Interferons in the central nervous system: A few instruments play many tunes

GLIA

Volumn 62, Issue 3, 2014, Pages 339-355

  Owens, Trevor ^a   Khorooshi, Reza ^a   Wlodarczyk, Agnieszka ^a   Asgari, Nasrin ^a,b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b LILLEBAELT HOSPITAL   (Denmark)

Author keywords

Astrocytes; IFNAR; Interferon; Microglia

Indexed keywords

INTERFERON;

AICARDI GOUTIERES SYNDROME; AMYOTROPHIC LATERAL SCLEROSIS; ANTIGEN ANTIBODY COMPLEX; ASTROCYTE; AUTOIMMUNE DISEASE; BIOLOGICAL ACTIVITY; BLOOD BRAIN BARRIER; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CHROMOSOME 10; CHROMOSOME 12; CHROMOSOME 19; CHROMOSOME 4; CHROMOSOME 9; CLINICAL TRIAL (TOPIC); DISEASE ACTIVITY; EPITHELIUM CELL; EXON; GLIA CELL; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; INFLAMMATION; INNATE IMMUNITY; INTRON; LIGAND BINDING; MICROGLIA; MOLECULAR WEIGHT; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; NERVE CELL; NEUROLOGIC DISEASE; NONHUMAN; PATHOGENESIS; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; VIRUS INFECTION; ANIMAL; CYTOLOGY; GLIA; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; NERVOUS SYSTEM DISEASES; PHYSIOLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; IMMUNE SYSTEM; INTERFERONS; NERVOUS SYSTEM DISEASES; NEUROGLIA;

EID: 84892497397     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22608     Document Type: Review

References (184)

1. 1993. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. The IFNB Multiple Sclerosis Study Group. Neurology 43:655-661.
2. Ablasser A, Schmid-Burgk JL, Hemmerling I, Horvath GL, Schmidt T, Latz E, Hornung V. 2013. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature. DOI: 10.1038/nature12640.
3. Abreu SL. 1982. Suppression of experimental allergic encephalomyelitis by interferon. Immunol Commun 11:1-7.
4. Akira S, Takeda K. 2004. Toll-like receptor signalling. Nat Rev Immunol 4:499-511.
5. Akwa Y, Hassett DE, Eloranta ML, Sandberg K, Masliah E, Powell H, Whitton JL, Bloom FE, Campbell IL. 1998. Transgenic expression of IFN-alpha in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration. J Immunol 161:5016-5026.
6. Al-Masri AN, Heidenreich F, Walter GF. 2009. Interferon-induced Mx proteins in brain tissue of multiple sclerosis patients. Eur J Neurol 16:721-726.
7. Alammar L, Gama L, Clements JE. 2011. Simian immunodeficiency virus infection in the brain and lung leads to differential type I IFN signaling during acute infection. J Immunol 186:4008-4018.
8. Almer G, Vukosavic S, Romero N, Przedborski S. 1999. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 72:2415-2425.
9. Ank N, Iversen MB, Bartholdy C, Staeheli P, Hartmann R, Jensen UB, Dagnaes-Hansen F, Thomsen AR, Chen Z, Haugen H, Klucher K, Paludan SR. 2008. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J Immunol 180:2474-2485.
10. Asgari N, Khorooshi R, Lillevang ST, Owens T. 2013. Complement-dependent pathogenicity of brain-specific antibodies in cerebrospinal fluid. J Neuroimmunol 254:76-82.
11. Asgari N, Owens T, Frokiaer J, Stenager E, Lillevang ST, Kyvik KO. 2011. Neuromyelitis optica (NMO)-an autoimmune disease of the central nervous system (CNS). Acta Neurol Scand 123:369-384.
12. Axtell RC, Steinman L. 2008. Type 1 interferons cool the inflamed brain. Immunity 28:600-602.
13. Babcock AA, Wirenfeldt M, Holm T, Nielsen HH, Dissing-Olesen L, Toft-Hansen H, Millward JM, Landmann R, Rivest S, Finsen B, Owens T. 2006. Toll-like receptor 2 signaling in response to brain injury: an innate bridge to neuroinflammation. J Neurosci 26:12826-12837.
14. Bailey-Bucktrout SL, Caulkins SC, Goings G, Fischer JA, Dzionek A, Miller SD. 2008. Cutting edge: central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis. J Immunol 180:6457-6461.
15. Ban M, Goris A, Lorentzen AR, Baker A, Mihalova T, Ingram G, Booth DR, Heard RN, Stewart GJ, Bogaert E, Dubois B, Harbo HF, Celius EG, Spurkland A, Strange R, Hawkins C, Robertson NP, Dudbridge F, Wason J, De Jager PL, Hafler D, Rioux JD, Ivinson AJ, McCauley JL, Pericak-Vance M, Oksenberg JR, Hauser SL, Sexton D, Haines J, Sawcer S, Compston A. 2009. Replication analysis identifies TYK2 as a multiple sclerosis susceptibility factor. Eur J Hum Genet 17:1309-1313.
16. Banchereau J, Pascual V. 2006. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25:383-392.
17. Barbalat R, Ewald SE, Mouchess ML, Barton GM. 2011. Nucleic acid recognition by the innate immune system. Annu Rev Immunol 29:185-214.
