Inhibition of caspase-8 activity promotes protective Th1- and Th2-mediated immunity to Leishmania major infection

Journal of Leukocyte Biology

Volumn 95, Issue 2, 2014, Pages 347-355

  Pereira Manfro, Wânia F ^a,e   Ribeiro Gomes, Flávia L ^a,b   Filardy, Alessandra Almeida ^a   Vellozo, Natália S ^a   Guillermo, Landi V C ^a,f   Silva, Elisabeth M ^a,g   Siegel, Richard M ^c   DosReis, George A ^a,d   Lopes, Marcela F ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^d Ministério de Ciência Tecnologia e Inovação Salvador   (Brazil)

^e STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^f FEDERAL UNIVERSITY OF THE STATE OF RIO DE JANEIRO   (Brazil)

^g FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Apoptosis; CD4 T cells; Cytokines; FasL; FLIP

Indexed keywords

CASPASE 8; CASPASE 9; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; NITRIC OXIDE; CYTOKINE; PARASITE ANTIGEN; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL SUSPENSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; LEISHMANIASIS; MOUSE; NECROPTOSIS; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL; T CELL CULTURE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; FASL; FLIP; HUMAN; IMMUNOLOGY; LEISHMANIA MAJOR; LYMPHOCYTE ACTIVATION; METABOLISM; PARASITOLOGY; TRANSGENIC MOUSE;

APOPTOSIS; CD4 T CELLS; CYTOKINES; FASL; FLIP;

ANIMALS; ANTIGENS, PROTOZOAN; APOPTOSIS; CASPASE 8; FEMALE; HUMANS; IMMUNITY, CELLULAR; INTERLEUKIN-4; LEISHMANIA MAJOR; LEISHMANIASIS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; TH1 CELLS; TH2 CELLS; VIRAL PROTEINS;

EID: 84897027004     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0912463     Document Type: Article

References (66)

