Granzyme B expression by CD8+ T cells is required for the development of experimental cerebral malaria

Journal of Immunology

Volumn 186, Issue 11, 2011, Pages 6148-6156

  Haque, Ashraful ^a   Best, Shannon E ^a   Unosson, Klara ^a   Amante, Fiona H ^a   De Labastida, Fabian ^a   Anstey, Nicholas M ^b   Karupiah, Gunasegaran ^c   Smyth, Mark J ^d   Heath, William R ^e   Engwerda, Christian R ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^c Biology and Environment   (Australia)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GAMMA INTERFERON; GRANZYME B; PERFORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MALARIA; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PATHOGENESIS; PLASMODIUM CHABAUDI; PLASMODIUM YOELII; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ADOPTIVE TRANSFER; ANIMALS; BRAIN; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; FEMALE; FLOW CYTOMETRY; GRANZYMES; HOST-PARASITE INTERACTIONS; INTERFERON-GAMMA; MALARIA, CEREBRAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERFORIN; PLASMODIUM CHABAUDI; PLASMODIUM YOELII;

EID: 79958031319     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003955     Document Type: Article

References (69)

1. World Health Organization. 2009. WHO Global Malaria Programme: World Malaria Report 2009. WHO Press, Geneva, Switzerland.
2. Dondorp, A. M., V. Desakorn, W. Pongtavornpinyo, D. Sahassananda, K. Silamut, K. Chotivanich, P. N.Newton, P. Pitisuttithum, A. M. Smithyman,N. J. White, and N. P. Day. 2005. Estimation of the total parasite biomass in acute falciparum malaria from plasma PfHRP2. PLoS Med. 2: e204.
3. Yeo, T. W., D. A. Lampah, R. Gitawati, E. Tjitra, E. Kenangalem, K. Piera, R. N. Price, S. B. Duffull, D. S. Celermajer, and N. M. Anstey. 2008. Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proc. Natl. Acad. Sci. USA 105: 17097-17102.
4. 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.
5. Taylor, T. E., W. J. Fu, R. A. Carr, R. O. Whitten, J. S. Mueller, N. G. Fosiko, S. Lewallen, N. G. Liomba, and M. E. Molyneux. 2004. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. [Published erratum appears in 2004 Nat. Med. 10: 435.] Nat. Med. 10: 143-145. (Pubitemid 38524882)
6. Pongponratn, E., G. D. Turner, N. P. Day, N. H. Phu, J. A. Simpson, K. Stepniewska, N. T. Mai, P. Viriyavejakul, S. Looareesuwan, T. T. Hien, et al. 2003. An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 69: 345-359.
7. Dondorp, A., F. Nosten, K. Stepniewska, N. Day, N. White; South East Asian Quinine Artesunate Malaria Trial (SEAQUAMAT) group. 2005. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet 366: 717-725.
8. Prakash, D., C. Fesel, R. Jain, P. A. Cazenave, G. C. Mishra, and S. Pied. 2006. Clusters of cytokines determine malaria severity in Plasmodium falciparum-infected patients from endemic areas of Central India. J. Infect. Dis. 194: 198-207.
9. McGuire, W., J. C. Knight, A. V. Hill, C. E. Allsopp, B. M. Greenwood, and D. Kwiatkowski. 1999. Severe malarial anemia and cerebral malaria are associated with different tumor necrosis factor promoter alleles. J. Infect. Dis. 179: 287-290.
10. McGuire, W., A. V. Hill, C. E. Allsopp, B. M. Greenwood, and D. Kwiatkowski. 1994. Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria. Nature 371: 508-510.
11. Kwiatkowski, D., A. V. Hill, I. Sambou, P. Twumasi, J. Castracane, K. R. Manogue, A. Cerami, D. R. Brewster, and B. M. Greenwood. 1990. TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201-1204.
12. Knight, J. C., I. Udalova, A. V. Hill, B. M. Greenwood, N. Peshu, K. Marsh, and D. Kwiatkowski. 1999. A polymorphism that affects OCT-1 binding to the TNF promoter region is associated with severe malaria. Nat. Genet. 22: 145-150.
