IFN-γ-producing CD4+ T cells promote experimental cerebral malaria by modulating CD8+ T cell accumulation within the brain

Journal of Immunology

Volumn 189, Issue 2, 2012, Pages 968-979

  Villegas Mendez, Ana ^a,d   Greig, Rachel ^a,e   Shaw, Tovah N ^a,d   De Souza, J Brian ^a,b   Findlay, Emily Gwyer ^a,f   Stumhofer, Jason S ^c,g   Hafalla, Julius C R ^a   Blount, Daniel G ^a,h   Hunter, Christopher A ^c   Riley, Eleanor M ^a   Couper, Kevin N ^a,d  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e Breakthrough Breast Cancer   (United Kingdom)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^h OXFORD BIOMEDICA UK LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN MALARIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; EXPERIMENTAL INFECTION; FEMALE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPHOCYTE MIGRATION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; T CELL DEPLETION; TISSUE DISTRIBUTION;

ADOPTIVE TRANSFER; ANIMALS; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, INNATE; INTERFERON-GAMMA; MALARIA, CEREBRAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMODIUM BERGHEI;

EID: 84863621019     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200688     Document Type: Article

References (52)

1. de Souza, J. B., J. C. Hafalla, E. M. Riley, and K. N. Couper. 2010. Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease. Parasitology 137: 755-772.
2. Riley, E. M., K. N. Couper, H. Helmby, J. C. Hafalla, J. B. de Souza, J. Langhorne, W. B. Jarra, and F. Zavala. 2010. Neuropathogenesis of human and murine malaria. Trends Parasitol. 26: 277-278.
3. Good, M. F., H. Xu, M. Wykes, and C. R. Engwerda. 2005. Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 23: 69-99. (Pubitemid 40563165)
4. Dai, M., S. E. Reznik, D. C. Spray, L. M. Weiss, H. B. Tanowitz, M. Gulinello, and M. S. Desruisseaux. 2010. Persistent cognitive and motor deficits after successful antimalarial treatment in murine cerebral malaria. Microbes Infect. 12: 1198-1207.
5. Reis, P. A., C. M. Comim, F. Hermani, B. Silva, T. Barichello, A. C. Portella, F. C. Gomes, I. M. Sab, V. S. Frutuoso, M. F. Oliveira, et al. 2010. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog. 6: e1000963.
6. Amani, V., A. M. Vigário, E. Belnoue, M. Marussig, L. Fonseca, D. Mazier, and L. Rénia. 2000. Involvement of IFN-γ receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 30: 1646-1655. (Pubitemid 30342807)
7. Belnoue, E., S. M. Potter, D. S. Rosa, M. Mauduit, A. C. Grüner, M. Kayibanda, A. J. Mitchell, N. H. Hunt, and L. Rénia. 2008. Control of pathogenic CD8+ T cell migration to the brain by IFN-γamma during experimental cerebral malaria. Parasite Immunol. 30: 544-553.
8. Miu, J., N. H. Hunt, and H. J. Ball. 2008. Predominance of interferon-related responses in the brain during murine malaria, as identified by microarray analysis. Infect. Immun. 76: 1812-1824. (Pubitemid 351656115)
9. Lovegrove, F. E., S. A. Gharib, S. N. Patel, C. A. Hawkes, K. C. Kain, and W. C. Liles. 2007. Expression microarray analysis implicates apoptosis and interferon-responsive mechanisms in susceptibility to experimental cerebral malaria. Am. J. Pathol. 171: 1894-1903.
10. Van den Steen, P. E., K. Deroost, I. Van Aelst, N. Geurts, E. Martens, S. Struyf, C. Q. Nie, D. S. Hansen, P. Matthys, J. Van Damme, and G. Opdenakker. 2008. CXCR3 determines strain susceptibility to murine cerebral malaria by mediating T lymphocyte migration toward IFN-γamma-induced chemokines. Eur. J. Immunol. 38: 1082-1095.
11. Miu, J., A. J. Mitchell, M. Müller, S. L. Carter, P. M. Manders, J. A. McQuillan, B. M. Saunders, H. J. Ball, B. Lu, I. L. Campbell, and N. H. Hunt. 2008. Chemokine gene expression during fatal murine cerebral malaria and protection due to CXCR3 deficiency. J. Immunol. 180: 1217-1230.
12. Campanella, G. S., A. M. Tager, J. K. El Khoury, S. Y. Thomas, T. A. Abrazinski, L. A. Manice, R. A. Colvin, and A. D. Luster. 2008. Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proc. Natl. Acad. Sci. USA 105: 4814-4819. (Pubitemid 351753829)
13. Nie, C. Q., N. J. Bernard, M. U. Norman, F. H. Amante, R. J. Lundie, B. S. Crabb, W. R. Heath, C. R. Engwerda, M. J. Hickey, L. Schofield, and D. S. Hansen. 2009. IP-10-mediated T cell homing promotes cerebral inflammation over splenic immunity to malaria infection. PLoS Pathog. 5:e1000369.
