1932

Abstract

remains a serious public health problem and a continuous challenge for the immune system due to the complexity and diversity of the pathogen. Recent advances from several laboratories in the characterization of the antibody response to the parasite have led to the identification of critical targets for protection and revealed a new mechanism of diversification based on the insertion of host receptors into immunoglobulin genes, leading to the production of receptor-based antibodies. These advances have opened new possibilities for vaccine design and passive antibody therapies to provide sterilizing immunity and control blood-stage parasites.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-042617-053301
2019-04-26
2024-12-02
Loading full text...

Full text loading...

/deliver/fulltext/immunol/37/1/annurev-immunol-042617-053301.html?itemId=/content/journals/10.1146/annurev-immunol-042617-053301&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    World Health Organ. 2017. World Malaria Report 2017 Geneva: World Health Organ.
    [Google Scholar]
  2. 2.
    Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B et al. 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526:7572207–11
    [Google Scholar]
  3. 3.
    Tilley L, Straimer J, Gnädig NF, Ralph SA, Fidock DA 2016. Artemisinin action and resistance in Plasmodium falciparum. . Trends Parasitol 32:9682–96
    [Google Scholar]
  4. 4.
    Fairhurst RM, Dondorp AM 2016. Artemisinin-resistant Plasmodium falciparum malaria. Emerging Infections 10 WM Scheld, JM Hughes, RJ Whitley 409–29 Washington, DC: ASM Press
    [Google Scholar]
  5. 5.
    Woodrow CJ, White NJ 2017. The clinical impact of artemisinin resistance in Southeast Asia and the potential for future spread. FEMS Microbiol. Rev. 41:134–48
    [Google Scholar]
  6. 6.
    Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD et al. 2010. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467:7314420–25
    [Google Scholar]
  7. 7.
    Loy DE, Liu W, Li Y, Learn GH, Plenderleith LJ et al. 2017. Out of Africa: origins and evolution of the human malaria parasites Plasmodium falciparum and Plasmodium vivax. Int. J. . Parasitol 47:2–387–97
    [Google Scholar]
  8. 8.
    Wright GJ, Rayner JC 2014. Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLOS Pathog 10:3e1003943
    [Google Scholar]
  9. 9.
    Kurup SP, Obeng-Adjei N, Anthony SM, Traore B, Doumbo OK et al. 2017. Regulatory T cells impede acute and long-term immunity to blood-stage malaria through CTLA-4. Nat. Med. 23:101220–25
    [Google Scholar]
  10. 10.
    Yam XY, Preiser PR 2017. Host immune evasion strategies of malaria blood stage parasite. Mol. BioSystems 13:122498–508
    [Google Scholar]
  11. 11.
    Portugal S, Obeng-Adjei N, Moir S, Crompton PD, Pierce SK 2017. Atypical memory B cells in human chronic infectious diseases: an interim report. Cell. Immunol. 321:18–25
    [Google Scholar]
  12. 12.
    Crompton PD, Moebius J, Portugal S, Waisberg M, Hart G et al. 2014. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu. Rev. Immunol. 32:157–87
    [Google Scholar]
  13. 13.
    Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M et al. 1999. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400:673973–77
    [Google Scholar]
  14. 14.
    Artavanis-Tsakonas K, Tongren JE, Riley EM 2003. The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin. Exp. Immunol. 133:2145–52
    [Google Scholar]
  15. 15.
    Langhorne J, Ndungu FM, Sponaas A-M, Marsh K 2008. Immunity to malaria: more questions than answers. Nat. Immunol. 9:7725–32
    [Google Scholar]
  16. 16.
    Cohen S, Carrington S, McGregor IA 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192:480733–37
    [Google Scholar]
  17. 17.
    McGregor IA, Carrington SP, Cohen S 1963. Treatment of East African P. falciparum malaria with West African human γ-globulin. Trans. R. Soc. Trop. Med. Hyg. 57:3170–75
    [Google Scholar]
  18. 18.
    Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H et al. 1991. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am. J. Trop. Med. Hyg. 45:3297–308
    [Google Scholar]
  19. 19.
    Marston HD, Paules CI, Fauci AS 2018. Monoclonal antibodies for emerging infectious diseases—borrowing from history. N. Engl. J. Med. 378:161469–72
    [Google Scholar]
  20. 20.
    Walker LM, Burton DR 2018. Passive immunotherapy of viral infections: “super-antibodies” enter the fray. Nat. Rev. Immunol. 18:5297–308
    [Google Scholar]
  21. 21.
    Burton DR 2017. What are the most powerful immunogen design vaccine strategies? Reverse vaccinology 2.0 shows great promise.. Cold Spring Harb. Perspect. Biol. 9:11a030262
    [Google Scholar]
  22. 22.
    Kwong PD 2017. What are the most powerful immunogen design vaccine strategies? A structural biologist's perspective.. Cold Spring Harb. Perspect. Biol. 9:11a029470
    [Google Scholar]
  23. 23.
