Towards the development of a fully protective Plasmodium falciparum antimalarial vaccine

References

• WHO. World Malaria Report. WHO, Geneva, Switzerland (2011).
   Google Scholar
• Murray CJ, Rosenfeld LC, Lim SS et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379(9814), 413–431 (2012).
   PubMed Web of Science ®Google Scholar
• Vaughan AM, Aly AS, Kappe SH. Malaria parasite pre-erythrocytic stage infection: gliding and hiding. Cell Host Microbe 4(3), 209–218 (2008).
   Google Scholar
• Farrow RE, Green J, Katsimitsoulia Z, Taylor WR, Holder AA, Molloy JE. The mechanism of erythrocyte invasion by the malarial parasite, Plasmodium falciparum. Semin. Cell Dev. Biol. 22(9), 953–960 (2011).
   Google Scholar
• Collins CR, Blackman MJ. Apicomplexan AMA1 in host cell invasion: a model at the junction? Cell Host Microbe 10(6), 531–533 (2011).
   Google Scholar
• Baum J, Richard D, Healer J et al. A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J. Biol. Chem. 281(8), 5197–5208 (2006).
   Google Scholar
• Herrington DA, Clyde DF, Losonsky G et al. Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature 328(6127), 257–259 (1987).
   PubMed Web of Science ®Google Scholar
• Nardin EH, Nussenzweig RS. T cell responses to pre-erythrocytic stages of malaria: role in protection and vaccine development against pre-erythrocytic stages. Annu. Rev. Immunol. 11, 687–727 (1993).
   PubMed Web of Science ®Google Scholar
• Nardin E. The past decade in malaria synthetic peptide vaccine clinical trials. Hum. Vaccin. 6(1), 27–38 (2010).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Romero P, Torres ML et al. Induction of protective immunity against experimental infection with malaria using synthetic peptides. Nature 328(6131), 629–632 (1987).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Amador R, Clavijo P et al. A synthetic vaccine protects humans against challenge with asexual blood stages of Plasmodium falciparum malaria. Nature 332(6160), 158–161 (1988).
   PubMed Web of Science ®Google Scholar
• Amador R, Moreno A, Murillo LA et al. Safety and immunogenicity of the synthetic malaria vaccine SPf66 in a large field trial. J. Infect. Dis. 166(1), 139–144 (1992).
   PubMed Web of Science ®Google Scholar
• Valero MV, Amador LR, Galindo C et al. Vaccination with SPf66, a chemically synthesised vaccine, against Plasmodium falciparum malaria in Colombia. Lancet 341(8847), 705–710 (1993).
   PubMed Web of Science ®Google Scholar
• Noya O, Gabaldón Berti Y, Alarcón de Noya B et al. A population-based clinical trial with the SPf66 synthetic Plasmodium falciparum malaria vaccine in Venezuela. J. Infect. Dis. 170(2), 396–402 (1994).
   PubMed Web of Science ®Google Scholar
• Sempértegui F, Estrella B, Moscoso J et al. Safety, immunogenicity and protective effect of the SPf66 malaria synthetic vaccine against Plasmodium falciparum infection in a randomized double-blind placebo-controlled field trial in an endemic area of Ecuador. Vaccine 12(4), 337–342 (1994).
   PubMed Web of Science ®Google Scholar
• Alonso PL, Smith T, Schellenberg JR et al. Randomised trial of efficacy of SPf66 vaccine against Plasmodium falciparum malaria in children in southern Tanzania. Lancet 344(8931), 1175–1181 (1994).
   PubMed Web of Science ®Google Scholar
• Valero MV, Amador R, Aponte JJ et al. Evaluation of SPf66 malaria vaccine during a 22-month follow-up field trial in the Pacific coast of Colombia. Vaccine 14(15), 1466–1470 (1996).
   PubMed Web of Science ®Google Scholar
• Acosta CJ, Galindo CM, Schellenberg D et al. Evaluation of the SPf66 vaccine for malaria control when delivered through the EPI scheme in Tanzania. Trop. Med. Int. Health 4(5), 368–376 (1999).
