Functional Antibodies and Protection against Blood-stage Malaria

Trends in Parasitology

Volumn 32, Issue 11, 2016, Pages 887-898

  Teo, Andrew ^a   Feng, Gaoqian ^b   Brown, Graham V ^a,c   Beeson, James G ^a,b,d   Rogerson, Stephen J ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b BURNET INSTITUTE   (Australia)

^c PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

antibody; immunity; naturally acquired; Plasmodium falciparum; vaccine design

Indexed keywords

PROTOZOON ANTIBODY; MALARIA VACCINE; PARASITE ANTIGEN;

COMPLEMENT FIXATION; ERYTHROCYTE; ERYTHROCYTE ADHESIVENESS; HUMAN; IMMUNITY; INFECTION PREVENTION; MALARIA FALCIPARUM; MEROZOITE; MICROBIAL GROWTH; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; RESPIRATORY BURST; REVIEW; ROSETTE FORMATION; BLOOD; IMMUNOLOGY; MALARIA, FALCIPARUM;

ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; HUMANS; IMMUNITY; MALARIA VACCINES; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM;

EID: 84994157121     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2016.07.003     Document Type: Review

References (92)

1. 1 World Health Organisation. World Malaria Report 2015., 2015.
2. 2 Cohen, S., et al. Gamma-globulin and acquired immunity to human malaria. Nature 192 (1961), 733–737.
3. 3 Riley, E.M., et al. Do maternally acquired antibodies protect infants from malaria infection?. Parasite Immunol. 23 (2001), 51–59.
4. 4 White, M.T., et al. A combined analysis of immunogenicity, antibody kinetics and vaccine efficacy from Phase 2 trials of the RTS,S malaria vaccine. BMC Med., 12, 2014, 117.
5. 5 Foquet, L., et al. Vaccine-induced monoclonal antibodies targeting circumsporozoite protein prevent Plasmodium falciparum infection. J. Clin. Invest. 124 (2014), 140–144.
6. 6 Beeson, J.G., et al. Correlates of protection for Plasmodium falciparum malaria vaccine development: current knowledge and future research. Malaria Vaccine Development: Over 40 Years of Trials and Tribulations, 2014, Future Medicine Ltd, 80–104.
7. 7 R.T.S.-S Clinical Trials Partnership. 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 (2015), 31–45.
8. 8 Fowkes, F.J., et al. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med., 7, 2010, e1000218.
9. 9 Weiss, G.E., et al. Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLoS Pathog., 11, 2015, e1004670.
10. 10 Richards, J.S., et al. Identification and prioritization of merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. J. Immunol. 191 (2013), 795–809.
11. 11 Beeson, J.G., et al. Merozoite surface proteins in red blood cell invasion, immunity and vaccines against malaria. FEMS Microbiol. Rev. 40 (2016), 343–372.
12. 12 Stanisic, D.I., et al. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Infect. Immun. 77 (2009), 1165–1174.
13. 13 Richards, J.S., et al. Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin. Infect. Dis. 51 (2010), e50–e60.
14. 14 Roussilhon, C., et al. Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS Med., 4, 2007, e320.
15. 15 O'Donnell, R.A., et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J. Exp. Med. 193 (2001), 1403–1412.
16. 16 Persson, K.E., et al. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J. Clin. Invest. 118 (2008), 342–351.
17. 17 Persson, K.E., et al. Erythrocyte-binding antigens of Plasmodium falciparum are targets of human inhibitory antibodies and function to evade naturally acquired immunity. J. Immunol. 191 (2013), 785–794.
18. 18 Boyle, M.J., et al. Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc. Nat. Acad. Sci. U.S.A. 107 (2010), 14378–14383.
19. 19 Boyle, M.J., et al. New approaches to studying Plasmodium falciparum merozoite invasion and insights into invasion biology. Int. J. Parasitol. 43 (2013), 1–10.
20. 20 Wilson, D.W., et al. Quantifying the importance of MSP1-19 as a target of growth-inhibitory and protective antibodies against Plasmodium falciparum in humans. PLoS ONE, 6, 2011, e27705.