    Lanzavecchia A, Frühwirth A, Perez L, Corti D 2016. Antibody-guided vaccine design: identification of protective epitopes. Curr. Opin. Immunol. 41:62–67
    [Google Scholar]
  24. 24.
    Offeddu V, Olotu A, Osier F, Marsh K, Matuschewski K, Thathy V 2017. High sporozoite antibody titers in conjunction with microscopically detectable blood infection display signatures of protection from clinical malaria. Front. Immunol. 8:488
    [Google Scholar]
  25. 25.
    Triller G, Scally SW, Costa G, Pissarev M, Kreschel C et al. 2017. Natural parasite exposure induces protective human anti-malarial antibodies. Immunity 47:1197–209
    [Google Scholar]
  26. 26.
    Hoffman SL, Oster CN, Plowe CV, Woollett GR, Beier JC et al. 1987. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science 237:4815639–42
    [Google Scholar]
  27. 27.
    Tran TM, Li S, Doumbo S, Doumtabe D, Huang CY et al. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin. Infect. Dis. 57:140–47
    [Google Scholar]
  28. 28.
    Rosenberg R, Wirtz RA, Schneider I, Burge R 1990. An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Trans. R. Soc. Trop. Med. Hyg. 84:2209–12
    [Google Scholar]
  29. 29.
    Beier JC, Davis JR, Vaughan JA, Noden BH, Beier MS 1991. Quantitation of Plasmodium falciparum sporozoites transmitted in vitro by experimentally infected Anopheles gambiae and Anopheles stephensi. Am. J. Hyg. Trop. . Med 44:5564–70
    [Google Scholar]
  30. 30.
    Medica DL, Sinnis P 2005. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect. Immun. 73:74363–69
    [Google Scholar]
  31. 31.
    Keitany GJ, Kim KS, Krishnamurty AT, Hondowicz BD, Hahn WO et al. 2016. Blood stage malaria disrupts humoral immunity to the pre-erythrocytic stage circumsporozoite protein. Cell Rep 17:3193–205
    [Google Scholar]
  32. 32.
    Vanderberg JP 2014. Imaging mosquito transmission of Plasmodium sporozoites into the mammalian host: immunological implications. Parasitol. Int. 63:1150–64
    [Google Scholar]
  33. 33.
    Offeddu V, Thathy V, Marsh K, Matuschewski K 2012. Naturally acquired immune responses against Plasmodium falciparum sporozoites and liver infection. Int. J. Parasitol. 42:6535–48
    [Google Scholar]
  34. 34.
    Nussenzweig RS, Vanderberg J, Most H, Orton C 1967. Protective immunity produced by the injection of X-irradiated sporozoites of Plasmodium berghei. . Nature 216:5111160–62
    [Google Scholar]
  35. 35.
    Clyde DF, Most H, McCarthy VC, Vanderberg JP 1973. Immunization of man against sporozoite-induced falciparum malaria. Am. J. Med. Sci. 266:3169–77
    [Google Scholar]
  36. 36.
    Rieckmann KH, Carson PE, Beaudoin RL, Cassells JS, Sell KW 1974. Sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg 68:3258–59
    [Google Scholar]
  37. 37.
    Hoffman SL, Goh LML, Luke TC, Schneider I, Le TP et al. 2002. Protection of humans against malaria by immunization with radiation‐attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185:81155–64
    [Google Scholar]
  38. 38.
    Schwartz L, Brown GV, Genton B, Moorthy VS 2012. A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar. J 11:111
    [Google Scholar]
  39. 39.
    Duffy PE, Sahu T, Akue A, Milman N, Anderson C 2014. Pre-erythrocytic malaria vaccines: identifying the targets. Expert Rev. Vaccines 11:101261–80
    [Google Scholar]
  40. 40.
    Draper SJ, Sack BK, King CR, Nielsen CM, Rayner JC et al. 2018. Malaria vaccines: recent advances and new horizons. Cell Host Microbe 24:143–56
    [Google Scholar]
  41. 41.
    Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M 1980. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207:442671–73
    [Google Scholar]
  42. 42.
    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. 151:61504–13
    [Google Scholar]
  43. 43.
    Cerami C, Frevert U, Sinnis P, Takacs B, Clavijo P et al. 1992. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70:61021–33
    [Google Scholar]
  44. 44.
    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. 177:51287–98
    [Google Scholar]
  45. 45.
    Dame JB, Williams JL, McCutchan TF, Weber JL, Wirtz RA et al. 1984. Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. . Science 225:4662593–99
    [Google Scholar]
  46. 46.
    Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P 2005. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J. Exp. Med. 201:127–33
    [Google Scholar]
  47. 47.
    Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R et al. 2007. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2:5316–27
    [Google Scholar]
  48. 48.
    Coppi A, Natarajan R, Pradel G, Bennett BL, James ER et al. 2011. The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. J. Exp. Med. 208:2341–56
    [Google Scholar]
  49. 49.