1. Sacks, D., Noben-Trauth, N. (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2, 845-858.
2. McMahon-Pratt, D., Alexander, J. (2004) Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol. Rev. 201, 206-224.
3. Kaye, P., Scott, P. (2011) Leishmaniasis: complexity at the host-pathogen interface. Nat. Rev. Microbiol. 9, 604-615.
4. Ribeiro-Gomes, F.L., Peters, N.C., Debrabant, A., Sacks, D. L. (2012) Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog. 8, e1002536.
5. Tacchini-Cottier, F., Zweifel, C., Belkaid, Y., Mukankundiye, C., Vasei, M., Launois, P., Milon, G., Louis, J. A. (2000) An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165, 2628-2636.
6. Ribeiro-Gomes, F. L., Otero, A. C., Gomes, N. A., Moniz-De-Souza, M. C., Cysne-Finkelstein, L., Arnholdt, A. C., Calich, V. L., Coutinho, S. G., Lopes, M. F., DosReis, G. A. (2004) Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172, 4454-4462.
7. Ribeiro-Gomes, F. L., Moniz-de-Souza, M. C., Borges, V. M., Nunes, M. P., Mantuano-Barradas, M., D'Avila, H., Bozza, P. T., Calich, V. L., DosReis, G. A. (2005) Turnover of neutrophils mediated by Fas ligand drives Leishmania major infection. J. Infect. Dis. 192, 1127-1134.
8. Ribeiro-Gomes, F. L., Moniz-de-Souza, M. C., Alexandre-Moreira, M. S., Dias, W. B., Lopes, M. F., Nunes, M. P., Lungarella, G., DosReis, G. A. (2007) Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase. J. Immunol. 179, 3988-3994.
9. Peters, N. C., Egen, J. G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P., Fay, M. P., Germain, R. N., Sacks, D. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974.
10. high regulatory phenotype in macrophages. J. Immunol. 185, 2044-2050.
11. Belkaid, Y., Piccirillo, C. A., Mendez, S., Shevach, E. M., Sacks, D. L. (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507.
12. Sacks, D., Anderson, C. (2004) Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol. Rev. 201, 225-238.
13. Siegel, R. M. (2006) Caspases at the crossroads of immune-cell life and death. Nat. Rev. Immunol. 6, 308-317.
14. Hahn, S., Stalder, T., Wernli, M., Burgin, D., Tschopp, J., Nagata, S., Erb, P. (1995) Down-modulation of CD4+ T helper type 2 and type 0 cells by T helper type 1 cells via Fas/Fas-ligand interaction. Eur. J. Immunol. 25, 2679-2685.
15. Watanabe, N., Arase, H., Kurasawa, K., Iwamoto, I., Kayagaki, N., Yagita, H., Okumura, K., Miyatake, S., Saito, T. (1997) Th1 and Th2 subsets equally undergo Fas-dependent and-independent activation-induced cell death. Eur. J. Immunol. 27, 1858-1864.
16. Zhang, X., Brunner, T., Carter, L., Dutton, R. W., Rogers, P., Bradley, L., Sato, T., Reed, J. C., Green, D., Swain, S. L. (1997) Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 185, 1837-1849.
17. Devadas, S., Das, J., Liu, C., Zhang, L., Roberts, A. I., Pan, Z., Moore, P. A., Das, G., Shi, Y. (2006) Granzyme B is critical for T cell receptorinduced cell death of type 2 helper T cells. Immunity 25, 237-247.
18. Lopes, M. F., Guillermo, L. V., Silva, E. M. (2007) Decoding caspase signaling in host immunity to the protozoan Trypanosoma cruzi. Trends Immunol. 28, 366-372.
19. Bertho, A. L., Santiago, M. A., Da-Cruz, A. M., Coutinho, S. G. (2000) Detection of early apoptosis and cell death in T CD4+ and CD8β cells from lesions of patients with localized cutaneous leishmaniasis. Braz. J. Med. Biol. Res. 33, 317-325.
20. Eidsmo, L., Wolday, D., Berhe, N., Sabri, F., Satti, I., El Hassan, A. M., Sundar, S., Chiodi, F., Akuffo, H. (2002) Alteration of Fas and Fas ligand expression during human visceral leishmaniasis. Clin. Exp. Immunol. 130, 307-313.