21. 21 Quelhas, D., et al. IgG against Plasmodium falciparum variant surface antigens and growth inhibitory antibodies in Mozambican children receiving intermittent preventive treatment with sulfadoxine-pyrimethamine. Immunobiology 216 (2011), 793–802.
22. 22 Chitnis, C.E., et al. Phase I clinical trial of a recombinant blood stage vaccine candidate for Plasmodium falciparum malaria based on MSP1 and EBA175. PLoS ONE, 10, 2015, e0117820.
23. 23 Irani, V., et al. Acquisition of functional antibodies that block the binding of erythrocyte-binding antigen 175 and protection against Plasmodium falciparum malaria in children. Clin. Infect. Dis. 61 (2015), 1244–1252.
24. 24 Reiling, L., et al. The Plasmodium falciparum erythrocyte invasion ligand Pfrh4 as a target of functional and protective human antibodies against malaria. PLoS ONE, 7, 2012, e45253.
25. 25 Tran, T.M., et al. Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. J. Infect. Dis. 209 (2014), 789–798.
26. 26 Patel, S.D., et al. Plasmodium falciparum merozoite surface antigen, PfRH5, elicits detectable levels of invasion-inhibiting antibodies in humans. J. Infect. Dis. 208 (2013), 1679–1687.
27. 27 Draper, S.J., et al. Recent advances in recombinant protein-based malaria vaccines. Vaccine 33 (2015), 7433–7443.
28. 28 Remarque, E.J., et al. Humoral immune responses to a single allele PfAMA1 vaccine in healthy malaria-naive adults. PLoS ONE, 7, 2012, e38898.
29. 29 Thera, M.A., et al. A field trial to assess a blood-stage malaria vaccine. N. Engl. J. Med. 365 (2011), 1004–1013.
30. 30 Malkin, E.M., et al. Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. Infect. Immun. 73 (2005), 3677–3685.
31. 31 Drew, D.R., et al. Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. PLoS ONE, 7, 2012, e51023.
32. 32 Mugyenyi, C.K., et al. Antibodies to polymorphic invasion-inhibitory and non-inhibitory epitopes of Plasmodium falciparum apical membrane antigen 1 in human malaria. PLoS ONE, 8, 2013, e68304.
33. 33 Murungi, L.M., et al. Targets and mechanisms associated with protection from severe Plasmodium falciparum malaria in Kenyan children. Infect. Immun. 84 (2016), 950–963.
34. 34 Miura, K., et al. Comparison of biological activity of human anti-apical membrane antigen-1 antibodies induced by natural infection and vaccination. J. Immunol. 181 (2008), 8776–8783.
35. 35 Srinivasan, P., et al. Immunization with a functional protein complex required for erythrocyte invasion protects against lethal malaria. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 10311–10316.
36. 36 McCallum, F.J., et al. Acquisition of growth-inhibitory antibodies against blood-stage Plasmodium falciparum. PLoS ONE, 3, 2008, e3571.
37. 37 Courtin, D., et al. The quantity and quality of African children's IgG responses to merozoite surface antigens reflect protection against Plasmodium falciparum malaria. PLoS ONE, 4, 2009, e7590.
38. 38 Dent, A.E., et al. Antibody-mediated growth inhibition of Plasmodium falciparum: relationship to age and protection from parasitemia in Kenyan children and adults. PLoS ONE, 3, 2008, e3557.
39. 39 Duncan, C.J., et al. Can growth inhibition assays (GIA) predict blood-stage malaria vaccine efficacy?. Hum. Vaccin. Immunother. 8 (2012), 706–714.
40. 40 Jogdand, P.S., et al. Flow cytometric readout based on Mitotracker Red CMXRos staining of live asexual blood stage malarial parasites reliably assesses antibody dependent cellular inhibition. Malar. J., 11, 2012, 235.
41. 41 Persson, K.E., et al. Development and optimization of high-throughput methods to measure Plasmodium falciparum-specific growth inhibitory antibodies. J. Clin. Microbio. 44 (2006), 1665–1673.
42. 42 Boyle, M.J., et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42 (2015), 580–590.
43. 43 Hill, D.L., et al. Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE, 8, 2013, e74627.
44. 44 Osier, F.H., et al. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med., 12, 2014, 108.
