Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW, 2009. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6: e1000048.
Bojang K, Milligan P, Pinder M, Doherty T, Leach A, Ofori-Anyinam O, Lievens M, Kester K, Schaecher K, Ballou WR, Cohen J, 2009. Five-year safety and immunogenicity of GlaxoSmithKline's candidate malaria vaccine RTS,S/AS02 following administration to semi-immune adult men living in a malaria-endemic region of The Gambia. Hum Vaccin 5: 242–247.
Brown GV, Moorthy VS, Reed Z, Mendis K, Arevalo-Herrera M, Alonso P, 2009. Priorities in research and development of vaccines against Plasmodium vivax malaria. Vaccine 27: 7228–7235.
Vekemans J, Leach A, Cohen J, 2009. Development of the RTS,S/AS malaria candidate vaccine. Vaccine 27 (Suppl 6): G67–G71.
Bejon P, Lusingu J, Olotu A, Leach A, Lievens M, Vekemans J, Mshamu S, Lang T, Gould J, Dubois MC, Demoitie MA, Stallaert JF, Vansadia P, Carter T, Njuguna P, Awuondo KO, Malabeja A, Abdul O, Gesase S, Mturi N, Drakeley CJ, Savarese B, Villafana T, Ballou WR, Cohen J, Riley EM, Lemnge MM, Marsh K, von Seidlein L, 2008. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 359: 2521–2532.
Herrera S, Bonelo A, Perlaza BL, Fernández OL, Victoria L, Lenis AM, Soto L, Hurtado H, Acuña LM, Vélez JD, Palacios R, Chen-Mok M, Corradin G, Arévalo-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. Am J Trop Med Hyg 73: 3–9.
Arevalo-Herrera M, Chitnis C, Herrera S, 2010. Current status of Plasmodium vivax vaccine. Hum Vaccin 6: 124–132.
Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM, 2007. Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77: 79–87.
Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA, 2009. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555–566.
Ejigiri I, Sinnis P, 2009. Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr Opin Microbiol 12: 401–407.
Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P, 2001. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem 276: 26784–26791.
Singh AP, Buscaglia CA, Wang Q, Levay A, Nussenzweig DR, Walker JR, Winzeler EA, Fujii H, Fontoura BM, Nussenzweig V, 2007. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131: 492–504.
Gysin J, Barnwell J, Schlesinger DH, Nussenzweig V, Nussenzweig RS, 1984. Neutralization of the infectivity of sporozoites of Plasmodium knowlesi by antibodies to a synthetic peptide. J Exp Med 160: 935–940.
McCarthy VC, Clyde DF, 1977. Plasmodium vivax: correlation of circumsporozoite precipitation (CSP) reaction with sporozoite-induced protective immunity in man. Exp Parasitol 41: 167–171.
Clyde DF, 1990. Immunity to falciparum and vivax malaria induced by irradiated sporozoites: a review of the University of Maryland studies 1971–1975. Bull World Health Organ 68: 9–12.
Herrington D, Davis J, Nardin E, Beier M, Cortese J, Eddy H, Losonsky G, Hollingdale M, Sztein M, Levine M, Nussenzweig RS, Clyde D, Edelman R, 1991. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am J Trop Med Hyg 45: 539–547.
Hoffman S, Miller L, 1996. Perspectives on malaria vaccine development. Hoffman S, ed. Malaria Vaccine Development. Washington, DC: ASM Press, 1–13.
Nussenzweig RS, Vanderberg J, Most H, Orton C, 1967. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216: 160–162.
Herrera S, Corradin G, Arevalo-Herrera M, 2007. An update on the search for a Plasmodium vivax vaccine. Trends Parasitol 23: 122–128.
Herrera S, Bonelo A, Perlaza BL, Valencia AZ, Cifuentes C, Hurtado S, Quintero G, Lopez JA, Corradin G, Arevalo-Herrera M, 2004. Use of long synthetic peptides to study the antigenicity and immunogenicity of the Plasmodium vivax circumsporozoite protein. Int J Parasitol 34: 1535–1546.
Dicko A, Sagara I, Ellis RD, Miura K, Guindo O, Kamate B, Sogoba M, Niambele MB, Sissoko M, Baby M, Dolo A, Mullen GE, Fay MP, Pierce M, Diallo DA, Saul A, Miller LH, Doumbo OK, 2008. Phase 1 study of a combination AMA1 blood stage malaria vaccine in Malian children. PLoS One 3: e1563.