21. Eidsmo, L., Nylen, S., Khamesipour, A., Hedblad, M. A., Chiodi, F., Akuffo, H. (2005) The contribution of the Fas/FasL apoptotic pathway in ulcer formation during Leishmania major-induced cutaneous Leishmaniasis. Am. J. Pathol. 166, 1099-1108.
22. Tasew, G., Nylen, S., Lieke, T., Lemu, B., Meless, H., Ruffin, N., Wolday, D., Asseffa, A., Yagita, H., Britton, S., Akuffo, H., Chiodi, F., Eidsmo, L. (2011) Systemic FasL and TRAIL neutralisation reduce leishmaniasis induced skin ulceration. PLoS Negl. Trop. Dis. 4, e844.
23. Desbarats, J., Stone, J. E., Lin, L., Zakeri, Z. F., Davis, G. S., Pfeiffer, L. M., Titus, R. G., Newell, M. K. (2000) Rapid early onset lymphocyte cell death in mice resistant, but not susceptible to Leishmania major infection. Apoptosis 5, 189-196.
24. Potestio, M., D'Agostino, P., Romano, G. C., Milano, S., Ferlazzo, V., Aquino, A., Di Bella, G., Caruso, R., Gambino, G., Vitale, G., Mansueto, S., Cillari, E. (2004) CD4+ CCR5+ and CD4+ CCR3+ lymphocyte subset and monocyte apoptosis in patients with acute visceral leishmaniasis. Immunology 113, 260-268.
25. Das, G., Vohra, H., Rao, K., Saha, B., Mishra, G. C. (1999) Leishmania donovani infection of a susceptible host results in CD4+ T-cell apoptosis and decreased Th1 cytokine production. Scand. J. Immunol. 49, 307-310.
26. Alexander, C. E., Kaye, P. M., Engwerda, C. R. (2001) CD95 is required for the early control of parasite burden in the liver of Leishmania donovani-infected mice. Eur. J. Immunol. 31, 1199-1210.
27. Conceicao-Silva, F., Hahne, M., Schroter, M., Louis, J., Tschopp, J. (1998) The resolution of lesions induced by Leishmania major in mice requires a functional Fas (APO-1, CD95) pathway of cytotoxicity. Eur. J. Immunol. 28, 237-245.
28. Huang, F. P., Xu, D., Esfandiari, E. O., Sands, W., Wei, X. Q., Liew, F. Y. (1998) Mice defective in Fas are highly susceptible to Leishmania major infection despite elevated IL-12 synthesis, strong Th1 responses, and enhanced nitric oxide production. J. Immunol. 160, 4143-4147.
29. Chakour, R., Allenbach, C., Desgranges, F., Charmoy, M., Mauel, J., Garcia, I., Launois, P., Louis, J., Tacchini-Cottier, F. (2009) A new function of the Fas-FasL pathway in macrophage activation. J. Leukoc. Biol. 86, 81-90.
30. Thome, M., Schneider, P., Hofmann, K., Fickenscher, H., Meinl, E., Neipel, F., Mattmann, C., Burns, K., Bodmer, J. L., Schroter, M., Scaffidi, C., Krammer, P. H., Peter, M. E., Tschopp, J. (1997) Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386, 517-521.
31. Wu, Z., Roberts, M., Porter, M., Walker, F., Wherry, E. J., Kelly, J., Gadina, M., Silva, E. M., DosReis, G. A., Lopes, M. F., O'Shea, J., Leonard, W. J., Ahmed, R., Siegel, R. M. (2004) Viral FLIP impairs survival of activated T cells and generation of CD8+ T cell memory. J. Immunol. 172, 6313-6323.
32. Chan, F. K., Shisler, J., Bixby, J. G., Felices, M., Zheng, L., Appel, M., Orenstein, J., Moss, B., Lenardo, M. J. (2003) A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 278, 51613-51621.
33. Mocarski, E. S., Upton, J. W., Kaiser, W. J. (2011) Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12, 79-88.
34. Kennedy, N. J., Kataoka, T., Tschopp, J., Budd, R. C. (1999) Caspase activation is required for T cell proliferation. J. Exp. Med. 190, 1891-1896.
35. Silva, E. M., Guillermo, L. V., Ribeiro-Gomes, F. L., De Meis, J., Pereira, R. M., Wu, Z., Calegari-Silva, T. C., Seabra, S. H., Lopes, U. G., Siegel, R. M., Dosreis, G. A., Lopes, M. F. (2005) Caspase-8 activity prevents type 2 cytokine responses and is required for protective T cell-mediated immunity against Trypanosoma cruzi infection. J. Immunol. 174, 6314-6321.