14. Belnoue, E., M. Kayibanda, A. M. Vigario, J. C. Deschemin, N. van Rooijen, M. Viguier, G. Snounou, and L. Rénia. 2002. On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J. Immunol. 169: 6369-6375. (Pubitemid 36903485)
15. Claser, C., B. Malleret, S. Y. Gun, A. Y. Wong, Z. W. Chang, P. Teo, P. C. See, S. W. Howland, F. Ginhoux, and L. Rénia. 2011. CD8+ T cells and IFN-γmediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS ONE 6: e18720.
16. Amante, F. H., A. Haque, A. C. Stanley, Fde. L. Rivera, L. M. Randall, Y. A. Wilson, G. Yeo, C. Pieper, B. S. Crabb, T. F. de Koning-Ward, et al. 2010. Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J. Immunol. 185: 3632-3642.
17. McCall, M. B., and R. W. Sauerwein. 2010. Interferon-γ-central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J. Leukoc. Biol. 88: 1131-1143.
18. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75: 163-189. (Pubitemid 38174573)
19. Horowitz, A., K. C. Newman, J. H. Evans, D. S. Korbel, D. M. Davis, and E. M. Riley. 2010. Cross-talk between T cells and NK cells generates rapid effector responses to Plasmodium falciparum-infected erythrocytes. J. Immunol. 184: 6043-6052.
20. Perry, J. A., C. S. Olver, R. C. Burnett, and A. C. Avery. 2005. Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation. J. Immunol. 174: 5921-5925. (Pubitemid 40663776)
21. Sponaas, A. M., E. T. Cadman, C. Voisine, V. Harrison, A. Boonstra, A. O'Garra, and J. Langhorne. 2006. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J. Exp. Med. 203: 1427-1433. (Pubitemid 43877605)
22. Mitchell, A. J., A. M. Hansen, L. Hee, H. J. Ball, S. M. Potter, J. C. Walker, and N. H. Hunt. 2005. Early cytokine production is associated with protection from murine cerebral malaria. Infect. Immun. 73: 5645-5653. (Pubitemid 41193000)
23. O'Connor, R. A., C. T. Prendergast, C. A. Sabatos, C. W. Lau, M. D. Leech, D. C. Wraith, and S. M. Anderton. 2008. Cutting edge: Th1 cells facilitate the entry of Th17 cells to the central nervous system during experimental autoimmune encephalomyelitis. J. Immunol. 181: 3750-3754.
24. Veldhoen, M., R. J. Hocking, R. A. Flavell, and B. Stockinger. 2006. Signals mediated by transforming growth factor-beta initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat. Immunol. 7:1151-1156. (Pubitemid 44594310)
25. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
26. Siffrin, V., H. Radbruch, R. Glumm, R. Niesner, M. Paterka, J. Herz, T. Leuenberger, S. M. Lehmann, S. Luenstedt, J. L. Rinnenthal, et al. 2010. In vivo imaging of partially reversible th17 cell-induced neuronal dysfunction in the course of encephalomyelitis. Immunity 33: 424-436.
27. Kebir, H., K. Kreymborg, I. Ifergan, A. Dodelet-Devillers, R. Cayrol, M. Bernard, F. Giuliani, N. Arbour, B. Becher, and A. Prat. 2007. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13: 1173-1175. (Pubitemid 47530640)
28. Das Sarma, J., B. Ciric, R. Marek, S. Sadhukhan, M. L. Caruso, J. Shafagh, D. C. Fitzgerald, K. S. Shindler, and A. Rostami. 2009. Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. J. Neuroinflammation 6: 14.
29. Ma, X., S. L. Reynolds, B. J. Baker, X. Li, E. N. Benveniste, and H. Qin. 2010. IL-17 enhancement of the IL-6 signaling cascade in astrocytes. J. Immunol. 184:4898-4906.
30. Stetson, D. B., M. Mohrs, R. L. Reinhardt, J. L. Baron, Z. E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198: 1069-1076. (Pubitemid 37248622)
31. Villegas-Mendez, A., J. B. de Souza, L. Murungi, J. C. Hafalla, T. N. Shaw, R. Greig, E. M. Riley, and K. N. Couper. 2011. Heterogeneous and tissuespecific regulation of effector T cell responses by IFN-γamma during Plasmodium berghei ANKA infection. J. Immunol. 187: 2885-2897.
32. Grau, G. E., H. Heremans, P. F. Piguet, P. Pointaire, P. H. Lambert, A. Billiau, and P. Vassalli. 1989. Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc. Natl. Acad. Sci. USA 86: 5572-5574. (Pubitemid 19185586)
