Induction of endogenous Type I interferon within the central nervous system plays a protective role in experimental autoimmune encephalomyelitis

Acta Neuropathologica

Volumn 130, Issue 1, 2015, Pages 107-118

  Khorooshi, Reza ^a   Mørch, Marlene Thorsen ^a   Holm, Thomas Hellesøe ^a,b   Berg, Carsten Tue ^a   Dieu, Ruthe Truong ^a   Dræby, Dina ^a   Issazadeh Navikas, Shohreh ^c   Weiss, Siegfried ^d   Lienenklaus, Stefan ^d   Owens, Trevor ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

EAE; Interferon alpha; Interferon beta; Macrophages; Microglia; Poly I:C

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD11B ANTIGEN; CD45 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 10; INTERLEUKIN 17; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYINOSINIC POLYCYTIDYLIC ACID; ALPHA BETA INTERFERON RECEPTOR; CXCL10 PROTEIN, MOUSE; IFNAR1 PROTEIN, MOUSE; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL INFILTRATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CHOROID PLEXUS; CISTERNA MAGNA; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; INTERFERON PRODUCTION; LEUKOCYTE COUNT; MENINX; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETICS; IMMUNOLOGY; LEUKOCYTE; METABOLISM; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SPINAL CORD; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BRAIN; CHEMOKINE CXCL10; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INTERFERON-ALPHA; INTERFERON-BETA; LEUKOCYTES; MENINGES; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEUROPROTECTIVE AGENTS; POLY I-C; RANDOM ALLOCATION; RECEPTOR, INTERFERON ALPHA-BETA; SPINAL CORD;

EID: 84931264040     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-015-1418-z     Document Type: Article

References (39)

