340
Views
14
CrossRef citations to date
0
Altmetric
Reviews

Polymorphism in liver-stage malaria vaccine candidate proteins: immune evasion and implications for vaccine design

, &
Pages 389-399 | Received 29 Aug 2015, Accepted 25 Nov 2015, Published online: 23 Dec 2015

References

  • Who. World Malaria Report 2013. World Health Organization; 2013. p. 1–255. http://www.who.int/malaria/publications/world_malaria_report_2013/report/en/
  • Frevert U, Krzych U. Plasmodium cellular effector mechanisms and the hepatic microenvironment. Front Microbiol. 2015;6:482.
  • Rts SCTP. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386(9988):31–45.
  • Hafalla JC, Silvie O, Matuschewski K. Cell biology and immunology of malaria. Immunol Rev. 2011;240(1):297–316.
  • Radtke AJ, Tse SW, Zavala F. From the draining lymph node to the liver: the induction and effector mechanisms of malaria-specific CD8+ T cells. Semin Immunopathol. 2015;37(3):211–220.
  • Urban BC, Ferguson DJ, Pain A, et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature. 1999;400(6739):73–77.
  • Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med. 2003;197(2):143–151.
  • Minigo G, Woodberry T, Piera KA, et al. Parasite-dependent expansion of TNF receptor II-positive regulatory T cells with enhanced suppressive activity in adults with severe malaria. PLoS Pathog. 2009;5(4):e1000402.
  • Hansen DS, Schofield L. Natural regulatory T cells in malaria: host or parasite allies? PLoS Pathog. 2010;6(4):e1000771.
  • Plebanski M, Lee EA, Hannan CM, et al. Altered peptide ligands narrow the repertoire of cellular immune responses by interfering with T-cell priming. Nat Med. 1999;5(5):565–571.
  • Plebanski M, Lee EAM, Hill AVS. Immune evasion in malaria: altered peptide ligands of the circumsporozoite protein. Parasitology. 1997;115:S55–S66.
  • Zheng H, Tan ZP, Xu WY. Immune evasion strategies of pre-erythrocytic malaria parasites. Mediat Inflamm. 2014;2014:362605.
  • Chakravarty S, Cockburn IA, Kuk S, et al. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med. 2007;13(9):1035–1041.
  • Corradin G, Levitskaya J. Priming of CD8(+) T cell responses to liver stage malaria parasite antigens. Front Immunol. 2014;5:527.
  • Wykes MN, Good MF. What really happens to dendritic cells during malaria? Nat Rev Microbiol. 2008;6(11):864–870.
  • Elliott SR, Spurck TP, Dodin JM, et al. Inhibition of dendritic cell maturation by malaria is dose dependent and does not require Plasmodium falciparum erythrocyte membrane protein 1. Infect Immun. 2007;75(7):3621–3632.
  • Wykes MN, Kay JG, Manderson A, et al. Rodent blood-stage Plasmodium survive in dendritic cells that infect naive mice. Proc Natl Acad Sci U S A. 2011;108(27):11205–11210.
  • Plebanski M, Hannan CM, Behboudi S, et al. Direct processing and presentation of antigen from malaria sporozoites by professional antigen-presenting cells in the induction of CD8 T-cell responses. Immunol Cell Biol. 2005;83(3):307–312.
  • Plebanski M, Aidoo M, Whittle HC, et al. Precursor frequency analysis of cytotoxic T lymphocytes to pre-erythrocytic antigens of Plasmodium falciparum in West Africa. J Immunol. 1997;158(6):2849–2855.
  • Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol. 2008;8(7):523–532.
  • Mills KH, McGuirk P. Antigen-specific regulatory T cells–their induction and role in infection. Semin Immunol. 2004;16(2):107–117.
  • Walther M, Jeffries D, Finney OC, et al. Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009;5(4):e1000364.
  • Todryk SM, Bejon P, Mwangi T, et al. Correlation of memory T cell responses against TRAP with protection from clinical malaria, and CD4 CD25 high T cells with susceptibility in Kenyans. Plos One. 2008;3(4):e2027.