18. Barbalat R, Lau L, Locksley RM, Barton GM. 2009. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10:1200-1207.
19. Barnett MH, Parratt JD, Cho ES, Prineas JW. 2009. Immunoglobulins and complement in postmortem multiple sclerosis tissue. Ann Neurol 65:32-46.
20. Beghi E, Chio A, Inghilleri M, Mazzini L, Micheli A, Mora G, Poloni M, Riva R, Serlenga L, Testa D, Tonali P. 2000. A randomized controlled trial of recombinant interferon beta-1a in ALS. Italian Amyotrophic Lateral Sclerosis Study Group. Neurology 54:469-474.
21. Bergkvist M, Martinsson T, Aman P, Sandberg-Wollheim M. 1996. No genetic linkage between multiple sclerosis and the interferon alpha/beta locus. J Neuroimmunol 65:163-165.
22. Bieber AJ, Suwansrinon K, Kerkvliet J, Zhang W, Pease LR, Rodriguez M. 2010. Allelic variation in the Tyk2 and EGF genes as potential genetic determinants of CNS repair. Proc Natl Acad Sci USA 107:792-797.
23. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, Stark GR. 2007. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 6:975-990.
24. Borysiewicz E, Fil D, Konat GW. 2009. Rho proteins are negative regulators of TLR2, TLR3, and TLR4 signaling in astrocytes. J Neurosci Res 87:1565-1572.
25. Boutros T, Croze E, Yong VW. 1997. Interferon-beta is a potent promoter of nerve growth factor production by astrocytes. J Neurochem 69:939-946.
26. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, Adzemovic M, Bauer J, Berger T, Fujihara K, Itoyama Y, Lassmann H. 2009. Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol 66:630-643.
27. Brandt ER, Mackay IR, Hertzog PJ, Cheetham BF, Sherritt M, Bernard CC. 1993. Molecular detection of interferon-alpha expression in multiple sclerosis brain. J Neuroimmunol 44:1-5.
28. Brod SA, Khan M, Kerman RH, Pappolla M. 1995. Oral administration of human or murine interferon alpha suppresses relapses and modifies adoptive transfer in experimental autoimmune encephalomyelitis. J Neuroimmunol 58:61-9.
29. Bsibsi M, Ravid R, Gveric D, van Noort JM. 2002. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61:1013-1021.
30. Campbell IL, Krucker T, Steffensen S, Akwa Y, Powell HC, Lane T, Carr DJ, Gold LH, Henriksen SJ, Siggins GR. 1999. Structural and functional neuropathology in transgenic mice with CNS expression of IFN-alpha. Brain Res 835:46-61.
31. Capra R, Sottini A, Cordioli C, Serana F, Chiarini M, Caimi L, Padovani A, Bergamaschi R, Imberti L. 2007. IFNbeta bioavailability in multiple sclerosis patients: MxA versus antibody-detecting assays. J Neuroimmunol 189:102-110.
32. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, Miller SD. 2005. Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49:360-374.
33. Chabot S, Williams G, Yong VW. 1997. Microglial production of TNF-alpha is induced by activated T lymphocytes. Involvement of VLA-4 and inhibition by interferonbeta-1b. J Clin Invest 100:604-612.
34. Chopy D, Detje CN, Lafage M, Kalinke U, Lafon M. 2011. The type I interferon response bridles rabies virus infection and reduces pathogenicity. J Neurovirol 17:353-367.
35. Christensen JE, Fenger C, Issazadeh-Navikas S, Krug A, Liljestrom P, Goriely S, Paludan SR, Finsen B, Christensen JP, Thomsen AR. 2012. Differential impact of interferon regulatory factor 7 in initiation of the type I interferon response in the lymphocytic choriomeningitis virus-infected central nervous system versus the periphery. J Virol 86:7384-7392.
36. Collins JM, Riccardi R, Trown P, O'Neill D, Poplack DG. 1985. Plasma and cerebrospinal fluid pharmacokinetics of recombinant interferon alpha A in monkeys: comparison of intravenous, intramuscular, and intraventricular delivery. Cancer Drug Deliv 2:247-253.
37. Costello DA, Lynch MA. 2013. Toll-like receptor 3 activation modulates hippocampal network excitability, via glial production of interferon-beta. Hippocampus 23:696-707.
38. Crow MK. 2007. Type I interferon in systemic lupus erythematosus. Curr Top Microbiol Immunol 316:359-386.
39. Crow YJ, Hayward BE, Parmar R, Robins P, Leitch A, Ali M, Black DN, van Bokhoven H, Brunner HG, Hamel BC, Corry PC, Cowan FM, Frints SG, Klepper J, Livingston JH, Lynch SA, Massey RF, Meritet JF, Michaud JL, Ponsot G, Voit T, Lebon P, Bonthron DT, Jackson AP, Barnes DE, Lindahl T. 2006a. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat Genet 38:917-920.