    Godson GN, Ellis J, Svec P, Schlesinger DH, Nussenzweig V 1983. Identification and chemical synthesis of a tandemly repeated immunogenic region of Plasmodium knowlesi circumsporozoite protein. Nature 305:592929–33
    [Google Scholar]
  50. 50.
    Zavala F 1983. Circumsporozoite proteins of malaria parasites contain a single immunodominant region with two or more identical epitopes. J. Exp. Med. 157:61947–57
    [Google Scholar]
  51. 51.
    Zavala F, Tam JP, Hollingdale MR, Cochrane AH, Quakyi I et al. 1985. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Science 228:47061436–40
    [Google Scholar]
  52. 52.
    Zavala F, Tam JP, Barr PJ, Romero PJ, Ley V et al. 1987. Synthetic peptide vaccine confers protection against murine malaria. J. Exp. Med. 166:51591–96
    [Google Scholar]
  53. 53.
    White MT, Bejon P, Olotu A, Griffin JT, Riley EM et al. 2013. The relationship between RTS,S vaccine-induced antibodies, CD4+ T cell responses and protection against Plasmodium falciparum infection. PLOS ONE 8:4e61395
    [Google Scholar]
  54. 54.
    White MT, Verity R, Griffin JT, Asante KP, Owusu-Agyei S et al. 2015. Immunogenicity of the RTS,S/AS01 malaria vaccine and implications for duration of vaccine efficacy: secondary analysis of data from a phase 3 randomised controlled trial. Lancet Infect. Dis. 15:121450–58
    [Google Scholar]
  55. 55.
    RTSS Clin. Trials Partnersh. 2015. 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 386:998831–45
    [Google Scholar]
  56. 56.
    Dups JN, Pepper M, Cockburn IA 2014. Antibody and B cell responses to Plasmodium sporozoites. Front. Microbiol. 5:625
    [Google Scholar]
  57. 57.
    Sultan AA, Thathy V, Frevert U, Robson KJ, Crisanti A et al. 1997. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90:3511–22
    [Google Scholar]
  58. 58.
    Ogwang C, Kimani D, Edwards NJ, Roberts R, Mwacharo J et al. 2015. Prime-boost vaccination with chimpanzee adenovirus and modified vaccinia Ankara encoding TRAP provides partial protection against Plasmodium falciparum infection in Kenyan adults. Sci. Transl. Med. 7:286286re5
    [Google Scholar]
  59. 59.
    Rampling T, Ewer KJ, Bowyer G, Bliss CM, Edwards NJ et al. 2016. Safety and high level efficacy of the combination malaria vaccine regimen of RTS,S/AS01B with chimpanzee adenovirus 63 and modified vaccinia Ankara vectored vaccines expressing ME-TRAP. J. Infect. Dis. 214:5772–81
    [Google Scholar]
  60. 60.
    Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M 2006. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol. Microbiol. 59:51369–79
    [Google Scholar]
  61. 61.
    Bergmann-Leitner ES, Mease RMDe La Vega P, Savranskaya T, Polhemus M, et al. 2010. Immunization with pre-erythrocytic antigen CelTOS from Plasmodium falciparum elicits cross-species protection against heterologous challenge with Plasmodium berghei. . PLOS ONE 5:e12294
    [Google Scholar]
  62. 62.
    Espinosa DA, Vega-Rodriguez J, Flores-Garcia Y, Noe AR, Muñoz C et al. 2017. The Plasmodium falciparum cell-traversal protein for ookinetes and sporozoites as a candidate for preerythrocytic and transmission-blocking vaccines. Infect. Immun. 85:2e00498–16
    [Google Scholar]
  63. 63.
    Hoffman SL, Billingsley PF, James E, Richman A, Loyevsky M et al. 2010. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum. Vaccin. 6:197–106
    [Google Scholar]
  64. 64.
    Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN et al. 2013. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341:61521359–65
    [Google Scholar]
  65. 65.
    Ishizuka AS, Lyke KE, DeZure A, Berry AA, Richie TL et al. 2016. Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Nat. Med. 22:6614–23
    [Google Scholar]
  66. 66.
    Mordmüller B, Surat G, Lagler H, Chakravarty S, Ishizuka AS et al. 2017. Sterile protection against human malaria by chemoattenuated PfSPZ vaccine. Nature 542:7642445–49
    [Google Scholar]
  67. 67.
    Sissoko M, Healy SA, Katile A, Omaswa F, Zaidi I et al. 2017. Safety and efficacy of PfSPZ vaccine against Plasmodium falciparum via direct venous inoculation in healthy malaria-exposed adults in Mali: a randomised, double-blind phase 1 trial. Lancet Infect. Dis. 17:498–509
    [Google Scholar]
  68. 68.
