IL-1β Signaling Promotes CNS-Intrinsic Immune Control of West Nile Virus Infection

PLoS Pathogens

Volumn 8, Issue 11, 2012, Pages

  Ramos, Hilario J ^a   Lanteri, Marion C ^b   Blahnik, Gabriele ^a   Negash, Amina ^a   Suthar, Mehul S ^a   Brassil, Margaret M ^a   Sodhi, Khushbu ^a   Treuting, Piper M ^a   Busch, Michael P ^b,c   Norris, Philip J ^b,c   Gale, Michael ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTERFERON; CD11B ANTIGEN; CD45 ANTIGEN; CRYOPYRIN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; VIRUS RNA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL ISOLATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MORTALITY; MOUSE; NONHUMAN; PARALYSIS; PROTEIN EXPRESSION; RADIOIMMUNOPRECIPITATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLEEN CELL; VIRUS LOAD; VIRUS REPLICATION; WEIGHT REDUCTION; WEST NILE FEVER; WESTERN BLOTTING;

ANIMALS; CARRIER PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; FEMALE; HUMANS; INFLAMMASOMES; INTERFERON TYPE I; INTERLEUKIN-1BETA; MALE; MICE; MICE, MUTANT STRAINS; NEURONS; SIGNAL TRANSDUCTION; VIRUS REPLICATION; WEST NILE FEVER; WEST NILE VIRUS;

ANIMALIA; FLAVIVIRUS; WEST NILE VIRUS;

EID: 84870793191     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003039     Document Type: Article

References (67)