40. Crow YJ, Leitch A, Hayward BE, Garner A, Parmar R, Griffith E, Ali M, Semple C, Aicardi J, Babul-Hirji R, Baumann C, Baxter P, Bertini E, Chandler KE, Chitayat D, Cau D, Dery C, Fazzi E, Goizet C, King MD, Klepper J, Lacombe D, Lanzi G, Lyall H, Martinez-Frias ML, Mathieu M, McKeown C, Monier A, Oade Y, Quarrell OW, Rittey CD, Rogers RC, Sanchis A, Stephenson JB, Tacke U, Till M, Tolmie JL, Tomlin P, Voit T, Weschke B, Woods CG, Lebon P, Bonthron DT, Ponting CP, Jackson AP. 2006b. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat Genet 38:910-916.
41. Crow YJ, Rehwinkel J. 2009. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum Mol Genet 18:R130-R136.
42. de Rivero Vaccari JP, Minkiewicz J, Wang X, De Rivero Vaccari JC, German R, Marcillo AE, Dietrich WD, Keane RW. 2012. Astrogliosis involves activation of retinoic acid-inducible gene-like signaling in the innate immune response after spinal cord injury. Glia 60:414-421.
43. De Simone R, Levi G, Aloisi F. 1998. Interferon gamma gene expression in rat central nervous system glial cells. Cytokine 10:418-422.
44. de Weerd NA, Nguyen T. 2012. The interferons and their receptors-distribution and regulation. Immunol Cell Biol 90:483-491.
45. Delhaye S, Paul S, Blakqori G, Minet M, Weber F, Staeheli P, Michiels T. 2006. Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci USA 103:7835-7840.
46. Detje CN, Meyer T, Schmidt H, Kreuz D, Rose JK, Bechmann I, Prinz M, Kalinke U. 2009. Local type I IFN receptor signaling protects against virus spread within the central nervous system. J Immunol 182:2297-2304.
47. 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.
48. Durelli L, Bongioanni MR, Cavallo R, Ferrero B, Ferri R, Ferrio MF, Bradac GB, Riva A, Vai S, Geuna M, Bergamini L, Bergamasco B. 1994. Chronic systemic high-dose recombinant interferon alfa-2a reduces exacerbation rate, MRI signs of disease activity, and lymphocyte interferon gamma production in relapsing-remitting multiple sclerosis. Neurology 44:406-413.
49. Durelli L, Conti L, Clerico M, Boselli D, Contessa G, Ripellino P, Ferrero B, Eid P, Novelli F. 2009. T-helper 17 cells expand in multiple sclerosis and are inhibited by interferon-beta. Ann Neurol 65:499-509.
50. Farina C, Aloisi F, Meinl E. 2007. Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138-145.
51. Feng X, Reder NP, Yanamandala M, Hill A, Franek BS, Niewold TB, Reder AT, Javed A. 2012. Type I interferon signature is high in lupus and neuromyelitis optica but low in multiple sclerosis. J Neurol Sci 313:48-53.
52. Field R, Campion S, Warren C, Murray C, Cunningham C. 2010. Systemic challenge with the TLR3 agonist poly I:C induces amplified IFNalpha/beta and IL-1beta responses in the diseased brain and exacerbates chronic neurodegeneration. Brain Behav Immun 24:996-1007.
53. Finsen B, Owens T. 2011. Innate immune responses in central nervous system inflammation. FEBS Lett 585:3806-3812.
54. Fritz-French C, Tyor W. 2012. Interferon-alpha (IFNalpha) neurotoxicity. Cytokine Growth Factor Rev 23:7-14.
55. Furr SR, Chauhan VS, Moerdyk-Schauwecker MJ, Marriott I. 2011. A role for DNA-dependent activator of interferon regulatory factor in the recognition of herpes simplex virus type 1 by glial cells. J Neuroinflammation 8:99.
56. Furr SR, Chauhan VS, Sterka D Jr, Grdzelishvili V, Marriott I. 2008. Characterization of retinoic acid-inducible gene-I expression in primary murine glia following exposure to vesicular stomatitis virus. J Neurovirol 14:503-513.
57. Gaillard PJ, van Der Meide PH, de Boer AG, Breimer DD. 2001. Glucocorticoid and type 1 interferon interactions at the blood-brain barrier: relevance for drug therapies for multiple sclerosis. Neuroreport 12:2189-2193.
58. Galligan CL, Pennell LM, Murooka TT, Baig E, Majchrzak-Kita B, Rahbar R, Fish EN. 2010. Interferon-beta is a key regulator of proinflammatory events in experimental autoimmune encephalomyelitis. Mult Scler 16:1458-1473.
59. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, Sun L, Chen ZJ. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341:903-906.
60. Gao X, Gillig TA, Ye P, D'Ercole AJ, Matsushima GK, Popko B. 2000. Interferon-gamma protects against cuprizone-induced demyelination. Mol Cell Neurosci 16:338-349.
61. Gesuete R, Packard AE, Vartanian KB, Conrad VK, Stevens SL, Bahjat FR, Yang T, Stenzel-Poore MP. 2012. Poly-ICLC preconditioning protects the blood-brain barrier against ischemic injury in vitro through type I interferon signaling. J Neurochem 123 Suppl 2:75-85.
62. Gilli F. 2010. Role of differential expression of interferon receptor isoforms on the response of multiple sclerosis patients to therapy with interferon beta. J Interferon Cytokine Res 30:733-741.
