The immunology of malaria infection

Current Opinion in Immunology

Volumn 12, Issue 4, 2000, Pages 437-441

  Plebanski, Magdalena ^a   Hill, Adrian VS ^b  

^a AUSTIN RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; MALARIA VACCINE;

IMMUNE RESPONSE; IMMUNITY; MALARIA; MALARIA CONTROL; PLASMODIUM FALCIPARUM; REVIEW; T LYMPHOCYTE;

EID: 0034044126     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(00)00117-5     Document Type: Review

References (75)

1. Snow R.W., Craig M., Deichmann U., Marsh K. Estimating mortality, morbidity and disability due to malaria among Africa's non-pregnant population. Bull World Health Organ. 77:1999;624-640.
2. Nardin E.H., Nussenzweig R.S. T cell responses to pre-erythrocytic stages of malaria: role in protection and vaccine development against pre-erythrocytic stages. Annu Rev Immunol. 11:1993;687-727.
3. Good M.F., Doolan D.L. Immune effector mechanisms in malaria. Curr Opin Immunol. 11:1999;412-419.
4. Miller L.H., Good M.F., Kaslow D.C. Vaccines against the blood stages of falciparum malaria. Adv Exp Med Biol. 452:1998;193-205.
5. Good M.F., Kaslow D.C., Miller L.H. Pathways and strategies for developing a malaria blood-stage vaccine. Annu Rev Immunol. 16:1998;57-87.
6. Newbold C.I., Craig A.G., Kyes S., Berendt A.R., Snow R.W., Peshu N., Marsh K. PfEMP1, polymorphism and pathogenesis. Ann Trop Med Parasitol. 91:1997;551-557.
7. Saul A. The role of variant surface antigens on malaria-infected red blood cells. Parasitol Today. 15:1999;455-457.
8. Hill A.V., Elvin J., Willis A.C., Aidoo M., Allsopp C.E., Gotch F.M., Gao X.M., Takiguchi M., Greenwood B.M., Townsend A.R.et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature. 360:1992;434-439.
9. Plebanski M., Aidoo M., Whittle H.C., Hill A.V. Precursor frequency analysis of cytotoxic T lymphocytes to pre-erythrocytic antigens of Plasmodium falciparum in West Africa. J Immunol. 158:1997;2849-2855.
10. Plebanski M., Lee E.A., Hill A.V. Immune evasion in malaria: altered peptide ligands of the circumsporozoite protein. Parasitology 115:S55-S66. 1997.
11. Gilbert S.C., Plebanski M., Gupta S., Morris J., Cox M., Aidoo M., Kwiatkowski D., Greenwood B.M., Whittle H.C., Hill A.V. Association of malaria parasite population structure, HLA, and immunological antagonism. Science. 279:1998;1173-1177.
12. + T cell epitope.
13. Flanagan K.L., Plebanski M., Akinwunmi P., Lee E.A., Reece W.H., Robson K.J., Hill A.V., Pinder M. 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. 29:1999;1943-1954.
14. Bull P.C., Lowe B.S., Kortok M., Molyneux C.S., Newbold C.I., Marsh K. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med. 4:1998;358-360.
15. Gupta S., Snow R.W., Donnelly C.A., Marsh K., Newbold C. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med. 5:1999;340-343. In a field study of African children, the first evidence is provided for strain-transcending protective immunity generated after only one or two infections.
16. Plebanski M., Lee E.A., Hannan C.M., Flanagan K.L., Gilbert S.C., Gravenor M.B., Hill A.V. Altered peptide ligands narrow the repertoire of cellular immune responses by interfering with T-cell priming. Nat Med. 5:1999;565-571.
17. Urban B.C., Ferguson D.J., Pain A., Willcox N., Plebanski M., Austyn J.M., Roberts D.J. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature. 400:1999;73-77. Identification of an alternative role for the CD36-binding polymorphic protein PfEMP-1 in immune evasion, by inactivation of dendritic cell function.
18. Quakyi I.A., Otoo L.N., Pombo D., Sugars L.Y., Menon A., DeGroot A.S., Johnson A., Alling D., Miller L.H., Good M.F. Differential non-responsiveness in humans of candidate Plasmodium falciparum vaccine antigens. Am J Trop Med Hyg. 41:1989;125-134.
19. Esposito F., Lombardi S., Modiano D., Habluetzel A., Del Nero L., Lamizana L., Pietra V., Rotigliano G., Corradin G., Ravot E.et al. In vitro immune recognition of synthetic peptides from the Plasmodium falciparum CS protein by individuals naturally exposed to different sporozoite challenge. Immunol Lett. 33:1992;187-199.
