Janus-like effects of type I interferon in autoimmune diseases

Immunological Reviews

Volumn 248, Issue 1, 2012, Pages 23-35

  Axtell, Robert C ^a   Raman, Chander ^b  

^a STANFORD UNIVERSITY   (United States)

^b and Clinical Center   (United States)

Author keywords

Autoimmunity; IL 7; Interferon; Th1; Th17

Indexed keywords

BELIMUMAB; BETA INTERFERON; BETA1A INTERFERON; CHEMOKINE; CYTOKINE; FINGOLIMOD; GLATIRAMER; INTERFERON; INTERFERON BETA SERINE; INTERLEUKIN 7; RECOMBINANT BETA INTERFERON; TOCILIZUMAB; USTEKINUMAB;

ALLERGIC ENCEPHALOMYELITIS; ANTIGEN PRESENTING CELL; ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ACTIVITY; DISEASE EXACERBATION; DRUG DOSE REDUCTION; DRUG SUBSTITUTION; DRUG TOLERABILITY; DRUG WITHDRAWAL; FLU LIKE SYNDROME; GENETIC POLYMORPHISM; HUMAN; LIVER INJURY; LYMPHOCYTE PROLIFERATION; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; RECURRENT DISEASE; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 CELL; TH17 CELL; TREATMENT OUTCOME; TREATMENT RESPONSE; ULCERATIVE COLITIS;

ANIMALS; AUTOIMMUNE DISEASES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS; HUMANS; INTERFERON TYPE I; INTERFERON-BETA; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; TH1 CELLS; TH17 CELLS;

EID: 84862748323     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2012.01131.x     Document Type: Article

References (152)

1. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 1957;147:258-267.
2. Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 2004;202:8-32.
3. Foster GR. Pegylated interferons for the treatment of chronic hepatitis C: pharmacological and clinical differences between peginterferon-alpha-2a and peginterferon-alpha-2b. Drugs 2010;70:147-165.
4. Kirkwood JM, et al. Mechanisms and management of toxicities associated with high-dose interferon alfa-2b therapy. J Clin Oncol 2002;20:3703-3718.
5. Arnason BG. Immunologic therapy of multiple sclerosis. Annu Rev Med 1999;50:291-302.
6. Nestle FO, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 2005;202:135-143.
7. Yao Y, et al. Type I interferon: potential therapeutic target for psoriasis? PLoS ONE 2008;3:e2737.
8. Palace J, Leite MI, Nairne A, Vincent A. Interferon Beta treatment in neuromyelitis optica: increase in relapses and aquaporin 4 antibody titers. Arch Neurol 2010;67:1016-1017.
9. Uzawa A, Mori M, Hayakawa S, Masuda S, Kuwabara S. Different responses to interferon beta-1b treatment in patients with neuromyelitis optica and multiple sclerosis. Eur J Neurol 2010;17:672-676.
10. Bennett L, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003;197:711-723.
11. Comi G, et al. Comparison of two dosing frequencies of subcutaneous interferon beta-1a in patients with a first clinical demyelinating event suggestive of multiple sclerosis (REFLEX): a phase 3 randomised controlled trial. Lancet Neurol 2012;11:33-41.
12. Chan S, Kingwell E, Oger J, Yoshida E, Tremlett H. High-dose frequency beta-interferons increase the risk of liver test abnormalities in multiple sclerosis: a longitudinal study. Mult Scler 2011;17:361-367.
13. Axtell RC, et al. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat Med 2010;16:406-412.
14. Comabella M, et al. A type I interferon signature in monocytes is associated with poor response to interferon-beta in multiple sclerosis. Brain 2009;132:3353-3365.
15. Malucchi S, et al. One-year evaluation of factors affecting the biological activity of interferon beta in multiple sclerosis patients. J Neurol 2010;258:895-903.
16. Rio J, et al. Defining the response to interferon-beta in relapsing-remitting multiple sclerosis patients. Ann Neurol 2006;59:344-352.
17. Hillert J, Olerup O. HLA and MS. Neurology 1993;43:2426-2427.
18. Mingioli ES, McFarlin DE. Leukocyte surface antigens in patients with multiple sclerosis. J Neuroimmunol 1984;6:131-139.
19. Kuchroo VK, Anderson AC, Waldner H, Munder M, Bettelli E, Nicholson LB. T cell response in experimental autoimmune encephalomyelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu Rev Immunol 2002;20:101-123.
20. Abreu SL. Suppression of experimental allergic encephalomyelitis by interferon. Immunol Commun 1982;11:1-7.
21. Galligan CL, et al. Interferon-beta is a key regulator of proinflammatory events in experimental autoimmune encephalomyelitis. Mult Scler 2010;16:1458-1473.
22. Prinz M, Kalinke U. New lessons about old molecules: how type I interferons shape Th1/Th17-mediated autoimmunity in the CNS. Trends Mol Med 2010;16:379-386.
23. Guo B, Chang EY, Cheng G. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J Clin Invest 2008;118:1680-1690.
24. Martin-Saavedra FM, Gonzalez-Garcia C, Bravo B, Ballester S. Beta interferon restricts the inflammatory potential of CD4+ cells through the boost of the Th2 phenotype, the inhibition of Th17 response and the prevalence of naturally occurring T regulatory cells. Mol Immunol 2008;45:4008-4019.
25. Annunziato F, Romagnani S. Heterogeneity of human effector CD4+ T cells. Arthritis Res Ther 2009;11:257.
26. Jager A, Kuchroo VK. Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand J Immunol 2010;72:173-184.
27. King C, Sprent J. Emerging cellular networks for regulation of T follicular helper cells. Trends Immunol 2012;33:59-65.
28. Harrington LE, Mangan PR, Weaver CT. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol 2006;18:349-356.
29. Olsson T. Cytokines in neuroinflammatory disease: role of myelin autoreactive T cell production of interferon-gamma. J Neuroimmunol 1992;40:211-218.
30. Bettelli E, Sullivan B, Szabo SJ, Sobel RA, Glimcher LH, Kuchroo VK. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J Exp Med 2004;200:79-87.
31. Stromnes IM, Cerretti LM, Liggitt D, Harris RA, Goverman JM. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat Med 2008;14:337-342.
32. Panitch HS, Hirsch RL, Haley AS, Johnson KP. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet 1987;1:893-895.