63. Gresser I, Morel-Maroger L, Riviere Y, Guillon JC, Tovey MG, Woodrow D, Sloper JC, Moss J. 1980. Interferon-induced disease in mice and rats. Ann N Y Acad Sci 350:12-20.
64. Gris D, Ye Z, Iocca HA, Wen H, Craven RR, Gris P, Huang M, Schneider M, Miller SD, Ting JP. 2010. NLRP3 plays a critical role in the development of experimental autoimmune encephalomyelitis by mediating Th1 and Th17 responses. J Immunol 185:974-981.
65. Guo B, Chang EY, Cheng G. 2008. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J Clin Invest 118:1680-1690.
66. Hanke ML, Kielian T. 2011. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin Sci (Lond) 121:367-387.
67. Hartung HP, Kieseier BC. 2010. Atacicept: targeting B cells in multiple sclerosis. Ther Adv Neurol Disord 3:205-216.
68. Hindinger C, Bergmann CC, Hinton DR, Phares TW, Parra GI, Hussain S, Savarin C, Atkinson RD, Stohlman SA. 2012. IFN-gamma signaling to astrocytes protects from autoimmune mediated neurological disability. PLoS One 7:e42088.
69. Hofer MJ, Campbell IL. 2013. Type I interferon in neurological disease-the devil from within. Cytokine Growth Factor Rev 24:257-267.
70. Holm TH, Draeby D, Owens T. 2012. Microglia are required for astroglial toll-like receptor 4 response and for optimal TLR2 and TLR3 response. Glia 60:630-638.
71. Hosmane S, Tegenge MA, Rajbhandari L, Uapinyoying P, Kumar NG, Thakor N, Venkatesan A. 2012. Toll/interleukin-1 receptor domain-containing adapter inducing interferon-beta mediates microglial phagocytosis of degenerating axons. J Neurosci 32:7745-7757.
72. Hosokawa M, Klegeris A, Maguire J, McGeer PL. 2003. Expression of complement messenger RNAs and proteins by human oligodendroglial cells. Glia 42:417-423.
73. Inoue M, Williams KL, Oliver T, Vandenabeele P, Rajan JV, Miao EA, Shinohara ML. 2012. Interferon-beta therapy against EAE is effective only when development of the disease depends on the NLRP3 inflammasome. Sci Signal 5:ra38.
74. Isaacs A, Lindenmann J. 1957. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 147:258-267.
75. Isaksson M, Ardesjo B, Ronnblom L, Kampe O, Lassmann H, Eloranta ML, Lobell A. 2009. Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur J Immunol 39:2925-2935.
76. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. 2005. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175:4320-4330.
77. Jaitin DA, Roisman LC, Jaks E, Gavutis M, Piehler J, Van der Heyden J, Uze G, Schreiber G. 2006. Inquiring into the differential action of interferons (IFNs): an IFN-alpha2 mutant with enhanced affinity to IFNAR1 is functionally similar to IFN-beta. Mol Cell Biol 26:1888-1897.
78. Jin YH, Kim SJ, So EY, Meng L, Colonna M, Kim BS. 2012. Melanoma differentiation-associated gene 5 is critical for protection against Theiler's virus-induced demyelinating disease. J Virol 86:1531-1543.
79. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 9:361-368.
80. Kalie E, Jaitin DA, Podoplelova Y, Piehler J, Schreiber G. 2008. The stability of the ternary interferon-receptor complex rather than the affinity to the individual subunits dictates differential biological activities. J Biol Chem 283:32925-32936.
81. Kallfass C, Ackerman A, Lienenklaus S, Weiss S, Heimrich B, Staeheli P. 2012. Visualizing production of beta interferon by astrocytes and microglia in brain of la crosse virus-infected mice. J Virol 86:11223-11230.
82. Kapil P, Butchi NB, Stohlman SA, Bergmann CC. 2012. Oligodendroglia are limited in type I interferon induction and responsiveness in vivo. Glia 60:1555-1566.
83. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373-384.
84. Kawamata T, Akiyama H, Yamada T, McGeer PL. 1992. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol 140:691-707.
85. Kawanokuchi J, Mizuno T, Takeuchi H, Kato H, Wang J, Mitsuma N, Suzumura A. 2006. Production of interferon-gamma by microglia. Mult Scler 12:558-564.
86. Khorooshi R, Owens T. 2010. Injury-induced Type I IFN signaling regulates inflammatory responses in the central nervous system. J Immunol 185:1258-1264.
87. Khorooshi R, Wlodarczyk A, Asgari N, Owens T. 2013. Neuromyelitis optica-like pathology is dependent on type I interferon response. Exp Neurol 247:744-747.
88. Kiefer R, Haas CA, Kreutzberg GW. 1991. Gamma interferon-like immunoreactive material in rat neurons: evidence against a close relationship to gamma interferon. Neuroscience 45:551-560.
89. Kim MY, Shu Y, Carsillo T, Zhang J, Yu L, Peterson C, Longhi S, Girod S, Niewiesk S, Oglesbee M. 2013. hsp70 and a novel axis of type I interferon-dependent antiviral immunity in the measles virus-infected brain. J Virol 87:998-1009.
