Immune escape and immune camouflage may reduce the efficacy of RTS,S vaccine in Malawi

References

• World Health Organisation. WHO | malaria. WHO. 2017 [accessed 2017 Jun 23]. http://www.who.int/mediacentre/factsheets/fs094/en/#.WU1EUDkCfpE.mendeley
   Google Scholar
• Schumacher R-F, Spinelli E. Malaria in children. Mediterr J Hematol Infect Dis. 2012;4(1):e2012073. doi:10.4084/mjhid.2012.073.
   PubMedGoogle Scholar
• Doolan DL, Dobaño C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev. 2009;22(1):13–36. doi:10.1128/CMR.00025-08.
   PubMed Web of Science ®Google Scholar
• Thera MA, Plowe CV. Vaccines for malaria: how close are we? Annu Rev Med. 2012;63(3):345–357. doi:10.1146/annurev-med-022411-192402.
   PubMedGoogle Scholar
• Schwenk RJ, Richie TL. Protective immunity to pre-erythrocytic stage malaria. Trends Parasitol. 2011;27(7):306–314. doi:10.1016/j.pt.2011.02.002.
   PubMed Web of Science ®Google Scholar
• Hoffman SL, Goh LML, Luke TC, Schneider I, Le TP, Doolan DL, Sacci J, de la Vega P, Dowler M, Paul C, et al. Protection of humans against malaria by immunization with radiation-attenuated plasmodium falciparum sporozoites. J Infect Dis. 2002;185(8):1155–1164. doi:10.1086/339409.
   PubMed Web of Science ®Google Scholar
• Hill AVS. Vaccines against malaria. Philos Trans R Soc Lond, B, Biol Sci. 2011;366(1579):2806–2814. doi:10.1098/rstb.2011.0091.
   PubMed Web of Science ®Google Scholar
• Zavala F, Tam JP, Barr PJ, Romero PJ, Ley V, Nussenzweig RS, Nussenzweig V. Synthetic peptide vaccine confers protection against murine malaria. J Exp Med. 1987;166(5):1591–1596. doi:10.1084/jem.166.5.1591.
   PubMed Web of Science ®Google Scholar
• Romero P, Maryanski JL, Corradin G, Nussenzweig RS, Nussenzweig V, Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature. 1989;341(6240):323–326. doi:10.1038/341323a0.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. First malaria vaccine receives positive scientific opinion from EMA. European Medicines Agency; 2015 Jul 24 [accessed 2017 Dec 10]. http://www.ema.europa.eu/docs/en_GB/document_library/Press_release/2015/07/WC500190447.pdf
   Google Scholar
• Kaslow DC, Biernaux S. RTS,S: toward a first landmark on the malaria vaccine technology roadmap. Vaccine. 2015;33(52):7425–7432. doi:10.1016/j.vaccine.2015.09.061.
   PubMed Web of Science ®Google Scholar
• Moorthy VS, Ballou WR. Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malar J. 2009;8(1):312. doi:10.1186/1475-2875-8-312.
   PubMedGoogle Scholar
• Ansong D, Asante KP, Vekemans J, Owusu SK, Owusu R, Brobby NAW, Dosoo D, Osei-Akoto A, Osei-Kwakye K, Asafo-Adjei E, et al. T cell responses to the RTS,S/AS01e and RTS,S/AS02D malaria candidate vaccines administered according to different schedules to Ghanaian children. PLoS One. 2011;6(4):e18891. doi:10.1371/journal.pone.0018891.
   PubMed Web of Science ®Google Scholar
• Sun P, Schwenk R, White K, Stoute JA, Cohen J, Ballou WR, Voss G, Kester KE, Heppner DG, Krzych U. Protective immunity induced with malaria vaccine, RTS,S, is linked to plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J Immunol. 2003;171(12):6961–6967. doi:10.4049/jimmunol.171.12.6961.
   PubMed Web of Science ®Google Scholar
• Riley EM, Stewart VA. Immune mechanisms in malaria: new insights in vaccine development. Nat Med. 2013;19(2):168–178. doi:10.1038/nm.3083.
   PubMed Web of Science ®Google Scholar
• World Health Organizaation. Weekly epidemiological record. World Health Organ Geneva. 2016;91(4):33–52. doi:10.1186/1750-9378-2-15.Voir.
