CD4 T cells from malaria-nonexposed individuals respond to the CD36-binding domain of Plasmodium falciparum erythrocyte membrane protein-1 via an MHC class II-TCR-independent pathway

Journal of Immunology

Volumn 176, Issue 9, 2006, Pages 5504-5512

  Ndungu, Francis M ^a,b   Sanni, Latifu ^a,c   Urban, Britta ^d   Stephens, Robin ^a   Newbold, Christopher I ^e   Marsh, Kevin ^b   Langhorne, Jean ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^c LEEDS GENERAL INFIRMARY   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; CD4 ANTIGEN; ERYTHROCYTE MEMBRANE PROTEIN 1; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN; PROTOZOAL PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD DONOR; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYSTEINE INTERDOMAIN REGION 1ALPHA; CYTOKINE PRODUCTION; DENDRITIC CELL; EXPOSURE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOLOGICAL MEMORY; IMMUNOREGULATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MALARIA; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DOMAIN;

EID: 33645959484     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.9.5504     Document Type: Article

References (43)

1. Good, M. F. 1990. Summary of the meeting on cellular mechanisms in malaria immunity. Immunol. Lett. 25: 1-10.
2. Good, M. F. 1994. Immunological responses from non-exposed donors to malaria antigens: implications for immunity and pathology. Immunol. Lett. 41: 123-125.
3. + T cells from nonexposed donors: potential for cross-reactive memory T cells to cause disease. Int. Immunol. 7: 821-833.
4. Goodier, M., P. Fey, K. Eichmann, and J. Langhome. 1992. Human peripheral blood γδ T cells respond to antigens of Plasmodium falciparum. Int. Immunol. 4: 33-41.
5. Dick, S., M. Waterfall, J. Currie, A. Maddy, and E. Riley. 1996. Naive human αβ T cells respond to membrane-associated components of malaria-infected erythrocytes by proliferation and production of interferon-γ. Immunology 88: 412-420.
6. Bilsborough, J., M. Carlisle, and M. F. Good. 1993. Identification of Caucasian CD4 T cell epitopes on the circumsporozoite protein of Plasmodium vivax. T cell memory. J. Immunol. 151: 890-899.
7. Ohta, N., K. Iwaki, M. Itoh, J. Fu, S. Nakashima, M. Hato, R. Tolle, H. Bujard, A. Saitoh, and K. Tanabe. 1997. Epitope analysis of human T-cell response to MSP-1 of Plasmodium falciparum in malaria-nonexposed individuals. Int. Arch. Allergy Immunol. 114: 15-22.
8. Rzepczyk, C. M., R. Ramasamy, D. A. Mutch, P. C. Ho, D. Battistutta, K. L. Anderson, D. Parkinson, T. J. Doran, and M. Honeyman. 1989. Analysis of human T cell response to two Plasmodium falciparum merozoite surface antigens. Eur. J. Immunol. 19: 1797-1802.
9. Zevering, Y., F. Amante, A. Smillie, J. Currier, G. Smith, R. A. Houghten, and M. F. Good. 1992. High frequency of malaria-specific T cells in non-exposed humans. Eur. J. Immunol. 22: 689-696.
10. Ballet, J. J., P. Druilhe, M. A. Querleux, C. Schmitt, and M. Agrapart. 1981. Parasite-derived mitogenic activity for human T cells in Plasmodium falciparum continuous cultures. Infect. Immun. 33: 758-762.
11. Greenwood, B. M., A. J. Oduloju, and T. A. Platts-Mills. 1979. Partial characterization of a malaria mitogen. Trans. R Soc. Trop. Med. Hyg. 73: 178-182.
12. Gabrielsen, A. A., Jr., and J. B. Jensen. 1982. Mitogenic activity of extracts from continuous cultures of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 31: 441-448.
13. Strickland, G. T. 1978. Lymphocyte mitogenic factor in sera from patients with falciparum malaria. Tropenmed. Parasitol. 29: 198-203.
14. Wyler, D. J., H. G. Herrod, and F. I. Weinbaum. 1979. Response of sensitized and unsensitized human lymphocyte subpopulations to Plasmodium falciparum antigens. Infect. Immun. 24: 106-110.
15. Chizzolini, C., and L. Perrin. 1986. Antigen-specific and MHC-restricted Plasmodium falciparum-induced human T lymphocyte clones. J. Immunol. 137: 1022-1028.
16. + malaria-specific responses from non-exposed donors. Int. Immunol. 4: 985-994.
17. Fern, J., and M. F. Good. 1992. Promiscuous malaria peptide epitope stimulates CD45Ra T cells from peripheral blood of nonexposed donors. J. Immunol. 148: 907-913.
18. Good, M. F., and J. Currier. 1992. The importance of T cell homing and the spleen in reaching a balance between malaria immunity and immunopathology: the moulding of immunity by early exposure to cross-reactive organisms. Immunol. Cell Biol. 70: 405-410.
19. Good, M. F., Y. Zevering, J. Currier, and J. Bilsborough. 1993. 'Original antigenic sin', T cell memory, and malaria sporozoite immunity: an hypothesis for immune evasion. Parasite Immunol. 15: 187-193.
