Type I interferons suppress CD4 + T-cell-dependent parasite control during blood-stage Plasmodium infection

European Journal of Immunology

Volumn 41, Issue 9, 2011, Pages 2688-2698

  Haque, Ashraful ^a   Best, Shannon E ^a   Ammerdorffer, Anne ^a   Desbarrieres, Laure ^a   de Oca, Marcela Montes ^a   Amante, Fiona H ^a   de Labastida Rivera, Fabian ^a   Hertzog, Paul ^b   Boyle, Glen M ^a   Hill, Geoffrey R ^a   Engwerda, Christian R ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Cytokines; Immune regulation; Interferons; Malaria; T helper cells

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERFERON; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TYPE; CELLULAR IMMUNITY; CHIMERA; CONTROLLED STUDY; ERYTHROCYTE; FATALITY; FEMALE; HEMATOPOIETIC CELL; IMMUNE RESPONSE; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PARASITE CONTROL; PARASITEMIA; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPLEEN; SYMPTOM; TH1 CELL;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; IMMUNE EVASION; IMMUNOSUPPRESSION; INTERFERON TYPE I; INTERFERON-GAMMA; LIFE CYCLE STAGES; MALARIA; MICE; MICE, INBRED C57BL; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TH1 CELLS; TRANSPLANTATION CHIMERA; VIRULENCE;

EID: 80052174883     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141539     Document Type: Article

References (53)

