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Special Report

EDiP: the Epitope Dilution Phenomenon. Lessons learnt from a malaria vaccine antigen and its applicability to polymorphic antigens

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Pages 13-21 | Received 17 Oct 2017, Accepted 17 Nov 2017, Published online: 11 Dec 2017

References

  • Remarque EJ, Faber BW, Kocken CH, et al. Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol. 2008;24:74–84. [Research Support, Non-U.S. Gov’t Review].
  • Narum DL, Thomas AW. Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol Biochem Parasitol. 1994;67: 59–68. [0166-6851(94)90096-5 pii].
  • Bannister LH, Hopkins JM, Dluzewski AR, et al. Plasmodium falciparum apical membrane antigen 1 (PfAMA-1) is translocated within micronemes along subpellicular microtubules during merozoite development. J Cell Sci. 2003;116:3825–3834.
  • Howell SA, Withers-Martinez C, Kocken CH, et al. Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J Biol Chem. 2001;276:31311–31320.
  • Kocken CH, Van der Wel AM, Dubbeld MA, et al. Precise timing of expression of a Plasmodium falciparum-derived transgene in Plasmodium berghei is a critical determinant of subsequent subcellular localization. J Biol Chem. 1998;273:15119–15124. [Research Support, Non-U.S. Gov’t].
  • Deans JA, Alderson T, Thomas AW, et al. Rat monoclonal antibodies which inhibit the in vitro multiplication of Plasmodium knowlesi. Clin Exp Immunol. 1982;49:297–309. [Research Support, Non-U.S. Gov’t].
  • Dutta S, Haynes JD, Moch JK, et al. Invasion-inhibitory antibodies inhibit proteolytic processing of apical membrane antigen 1 of Plasmodium falciparum merozoites. Proc Natl Acad Sci U S A. 2003;100:12295–12300. [In Vitro Research Support, U.S. Gov’t, Non-P.H.S.].
  • Dutta S, Haynes JD, Barbosa A, et al. Mode of action of invasion-inhibitory antibodies directed against apical membrane antigen 1 of Plasmodium falciparum. Infect Immun. 2005;73:2116–2122. [Research Support, U.S. Gov’t, Non-P.H.S.].
  • Thomas AW, Deans JA, Mitchell GH, et al. The Fab fragments of monoclonal IgG to a merozoite surface antigen inhibit Plasmodium knowlesi invasion of erythrocytes. MolBiochemParasitol. 1984;13:187–199. [0166-6851(84)90112-9 pii].
  • Anders RF, Crewther PE, Edwards S, et al. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine. 1998;16:240–247. [S0264-410X(97)88331-4 pii].
  • Hodder AN, Crewther PE, Anders RF. Specificity of the protective antibody response to apical membrane antigen 1. Infect Immun. 2001;69: 3286–3294.
  • Takala SL, Coulibaly D, Thera MA, et al. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med. 2009;1:2ra5.
  • Faber BW, Abdul KK, Rodriguez-Garcia R, et al. Low levels of polymorphisms and no evidence for diversifying selection on the Plasmodium knowlesi apical membrane antigen 1 gene. PLoS One. 2015;10:e0124400. [PONE-D-14-56179 pii].
  • Pizarro JC, Vulliez-Le Normand B, Chesne-Seck ML, et al. Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science. 2005;308:408–411. [Research Support, Non-U.S. Gov’t].
  • Chesne-Seck ML, Pizarro JC, Vulliez-Le Normand B, et al. Structural comparison of apical membrane antigen 1 orthologues and paralogues in apicomplexan parasites. Mol Biochem Parasitol. 2005;144:55–67. [Comparative Study Research Support, Non-U.S. Gov’t].
  • Remarque EJ, Faber BW, Kocken CH, et al. A diversity-covering approach to immunization with Plasmodium falciparum apical membrane antigen 1 induces broader allelic recognition and growth inhibition responses in rabbits. Infect Immun. 2008;76:2660–2670. [Research Support, Non-U.S. Gov’t].
  • Genetic distances for AMA1. [cited 30 Nov 2017]. Available from: http://www.bprc.nl/cdn/edip/ama1/
  • Smith DJ, Lapedes AS, De Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science. 2004;305:371–376. [1097211 pii].
