Activation of innate immune responses in the central nervous system during reovirus myelitis

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 8107-8118

  Schittone, Stephanie A ^a,b   Dionne, Kalen R ^a,b   Tyler, Kenneth L ^a,b,c   Clarke, Penny ^a  

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

^b UNIVERSITY OF COLORADO   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1BETA; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RESPONSE; EMBRYO; EX VIVO STUDY; GENE EXPRESSION; GLIOSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; MYELITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REOVIRUS INFECTION; SIGNAL TRANSDUCTION;

ANIMALS; CYTOKINES; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; MAMMALIAN ORTHOREOVIRUS 3; MICE; MICE, KNOCKOUT; MYELITIS; NEUROGLIA; RECEPTOR, INTERFERON ALPHA-BETA; REOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; SPINAL CORD;

ANIMALIA; MURINAE; MUS; ORTHOREOVIRUS;

EID: 84864387229     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00171-12     Document Type: Article

References (80)

1. Abele R, Tampe R. 2004. The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology 19:216-224.
2. Allaman I, et al. 2010. Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J. Neurosci. 30:3326-3338.
3. Batchelor PE, Tan S, Wills TE, Porritt MJ, Howells DW. 2008. Comparison of inflammation in the brain and spinal cord following mechanical injury. J. Neurotrauma 25:1217-1225.
4. Beckham JD, Tuttle KD, Tyler KL. 2010. Caspase-3 activation is required for reovirus-induced encephalitis in vivo. J. Neurovirol. 16:306-317.
5. Berens HM, Tyler KL. 2011. The pro-apoptotic Bcl-2 protein Bax plays an important role in the pathogenesis of reovirus encephalitis. J. Virol. 85:3858-3871.
6. Bernardino L, et al. 2008. Inflammatory events in hippocampal slice cultures prime neuronal susceptibility to excitotoxic injury: a crucial role of P2X7 receptor-mediated IL-1β release. J. Neurochem. 106:271-280.
7. Beutler B. 2009. Microbe sensing, positive feedback loops, and the pathogenesis of inflammatory diseases. Immunol. Rev. 227:248-263.
8. Blakely PK, Kleinschmidt-DeMasters BK, Tyler KL, Irani DN. 2009. Disrupted glutamate transporter expression in the spinal cord with acute flaccid paralysis caused by West Nile virus infection. J. Neuropathol. Exp. Neurol. 68:1061-1072.
9. Bonjardim CA, Ferreira PC, Kroon EG. 2009. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122:1-11.
10. Bordignon J, et al. 2008. Expression profile of interferon stimulated genes in central nervous system of mice infected with dengue virus type-1. Virology 377:319-329.
11. Buchanan MM, Hutchinson M, Watkins LR, Yin H. 2010. Toll-like receptor 4 in CNS pathologies. J. Neurochem. 114:13-27.
12. Chan WY, Kohsaka S, Rezaie P. 2007. The origin and cell lineage of microglia-new concepts. Brain Res. Rev. 53:344-354.
13. Civas A, Island ML, Genin P, Morin P, Navarro S. 2002. Regulation of virus-induced interferon-A genes. Biochimie 84:643-654.
14. Clarke P, Beckham JD, Leser JS, Hoyt CC, Tyler KL. 2009. Fas-mediated apoptotic signaling in the mouse brain following reovirus infection. J. Virol. 83:6161-6170.
15. Clarke P, Richardson-Burns SM, DeBiasi RL, Tyler KL. 2005. Mechanisms of apoptosis during reovirus infection. Curr. Top. Microbiol. Immunol. 289:1-24.
16. Clarke P, Tyler KL. 2009. Apoptosis in animal models of virus-induced disease. Nat. Rev. Microbiol. 7:144-155.
17. Daffis S, Samuel MA, Suthar MS, Gale M, Jr, Diamond MS. 2008. Toll-like receptor 3 has a protective role against West Nile virus infection. J. Virol. 82:10349-10358.
18. Dionne KR, Galvin JM, Schittone SA, Clarke P, Tyler KL. 2011. Type I interferon signaling limits reoviral tropism within the brain and prevents lethal systemic infection. J. Neurovirol. 17:314-326.
19. Dionne KR, Leser JS, Lorenzen KA, Beckham JD, Tyler KL. 2011. A brain slice culture model of viral encephalitis reveals an innate CNS cytokine response profile and the therapeutic potential of caspase inhibition. Exp. Neurol. 228:222-231.
20. Falschlehner C, Schaefer U, Walczak H. 2009. Following TRAIL's path in the immune system. Immunology 127:145-154.