  • Boyle MJ, Jagannathan P, Farrington LA, et al. Decline of FoxP3+ regulatory CD4 T cells in peripheral blood of children heavily exposed to malaria. PLoS Pathog. 2015;11(7):e1005041.
  • Ndure J, Flanagan KL. Targeting regulatory T cells to improve vaccine immunogenicity in early life. Front Microbiol. 2014;5:477.
  • Moore AC, Gallimore A, Draper SJ, et al. Anti-CD25 antibody enhancement of vaccine-induced immunogenicity: increased durable cellular immunity with reduced immunodominance. J Immunol. 2005;175(11):7264–7273.
  • Scholzen A, Mittag D, Rogerson SJ, et al. Plasmodium falciparum-mediated induction of human CD25Foxp3 CD4 T cells is independent of direct TCR stimulation and requires IL-2, IL-10 and TGFbeta. PLoS Pathog. 2009;5(8):e1000543.
  • Casares S, Brumeanu TD, Richie TL. The RTS,S malaria vaccine. Vaccine. 2010;28(31):4880–4894.
  • Reece WH, Pinder M, Gothard PK, et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat Med. 2004;10(4):406–410.
  • Evavold BD, Allen PM. Separation of IL-4 production from Th cell proliferation by an altered T cell receptor ligand. Science. 1991;252(5010):1308–1310.
  • Plebanski M, Lee EA, Hill AV. Immune evasion in malaria: altered peptide ligands of the circumsporozoite protein. Parasitology. 1997;115(Suppl):S55–S66.
  • Plassmeyer ML, Reiter K, Shimp RL Jr, et al. Structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate. J Biol Chem. 2009;284(39):26951–26963.
  • Singh JP, Verma S, Bhattacharya PR, et al. Plasmodium falciparum circumsporozoite protein: epidemiological variations among field isolates prevalent in India. Trop Med Int Health. 2009;14(8):957–966.
  • Gandhi K, Thera MA, Coulibaly D, et al. Next generation sequencing to detect variation in the Plasmodium falciparum circumsporozoite protein. Am J Trop Med Hyg. 2012;86(5):775–781.
  • Alloueche A, Silveira H, Conway DJ, et al. High-throughput sequence typing of T-cell epitope polymorphisms in Plasmodium falciparum circumsporozoite protein. Mol Biochem Parasitol. 2000;106(2):273–282.
  • Escalante AA, Grebert HM, Isea R, et al. A study of genetic diversity in the gene encoding the circumsporozoite protein (CSP) of Plasmodium falciparum from different transmission areas–XVI. Asembo Bay Cohort Project. Mol Biochem Parasitol. 2002;125(1–2):83–90.
  • Neafsey DE, Juraska M, Bedford T, et al. Genetic diversity and protective efficacy of the RTS,S/AS01 malaria vaccine. N Engl J Med. 2015;373(21):2025–2037.
  • McCutchan TF, Good MF, Miller LH. Polymorphism in the circumsporozoite (CS) protein of Plasmodium falciparum. Parasitol Today. 1989;5(5):143–146.
  • Kumkhaek C, Phra-Ek K, Renia L, et al. Are extensive T cell epitope polymorphisms in the Plasmodium falciparum circumsporozoite antigen, a leading sporozoite vaccine candidate, selected by immune pressure? J Immunol. 2005;175(6):3935–3939.
  • Gandhi K, Thera MA, Coulibaly D, et al. Variation in the circumsporozoite protein of Plasmodium falciparum: vaccine development implications. Plos One. 2014;9(7):e101783.
  • Plebanski M, Flanagan KL, Lee EA, et al. Interleukin 10-mediated immunosuppression by a variant CD4 T cell epitope of Plasmodium falciparum. Immunity. 1999;10(6):651–660.
  • Jalloh A, Jalloh M, Matsuoka H. T-cell epitope polymorphisms of the Plasmodium falciparum circumsporozoite protein among field isolates from Sierra Leone: age-dependent haplotype distribution? Malar J. 2009;8:120.
