IL-33 signaling is essential to attenuate viral-induced encephalitis development by downregulating iNOS expression in the central nervous system

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Franca, Rafael F O ^a   Costa, Renata S ^b   Silva, Jaqueline R ^b   Peres, Raphael S ^b   Mendonça, Leila R ^a   Colón, David F ^b   Alves Filho, José Carlos ^b   Cunha, Fernando Q ^b  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Experimental viral encephalitis; Flavivirus; Interleukin 33; Nitric oxide; ST2 receptor

Indexed keywords

GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR 4; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; STAT6 PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; DIFFERENTIATION ANTIGEN; IL1RL1 PROTEIN, MOUSE; IL33 PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR LIKE 1 PROTEIN; MESSENGER RNA; MONOCYTE-MACROPHAGE DIFFERENTIATION ANTIGEN; STAT6 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; GENE EXPRESSION; INFECTION SENSITIVITY; INNATE IMMUNITY; MORTALITY RATE; MOUSE; NEUROPATHOLOGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SURVIVAL RATE; UPREGULATION; VIRUS ENCEPHALITIS; VIRUS LOAD; ANIMAL; BAGG ALBINO MOUSE; CENTRAL NERVOUS SYSTEM; DEFICIENCY; DISEASE MODEL; FEMALE; FLAVIVIRIDAE INFECTION; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; ANTIGENS, DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CYTOKINES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENCEPHALITIS, VIRAL; FEMALE; FLAVIVIRIDAE INFECTIONS; FLOW CYTOMETRY; INTERLEUKIN-1 RECEPTOR-LIKE 1 PROTEIN; INTERLEUKIN-33; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NITRIC OXIDE SYNTHASE TYPE II; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR;

EID: 85007477165     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0628-1     Document Type: Article

References (40)

