, USA 92, 40664068.CrossRefGoogle Scholar
Schneider, J., Gilbert, S. C., Blanchard, T. J., Hanke, T., Robson, K. J., Hannan, C. M., Becker, M., Sinden, R., Smith, G. L. and Hill, A. V. ( 1998). Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nature Medicine 4, 397402.CrossRefGoogle Scholar
Schneider, J., Langermans, J. A., Gilbert, S. C., Blanchard, T. J., Twigg, S., Naitza, S., Hannan, C. M., Aidoo, M., Crisanti, A., Robson, K. J., Smith, G. L., Hill, A. V. and Thomas, A. W. ( 2001). A prime-boost immunisation regimen using DNA followed by recombinant modified vaccinia virus Ankara induces strong cellular immune responses against the Plasmodium falciparum TRAP antigen in chimpanzees. Vaccine 19, 45954602.CrossRefGoogle Scholar
Schofield, L., Hewitt, M. C., Evans, K., Siomos, M. A. and Seeberger, P. H. ( 2002). Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418, 785789.CrossRefGoogle Scholar
Schofield, L. and Mueller, I. ( 2006). Clinical immunity to malaria. Current Molecular Medicine 6, 205221.CrossRefGoogle Scholar
Schofield, L., Villaquiran, J., Ferreira, A., Schellekens, H., Nussenzweig, R. and Nussenzweig, V. ( 1987). Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664666.CrossRefGoogle Scholar
Schwenk, R., Asher, L. V., Chalom, I., Lanar, D., Sun, P., White, K., Keil, D., Kester, K. E., Stoute, J., Heppner, D. G. and Krzych, U. ( 2003). Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine. Parasite Immunology 25, 17125.CrossRefGoogle Scholar
Scorza, T., Grubb, K., Smooker, P., Rainczuk, A., Proll, D. and Spithill, T. W. ( 2005). Induction of strain-transcending immunity against Plasmodium chabaudi adami malaria with a multiepitope DNA vaccine. Infection and Immunity 73, 29742985.CrossRefGoogle Scholar
Sedegah, M., Brice, G. T., Rogers, W. O., Doolan, D. L., Charoenvit, Y., Jones, T. R., Majam, V. F., Belmonte, A., Lu, M., Belmonte, M., Carucci, D. J. and Hoffman, S. L. ( 2002). Persistence of protective immunity to malaria induced by DNA priming and poxvirus boosting: characterization of effector and memory CD8(+)-T-cell populations. Infection and Immunity 70, 34933499.CrossRefGoogle Scholar
Sedegah, M., Charoenvit, Y., Aguiar, J., Sacci, J., Hedstrom, R., Kumar, S., Belmonte, A., Lanar, D. E., Jones, T. R., Abot, E., Druilhe, P., Corradin, G., Epstein, J. E., Richie, T. L., Carucci, D. J. and Hoffman, S. L. ( 2004 b). Effect on antibody and T-cell responses of mixing five GMP-produced DNA plasmids and administration with plasmid expressing GM-CSF. Genes Immunology 5, 553561.Google Scholar
Sedegah, M., Charoenvit, Y., Minh, L., Belmonte, M., Majam, V. F., Abot, S., Ganeshan, H., Kumar, S., Bacon, D. J., Stowers, A., Narum, D. L., Carucci, D. J. and Rogers, W. O. ( 2004 a). Reduced immunogenicity of DNA vaccine plasmids in mixtures. Gene Therapy 11, 448456.Google Scholar
Sedegah, M., Hedstrom, R., Hobart, P. and Hoffman, S. L. ( 1994). Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. Proceedings of the National Academy of Sciences, USA 91, 98669870.CrossRefGoogle Scholar
Sedegah, M., Jones, T. R., Kaur, M., Hedstrom, R., Hobart, P., Tine, J. A. and Hoffman, S. L. ( 1998). Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proceedings of the National Academy of Sciences, USA 95, 76487653.CrossRefGoogle Scholar
Sedegah, M., Rogers, W. O., Belmonte, A., Belmonte, M., Banania, G., Patterson, N., Ferrari, M., Kaslow, D. C., Carucci, D. J., Richie, T. L. and Doolan, D. L. ( 2006). Vaxfectin enhances immunogenicity and protective efficacy of P. yoelii circumsporozoite DNA vaccines. Vaccine 24, 19211927.Google Scholar
Sedegah, M., Weiss, W., Sacci, J. B. Jr., Charoenvit, Y., Hedstrom, R., Gowda, K., Majam, V. F., Tine, J., Kumar, S., Hobart, P. and Hoffman, S. L. ( 2000). Improving protective immunity induced by DNA-based immunization: priming with antigen and GM-CSF-encoding plasmid DNA and boosting with antigen-expressing recombinant poxvirus. Journal of Immunology 164, 59055912.CrossRefGoogle Scholar
Sette, A., Newman, M., Livingston, B., McKinney, D., Sidney, J., Ishioka, G., Tangri, S., Alexander, J., Fikes, J. and Chesnut, R. ( 2002). Optimizing vaccine design for cellular processing, MHC binding and TCR recognition. Tissue Antigens 59, 443451.CrossRefGoogle Scholar
Singh, S. K., Hora, R., Belrhali, H., Chitnis, C. E. and Sharma, A. ( 2006). Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature 439, 741744.CrossRefGoogle Scholar
Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y. and Hay, S. I. ( 2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214217.CrossRefGoogle Scholar
Spirig, R., Peduzzi, E., Patarroyo, M. E., Pluschke, G. and Daubenberger, C. A. ( 2005). Structural and functional characterisation of the Toll like receptor 9 of Aotus nancymaae, a non-human primate model for malaria vaccine development. Immunogenetics 57, 283288.CrossRefGoogle Scholar
Stoute, J. A., Kester, K. E., Krzych, U., Wellde, B. T., Hall, T., White, K., Glenn, G., Ockenhouse, C. F., Garcon, N., Schwenk, R., Lanar, D. E., Sun, P., Momin, P., Wirtz, R. A., Golenda, C., Slaoui, M., Wortmann, G., Holland, C., Dowler, M., Cohen, J. and Ballou, W. R. ( 1998). Long-term efficacy and immune responses following immunization with the RTS,S malaria vaccine. Journal of Infectious Diseases 178, 11391144.CrossRefGoogle Scholar
Stoute, J. A., Slaoui, M., Heppner, D. G., Momin, P., Kester, K. E., Desmons, P., Wellde, B. T., Garcon, N., Krzych, U. and Marchand, M. ( 1997). A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. New England Journal of Medicine 336, 8691.Google Scholar
Stowers, A. and Carter, R. ( 2001). Current developments in malaria transmission-blocking vaccines. Expert Opinions on Biological Therapeutics 1, 619628.Google Scholar
Stubbs, J., Simpson, K. M., Triglia, T., Plouffe, D., Tonkin, C. J., Duraisingh, M. T., Maier, A. G., Winzeler, E. A. and Cowman, A. F. ( 2005). Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309, 13841387.Google Scholar
Sun, P., Schwenk, R., White, K., Stoute, J. A., Cohen, J., Ballou, W. R., Voss, G., Kester, K. E., Heppner, D. G. and Krzych, U. ( 2003). Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. Journal of Immunology 171, 69616967.CrossRefGoogle Scholar
Targett, G. A. ( 2005). Malaria vaccines 1985–2005: a full circle? Trends in Parasitology 21, 499503.Google Scholar
Todryk, S. M. and Walther, M. ( 2005). Building better T-cell-inducing malaria vaccines. Immunology 115, 163169.CrossRefGoogle Scholar
Tolia, N. H., Enemark, E. J., Sim, B. K. and Joshua-Tor, L. ( 2005). Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122, 183193. (Erratum in Cell 2005; 122, 485.)CrossRefGoogle Scholar
Triglia, T., Healer, J., Caruana, S. R., Hodder, A. N., Anders, R. F., Crabb, B. S. and Cowman, A. F. ( 2000). Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Molecular Microbiology 38, 706718.CrossRefGoogle Scholar
Tsai, C. W., Duggan, P. F., Shimp, R. L. Jr., Miller, L. H. and Narum, D. L. ( 2006). Overproduction of Pichia pastoris or Plasmodium falciparum protein disulfide isomerase affects expression, folding and O-linked glycosylation of a malaria vaccine candidate expressed in P. pastoris. Journal of Biotechnology 121, 458470.CrossRefGoogle Scholar
Tsuboi, T., Tachibana, M., Kaneko, O. and Torii, M. ( 2003). Transmission-blocking vaccine of vivax malaria. Parasitology International 52, 111.CrossRefGoogle Scholar
Tsuji, M. and Zavala, F. ( 2003). T cells as mediators of protective immunity against liver stages of Plasmodium. Trends in Parasitology 19, 8893.CrossRefGoogle Scholar
Vanderberg, J. P. and Frevert, U. ( 2004). Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. International Journal for Parasitology 34, 991996.CrossRefGoogle Scholar
Van der Kolk, M., De Vlas, S. J., Saul, A., van de Vegte-Bolmer, M., Eling, W. M. and Sauerwein, R. W. ( 2005). Evaluation of the standard membrane feeding assay (SMFA) for the determination of malaria transmission-reducing activity using empirical data. Parasitology 130, 1322.CrossRefGoogle Scholar
Van Dijk, M. R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M. W., van Schaijk, B., van Gemert, G. J., Sauerwein, R. W., Mota, M. M., Waters, A. P. and Janse, C. J. ( 2005). Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proceedings of the National Academy of Sciences, USA 102, 1219412199.CrossRefGoogle Scholar
Verhage, D. F., Telgt, D. S., Bousema, J. T., Hermsen, C. C., van Gemert, G. J., van der Meer, J. W. and Sauerwein, R. W. ( 2005). Clinical outcome of experimental human malaria induced by Plasmodium falciparum-infected mosquitoes. Netherlands Journal of Medicine 63, 5258.Google Scholar
Vuola, J. M., Keating, S., Webster, D. P., Berthoud, T., Dunachie, S., Gilbert, S. C. and Hill, A. V. ( 2005). Differential immunogenicity of various heterologous prime-boost vaccine regimens using DNA and viral vectors in healthy volunteers. Journal of Immunology 174, 449455.CrossRefGoogle Scholar