20. Allsopp, C. E., L. A. Sanni, L. Reubsaet, F. Ndungu, C. Newbold, T. Mwangi, K. Marsh, and J. Langhome. 2002. CD4 T cell responses to a variant antigen of the malaria parasite Plasmodium falciparum, erythrocyte membrane protein-1, in individuals living in malaria-endemic areas. J. Infect. Dis. 185: 812-819.
21. Baruch, D. I., X. C. Ma, B. Pasloske, R. J. Howard, and L. H. Miller. 1999. CD36 peptides that block cytoadherence define the CD36 binding region for Plasmodium falciparum-infected erythrocytes. Blood 94: 2121-2127.
22. Newbold, C., A. Craig, S. Kyes, A. Rowe, D. Fernandez-Reyes, and T. Fagan. 1999. Cytoadherence, pathogenesis and the infected red cell surface in Plasmodium falciparum. Int. J. Parasitol. 29: 927-937.
23. Baruch, D. I. 1999. Adhesive receptors on malaria-parasitized red cells. Baillieres Best Pract. Res. Clin. Haematol 12: 747-761.
24. Baruch, D. I., X. C. Ma, H. B. Singh, X. Bi, B. L. Pasloske, and R. J. Howard. 1997. Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood 90: 3766-3775.
25. Baruch, D. I., B. Gamain, J. W. Barnwell, J. S. Sullivan, A. Stowers, G. G. Galland, L. H. Miller, and W. E. Collins. 2002. Immunization of Aotus monkeys with a functional domain of the Plasmodium falciparum variant antigen induces protection against a lethal parasite line. Proc. Natl. Acad. Sci. USA 99: 3860-3865.
26. + T cells: activation with high-dose IL-2 renders naive T cells responsive to IL-12 and/or IL-18 in the absence of TCR ligation. Eur. J. Immunol. 33: 1788-1798.
27. + T cells: evidence for two distinct pathways for promoter activation. Eur. J. Immunol. 29: 548-555.
28. Yang, J., H. Zhu, T. L. Murphy, W. Ouyang, and K. M. Murphy. 2001. IL-18-stimulated GADD45 β required in cytokine-induced, but not TCR-induced, IFN-γ production. Nat. Immunol. 2: 157-164.
29. Urban, B. C., N. Willcox, and D. J. Roberts. 2001. A role for CD36 in the regulation of dendritic cell function. Proc. Natl. Acad. Sci. USA 98: 8750-8755.
30. Mbogo, C. N., R. W. Snow, C. P. Khamala, E. W. Kabiru, J. H. Ouma, J. I. Githure, K. Marsh, and J. C. Beier. 1995. Relationships between Plasmodium falciparum transmission by vector populations and the incidence of severe disease at nine sites on the Kenyan coast. Am. J. Trop. Med. Hyg. 52: 201-206.
31. Matthews, J. B., A. A. Besong, T. R. Green, M. H. Stone, B. M. Wroblewski, J. Fisher, and E. Ingham. 2000. Evaluation of the response of primary human peripheral blood mononuclear phagocytes to challenge with in vitro generated clinically relevant UHMWPE particles of known size and dose. J. Biomed. Mater. Res. 52: 296-307.
32. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193: 673-675.
33. Parish, C. R. 1999. Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol. Cell Biol. 77: 499-508.
34. Allsopp, C. E., S. J. Nicholls, and J. Langhome. 1998. A flow cytometric method to assess antigen-specific proliferative responses of different subpopulations of fresh and cryopreserved human peripheral blood mononuclear cells. J. Immunol. Methods 214: 175-186.
35. Dzionek, A., A. Fuchs, P. Schmidt, S. Cremer, M. Zysk, S. Miltenyi, D. W. Buck, and J. Schmitz. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165: 6037-6046.
36. Dzionek, A., Y. Sohma, J. Nagafune, M. Cella, M. Colonna, F. Facchetti, G. Gunther, I. Johnston, A. Lanzavecchia, T. Nagasaka, et al. 2001. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon α/β induction. J. Exp. Med. 194: 1823-1834.
37. Ndungu, F. M., B. C. Urban, K. Marsh, and J. Langhome. 2005. Regulation of immune response by Plasmodium-infected red blood cells. Parasite Immunol. 27: 373-384.
38. Seder, R. A., R. N. Germain, P. S. Linsley, and W. E. Paul. 1994. CD28-mediated costimulation of interleukin 2 (IL-2) production plays a critical role in T cell priming for IL-4 and interferon γ production. J. Exp. Med. 179: 299-304.
39. Muller-Alouf, H., C. Carnoy, M. Simonet, and J. E. Alouf. 2001. Superantigen bacterial toxins: state of the art. Toxicon 39: 1691-1701.
40. Shoukry, N. H., P. M. Lavoie, J. Thibodeau, S. D'Souza, and R. P. Sekaly. 1997. MHC class II-dependent peptide antigen versus superantigen presentation to T cells. Hum. Immunol. 54: 194-201.
41. Urban, B. C., D. J. Ferguson, A. Pain, N. Willcox, M. Plebanski, J. M. Austyn, and D. J. Roberts. 1999. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400: 73-77.
42. 42: Baruch, D. I., B. Gamain, and L. H. Miller. 2003. DNA Immunization with the cysteine-rich interdomain region 1 of the Plasmodium falciparum variant antigen elicits limited cross-reactive antibody responses. Infect. Immun. 71: 4536-4543.
43. Gratepanche, S., B. Gamain, J. D. Smith, B. A. Robinson, A. Saul, and L. H. Miller. 2003. Induction of crossreactive antibodies against the Plasmodium falciparum variant protein. Proc. Natl. Acad. Sci. USA 100: 13007-13012.