20. Doolan D.L., Khamboonruang C., Beck H.P., Houghten R.A., Good M.F. Cytotoxic T lymphocyte (CTL) low-responsiveness to the Plasmodium falciparum circumsporozoite protein in naturally-exposed endemic populations: analysis of human CTL response to most known variants. Int Immunol. 5:1993;37-46.
21. Doolan D., Beck H.P., Good M.F. Evidence for limited activation of distinct CD4+ T cell subsets in response to the Plasmodium falciparum circumsporozoite protein in Papua New Guinea. Parasite Immunol. 16:1994;129-136.
22. Aidoo M., Lalvani A., Allsopp C.E., Plebanski M., Meisner S.J., Krausa P., Browning M., Morris-Jones S., Gotch F., Fidock D.A.et al. Identification of conserved antigenic components for a cytotoxic T lymphocyte-inducing vaccine against malaria. Lancet. 345:1995;1003-1007.
23. Good M.F., Pombo D., Quakyi I.A., Riley E.M., Houghten R.A., Menon A., Alling D.W., Berzofsky J.A., Miller L.H. Human T-cell recognition of the circumsporozoite protein of Plasmodium falciparum: immuno-dominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci USA. 85:1988;1199-1203.
24. Troye-Blomberg M., Romero P., Patarroyo M.E., Bjorkman A., Perlmann P. Regulation of the immune response in Plasmodium falciparum malaria. III. Proliferative response to antigen in vitro and subset composition of T cells from patients with acute infection or from immune donors. Clin Exp Immunol. 58:1984;380-387.
25. Ho M., Webster H.K., Looareesuwan S., Supanaranond W., Phillips R.E., Chanthavanich P., Warrell D.A. Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J Infect Dis. 153:1986;763-771.
26. Ho M., Webster H.K., Green B., Looareesuwan S., Kongchareon S., White N.J. Defective production of and response to IL-2 in acute human falciparum malaria. J Immunol. 141:1988;2755-2759.
27. Hviid L., Theander T.G., Abu-Zeid Y.A., Abdulhadi N.H., Jakobsen P.H., Saeed B.O., Jepsen S., Bayoumi R.A., Jensen J.B. Loss of cellular immune reactivity during acute Plasmodium falciparum malaria. FEMS Microbiol Immunol. 3:1991;219-227.
28. Hoffman S.L., Franke E.D. Inducing protective immune responses against the sporozoite and liver stages of Plasmodium. Immunol Lett. 41:1994;89-94.
29. Lockyer M.J., Marsh K., Newbold C.I. Wild isolates of Plasmodium falciparum show extensive polymorphism in T cell epitopes of the circumsporozoite protein. Mol Biochem Parasitol. 37:1989;275-280.
30. Riley E.M., Allen S.J., Bennett S., Thomas P.J., O'Donnell A., Lindsay S.W., Good M.F., Greenwood B.M. Recognition of dominant T cell-stimulating epitopes from the circumsporozoite protein of Plasmodium falciparum and relationship to malaria morbidity in Gambian children. Trans R Soc Trop Med Hyg. 84:1990;648-657.
31. Hoffman S.L., Oster C.N., Plowe C.V., Woollett G.R., Beier J.C., Chulay J.D., Wirtz R.A., Hollingdale M.R., Mugambi M. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science. 237:1987;639-642.
32. Stoute J.A., Slaoui M., Heppner D.G., Momin P., Kester K.E., Desmons P., Wellde B.T., Garcon N., Krzych U., Marchand M. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. N Engl J Med. 336:1997;86-91.
33. Herrington D., Davis J., Nardin E., Beier M., Cortese J., Eddy H., Losonsky G., Hollingdale M., Sztein M., Levine M. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am J Trop Med Hyg. 45:1991;539-547.
34. Gilbert S.C., Plebanski M., Harris S.J., Allsopp C.E., Thomas R., Layton G.T., Hill A.V. A protein particle vaccine containing multiple malaria epitopes. Nat Biotechnol. 15:1997;1280-1284.
35. Plebanski M., Gilbert S.C., Schneider J., Hannan C.M., Layton G., Blanchard T., Becker M., Smith G., Butcher G., Sinden R.E., Hill A.V. Protection from Plasmodium berghei infection by priming and boosting T cells to a single class I-restricted epitope with recombinant carriers suitable for human use. Eur J Immunol. 28:1998;4345-4355.
36. Schneider J., Gilbert S.C., Blanchard T.J., Hanke T., Robson K.J., Hannan C.M., Becker M., Sinden R., Smith G.L., Hill A.V. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med. 4:1998;397-402.