90. Kim SH, Kim W, Li XF, Jung IJ, Kim HJ. 2012. Does interferon beta treatment exacerbate neuromyelitis optica spectrum disorder? Mult Scler 18:1480-1483.
91. Kim SS, Richman DP, Zamvil SS, Agius MA. 2011. Accelerated central nervous system autoimmunity in BAFF-receptor-deficient mice. J Neurol Sci 306:9-15.
92. Kirou KA, Lee C, George S, Louca K, Peterson MG, Crow MK. 2005. Activation of the interferon-alpha pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum 52:1491-1503.
93. Knobler RL, Panitch HS, Braheny SL, Sipe JC, Rice GP, Huddlestone JR, Francis GS, Hooper CK, Kamin-Lewis RM, Johnson KP, Oldstone MBA, Merigan TC. 1984. Systemic alpha-interferon therapy of multiple sclerosis. Neurology 34:1273-1279.
94. Kraus J, Ling AK, Hamm S, Voigt K, Oschmann P, Engelhardt B. 2004. Interferon-beta stabilizes barrier characteristics of brain endothelial cells in vitro. Ann Neurol 56:192-205.
95. Krumbholz M, Faber H, Steinmeyer F, Hoffmann LA, Kumpfel T, Pellkofer H, Derfuss T, Ionescu C, Starck M, Hafner C, Hohlfeld R, Meinl E. 2008. Interferon-beta increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain 131:1455-1463.
96. Kumaran J, Wei L, Kotra LP, Fish EN. 2007. A structural basis for interferon-alpha-receptor interactions. FASEB J 21:3288-3296.
97. Lande R, Gafa V, Serafini B, Giacomini E, Visconti A, Remoli ME, Severa M, Parmentier M, Ristori G, Salvetti M, Aloisi F, Coccia EM. 2008. Plasmacytoid dendritic cells in multiple sclerosis: intracerebral recruitment and impaired maturation in response to interferon-beta. J Neuropathol Exp Neurol 67:388-401.
98. Larsen PH, Holm TH, Owens T. 2007. Toll-like receptors in brain development and homeostasis. Sci STKE 2007:pe47.
99. Lebon P, Badoual J, Ponsot G, Goutieres F, Hemeury-Cukier F, Aicardi J. 1988. Intrathecal synthesis of interferon-alpha in infants with progressive familial encephalopathy. J Neurol Sci 84:201-208.
100. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. 2005. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202:473-477.
101. Levin D, Harari D, Schreiber G. 2011. Stochastic receptor expression determines cell fate upon interferon treatment. Mol Cell Biol 31:3252-3266.
102. Levy DE, Marie IJ, Durbin JE. 2011. Induction and function of type I and III interferon in response to viral infection. Curr Opin Virol 1:476-486.
103. Leyva L, Fernandez O, Fedetz M, Blanco E, Fernandez VE, Oliver B, Leon A, Pinto-Medel MJ, Mayorga C, Guerrero M, Luque G, Alcina A, Matesanz F. 2005. IFNAR1 and IFNAR2 polymorphisms confer susceptibility to multiple sclerosis but not to interferon-beta treatment response. J Neuroimmunol 163:165-171.
104. Li J, Hu S, Zhou L, Ye L, Wang X, Ho J, Ho W. 2011. Interferon lambda inhibits herpes simplex virus type I infection of human astrocytes and neurons. Glia 59:58-67.
105. Li J, Liu Y, Zhang X. 2010. Murine coronavirus induces type I interferon in oligodendrocytes through recognition by RIG-I and MDA5. J Virol 84:6472-6482.
106. Longhini AL, von Glehn F, Brandao CO, de Paula RF, Pradella F, Moraes AS, Farias AS, Oliveira EC, Quispe-Cabanillas JG, Abreu CH, Damasceno A, Damasceno BP, Balashov KE, Santos LM. 2011. Plasmacytoid dendritic cells are increased in cerebrospinal fluid of untreated patients during multiple sclerosis relapse. J Neuroinflammation 8:2.
107. Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Ronnblom L, Sturfelt G, Eloranta ML, Bengtsson AA. 2009. C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 60:3081-3090.
108. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM, Trebst C, Weinshenker B, Wingerchuk D, Parisi JE, Lassmann H. 2002. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125:1450-1461.
109. Marta M. 2009. Toll-like receptors in multiple sclerosis mouse experimental models. Ann N Y Acad Sci 1173:458-462.
110. Marta M, Andersson A, Isaksson M, Kampe O, Lobell A. 2008. Unexpected regulatory roles of TLR4 and TLR9 in experimental autoimmune encephalomyelitis. Eur J Immunol 38:565-575.
111. Marta M, Meier UC, Lobell A. 2009. Regulation of autoimmune encephalomyelitis by toll-like receptors. Autoimmun Rev 8:506-509.
112. McKimmie CS, Fazakerley JK. 2005. In response to pathogens, glial cells dynamically and differentially regulate Toll-like receptor gene expression. J Neuroimmunol 169:116-125.
113. McKimmie CS, Johnson N, Fooks AR, Fazakerley JK. 2005. Viruses selectively upregulate Toll-like receptors in the central nervous system. Biochem Biophys Res Commun 336:925-933.