1. Kramer LD, Li J, Shi PY, (2007) West Nile virus. Lancet Neurol 6: 171-181.
2. Poidinger M, Hall RA, Mackenzie JS, (1996) Molecular characterization of the Japanese encephalitis serocomplex of the flavivirus genus. Virology 218: 417-421.
3. Gubler DJ, (2007) The continuing spread of West Nile virus in the western hemisphere. Clin Infect Dis 45: 1039-1046.
4. Hayes EB, Komar N, Nasci RS, Montgomery SP, O'Leary DR, et al. (2005) Epidemiology and transmission dynamics of West Nile virus disease. Emerg Infect Dis 11: 1167-1173.
5. Samuel MA, Diamond MS, (2006) Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J Virol 80: 9349-9360.
6. Davis LE, DeBiasi R, Goade DE, Haaland KY, Harrington JA, et al. (2006) West Nile virus neuroinvasive disease. Ann Neurol 60: 286-300.
7. Sejvar JJ, Haddad MB, Tierney BC, Campbell GL, Marfin AA, et al. (2003) Neurologic manifestations and outcome of West Nile virus infection. JAMA 290: 511-515.
8. Byrne SN, Halliday GM, Johnston LJ, King NJ, (2001) Interleukin-1beta but not tumor necrosis factor is involved in West Nile virus-induced Langerhans cell migration from the skin in C57BL/6 mice. J Invest Dermatol 117: 702-709.
9. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, et al. (2010) IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog 6: e1000757.
10. Diamond MS, Sitati EM, Friend LD, Higgs S, Shrestha B, et al. (2003) A critical role for induced IgM in the protection against West Nile virus infection. J Exp Med 198: 1853-1862.
11. Lazear HM, Pinto AK, Vogt MR, Gale M Jr, Diamond MS, (2011) Beta interferon controls West Nile virus infection and pathogenesis in mice. J Virol 85: 7186-7194.
12. Samuel MA, Diamond MS, (2005) Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79: 13350-13361.
13. Shrestha B, Wang T, Samuel MA, Whitby K, Craft J, et al. (2006) Gamma interferon plays a crucial early antiviral role in protection against West Nile virus infection. J Virol 80: 5338-5348.
14. Shrestha B, Diamond MS, (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78: 8312-8321.
15. Wang Y, Lobigs M, Lee E, Mullbacher A, (2003) CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis. J Virol 77: 13323-13334.
16. Shrestha B, Samuel MA, Diamond MS, (2006) CD8+ T cells require perforin to clear West Nile virus from infected neurons. J Virol 80: 119-129.
17. King NJ, Getts DR, Getts MT, Rana S, Shrestha B, et al. (2007) Immunopathology of flavivirus infections. Immunol Cell Biol 85: 33-42.
18. Shrestha B, Zhang B, Purtha WE, Klein RS, Diamond MS, (2008) Tumor necrosis factor alpha protects against lethal West Nile virus infection by promoting trafficking of mononuclear leukocytes into the central nervous system. J Virol 82: 8956-8964.
19. Szretter KJ, Daffis S, Patel J, Suthar MS, Klein RS, et al. (2010) The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J Virol 84: 12125-12138.
20. Town T, Bai F, Wang T, Kaplan AT, Qian F, et al. (2009) Toll-like receptor 7 mitigates lethal West Nile encephalitis via interleukin 23-dependent immune cell infiltration and homing. Immunity 30: 242-253.
21. Ichikawa T, Nakao K, Nakata K, Yamashita M, Hamasaki K, et al. (2002) Involvement of IL-1beta and IL-10 in IFN-alpha-mediated antiviral gene induction in human hepatoma cells. Biochem Biophys Res Commun 294: 414-422.
22. Daniels HM, Meager A, Eddleston AL, Alexander GJ, Williams R, (1990) Spontaneous production of tumour necrosis factor alpha and interleukin-1 beta during interferon-alpha treatment of chronic HBV infection. Lancet 335: 875-877.
23. Ben-Sasson SZ, Caucheteux S, Crank M, Hu-Li J, Paul WE, (2011) IL-1 acts on T cells to enhance the magnitude of in vivo immune responses. Cytokine 56: 122-125.
24. Kanneganti TD, (2010) Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10: 688-698.
25. Dinarello CA, (1996) Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
26. Muzio M, Ni J, Feng P, Dixit VM, (1997) IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612-1615.
27. Martinon F, Burns K, Tschopp J, (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
28. Tschopp J, Martinon F, Burns K, (2003) NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 4: 95-104.
29. Dinarello CA, (1998) Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci 856: 1-11.
30. Bryant C, Fitzgerald KA, (2009) Molecular mechanisms involved in inflammasome activation. Trends Cell Biol 19: 455-464.
31. Rajan JV, Warren SE, Miao EA, Aderem A, (2010) Activation of the NLRP3 inflammasome by intracellular poly I:C. FEBS Lett 584: 4627-4632.
32. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, et al. (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30: 556-565.
33. Schmitz N, Kurrer M, Bachmann MF, Kopf M, (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 79: 6441-6448.
34. Thomas PG, Dash P, Aldridge JR Jr, Ellebedy AH, Reynolds C, et al. (2009) The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30: 566-575.
35. Sergerie Y, Rivest S, Boivin G, (2007) Tumor necrosis factor-alpha and interleukin-1 beta play a critical role in the resistance against lethal herpes simplex virus encephalitis. J Infect Dis 196: 853-860.
36. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A, (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206: 79-87.