   PubMed Web of Science ®Google Scholar
• D’Alessandro U, Leach A, Drakeley CJ et al. Efficacy trial of malaria vaccine SPf66 in Gambian infants. Lancet 346(8973), 462–467 (1995).
   PubMed Web of Science ®Google Scholar
• Nosten F, Luxemburger C, Kyle DE et al. Randomised double-blind placebo-controlled trial of SPf66 malaria vaccine in children in northwestern Thailand. Shoklo SPf66 Malaria Vaccine Trial Group. Lancet 348(9029), 701–707 (1996).
   PubMed Web of Science ®Google Scholar
• Kashala O, Amador R, Valero MV et al. Safety, tolerability and immunogenicity of new formulations of the Plasmodium falciparum malaria peptide vaccine SPf66 combined with the immunological adjuvant QS-21. Vaccine 20(17–18), 2263–2277 (2002).
   PubMed Web of Science ®Google Scholar
• Bermúdez A, Reyes C, Guzmán F et al. Synthetic vaccine update: applying lessons learned from recent SPf66 malarial vaccine physicochemical, structural and immunological characterization. Vaccine 25(22), 4487–4501 (2007).
   Google Scholar
• Calvo M, Guzman F, Perez E, Segura CH, Molano A, Patarroyo ME. Specific interactions of synthetic peptides derived from P. falciparum merozoite proteins with human red blood cells. Pept. Res. 4(6), 324–333 (1991).
   PubMedGoogle Scholar
• Gardner MJ, Hall N, Fung E et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419(6906), 498–511 (2002).
   PubMed Web of Science ®Google Scholar
• Bozdech Z, Llinás M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1(1), E5 (2003).
   PubMed Web of Science ®Google Scholar
• Lasonder E, Janse CJ, van Gemert GJ et al. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog. 4(10), e1000195 (2008).
   Google Scholar
• Garcia JE, Puentes A, Patarroyo ME. Developmental biology of sporozoite-host interactions in Plasmodium falciparum malaria: implications for vaccine design. Clin. Microbiol. Rev. 19(4), 686–707 (2006).
   PubMed Web of Science ®Google Scholar
• Curtidor H, Vanegas M, Alba MP, Patarroyo ME. Functional, immunological and three-dimensional analysis of chemically synthesised sporozoite peptides as components of a fully-effective antimalarial vaccine. Curr. Med. Chem. 18(29), 4470–4502 (2011).
   PubMed Web of Science ®Google Scholar
• Rodriguez LE, Curtidor H, Urquiza M, Cifuentes G, Reyes C, Patarroyo ME. Intimate molecular interactions of P. falciparum merozoite proteins involved in invasion of red blood cells and their implications for vaccine design. Chem. Rev. 108(9), 3656–3705 (2008).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Patarroyo MA. Emerging rules for subunit-based, multiantigenic, multistage chemically synthesized vaccines. Acc. Chem. Res. 41(3), 377–386 (2008).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Bermúdez A, Patarroyo MA. Structural and immunological principles leading to chemically synthesized, multiantigenic, multistage, minimal subunit-based vaccine development. Chem. Rev. 111(5), 3459–3507 (2011).
   PubMed Web of Science ®Google Scholar
• Tham WH, Healer J, Cowman AF. Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends Parasitol. 28(1), 23–30 (2012).
   PubMed Web of Science ®Google Scholar
• Iyer J, Grüner AC, Rénia L, Snounou G, Preiser PR. Invasion of host cells by malaria parasites: a tale of two protein families. Mol. Microbiol. 65(2), 231–249 (2007).
   Web of Science ®Google Scholar
• Hayton K, Gaur D, Liu A et al. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4(1), 40–51 (2008).
   PubMed Web of Science ®Google Scholar
• Chen L, Lopaticki S, Riglar DT et al. An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum. PLoS Pathog. 7(9), e1002199 (2011).
   PubMed Web of Science ®Google Scholar
• Crosnier C, Bustamante LY, Bartholdson SJ et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480(7378), 534–537 (2011).
   PubMed Web of Science ®Google Scholar
• Srinivasan P, Beatty WL, Diouf A et al. Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc. Natl Acad. Sci. USA 108(32), 13275–13280 (2011).