114. Mero IL, Lorentzen AR, Ban M, Smestad C, Celius EG, Aarseth JH, Myhr KM, Link J, Hillert J, Olsson T, Kockum I, Masterman T, Oturai AB, Sondergaard HB, Sellebjerg F, Saarela J, Kemppinen A, Elovaara I, Spurkland A, Dudbridge F, Lie BA, Harbo HF. 2010. A rare variant of the TYK2 gene is confirmed to be associated with multiple sclerosis. Eur J Hum Genet 18:502-504.
115. Miyatake Y, Ikeda H, Ishizu A, Baba T, Ichihashi T, Suzuki A, Tomaru U, Kasahara M, Yoshiki T. 2006. Role of neuronal interferon-gamma in the development of myelopathy in rats infected with human T-cell leukemia virus type 1. Am J Pathol 169:189-199.
116. Mujtaba MG, Streit WJ, Johnson HM. 1998. IFN-tau suppresses both the autoreactive humoral and cellular immune responses and induces stable remission in mice with chronic experimental allergic encephalomyelitis. Cell Immunol 186:94-102.
117. Nagano Y, Kojima Y. 1958. Inhibition of vaccinia infection by a liquid factor in tissues infected by homologous virus. C R Seances Soc Biol Fil 152:1627-1629.
118. Naves R, Singh SP, Cashman KS, Rowse AL, Axtell RC, Steinman L, Mountz JD, Steele C, De Sarno P, Raman C. 2013. The interdependent, overlapping, and differential roles of type i and ii ifns in the pathogenesis of experimental autoimmune encephalomyelitis. J Immunol 191:2967-2977.
119. Nishiyama S, Ito T, Misu T, Takahashi T, Kikuchi A, Suzuki N, Jin K, Aoki M, Fujihara K, Itoyama Y. 2009. A case of NMO seropositive for aquaporin-4 antibody more than 10 years before onset. Neurology 72:1960-1961.
120. Okada K, Kuroda E, Yoshida Y, Yamashita U, Suzumura A, Tsuji S. 2005. Effects of interferon-beta on the cytokine production of astrocytes. J Neuroimmunol 159:48-54.
121. Ousman SS, Wang J, Campbell IL. 2005. Differential regulation of interferon regulatory factor (IRF)-7 and IRF-9 gene expression in the central nervous system during viral infection. J Virol 79:7514-7527.
122. Owens T, Bechmann I, Engelhardt B. 2008. Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 67:1113-1121.
123. Ozato K, Uno K, Iwakura Y. 2007. Another road to interferon: Yasuichi Nagano's journey. J Interferon Cytokine Res 27:349-352.
124. Palace J, Leite MI, Nairne A, Vincent A. 2010. Interferon Beta treatment in neuromyelitis optica: increase in relapses and aquaporin 4 antibody titers. Arch Neurol 67:1016-1017.
125. Palma JP, Kwon D, Clipstone NA, Kim BS. 2003. Infection with Theiler's murine encephalomyelitis virus directly induces proinflammatory cytokines in primary astrocytes via NF-kappaB activation: potential role for the initiation of demyelinating disease. J Virol 77:6322-6331.
126. Pashenkov M, Huang YM, Kostulas V, Haglund M, Soderstrom M, Link H. 2001. Two subsets of dendritic cells are present in human cerebrospinal fluid. Brain 124:480-492.
127. Peltier DC, Simms A, Farmer JR, Miller DJ. 2010. Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J Immunol 184:7010-7021.
128. Pestka S, Krause CD, Walter MR. 2004. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202:8-32.
129. Platanias LC. 2005. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5:375-386.
130. Prat A, Biernacki K, Wosik K, Antel JP. 2001. Glial cell influence on the human blood-brain barrier. Glia 36:145-155.
131. Prehaud C, Megret F, Lafage M, Lafon M. 2005. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 79:12893-12904.
132. Prinz M, Schmidt H, Mildner A, Knobeloch KP, Hanisch UK, Raasch J, Merkler D, Detje C, Gutcher I, Mages J, Lang R, Martin R, Gold R, Becher B, Bruck W, Kalinke U. 2008. Distinct and nonredundant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system. Immunity 28:675-686.
133. Prokunina-Olsson L, Muchmore B, Tang W, Pfeiffer RM, Park H, Dickensheets H, Hergott D, Porter-Gill P, Mumy A, Kohaar I, Chen S, Brand N, Tarway M, Liu L, Sheikh F, Astemborski J, Bonkovsky HL, Edlin BR, Howell CD, Morgan TR, Thomas DL, Rehermann B, Donnelly RP, O'Brien TR, and others. 2013. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat Genet 45:164-71.
134. Ragimbeau J, Dondi E, Alcover A, Eid P, Uze G, Pellegrini S. 2003. The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression. EMBO J 22:537-547.
135. Raison CL, Borisov AS, Majer M, Drake DF, Pagnoni G, Woolwine BJ, Vogt GJ, Massung B, Miller AH. 2009. Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression. Biol Psychiatry 65:296-303.