13. Day, N. P., T. T. Hien, T. Schollaardt, P. P. Loc, L. V. Chuong, T. T. Chau, N. T. Mai, N. H. Phu, D. X. Sinh, N. J. White, and M. Ho. 1999. The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J. Infect. Dis. 180: 1288-1297.
14. 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)
15. 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.
16. 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)
17. Hermsen, C., T. van de Wiel, E. Mommers, R. Sauerwein, and W. Eling. 1997. Depletion of CD4+ or CD8+ T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology 114: 7-12. (Pubitemid 27022698)
18. 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)
19. deWalick, S., F. H. Amante, K. A. McSweeney, L. M. Randall, A. C. Stanley, A. Haque, R. D. Kuns, K. P. MacDonald, G. R. Hill, and C. R. Engwerda. 2007. Cutting edge: conventional dendritic cells are the critical APC required for the induction of experimental cerebral malaria. J. Immunol. 178: 6033-6037.
20. Lundie, R. J., T. F. de Koning-Ward, G. M. Davey, C. Q. Nie, D. S. Hansen, L. S. Lau, J. D. Mintern, G. T. Belz, L. Schofield, F. R. Carbone, et al. 2008. Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells. Proc. Natl. Acad. Sci. USA 105: 14509-14514.
21. Randall, L. M., F. H. Amante, K. A. McSweeney, Y. Zhou, A. C. Stanley, A. Haque, M. K. Jones, G. R. Hill, G. M. Boyle, and C. R. Engwerda. 2008. Common strategies to prevent and modulate experimental cerebral malaria in mouse strains with different susceptibilities. Infect. Immun. 76: 3312-3320.
22. 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)
23. 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.
24. 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.
25. 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.
26. Pollay, M., and P. A. Roberts. 1980. Blood-brain barrier: a definition of normal and altered function. Neurosurgery 6: 675-685.
27. Engelhardt, B., M. T. Martin-Simonet, L. S. Rott, E. C. Butcher, and S. A. Michie. 1998. Adhesion molecule phenotype of T lymphocytes in inflamed CNS. J. Neuroimmunol. 84: 92-104.
28. Kang, H., O. Liesenfeld, J. S. Remington, J. Claflin, X. Wang, and Y. Suzuki. 2003. TCRV beta 8+ T cells prevent development of toxoplasmic encephalitis in BALB/c mice genetically resistant to the disease. J. Immunol. 170: 4254-4259. (Pubitemid 36428192)
29. Masson, F., T. Calzascia, W. Di Berardino-Besson, N. de Tribolet, P. Y. Dietrich, and P. R. Walker. 2007. Brain microenvironment promotes the final functional maturation of tumor-specific effector CD8+ T cells. J. Immunol. 179: 845-853.
30. Tatum, A. M., L. M. Mylin, S. J. Bender, M. A. Fischer, B. A. Vigliotti, M. J. Tevethia, S. S. Tevethia, and T. D. Schell. 2008. CD8+ T cells targeting a single immunodominant epitope are sufficient for elimination of established SV40 T antigen-induced brain tumors. J. Immunol. 181: 4406-4417.
31. Walker, P. R., T. Calzascia, V. Schnuriger, N. Scamuffa, P. Saas, N. de Tribolet, and P. Y. Dietrich. 2000. The brain parenchyma is permissive for full antitumor CTL effector function, even in the absence of CD4 T cells. J. Immunol. 165: 3128-3135.
32. Huseby, E. S., D. Liggitt, T. Brabb, B. Schnabel, C. Ohlén, and J. Goverman. 2001. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J. Exp. Med. 194: 669-676.
33. Sanchez-Ruiz, M., L. Wilden, W. Müller, W. Stenzel, A. Brunn, H. Miletic, D. Schlüter, and M. Deckert. 2008. Molecular mimicry between neurons and an intracerebral pathogen induces a CD8 T cell-mediated autoimmune disease. J. Immunol. 180: 8421-8433.