33. Ferber IA, et al. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J Immunol 1996;156:5-7.
34. Harrington LE, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005;6:1123-1132.
35. Langrish CL, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005;201:233-240.
36. Haak S, et al. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest 2009;119:61-69.
37. Ke Y, et al. Anti-inflammatory role of IL-17 in experimental autoimmune uveitis. J Immunol 2009;182:3183-3190.
38. Durelli L, et al. T-helper 17 cells expand in multiple sclerosis and are inhibited by interferon-beta. Ann Neurol 2009;65:499-509.
39. Lock C, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002;8:500-508.
40. Kroenke MA, Carlson TJ, Andjelkovic AV, Segal BM. 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 2008;205:1535-1541.
41. Nagai T, Devergne O, van Seventer GA, van Seventer JM. Interferon-beta mediates opposing effects on interferon-gamma-dependent Interleukin-12 p70 secretion by human monocyte-derived dendritic cells. Scand J Immunol 2007;65:107-117.
42. McRae BL, Semnani RT, Hayes MP, van Seventer GA. Type I IFNs inhibit human dendritic cell IL-12 production and Th1 cell development. J Immunol 1998;160:4298-4304.
43. Ramgolam VS, Sha Y, Jin J, Zhang X, Markovic-Plese S. IFN-beta inhibits human Th17 cell differentiation. J Immunol 2009;183:5418-5427.
44. Benveniste EN, Qin H. Type I interferons as anti-inflammatory mediators. Sci STKE 2007;2007:pe70.
45. Hesse D, Sorensen PS. Using measurements of neutralizing antibodies: the challenge of IFN-beta therapy. Eur J Neurol 2007;14:850-859.
46. Grossberg SE, Oger J, Grossberg LD, Gehchan A, Klein JP. Frequency and magnitude of interferon beta neutralizing antibodies in the evaluation of interferon beta immunogenicity in patients with multiple sclerosis. J Interferon Cytokine Res 2010;31:337-344.
47. Hegen H, et al. Persistency of neutralizing antibodies depends on titer and interferon-beta preparation. Mult Scler 2011; doi:10.1177/1352458511426738.
48. Lanzillo R, et al. Predictive factors of neutralizing antibodies development in relapsing-remitting multiple sclerosis patients on interferon Beta-1b therapy. Neurol Sci 2011;32:287-292.
49. Hartung HP, et al. Interferon beta-1b-neutralizing antibodies 5years after clinically isolated syndrome. Neurology 2011;77:835-843.
50. Massart C, et al. Determination of interferon beta neutralizing antibodies in multiple sclerosis: improvement of clinical sensitivity of a cytopathic effect assay. Clin Chim Acta 2008;391:98-101.
51. Serrano-Fernandez P, et al. Time course transcriptomics of IFNB1b drug therapy in multiple sclerosis. Autoimmunity 2010;43:172-178.
52. Rani MR, et al. Heterogeneous, longitudinally stable molecular signatures in response to interferon-beta. Ann N Y Acad Sci 2009;1182:58-68.
53. Rudick RA, et al. Excessive biologic response to IFNbeta is associated with poor treatment response in patients with multiple sclerosis. PLoS ONE 2011;6:e19262.
54. Tzartos JS, et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008;172:146-155.
55. Werner JL, et al. Neutrophils produce interleukin 17A (IL-17A) in a dectin-1- and IL-23-dependent manner during invasive fungal infection. Infect Immun 2011;79:3966-3977.
56. Bushnell SE, et al. Serum IL-17F does not predict poor response to IM IFNβ-1a in relapsing-remitting MS. Neurology 2012; doi:10.1212/WNL.0b013e318259e123.
57. Navarra SV, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011;377:721-731.
58. Preble OT, Black RJ, Friedman RM, Klippel JH, Vilcek J. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon. Science 1982;216:429-431.
59. Cunninghame Graham DS, et al. Association of NCF2, IKZF1, IRF8, IFIH1, and TYK2 with systemic lupus erythematosus. PLoS Genet 2011;7:e1002341.
60. Fu Q, et al. Association of a functional IRF7 variant with systemic lupus erythematosus. Arthritis Rheum 2011;63:749-754.
61. Ramos PS, et al. Genetic analyses of interferon pathway-related genes reveal multiple new loci associated with systemic lupus erythematosus. Arthritis Rheum 2011;63:2049-2057.
62. Sandling JK, et al. A candidate gene study of the type I interferon pathway implicates IKBKE and IL8 as risk loci for SLE. Eur J Hum Genet 2011;19:479-484.
63. Kono DH, Baccala R, Theofilopoulos AN. Inhibition of lupus by genetic alteration of the interferon-alpha/beta receptor. Autoimmunity 2003;36:503-510.
64. Nacionales DC, et al. Deficiency of the type I interferon receptor protects mice from experimental lupus. Arthritis Rheum 2007;56:3770-3783.