36. Chun, H. J., Zheng, L., Ahmad, M., Wang, J., Speirs, C. K., Siegel, R. M., Dale, J. K., Puck, J., Davis, J., Hall, C. G., Skoda-Smith, S., Atkinson, T. P., Straus, S. E., Lenardo, M. J. (2002) Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 419, 395-399.
37. Kataoka, T., Tschopp, J. (2004) N-terminal fragment of c-FLIP(L) processed by caspase 8 specifically interacts with TRAF2 and induces activation of the NF-κB signaling pathway. Mol. Cell. Biol. 24, 2627-2636.
38. Belkaid, Y., Mendez, S., Lira, R., Kadambi, N., Milon, G., Sacks, D. (2000) A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165, 969-977.
39. Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S., Tannenbaum, S. R. (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138.
40. Reinhardt, R. L., Khoruts, A., Merica, R., Zell, T., Jenkins, M. K. (2001) Visualizing the generation of memory CD4 T cells in the whole body. Nature 410, 101-105.
41. Darrah, P. A., Patel, D. T., De Luca, P. M., Lindsay, R. W., Davey, D. F., Flynn, B. J., Hoff, S. T., Andersen, P., Reed, S. G., Morris, S. L., Roederer, M., Seder, R. A. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13, 843-850.
42. Su, H., Bidere, N., Zheng, L., Cubre, A., Sakai, K., Dale, J., Salmena, L., Hakem, R., Straus, S., Lenardo, M. (2005) Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 307, 1465-1468.
43. Tseveleki, V., Bauer, J., Taoufik, E., Ruan, C., Leondiadis, L., Haralambous, S., Lassmann, H., Probert, L. (2004) Cellular FLIP (long isoform) overexpression in T cells drives Th2 effector responses and promotes immunoregulation in experimental autoimmune encephalomyelitis. J. Immunol. 173, 6619-6626.
44. Wu, W., Rinaldi, L., Fortner, K. A., Russell, J. Q., Tschopp, J., Irvin, C., Budd, R. C. (2004) Cellular FLIP long form-transgenic mice manifest a Th2 cytokine bias and enhanced allergic airway inflammation. J. Immunol. 172, 4724-4732.
45. Lopes, M. F., Nunes, M. P., Henriques-Pons, A., Giese, N., Morse III H. C., Davidson, W. F., Araujo-Jorge, T. C., DosReis, G. A. (1999) Increased susceptibility of Fas ligand-deficient gld mice to Trypanosoma cruzi infection due to a Th2-biased host immune response. Eur. J. Immunol. 29, 81-89.
46. Tseveleki, V., Tsagozis, P., Koutsoni, O., Dotsika, E., Probert, L. (2007) Cellular FLIP long isoform transgenic mice overcome inherent Th2-biased immune responses to efficiently resolve Leishmania major infection. Int. Immunol. 19, 1183-1189.
47. Carter, K. C., Gallagher, G., Baillie, A. J., Alexander, J. (1989) The induction of protective immunity to Leishmania major in the BALB/c mouse by interleukin 4 treatment. Eur. J. Immunol. 19, 779-782.
48. Lezama-Davila, C. M., Williams, D. M., Gallagher, G., Alexander, J. (1992) Cytokine control of Leishmania infection in the BALB/c mouse: enhancement and inhibition of parasite growth by local administration of IL-2 or IL-4 is species and time dependent. Parasite Immunol. 14, 37-48.
49. Biedermann, T., Zimmermann, S., Himmelrich, H., Gumy, A., Egeter, O., Sakrauski, A. K., Seegmuller, I., Voigt, H., Launois, P., Levine, A. D., Wagner, H., Heeg, K., Louis, J. A., Rocken, M. (2001) IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat. Immunol. 2, 1054-1060.
50. Himmelrich, H., Launois, P., Maillard, I., Biedermann, T., Tacchini-Cottier, F., Locksley, R. M., Rocken, M., Louis, J. A. (2000) In BALB/c mice, IL-4 production during the initial phase of infection with Leishmania major is necessary and sufficient to instruct Th2 cell development resulting in progressive disease. J. Immunol. 164, 4819-4825.
51. Radwanska, M., Cutler, A. J., Hoving, J. C., Magez, S., Holscher, C., Bohms, A., Arendse, B., Kirsch, R., Hunig, T., Alexander, J., Kaye, P., Brombacher, F. (2007) Deletion of IL-4Rα on CD4 T cells renders BALB/c mice resistant to Leishmania major infection. PLoS Pathog. 3, e68.
