Inflammasome-derived IL-1β production induces nitric oxide-mediated resistance to Leishmania

Nature Medicine

Volumn 19, Issue 7, 2013, Pages 909-915

  Lima Junior, Djalma S ^a   Costa, Diego L ^a   Carregaro, Vanessa ^b   Cunha, Larissa D ^a   Silva, Alexandre L N ^a   Mineo, Tiago W P ^a,e   Gutierrez, Fredy R S ^a,f   Bellio, Maria ^b   Bortoluci, Karina R ^c   Flavell, Richard A ^d   Bozza, Marcelo T ^b   Silva, João S ^a   Zamboni, Dario S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^f CENTRO DE INVESTIGACIONES   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; GAMMA INTERFERON; GLIBENCLAMIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CYTOKINE PRODUCTION; HOST RESISTANCE; IMMUNE RESPONSE; IN VIVO STUDY; INFECTION RESISTANCE; LEISHMANIA; LEISHMANIA BRAZILIENSIS; LEISHMANIA INFANTUM; LEISHMANIASIS; MACROPHAGE; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; MOUSE; NONHUMAN; PARASITE REPLICATION; PRIORITY JOURNAL; WESTERN BLOTTING;

ANIMALS; CARRIER PROTEINS; CASPASE 1; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DISEASE RESISTANCE; FEMALE; INFLAMMASOMES; INTERLEUKIN-1BETA; LEISHMANIA; LEISHMANIASIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II;

LEISHMANIA AMAZONENSIS; LEISHMANIA BRAZILIENSIS; LEISHMANIA INFANTUM; MUS;

EID: 84880255426     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3221     Document Type: Article

References (51)