34. Schaeffer, M., S. J. Han, T. Chtanova, G. G. van Dooren, P. Herzmark, Y. Chen, B. Roysam, B. Striepen, and E. A. Robey. 2009. Dynamic imaging of T cell-parasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J. Immunol. 182: 6379-6393.
35. Wilson, E. H., T. H. Harris, P. Mrass, B. John, E. D. Tait, G. F. Wu, M. Pepper, E. J. Wherry, F. Dzierzinski, D. Roos, et al. 2009. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30: 300-311.
36. Galea, I., M. Bernardes-Silva, P. A. Forse, N. van Rooijen, R. S. Liblau, and V. H. Perry. 2007. An antigen-specific pathway for CD8 T cells across the blood-brain barrier. J. Exp. Med. 204: 2023-2030.
37. Velicu, S., Y. Han, I. Ulasov, I. E. Brown, A. El Andaloussi, T. F. Gajewski, and M. S. Lesniak. 2006. Cross-priming of T cells to intracranial tumor antigens elicits an immune response that fails in the effector phase but can be augmented with local immunotherapy. J. Neuroimmunol. 174: 74-81.
38. Heusel, J. W., R. L. Wesselschmidt, S. Shresta, J. H. Russell, and T. J. Ley. 1994. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76: 977-987.
39. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
40. Amante, F. H., A. C. Stanley, L. M. Randall, Y. Zhou, A. Haque, K. McSweeney, A. P. Waters, C. J. Janse, M. F. Good, G. R. Hill, and C. R. Engwerda. 2007. A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria. Am. J. Pathol. 171: 548-559.
41. Amani, V., A. M. Vigário, E. Belnoue, M. Marussig, L. Fonseca, D. Mazier, and L. Rénia. 2000. Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 30: 1646-1655.
42. Vignali, D. A., L. W. Collison, and C. J. Workman. 2008. How regulatory T cells work. Nat. Rev. Immunol. 8: 523-532.
43. 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.
44. Jenkins, M. R., A. Tsun, J. C. Stinchcombe, and G. M. Griffiths. 2009. The strength of T cell receptor signal controls the polarization of cytotoxic machinery to the immunological synapse. Immunity 31: 621-631.
45. Jenkins, M. R., R. Webby, P. C. Doherty, and S. J. Turner. 2006. Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J. Immunol. 177: 2917-2925.
46. McLachlan, J. B., D. M. Catron, J. J. Moon, and M. K. Jenkins. 2009. Dendritic cell antigen presentation drives simultaneous cytokine production by effector and regulatory T cells in inflamed skin. Immunity 30: 277-288.
47. Wakim, L. M., J. Waithman, N. van Rooijen, W. R. Heath, and F. R. Carbone. 2008. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319: 198-202.
48. Belnoue, E., F. T. Costa, A. M. Vigário, T. Voza, F. Gonnet, I. Landau, N. Van Rooijen, M. Mack,W. A. Kuziel, and L. Rénia. 2003. Chemokine receptor CCR2 is not essential for the development of experimental cerebral malaria. Infect. Immun. 71: 3648-3651.
49. Lou, J., Y. Gasche, L. Zheng, B. Critico, C. Monso-Hinard, P. Juillard, P. Morel, W. A. Buurman, and G. E. Grau. 1998. Differential reactivity of brain microvascular endothelial cells to TNF reflects the genetic susceptibility to cerebral malaria. Eur. J. Immunol. 28: 3989-4000.
50. Monso-Hinard, C., J. N. Lou, C. Behr, P. Juillard, and G. E. Grau. 1997. Expression of major histocompatibility complex antigens on mouse brain microvascular endothelial cells in relation to susceptibility to cerebral malaria. Immunology 92: 53-59.
51. Grossman, W. J., J. W. Verbsky, W. Barchet, M. Colonna, J. P. Atkinson, and T. J. Ley. 2004. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 21: 589-601.
52. Gondek, D. C., L. F. Lu, S. A. Quezada, S. Sakaguchi, and R. J. Noelle. 2005. Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol. 174: 1783-1786.
53. Zhao, D. M., A. M. Thornton, R. J. DiPaolo, and E. M. Shevach. 2006. Activated CD4+CD25+ T cells selectively kill B lymphocytes. Blood 107: 3925-3932.