1. WHO, Guidelines for the treatment of malaria. Second edition 2010.
2. Dondorp, A. M., Desakorn, V., Pongtavornpinyo, W., Sahassananda, D., Silamut, K., Chotivanich, K., Newton, P. N. et al., Estimation of the total parasite biomass in acute falciparum malaria from plasma PfHRP2. PLoS Med. 2005. 2: e204.
3. Bousema, J. T., Gouagna, L. C., Drakeley, C. J., Meutstege, A. M., Okech, B. A., Akim, I. N., Beier, J. C., Githure, J. I. and Sauerwein, R. W., Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malar. J. 2004. 3: 18.
4. Males, S., Gaye, O. and Garcia, A., Long-term asymptomatic carriage of Plasmodium falciparum protects from malaria attacks: a prospective study among Senegalese children. Clin. Infect. Dis. 2008. 46: 516-522.
5. Good, M. F., Kaslow, D. C. and Miller, L. H., Pathways and strategies for developing a malaria blood-stage vaccine. Annu. Rev. Immunol. 1998. 16: 57-87.
6. Freitas do Rosario, A. P., Muxel, S. M., Rodriguez-Malaga, S. M., Sardinha, L. R., Zago, C. A., Castillo-Mendez, S. I., Alvarez, J. M. and D'Imperio Lima, M. R., Gradual decline in malaria-specific memory T cell responses leads to failure to maintain long-term protective immunity to Plasmodium chabaudi AS despite persistence of B cell memory and circulating antibody. J. Immunol. 2008. 181: 8344-8355.
7. Hargreaves, J., Yoeli, M. and Nussenzweig, R. S., Immunological studies in rodent malaria. I: Protective immunity induced in mice by mild strains of Plasmodium berghei yoelii against a virulent and fatal line of this plasmodium. Ann. Trop. Med. Parasitol. 1975. 69: 289-299.
8. Weinbaum, F. I., Evans, C. B. and Tigelaar, R. E., Immunity to Plasmodium berghei yoelii in mice. I. The course of infection in T cell and B cell deficient mice. J. Immunol. 1976. 117: 1999-2005.
9. Suss, G., Eichmann, K., Kury, E., Linke, A. and Langhorne, J., Roles of CD4- and CD8-bearing T lymphocytes in the immune response to the erythrocytic stages of Plasmodium chabaudi. Infect. Immun. 1988. 56: 3081-3088.
10. Russell, E. S., Neufield, E. F. and Higgins, C. T., Comparison of normal blood picture of young adults from 18 inbred strains of mice. Proc. Soc. Exp. Biol. Med. 1951. 78: 761-766.
11. Meding, S. J., Cheng, S. C., Simon-Haarhaus, B. and Langhorne, J., Role of gamma interferon during infection with Plasmodium chabaudi chabaudi. Infect. Immun. 1990. 58: 3671-3678.
12. Podoba, J. E. and Stevenson, M. M., CD4+and CD8+T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infect. Immun. 1991. 59: 51-58.
13. Taylor-Robinson, A. W., Phillips, R. S., Severn, A., Moncada, S. and Liew, F. Y., The role of TH1 and TH2 cells in a rodent malaria infection. Science 1993. 260: 1931-1934.
14. Langhorne, J., Meding, S. J., Eichmann, K. and Gillard, S. S., The response of CD4+T cells to Plasmodium chabaudi chabaudi. Immunol. Rev. 1989. 112: 71-94.
15. Meding, S. J. and Langhorne, J., CD4+T cells and B cells are necessary for the transfer of protective immunity to Plasmodium chabaudi chabaudi. Eur. J. Immunol. 1991. 21: 1433-1438.
16. Xu, H., Hodder, A. N., Yan, H., Crewther, P. E., Anders, R. F. and Good, M. F., CD4+T cells acting independently of antibody contribute to protective immunity to Plasmodium chabaudi infection after apical membrane antigen 1 immunization. J. Immunol. 2000. 165: 389-396.
17. Good, M. F., Xu, H., Wykes, M. and Engwerda, C. R., Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 2005. 23: 69-99.
18. Renia, L., Potter, S. M., Mauduit, M., Rosa, D. S., Kayibanda, M., Deschemin, J. C., Snounou, G. and Gruner, A. C., Pathogenic T cells in cerebral malaria. Int. J. Parasitol. 2006. 36: 547-554.
19. Potter, S., Chan-Ling, T., Ball, H. J., Mansour, H., Mitchell, A., Maluish, L. and Hunt, N. H., Perforin mediated apoptosis of cerebral microvascular endothelial cells during experimental cerebral malaria. Int. J. Parasitol. 2006. 36: 485-496.
20. Nitcheu, J., Bonduelle, O., Combadiere, C., Tefit, M., Seilhean, D., Mazier, D. and Combadiere, B., Perforin-dependent brain-infiltrating cytotoxic CD8+T lymphocytes mediate experimental cerebral malaria pathogenesis. J. Immunol. 2003. 170: 2221-2228.
21. Belnoue, E., Kayibanda, M., Vigario, A. M., Deschemin, J. C., van Rooijen, N., Viguier, M., Snounou, G. and Renia, L., On the pathogenic role of brain-sequestered alphabeta CD8+T cells in experimental cerebral malaria. J. Immunol. 2002. 169: 6369-6375.
22. Hermsen, C., van de Wiel, T., Mommers, E., Sauerwein, R. and Eling, W., Depletion of CD4+or CD8+T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology 1997. 114: 7-12.
23. Haque, A., Best, S. E., Unosson, K., Amante, F. H., de Labastida, F., Anstey, N. M., Karupiah, G., et al., Granzyme B expression by CD8+T cells is required for the development of experimental cerebral malaria. J. Immunol. 2011. 186: 6148-6156.
24. Amante, F. H., Haque, A., Stanley, A. C., Rivera Fde, L., Randall, L. M., Wilson, Y. A., Yeo, G. et al., Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J. Immunol. 2010. 185: 3632-3642.
25. Yanez, D. M., Manning, D. D., Cooley, A. J., Weidanz, W. P. and van der Heyde, H. C., Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 1996. 157: 1620-1624.
26. Baptista, F. G., Pamplona, A., Pena, A. C., Mota, M. M., Pied, S. and Vigario, A. M., Accumulation of Plasmodium berghei-infected red blood cells in the brain is crucial for the development of cerebral malaria in mice. Infect Immun. 2010. 78: 4033-4039.