21. Farina C, Aloisi F, Meinl E. 2007. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 28:138-145.
22. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG. 2009. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol. Neurodegener. 4:47.
23. Friedlander RM. 2003. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 348:1365-1375.
24. Fuller S, Steele M, Munch G. 2009. Activated astroglia during chronic inflammation in Alzheimer's disease-Do they neglect their neurosupportive roles? Mutat. Res. 690:40-49.
25. Gavillet M, Allaman I, Magistretti PJ. 2008. Modulation of astrocytic metabolic phenotype by proinflammatory cytokines. Glia 56:975-989.
26. Girard S, et al. 1999. Poliovirus induces apoptosis in the mouse central nervous system. J. Virol. 73:6066-6072.
27. Goodman AG, et al. 2010. The alpha/beta interferon receptor provides protection against influenza virus replication but is dispensable for inflammatory response signaling. J. Virol. 84:2027-2037.
28. Goody RJ, Beckham JD, Rubtsova K, Tyler KL. 2007. JAK-STAT signaling pathways are activated in the brain following reovirus infection. J. Neurovirol. 13:373-383.
29. Goody RJ, Hoyt CC, Tyler KL. 2005. Reovirus infection of the CNS enhances iNOS expression in areas of virus-induced injury. Exp. Neurol. 195:379-390.
30. Goody RJ, Schittone SA, Tyler KL. 2008. Experimental reovirus-induced acute flaccid paralysis and spinal motor neuron cell death. J. Neuropathol. Exp. Neurol. 67:231-239.
31. Haller O, Stertz S, Kochs G. 2007. The Mx GTPase family of interferoninduced antiviral proteins. Microbes Infect. 9:1636-1643.
32. Harty RN, Pitha PM, Okumura A. 2009. Antiviral activity of innate immune protein ISG15. J. Innate Immun. 1:397-404.
33. Holm GH, et al. 2007. Retinoic acid-inducible gene-I and interferon-beta promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J. Biol. Chem. 282:21953-21961.
34. Hu X, Chakravarty SD, Ivashkiv LB. 2008. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol. Rev. 226: 41-56.
35. Huang X, et al. 2008. Interferon-induced protein IFIT4 is associated with systemic lupus erythematosus and promotes differentiation of monocytes into dendritic cell-like cells. Arthritis Res. Ther. 10:R91. doi:10.1186/ ar2475.
36. Imai Y, Kohsaka S. 2002. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40:164-174.
37. Johansson C, et al. 2007. Type I interferons produced by hematopoietic cells protect mice against lethal infection by mammalian reovirus. J. Exp. Med. 204:1349-1358.
38. Kajaste-Rudnitski A, et al. 2006. The 2',5'-oligoadenylate synthetase 1b isa potent inhibitor of West Nile virus replication inside infected cells. J. Biol. Chem. 281:4624-4637.
39. Kanazawa H, Ohsawa K, Sasaki Y, Kohsaka S, Imai Y. 2002. Macrophage/ microglia-specific protein Iba1 enhances membrane ruffling and Rac activation via phospholipase C-gamma-dependent pathway. J. Biol. Chem. 277:20026-20032.
40. Kawai T, Akira S. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143:1-20.
41. Kawanokuchi J, et al. 2006. Production of interferon-gamma by microglia. Mult. Scler. 12:558-564.
42. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM. 2002. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods 115:97-105.
43. Kigerl KA, et al. 2007. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J. Neurochem. 102:37-50.
44. Kraft AD, McPherson CA, Harry GJ. 2009. Heterogeneity of microglia and TNF signaling as determinants for neuronal death or survival. Neurotoxicology 30:785-793.
45. Lehnardt S. 2010. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58:253-263.
46. Loo YM, et al. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335-345.
47. Maher SG, Romero-Weaver AL, Scarzello AJ, Gamero AM. 2007. Interferon: cellular executioner or white knight? Curr. Med. Chem. 14: 1279-1289.
48. Marsh BJ, Williams-Karnesky RL, Stenzel-Poore MP. 2009. Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 158:1007-1020.
49. Matsumoto H, et al. 2007. Antibodies to CD11b, CD68, and lectin label neutrophils rather than microglia in traumatic and ischemic brain lesions. J. Neurosci. Res. 85:994-1009.
50. Mendez II, Hermann LL, Hazelton PR, Coombs KM. 2000. A comparative analysis of freon substitutes in the purification of reovirus and calicivirus. J. Virol. Methods 90:59.