Elliott SL, Suhrbier A, Miles JJ, Lawrence G, Pye SJ, Le TT, Rosenstengel A, Nguyen T, Allworth A, Burrows SR, Cox J, Pye D, Moss DJ, Bharadwaj M, 2008. Phase I trial of a CD8+ T-cell peptide epitope-based vaccine for infectious mononucleosis. J Virol 82: 1448–1457.
Wu Y, Ellis RD, Shaffer D, Fontes E, Malkin EM, Mahanty S, Fay MP, Narum D, Rausch K, Miles AP, Aebig J, Orcutt A, Muratova O, Song G, Lambert L, Zhu D, Miura K, Long C, Saul A, Miller LH, Durbin AP, 2008. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS ONE 3: e2636.
Karbach J, Gnjatic S, Bender A, Neumann A, Weidmann E, Yuan J, Ferrara CA, Hoffmann E, Old LJ, Altorki NK, Jager E, 2010. Tumor-reactive CD8+ T-cell responses after vaccination with NY-ESO-1 peptide, CpG 7909 and Montanide ISA-51: association with survival. Int J Cancer 126: 909–918.
Valmori D, Pessi A, Bianchi E, Corradin G, 1992. Use of human universally antigenic tetanus toxin T cell epitopes as carriers for human vaccination. J Immunol 149: 717–721.
Verdini A, Terenzi S, Brossard V, Roggero M, Corradin G, 2008. Oxidative folding of synthetic polypeptides S-protected as tert-butylthio derivatives. J Pept Sci 14: 1271–1282.
Atherton E, Logan JC, Sheppard RC, 1981. Peptide synthesis procedures for solid phase synthesis using N-fluorenylmethysoxycarbamylamino-acid on polymide supports: synthesis of substance P and of acyl carrier protein 65-74 decapeptide. J Chem Soc Lond Perkin Trans 1: 538–548.
Arevalo-Herrera M, Roggero MA, Gonzalez JM, Vergara J, Corradin G, Lopez JA, Herrera S, 1998. 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 92: 539–551.
Herrera S, Fernandez O, Manzano MR, Murrain B, Vergara J, Blanco P, Palacios R, Velez JD, Epstein JE, Chen-Mok M, Reed ZH, Arevalo-Herrera M, 2009. Successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. Am J Trop Med Hyg 81: 740–746.
Solarte Y, Manzano Mdel R, Rocha L, Castillo Z, James MA, Herrera S, Arevalo-Herrera M, 2007. Effects of anticoagulants on Plasmodium vivax oocyst development in Anopheles albimanus mosquitoes. Am J Trop Med Hyg 77: 242–245.
Herrera S, Fernández OL, Vera O, Cardenas W, Ramirez O, Palacios R, Chen-Mok M, Corradin G, Arévalo-Herrera M, 2011. Phase I safety and immunogenicity trial of Plasmodium vivax CS-derived long synthetic peptides adjuvanted with Montanide ISA 720 or ISA 51. Am J Trop Med Hyg 84 (Suppl 2): 12–20.
Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V, 1993. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177: 1287–1298.
Calvo-Calle JM, Oliveira GA, Watta CO, Soverow J, Parra-Lopez C, Nardin EH, 2006. A linear peptide containing minimal T- and B-cell epitopes of Plasmodium falciparum circumsporozoite protein elicits protection against transgenic sporozoite challenge. Infect Immun 74: 6929–6939.
Arevalo-Herrera M, Herrera S, 2001. Plasmodium vivax malaria vaccine development. Mol Immunol 38: 443–455.
Hurtado S, Salas ML, Romero JF, Zapata JC, Ortiz H, Arevalo-Herrera M, Herrera S, 1997. Regular production of infective sporozoites of Plasmodium falciparum and P. vivax in laboratory-bred Anopheles albimanus. Ann Trop Med Parasitol 91: 49–60.
Bongfen SE, Ntsama PM, Offner S, Smith T, Felger I, Tanner M, Alonso P, Nebie I, Romero JF, Silvie O, Torgler R, Corradin G, 2009. The N-terminal domain of Plasmodium falciparum circumsporozoite protein represents a target of protective immunity. Vaccine 27: 328–335.
Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P, 2005. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201: 27–33.
Prato S, Maxwell T, Pinzon-Charry A, Schmidt CW, Corradin G, Lopez JA, 2005. MHC class I-restricted exogenous presentation of a synthetic 102-mer malaria vaccine polypeptide. Eur J Immunol 35: 681–689.
Stevenson MM, Urban BC, 2006. Antigen presentation and dendritic cell biology in malaria. Parasite Immunol 28: 5–14.
Nardin EH, Nussenzweig V, Nussenzweig RS, Collins WE, Harinasuta KT, Tapchaisri P, Chomcharn Y, 1982. Circumsporozoite proteins of human malaria parasites Plasmodium falciparum and Plasmodium vivax. J Exp Med 156: 20–30.
Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS, 1984. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells: an in vitro assay of protective antibodies. J Immunol 132: 909–913.
Stewart MJ, Nawrot RJ, Schulman S, Vanderberg JP, 1986. Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect Immun 51: 859–864.
Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M, 1980. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71–73.
Potocnjak P, Yoshida N, Nussenzweig RS, Nussenzweig V, 1980. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med 151: 1504–1513.
Moorthy VS, Ballou WR, 2009. Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malar J 8: 312.
Sacarlal J, Aide P, Aponte JJ, Renom M, Leach A, Mandomando I, Lievens M, Bassat Q, Lafuente S, Macete E, Vekemans J, Guinovart C, Sigauque B, Sillman M, Milman J, Dubois MC, Demoitie MA, Thonnard J, Menendez C, Ballou WR, Cohen J, Alonso PL, 2009. Long-term safety and efficacy of the RTS,S/AS02A malaria vaccine in Mozambican children. J Infect Dis 200: 329–336.
Hoffman SL, Wistar R Jr, Ballou WR, Hollingdale MR, Wirtz RA, Schneider I, Marwoto HA, Hockmeyer WT, 1986. Immunity to malaria and naturally acquired antibodies to the circumsporozoite protein of Plasmodium falciparum. N Engl J Med 315: 601–606.
Nardin EH, Nussenzweig RS, McGregor IA, Bryan JH, 1979. Antibodies to sporozoites: their frequent occurrence in individuals living in an area of hyperendemic malaria. Science 206: 597–599.
Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, Molina DM, Burk CR, Waisberg M, Jasinskas A, Tan X, Doumbo S, Doumtabe D, Kone Y, Narum DL, Liang X, Doumbo OK, Miller LH, Doolan DL, Baldi P, Felgner PL, Pierce SK, 2010. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA 107: 6958–6963.
Daubersies P, Thomas AW, Millet P, Brahimi K, Langermans JA, Ollomo B, BenMohamed L, Slierendregt B, Eling W, Van Belkum A, Dubreuil G, Meis JF, Guerin-Marchand C, Cayphas S, Cohen J, Gras-Masse H, Druilhe P, 2000. Protection against Plasmodium falciparum malaria in chimpanzees by immunization with the conserved pre-erythrocytic liver-stage antigen 3. Nat Med 6: 1258–1263.
Galinski MR, Barnwell JW, 2008. Plasmodium vivax: who cares? Malar J 7 (Suppl 1): S9.
Herrera S, Perlaza BL, Bonelo A, Arevalo-Herrera M, 2002. Aotus monkeys: their great value for anti-malaria vaccines and drug testing. Int J Parasitol 32: 1625–1635.
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Plasmodium vivax circumsporozoite (CS) protein is a leading malaria vaccine candidate previously assessed in animals and humans. Here, combinations of three synthetic polypeptides corresponding to amino (N), central repeat (R), and carboxyl (C) regions of the CS protein formulated in Montanide ISA 720 or Montanide ISA 51 adjuvants were assessed for immunogenicity in rodents and primates. BALB/c mice and Aotus monkeys were divided into test and control groups and were immunized three times with doses of 50 and 100 μg of vaccine or placebo. Antigen-specific antimalarial antibodies were determined by enzyme-linked immunosorbent assay, immunofluorescent antibody test, and IFN-γ responses by enzyme-linked immunosorbent spot (ELIspot). Both vaccine formulations were highly immunogenic in both species. Mice developed better antibody responses against C and R polypeptides, whereas the N polypeptide was more immunogenic in monkeys. Anti-peptide antibodies remained detectable for several months and recognized native proteins on sporozoites. Differences between Montanide ISA 720 and Montanide ISA 51 formulations were not significant.