37. Sedegah M., Jones T.R., Kaur M., Hedstrom R., Hobart P., Tine J.A., Hoffman S.L. Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proc Natl Acad Sci USA. 95:1998;7648-7653.
38. Renggli J., Valmori D., Romero J.F., Eberl G., Romero P., Betschart B., Corradin G. CD8+ T-cell protective immunity induced by immunization with Plasmodium berghei CS protein-derived synthetic peptides: evidence that localization of peptide-specific CTLs is crucial for protection against malaria. Immunol Lett. 46:1995;199-205.
39. Rodrigues M., Nussenzweig R.S., Romero P., Zavala F. The in vivo cytotoxic activity of CD8+ T cell clones correlates with their levels of expression of adhesion molecules. J Exp Med. 175:1992;895-905.
40. Croft M. Activation of naive, memory and effector T cells. Curr Opin Immunol. 6:1994;431-437.
41. Watts T.H., DeBenedette M.A. T cell co-stimulatory molecules other than CD28. Curr Opin Immunol. 11:1999;286-293.
42. Le Moine O., Louis H., Sermon F., Goldman M., Deviere J. Interleukin-10 and liver diseases. Acta Gastroenterol Belg. 62:1999;1-8.
43. Aidoo M., Lalvani A., Gilbert S.C., Hu J.T., Daubersies P., Hurt N., Whittle H.C., Druihle P., Hill A.V. Cytotoxic T-lymphocyte epitopes for HLA-B53 and other HLA types in the malaria vaccine candidate liver-stage antigen 3. Infect Immun. 68:2000;227-232.
44. Davenport M.P. Antagonists or altruists: do viral mutants modulate T-cell responses? Immunol Today. 16:1995;432-436.
45. Nardin E., Munesinghe Y.D., Moreno A., Clavijo P., Calle M.C., Edelman R., Davis J., Herrington D., Nussenzweig R.S. T cell responses to repeat and non-repeat regions of the circumsporozoite protein detected in volunteers immunized with Plasmodium falciparum sporozoites. Mem Inst Oswaldo Cruz. 3:1992;223-227.
46. Tsuji M., Romero P., Nussenzweig R.S., Zavala F. CD4+ cytolytic T cell clone confers protection against murine malaria. J Exp Med. 172:1990;1353-1357.
47. Takita-Sonoda Y., Tsuji M., Kamboj K., Nussenzweig R.S., Clavijo P., Zavala F. Plasmodium yoelii: peptide immunization induces protective CD4+ T cells against a previously unrecognized cryptic epitope of the circumsporozoite protein. Exp Parasitol. 84:1996;223-230.
48. Renia L., Grillot D., Marussig M., Corradin G., Miltgen F., Lambert P.H., Mazier D., Del Giudice G. Effector functions of circumsporozoite peptide-primed CD4+ T cell clones against Plasmodium yoelii liver stages. J Immunol. 150:1993;1471-1478.
49. Weiss W.R., Sedegah M., Berzofsky J.A., Hoffman S.L. The role of CD4+ T cells in immunity to malaria sporozoites. J Immunol. 151:1993;2690-2698.
50. + T cell epitope.
51. Doolan D.L., Hoffman S.L. IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. J Immunol. 163:1999;884-892.
52. Rzepczyk C.M., Anderson K., Stamatiou S., Townsend E., Allworth A., McCormack J., Whitby M. Gamma delta T cells: their immunobiology and role in malaria infections. Int J Parasitol. 27:1997;191-200.
53. Langhorne J., Mombaerts P., Tonegawa S. Alpha beta and gamma delta T cells in the immune response to the erythrocytic stages of malaria in mice. Int Immunol. 7:1995;1005-1011.
54. Lalvani A., Moris P., Voss G., Pathan A.A., Kester K.E., Brookes R., Lee E., Koutsoukos M., Plebanski M., Delchambre M.et al. Potent induction of focused Th1-type cellular and humoral immune responses by RTS,S/SBAS2, a recombinant Plasmodium falciparum malaria vaccine. J Infect Dis. 180:1999;1656-1664.
55. Akdis C.A., Blaser K. IL-10-induced anergy in peripheral T cell and reactivation by microenvironmental cytokines: two key steps in specific immunotherapy. FASEB J. 13:1999;603-609.
56. Groux H., Powrie F. Regulatory T cells and inflammatory bowel disease. Immunol Today. 20:1999;442-445.
57. Winkler S., Willheim M., Baier K., Schmid D., Aichelburg A., Graninger W., Kremsner P.G. Reciprocal regulation of Th1- and Th2-cytokine-producing T cells during clearance of parasitemia in Plasmodium falcipaum malaria. Infect Immun. 66:1998;6040-6044.