37. Hurgin V, Novick D, Werman A, Dinarello CA, Rubinstein M, (2007) Antiviral and immunoregulatory activities of IFN-gamma depend on constitutively expressed IL-1alpha. Proc Natl Acad Sci U S A 104: 5044-5049.
38. Liang XH, Goldman JE, Jiang HH, Levine B, (1999) Resistance of interleukin-1beta-deficient mice to fatal Sindbis virus encephalitis. J Virol 73: 2563-2567.
39. Prow NA, Irani DN, (2008) The inflammatory cytokine, interleukin-1 beta, mediates loss of astroglial glutamate transport and drives excitotoxic motor neuron injury in the spinal cord during acute viral encephalomyelitis. J Neurochem 105: 1276-1286.
40. Das S, Mishra MK, Ghosh J, Basu A, (2008) Japanese Encephalitis Virus infection induces IL-18 and IL-1beta in microglia and astrocytes: correlation with in vitro cytokine responsiveness of glial cells and subsequent neuronal death. J Neuroimmunol 195: 60-72.
41. Kaushik DK, Gupta M, Kumawat KL, Basu A, (2012) NLRP3 Inflammasome: Key Mediator of Neuroinflammation in Murine Japanese Encephalitis. PLoS One 7: e32270.
42. Lai L, Lee TH, Tobler L, Wen L, Shi P, et al. (2012) Relative distribution of West Nile virus RNA in blood compartments: implications for blood donor nucleic acid amplification technology screening. Transfusion 52: 447-454.
43. Appler KK, Brown AN, Stewart BS, Behr MJ, Demarest VL, et al. (2010) Persistence of West Nile virus in the central nervous system and periphery of mice. PLoS One 5: e10649.
44. Keller BC, Fredericksen BL, Samuel MA, Mock RE, Mason PW, et al. (2006) Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J Virol 80: 9424-9434.
45. Samuel MA, Whitby K, Keller BC, Marri A, Barchet W, et al. (2006) PKR and RNase L contribute to protection against lethal West Nile Virus infection by controlling early viral spread in the periphery and replication in neurons. J Virol 80: 7009-7019.
46. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, et al. (2010) 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468: 452-456.
47. Perwitasari O, Cho H, Diamond MS, Gale M Jr, (2011) Inhibitor of kappaB kinase epsilon (IKK(epsilon)), STAT1, and IFIT2 proteins define novel innate immune effector pathway against West Nile virus infection. J Biol Chem 286: 44412-44423.
48. Suthar MS, Brassil MM, Blahnik G, Gale M Jr, (2012) Infectious clones of novel lineage 1 and lineage 2 West Nile virus strains WNV-TX02 and WNV-Madagascar. J Virol 86: 7704-7709.
49. Rajan JV, Rodriguez D, Miao EA, Aderem A, (2011) The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J Virol 85: 4167-4172.
50. Poeck H, Bscheider M, Gross O, Finger K, Roth S, et al. (2010) Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat Immunol 11: 63-69.
51. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
52. Burckstummer T, Baumann C, Bluml S, Dixit E, Durnberger G, et al. (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
53. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514-518.
54. Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M Jr, (2008) Establishment and maintenance of the innate antiviral response to West Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol 82: 609-616.
55. Bartholdy C, Christensen JE, Grujic M, Christensen JP, Thomsen AR, (2009) T-cell intrinsic expression of MyD88 is required for sustained expansion of the virus-specific CD8+ T-cell population in LCMV-infected mice. J Gen Virol 90: 423-431.
56. Rahman AH, Cui W, Larosa DF, Taylor DK, Zhang J, et al. (2008) MyD88 plays a critical T cell-intrinsic role in supporting CD8 T cell expansion during acute lymphocytic choriomeningitis virus infection. J Immunol 181: 3804-3810.
57. Quigley M, Martinez J, Huang X, Yang Y, (2009) A critical role for direct TLR2-MyD88 signaling in CD8 T-cell clonal expansion and memory formation following vaccinia viral infection. Blood 113: 2256-2264.
58. Zhao Y, De Trez C, Flynn R, Ware CF, Croft M, et al. (2009) The adaptor molecule MyD88 directly promotes CD8 T cell responses to vaccinia virus. J Immunol 182: 6278-6286.
59. Fensterl V, Wetzel JL, Ramachandran S, Ogino T, Stohlman SA, et al. (2012) Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog 8: e1002712.
60. Chang DM, Shaio MF, (1994) Production of interleukin-1 (IL-1) and IL-1 inhibitor by human monocytes exposed to dengue virus. J Infect Dis 170: 811-817.
61. Barros VE, Ferreira BR, Livonesi M, Figueiredo LT, (2009) Cytokine and nitric oxide production by mouse macrophages infected with Brazilian flaviviruses. Rev Inst Med Trop Sao Paulo 51: 141-147.
62. Kong KF, Wang X, Anderson JF, Fikrig E, Montgomery RR, (2008) West nile virus attenuates activation of primary human macrophages. Viral Immunol 21: 78-82.
63. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, et al. (2006) Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
64. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, et al. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267: 2000-2003.
65. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, et al. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
66. Shrestha B, Samuel MA, Diamond MS, (2006) CD8+ T cells require perforin to clear West Nile virus from infected neurons. JVirol 80: 119-129.
67. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M, (2003) B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol 77: 2578-2586.