   Google Scholar
• Gordon DM, Mc Govern TW, Krzych U, Cohen JC, Schneider I, La Chance R, Heppner DG, Yuan G, Hollingdale M, Slaoui M, et al. Safety, immunogenicity, and efficacy of a recombinantly produced plasmodium falciparum circumsporozoite protein-hepatitis b surface antigen subunit vaccine. J Infect Dis. 1995;171(6):1576–1585. doi:10.1093/infdis/171.6.1576.
   PubMed Web of Science ®Google Scholar
• Stoute JA, Slaoui M, Heppner DG, Momin P, Kester KE, Desmons P, Wellde BT, Garçon N, Krzych U, Marchand M, et al. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S malaria vaccine evaluation group. N Engl J Med. 1997;336(2):86–91. doi:10.1056/NEJM199701093360202.
   PubMed Web of Science ®Google Scholar
• Bojang KA, Milligan PJM, Pinder M, Vigneron L, Alloueche A, Kester KE, Ballou WR, Conway DJ, Reece WHH, Gothard P, et al. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in the Gambia: A randomised trial. Lancet. 2001;358(9297):1927–1934. doi:10.1016/S0140-6736(01)06957-4.
   PubMed Web of Science ®Google Scholar
• Alonso PL, Sacarlal J, Aponte JJ, Leach A, Macete E, Milman J, Mandomando I, Spiessens B, Guinovart C, Espasa M, et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet. 2004;364(9443):1411–1420. doi:10.1016/S0140-6736(04)17223-1.
   PubMed Web of Science ®Google Scholar
• Aponte JJ, Aide P, Renom M, Mandomando I, Bassat Q, Sacarlal J, Manaca MN, Lafuente S, Barbosa A, Leach A, et al. Safety of the RTS,S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled phase I/IIb trial. Lancet. 2007;370(9598):1543–1551. doi:10.1016/S0140-6736(07)61542-6.
   PubMed Web of Science ®Google Scholar
• Bejon P, Lusingu J, Olotu A, Leach A, Lievens M, Vekemans J, Mshamu S, Lang T, Gould J, Dubois M-C, et al. Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med. 2008;359(24):2521–2532. doi:10.1056/NEJMoa1208410.
   PubMed Web of Science ®Google Scholar
• Abdulla S, Oberholzer R, Juma O, Kubhoja S, Machera F, Membi C, Omari S, Urassa A, Mshinda H, Jumanne A. Safety and immunogenicity of RTS, S/AS02D malaria vaccine in infants. N Engl J Med. 2008;359(24):2533–2544. doi:10.1056/NEJMoa0807773.
   PubMed Web of Science ®Google Scholar
• Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, Methogo BGNO, Doucka Y, Flamen A, Mordmüller B, et al. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med. 2011;365(20):1863–1875. doi:10.1056/NEJMoa1110039.
   PubMed Web of Science ®Google Scholar
• Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BGNO, Kabwende AL, Adegnika AA, Mordmüller B, Issifou S, Kremsner PG, et al. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med. 2012;367(24):2284–2295. doi:10.1056/NEJMoa1208394.
   PubMed Web of Science ®Google Scholar
• The RTS,S Clinical Trials Partnership. Efficacy and safety of the RTS,S/AS01 malaria vaccine during 18 months after vaccination: A phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med. 2014;11(7):e1001685. doi:10.1371/journal.pmed.1001685.
   PubMed Web of Science ®Google Scholar
• Bejon P, White MT, Olotu A, Bojang K, Lusingu JPA, Salim N, Otsyula NN, Agnandji ST, Asante KP, Owusu-Agyei S, et al. Efficacy of RTS,S malaria vaccines: individual-participant pooled analysis of phase 2 data. Lancet Infect Dis. 2013;13(4):319–327. doi:10.1016/S1473-3099(13)70005-7.
   PubMed Web of Science ®Google Scholar
• Bailey JA, Mvalo T, Aragam N, Weiser M, Congdon S, Kamwendo D, Martinson F, Hoffman I, Meshnick SR, Juliano JJ. Use of massively parallel pyrosequencing to evaluate the diversity of and selection on plasmodium falciparum csp T-cell epitopes in Lilongwe, Malawi. J Infect Dis. 2012;206(4):580–587. doi:10.1093/infdis/jis329.