  • Barry AE, Schultz L, Buckee CO, et al. Contrasting population structures of the genes encoding ten leading vaccine-candidate antigens of the human malaria parasite, Plasmodium falciparum. Plos One. 2009;4(12):e8497.
  • Qari SH, Collins WE, Lobel HO, et al. A study of polymorphism in the circumsporozoite protein of human malaria parasites. Am J Trop Med Hyg. 1994;50(1):45–51.
  • Gilbert SC, Plebanski M, Gupta S, et al. Association of malaria parasite population structure, HLA, and immunological antagonism. Science. 1998;279(5354):1173–1177.
  • Udhayakumar V, Shi YP, Kumar S, et al. Antigenic diversity in the circumsporozoite protein of Plasmodium falciparum abrogates cytotoxic-T-cell recognition. Infect Immun. 1994;62(4):1410–1413.
  • Udhayakumar V, Ongecha JM, Shi YP, et al. Cytotoxic T cell reactivity and HLA-B35 binding of the variant Plasmodium falciparum circumsporozoite protein CD8+ CTL epitope in naturally exposed Kenyan adults. Eur J Immunol. 1997;27(8):1952–1957.
  • Lalvani A, Aidoo M, Allsopp CE, et al. An HLA-based approach to the design of a CTL-inducing vaccine against Plasmodium falciparum. Res Immunol. 1994;145(6):461–468.
  • Hill AV, Allsopp CE, Kwiatkowski D, et al. Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991;352(6336):595–600.
  • Kijak GH, Walsh AM, Koehler RN, et al. HLA class I allele and haplotype diversity in Ugandans supports the presence of a major east African genetic cluster. Tissue Antigens. 2009;73(3):262–269.
  • Zevering Y, Khamboonruang C, Good MF. Human and murine T-cell responses to allelic forms of a malaria circumsporozoite protein epitope support a polyvalent vaccine strategy. Immunology. 1998;94(3):445–454.
  • Hill AV, Reyes-Sandoval A, O’Hara G, et al. Prime-boost vectored malaria vaccines: progress and prospects. Hum Vaccin. 2010;6(1):78–83.
  • Hodgson SH, Ewer KJ, Bliss CM, et al. Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. J Infect Dis. 2015;211(7):1076–1086.
  • Hafalla JC, Bauza K, Friesen J, et al. Identification of targets of CD8(+) T cell responses to malaria liver stages by genome-wide epitope profiling. PLoS Pathog. 2013;9(5):e1003303.
  • Wizel B, Houghten RA, Parker KC, et al. Irradiated sporozoite vaccine induces HLA-B8-restricted cytotoxic T lymphocyte responses against two overlapping epitopes of the Plasmodium falciparum sporozoite surface protein 2. J Exp Med. 1995;182(5):1435–1445.
  • Aidoo M, Lalvani A, Allsopp CE, et al. Identification of conserved antigenic components for a cytotoxic T lymphocyte-inducing vaccine against malaria. Lancet. 1995;345(8956):1003–1007.
  • Gonzalez JM, Peter K, Esposito F, et al. HLA-A*0201 restricted CD8+ T-lymphocyte responses to malaria: identification of new Plasmodium falciparum epitopes by IFN-gamma ELISPOT. Parasite Immunol. 2000;22(10):501–514.
  • Dodoo D, Hollingdale MR, Anum D, et al. Measuring naturally acquired immune responses to candidate malaria vaccine antigens in Ghanaian adults. Malar J. 2011;10:168.
  • Flanagan KL, Mwangi T, Plebanski M, et al. Ex vivo interferon-gamma immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of Plasmodium falciparum infection. Am J Trop Med Hyg. 2003;68(4):421–430.
  • Flanagan KL, Plebanski M, Akinwunmi P, et al. Broadly distributed T cell reactivity, with no immunodominant loci, to the pre-erythrocytic antigen thrombospondin-related adhesive protein of Plasmodium falciparum in West Africans. Eur J Immunol. 1999;29(6):1943–1954.