65. Liu Z, et al. Interferon-alpha accelerates murine systemic lupus erythematosus in a T cell-dependent manner. Arthritis Rheum 2011;63:219-229.
66. Ramanujam M, et al. Interferon-alpha treatment of female (NZW x BXSB)F(1) mice mimics some but not all features associated with the Yaa mutation. Arthritis Rheum 2009;60:1096-1101.
67. Merrill JT, et al. Safety profile and clinical activity of sifalimumab, a fully human anti-interferon alpha monoclonal antibody, in systemic lupus erythematosus: a phase I, multicentre, double-blind randomised study. Ann Rheum Dis 2011;70:1905-1913.
68. Yao Y, et al. Neutralization of interferon-alpha/beta-inducible genes and downstream effect in a phase I trial of an anti-interferon-alpha monoclonal antibody in systemic lupus erythematosus. Arthritis Rheum 2009;60:1785-1796.
69. Shah K, et al. Dysregulated balance of Th17 and Th1 cells in systemic lupus erythematosus. Arthritis Res Ther 2010;12:R53.
70. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006;24:179-189.
71. van den Berg A, et al. Interleukin-17 induces hyperresponsive interleukin-8 and interleukin-6 production to tumor necrosis factor-alpha in structural lung cells. Am J Respir Cell Mol Biol 2005;33:97-104.
72. Hwang SY, et al. IL-17 induces production of IL-6 and IL-8 in rheumatoid arthritis synovial fibroblasts via NF-kappaB- and PI3-kinase/Akt-dependent pathways. Arthritis Res Ther 2004;6:R120-128.
73. Illei GG, et al. Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study. Arthritis Rheum 2010;62:542-552.
74. De Souza A, Ali-Shaw T, Strober BE, Franks AG, Jr. Successful treatment of subacute lupus erythematosus with ustekinumab. Arch Dermatol 2011;147:896-898.
75. Pittock SJ, et al. Neuromyelitis optica and non organ-specific autoimmunity. Arch Neurol 2008;65:78-83.
76. Nakashima I, et al. Clinical and MRI features of Japanese patients with multiple sclerosis positive for NMO-IgG. J Neurol Neurosurg Psychiatry 2006;77:1073-1075.
77. Pittock SJ, Weinshenker BG, Lucchinetti CF, Wingerchuk DM, Corboy JR, Lennon VA. Neuromyelitis optica brain lesions localized at sites of high aquaporin 4 expression. Arch Neurol 2006;63:964-968.
78. Barkhof F, et al. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 1997;120(Pt 11):2059-2069.
79. Ishizu T, et al. Intrathecal activation of the IL-17/IL-8 axis in opticospinal multiple sclerosis. Brain 2005;128:988-1002.
80. Icoz S, et al. Enhanced IL-6 production in aquaporin-4 antibody positive neuromyelitis optica patients. Int J Neurosci 2010;120:71-75.
81. Wang HH, et al. Interleukin-17-secreting T cells in neuromyelitis optica and multiple sclerosis during relapse. J Clin Neurosci 2011;18:1313-1317.
82. Ye P, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001;194:519-527.
83. Zhang Z, et al. Interleukin-17 causes neutrophil mediated inflammation in ovalbumin-induced uveitis in DO11.10 mice. Cytokine 2009;46:79-91.
84. Herges K, et al. Protective effect of an elastase inhibitor in a neuromyelitis optica-like disease driven by a peptide of myelin oligodendroglial glycoprotein. Mult Scler 2012;18:398-408.
85. Shimizu J, et al. IFNbeta-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 2010;75:1423-1427.
86. Warabi Y, Matsumoto Y, Hayashi H. Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J Neurol Sci 2007;252:57-61.
87. Feng X, et al. Type I interferon signature is high in lupus and neuromyelitis optica but low in multiple sclerosis. J Neurol Sci 2012;313:48-53.
88. Mehta LR, et al. Neuromyelitis optica spectrum disorder in a patient with systemic lupus erythematosus and anti-phospholipid antibody syndrome. Mult Scler 2008;14:425-427.
89. Racz E, et al. Effective treatment of psoriasis with narrow-band UVB phototherapy is linked to suppression of the IFN and Th17 pathways. J Invest Dermatol 2011;131:1547-1558.
90. Cargill M, et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am J Hum Genet 2007;80:273-290.
91. Nair RP, et al. Polymorphisms of the IL12B and IL23R genes are associated with psoriasis. J Invest Dermatol 2008;128:1653-1661.
92. Chan JR, et al. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 2006;203:2577-2587.
93. Krueger GG, et al. A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N Engl J Med 2007;356:580-592.
94. Segal BM, Constantinescu CS, Raychaudhuri A, Kim L, Fidelus-Gort R, Kasper LH. Repeated subcutaneous injections of IL12/23 p40 neutralising antibody, ustekinumab, in patients with relapsing-remitting multiple sclerosis: a phase II, double-blind, placebo-controlled, randomised, dose-ranging study. Lancet Neurol 2008;7:796-804.