Financial support: This work was supported by the National Institute of Allergy and Infectious Diseases through Tropical Medicine Research Centers NIAID/TMRC grant no. 49486, the Instituto Colombiano para el Desarrollo de la Ciencia y Tecnología ‘Francisco José de Caldas' COLCIENCIAS grant no. 487-2003, and the Ministry for Social Protection/Colciencias no. 255-2004
Authors' addresses: Myriam Arévalo-Herrera, Omaira Vera, Angélica Castellanos, Nora Céspedes, Liliana Soto, and Sócrates Herrera, Instituto de Inmunología, Edificio de Microbiología, Facultad de Salud, Universidad del Valle and Malaria Vaccine and Drug Development Center, Cali, Colombia, E-mails: marevalo@inmuno.org, ovlizcano@gmail.com, ncespedes@inmuno.org, lsoto@inmuno.org, and sherrera@inmuno.org. Giampietro Corradin, Biochemistry Institute, University of Lausanne, Lausanne, Switzerland, E-mail: giampietro.corradin@unil.ch.
Reprint requests: Sócrates Herrera, Malaria Vaccine and Drug Development Center, Carrera 37 - 2Bis No. 5E - 08, Cali, Colombia, E-mail: sherrera@inmuno.org.
Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW, 2009. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6: e1000048.
Bojang K, Milligan P, Pinder M, Doherty T, Leach A, Ofori-Anyinam O, Lievens M, Kester K, Schaecher K, Ballou WR, Cohen J, 2009. Five-year safety and immunogenicity of GlaxoSmithKline's candidate malaria vaccine RTS,S/AS02 following administration to semi-immune adult men living in a malaria-endemic region of The Gambia. Hum Vaccin 5: 242–247.
Brown GV, Moorthy VS, Reed Z, Mendis K, Arevalo-Herrera M, Alonso P, 2009. Priorities in research and development of vaccines against Plasmodium vivax malaria. Vaccine 27: 7228–7235.
Vekemans J, Leach A, Cohen J, 2009. Development of the RTS,S/AS malaria candidate vaccine. Vaccine 27 (Suppl 6): G67–G71.
Bejon P, Lusingu J, Olotu A, Leach A, Lievens M, Vekemans J, Mshamu S, Lang T, Gould J, Dubois MC, Demoitie MA, Stallaert JF, Vansadia P, Carter T, Njuguna P, Awuondo KO, Malabeja A, Abdul O, Gesase S, Mturi N, Drakeley CJ, Savarese B, Villafana T, Ballou WR, Cohen J, Riley EM, Lemnge MM, Marsh K, von Seidlein L, 2008. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 359: 2521–2532.
Herrera S, Bonelo A, Perlaza BL, Fernández OL, Victoria L, Lenis AM, Soto L, Hurtado H, Acuña LM, Vélez JD, Palacios R, Chen-Mok M, Corradin G, Arévalo-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. Am J Trop Med Hyg 73: 3–9.
Arevalo-Herrera M, Chitnis C, Herrera S, 2010. Current status of Plasmodium vivax vaccine. Hum Vaccin 6: 124–132.
Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM, 2007. Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77: 79–87.
Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA, 2009. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555–566.
Ejigiri I, Sinnis P, 2009. Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr Opin Microbiol 12: 401–407.
Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P, 2001. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem 276: 26784–26791.
Singh AP, Buscaglia CA, Wang Q, Levay A, Nussenzweig DR, Walker JR, Winzeler EA, Fujii H, Fontoura BM, Nussenzweig V, 2007. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131: 492–504.
Gysin J, Barnwell J, Schlesinger DH, Nussenzweig V, Nussenzweig RS, 1984. Neutralization of the infectivity of sporozoites of Plasmodium knowlesi by antibodies to a synthetic peptide. J Exp Med 160: 935–940.
McCarthy VC, Clyde DF, 1977. Plasmodium vivax: correlation of circumsporozoite precipitation (CSP) reaction with sporozoite-induced protective immunity in man. Exp Parasitol 41: 167–171.