  • Wang R, Charoenvit Y, Corradin G, et al. Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J Immunol. 1996;157(9):4061–4067.
  • Khusmith S, Charoenvit Y, Kumar S, et al. Protection against malaria by vaccination with sporozoite surface protein 2 plus CS protein. Science. 1991;252(5006):715–718.
  • Khusmith S, Sedegah M, Hoffman SL. Complete protection against Plasmodium yoelii by adoptive transfer of a CD8+ cytotoxic T-cell clone recognizing sporozoite surface protein 2. Infect Immun. 1994;62(7):2979–2983.
  • Schneider J, Gilbert SC, Blanchard TJ, et al. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med. 1998;4(4):397–402.
  • Ewer KJ, O’Hara GA, Duncan CJ, et al. Protective CD8+ T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat Commun. 2013;4:2836.
  • Robson KJ, Hall JR, Davies LC, et al. Polymorphism of the TRAP gene of Plasmodium falciparum. Proc Biol Sci. 1990;242(1305):205–216.
  • Flanagan KL, Plebanski M, Odhiambo K, et al. Cellular reactivity to the P. falciparum protein trap in adult kenyans: novel epitopes, complex cytokine patterns, and the impact of natural antigenic variation. Am J Trop Med Hyg. 2006;74(3):367–375.
  • Mwacharo J, Dunachie SJ, Kai O, et al. Quantitative PCR evaluation of cellular immune responses in Kenyan children vaccinated with a candidate malaria vaccine. Plos One. 2009;4(12):e8434.
  • Kester KE, Gray Heppner D Jr, Moris P, et al. Sequential Phase 1 and Phase 2 randomized, controlled trials of the safety, immunogenicity and efficacy of combined pre-erythrocytic vaccine antigens RTS,S and TRAP formulated with AS02 Adjuvant System in healthy, malaria naive adults. Vaccine. 2014;32(49):6683–6691.
  • Bucci K, Kastens W, Hollingdale MR, et al. Influence of age and HLA type on interferon-gamma (IFN-gamma) responses to a naturally occurring polymorphic epitope of Plasmodium falciparum liver stage antigen-1 (LSA-1). Clin Exp Immunol. 2000;122(1):94–100.
  • Ravichandran M, Doolan DL, Cox-Singh J, et al. Research note: HLA degenerate T-cell epitopes from Plasmodium falciparum liver stage-specific antigen 1 (LSA-1) are highly conserved in isolates from geographically distinct areas. Parasite Immunol. 2000;22(9):469–473.
  • Prieur E, Druilhe P. The malaria candidate vaccine liver stage antigen-3 is highly conserved in Plasmodium falciparum isolates from diverse geographical areas. Malar J. 2009;8:247.
  • Jongwutiwes S, Putaporntip C, Karnchaisri K, et al. Positive selection on the Plasmodium falciparum sporozoite threonine-asparagine-rich protein: analysis of isolates mainly from low endemic areas. Gene. 2008;410(1):139–146.
  • Bongartz M, Rezbach P, Borrmann S, et al. Age-dependent enhancement of IFN-gamma responses to Plasmodium falciparum liver stage antigen-1 T cell epitopes. Parasitol Res. 2002;88(12):1083–1089.
  • John CC, Sumba PO, Ouma JH, et al. Cytokine responses to Plasmodium falciparum liver-stage antigen 1 vary in rainy and dry seasons in highland Kenya. Infect Immun. 2000;68(9):5198–5204.
  • Aidoo M, Lalvani A, Gilbert SC, et al. Cytotoxic T-lymphocyte epitopes for HLA-B53 and other HLA types in the malaria vaccine candidate liver-stage antigen 3. Infect Immun. 2000;68(1):227–232.
  • Aidoo M, Udhayakumar V. Field studies of cytotoxic T lymphocytes in malaria infections: implications for malaria vaccine development. Parasitol Today. 2000;16(2):50–56.