33. Kwok, L. Y., H. Miletic, S. Lütjen, S. Soltek, M. Deckert, and D. Schlüter. 2002. Protective immunosurveillance of the central nervous system by Listeria-specific CD4 and CD8 T cells in systemic listeriosis in the absence of intracerebral Listeria. J. Immunol. 169: 2010-2019. (Pubitemid 34857665)
34. Wilson, E. H., W. Weninger, and C. A. Hunter. 2010. Trafficking of immune cells in the central nervous system. J. Clin. Invest. 120: 1368-1379.
35. Mayer, K. D., K. Mohrs, S. R. Crowe, L. L. Johnson, P. Rhyne, D. L. Woodland, and M. Mohrs. 2005. The functional heterogeneity of type 1 effector T cells in response to infection is related to the potential for IFN-γ production. J. Immunol. 174: 7732-7739. (Pubitemid 40806279)
36. Grau, G. E., L. F. Fajardo, P. F. Piguet, B. Allet, P. H. Lambert, and P. Vassalli. 1987. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237: 1210-1212. (Pubitemid 17124914)
37. Engwerda, C. R., T. L. Mynott, S. Sawhney, J. B. De Souza, Q. D. Bickle, and P. M. Kaye. 2002. Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J. Exp. Med. 195: 1371-1377. (Pubitemid 34564338)
38. Franke-Fayard, B., J. Fonager, A. Braks, S. M. Khan, and C. J. Janse. 2010. Sequestration and tissue accumulation of human malaria parasites: can we learn anything from rodent models of malaria? PLoS Pathog. 6: e1001032.
39. Toy, D., D. Kugler, M. Wolfson, T. Vanden Bos, J. Gurgel, J. Derry, J. Tocker, and J. Peschon. 2006. Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J. Immunol. 177: 36-39. (Pubitemid 43939112)
40. Sarkar, S., L. A. Cooney, and D. A. Fox. 2010. The role of T helper type 17 cells in inflammatory arthritis. Clin. Exp. Immunol. 159: 225-237.
41. Ishida, H., C. Matsuzaki-Moriya, T. Imai, K. Yanagisawa, Y. Nojima, K. Suzue, M. Hirai, Y. Iwakura, A. Yoshimura, S. Hamano, et al. 2010. Development of experimental cerebral malaria is independent of IL-23 and IL-17. Biochem. Biophys. Res. Commun. 402: 790-795.
42. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
43. Grau, G. E., P. F. Piguet, H. D. Engers, J. A. Louis, P. Vassalli, and P. H. Lambert. 1986. L3T4+ T lymphocytes play a major role in the pathogenesis of murine cerebral malaria. J. Immunol. 137: 2348-2354. (Pubitemid 16020735)
44. Yañez, D. M., D. D. Manning, A. J. Cooley, W. P. Weidanz, and H. C. van der Heyde. 1996. Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 157: 1620-1624. (Pubitemid 126449102)
45. Haque, A., S. E. Best, A. Ammerdorffer, L. Desbarrieres, M. M. de Oca, F. H. Amante, F. de Labastida Rivera, P. Hertzog, G. M. Boyle, G. R. Hill, and C. R. Engwerda. 2011. Type I interferons suppress CD4+ T cell-dependent parasite control during blood-stage Plasmodium infection. Eur. J. Immunol. 41: 2688-2698.
46. Hirunpetcharat, C., and M. F. Good. 1998. Deletion of Plasmodium bergheispecific CD4+ T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc. Natl. Acad. Sci. USA 95: 1715-1720. (Pubitemid 28103459)
47. Haque, A., S. E. Best, K. Unosson, F. H. Amante, F. de Labastida, N. M. Anstey, G. Karupiah, M. J. Smyth, W. R. Heath, and C. R. Engwerda. 2011. Granzyme B expression by CD8+ T cells is required for the development of experimental cerebral malaria. J. Immunol. 186: 6148-6156.
48. Potter, S., T. Chan-Ling, H. J. Ball, H. Mansour, A. Mitchell, L. Maluish, and N. H. Hunt. 2006. Perforin mediated apoptosis of cerebral microvascular endothelial cells during experimental cerebral malaria. Int. J. Parasitol. 36: 485-496. (Pubitemid 43728781)
49. Nitcheu, J., O. Bonduelle, C. Combadiere, M. Tefit, D. Seilhean, D. Mazier, and B. Combadiere. 2003. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J. Immunol. 170: 2221-2228. (Pubitemid 36197447)
50. McQuillan, J. A., A. J. Mitchell, Y. F. Ho, V. Combes, H. J. Ball, J. Golenser, G. E. Grau, and N. H. Hunt. 2011. Coincident parasite and CD8 T cell sequestration is required for development of experimental cerebral malaria. Int. J. Parasitol. 41: 155-163.
51. Baptista, F. G., A. Pamplona, A. C. Pena, M. M. Mota, S. Pied, and A. M. Vigário. 2010. Accumulation of Plasmodium berghei-infected red blood cells in the brain is crucial for the development of cerebral malaria in mice. Infect. Immun. 78: 4033-4039.
52. Haldar, K., S. C. Murphy, D. A. Milner, and T. E. Taylor. 2007. Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu. Rev. Pathol. 2: 217-249. (Pubitemid 46448065)