1. Tanaka H, Weigl DR, de Souza LO. The replication of Rocio virus in brain tissue of suckling mice. Study by electron microscopy. Arch Virol. 1983;78:309-14.
2. de Barros VE, Saggioro FP, Neder L, de Oliveira Franca RF, Mariguela V, Chavez JH, Penharvel S, Forjaz J, da Fonseca BA, Figueiredo LT. An experimental model of meningoencephalomyelitis by Rocio flavivirus in BALB/c mice: inflammatory response, cytokine production, and histopathology. Am J Trop Med Hyg. 2011;85:363-73.
3. Chavez JH, Franca RF, Oliveira CJ, de Aquino MT, Farias KJ, Machado PR, de Oliveira TF, Yokosawa J, Soares EG, da Silva JS et al. Influence of the CCR-5/MIP-1 alpha axis in the pathogenesis of Rocio virus encephalitis in a mouse model. Am J Trop Med Hyg. 2013;89:1013-8.
4. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 2005;23:479-90.
5. Liew FY, Pitman NI, McInnes IB. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol. 2010;10:103-10.
6. Talabot-Ayer D, Calo N, Vigne S, Lamacchia C, Gabay C, Palmer G. The mouse interleukin (Il)33 gene is expressed in a cell type-and stimulus-dependent manner from two alternative promoters. J Leukoc Biol. 2012;91:119-25.
7. Xu D, Chan WL, Leung BP, Huang F, Wheeler R, Piedrafita D, Robinson JH, Liew FY. Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J Exp Med. 1998;187:787-94.
8. Sesti-Costa R, Silva GK, Proenca-Modena JL, Carlos D, Silva ML, Alves-Filho JC, Arruda E, Liew FY, Silva JS. The IL-33/ST2 pathway controls coxsackievirus B5-induced experimental pancreatitis. J Immunol. 2013;191:283-92.
9. Rostan O, Gangneux JP, Piquet-Pellorce C, Manuel C, McKenzie AN, Guiguen C, Samson M, Robert-Gangneux F. The IL-33/ST2 axis is associated with human visceral leishmaniasis and suppresses Th1 responses in the livers of BALB/c mice infected with Leishmania donovani. MBio. 2013;4:e00383-00313.
10. Hung LY, Lewkowich IP, Dawson LA, Downey J, Yang Y, Smith DE, Herbert DR. IL-33 drives biphasic IL-13 production for noncanonical type 2 immunity against hookworms. Proc Natl Acad Sci U S A. 2013;110:282-7.
11. Yasuda K, Muto T, Kawagoe T, Matsumoto M, Sasaki Y, Matsushita K, Taki Y, Futatsugi-Yumikura S, Tsutsui H, Ishii KJ et al. Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. Proc Natl Acad Sci U S A. 2012;109:3451-6.
12. Bonilla WV, Frohlich A, Senn K, Kallert S, Fernandez M, Johnson S, Kreutzfeldt M, Hegazy AN, Schrick C, Fallon PG et al. The alarmin interleukin-33 drives protective antiviral CD8(+) T cell responses. Science. 2012;335:984-9.
13. Jackson DJ, Makrinioti H, Rana BM, Shamji BW, Trujillo-Torralbo MB, Footitt J, Jerico D-R, Telcian AG,Nikonova A, Zhu J et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. Am J Respir Crit Care Med. 2014;190:1373-82.
14. Villarreal DO, Weiner DB. Interleukin 33: a switch-hitting cytokine. Curr Opin Immunol. 2014;28:102-6.
15. Kurowska-Stolarska M, Stolarski B, Kewin P, Murphy G, Corrigan CJ, Ying S, Pitman N, Mirchandani A, Rana B, van Rooijen N et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol. 2009;183:6469-77.
16. Hiroi M, Sakaeda Y, Yamaguchi H, Ohmori Y. Anti-inflammatory cytokine interleukin-4 inhibits inducible nitric oxide synthase gene expression in the mouse macrophage cell line RAW264.7 through the repression of octamer-dependent transcription. Mediators Inflamm. 2013;2013:369693.
17. Jones LA, Roberts F, Nickdel MB, Brombacher F, McKenzie AN, Henriquez FL, Alexander J, Roberts CW et al. IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur J Immunol. 2010;40:426-36.
18. Lohning M, Stroehmann A, Coyle AJ, Grogan JL, Lin S, Gutierrez-Ramos JC, Levinson D, Radbruch A, Kamradt T. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci U S A. 1998; 95:6930-5.
19. Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, Smith DE, Dekruyff RH, Umetsu DT. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol. 2011;12:631-8.
20. Jiang HR, Milovanovic M, Allan D, Niedbala W, Besnard AG, Fukada SY, Alves-Filho JC, Togbe D, Goodyear CS, Linington C et al. IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur J Immunol. 2012;42:1804-14.
21. Gadani SP, Walsh JT, Smirnov I, Zheng J, Kipnis J. The glia-derived alarmin IL-33 orchestrates the immune response and promotes recovery following CNS injury. Neuron. 2015;85:703-9.
22. Griffin DE. Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol. 2003;3:493-502.
23. Chen H, Sun Y, Lai L, Wu H, Xiao Y, Ming B, Gao M, Zou H, Xiong P, Xu Y et al. Interleukin-33 is released in spinal cord and suppresses experimental autoimmune encephalomyelitis in mice. Neuroscience. 2015;308:157-68.
24. Su Z, Lin J, Lu F, Zhang X, Zhang L, Gandhi NB, de Paiva CS, Pflugfelder SC, Li DQ. Potential autocrine regulation of interleukin-33/ST2 signaling of dendritic cells in allergic inflammation. Mucosal Immunol. 2013;6:921-30.
25. Kim JH, Choi JY, Kim SB, Uyangaa E, Patil AM, Han YW, Park SY, Lee JH, Kim K, Eo SK. CD11c(hi) dendritic cells regulate Ly-6C(hi) monocyte differentiation to preserve immune-privileged CNS in lethal neuroinflammation. Sci Rep. 2015;5:17548.
26. Roe K, Kumar M, Lum S, Orillo B, Nerurkar VR, Verma S. West Nile virusinduced disruption of the blood-brain barrier in mice is characterized by the degradation of the junctional complex proteins and increase in multiple matrix metalloproteinases. J Gen Virol. 2012;93:1193-203.
27. Li F, Wang Y, Yu L, Cao S, Wang K, Yuan J, Wang C, Cui M, Fu ZF. Viral infection of the central nervous system and neuroinflammation precede blood-brain barrier disruption during Japanese encephalitis virus infection. J Virol. 2015;89:5602-14.
28. Kuang Y, Lackay SN, Zhao L, Fu ZF. Role of chemokines in the enhancement of BBB permeability and inflammatory infiltration after rabies virus infection. Virus Res. 2009;144:18-26.
29. Toborek M, Lee YW, Flora G, Pu H, Andras IE, Wylegala E, Hennig B, Nath A. Mechanisms of the blood-brain barrier disruption in HIV-1 infection. Cell Mol Neurobiol. 2005;25:181-99.
30. Moss DW, Bates TE. Activation of murine microglial cell lines by lipopolysaccharide and interferon-gamma causes NO-mediated decreases in mitochondrial and cellular function. Eur J Neurosci. 2001;13:529-38.
31. Gao K, Li X, Zhang L, Bai L, Dong W, Shi G, Xia X, Wu L. Transgenic expression of IL-33 activates CD8(+) T cells and NK cells and inhibits tumor growth and metastasis in mice. Cancer Lett. 2013;335:463-71.
32. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8:57-69.
33. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci. 2007;8:766-75.
34. Barros VE, Ferreira BR, Livonesi M, Figueiredo LT. Cytokine and nitric oxide production by mouse macrophages infected with Brazilian flaviviruses. Rev Inst Med Trop Sao Paulo. 2009;51:141-7.
35. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723-37.
36. Baruch K, Kertser A, Porat Z, Schwartz M. Cerebral nitric oxide represses choroid plexus NFkappaB-dependent gateway activity for leukocyte trafficking. EMBO J. 2015;34:1816-28.
37. Shechter R, Miller O, Yovel G, Rosenzweig N, London A, Ruckh J, Kim KW, Klein E, Kalchenko V, Bendel P et al. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity. 2013;38:555-69.
38. Franca RF, Zucoloto S, da Fonseca BA. A BALB/c mouse model shows that liver involvement in dengue disease is immune-mediated. Exp Mol Pathol. 2010;89:321-6.
39. Miller SD, Karpus WJ, Davidson TS. Experimental autoimmune encephalomyelitis in the mouse. Curr Protoc Immunol. 2010;Chapter 15:Unit 15 11.
40. Paula A. Pino and Astrid E. Cardona: Isolation of brain and spinal cord mononuclear cells using percoll gradients. J Vis Exp 2011;(48):2348 doi: 10. 3791/2348.