  • Dutta S, Lee SY, Batchelor AH, et al. Structural basis of antigenic escape of a malaria vaccine candidate. Proc Natl Acad Sci U S A. 2007;104:12488–12493. [Research Support, U.S. Gov’t, Non-P.H.S.].
  • Escalante AA, Lal AA, Ayala FJ. Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics. 1998;149: 189–202. [Comparative Study Research Support, U.S. Gov’t, Non-P.H.S. Research Support, U.S. Gov’t, P.H.S.].
  • Ord RL, Tami A, Sutherland CJ. ama1 genes of sympatric Plasmodium vivax and P. falciparum from Venezuela differ significantly in genetic diversity and recombination frequency. PLoS One. 2008;3: e3366.
  • Polley SD, Chokejindachai W, Conway DJ. Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics. 2003;165: 555–561. [Research Support, Non-U.S. Gov’t].
  • Verra F, Hughes AL. Evidence for ancient balanced polymorphism at the apical membrane antigen-1 (AMA-1) locus of Plasmodium falciparum. Mol Biochem Parasitol. 2000;105: 149–153. [S0166-6851(99)00162-0 pii].
  • Thera MA, Doumbo OK, Coulibaly D, et al. A field trial to assess a blood-stage malaria vaccine. N Eng J Med. 2011;365:1004–1013.
  • Remarque EJ, Roestenberg M, Younis S, et al. Humoral immune responses to a single allele PfAMA1 vaccine in healthy malaria-naive adults. PLoS One. 2012;7:e38898. [Clinical Trial Research Support, Non-U.S. Gov’t].
  • Kennedy MC, Wang J, Zhang Y, et al. In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun. 2002;70:6948–6960.
  • Kocken CH, Withers-Martinez C, Dubbeld MA, et al. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun. 2002;70:4471–4476. [Research Support, Non-U.S. Gov’t].
  • Kusi KA, Faber BW, Riasat V, et al. Generation of humoral immune responses to multi-allele PfAMA1 vaccines; effect of adjuvant and number of component alleles on the breadth of response. PLoS One. 2010;5:e15391. [Research Support, Non-U.S. Gov’t].
  • Kusi KA, Remarque EJ, Riasat V, et al. Safety and immunogenicity of multi-antigen AMA1-based vaccines formulated with CoVaccine HT and Montanide ISA 51 in rhesus macaques. Malar J. 2011;10:182. [Research Support, Non-U.S. Gov’t].
  • Kusi KA, Faber BW, Van der Eijk M, et al. Immunization with different PfAMA1 alleles in sequence induces clonal imprint humoral responses that are similar to responses induced by the same alleles as a vaccine cocktail in rabbits. Malar J. 2011;10:40. [Research Support, Non-U.S. Gov’t].
  • Kusi KA, Faber BW, Thomas AW, et al. Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS One. 2009;4:e8110. [Research Support, Non-U.S. Gov’t].
  • Sirima SB, Durier C, Kara L, et al. Safety and immunogenicity of a recombinant Plasmodium falciparum AMA1-DiCo malaria vaccine adjuvanted with GLA-SE or Alhydrogel(R) in European and African adults: a phase 1a/1b, randomized, double-blind multi-centre trial. Vaccine. 2017 Sep 22. PubMed PMID: 28947345. DOI:10.1016/j.vaccine.2017.09.027.
  • Safety and Immunogenicity of Recombinant Pichia Pastoris AMA1-DiCo Candidate Malaria Vaccine with GLA-SE and Alhydrogel ® as Adjuvant in Healthy Malaria Non-Exposed European and Malaria Exposed African Adults (AMA1-DiCo). [cited 30 Nov 2017]. Available from: https://clinicaltrials.gov/ct2/show/NCT02014727/
  • Dutta S, Dlugosz LS, Drew DR, et al. Overcoming antigenic diversity by enhancing the immunogenicity of conserved epitopes on the malaria vaccine candidate apical membrane antigen-1. PLoS Pathog. 2013;9:e1003840.
  • Faber BW, Younis S, Remarque EJ, et al. Diversity covering AMA1-MSP119 fusion proteins as malaria vaccines. Infect Immun. 2013;81:1479–1490. [Research Support, Non-U.S. Gov’t].