   PubMed Web of Science ®Google Scholar
• Tonkin ML, Roques M, Lamarque MH et al. Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333(6041), 463–467 (2011).
   PubMed Web of Science ®Google Scholar
• Lamarque M, Besteiro S, Papoin J et al. The RON2–AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathog. 7(2), e1001276 (2011).
   PubMed Web of Science ®Google Scholar
• Tyler JS, Boothroyd JC. The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathog. 7(2), e1001282 (2011).
   Google Scholar
• Perlmann H, Berzins K, Wahlgren M et al. Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. J. Exp. Med. 159(6), 1686–1704 (1984).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Cifuentes G, Martínez NL, Patarroyo MA. Atomic fidelity of subunit-based chemically synthesized antimalarial vaccine components. Prog. Biophys. Mol. Biol. 102(1), 38–44 (2010).
   PubMed Web of Science ®Google Scholar
• Cole-Tobian JL, Michon P, Biasor M et al. Strain-specific duffy binding protein antibodies correlate with protection against infection with homologous compared to heterologous Plasmodium vivax strains in Papua New Guinean children. Infect. Immun. 77(9), 4009–4017 (2009).
   PubMed Web of Science ®Google Scholar
• Fowkes FJ, Richards JS, Simpson JA, Beeson JG. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med. 7(1), e1000218 (2010).
   PubMed Web of Science ®Google Scholar
• Cifuentes G, Bermúdez A, Rodriguez R, Patarroyo MA, Patarroyo ME. Shifting the polarity of some critical residues in malarial peptides’ binding to host cells is a key factor in breaking conserved antigens’ code of silence. Med. Chem. 4(3), 278–292 (2008).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Alba MP, Vargas LE, Silva Y, Rosas J, Rodríguez R. Peptides inducing short-lived antibody responses against Plasmodium falciparum malaria have shorter structures and are read in a different MHC II functional register. Biochemistry 44(18), 6745–6754 (2005).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Bermúdez A, Salazar LM, Espejo F. High non-protective, long-lasting antibody levels in malaria are associated with haplotype shifting in MHC-peptide-TCR complex formation: a new mechanism for immune evasion. Biochimie 88(7), 775–784 (2006).
   Google Scholar
• Patarroyo ME, Cifuentes G, Piraján C, Moreno-Vranich A, Vanegas M. Atomic evidence that modification of H-bonds established with amino acids critical for host-cell binding induces sterile immunity against malaria. Biochem. Biophys. Res. Commun. 394(3), 529–535 (2010).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Almonacid H, Moreno-Vranich A. The role of amino acid electron-donor/acceptor atoms in host-cell binding peptides is associated with their 3D structure and HLA-binding capacity in sterile malarial immunity induction. Biochem. Biophys. Res. Commun. 417(3), 938–944 (2012).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Cifuentes G, Rodríguez R. Structural characterisation of sporozoite components for a multistage, multiepitope, antimalarial vaccine. Int. J. Biochem. Cell Biol. 40(3), 543–557 (2008).
   PubMed Web of Science ®Google Scholar
• Genton B, Al-Yaman F, Betuela I et al. Safety and immunogenicity of a three-component blood-stage malaria vaccine (MSP1, MSP2, RESA) against Plasmodium falciparum in Papua New Guinean children. Vaccine 22(1), 30–41 (2003).
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Imoukhuede EB, Milligan P et al. A randomised, double-blind, controlled vaccine efficacy trial of DNA/MVA ME-TRAP against malaria infection in Gambian adults. PLoS Med. 1(2), e33 (2004).
   PubMedGoogle Scholar
• Bejon P, Mwacharo J, Kai O et al. A Phase 2b randomised trial of the candidate malaria vaccines FP9 ME-TRAP and MVA ME-TRAP among children in Kenya. PLoS Clin. Trials 1(6), e29 (2006).
   PubMedGoogle Scholar
• Coppel RL. Vaccinating with the genome: a Sisyphean task? Trends Parasitol. 25(5), 205–212 (2009).
   PubMed Web of Science ®Google Scholar
• Holder AA. The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136(12), 1445–1456 (2009).
   PubMed Web of Science ®Google Scholar
• Richards JS, Beeson JG. The future for blood-stage vaccines against malaria. Immunol. Cell Biol. 87(5), 377–390 (2009).