1. Reithinger, R. et al. Cutaneous leishmaniasis. Lancet Infect. Dis. 7, 581-596 (2007).
2. Chappuis, F. et al. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat. Rev. Microbiol. 5, 873-882 (2007).
3. Bosque, F., Saravia, N.G., Valderrama, L. & Milon, G. Distinct innate and acquired immune responses to Leishmania in putative susceptible and resistant human populations endemically exposed to L. (Viannia) panamensis infection. Scand. J. Immunol. 51, 533-541 (2000).
4. Liu, D. & Uzonna, J.E. The early interaction of Leishmania with macrophages and dendritic cells and its influence on the host immune response. Front. Cell Infect. Microbiol. 2, 83 (2012).
5. Mosser, D.M. & Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969 (2008).
6. Green, S.J., Crawford, R.M., Hockmeyer, J.T., Meltzer, M.S. & Nacy, C.A. Leishmania major amastigotes initiate the l-arginine-dependent killing mechanism in IFN-(-stimulated macrophages by induction of tumor necrosis factor-a. J. Immunol. 145, 4290-4297 (1990).
7. Green, S.J., Meltzer, M.S., Hibbs, J.B. Jr. & Nacy, C.A. Activated macrophages destroy intracellular Leishmania major amastigotes by an l-arginine-dependent killing mechanism. J. Immunol. 144, 278-283 (1990).
8. Mukbel, R.M. et al. Macrophage killing of Leishmania amazonensis amastigotes requires both nitric oxide and superoxide. Am. J. Trop. Med. Hyg. 76, 669-675 (2007).
9. Chen, G., Shaw, M.H., Kim, Y.G. & Nunez, G. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 4, 365-398 (2009).
10. Martinon, F., Mayor, A. & Tschopp, J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265 (2009).
11. Wen, H., Ting, J.P. & O'Neill, L.A. A role for the NLRP3 inflammasome in metabolic diseases -did Warburg miss inflammation? Nat. Immunol. 13, 352-357 (2012).
12. Franchi, L., Kanneganti, T.D., Dubyak, G.R. & Nunez, G. Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 282, 18810-18818 (2007).
13. Pétrilli, V. et al. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14, 1583-1589 (2007).
14. Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677 (2008).
15. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
16. Mariathasan, S. et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232 (2006).
17. Mariathasan, S. et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218 (2004).
18. Sutterwala, F.S. et al. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204, 3235-3245 (2007).
19. Suzuki, T. et al. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 3, e111 (2007).
20. Zamboni, D.S. et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7, 318-325 (2006).
21. Hamon, M.A. & Cossart, P. K+ efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins. Infect. Immun. 79, 2839-2846 (2011).
22. Lamkanfi, M. et al. Glyburide inhibits the Cryopyrin/Nalp3 inflammasome. J. Cell Biol. 187, 61-70 (2009).
23. Montaser, M., Lalmanach, G. & Mach, L. CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells. Biol. Chem. 383, 1305-1308 (2002).
24. Liew, F.Y. et al. Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur. J. Immunol. 21, 3009-3014 (1991).
25. Stenger, S., Thuring, H., Rollinghoff, M. & Bogdan, C. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J. Exp. Med. 180, 783-793 (1994).
26. Belkaid, Y. et al. 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 (2000).
27. Andrade, Z.A., Reed, S.G., Roters, S.B. & Sadigursky, M. Immunopathology of experimental cutaneous leishmaniasis. Am. J. Pathol. 114, 137-148 (1984).
28. Fernandez-Figueroa, E.A. et al. Disease severity in patients infected with Leishmania mexicana relates to IL-1ß. PLoS Negl. Trop. Dis. 6, e1533 (2012).
29. Moravej, A. et al. IL-1ß (-511T/C) gene polymorphism not IL-1ß (+3953T/C) and LT-a (+252A/G) gene variants confers susceptibility to visceral leishmaniasis. Mol. Biol. Rep. 39, 6907-6914 (2012).
30. Ferreira, S.H., Lorenzetti, B.B., Bristow, A.F. & Poole, S. Interleukin-1 ß as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 334, 698-700 (1988).
31. Moncada, S., Palmer, R.M. & Higgs, E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142 (1991).
32. Nathan, C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064 (1992).
33. Werner-Felmayer, G. et al. Tetrahydrobiopterin-dependent formation of nitrite and nitrate in murine fibroblasts. J. Exp. Med. 172, 1599-1607 (1990).
34. Debus, A., Glasner, J., Rollinghoff, M. & Gessner, A. High levels of susceptibility and T helper 2 response in MyD88-deficient mice infected with Leishmania major are interleukin-4 dependent. Infect. Immun. 71, 7215-7218 (2003).
35. Muraille, E. et al. Genetically resistant mice lacking MyD88-adapter protein display a high susceptibility to Leishmania major infection associated with a polarized Th2 response. J. Immunol. 170, 4237-4241 (2003).
36. Gregory, D.J. & Olivier, M. Subversion of host cell signalling by the protozoan parasite Leishmania. Parasitology 130 (suppl.), S27-S35 (2005).
37. Shio, M.T. et al. Host cell signalling and Leishmania mechanisms of evasion. J. Trop. Med. 2012, 819512 (2012).
38. Soong, L. Modulation of dendritic cell function by Leishmania parasites. J. Immunol. 180, 4355-4360 (2008).
39. Xin, L., Li, K. & Soong, L. Down-regulation of dendritic cell signaling pathways by Leishmania amazonensis amastigotes. Mol. Immunol. 45, 3371-3382 (2008).
40. Sacks, D. & Noben-Trauth, N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2, 845-858 (2002).
41. Satoskar, A.R. et al. Enhanced Th2-like responses in IL-1 type 1 receptor-deficient mice. Eur. J. Immunol. 28, 2066-2074 (1998).
42. Kostka, S.L., Knop, J., Konur, A., Udey, M.C. & von Stebut, E. Distinct roles for IL-1 receptor type I signaling in early versus established Leishmania major infections. J. Invest. Dermatol. 126, 1582-1589 (2006).
43. Kautz-Neu, K. et al. IL-1 signalling is dispensable for protective immunity in Leishmania-resistant mice. Exp. Dermatol. 20, 76-78 (2011).
44. Kuida, K. et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1ß converting enzyme. Science 267, 2000-2003 (1995).
45. Lara-Tejero, M. et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412 (2006).
46. Späth, G.F. & Beverley, S.M. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp. Parasitol. 99, 97-103 (2001).
47. Afonso, L.C. & Scott, P. Immune responses associated with susceptibility of C57BL/10 mice to Leishmania amazonensis. Infect. Immun. 61, 2952-2959 (1993).
48. Marim, F.M., Silveira, T.N., Lima, D.S. Jr. & Zamboni, D.S. A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PLoS ONE 5, e15263 (2010).
49. Darrah, P.A. et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13, 843-850 (2007).
50. Green, L.C., Tannenbaum, S.R. & Goldman, P. Nitrate synthesis in the germfree and conventional rat. Science 212, 56-58 (1981).
51. Naviaux, R.K., Costanzi, E., Haas, M. & Verma, I.M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70, 5701-5705 (1996). Inflamatórias Estado Estado