Walther, M. ( 2006). Advances in vaccine development against the pre-erythrocytic stage of Plasmodium falciparum malaria. Expert Reviews of Vaccines 5, 8193.CrossRefGoogle Scholar
Walther, M., Thompson, F. M., Dunachie, S., Keating, S., Todryk, S., Berthoud, T., Andrews, L., Andersen, R. F., Moore, A., Gilbert, S. C., Poulton, I., Dubovsky, F., Tierney, E., Correa, S., Huntcooke, A., Butcher, G., Williams, J., Sinden, R. E. and Hill, A. V. ( 2006). Safety, immunogenicity, and efficacy of prime-boost immunization with recombinant poxvirus FP9 and modified vaccinia virus Ankara encoding the full-length Plasmodium falciparum circumsporozoite protein. Infection and Immunity 74, 27062716.CrossRefGoogle Scholar
Wang, L., Goschnick, M. W. and Coppel, R. L. ( 2004). Oral immunization with a combination of Plasmodium yoelii merozoite surface proteins 1 and 4/5 enhances protection against lethal malaria challenge. Infection and Immunity 72, 61726175.CrossRefGoogle Scholar
Wang, R., Epstein, J., Charoenvit, Y., Baraceros, F. M., Rahardjo, N., Gay, T., Banania, J. G., Chattopadhyay, R., de la Vega, P., Richie, T. L., Tornieporth, N., Doolan, D. L., Kester, K. E., Heppner, D. G, Norman, J., Carucci, D. J., Cohen, J. D. and Hoffman, S. L. ( 2004). Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. Journal of Immunology 172, 55615569.CrossRefGoogle Scholar
Wang, R., Richie, T. L., Baraceros, M. F., Rahardjo, N., Gay, T., Banania, J. G., Charoenvit, Y., Epstein, J. E., Luke, T., Freilich, D. A., Norman, J. and Hoffman, S. L. ( 2005). Boosting of DNA vaccine-elicited gamma interferon responses in humans by exposure to malaria parasites. Infection and Immunity 73, 28632872.CrossRefGoogle Scholar
Webster, D. P., Dunachie, S., Vuola, J. M., Berthoud, T., Keating, S., Laidlaw, S. M., McConkey, S. J., Poulton, I., Andrews, L., Andersen, R. F., Bejon, P., Butcher, G., Sinden, R., Skinner, M. A., Gilbert, S. C. and Hill, A. V. ( 2005). Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proceedings of the National Academy of Sciences, USA 102, 48364841.CrossRefGoogle Scholar
Weiss, W. R., Ishii, K. J., Hedstrom, R. C., Sedegah, M., Ichino, M., Barnhart, K., Klinman, D. M. and Hoffman, S. L. ( 1998). A plasmid encoding murine granulocyte-macrophage colony-stimulating factor increases protection conferred by a malaria DNA vaccine. Journal of Immunology 161, 23252332.Google Scholar
WHO ( 2005). World Malaria Report 2005 (http://rbm.who.int/wmr2005/index.html), ISBN 92 4 159319 9.
WHO ( 2006). New Vaccines against Infectious Diseases: Research and Development Status; IVR, WHO, April 2005, updated February 2006, http://www.who.int/vaccine_research/documents/en/Status_Table.pdf. [The malaria vaccine section of this table, which lists malaria vaccines in clinical development, updates a more comprehensive table published in October, 2004 that additionally includes malaria vaccines in research and preclinical development, entitled “Portfolio of candidate malaria vaccines currently in development” (the rainbow table), http://www.who.int/vaccine_research/documents/malaria_table.pdf]
Wilson, N. S., Behrens, G. M., Lundie, R. J., Smith, C. M., Waithman, J., Young, L., Forehan, S. P., Mount, A., Steptoe, R. J., Shortman, K. D., de Koning-Ward, T. F., Belz, G. T., Carbone, F. R., Crabb, B. S., Heath, W. R. and Villadangos, J. A. ( 2006). Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nature Immunology 7, 165172.CrossRefGoogle Scholar
Wizel, B., Houghten, R. A., Parker, K. C., Coligan, J. E., Church, P., Gordon, D. M., Ballou, W. R. and Hoffman, S. L. ( 1995). Irradiated sporozoite vaccine induces HLA-B8-restricted cytotoxic T lymphocyte responses against two overlapping epitopes of the Plasmodium falciparum sporozoite surface protein 2. Journal of Experimental Medicine 182, 14351445.CrossRefGoogle Scholar
Yoshida, N., Nussenzweig, R. S., Potocnjak, P., Nussenzweig, V. and Aikawa, M. ( 1980). Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207, 7173.CrossRefGoogle Scholar
Zhang, D. and Pan, W. ( 2005). Evaluation of three Pichia pastoris-expressed Plasmodium falciparum merozoite proteins as a combination vaccine against infection with blood-stage parasites. Infection and Immunity 73, 65306536.CrossRefGoogle Scholar