The interdependent, overlapping, and differential roles of type i and II IFNs in the pathogenesis of experimental autoimmune encephalomyelitis

Journal of Immunology

Volumn 191, Issue 6, 2013, Pages 2967-2977

  Naves, Rodrigo ^a,e   Singh, Simer P ^a,f   Cashman, Kevin S ^b   Rowse, Amber L ^b   Axtell, Robert C ^c   Steinman, Lawrence ^c   Mountz, John D ^a   Steele, Chad ^a,b   De Sarno, Patrizia ^d   Raman, Chander ^a,b  

^a The University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^f UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; GAMMA INTERFERON; INTERFERON;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE SEVERITY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL;

ADOPTIVE TRANSFER; ANIMALS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE I; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; TH17 CELLS;

EID: 84884239709     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300419     Document Type: Article

References (71)

1. Borden, E. C., G. C. Sen, G. Uze, R. H. Silverman, R. M. Ransohoff, G. R. Foster, and G. R. Stark. 2007. Interferons at age 50: past, current and future impact on biomedicine. Nat. Rev. Drug Discov. 6: 975-990.
2. Farrar, M. A., and R. D. Schreiber. 1993. The molecular cell biology of interferon-g and its receptor. Annu. Rev. Immunol. 11: 571-611.
3. Theofilopoulos, A. N., R. Baccala, B. Beutler, and D. H. Kono. 2005. Type I interferons (a/b) in immunity and autoimmunity. Annu. Rev. Immunol. 23: 307-336.
4. Pace, J. L. 1988. Synergistic interactions between IFN-g and IFN-b in priming murine macrophages for tumor cell killing. J. Leukoc. Biol. 44: 514-520.
5. Dezfouli, S., I. Hatzinisiriou, and S. J. Ralph. 2003. Enhancing CTL responses to melanoma cell vaccines in vivo: synergistic increases obtained using IFNg primed and IFNb treated B7-1+ B16-F10 melanoma cells. Immunol. Cell Biol. 81: 459-471.
6. Peng, T., J. Zhu, Y. Hwangbo, L. Corey, and R. E. Bumgarner. 2008. Independent and cooperative antiviral actions of b interferon and g interferon against herpes simplex virus replication in primary human fibroblasts. J. Virol. 82: 1934-1945.
7. Gough, D. J., N. L. Messina, L. Hii, J. A. Gould, K. Sabapathy, A. P. Robertson, J. A. Trapani, D. E. Levy, P. J. Hertzog, C. J. Clarke, and R. W. Johnstone. 2010. Functional crosstalk between type I and II interferon through the regulated expression of STAT1. PLoS Biol. 8: e1000361.
8. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-g and-a/b signaling components in caveolar membrane domains. Science 288: 2357-2360.
9. Compston, A., and A. Coles. 2002. Multiple sclerosis. Lancet 359: 1221-1231.
10. Guo, B., E. Y. Chang, and G. Cheng. 2008. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J. Clin. Invest. 118: 1680-1690.
11. Prinz, M., H. Schmidt, A. Mildner, K. P. Knobeloch, U. K. Hanisch, J. Raasch, D. Merkler, C. Detje, I. Gutcher, J. Mages, 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.
12. Teige, I., A. Treschow, A. Teige, R. Mattsson, V. Navikas, T. Leanderson, R. Holmdahl, and S. Issazadeh-Navikas. 2003. IFN-b gene deletion leads to augmented and chronic demyelinating experimental autoimmune encephalomyelitis. J. Immunol. 170: 4776-4784.
13. Giovannoni, G., and D. H. Miller. 1999. Multiple sclerosis and its treatment. J. R. Coll. Physicians Lond. 33: 315-322.
14. Markowitz, C. E. 2007. Interferon-b: mechanism of action and dosing issues. Neurology 68(24, Suppl. 4): S8-S11.
15. Panitch, H. S. 1995. Early treatment trials with interferon b in multiple sclerosis. Mult. Scler. 1(Suppl. 1): S17-S21.
16. Tourbah, A., and O. Lyon-Caen. 2007. Interferons in multiple sclerosis: ten years' experience. Biochimie 89: 899-902.