    Jongo SA, Shekalage SA, Church LWP, Ruben AJ, Schindler T et al. 2018. Safety, immunogenicity, and protective efficacy against controlled human malaria infection of Plasmodium falciparum sporozoites vaccine in Tanzanian adults. Am. J. Trop. Med. Hyg. 99:338–49
    [Google Scholar]
  69. 69.
    Foquet L, Hermsen CC, van Gemert G-J, Van Braeckel E, Weening KE et al. 2013. Vaccine-induced monoclonal antibodies targeting circumsporozoite protein prevent Plasmodium falciparum infection. J. Clin. Investig. 124:1140–44
    [Google Scholar]
  70. 70.
    Oyen D, Torres JL, Wille-Reece U, Ockenhouse CF, Emerling D et al. 2017. Structural basis for antibody recognition of the NANP repeats in Plasmodium falciparum circumsporozoite protein. PNAS 114:48E10438–45
    [Google Scholar]
  71. 71.
    Tan J, Sack BK, Oyen D, Zenklusen I, Piccoli L et al. 2018. A public antibody lineage that potently inhibits malaria infection through dual binding to the circumsporozoite protein. Nat. Med. 24:4401–7
    [Google Scholar]
  72. 72.
    Kisalu NK, Idris AH, Weidle C, Flores-Garcia Y, Flynn BJ et al. 2018. A human monoclonal antibody prevents malaria infection by targeting a new site of vulnerability on the parasite. Nat. Med. 24:4408–16
    [Google Scholar]
  73. 73.
    Scally SW, Murugan R, Bosch A, Triller G, Costa G et al. 2018. Rare PfCSP C-terminal antibodies induced by live sporozoite vaccination are ineffective against malaria infection. J. Exp. Med. 215:163–75
    [Google Scholar]
  74. 74.
    Murugan R, Buchauer L, Triller G, Kreschel C, Costa G et al. 2018. Clonal selection drives protective memory B cell responses in controlled human malaria infection. Sci. Immunol. 3:20eaap8029
    [Google Scholar]
  75. 75.
    Imkeller K, Scally SW, Bosch A, Martí GP, Costa G et al. 2018. Antihomotypic affinity maturation improves human B cell responses against a repetitive epitope. Science 360:63951358–62
    [Google Scholar]
  76. 76.
    Swearingen KE, Lindner SE, Shi L, Shears MJ, Harupa A et al. 2016. Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLOS Pathog 12:4e1005606
    [Google Scholar]
  77. 77.
    Arun Kumar K, Sano G-I, Boscardin S, Nussenzweig RS, Nussenzweig MC et al. 2006. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 444:7121937–40
    [Google Scholar]
  78. 78.
    Zenklusen I, Jongo S, Abdulla S, Ramadhani K, Lee Sim BK et al. 2018. Immunization of malaria-preexposed volunteers with PfSPZ vaccine elicits long-lived IgM invasion-inhibitory and complement-fixing antibodies. J. Infect. Dis. 217:101569–78
    [Google Scholar]
  79. 79.
    Weill J-C, Weller S, Reynaud C-A 2009. Human marginal zone B cells. Annu. Rev. Immunol. 27:267–85
    [Google Scholar]
  80. 80.
    Regules JA, Cicatelli SB, Bennett JW, Paolino KM, Twomey PS et al. 2016. Fractional third and fourth dose of RTS,S/AS01 malaria candidate vaccine: a phase 2a controlled human malaria parasite infection and immunogenicity study. J. Infect. Dis. 214:5762–71
    [Google Scholar]
  81. 81.
    Osier FHA, Fegan G, Polley SD, Murungi L, Verra F et al. 2008. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect. Immun. 76:52240–48
    [Google Scholar]
  82. 82.
    Osier FHA, Mackinnon MJ, Crosnier C, Fegan G, Kamuyu G et al. 2014. New antigens for a multicomponent blood-stage malaria vaccine. Sci. Transl. Med. 6:247247ra102
    [Google Scholar]
  83. 83.
    Fowkes FJI, Richards JS, Simpson JA, Beeson JG 2010. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLOS Med 7:1e1000218
    [Google Scholar]
  84. 84.
    Cheng XJ, Hayasaka H, Watanabe K, Tao YL, Liu JY et al. 2007. Production of high-affinity human monoclonal antibody Fab fragments to the 19-kilodalton C-terminal merozoite surface protein 1 of Plasmodium falciparum. Infect. . Immun 75:73614–20
    [Google Scholar]
  85. 85.
    Stubbs J, Olugbile S, Saidou B, Simpore J, Corradin G, Lanzavecchia A 2011. Strain-transcending Fc-dependent killing of Plasmodium falciparum by merozoite surface protein 2 allele-specific human antibodies. Infect. Immun. 79:31143–52
    [Google Scholar]
  86. 86.
    Maskus DJ, Królik M, Bethke S, Spiegel H, Kapelski S et al. 2016. Characterization of a novel inhibitory human monoclonal antibody directed against Plasmodium falciparum apical membrane antigen 1. Sci. Rep. 6:39462
    [Google Scholar]
  87. 87.