Clyde DF, 1990. Immunity to falciparum and vivax malaria induced by irradiated sporozoites: a review of the University of Maryland studies 1971–1975. Bull World Health Organ 68: 9–12.
Herrington D, Davis J, Nardin E, Beier M, Cortese J, Eddy H, Losonsky G, Hollingdale M, Sztein M, Levine M, Nussenzweig RS, Clyde D, Edelman R, 1991. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am J Trop Med Hyg 45: 539–547.
Hoffman S, Miller L, 1996. Perspectives on malaria vaccine development. Hoffman S, ed. Malaria Vaccine Development. Washington, DC: ASM Press, 1–13.
Nussenzweig RS, Vanderberg J, Most H, Orton C, 1967. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216: 160–162.
Herrera S, Corradin G, Arevalo-Herrera M, 2007. An update on the search for a Plasmodium vivax vaccine. Trends Parasitol 23: 122–128.
Herrera S, Bonelo A, Perlaza BL, Valencia AZ, Cifuentes C, Hurtado S, Quintero G, Lopez JA, Corradin G, Arevalo-Herrera M, 2004. Use of long synthetic peptides to study the antigenicity and immunogenicity of the Plasmodium vivax circumsporozoite protein. Int J Parasitol 34: 1535–1546.
Dicko A, Sagara I, Ellis RD, Miura K, Guindo O, Kamate B, Sogoba M, Niambele MB, Sissoko M, Baby M, Dolo A, Mullen GE, Fay MP, Pierce M, Diallo DA, Saul A, Miller LH, Doumbo OK, 2008. Phase 1 study of a combination AMA1 blood stage malaria vaccine in Malian children. PLoS One 3: e1563.
Elliott SL, Suhrbier A, Miles JJ, Lawrence G, Pye SJ, Le TT, Rosenstengel A, Nguyen T, Allworth A, Burrows SR, Cox J, Pye D, Moss DJ, Bharadwaj M, 2008. Phase I trial of a CD8+ T-cell peptide epitope-based vaccine for infectious mononucleosis. J Virol 82: 1448–1457.
Wu Y, Ellis RD, Shaffer D, Fontes E, Malkin EM, Mahanty S, Fay MP, Narum D, Rausch K, Miles AP, Aebig J, Orcutt A, Muratova O, Song G, Lambert L, Zhu D, Miura K, Long C, Saul A, Miller LH, Durbin AP, 2008. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS ONE 3: e2636.
Karbach J, Gnjatic S, Bender A, Neumann A, Weidmann E, Yuan J, Ferrara CA, Hoffmann E, Old LJ, Altorki NK, Jager E, 2010. Tumor-reactive CD8+ T-cell responses after vaccination with NY-ESO-1 peptide, CpG 7909 and Montanide ISA-51: association with survival. Int J Cancer 126: 909–918.
Valmori D, Pessi A, Bianchi E, Corradin G, 1992. Use of human universally antigenic tetanus toxin T cell epitopes as carriers for human vaccination. J Immunol 149: 717–721.
Verdini A, Terenzi S, Brossard V, Roggero M, Corradin G, 2008. Oxidative folding of synthetic polypeptides S-protected as tert-butylthio derivatives. J Pept Sci 14: 1271–1282.
Atherton E, Logan JC, Sheppard RC, 1981. Peptide synthesis procedures for solid phase synthesis using N-fluorenylmethysoxycarbamylamino-acid on polymide supports: synthesis of substance P and of acyl carrier protein 65-74 decapeptide. J Chem Soc Lond Perkin Trans 1: 538–548.
Arevalo-Herrera M, Roggero MA, Gonzalez JM, Vergara J, Corradin G, Lopez JA, Herrera S, 1998. 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 92: 539–551.
Herrera S, Fernandez O, Manzano MR, Murrain B, Vergara J, Blanco P, Palacios R, Velez JD, Epstein JE, Chen-Mok M, Reed ZH, Arevalo-Herrera M, 2009. Successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. Am J Trop Med Hyg 81: 740–746.
Solarte Y, Manzano Mdel R, Rocha L, Castillo Z, James MA, Herrera S, Arevalo-Herrera M, 2007. Effects of anticoagulants on Plasmodium vivax oocyst development in Anopheles albimanus mosquitoes. Am J Trop Med Hyg 77: 242–245.