   PubMed Web of Science ®Google Scholar
• Moise L, Gutierrez A, Kibria F, Martin R, Tassone R, Liu R, Terry F, Martin B, De Groot AS. iVAX: an integrated toolkit for the selection and optimization of antigens and the design of epitope-driven vaccines. Hum Vaccin Immunother. 2015;11(9):2312–2321. doi:10.1080/21645515.2015.1061159.
   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. 1993;(11)687–727. doi:10.1146/annurev.iy.11.040193.003351.
   PubMedGoogle Scholar
• Plotkin S, Orenstein W, Offit P, Edwards K. Plotkin’s vaccines. Seventh. Philadelphia (PA): Elsevier; 2018.
   Google Scholar
• Moise L, Gutierrez AH, Bailey-Kellogg C, Terry F, Leng Q, Abdel Hady KM, VerBerkmoes NC, Sztein MB, Losikoff PT, Martin WD, et al. The two-faced T cell epitope: examining the host-microbe interface with JanusMatrix. Hum Vaccin Immunother. 2013;9(7):1577–1586. doi:10.4161/hv.24615.
   PubMed Web of Science ®Google Scholar
• Zeeshan M, Alam MT, Vinayak S, Bora H, Tyagi RK, Alam MS, Choudhary V, Mittra P, Lumb V, Bharti PK, et al. Genetic variation in the plasmodium falciparum circumsporozoite protein in india and its relevance to RTS,S malaria vaccine. PLoS One. 2012;7(8):e43430. doi:10.1371/journal.pone.0043430.
   PubMed Web of Science ®Google Scholar
• Losikoff PT, Mishra S, Terry F, Gutierrez A, Ardito MT, Fast L, Nevola M, Martin WD, Bailey-Kellogg C, De Groot AS, et al. HCV epitope, homologous to multiple human protein sequences, induces a regulatory T cell response in infected patients. J Hepatol. 2015;62(1):48–55. doi:10.1016/j.jhep.2014.08.026.
   PubMed Web of Science ®Google Scholar
• Liu R, Moise L, Tassone R, Gutierrez AH, Terry FE, Sangare K, Ardito MT, Martin WD, De Groot AS. H7N9 T-cell epitopes that mimic human sequences are less immunogenic and may induce treg-mediated tolerance. Hum Vaccin Immunother. 2015;11(9):2241–2252. doi:10.1080/21645515.2015.1052197.
   PubMed Web of Science ®Google Scholar
• Gutiérrez AH, Rapp-Gabrielson VJ, Terry FE, Loving CL, Moise L, Martin WD, De Groot AS. T-cell epitope content comparison (EpiCC) of swine H1 influenza A virus hemagglutinin. Influenza Other Respir Viruses. 2017;11(6):531–542. doi:10.1111/irv.12513.
   PubMed Web of Science ®Google Scholar
• Hoffman SL, Isenbarger D, Long GW, Sedegah M, Szarfman A, Waters L, Hollingdale MR, van der Meide PH, Finbloom DS, Ballou WR. Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes. Science. 1989;244(4908):1078–1081. doi:10.1126/science.2524877.
   PubMed Web of Science ®Google Scholar
• Weiss WR, Mellouk S, Houghten RA, Sedegah M, Kumar S, Good MF, Berzofsky JA, Miller LH, Hoffman SL. Cytotoxic T cells recognize a peptide from the circumsporozoite protein on malaria-infected hepatocytes. J Exp Med. 1990;171(3):763–773. doi:10.1084/jem.171.3.763.
   PubMed Web of Science ®Google Scholar
• Charoenvit Y, Collins WE, Jones TR, Millet P, Yuan L, Campbell GH, Beaudoin RL, Broderson JR, Hoffman SL. Inability of malaria vaccine to induce antibodies to a protective epitope within its sequence. Science. 1991;251(4994):668–671. doi:10.1126/science.1704150.