17. Brosnan, C. F., B. Cannella, L. Battistini, and C. S. Raine. 1995. Cytokine localization in multiple sclerosis lesions: correlation with adhesion molecule expression and reactive nitrogen species. Neurology 45(6, Suppl. 6): S16-S21.
18. Olsson, T. 1992. Cytokines in neuroinflammatory disease: role of myelin autoreactive T cell production of interferon-gamma. J. Neuroimmunol. 40: 211-218.
19. Renno, T., J. Y. Lin, C. Piccirillo, J. Antel, and T. Owens. 1994. Cytokine production by cells in cerebrospinal fluid during experimental allergic encephalomyelitis in SJL/J mice. J. Neuroimmunol. 49: 1-7.
20. Renno, T., V. Taupin, L. Bourbonnière, G. Verge, E. Tran, R. De Simone, M. Krakowski, M. Rodriguez, A. Peterson, and T. Owens. 1998. Interferon-g in progression to chronic demyelination and neurological deficit following acute EAE. Mol. Cell. Neurosci. 12: 376-389.
21. Ferber, I. A., S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C. G. Fathman. 1996. Mice with a disrupted IFN-g gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156: 5-7.
22. Krakowski, M., and T. Owens. 1996. Interferon-g confers resistance to experimental allergic encephalomyelitis. Eur. J. Immunol. 26: 1641-1646.
23. Willenborg, D. O., S. Fordham, C. C. Bernard, W. B. Cowden, and I. A. Ramshaw. 1996. IFN-g plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157: 3223-3227.
24. Billiau, A., H. Heremans, F. Vandekerckhove, R. Dijkmans, H. Sobis, E. Meulepas, and H. Carton. 1988. Enhancement of experimental allergic encephalomyelitis in mice by antibodies against IFN-g. J. Immunol. 140: 1506-1510.
25. Duong, T. T., J. St Louis, J. J. Gilbert, F. D. Finkelman, and G. H. Strejan. 1992. Effect of anti-interferon-g and anti-interleukin-2 monoclonal antibody treatment on the development of actively and passively induced experimental allergic encephalomyelitis in the SJL/J mouse. J. Neuroimmunol. 36: 105-115.
26. Lublin, F. D., R. L. Knobler, B. Kalman, M. Goldhaber, J. Marini, M. Perrault, C. D'Imperio, J. Joseph, S. S. Alkan, and R. Korngold. 1993. Monoclonal anti-g interferon antibodies enhance experimental allergic encephalomyelitis. Autoimmunity 16: 267-274.
27. Chu, C. Q., S. Wittmer, and D. K. Dalton. 2000. Failure to suppress the expansion of the activated CD4 T cell population in interferon g-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 192: 123-128.
28. Furlan, R., E. Brambilla, F. Ruffini, P. L. Poliani, A. Bergami, P. C. Marconi, D. M. Franciotta, G. Penna, G. Comi, L. Adorini, and G. Martino. 2001. Intrathecal delivery of IFN-g protects C57BL/6 mice from chronic-progressive experimental autoimmune encephalomyelitis by increasing apoptosis of central nervous system-infiltrating lymphocytes. J. Immunol. 167: 1821-1829.
29. Heremans, H., C. Dillen, M. Groenen, E. Martens, and A. Billiau. 1996. Chronic relapsing experimental autoimmune encephalomyelitis (CREAE) in mice: enhancement by monoclonal antibodies against interferon-g. Eur. J. Immunol. 26: 2393-2398.
30. Voorthuis, J. A., B. M. Uitdehaag, C. J. De Groot, P. H. Goede, P. H. van der Meide, and C. D. Dijkstra. 1990. Suppression of experimental allergic encephalomyelitis by intraventricular administration of interferon-gamma in Lewis rats. Clin. Exp. Immunol. 81: 183-188.
31. Panitch, H. S., R. L. Hirsch, A. S. Haley, and K. P. Johnson. 1987. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet 1: 893-895.
32. Kroenke, M. A., T. J. Carlson, A. V. Andjelkovic, and B. M. Segal. 2008. IL-12-and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 205: 1535-1541.
33. O'Connor, R. A., K. H. Malpass, and S. M. Anderton. 2007. The inflamed central nervous system drives the activation and rapid proliferation of Foxp3+ regulatory T cells. J. Immunol. 179: 958-966.