    Beeson JG, Drew DR, Boyle MJ, Feng G, Fowkes FJI, Richards JS 2016. Merozoite surface proteins in red blood cell invasion, immunity and vaccines against malaria. FEMS Microbiol. Rev. 40:3343–72
    [Google Scholar]
  88. 88.
    Riley EM, Stewart VA 2013. Immune mechanisms in malaria: new insights in vaccine development. Nat. Med. 19:2168–78
    [Google Scholar]
  89. 89.
    Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T 1975. Invasion of erythrocytes by malaria merozoites. Science 187:4178748–50
    [Google Scholar]
  90. 90.
    Gilson PR, Crabb BS 2009. Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int. J. Parasitol. 39:191–96
    [Google Scholar]
  91. 91.
    Weiss GE, Crabb BS, Gilson PR 2016. Overlaying molecular and temporal aspects of malaria parasite invasion. Trends Parasitol 32:4284–95
    [Google Scholar]
  92. 92.
    Cowman AF, Tonkin CJ, Tham W-H, Duraisingh MT 2017. The molecular basis of erythrocyte invasion by malaria parasites. Cell Host Microbe 22:232–45
    [Google Scholar]
  93. 93.
    Boyle MJ, Langer C, Chan J-A, Hodder AN, Coppel RL et al. 2014. Sequential processing of merozoite surface proteins during and after erythrocyte invasion by Plasmodium falciparum. Infect. . Immun 82:3924–36
    [Google Scholar]
  94. 94.
    Bruce MC, Galinski MR, Barnwell JW, Donnelly CA, Walmsley M et al. 2000. Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121:3257–72
    [Google Scholar]
  95. 95.
    Henning L, Schellenberg D, Smith T, Henning D, Alonso P et al. 2004. A prospective study of Plasmodium falciparum multiplicity of infection and morbidity in Tanzanian children. Trans. R. Soc. Trop. Med. Hyg. 98:12687–94
    [Google Scholar]
  96. 96.
    Bendixen M, Msangeni HA, Pedersen BV, Shayo D, Bodker R 2001. Diversity of Plasmodium falciparum populations and complexity of infections in relation to transmission intensity and host age: a study from the Usambara Mountains, Tanzania. Trans. R. Soc. Trop. Med. Hyg. 95:2143–48
    [Google Scholar]
  97. 97.
    Duncan CJA, Hill AVS, Ellis RD 2014. Can growth inhibition assays (GIA) predict blood-stage malaria vaccine efficacy?. Hum. Vaccin. Immunother. 8:6706–14
    [Google Scholar]
  98. 98.
    Joos C, Marrama L, Polson HEJ, Corre S, Diatta A-M et al. 2010. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLOS ONE 5:3e9871
    [Google Scholar]
  99. 99.
    Kapelski S, Klockenbring T, Fischer R, Barth S, Fendel R 2014. Assessment of the neutrophilic antibody-dependent respiratory burst (ADRB) response to Plasmodium falciparum. J. Leukoc. . Biol 96:61131–42
    [Google Scholar]
  100. 100.
    Llewellyn D, Miura K, Fay MP, Williams AR, Murungi LM et al. 2015. Standardization of the antibody-dependent respiratory burst assay with human neutrophils and Plasmodium falciparum malaria. Sci. Rep. 5:14081
    [Google Scholar]
  101. 101.
    Osier FHA, Feng G, Boyle MJ, Langer C, Zhou J et al. 2014. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med 12:1108
    [Google Scholar]
  102. 102.
    Boyle MJ, Reiling L, Feng G, Langer C, Osier FHA et al. 2015. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42:3580–90
    [Google Scholar]
  103. 103.
    Baum J, Chen L, Healer J, Lopaticki S, Boyle M et al. 2009. Reticulocyte-binding protein homologue 5—an essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum. Int. J. Parasitol 39:3371–80
    [Google Scholar]
  104. 104.
    Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M et al. 2011. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. . Nature 480:7378534–37
    [Google Scholar]
  105. 105.
    Bustamante LY, Bartholdson SJ, Crosnier C, Campos MG, Wanaguru M et al. 2013. A full-length recombinant Plasmodium falciparum PfRH5 protein induces inhibitory antibodies that are effective across common PfRH5 genetic variants. Vaccine 31:2373–79
    [Google Scholar]
  106. 106.
    Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J et al. 2012. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487:7407375–79
    [Google Scholar]
  107. 107.
    Williams AR, Douglas AD, Miura K, Illingworth JJ, Choudhary P et al. 2012. Enhancing blockade of Plasmodium falciparum erythrocyte invasion: assessing combinations of antibodies against PfRH5 and other merozoite antigens. PLOS Pathog 8:11e1002991
    [Google Scholar]
  108. 108.
    Wright KE, Hjerrild KA, Bartlett J, Douglas AD, Jin J et al. 2014. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature 515:7527427–30
    [Google Scholar]
  109. 109.