   PubMed Web of Science ®Google Scholar
• Charoenvit Y, Mellouk S, Cole C, Bechara R, Leef MF, Sedegah M, Yuan LF, Robey FA, Beaudoin RL, Hoffman SL. Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. J Immunol. 1991;146:1020–1025.
   PubMed Web of Science ®Google Scholar
• Crotty S. Follicular helper CD4 T cells. Annu Rev Immunol. 2011;29(1):621–663. doi:10.1146/annurev-immunol-031210-101400.
   PubMed Web of Science ®Google Scholar
• Laidlaw BJ, Craft JE, Kaech SM. The multifaceted role of CD4+ T cells in CD8+ T cell memory. Nat Rev Immunol. 2016;16(2):102–111. doi:10.1038/nri.2015.10.
   PubMed Web of Science ®Google Scholar
• Bronke C, Almeida CAM, Mckinnon E, Roberts SG, Keane NM, Chopra A, Carlson JM, Heckerman D, Mallal S, John M. HIV escape mutations occur preferentially at HLA-binding sites of CD8 T-cell epitopes. Aids. 2013;27(6):899–905. doi:10.1097/QAD.0b013e32835e1616.
   PubMed Web of Science ®Google Scholar
• Vossen MTM, Westerhout EM, Söderberg-Nauclér C, Wiertz EJHJ. Viral immune evasion: A masterpiece of evolution. Immunogenetics. 2002;54(8):527–542. doi:10.1007/s00251-002-0493-1.
   PubMed Web of Science ®Google Scholar
• John M, Gaudieri S. Influence of HIV and HCV on T cell antigen presentation and challenges in the development of vaccines. Front Microbiol. 2014;5:514. doi:10.3389/fmicb.2014.00514.
   PubMed Web of Science ®Google Scholar
• Good MF, Pombo D, Maloy WL, de la Cruz VF, Miller LH, Berzofsky JA. Parasite polymorphism present within minimal T cell epitopes of Plasmodium falciparum circumsporozoite protein. J Immunol. 1988;140:1645–1650.
   PubMed Web of Science ®Google Scholar
• Hill AV, Elvin J, Willis AC, Aidoo M, Allsopp CE, Gotch FM, Gao XM, Takiguchi M, Greenwood BM, Townsend AR, et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature. 1992;360(6403):434–439. doi:10.1038/360434a0.
   PubMed Web of Science ®Google Scholar
• Good MF, Kumar S, Miller LH. The real difficulties for malaria sporozoite vaccine development: nonresponsiveness and antigenic variation. Immunol Today. 1988;9(11):351–355. doi:10.1016/0167-5699(88)91336-9.
   PubMedGoogle Scholar
• Good MF, Pombo D, Quakyi IA, Riley EM, Houghten RA, Menon A, Alling DW, Berzofsky JA, Miller LH. Human T-cell recognition of the circumsporozoite protein of Plasmodium falciparum: immunodominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci USA. 1988;85(4):1199–1203. doi:10.1073/pnas.85.4.1199.
   PubMed Web of Science ®Google Scholar
• De Groot AS, Moise L, Liu R, Gutierrez AH, Tassone R, Bailey-Kellogg C, Martin W. Immune camouflage: relevance to vaccines and human immunology. Hum Vaccin Immunother. 2014;10(12):3570–3575. doi:10.4161/hv.36134.
   PubMed Web of Science ®Google Scholar
• Cohen J, Garcon N, Voss G, inventors; GlaxoSmithKline Biologicals SA, assignee. Vaccines. United States patent US20050002958A1. 2005 Jan 6.
   Google Scholar
• Southwood S, Sidney J, Kondo A, Del Guercio MF, Appella E, Hoffman S, Kubo RT, Chesnut RW, Grey HM, Sette A. Several common HLA-DR types share largely overlapping peptide binding repertoires. J Immunol. 1998;160:3363–3373.
   PubMed Web of Science ®Google Scholar
• Moise L, Beseme S, Tassone R, Liu R, Kibria F, Terry F, Martin W, De Groot AS. T cell epitope redundancy: cross-conservation of the TCR face between pathogens and self and its implications for vaccines and autoimmunity. Expert Rev Vaccines. 2016;15(5):607–617. doi:10.1586/14760584.2016.1123098.
   PubMed Web of Science ®Google Scholar