34. Steinman, L. 2008. A rush to judgment on Th17. J. Exp. Med. 205: 1517-1522.
35. Stromnes, I. M., L. M. Cerretti, D. Liggitt, R. A. Harris, and J. M. Goverman. 2008. Differential regulation of central nervous system autoimmunity by TH1 and TH17 cells. Nat. Med. 14: 337-342.
36. Axtell, R. C., B. A. de Jong, K. Boniface, L. F. van der Voort, R. Bhat, P. De Sarno, R. Naves, M. Han, F. Zhong, J. G. Castellanos, et al. 2010. T helper type 1 and 17 cells determine efficacy of interferon-b in multiple sclerosis and experimental encephalomyelitis. Nat. Med. 16: 406-412.
37. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
38. Axtell, R. C., M. S. Webb, S. R. Barnum, and C. Raman. 2004. Cutting edge: critical role for CD5 in experimental autoimmune encephalomyelitis: inhibition of engagement reverses disease in mice. J. Immunol. 173: 2928-2932.
39. Sestero, C. M., D. J. McGuire, P. De Sarno, E. C. Brantley, G. Soldevila, R. C. Axtell, and C. Raman. 2012. CD5-dependent CK2 activation pathway regulates threshold for T cell anergy. J. Immunol. 189: 2918-2930.
40. De Sarno, P., R. C. Axtell, C. Raman, K. A. Roth, D. R. Alessi, and R. S. Jope. 2008. Lithium prevents and ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 181: 338-345.
41. Abromson-Leeman, S., R. Bronson, Y. Luo, M. Berman, R. Leeman, J. Leeman, and M. Dorf. 2004. T-cell properties determine disease site, clinical presentation, and cellular pathology of experimental autoimmune encephalomyelitis. Am. J. Pathol. 165: 1519-1533.
42. Wensky, A. K., G. C. Furtado, M. C. Marcondes, S. Chen, D. Manfra, S. A. Lira, D. Zagzag, and J. J. Lafaille. 2005. IFN-g determines distinct clinical outcomes in autoimmune encephalomyelitis. J. Immunol. 174: 1416-1423.
43. Jäger, A., V. Dardalhon, R. A. Sobel, E. Bettelli, and V. K. Kuchroo. 2009. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 183: 7169-7177.
44. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
45. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
46. Szabo, S. J., B. M. Sullivan, S. L. Peng, and L. H. Glimcher. 2003. Molecular mechanisms regulating Th1 immune responses. Annu. Rev. Immunol. 21: 713-758.
47. Lees, J. R., P. T. Golumbek, J. Sim, D. Dorsey, and J. H. Russell. 2008. Regional CNS responses to IFN-g determine lesion localization patterns during EAE pathogenesis. J. Exp. Med. 205: 2633-2642.
48. Dev, K. K., F. Mullershausen, H. Mattes, R. R. Kuhn, G. Bilbe, D. Hoyer, and A. Mir. 2008. Brain sphingosine-1-phosphate receptors: implication for FTY720 in the treatment of multiple sclerosis. Pharmacol. Ther. 117: 77-93.
49. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
50. Xin, L., D. A. Vargas-Inchaustegui, S. S. Raimer, B. C. Kelly, J. Hu, L. Zhu, J. Sun, and L. Soong. 2010. Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites. J. Immunol. 184: 7047-7056.
51. Critchfield, J. M., M. K. Racke, J. C. Zúñiga-Pflücker, B. Cannella, C. S. Raine, J. Goverman, and M. J. Lenardo. 1994. T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science 263: 1139-1143.
52. Weishaupt, A., S. Jander, W. Brück, T. Kuhlmann, M. Stienekemeier, T. Hartung, K. V. Toyka, G. Stoll, and R. Gold. 2000. Molecular mechanisms of high-dose antigen therapy in experimental autoimmune encephalomyelitis: rapid induction of Th1-type cytokines and inducible nitric oxide synthase. J. Immunol. 165: 7157-7163.
53. Delhaye, S., S. Paul, G. Blakqori, M. Minet, F. Weber, P. Staeheli, and T. Michiels. 2006. Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. USA 103: 7835-7840.
54. Miller, S. D., E. J. McMahon, B. Schreiner, and S. L. Bailey. 2007. Antigen presentation in the CNS by myeloid dendritic cells drives progression of relapsing experimental autoimmune encephalomyelitis. Ann. N. Y. Acad. Sci. 1103: 179-191.