95. Coimbra S, et al. Interleukin (IL)-22, IL-17, IL-23, IL-8, vascular endothelial growth factor and tumour necrosis factor-alpha levels in patients with psoriasis before, during and after psoralen-ultraviolet A and narrowband ultraviolet B therapy. Br J Dermatol 2010;163:1282-1290.
96. Fujishima S, et al. Involvement of IL-17F via the induction of IL-6 in psoriasis. Arch Dermatol Res 2010;302:499-505.
97. Hueber W, et al. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med 2010;2:52ra72.
98. van der Fits L, van der Wel LI, Laman JD, Prens EP, Verschuren MC. In psoriasis lesional skin the type I interferon signaling pathway is activated, whereas interferon-alpha sensitivity is unaltered. J Invest Dermatol 2004;122:51-60.
99. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 2011;29:163-183.
100. Hida S, et al. CD8(+) T cell-mediated skin disease in mice lacking IRF-2, the transcriptional attenuator of interferon-alpha/beta signaling. Immunity 2000;13:643-655.
101. Scavo S, et al. Verrucous psoriasis in a patient with chronic C hepatitis treated with interferon. Clin Drug Investig 2004;24:427-429.
102. La Mantia L, Capsoni F. Psoriasis during interferon beta treatment for multiple sclerosis. Neurol Sci 2010;31:337-339.
103. Lopez-Lerma I, Iranzo P, Herrero C. New-onset psoriasis in a patient treated with interferon beta-1a. Br J Dermatol 2009;160:716-717.
104. Webster GF, Knobler RL, Lublin FD, Kramer EM, Hochman LR. Cutaneous ulcerations and pustular psoriasis flare caused by recombinant interferon beta injections in patients with multiple sclerosis. J Am Acad Dermatol 1996;34:365-367.
105. Seckin D, Durusoy C, Sahin S. Concomitant vitiligo and psoriasis in a patient treated with interferon alfa-2a for chronic hepatitis B infection. Pediatr Dermatol 2004;21:577-579.
106. Downs AM, Dunnill MG. Exacerbation of psoriasis by interferon-alpha therapy for hepatitis C. Clin Exp Dermatol 2000;25:351-352.
107. Musch E, Andus T, Malek M. Induction and maintenance of clinical remission by interferon-beta in patients with steroid-refractory active ulcerative colitis-an open long-term pilot trial. Aliment Pharmacol Ther 2002;16:1233-1239.
108. Pena-Rossi C, et al. Clinical trial: a multicentre, randomized, double-blind, placebo-controlled, dose-finding, phase II study of subcutaneous interferon-beta-1a in moderately active ulcerative colitis. Aliment Pharmacol Ther 2008;28:758-767.
109. Mannon PJ, et al. Suppression of inflammation in ulcerative colitis by interferon-{beta}-1a is accompanied by inhibition of IL-13 production. Gut 2010;60:449-455.
110. Martinelli S, et al. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J Biol Chem 2004;279:44123-44132.
111. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010;33:657-670.
112. Krumbholz M, et al. Interferon-beta increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain 2008;131:1455-1463.
113. Kato A, Truong-Tran AQ, Scott AL, Matsumoto K, Schleimer RP. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J Immunol 2006;177:7164-7172.
114. Ittah M, et al. B cell-activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cells in primary Sjogren's syndrome. Arthritis Res Ther 2006;8:R51.
115. Vaknin-Dembinsky A, Brill L, Orpaz N, Abramsky O, Karussis D. Preferential increase of B-cell activating factor in the cerebrospinal fluid of neuromyelitis optica in a white population. Mult Scler 2010;16:1453-1457.
116. Becker-Merok A, Nikolaisen C, Nossent HC. B-lymphocyte activating factor in systemic lupus erythematosus and rheumatoid arthritis in relation to autoantibody levels, disease measures and time. Lupus 2006;15:570-576.
117. Liu Z, Davidson A. BAFF and selection of autoreactive B cells. Trends Immunol 2011;32:388-394.
118. Hsu HC, et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 2008;9:166-175.
119. Xie S, et al. IL-17 activates the canonical NF-kappaB signaling pathway in autoimmune B cells of BXD2 mice to upregulate the expression of regulators of G-protein signaling 16. J Immunol 2010;184:2289-2296.
120. Tohyama M, et al. IL-17 and IL-22 mediate IL-20 subfamily cytokine production in cultured keratinocytes via increased IL-22 receptor expression. Eur J Immunol 2009;39:2779-2788.
121. Tohyama M, Yang L, Hanakawa Y, Dai X, Shirakata Y, Sayama K. IFN-alpha enhances IL-22 receptor expression in keratinocytes: a possible role in the development of psoriasis. J Invest Dermatol 2012; doi:10.1038/jid.2011.468.