45. 45 Sakamoto, H., et al. Antibodies against a Plasmodium falciparum antigen PfMSPDBL1 inhibit merozoite invasion into human erythrocytes. Vaccine 30 (2012), 1972–1980.
46. 46 Chiu, C.Y., et al. Antibodies to the Plasmodium falciparum proteins MSPDBL1 and MSPDBL2 opsonise merozoites, inhibit parasite growth, and predict protection from clinical malaria. J. Infect. Dis. 212 (2015), 406–415.
47. 47 Bouharoun-Tayoun, H., et al. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182 (1995), 409–418.
48. 48 McCarthy, J.S., et al. A Phase 1 trial of MSP2-C1, a blood-stage malaria vaccine containing 2 isoforms of MSP2 formulated with Montanide(R) ISA 720. PLoS ONE, 6, 2011, e24413.
49. 49 Druilhe, P., et al. A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS Med., 2, 2005, e344.
50. 50 Galamo, C.D., et al. Anti-MSP1 block 2 antibodies are effective at parasite killing in an allele-specific manner by monocyte-mediated antibody-dependent cellular inhibition. J. Infect. Dis. 199 (2009), 1151–1154.
51. 51 Joos, C., et al. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonised with human serum antibodies. PLoS ONE, 5, 2010, e9871.
52. 52 Greve, B., et al. High oxygen radical production is associated with fast parasite clearance in children with Plasmodium falciparum malaria. J. Infect. Dis. 179 (1999), 1584–1586.
53. 53 Perraut, R., et al. Association of antibody responses to the conserved Plasmodium falciparum merozoite surface protein 5 with protection against clinical malaria. PLoS ONE, 9, 2014, e101737.
54. 54 Carlson, J., et al. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336 (1990), 1457–1460.
55. 55 Fried, M., et al. Maternal antibodies block malaria. Nature 395 (1998), 851–852.
56. 56 Jaworowski, A., et al. Relationship between human immunodeficiency virus type 1 coinfection, anemia, and levels and function of antibodies to variant surface antigens in pregnancy-associated malaria. Clin. Vaccine Immunol. 16 (2009), 312–319.
57. 57 Raj, D.K., et al. Antibodies to PfSEA-1 block parasite egress from RBCs and protect against malaria infection. Science 344 (2014), 871–877.
58. 58 Chan, J.A., et al. Surface antigens of Plasmodium falciparum-infected erythrocytes as immune targets and malaria vaccine candidates. Cell Mol. Life Sci. 71 (2014), 3633–3657.
59. 59 Bengtsson, A., et al. A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesion-inhibitory antibodies. J. Immunol. 190 (2013), 240–249.
60. 60 Turner, L., et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498 (2013), 502–505.
61. 61 Chan, J.A., et al. Targets of antibodies against Plasmodium falciparum-infected erythrocytes in malaria immunity. J. Clin. Invest. 122 (2012), 3227–3238.
62. 62 Scherf, A., et al. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. Embo J. 17 (1998), 5418–5426.
63. 63 Smith, J.D., et al. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol. Biochem. Parasitol. 110 (2000), 293–310.
64. 64 Ochola, L.B., et al. Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS ONE, 6, 2011, e14741.
65. 65 Oleinikov, A.V., et al. High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 Plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies. PLoS Pathog., 5, 2009, e1000386.
66. 66 Turner, L., et al. IgG antibodies to endothelial protein C receptor-binding cysteine-rich interdomain region domains of Plasmodium falciparum erythrocyte membrane protein 1 are acquired early in life in individuals exposed to malaria. Infect. Immun. 83 (2015), 3096–3103.
67. 67 Salanti, A., et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200 (2004), 1197–1203.
68. 68 Clausen, T.M., et al. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J. Biol. Chem. 287 (2012), 23332–23345.
69. 69 Gamain, B., et al. Identification of multiple chondroitin sulfate A (CSA)-binding domains in the var2CSA gene transcribed in CSA-binding parasites. J. Infect. Dis. 191 (2005), 1010–1013.