1. Asgari N, Khorooshi R, Lillevang ST, Owens T (2013) Complement-dependent pathogenicity of brain-specific antibodies in cerebrospinal fluid. J Neuroimmunol 254:76–82. doi:10.1016/j.jneuroim.2012.09.010
2. Babcock AA, Kuziel WA, Rivest S, Owens T (2003) Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 23:7922–7930
3. Benveniste EN, Qin H (2007) Type I interferons as anti-inflammatory mediators. Sci STKE 2007:pe70. doi:10.1126/stke.4162007pe70
4. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, Kuchroo VK (1998) IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 161:3299–3306
5. Cedile O, Lobner M, Toft-Hansen H, Frank I, Wlodarczyk A, Irla M, Owens T (2014) Thymic CCL2 influences induction of T-cell tolerance. J Autoimmun 55:73–85. doi:10.1016/j.jaut.2014.07.004
6. Chang EY, Guo B, Doyle SE, Cheng G (2007) Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J Immunol 178:6705–6709
7. Dann A, Poeck H, Croxford AL, Gaupp S, Kierdorf K, Knust M, Pfeifer D, Maihoefer C, Endres S, Kalinke U et al (2012) Cytosolic RIG-I-like helicases act as negative regulators of sterile inflammation in the CNS. Nat Neurosci 15:98–106. doi:10.1038/nn.2964
8. Deonarain R, Alcami A, Alexiou M, Dallman MJ, Gewert DR, Porter AC (2000) Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J Virol 74:3404–3409
9. Elhofy A, Wang J, Tani M, Fife BT, Kennedy KJ, Bennett J, Huang D, Ransohoff RM, Karpus WJ (2005) Transgenic expression of CCL2 in the central nervous system prevents experimental autoimmune encephalomyelitis. J Leukoc Biol 77:229–237
10. Erlandsson L, Blumenthal R, Eloranta ML, Engel H, Alm G, Weiss S, Leanderson T (1998) Interferon-beta is required for interferon-alpha production in mouse fibroblasts. Curr Biol 8:223–226
11. Furlan R, Pluchino S, Marconi PC, Martino G (2003) Cytokine gene delivery into the central nervous system using intrathecally injected nonreplicative viral vectors. Methods Mol Biol 215:279–289
12. 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. doi:10.1172/JCI33342
13. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387–1394
14. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N et al (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434:772–777. doi:10.1038/nature03464
15. Huang D, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713–726
16. 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. doi:10.1128/JVI.01093-12
17. Khorooshi R, Owens T (2013) Detection and cellular localization of phospho-STAT2 in the central nervous system by immunohistochemical staining. Methods Mol Biol 967:179–188. doi:10.1007/978-1-62703-242-1_13
18. Khorooshi R, Owens T (2010) Injury-induced type I IFN signaling regulates inflammatory responses in the central nervous system. J Immunol 185:1258–1264. doi:10.4049/jimmunol.0901753
19. Kong Y, Le Y (2011) Toll-like receptors in inflammation of the central nervous system. Int Immunopharmacol 11:1407–1414. doi:10.1016/j.intimp.2011.04.025
20. Kwilasz AJ, Grace PM, Serbedzija P, Maier SF, Watkins LR (2014) The therapeutic potential of interleukin-10 in neuroimmune diseases. Neuropharmacology. doi:10.1016/j.neuropharm.2014.10.020
21. Lienenklaus S, Cornitescu M, Zietara N, Lyszkiewicz M, Gekara N, Jablonska J, Edenhofer F, Rajewsky K, Bruder D, Hafner M et al (2009) Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol 183:3229–3236. doi:10.4049/jimmunol.0804277
22. Mahad DJ, Ransohoff RM (2003) The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 15:23–32
23. Martino G, Furlan R, Comi G, Adorini L (2001) The ependymal route to the CNS: an emerging gene-therapy approach for MS. Trends Immunol 22:483–490
24. Mills Ko E, Ma JH, Guo F, Miers L, Lee E, Bannerman P, Burns T, Ko D, Sohn J, Soulika AM et al (2014) Deletion of astroglial CXCL10 delays clinical onset but does not affect progressive axon loss in a murine autoimmune multiple sclerosis model. J Neuroinflammation 11:105. doi:10.1186/1742-2094-11-105
25. Millward JM, Lobner M, Wheeler RD, Owens T (2010) Inflammation in the central nervous system and Th17 responses are inhibited by IFN-{gamma}-induced IL-18 binding protein. J Immunol 185:2458–2466. doi:10.4049/jimmunol.0902153
26. Mony JT, Khorooshi R, Owens T (2014) MOG extracellular domain (p1-125) triggers elevated frequency of CXCR3+ CD4+ Th1 cells in the CNS of mice and induces greater incidence of severe EAE. Mult Scler 20:1312–1321. doi:10.1177/1352458514524086
27. Muller M, Carter S, Hofer MJ, Campbell IL (2010) Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity–a tale of conflict and conundrum. Neuropathol Appl Neurobiol 36:368–387. doi:10.1111/j.1365-2990.2010.01089.x
28. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M (1994) Functional role of type I and type II interferons in antiviral defense. Science 264:1918–1921
29. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72–86
30. Owens T, Khorooshi R, Wlodarczyk A, Asgari N (2014) Interferons in the central nervous system: a few instruments play many tunes. Glia 62:339–355. doi:10.1002/glia.22608
31. Prinz M, Schmidt H, Mildner A, Knobeloch KP, Hanisch UK, Raasch J, Merkler D, Detje C, Gutcher I, Mages J et al (2008) Distinct and nonredundant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system. Immunity 28:675–686. doi:10.1016/j.immuni.2008.03.011
32. 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. doi:10.1186/1742-2094-8-181
33. Scheu S, Dresing P, Locksley RM (2008) Visualization of IFNbeta production by plasmacytoid versus conventional dendritic cells under specific stimulation conditions in vivo. Proc Natl Acad Sci 105:20416–20421. doi:10.1073/pnas.0808537105
34. Simmons SB, Pierson ER, Lee SY, Goverman JM (2013) Modeling the heterogeneity of multiple sclerosis in animals. Trends Immunol 34:410–422. doi:10.1016/j.it.2013.04.006
35. 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
36. Touil T, Fitzgerald D, Zhang GX, Rostami A, Gran B (2006) Cutting edge: TLR3 stimulation suppresses experimental autoimmune encephalomyelitis by inducing endogenous IFN-beta. J Immunol 177:7505–7509 (pii: 177/11/7505)
37. Tzima S, Victoratos P, Kranidioti K, Alexiou M, Kollias G (2009) Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. J Exp Med 206:1167–1179. doi:10.1084/jem.20081582
38. Yu M, Levine SJ (2011) Toll-like receptor, RIG-I-like receptors and the NLRP3 inflammasome: key modulators of innate immune responses to double-stranded RNA viruses. Cytokine Growth Factor Rev 22:63–72. doi:10.1016/j.cytogfr.2011.02.001
39. Zhang L, Yuan S, Cheng G, Guo B (2011) Type I IFN promotes IL-10 production from T cells to suppress Th17 cells and Th17-associated autoimmune inflammation. PLoS One 6:e28432. doi:10.1371/journal.pone.0028432