  • Miura K, Herrera R, Diouf A, et al. Overcoming allelic specificity by immunization with five allelic forms of Plasmodium falciparum apical membrane antigen 1. Infect Immun. 2013;81:1491–1501. [Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov’t].
  • Kusi KA, Dodoo D, Bosomprah S, et al. Measurement of the plasma levels of antibodies against the polymorphic vaccine candidate apical membrane antigen 1 in a malaria-exposed population. BMC Infect Dis. 2012;12:32. [Research Support, Non-U.S. Gov’t].
  • Osier FH, Fegan G, Polley SD, et al. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun. 2008;76:2240–2248. [Research Support, Non-U.S. Gov’t Validation Studies].
  • Daou M, Kouriba B, Ouedraogo N, et al. Protection of Malian children from clinical malaria is associated with recognition of multiple antigens. Malar J. 2015;14:56.
  • Davenport FM, Hennessy AV. Predetermination by infection and by vaccination of antibody response to influenza virus vaccines. J Exp Med. 1957;106:835–850.
  • Carter DM, Bloom CE, Nascimento EJ, et al. Sequential seasonal H1N1 influenza virus infections protect ferrets against novel 2009 H1N1 influenza. J Virol. 2013;87:1400–1410.
  • Genetic distances for influenza. [cited 30 Nov 2017]. Available from: http://www.bprc.nl/cdn/edip/dengue/
  • Huber VC, Thomas PG, McCullers JA. A multi-valent vaccine approach that elicits broad immunity within an influenza subtype. Vaccine. 2009;27:1192–1200. [S0264-410X(08)01747-7 pii].
  • Prabakaran M, Leyrer S, He F, et al. Progress toward a universal H5N1 vaccine: a recombinant modified vaccinia virus Ankara-expressing trivalent hemagglutinin vaccine. PLoS One. 2014;9:e107316.
  • Schwartzman LM, Cathcart AL, Pujanauski LM, et al. An intranasal virus-like particle vaccine broadly protects mice from multiple subtypes of influenza A virus. MBio. 2015;6. [mBio.01044-15 pii].
  • Zebedee SL, Lamb RA. Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol. 1988;62:2762–2772.
  • Bachmann MF, Jennings GT. Virus-like particles: combining innate and adaptive immunity for effective vaccination. In: Kaufmann SHE, editor. Novel vaccination strategies. Weinheim: Wiley-VCH Verlag; 2004. p. 415–431.
  • Schiller J, Chackerian B. Why HIV virions have low numbers of envelope spikes: implications for vaccine development. PLoS Pathog. 2014;10:e1004254.
  • Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10: 787–796. [nri2868 pii].
  • Pushko P, Pearce MB, Ahmad A, et al. Influenza virus-like particle can accommodate multiple subtypes of hemagglutinin and protect from multiple influenza types and subtypes. Vaccine. 2011;29:5911–5918. [S0264-410X(11)00932-7 pii].
  • EduFluVac. [cited 30 Nov 2017]. Available from: www.edufluvac.eu
  • Genetic distances for Dengue. [cited 30 Nov 2017]. Available from: http://www.bprc.nl/cdn/edip/fluh1-ha1/
  • Balakrishnan T, Bela-Ong DB, Toh YX, et al. Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection. PLoS One. 2011;6:e29430. [PONE-D-11-12462 pii].
  • Sabin AB. Research on dengue during World War II. Am J Trop Med Hyg. 1952;1:30–50.
  • Anderson KB, Gibbons RV, Cummings DA, et al. A shorter time interval between first and second dengue infections is associated with protection from clinical illness in a school-based cohort in Thailand. J Infect Dis. 2014;209:360–368. [jit436 pii].
  • Capeding MR, Tran NH, Hadinegoro SR, et al. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet. 2014. [S0140-6736(14)61060-6 pii]. DOI:10.1016/S0140-6736(14)61060-6.
  • Halstead SB. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res. 2003;60:421–467.
  • Hadinegoro SR, Arredondo-Garc¡a JL, Capeding MR, et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med. 2015;373:1195–1206.
  • Guy B, Lang J, Saville M, et al. Vaccination against dengue: challenges and current developments. Annu Rev Med. 2016;67:387–404.
  • Dejnirattisai W, Wongwiwat W, Supasa S, et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol. 2014. [ni.3058 pii].