70. 70 Bordbar, B., et al. Identification of Id1-DBL2X of VAR2CSA as a key domain inducing highly inhibitory and cross-reactive antibodies. Vaccine 30 (2012), 1343–1348.
71. 71 Avril, M., et al. Immunization with VAR2CSA-DBL5 recombinant protein elicits broadly cross-reactive antibodies to placental Plasmodium falciparum-infected erythrocytes. Infect. Immun. 78 (2010), 2248–2256.
72. 72 Nielsen, M.A., et al. Induction of adhesion-inhibitory antibodies against placental Plasmodium falciparum parasites by using single domains of VAR2CSA. Infect. Immun. 77 (2009), 2482–2487.
73. 73 Obiakor, H., et al. Identification of VAR2CSA domain-specific inhibitory antibodies of the Plasmodium falciparum erythrocyte membrane protein 1 using a novel flow cytometry assay. Clin. Vaccine Immunol. 20 (2013), 433–442.
74. 74 Tutterrow, Y.L., et al. High levels of antibodies to multiple domains and strains of VAR2CSA correlate with the absence of placental malaria in Cameroonian women living in an area of high Plasmodium falciparum transmission. Infect. Immun. 80 (2012), 1479–1490.
75. 75 Staalsoe, T., et al. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet 363 (2004), 283–289.
76. 76 Dechavanne, S., et al. Parity-dependent recognition of DBL1X-3X suggests an important role of the VAR2CSA high-affinity CSA-binding region in the development of the humoral response against placental malaria. Infect. Immun. 83 (2015), 2466–2474.
77. 77 Duffy, P.E., Fried, M., 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 (2003), 6620–6623.
78. 78 Ndam, N.T., et al. Protective antibodies against placental malaria and poor outcomes during pregnancy, Benin. Emerg. Infect. Dis. 21 (2015), 813–823.
79. 79 Rowe, A., et al. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun. 63 (1995), 2323–2326.
80. 80 al-Yaman, F., et al. Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans. R. Soc. Trop. Med. Hyg. 89 (1995), 55–58.
81. 81 Cockburn, I.A., et al. A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 272–277.
82. 82 Tham, W.H., et al. Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 17327–17332.
83. 83 Ghumra, A., et al. Immunisation with recombinant PfEMP1 domains elicits functional rosette-inhibiting and phagocytosis-inducing antibodies to Plasmodium falciparum. PLoS ONE, 6, 2011, e16414.
84. 84 Schofield, L., Intravascular infiltrates and organ-specific inflammation in malaria pathogenesis. Immunol. Cell Biol. 85 (2007), 130–137.
85. 85 Lee, S.H., et al. Antibody-dependent red cell removal during P. falciparum malaria: the clearance of red cells sensitized with an IgG anti-D. Br. J. Haematol. 73 (1989), 396–402.
86. 86 Zhou, J., et al. Opsonization of malaria-infected erythrocytes activates the inflammasome and enhances inflammatory cytokine secretion by human macrophages. Malar. J., 11, 2012, 343.
87. 87 Feng, G., et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes are associated with protection from treatment failure and the development of anemia in pregnancy. J. Infect. Dis. 200 (2009), 299–306.
88. 88 Ataíde, R., et al. Antibodies that induce phagocytosis of malaria infected erythrocytes: effect of HIV infection and correlation with clinical outcomes. PLoS ONE, 6, 2011, e22491.
89. 89 Hasang, W., et al. HIV-1 infection and antibodies to Plasmodium falciparum in adults. J. Infect. Dis. 210 (2014), 1407–1414.
90. 90 Subramaniam, K.S., et al. HIV malaria co-infection is associated with atypical memory B cell expansion and a reduced antibody response to a broad array of Plasmodium falciparum antigens in Rwandan adults. PLoS ONE, 10, 2015, e0124412.
91. 91 Chua, C.L., et al. Monocytes and macrophages in malaria: protection or pathology?. Trends Parasitol. 29 (2013), 26–34.
92. 92 Zhou, J., et al. CD14 hi CD16+ monocytes phagocytose antibody-opsonised Plasmodium falciparum infected erythrocytes more efficiently than other monocyte subsets, and require CD16 and complement to do so. BMC Medicine, 13, 2015, 154.