122. Kebir H, et al. Human Th17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007;13:1173-1175.
123. Eyerich S, et al. IL-22 and TNF-alpha represent a key cytokine combination for epidermal integrity during infection with Candida albicans. Eur J Immunol 2011;41:1894-1901.
124. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004;21:241-254.
125. Pender MP. Does Epstein-Barr virus infection in the brain drive the development of multiple sclerosis? Brain 2009;132:3196-3198.
126. Mehling M, Kappos L, Derfuss T. Fingolimod for multiple sclerosis: mechanism of action, clinical outcomes, and future directions. Curr Neurol Neurosci Rep 2011;11:492-497.
127. Shiow LR, et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 2006;440:540-544.
128. Hartung HP, Kieseier BC. Atacicept: targeting B cells in multiple sclerosis. Ther Adv Neurol Disord 2010;3:205-216.
129. Kim SS, Richman DP, Zamvil SS, Agius MA. Accelerated central nervous system autoimmunity in BAFF-receptor-deficient mice. J Neurol Sci 2011;306:9-15.
130. Yang M, et al. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol 2010;184:3321-3325.
131. Zhang X, Deriaud E, Jiao X, Braun D, Leclerc C, Lo-Man R. Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells. J Exp Med 2007;204:1107-1118.
132. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005;5:375-386.
133. Berenson LS, Gavrieli M, Farrar JD, Murphy TL, Murphy KM. Distinct characteristics of murine STAT4 activation in response to IL-12 and IFN-alpha. J Immunol 2006;177:5195-5203.
134. Tanabe Y, Nishibori T, Su L, Arduini RM, Baker DP, David M. Cutting edge: role of STAT1, STAT3, and STAT5 in IFN-alpha beta responses in T lymphocytes. J Immunol 2005;174:609-613.
135. Catalfamo M, et al. CD4 and CD8 T cell immune activation during chronic HIV infection: roles of homeostasis, HIV, type I IFN, and IL-7. J Immunol 2011;186:2106-2116.
136. Nguyen KB, Cousens LP, Doughty LA, Pien GC, Durbin JE, Biron CA. Interferon alpha/beta-mediated inhibition and promotion of interferon gamma: STAT1 resolves a paradox. Nat Immunol 2000;1:70-76.
137. Wong LH, Hatzinisiriou I, Devenish RJ, Ralph SJ. IFN-gamma priming up-regulates IFN-stimulated gene factor 3 (ISGF3) components, augmenting responsiveness of IFN-resistant melanoma cells to type I IFNs. J Immunol 1998;160:5475-5484.
138. Chitnis T, et al. Effect of targeted disruption of STAT4 and STAT6 on the induction of experimental autoimmune encephalomyelitis. J Clin Invest 2001;108:739-747.
139. Lee LF, et al. IL-7 promotes T(H)1 development and serum IL-7 predicts clinical response to interferon-beta in multiple sclerosis. Sci Transl Med 2011;3:93ra68.
140. Gregory SG, et al. Interleukin 7 receptor alpha chain (IL7R) shows allelic and functional association with multiple sclerosis. Nat Genet 2007;39:1083-1091.
141. Lundmark F, et al. Variation in interleukin 7 receptor alpha chain (IL7R) influences risk of multiple sclerosis. Nat Genet 2007;39:1108-1113.
142. von Freeden-Jeffry U, Vieira P, Lucian LA, McNeil T, Burdach SE, Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 1995;181:1519-1526.
143. Seddon B, Tomlinson P, Zamoyska R. Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol 2003;4:680-686.
144. Puel A, Ziegler SF, Buckley RH, Leonard WJ. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat Genet 1998;20:394-397.
145. Liu X, et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat Med 2010;16:191-197.
146. Davis CC, Marti LC, Sempowski GD, Jeyaraj DA, Szabolcs P. Interleukin-7 permits Th1/Tc1 maturation and promotes ex vivo expansion of cord blood T cells: a critical step toward adoptive immunotherapy after cord blood transplantation. Cancer Res 2010;70:5249-5258.
147. Ariizumi K, Meng Y, Bergstresser PR, Takashima A. IFN-gamma-dependent IL-7 gene regulation in keratinocytes. J Immunol 1995;154:6031-6039.
148. Oshima S, et al. Interferon regulatory factor 1 (IRF-1) and IRF-2 distinctively up-regulate gene expression and production of interleukin-7 in human intestinal epithelial cells. Mol Cell Biol 2004;24:6298-6310.
149. Nanjappa SG, Kim EH, Suresh M. Immunotherapeutic effects of IL-7 during a chronic viral infection in mice. Blood 2011;117:5123-5132.
150. Gregersen PK, Olsson LM. Recent advances in the genetics of autoimmune disease. Annu Rev Immunol 2009;27:363-391.
151. Herrier RN. Advances in the treatment of moderate-to-severe plaque psoriasis. Am J Health Syst Pharm 2011;68:795-806.
152. Bellesi M, Logullo F, Di Bella P, Provinciali L. CNS demyelination during anti-tumor necrosis factor alpha therapy. J Neurol 2006;253:668-669.