51. Milligan ED, Watkins LR. 2009. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10:23-36.
52. Mir M, et al. 2009. Tumor necrosis factor alpha and interferon gamma cooperatively induce oxidative stress and motoneuron death in rat spinal cord embryonic explants. Neuroscience 162:959-971.
53. Morrey JD, et al. 2008. West Nile virus-induced acute flaccid paralysis is prevented by monoclonal antibody treatment when administered after infection of spinal cord neurons. J. Neurovirol. 14:152-163.
54. Nakhaei P, Genin P, Civas A, Hiscott J. 2009. RIG-I-like receptors: sensing and responding toRNAvirus infection. Semin. Immunol. 21:215-222.
55. Napoli I, Neumann H. 2009. Microglial clearance function in health and disease. Neuroscience 158:1030-1038.
56. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
57. Ohsawa K, Imai Y, Sasaki Y, Kohsaka S. 2004. Microglia/macrophagespecific protein Iba1 binds to fimbrin and enhances its actin-bundling activity. J. Neurochem. 88:844-856.
58. Park KM, Bowers WJ. 2010. Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal. 22:977-983.
59. Park SY, et al. 2004. IFN-gamma enhances TRAIL-induced apoptosis through IRF-1. Eur. J. Biochem. 271:4222-4228.
60. 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.
61. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
62. Ransohoff RM, Perry VH. 2009. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27:119-145.
63. Richardson-Burns SM, Kominsky DJ, Tyler KL. 2002. Reovirus-induced neuronal apoptosis is mediated by caspase 3 and is associated with the activation of death receptors. J. Neurovirol. 8:365-380.
64. Richardson-Burns SM, Tyler KL. 2005. Minocycline delays disease onset and mortality in reovirus encephalitis. Exp. Neurol. 192:331-339.
65. Romieu-Mourez R, et al. 2009. Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype. J. Immunol. 182:7963-7973.
66. Sadler AJ, Williams BR. 2008. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8:559-568.
67. Sarkar A, Mitra S, Mehta S, Raices R, Wewers MD. 2009. Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 4:e7140. doi:10.1371/journal.pone.0007140.
68. Savitsky D, Tamura T, Yanai H, Taniguchi T. 2010. Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol. Immunother. 59:489-510.
69. Sharma A, Maheshwari RK. 2009. Oligonucleotide array analysis of Tolllike receptors and associated signalling genes in Venezuelan equine encephalitis virus-infected mouse brain. J. Gen. Virol. 90:1836-1847.
70. Smith JA, et al. 2009. Estrogen partially down-regulates PTEN to prevent apoptosis in VSC4.1 motoneurons following exposure to IFN-gamma. Brain Res. 1301:163-170.
71. So EY, Kim BS. 2009. Theiler's virus infection induces TLR3-dependent upregulation of TLR2 critical for proinflammatory cytokine production. Glia 57:1216-1226.
72. Tamura T, Yanai H, Savitsky D, Taniguchi T. 2008. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 26:535-584.
73. Tribouillard-Tanvier D, Striebel JF, Peterson KE, Chesebro B. 2009. Analysis of protein levels of 24 cytokines in Scrapie agent-infected brain and glial cell cultures from mice differing in prion protein expression levels. J. Virol. 83:11244-11253.
74. Tsunoda I, Lane TE, Blackett J, Fujinami RS. 2004. Distinct roles for IP-10/CXCL10 in three animal models, Theiler's virus infection, EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10. Mult. Scler. 10:26-34.
75. Tyler KL, Leser JS, Phang TL, Clarke P. 2010. Gene expression in the brain during reovirus encephalitis. J. Neurovirol. 16:56-71.
76. Wacher C, et al. 2007. Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J. Virol. 81:860-871.
77. Watkins LR, et al. 2007. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids. Norman Cousins Lecture. Brain Behav. Immun. 21:131-146.
78. Wilkins C, Gale M, Jr. 2010. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 22:41-47.
79. Xagorari A, Chlichlia K. 2008. Toll-like receptors and viruses: induction of innate antiviral immune responses. Open Microbiol. J. 2:49-59.
80. Zhang B, Chan YK, Lu B, Diamond MS, Klein RS. 2008. CXCR3 mediates region-specific antiviral T cell trafficking within the central nervous system during West Nile virus encephalitis. J. Immunol. 180:2641-2649.