   PubMed Web of Science ®Google Scholar
• Suárez CF, Patarroyo ME, Trujillo E et al. Owl monkey MHC-DRB exon 2 reveals high similarity with several HLA-DRB lineages. Immunogenetics 58(7), 542–558 (2006).
   PubMed Web of Science ®Google Scholar
• Stern LJ, Brown JH, Jardetzky TS et al. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature 368(6468), 215–221 (1994).
   PubMed Web of Science ®Google Scholar
• Corper AL, Stratmann T, Apostolopoulos V et al. A structural framework for deciphering the link between I-Ag7 and autoimmune diabetes. Science 288(5465), 505–511 (2000).
   PubMed Web of Science ®Google Scholar
• Rudolph MG, Stanfield RL, Wilson IA. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24, 419–466 (2006).
   PubMed Web of Science ®Google Scholar
• Marrack P, Scott-Browne JP, Dai S, Gapin L, Kappler JW. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu. Rev. Immunol. 26, 171–203 (2008).
   Google Scholar
• Sant AJ, Chaves FA, Jenks SA et al. The relationship between immunodominance, DM editing, and the kinetic stability of MHC class II:peptide complexes. Immunol. Rev. 207, 261–278 (2005).
   PubMed Web of Science ®Google Scholar
• Patarroyo ME, Cifuentes G, Salazar LM, Espejo F, Alba MP, Bermúdez A. Based on HLA-DR beta1* allele binding specificities, striking differences in distance and TCR Contacting Residue Orientation can be observed in modified protection-inducing malarial synthetic peptides. Curr. Med. Chem. 12(24), 2849–2865 (2005).
   Google Scholar
• Epstein JE, Tewari K, Lyke KE et al. Live attenuated malaria vaccine designed to protect through hepatic CD8? T cell immunity. Science 334(6055), 475–480 (2011).
   PubMed Web of Science ®Google Scholar
• Casares S, Brumeanu TD, Richie TL. The RTS,S malaria vaccine. Vaccine 28(31), 4880–4894 (2010).
   PubMed Web of Science ®Google Scholar
• Ballou WR. The development of the RTS,S malaria vaccine candidate: challenges and lessons. Parasite Immunol. 31(9), 492–500 (2009).
   PubMed Web of Science ®Google Scholar
• Bejon P, Lusingu J, Olotu A et al. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N. Engl. J. Med. 359(24), 2521–2532 (2008).
   PubMed Web of Science ®Google Scholar
• Sacarlal J, Aide P, Aponte JJ et al. Long-term safety and efficacy of the RTS,S/AS02A malaria vaccine in Mozambican children. J. Infect. Dis. 200(3), 329–336 (2009).
   PubMed Web of Science ®Google Scholar
• Polhemus ME, Remich SA, Ogutu BR et al. Evaluation of RTS,S/AS02A and RTS,S/AS01B in adults in a high malaria transmission area. PLoS ONE 4(7), e6465 (2009).
   PubMed Web of Science ®Google Scholar
• Asante KP, Abdulla S, Agnandji S et al. Safety and efficacy of the RTS,S/AS01E candidate malaria vaccine given with expanded-programme-on-immunisation vaccines: 19 month follow-up of a randomised, open-label, Phase 2 trial. Lancet Infect. Dis. 11(10), 741–749 (2011).
   PubMed Web of Science ®Google Scholar
• Agnandji ST, Lell B, Soulanoudjingar SS et al. First results of Phase 3 trial of RTS, S/AS01 malaria vaccine in African children. N. Engl. J. Med. 365(20), 1863–1875 (2011).
   PubMed Web of Science ®Google Scholar
• Bojang KA, Milligan PJ, Pinder M et al.; RTS, S Malaria Vaccine Trial Team. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 358(9297), 1927–1934 (2001).
   PubMed Web of Science ®Google Scholar
• Alonso PL, Sacarlal J, Aponte JJ et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364(9443), 1411–1420 (2004).
   PubMed Web of Science ®Google Scholar
• White NJ. A vaccine for malaria. N. Engl. J. Med. 365(20), 1926–1927 (2011).