136. Rho MB, Wesselingh S, Glass JD, McArthur JC, Choi S, Griffin J, Tyor WR. 1995. A potential role for interferon-alpha in the pathogenesis of HIV-associated dementia. Brain Behav Immun 9:366-377.
137. Ricklin D, Hajishengallis G, Yang K, Lambris JD. 2010. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11:785-797.
138. Rivieccio MA, John GR, Song X, Suh HS, Zhao Y, Lee SC, Brosnan CF. 2005. The cytokine IL-1beta activates IFN response factor 3 in human fetal astrocytes in culture. J Immunol 174:3719-3726.
139. Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W, Mandler RN, Weinshenker BG, Pittock SJ, Wingerchuk DM, Lucchinetti CF. 2007. Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 130:1194-1205.
140. Ross TM, Martinez PM, Renner JC, Thorne RG, Hanson LR, Frey WH IInd. 2004. Intranasal administration of interferon beta bypasses the blood-brain barrier to target the central nervous system and cervical lymph nodes: a non-invasive treatment strategy for multiple sclerosis. J Neuroimmunol 151:66-77.
141. Roth-Cross JK, Bender SJ, Weiss SR. 2008. Murine coronavirus mouse hepatitis virus is recognized by MDA5 and induces type I interferon in brain macrophages/microglia. J Virol 82:9829-9838.
142. Rubio N, Palomo M, Alcami A. 2010. Interferon-alpha/beta genes are up-regulated in murine brain astrocytes after infection with Theiler's murine encephalomyelitis virus. J Interferon Cytokine Res 30:253-262.
143. Rutherford MN, Hannigan GE, Williams BR. 1988. Interferon-induced binding of nuclear factors to promoter elements of the 2-5A synthetase gene. EMBO J 7:751-759.
144. Saadoun S, Waters P, Bell BA, Vincent A, Verkman AS, Papadopoulos MC. 2010. Intra-cerebral injection of neuromyelitis optica immunoglobulin G and human complement produces neuromyelitis optica lesions in mice. Brain 133:349-361.
145. Sakaguchi T, Irie T, Kawabata R, Yoshida A, Maruyama H, Kawakami H. 2011. Optineurin with amyotrophic lateral sclerosis-related mutations abrogates inhibition of interferon regulatory factor-3 activation. Neurosci Lett 505:279-281.
146. Salem M, Mony JT, Lobner M, Khorooshi R, Owens T. 2011. Interferon regulatory factor-7 modulates experimental autoimmune encephalomyelitis in mice. J Neuroinflammation 8:181-189.
147. Santer DM, Yoshio T, Minota S, Moller T, Elkon KB. 2009. Potent induction of IFN-alpha and chemokines by autoantibodies in the cerebrospinal fluid of patients with neuropsychiatric lupus. J Immunol 182:1192-1201.
148. Schindler C, Levy DE, Decker T. 2007. JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282:20059-20063.
149. Schindler C, Plumlee C. 2008. Inteferons pen the JAK-STAT pathway. Semin Cell Dev Biol 19:311-318.
150. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485.
151. Severa M, Remoli ME, Giacomini E, Ragimbeau J, Lande R, Uze G, Pellegrini S, Coccia EM. 2006. Differential responsiveness to IFN-alpha and IFN-beta of human mature DC through modulation of IFNAR expression. J Leukoc Biol 79:1286-1294.
152. Shaw PJ, Lukens JR, Burns S, Chi H, McGargill MA, Kanneganti TD. 2010. Cutting edge: critical role for PYCARD/ASC in the development of experimental autoimmune encephalomyelitis. J Immunol 184:4610-4614.
153. Shiozawa S, Kuroki Y, Kim M, Hirohata S, Ogino T. 1992. Interferon-alpha in lupus psychosis. Arthritis Rheum 35:417-422.
154. So EY, Kang MH, Kim BS. 2006. Induction of chemokine and cytokine genes in astrocytes following infection with Theiler's murine encephalomyelitis virus is mediated by the Toll-like receptor 3. Glia 53:858-867.
155. Sommereyns C, Paul S, Staeheli P, Michiels T. 2008. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4:e1000017.
156. Sorgeloos F, Kreit M, Hermant P, Lardinois C, Michiels T. 2013. Antiviral type I and type III interferon responses in the central nervous system. Viruses 5:834-857.
157. Spach KM, Noubade R, McElvany B, Hickey WF, Blankenhorn EP, Teuscher C. 2009. A single nucleotide polymorphism in Tyk2 controls susceptibility to experimental allergic encephalomyelitis. J Immunol 182:7776-7783.
158. Staeheli P, Danielson P, Haller O, Sutcliffe JG. 1986. Transcriptional activation of the mouse Mx gene by type I interferon. Mol Cell Biol 6:4770-4774.
159. Stone LA, Frank JA, Albert PS, Bash CN, Calabresi PA, Maloni H, McFarland HF. 1997. Characterization of MRI response to treatment with interferon beta-1b: contrast-enhancing MRI lesion frequency as a primary outcome measure. Neurology 49:862-869.
160. Taniguchi T, Takaoka A. 2001. A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol 2:378-386.
161. Tarassishin L, Suh HS, Lee SC. 2011. Interferon regulatory factor 3 plays an anti-inflammatory role in microglia by activating the PI3K/Akt pathway. J Neuroinflammation 8:187.