Herrera S, Fernández OL, Vera O, Cardenas W, Ramirez O, Palacios R, Chen-Mok M, Corradin G, Arévalo-Herrera M, 2011. Phase I safety and immunogenicity trial of Plasmodium vivax CS-derived long synthetic peptides adjuvanted with Montanide ISA 720 or ISA 51. Am J Trop Med Hyg 84 (Suppl 2): 12–20.
Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V, 1993. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177: 1287–1298.
Calvo-Calle JM, Oliveira GA, Watta CO, Soverow J, Parra-Lopez C, Nardin EH, 2006. A linear peptide containing minimal T- and B-cell epitopes of Plasmodium falciparum circumsporozoite protein elicits protection against transgenic sporozoite challenge. Infect Immun 74: 6929–6939.
Arevalo-Herrera M, Herrera S, 2001. Plasmodium vivax malaria vaccine development. Mol Immunol 38: 443–455.
Hurtado S, Salas ML, Romero JF, Zapata JC, Ortiz H, Arevalo-Herrera M, Herrera S, 1997. Regular production of infective sporozoites of Plasmodium falciparum and P. vivax in laboratory-bred Anopheles albimanus. Ann Trop Med Parasitol 91: 49–60.
Bongfen SE, Ntsama PM, Offner S, Smith T, Felger I, Tanner M, Alonso P, Nebie I, Romero JF, Silvie O, Torgler R, Corradin G, 2009. The N-terminal domain of Plasmodium falciparum circumsporozoite protein represents a target of protective immunity. Vaccine 27: 328–335.
Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P, 2005. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201: 27–33.
Prato S, Maxwell T, Pinzon-Charry A, Schmidt CW, Corradin G, Lopez JA, 2005. MHC class I-restricted exogenous presentation of a synthetic 102-mer malaria vaccine polypeptide. Eur J Immunol 35: 681–689.
Stevenson MM, Urban BC, 2006. Antigen presentation and dendritic cell biology in malaria. Parasite Immunol 28: 5–14.
Nardin EH, Nussenzweig V, Nussenzweig RS, Collins WE, Harinasuta KT, Tapchaisri P, Chomcharn Y, 1982. Circumsporozoite proteins of human malaria parasites Plasmodium falciparum and Plasmodium vivax. J Exp Med 156: 20–30.
Hollingdale MR, Nardin EH, Tharavanij S, Schwartz AL, Nussenzweig RS, 1984. Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells: an in vitro assay of protective antibodies. J Immunol 132: 909–913.
Stewart MJ, Nawrot RJ, Schulman S, Vanderberg JP, 1986. Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect Immun 51: 859–864.
Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M, 1980. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71–73.
Potocnjak P, Yoshida N, Nussenzweig RS, Nussenzweig V, 1980. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med 151: 1504–1513.
Moorthy VS, Ballou WR, 2009. Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malar J 8: 312.
Sacarlal J, Aide P, Aponte JJ, Renom M, Leach A, Mandomando I, Lievens M, Bassat Q, Lafuente S, Macete E, Vekemans J, Guinovart C, Sigauque B, Sillman M, Milman J, Dubois MC, Demoitie MA, Thonnard J, Menendez C, Ballou WR, Cohen J, Alonso PL, 2009. Long-term safety and efficacy of the RTS,S/AS02A malaria vaccine in Mozambican children. J Infect Dis 200: 329–336.
Hoffman SL, Wistar R Jr, Ballou WR, Hollingdale MR, Wirtz RA, Schneider I, Marwoto HA, Hockmeyer WT, 1986. Immunity to malaria and naturally acquired antibodies to the circumsporozoite protein of Plasmodium falciparum. N Engl J Med 315: 601–606.
Nardin EH, Nussenzweig RS, McGregor IA, Bryan JH, 1979. Antibodies to sporozoites: their frequent occurrence in individuals living in an area of hyperendemic malaria. Science 206: 597–599.
Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, Molina DM, Burk CR, Waisberg M, Jasinskas A, Tan X, Doumbo S, Doumtabe D, Kone Y, Narum DL, Liang X, Doumbo OK, Miller LH, Doolan DL, Baldi P, Felgner PL, Pierce SK, 2010. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA 107: 6958–6963.
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