   PubMed Web of Science ®Google Scholar
• Duncan CJ, Hill AV. What is the efficacy of the RTS,S malaria vaccine? BMJ 343, d7728 (2011).
   Google Scholar
• Anders RF. The case for a subunit vaccine against malaria. Trends Parasitol. 27(8), 330–334 (2011).
   Google Scholar
• Butler D. Malaria vaccine results face scrutiny. Nature 478(7370), 439–440 (2011).
   Google Scholar
• Nussenzweig V, Good MF, Hill AV. Mixed results for a malaria vaccine. Nat. Med. 17(12), 1560–1561 (2011).
   PubMed Web of Science ®Google Scholar
• [No authors listed]. A vaccine for malaria: prospects and predicaments. Lancet 378(9802), 1528 (2011).
   Google Scholar
• Recker M, Buckee CO, Serazin A et al. Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathog. 7(3), e1001306 (2011).
   PubMed Web of Science ®Google Scholar
• Healer J, Murphy V, Hodder AN et al. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum. Mol. Microbiol. 52(1), 159–168 (2004).
   PubMed Web of Science ®Google Scholar
• Tonon AP, Hoffmann EH, Silveira LA et al. Plasmodium falciparum: sequence diversity and antibody recognition of the Merozoite surface protein-2 (MSP-2) in Brazilian Amazonia. Exp. Parasitol. 108(3-4), 114–125 (2004).
   Google Scholar
• Miller LH, Roberts T, Shahabuddin M, McCutchan TF. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Mol. Biochem. Parasitol. 59(1), 1–14 (1993).
   PubMed Web of Science ®Google Scholar
• Barfod L, Dalgaard MB, Pleman ST, Ofori MF, Pleass RJ, Hviid L. Evasion of immunity to Plasmodium falciparum malaria by IgM masking of protective IgG epitopes in infected erythrocyte surface-exposed PfEMP1. Proc. Natl Acad. Sci. USA 108(30), 12485–12490 (2011).
   PubMed Web of Science ®Google Scholar
• Patarroyo MA, Bermúdez A, López C, Yepes G, Patarroyo ME. 3D analysis of the TCR/pMHC II complex formation in monkeys vaccinated with the first peptide inducing sterilizing immunity against human malaria. PLoS ONE 5(3), e9771 (2010).
   PubMed Web of Science ®Google Scholar
• Schwartz L, Brown GV, Genton B, Moorthy VS. A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar. J. 11, 11 (2012).
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Reed Z, Smith PG; WHO Malaria Vaccine Advisory Committee. MALVAC 2008: Measures of efficacy of malaria vaccines in Phase 2b and Phase 3 trials – scientific, regulatory and public health perspectives. Vaccine 27(5), 624–628 (2009).
   PubMed Web of Science ®Google Scholar
• Menéndez C, Moorthy VS, Reed Z, Bardají A, Alonso P, Brown GV. Development of vaccines to prevent malaria in pregnant women: WHO MALVAC meeting report. Expert Rev. Vaccines 10(9), 1271–1280 (2011).
   PubMed Web of Science ®Google Scholar
• Cifuentes G, Guzmán F, Alba MP, Salazar LM, Patarroyo ME. Analysis of a Plasmodium falciparum EBA-175 peptide with high binding capacity to erythrocytes and their analogues using 1H NMR. J. Struct. Biol. 141(2), 115–121 (2003).
   Google Scholar
• Tolia NH, Enemark EJ, Sim BK, Joshua-Tor L. Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122(2), 183–193 (2005).
   PubMed Web of Science ®Google Scholar
• Alba MP, Salazar LM, Puentes A, Pinto M, Torres E, Patarroyo ME. 6746 SERA peptide analogues immunogenicity and protective efficacy against malaria is associated with short alpha helix formation: malaria protection associated with peptides alpha helix shortening. Peptides 24(7), 999–1006 (2003).
   Google Scholar
• Hodder AN, Malby RL, Clarke OB et al. Structural insights into the protease-like antigen Plasmodium falciparum SERA5 and its noncanonical active-site serine. J. Mol. Biol. 392(1), 154–165 (2009).
   PubMed Web of Science ®Google Scholar