  • Doria-Rose NA, Schramm CA, Gorman J, et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature. 2014;509:55–62. [nature13036 pii].
  • Liao HX, Lynch R, Zhou T, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 2013;496:469–476. [nature12053 pii].
  • Gao F, Bonsignori M, Liao HX, et al. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell. 2014 Jul 31;158:481–491. Epub 2014 Jul 24. PubMed PMID: 25065977. DOI:10.1016/j.cell.2014.06.022.
  • Sather DN, Carbonetti S, Malherbe DC, et al. Emergence of broadly neutralizing antibodies and viral coevolution in two subjects during the early stages of infection with human immunodeficiency virus type 1. J Virol. 2014 Nov;88:12968–12981. Epub 2014 Aug 13. PubMed PMID: 25122781.
  • Sliepen K, Sanders RW. HIV-1 envelope glycoprotein immunogens to induce broadly neutralizing antibodies. Expert Rev Vaccines. 2016;1–17. DOI:10.1586/14760584.2016.1129905.
  • Kwong PD, Doyle ML, Casper DJ, et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 2002;420:678–682.
  • Jardine J, Julien JP, Menis S, et al. Rational HIV immunogen design to target specific germline B cell receptors. Science. 2013;340:711–716. Epub 2013 Mar 28.
  • Hoot S, McGuire AT, Cohen KW, et al. Recombinant HIV envelope proteins fail to engage germline versions of anti-CD4bs bNAbs. PLoS Pathog. 2013;9:e1003106. [PPATHOGENS-D-12-02139 pii].
  • Xiao X, Chen W, Feng Y, et al. Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem Biophys Res Commun. 2009;390:404–409. [S0006-291X(09)01817-8 pii].
  • Haynes BF, Kelsoe G, Harrison SC, et al. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study . NatBiotechnol. 2012;30:423–433. [nbt.2197 pii].
  • Jardine JG, Ota T, Sok D, et al. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science. 2015;349:156–161.
  • Dosenovic P, Von Boehmer L, Escolano A, et al. Immunization for HIV-1 broadly neutralizing antibodies in human Ig knockin mice. Cell. 2015;161:1505–1515.
  • Bhiman JN, Anthony C, Doria-Rose NA, et al. Viral variants that initiate and drive maturation of V1V2-directed HIV-1 broadly neutralizing antibodies. Nat Med. 2015;21:1332–1336. [nm.3963 pii].
  • Wang S, Mata-Fink J, Kriegsman B, et al. Manipulating the selection forces during affinity maturation to generate cross-reactive HIV antibodies. Cell. 2015;160:785–797. [S0092-8674(15)00070-7 pii].
  • Sanders RW, Van Gils MJ, Derking R, et al. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science. 2015;349:aac4223.
  • Escolano A, Steichen JM, Dosenovic P, et al. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell. 2016 Sep 8;166:1445–1458.e12. PubMed PMID: 27610569.
  • Scarselli M, Arico B, Brunelli B, et al. Rational design of a meningococcal antigen inducing broad protective immunity. Sci Transl Med. 2011;3:91ra62. [3/91/91ra62 pii].
  • Angeletti D, Gibbs JS, Angel M, et al. Defining B cell immunodominance to viruses. Nat Immunol. 2017 Feb 13. PubMed PMID: 28192417. DOI:10.1038/ni.3680.
  • Thrane S, Janitzek CM, Agerbaek MO, et al. A novel virus-like particle based vaccine platform displaying the placental malaria antigen VAR2CSA. PLoSOne. 2015;10:e0143071. [PONE-D-15-32548 pii].
  • Brune KD, Leneghan DB, Brian IJ, et al. Plug-and-display: decoration of virus-like particles via isopeptide bonds for modular immunization. Sci Rep. 2016;6:19234. [srep19234 pii].
  • Kanekiyo M, Wei CJ, Yassine HM, et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature. 2013. [nature12202 pii]. DOI:10.1038/nature12202.
  • Walsh SR, Moodie Z, Fiore-Gartland AJ, et al. Vaccination with heterologous HIV-1 envelope sequences and heterologous adenovirus vectors increases T-cell responses to conserved regions: HVTN 083. J Infect Dis. 2016;213:541–550. [jiv496 pii].