52. Kopf, M., Brombacher, F., Kohler, G., Kienzle, G., Widmann, K. H., Lefrang, K., Humborg, C., Ledermann, B., Solbach, W. (1996) IL-4-deficient Balb/c mice resist infection with Leishmania major. J. Exp. Med. 184, 1127-1136.
53. Mohrs, M., Ledermann, B., Kohler, G., Dorfmuller, A., Gessner, A., Brombacher, F. (1999) Differences between IL-4-and IL-4 receptor α-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162, 7302-7308.
54. Noben-Trauth, N., Paul, W. E., Sacks, D. L. (1999) IL-4-and IL-4 receptor-deficient BALB/c mice reveal differences in susceptibility to Leishmania major parasite substrains. J. Immunol. 162, 6132-6140.
55. Kropf, P., Herath, S., Weber, V., Modolell, M., Muller, I. (2003) Factors influencing Leishmania major infection in IL-4-deficient BALB/c mice. Parasite Immunol. 25, 439-447.
56. Leal, L. M., Moss, D. W., Kuhn, R., Muller, W., Liew, F. Y. (1993) Interleukin-4 transgenic mice of resistant background are susceptible to Leishmania major infection. Eur. J. Immunol. 23, 566-569.
57. Erb, K. J., Blank, C., Moll, H. (1996) Susceptibility to Leishmania major in IL-4 transgenic mice is not correlated with the lack of a Th1 immune response. Immunol. Cell Biol. 74, 239-244.
58. Bogdan, C., Stenger, S., Rollinghoff, M., Solbach, W. (1991) Cytokine interactions in experimental cutaneous leishmaniasis. Interleukin 4 synergizes with interferon-γ to activate murine macrophages for killing of Leishmania major amastigotes. Eur. J. Immunol. 21, 327-333.
59. Belosevic, M., Davis, C. E., Meltzer, M. S., Nacy, C. A. (1988) Regulation of activated macrophage antimicrobial activities. Identification of lymphokines that cooperate with IFN-γ for induction of resistance to infection. J. Immunol. 141, 890-896.
60. Stenger, S., Solbach, W., Rollinghoff, M., Bogdan, C. (1991) Cytokine interactions in experimental cutaneous leishmaniasis. II. Endogenous tumor necrosis factor-α production by macrophages is induced by the synergistic action of interferon (IFN)-γ and interleukin (IL) 4 and accounts for the antiparasitic effect mediated by IFN-γ and IL 4. Eur. J. Immunol. 21, 1669-1675.
61. Gallina, G., Dolcetti, L., Serafini, P., De Santo, C., Marigo, I., Colombo, M. P., Basso, G., Brombacher, F., Borrello, I., Zanovello, P., Bicciato, S., Bronte, V. (2006) Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 116, 2777-2790.
62. Lai, Y. H., Heslan, J. M., Poppema, S., Elliott, J. F., Mosmann, T. R. (1996) Continuous administration of IL-13 to mice induces extramedullary hemopoiesis and monocytosis. J. Immunol. 156, 3166-3173.
63. Jacobsen, S. E., Okkenhaug, C., Veiby, O. P., Caput, D., Ferrara, P., Minty, A. (1994) Interleukin 13: novel role in direct regulation of proliferation and differentiation of primitive hematopoietic progenitor cells. J. Exp. Med. 180, 75-82.
64. Goncalves, R., Zhang, X., Cohen, H., Debrabant, A., Mosser, D. M. (2011) Platelet activation attracts a subpopulation of effector monocytes to sites of Leishmania major infection. J. Exp. Med. 208, 1253-1265.
65. Pereira, W. F., Ribeiro-Gomes, F. L., Guillermo, L. V., Vellozo, N. S., Montalvao, F., Dosreis, G. A., Lopes, M. F. (2011) Myeloid-derived suppressor cells help protective immunity to Leishmania major infection despite suppressed T cell responses. J. Leukoc. Biol. 90, 1191-1197.
66. Wang, Z. E., Reiner, S. L., Zheng, S., Dalton, D. K., Locksley, R. M. (1994) CD4+ effector cells default to the Th2 pathway in interferon γ-deficient mice infected with Leishmania major. J. Exp. Med. 179, 1367-1371.