    Chen L, Lopaticki S, Riglar DT, Dekiwadia C, Uboldi AD et al. 2011. An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum. . PLOS Pathog 7:9e1002199
    [Google Scholar]
  110. 110.
    Reddy KS, Amlabu E, Pandey AK, Mitra P, Chauhan VS, Gaur D 2015. Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. PNAS 112:41179–84
    [Google Scholar]
  111. 111.
    Volz JC, Yap A, Sisquella X, Thompson JK, Lim NTY et al. 2016. Essential role of the PfRh5/PfRipr/CyRPA complex during Plasmodium falciparum invasion of erythrocytes. Cell Host Microbe 20:160–71
    [Google Scholar]
  112. 112.
    Galaway F, Drought LG, Fala M, Cross N, Kemp AC et al. 2017. P113 is a merozoite surface protein that binds the N terminus of Plasmodium falciparum RH5. Nat. Commun. 8:14333
    [Google Scholar]
  113. 113.
    Chiu CYH, Healer J, Thompson JK, Chen L, Kaul A et al. 2014. Association of antibodies to Plasmodium falciparum reticulocyte binding protein homolog 5 with protection from clinical malaria. Front. Microbiol. 5:314
    [Google Scholar]
  114. 114.
    Tran TM, Ongoiba A, Coursen J, Crosnier C, Diouf A et al. 2014. Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. J. Infect. Dis. 209:5789–98
    [Google Scholar]
  115. 115.
    Douglas AD, Baldeviano GC, Lucas CM, Lugo-Roman LA, Crosnier C et al. 2015. A PfRH5-based vaccine is efficacious against heterologous strain blood-stage Plasmodium falciparum infection in Aotus monkeys. Cell Host Microbe 17:1130–39
    [Google Scholar]
  116. 116.
    Srinivasan P, Ekanem E, Diouf A, Tonkin ML, Miura K et al. 2014. Immunization with a functional protein complex required for erythrocyte invasion protects against lethal malaria. PNAS 111:2810311–16
    [Google Scholar]
  117. 117.
    Srinivasan P, Baldeviano GC, Miura K, Diouf A, Ventocilla JA et al. 2017. A malaria vaccine protects Aotus monkeys against virulent Plasmodium falciparum infection. NPJ Vaccines 2:14
    [Google Scholar]
  118. 118.
    Nunes JK, Woods C, Carter T, Raphael T, Morin MJ et al. 2014. Development of a transmission-blocking malaria vaccine: progress, challenges, and the path forward. Vaccine 32:435531–39
    [Google Scholar]
  119. 119.
    Sinden RE 2017. Developing transmission-blocking strategies for malaria control. PLOS Pathog 13:7e1006336
    [Google Scholar]
  120. 120.
    malERA Consult. Group Vaccines. 2011. A research agenda for malaria eradication: vaccines. PLOS Med 8:1e1000398
    [Google Scholar]
  121. 121.
    Sauerwein RW, Bousema T 2015. Transmission blocking malaria vaccines: assays and candidates in clinical development. Vaccine 33:527476–82
    [Google Scholar]
  122. 122.
    Kapulu MC, Da DF, Miura K, Li Y, Blagborough AM et al. 2015. Comparative assessment of transmission-blocking vaccine candidates against Plasmodium falciparum. Sci. . Rep 5:11193
    [Google Scholar]
  123. 123.
    Molina-Cruz A, Garver LS, Alabaster A, Bangiolo L, Haile A et al. 2013. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340:6135984–87
    [Google Scholar]
  124. 124.
    Carter R, Graves PM, Keister DB, Quakyi IA 1990. Properties of epitopes of Pfs 48/45, a target of transmission blocking monoclonal antibodies, on gametes of different isolates of Plasmodium falciparum. . Parasite Immunol 12:6587–603
    [Google Scholar]
  125. 125.
    Rener J, Graves PM, Carter R, Williams JL, Burkot TR 1983. Target antigens of transmission-blocking immunity on gametes of Plasmodium falciparum. J. Exp. . Med 158:3976–81
    [Google Scholar]
  126. 126.
    Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave JP, Smits MA et al. 1985. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J. Exp. Med. 162:51460–76
    [Google Scholar]
  127. 127.
    Stone WJR, Campo JJ, Ouédraogo AL, Meerstein-Kessel L, Morlais I et al. 2018. Unravelling the immune signature of Plasmodium falciparum transmission-reducing immunity. Nat. Commun 9:558 Correction. 2018. Nat. Commun. 9:1498
    [Google Scholar]
  128. 128.
    Scally SW, McLeod B, Bosch A, Miura K, Liang Q et al. 2017. Molecular definition of multiple sites of antibody inhibition of malaria transmission-blocking vaccine antigen Pfs25. Nat. Commun. 8:11568
    [Google Scholar]
  129. 129.
    Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC et al. 1995. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:177–87
    [Google Scholar]
  130. 130.
    Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE et al. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:1101–10
    [Google Scholar]
  131. 131.
    Fernandez V, Hommel M, Chen Q, Hagblom P, Wahlgren M 1999. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the Rif gene family and are the target of human immune responses. J. Exp. Med. 190:101393–404
    [Google Scholar]
  132. 132.
    Kyes SA, Rowe JA, Kriek N, Newbold CI 1999. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. . PNAS 96:169333–38
    [Google Scholar]
  133. 133.
    Kaviratne M, Khan SM, Jarra W, Preiser PR 2002. Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryot. Cell 1:6926–35
    [Google Scholar]
  134. 134.
    Scherf A, Lopez-Rubio J-J, Riviere L 2008. Antigenic variation in Plasmodium falciparum. Annu. Rev. . Microbiol 62:445–70
    [Google Scholar]
  135. 135.
    Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L et al. 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200:91197–203
    [Google Scholar]
  136. 136.
    Rowe JA, Claessens A, Corrigan RA, Arman M 2009. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev. Mol. Med. 11:e16
    [Google Scholar]
  137. 137.
    Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JEV et al. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498:7455502–5
    [Google Scholar]
  138. 138.
    Bull PC, Abdi AI 2016. The role of PfEMP1 as targets of naturally acquired immunity to childhood malaria: prospects for a vaccine. Parasitology 143:2171–86
    [Google Scholar]
  139. 139.
    Avril M, Tripathi AK, Brazier AJ, Andisi C, Janes JH et al. 2012. A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells. PNAS 109:26E1782–90
    [Google Scholar]
  140. 140.
    Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC et al. 2012. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. PNAS 109:26E1772–81
    [Google Scholar]
  141. 141.
    Azasi Y, Lindergard G, Ghumra A, Mu J, Miller LH, Rowe JA 2018. Infected erythrocytes expressing DC13 PfEMP1 differ from recombinant proteins in EPCR-binding function. PNAS 115:51063–68
    [Google Scholar]
  142. 142.
    Avril M, Bernabeu M, Benjamin M, Brazier AJ, Smith JD 2016. Interaction between endothelial protein C receptor and intercellular adhesion molecule 1 to mediate binding of Plasmodium falciparum-infected erythrocytes to endothelial cells. mBio 7:4e00615–16
    [Google Scholar]
  143. 143.
    Lennartz F, Adams Y, Bengtsson A, Olsen RW, Turner L et al. 2017. Structure-guided identification of a family of dual receptor-binding PfEMP1 that is associated with cerebral malaria. Cell Host Microbe 21:3403–14
    [Google Scholar]
  144. 144.
    Cunnington AJ, Riley EM, Walther M 2013. Stuck in a rut? Reconsidering the role of parasite sequestration in severe malaria syndromes. Trends Parasitol 29:12585–92
    [Google Scholar]
  145. 145.
    Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE 1998. Maternal antibodies block malaria. Nature 395:6705851–52
    [Google Scholar]
  146. 146.
    Fried M, Duffy PE 2015. Designing a VAR2CSA-based vaccine to prevent placental malaria. Vaccine 33:527483–88
    [Google Scholar]
  147. 147.
    Magistrado P, Salanti A, Tuikue Ndam NG, Mwakalinga SB, Resende M et al. 2008. VAR2CSA expression on the surface of placenta-derived Plasmodium falciparum-infected erythrocytes. J. Infect. Dis. 198:71071–74
    [Google Scholar]
  148. 148.
    McRobert L, Preiser P, Sharp S, Jarra W, Kaviratne M et al. 2004. Distinct trafficking and localization of STEVOR proteins in three stages of the Plasmodium falciparum life cycle. Infect. Immun. 72:116597–602
    [Google Scholar]
  149. 149.
    Blythe JE, Yam XY, Kuss C, Bozdech Z, Holder AA et al. 2008. Plasmodium falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites. Infect. Immun. 76:73329–36
    [Google Scholar]
  150. 150.
    Khattab A, Meri S 2011. Exposure of the Plasmodium falciparum clonally variant STEVOR proteins on the merozoite surface. Malar. J 10:158
    [Google Scholar]
  151. 151.
    Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M et al. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419:6906520–26
    [Google Scholar]
  152. 152.
    Petter M, Haeggström M, Khattab A, Fernandez V, Klinkert M-Q, Wahlgren M 2007. Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns. Mol. Biochem. Parasitol. 156:151–61
    [Google Scholar]
  153. 153.
    Sanyal S, Egee S, Bouyer G, Perrot S, Safeukui I et al. 2012. Plasmodium falciparum STEVOR proteins impact erythrocyte mechanical properties. Blood 119:2e1–8
    [Google Scholar]
  154. 154.
    Niang M, Bei AK, Madnani KG, Pelly S, Dankwa S et al. 2014. STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host Microbe 16:181–93
    [Google Scholar]
  155. 155.