162. Tedeschi B, Barrett JN, Keane RW. 1986. Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells. J Cell Biol 102:2244-2253.
163. Teige I, Treschow A, Teige A, Mattsson R, Navikas V, Leanderson T, Holmdahl R, Issazadeh-Navikas S. 2003. IFN-beta gene deletion leads to augmented and chronic demyelinating experimental autoimmune encephalomyelitis. J Immunol 170:4776-4784.
164. Theis M, Giaume C. 2012. Connexin-based intercellular communication and astrocyte heterogeneity. Brain Res 1487:88-98.
165. Theofilopoulos AN, Baccala R, Beutler B, Kono DH. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23:307-336.
166. Thomas C, Moraga I, Levin D, Krutzik PO, Podoplelova Y, Trejo A, Lee C, Yarden G, Vleck SE, Glenn JS, Nolan GP, Piehler J, Schreiber G, Garcia KC. 2011. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146:621-632.
167. Tomizawa Y, Yokoyama K, Saiki S, Takahashi T, Matsuoka J, Hattori N. 2012. Blood-brain barrier disruption is more severe in neuromyelitis optica than in multiple sclerosis and correlates with clinical disability. J Int Med Res 40:1483-1491.
168. Town T, Jeng D, Alexopoulou L, Tan J, Flavell RA. 2006. Microglia recognize double-stranded RNA via TLR3. J Immunol 176:3804-3812.
169. Traugott U, Lebon P. 1988. Multiple sclerosis: involvement of interferons in lesion pathogenesis. Ann Neurol 24:243-251.
170. Trysberg E, Nylen K, Rosengren LE, Tarkowski A. 2003. Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum 48:2881-2887.
171. van Heteren JT, Rozenberg F, Aronica E, Troost D, Lebon P, Kuijpers TW. 2008. Astrocytes produce interferon-alpha and CXCL10, but not IL-6 or CXCL8, in Aicardi-Goutieres syndrome. Glia 56:568-578.
172. Veerhuis R, Janssen I, De Groot CJ, Van Muiswinkel FL, Hack CE, Eikelenboom P. 1999. Cytokines associated with amyloid plaques in Alzheimer's disease brain stimulate human glial and neuronal cell cultures to secrete early complement proteins, but not C1-inhibitor. Exp Neurol 160:289-299.
173. Veldhuis WB, Floris S, van der Meide PH, Vos IM, de Vries HE, Dijkstra CD, Bar PR, Nicolay K. 2003. Interferon-beta prevents cytokine-induced neutrophil infiltration and attenuates blood-brain barrier disruption. J Cereb Blood Flow Metab 23:1060-1069.
174. Villalba M, Hott M, Martin C, Aguila B, Valdivia S, Quezada C, Zambrano A, Concha MI, Otth C. 2012. Herpes simplex virus type 1 induces simultaneous activation of Toll-like receptors 2 and 4 and expression of the endogenous ligand serum amyloid A in astrocytes. Med Microbiol Immunol 201:371-379.
175. Wang J, Campbell IL, Zhang H. 2008. Systemic interferon-alpha regulates interferon-stimulated genes in the central nervous system. Mol Psychiatry 13:293-301.
176. Wang R, Yang B, Zhang D. 2011. Activation of interferon signaling pathways in spinal cord astrocytes from an ALS mouse model. Glia 59:946-958.
177. Ward LA, Massa PT. 1995. Neuron-specific regulation of major histocompatibility complex class I, interferon-beta, and anti-viral state genes. J Neuroimmunol 58:145-155.
178. Weinshenker BG, Wingerchuk DM, Pittock SJ, Lucchinetti CF, Lennon VA. 2006. NMO-IgG: a specific biomarker for neuromyelitis optica. Dis Markers 22:197-206.
179. Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. 2007. The spectrum of neuromyelitis optica. Lancet Neurol 6:805-815.
180. Witwer KW, Gama L, Li M, Bartizal CM, Queen SE, Varrone JJ, Brice AK, Graham DR, Tarwater PM, Mankowski JL, Zink MC, Clements JE. 2009. Coordinated regulation of SIV replication and immune responses in the CNS. PLoS One 4:e8129.
181. Xu L, Yang L, Liu W. 2013. Distinct evolution process among type I interferon in mammals. Protein Cell 4:383-392.
182. Yamada T, Horisberger MA, Kawaguchi N, Moroo I, Toyoda T. 1994. Immunohistochemistry using antibodies to alpha-interferon and its induced protein, MxA, in Alzheimer's and Parkinson's disease brain tissues. Neurosci Lett 181:61-64.
183. Yu M, Nishiyama A, Trapp BD, Tuohy VK. 1996. Interferon-beta inhibits progression of relapsing-remitting experimental autoimmune encephalomyelitis. J Neuroimmunol 64:91-100.
184. Zhou L, Wang X, Wang YJ, Zhou Y, Hu S, Ye L, Hou W, Li H, Ho WZ. 2009. Activation of toll-like receptor-3 induces interferon-lambda expression in human neuronal cells. Neuroscience 159:629-637.