55. Town, T., D. Jeng, L. Alexopoulou, J. Tan, and R. A. Flavell. 2006. Microglia recognize double-stranded RNA via TLR3. J. Immunol. 176: 3804-3812.
56. Rowse, A. L., R. Naves, K. S. Cashman, D. J. McGuire, T. Mbana, C. Raman, and P. De Sarno. 2012. Lithium controls central nervous system autoimmunity through modulation of IFN-g signaling. PLoS ONE 7: e52658.
57. Antel, J. P., and V. E. Miron. 2008. Central nervous system effects of current and emerging multiple sclerosis-directed immuno-therapies. Clin. Neurol. Neurosurg. 110: 951-957.
58. Barin, J. G., M. V. Talor, G. C. Baldeviano, M. Kimura, N. R. Rose, and D. Ciháková. 2010. Mechanisms of IFNg regulation of autoimmune myocarditis. Exp. Mol. Pathol. 89: 83-91.
59. Sethna, M. P., and L. A. Lampson. 1991. Immune modulation within the brain: recruitment of inflammatory cells and increased major histocompatibility antigen expression following intracerebral injection of interferon-gamma. J. Neuroimmunol. 34: 121-132.
60. Simmons, R. D., and D. O. Willenborg. 1990. Direct injection of cytokines into the spinal cord causes autoimmune encephalomyelitis-like inflammation. J. Neurol. Sci. 100: 37-42.
61. Jagessar, S. A., B. Gran, N. Heijmans, J. Bauer, J. D. Laman, B. A. 't Hart, and C. S. Constantinescu. 2012. Discrepant effects of human interferon-gamma on clinical and immunological disease parameters in a novel marmoset model for multiple sclerosis. J. Neuroimmune Pharmacol. 7: 253-265.
62. Liu, J., X. Guan, and X. Ma. 2007. Regulation of IL-27 p28 gene expression in macrophages through MyD88-and interferon-g-mediated pathways. J. Exp. Med. 204: 141-152.
63. Murugaiyan, G., A. Mittal, and H. L. Weiner. 2010. Identification of an IL-27/ osteopontin axis in dendritic cells and its modulation by IFN-g limits IL-17-mediated autoimmune inflammation. Proc. Natl. Acad. Sci. USA 107: 11495-11500.
64. Hu, X., and L. B. Ivashkiv. 2009. Cross-regulation of signaling pathways by interferon-g: implications for immune responses and autoimmune diseases. Immunity 31: 539-550.
65. Willenborg, D. O., S. A. Fordham, M. A. Staykova, I. A. Ramshaw, and W. B. Cowden. 1999. IFN-g is critical to the control of murine autoimmune encephalomyelitis and regulates both in the periphery and in the target tissue: a possible role for nitric oxide. J. Immunol. 163: 5278-5286.
66. Butzkueven, H., J. G. Zhang, M. Soilu-Hanninen, H. Hochrein, F. Chionh, K. A. Shipham, B. Emery, A. M. Turnley, S. Petratos, M. Ernst, et al. 2002. LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat. Med. 8: 613-619.
67. Cash, E., A. Minty, P. Ferrara, D. Caput, D. Fradelizi, and O. Rott. 1994. Macrophage-inactivating IL-13 suppresses experimental autoimmune encephalomyelitis in rats. J. Immunol. 153: 4258-4267.
68. de Vries, J. E. 1998. The role of IL-13 and its receptor in allergy and inflammatory responses. J. Allergy Clin. Immunol. 102: 165-169.
69. Linker, R. A., N. Kruse, S. Israel, T. Wei, S. Seubert, A. Hombach, B. Holtmann, F. Luhder, R. M. Ransohoff, M. Sendtner, and R. Gold. 2008. Leukemia inhibitory factor deficiency modulates the immune response and limits autoimmune demyelination: a new role for neurotrophic cytokines in neuroinflammation. J. Immunol. 180: 2204-2213.
70. Ramgolam, V. S., Y. Sha, J. Jin, X. Zhang, and S. Markovic-Plese. 2009. IFN-b inhibits human Th17 cell differentiation. J. Immunol. 183: 5418-5427.
71. Vilela, M. C., D. S. Mansur, N. Lacerda-Queiroz, D. H. Rodrigues, G. K. Lima, R. M. Arantes, E. G. Kroon, M. A. da Silva Campos, M. M. Teixeira, and A. L. Teixeira. 2009. The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann. N. Y. Acad. Sci. 1153: 256-263.