58. Winkler S., Willheim M., Baier K., Schmid D., Aichelburg A., Graninger W., Kremsner P.G. Frequency of cytokine producing T cells in patients of different age groups with Plasmodium falciparum malaria. J Infect Dis. 179:1999;209-216.
59. Luty A.J., Lell B., Schmidt-Ott R., Lehman L.G., Luckner D., Greve B., Matousek P., Herbich K., Schmid D., Migot-Nabias F.et al. Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis. 179:1999;980-988.
60. Ferrante A., Kumaratilake L., Rzepczyk C.M., Dayer J.M. Killing of Plasmodium falciparum by cytokine activated effector cells (neutrophils and macrophages). Immunol Lett. 25:1990;179-187.
61. Stevenson M.M., Ghadirian E., Phillips N.C., Rae D., Podoba J.E. Role of mononuclear phagocytes in elimination of Plasmodium chabaudi AS infection. Parasite Immunol. 11:1989;529-544.
62. Ockenhouse C.F., Schulman S., Shear H.L. Induction of crisis forms in the human malaria parasite Plasmodium falciparum by gamma-interferon-activated, monocyte-derived macrophages. J Immunol. 133:1984;1601-1608.
63. Bouharoun-Tayoun H., Oeuvray C., Lunel F., Druilhe P. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J Exp Med. 182:1995;409-418.
64. Leitner W.W., Krzych U. Plasmodium falciparum malaria blood stage parasites preferentially inhibit macrophages with high phagocytic activity. Parasite Immunol. 19:1997;103-110.
65. Hirunpetcharat C., Good M.F. Deletion of Plasmodium berghei-specific CD4+ T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc Natl Acad Sci USA. 95:1998;1715-1720.
66. Kyes S.A., Rowe J.A., Kriek N., Newbold C.I. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci USA. 96:1999;9333-9338. Description of a new, variable protein family that may challenge the assumed paramount importance of PfEMP1 in protection and immune evasion for blood-stage malaria.
67. Wellems T.E., Su X.Z., Ferdig M., Fidock D.A. Genome projects, genetic analysis, and the changing landscape of malaria research. Curr Opin Microbiol. 2:1999;415-419.
68. Wang R., Doolan D.L., Le T.P., Hedstrom R.C., Coonan K.M., Charoenvit Y., Jones T.R., Hobart P., Margalith M., Ng J.et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science. 282:1998;476-480.
69. Ockenhouse C.F., Sun P.F., Lanar D.E., Wellde B.T., Hall B.T., Kester K., Stoute J.A., Magill A., Krzych U., Farley L.et al. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J Infect Dis. 177:1998;1664-1673.
70. Saul A., Lawrence G., Smillie A., Rzepczyk C.M., Reed C., Taylor D., Anderson K., Stowers A., Kemp R., Allworth A.et al. Human phase I vaccine trials of 3 recombinant asexual stage malaria antigens with Montanide ISA720 adjuvant. Vaccine. 17:1999;3145-3159. This shows induction of antibodies and cellular immune responses to all three antigens tested: MSP1, MSP2 and RESA.
71. Keitel W.A., Kester K.E., Atmar R.L., White A.C., Bond N.H., Holland C.A., Krzych U., Palmer D.R., Egan A., Diggs C.et al. Phase I trial of two recombinant vaccines containing the 19kd carboxy terminal fragment of Plasmodium falciparum merozoite surface protein 1 (msp-1(19)) and T helper epitopes of tetanus toxoid. Vaccine. 18:1999;531-539.
72. Stoute J.A., Kester K.E., Krzych U., Wellde B.T., Hall T., White K., Glenn G., Ockenhouse C.F., Garcon N., Schwenk R.et al. Long-term efficacy and immune responses following immunization with the RTS,S malaria vaccine. J Infect Dis. 178:1998;1139-1144.
73. Schneider J., Gilbert S.C., Hannan C.M., Degano P., Prieur E., Sheu E.G., Plebanski M., Hill A.V. Induction of CD8+ T cells using heterologous prime-boost immunisation strategies. Immunol Rev. 170:1999;29-38.
74. Li S., Rodrigues M., Rodriguez D., Rodriguez J.R., Esteban M., Palese P., Nussenzweig R.S., Zavala F. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria. Proc Natl Acad Sci USA. 90:1993;5214-5218.
75. Miyahira Y., Garcia-Sastre A., Rodriguez D., Rodriguez J.R., Murata K., Tsuji M., Palese P., Esteban M., Zavala F., Nussenzweig R.S. Recombinant viruses expressing a human malaria antigen can elicit potentially protective immune CD8+ responses in mice. Proc Natl Acad Sci USA. 95:1998;3954-3959.