27. Haque, A., Best, S. E., Amante, F. H., Ammerdorffer, A., de Labastida, F., Pereira, T., Ramm, G. A. and Enwgerda, C. R., High parasite burdens cause liver damage in mice following Plasmodium berghei ANKA infection, independent of CD8+T cell-mediated immune pathology. Infect. Immun. 2011. 79: 1882-1888.
28. Lundie, R. J., de Koning-Ward, T. F., Davey, G. M., Nie, C. Q., Hansen, D. S., Lau, L. S., Mintern, J. D. et al., Blood-stage Plasmodium infection induces CD8+T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+dendritic cells. Proc. Natl. Acad. Sci. USA 2008. 105: 14509-14514.
29. Haque, A., Best, S. E., Amante, F. H., Mustafah, S., Desbarrieres, L., de Labastida, F., Sparwasser, T., et al., CD4+natural regulatory T cells prevent experimental cerebral malaria via CTLA-4 when expanded in vivo. PLoS Pathog. 2010. 6: e1001221.
30. Grau, G. E., Heremans, H., Piguet, P. F., Pointaire, P., Lambert, P. H., Billiau, A. and Vassalli, P., Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc Natl. Acad. Sci. USA 1989. 86: 5572-5574.
31. deWalick, S., Amante, F. H., McSweeney, K. A., Randall, L. M., Stanley, A. C., Haque, A., Kuns, R. D. et al., Cutting edge: conventional dendritic cells are the critical APC required for the induction of experimental cerebral malaria. J. Immunol. 2007. 178: 6033-6037.
32. Voisine, C., Mastelic, B., Sponaas, A. M. and Langhorne, J., Classical CD11c+dendritic cells, not plasmacytoid dendritic cells, induce T cell responses to Plasmodium chabaudi malaria. Int. J. Parasitol. 2010. 40: 711-719.
33. Longhi, M. P., Trumpfheller, C., Idoyaga, J., Caskey, M., Matos, I., Kluger, C., Salazar, A. M. et al., Dendritic cells require a systemic type I interferon response to mature and induce CD4+Th1 immunity with poly IC as adjuvant. J. Exp. Med. 2009. 206: 1589-1602.
34. Kohlmeier, J. E., Cookenham, T., Roberts, A. D., Miller, S. C. and Woodland, D. L., Type I interferons regulate cytolytic activity of memory CD8(+) T cells in the lung airways during respiratory virus challenge. Immunity 2010. 33: 96-105.
35. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A., Oni, T., Wilkinson, K. A. et al., An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010. 466: 973-977.
36. Isaacs, A. and Lindenmann, J., Virus interference. I. The interferon. Proc. R Soc. Lond. B Biol. Sci. 1957. 147: 258-267.
37. Isaacs, A., Lindenmann, J. and Valentine, R. C., Virus interference. II. Some properties of interferon. Proc. R Soc. Lond. B Biol. Sci. 1957. 147: 268-273.
38. Xin, L., Vargas-Inchaustegui, D. A., Raimer, S. S., Kelly, B. C., Hu, J., Zhu, L., Sun, J. and Soong, L., Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites. J. Immunol. 2010. 184: 7047-7056.
39. Martin, D. L., Murali-Krishna, K. and Tarleton, R. L., Generation of Trypanosoma cruzi-specific CD8+T-cell immunity is unaffected by the absence of type I interferon signaling. Infect. Immun. 2010. 78: 3154-3159.
40. Buxbaum, L. U., Type I IFNs promote the early IFN-gamma response and the IL-10 response in Leishmania mexicana infection. Parasite Immunol. 2010. 32: 153-160.
41. Huang, K. Y., Schultz, W. W. and Gordon, F. B., Interferon induced by Plasmodium berghei. Science 1968. 162: 123-124.
42. Jahiel, R. I., Vilcek, J., Nussenzweig, R. and Vanderberg, J., Interferon inducers protect mice against plasmodium berghei malaria. Science 1968. 161: 802-804.
43. Vigario, A. M., Belnoue, E., Gruner, A. C., Mauduit, M., Kayibanda, M., Deschemin, J. C., Marussig, M. et al., Recombinant human IFN-alpha inhibits cerebral malaria and reduces parasite burden in mice. J. Immunol. 2007. 178: 6416-6425.
44. Engwerda, C., Belnoue, E., Gruner, A. C. and Renia, L., Experimental models of cerebral malaria. Curr. Top. Microbiol. Immunol. 2005. 297: 103-143.
45. Kwiatkowski, D., Genetic dissection of the molecular pathogenesis of severe infection. Intensive Care Med. 2000. 26: S89-S97.
46. Bennett, S. R., Carbone, F. R., Karamalis, F., Miller, J. F. and Heath, W. R., Induction of a CD8+cytotoxic T lymphocyte response by cross-priming requires cognate CD4+T cell help. J. Exp. Med. 1997. 186: 65-70.
47. Cardin, R. D., Brooks, J. W., Sarawar, S. R. and Doherty, P. C., Progressive loss of CD8+T cell-mediated control of a gamma-herpesvirus in the absence of CD4+T cells. J. Exp. Med. 1996. 184: 863-871.
48. Keene, J. A. and Forman, J., Helper activity is required for the in vivo generation of cytotoxic T lymphocytes. J. Exp. Med. 1982. 155: 768-782.
49. von Herrath, M. G., Yokoyama, M., Dockter, J., Oldstone, M. B. and Whitton, J. L., CD4-deficient mice have reduced levels of memory cytotoxic T lymphocytes after immunization and show diminished resistance to subsequent virus challenge. J. Virol. 1996. 70: 1072-1079.
50. Hwang, S. Y., Hertzog, P. J., Holland, K. A., Sumarsono, S. H., Tymms, M. J., Hamilton, J. A., Whitty, G. et al., A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beta and alters macrophage responses. Proc. Natl. Acad. Sci. USA 1995. 92: 11284-11288.
51. Swann, J. B., Hayakawa, Y., Zerafa, N., Sheehan, K. C., Scott, B., Schreiber, R. D., Hertzog, P. and Smyth, M. J., Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J. Immunol. 2007. 178: 7540-7549.
52. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J. and Carbone, F. R., T cell receptor antagonist peptides induce positive selection. Cell 1994. 76: 17-27.
53. Amante, F. H., Stanley, A. C., Randall, L. M., Zhou, Y., Haque, A., McSweeney, K., Waters, A. P., et al., A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria. Am. J. Pathol. 2007. 171: 548-559.