    Niang M, Yan Yam X, Preiser PR 2009. The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte. PLOS Pathog 5:2e1000307
    [Google Scholar]
  156. 156.
    Goel S, Palmkvist M, Moll K, Joannin N, Lara P et al. 2015. RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nat. Med. 21:4314–17
    [Google Scholar]
  157. 157.
    Tan J, Pieper K, Piccoli L, Abdi A, Foglierini M et al. 2016. A LAIR1 insertion generates broadly reactive antibodies against malaria variant antigens. Nature 529:7584105–9
    [Google Scholar]
  158. 158.
    Saito F, Hirayasu K, Satoh T, Wang CW, Lusingu J et al. 2017. Immune evasion of Plasmodium falciparum by RIFIN via inhibitory receptors. Nature 552:7683101–5 Corrigendum. 2018 Nature554554
    [Google Scholar]
  159. 159.
    Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 4:3358–60
    [Google Scholar]
  160. 160.
    Giha HA, Staalsoe T, Dodoo D, Roper C, Satti GMH et al. 2000. Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immunol. Lett. 71:2117–26
    [Google Scholar]
  161. 161.
    Duffy PE, Fried M 2003. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infect. Immun. 71:116620–23
    [Google Scholar]
  162. 162.
    Barfod L, Bernasconi NL, Dahlbäck M, Jarrossay D, Andersen PH et al. 2006. Human pregnancy-associated malaria-specific B cells target polymorphic, conformational epitopes in VAR2CSA. Mol. Microbiol. 63:2335–47
    [Google Scholar]
  163. 163.
    Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F et al. 2010. Chondroitin sulfate A-adhering Plasmodium falciparum-infected erythrocytes express functionally important antibody epitopes shared by multiple variants. J. Immunol. 185:127553–61
    [Google Scholar]
  164. 164.
    Pehrson C, Salanti A, Theander TG, Nielsen MA 2017. Pre-clinical and clinical development of the first placental malaria vaccine. Expert Rev. Vaccines 16:6613–24
    [Google Scholar]
  165. 165.
    Stanley HA, Mayes JT, Cooper NR, Reese RT 1984. Complement activation by the surface of Plasmodium falciparum infected erythrocytes. Mol. Immunol. 21:2145–50
    [Google Scholar]
  166. 166.
    Arora G, Hart GT, Manzella-Lapeira J, Doritchamou JYA, Narum DL et al. 2018. NK cells inhibit Plasmodium falciparum growth in red blood cells via antibody-dependent cellular cytotoxicity. eLife 7:e36806
    [Google Scholar]
  167. 167.
    Teo A, Hasang W, Boeuf P, Rogerson S 2015. A robust phagocytosis assay to evaluate the opsonic activity of antibodies against Plasmodium falciparum-infected erythrocytes. Malaria Vaccines: Methods and Protocols A Vaughan 145–52 New York: Springer
    [Google Scholar]
  168. 168.
    Higgins MK, Carrington M 2014. Sequence variation and structural conservation allows development of novel function and immune evasion in parasite surface protein families. Protein Sci 23:4354–65
    [Google Scholar]
  169. 169.
    Newbold CI, Pinches R, Roberts DJ, Marsh K 1992. Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Exp. Parasitol. 75:3281–92
    [Google Scholar]
  170. 170.
    Pieper K, Tan J, Piccoli L, Foglierini M, Barbieri S et al. 2017. Public antibodies to malaria antigens generated by two LAIR1 insertion modalities. Nature 548:7669597–601
    [Google Scholar]
  171. 171.
    Lanzavecchia A 2018. Dissecting human antibody responses: useful, basic and surprising findings. EMBO Mol. Med. 10:3e8879
    [Google Scholar]
  172. 172.
    Hsieh F-L, Higgins MK 2017. The structure of a LAIR1-containing human antibody reveals a novel mechanism of antigen recognition. eLife 6:e27311
    [Google Scholar]
  173. 173.
    Reed JH, Jackson J, Christ D, Goodnow CC 2016. Clonal redemption of autoantibodies by somatic hypermutation away from self-reactivity during human immunization. J. Exp. Med. 213:71255–65
    [Google Scholar]
  174. 174.
    Jardine JG, Ota T, Sok D, Pauthner M, Kulp DW et al. 2015. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science 349:6244156–61
    [Google Scholar]
  175. 175.
    Briney B, Sok D, Jardine JG, Kulp DW, Skog P et al. 2016. Tailored immunogens direct affinity maturation toward HIV neutralizing antibodies. Cell 166:61459–70.e11
    [Google Scholar]
  176. 176.
    Ehrlich P 1901. Die Seitenkettentheorie und ihre Gegner. Münchner Med. Wochenschr. 48:2123–24
    [Google Scholar]
/content/journals/10.1146/annurev-immunol-042617-053301
Loading
/content/journals/10.1146/annurev-immunol-042617-053301
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error