  • Flanagan KL, van Crevel R, Curtis N, et al. Heterologous (‘nonspecific’) and sex-differential effects of vaccines: epidemiology, clinical trials, and emerging immunologic mechanisms. Clin Infect Dis. 2013;57(2):283–289.
  • Benn CS, Netea MG, Selin LK, et al. A small jab - a big effect: nonspecific immunomodulation by vaccines. Trends Immunol. 2013;34(9):431–439.
  • Aaby P, Roth A, Ravn H, et al. Randomized trial of BCG vaccination at birth to low-birth-weight children: beneficial nonspecific effects in the neonatal period? J Infect Dis. 2011;204(2):245–252.
  • Aaby P, Martins CL, Garly ML, et al. Non-specific effects of standard measles vaccine at 4.5 and 9 months of age on childhood mortality: randomised controlled trial. Brit Med J. 2010;341:c6495.
  • Aaby P, Benn C, Nielsen J, et al. Testing the hypothesis that diphtheria-tetanus-pertussis vaccine has negative non-specific and sex-differential effects on child survival in high-mortality countries. BMJ Open. 2012;2(3):e000707.
  • Flanagan KL, Klein SL, Skakkebaek NE, et al. Sex differences in the vaccine-specific and non-targeted effects of vaccines. Vaccine. 2011;29(13):2349–2354.
  • Welsh RM, Che JW, Brehm MA, et al. Heterologous immunity between viruses. Immunol Rev. 2010;235(1):244–266.
  • Gil A, Kenney LL, Mishra R, et al. Vaccination and heterologous immunity: educating the immune system. Trans R Soc Trop Med Hyg. 2015;109(1):62–69.
  • Mathurin KS, Martens GW, Kornfeld H, et al. CD4 T-cell-mediated heterologous immunity between mycobacteria and poxviruses. J Virol. 2009;83(8):3528–3539.
  • Tinto H, D’Alessandro U, Sorgho H, et al. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386(9988):31–45.
  • Aaby P, Rodrigues A, Kofoed PE, et al. RTS,S/AS01 malaria vaccine and child mortality. Lancet. 2015;386(10005):1735–1736.
  • Cohen J, Nussenzweig V, Nussenzweig R, et al. From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Hum Vaccin. 2010;6(1):90–96.
  • de la Cruz VF, Maloy WL, Miller LH, et al. Lack of cross-reactivity between variant T cell determinants from malaria circumsporozoite protein. J Immunol. 1988;141(7):2456–2460.
  • Epstein JE, Richie TL. The whole parasite, pre-erythrocytic stage approach to malaria vaccine development: a review. Curr Opin Infect Dis. 2013;26(5):420–428.
  • Richie TL, Billingsley PF, Sim BK, et al. Progress with Plasmodium falciparum sporozoite (PfSPZ)-based malaria vaccines. Vaccine. 2015. [Epub ahead of print]. doi:10.1016/j.vaccine.2015.09.096
  • Bijker EM, Borrmann S, Kappe SH, et al.. Novel approaches to whole sporozoite vaccination against malaria. Vaccine. 2015. [Epub ahead of print]. doi:10.1016/j.vaccine.2015.09.095
  • Rivoltini L, Squarcina P, Loftus DJ, et al. A superagonist variant of peptide MART1/Melan A27-35 elicits anti-melanoma CD8+ T cells with enhanced functional characteristics: implication for more effective immunotherapy. Cancer Res. 1999;59(2):301–306.
  • Fong L, Hou Y, Rivas A, et al. Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc Natl Acad Sci U S A. 2001;98(15):8809–8814.
  • Hoppes R, Oostvoges R, Luimstra JJ, et al. Altered peptide ligands revisited: vaccine design through chemically modified HLA-A2-restricted T cell epitopes. J Immunol. 2014;193(10):4803–4813.
  • Wilson KL, Xiang SD, Plebanski M. Montanide, Poly I:C and nanoparticle based vaccines promote differential suppressor and effector cell expansion: a study of induction of CD8 T cells to a minimal Plasmodium berghei epitope. Front Microbiol. 2015;6:29.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.