54. Gondek, D. C., V. Devries, E. C. Nowak, L. F. Lu, K. A. Bennett, Z. A. Scott, and R. J. Noelle. 2008. Transplantation survival is maintained by granzyme B+ regulatory cells and adaptive regulatory T cells. J. Immunol. 181: 4752-4760.
55. Cao, X., S. F. Cai, T. A. Fehniger, J. Song, L. I. Collins, D. R. Piwnica-Worms, and T. J. Ley. 2007. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27: 635-646.
56. Haque, A., S. E. Best, F. H. Amante, S. Mustafah, L. Desbarrieres, F. de Labastida, T. Sparwasser, G. R. Hill, and C. R. Engwerda. 2010. CD4+ natural regulatory T cells prevent experimental cerebral malaria via CTLA-4 when expanded in vivo. PLoS Pathog. 6: e1001221.
57. Dondorp, A. M., E. Pongponratn, and N. J. White. 2004. Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Trop. 89: 309-317.
58. Binder, G. K., and D. E. Griffin. 2001. Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293: 303-306.
59. Borrow, P., P. Tonks, C. J.Welsh, and A. A. Nash. 1992. The role of CD8+T cells in the acute and chronic phases of Theiler's murine encephalomyelitis virus-induced disease in mice. J. Gen. Virol. 73: 1861-1865.
60. Subak-Sharpe, I., H. Dyson, and J. Fazakerley. 1993. In vivo depletion of CD8+ T cells prevents lesions of demyelination in Semliki Forest virus infection. J. Virol. 67: 7629-7633.
61. Brown, C. R., C. S. David, S. J. Khare, and R. McLeod. 1994. Effects of human class I transgenes on Toxoplasma gondii cyst formation. J. Immunol. 152: 4537-4541. (Pubitemid 24134411)
62. Gazzinelli, R. T., A. Brézin, Q. Li, R. B. Nussenblatt, and C. C. Chan. 1994. Toxoplasma gondii: acquired ocular toxoplasmosis in the murine model, protective role of TNF-alpha and IFN-gamma. Exp. Parasitol. 78: 217-229.
63. Bettini, M., K. Rosenthal, and B. D. Evavold. 2009. Pathogenic MOG-reactive CD8+ T cells require MOG-reactive CD4+ T cells for sustained CNS inflammation during chronic EAE. J. Neuroimmunol. 213: 60-68.
64. Mars, L. T., J. Bauer, D. A. Gross, F. Bucciarelli, H. Firat, D. Hudrisier, F. Lemonnier, K. Kosmatopoulos, and R. S. Liblau. 2007. CD8 T cell responses to myelin oligodendrocyte glycoprotein-derived peptides in humanized HLA-A*0201-transgenic mice. J. Immunol. 179: 5090-5098.
65. Murray, P. D., K. D. Pavelko, J. Leibowitz, X. Lin, and M. Rodriguez. 1998. CD4(+) and CD8(+) T cells make discrete contributions to demyelination and neurologic disease in a viral model of multiple sclerosis. J. Virol. 72: 7320-7329. (Pubitemid 28377863)
66. Plautz, G. E., S. Mukai, P. A. Cohen, and S. Shu. 2000. Cross-presentation of tumor antigens to effector T cells is sufficient to mediate effective immunotherapy of established intracranial tumors. J. Immunol. 165: 3656-3662. (Pubitemid 32057270)
67. Hayashi, T., S. Nagai, H. Fujii, Y. Baba, E. Ikeda, T. Kawase, and S. Koyasu. 2009. Critical roles of NK and CD8+ T cells in central nervous system listeriosis. J. Immunol. 182: 6360-6368.
68. 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)
69. Virna, S., M. Deckert, S. Lütjen, S. Soltek, K. E. Foulds, H. Shen, H. Körner, J. D. Sedgwick, and D. Schlüter. 2006. TNF is important for pathogen control and limits brain damage in murine cerebral listeriosis. J. Immunol. 177: 3972-3982. (Pubitemid 44359930)