1,936
Views
82
CrossRef citations to date
0
Altmetric
Review Article

The type I interferon system in the etiopathogenesis of autoimmune diseases

Pages 227-237 | Received 14 Sep 2011, Accepted 14 Sep 2011, Published online: 09 Nov 2011

References

  • Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc B. 1957;147:258–67.
  • Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med. 2007;13:543–51.
  • Davis AM, Ramos HJ, Davis LS, Farrar JD. Cutting edge: a T-bet-independent role for IFN-α/β in regulating IL-2 secretion in human CD4+ central memory T cells. J Immunol. 2008;181:8204–8.
  • Ramos HJ, Davis AM, Cole AG, Schatzle JD, Forman J, Farrar JD. Reciprocal responsiveness to interleukin-12 and interferon-alpha specifies human CD8+ effector versus central memory T-cell fates. Blood. 2009;113:5516–25.
  • Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003;19:225–34.
  • Le Bon A, Thompson C, Kamphuis E, Durand V, Rossmann C, Kalinke U, Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J Immunol. 2006;176:2074–8.
  • Öberg K, Funa K, Alm G. Effects of leukocyte interferon on clinical symptoms and hormone levels in patients with mid-gut carcinoid tumors and carcinoid syndrome. N Engl J Med. 1983;309:129–33.
  • Öberg K, Alm G, Lindstrom H, Lundqvist G. Successful treatment of therapy-resistant pancreatic cholera with human leucocyte interferon. Lancet. 1985;1:725–7.
  • Hagberg H, Alm G, Bjorkholm M, Glimelius B, Killander A, Simonsson B, Alpha interferon treatment of patients with hairy-cell leukaemia. Scand J Haematol. 1985;35:66–70.
  • Janson ET, Rönnblom L, Ahlstrom H, Grander D, Alm G, Einhorn S, Treatment with alpha-interferon versus alpha-interferon in combination with streptozocin and doxorubicin in patients with malignant carcinoid tumors: a randomized trial. Ann Oncol. 1992;3:635–8.
  • Burman P, Karlsson FA, Öberg K, Alm G. Autoimmune thyroid disease in interferon-treated patients. Lancet. 1985;2:100–1.
  • Karlsson-Parra A, Burman P, Hagberg H, Öberg K, Alm G, Klareskog L, Autoantibodies to epithelial cells in patients on long-term therapy with leucocyte-derived interferon-alpha (IFN-α). Clin Exp Immunol.1990;81:72–5.
  • Rönnblom LE, Alm GV, Öberg KE. Possible induction of systemic lupus erythematosus by interferon-α treatment in a patient with a malignant carcinoid tumour. J Intern Med. 1990;227:207–10.
  • Rönnblom LE, Alm GV, Öberg KE. Autoimmunity after α-interferon therapy for malignant carcinoid tumors. Ann Intern Med. 1991;115:178–83.
  • Krause CD, Pestka S. Evolution of the class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol Ther. 2005;106:299–346.
  • Rönnblom L, Alm GV. Limiting dilution analysis of human peripheral blood mononuclear leukocytes that react to human amnion cells and protect these against viral challenge. Eur J Immunol. 1982;12:437–41.
  • Rönnblom L, Ramstedt U, Alm GV. Properties of human natural interferon-producing cells stimulated by tumor cell lines. Eur J Immunol. 1983;13:471–6.
  • Fitzgerald-Bocarsly P, Dai J, Singh S. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 2008;19:3–19.
  • Barber GN. Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Curr Opin Immunol. 2011;23:10–20.
  • Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005;5:375–86.
  • Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001;14:778–809.
  • Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197:711–23.
  • Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA. 2003;100:2610–5.
  • Strandberg L, Ambrosi A, Espinosa A, Ottosson L, Eloranta ML, Zhou W, Interferon-α induces up-regulation and nuclear translocation of the Ro52 autoantigen as detected by a panel of novel Ro52-specific monoclonal antibodies. J Clin Immunol. 2008;28:220–31.
  • Stahl-Hallengren C, Jonsen A, Nived O, Sturfelt G. Incidence studies of systemic lupus erythematosus in Southern Sweden: increasing age, decreasing frequency of renal manifestations and good prognosis. J Rheumatol. 2000;27:685–91.
  • Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med. 2008;358:929–39.
  • Hooks JJ, Moutsopoulos HM, Geis SA, Stahl NI, Decker JL, Notkins AL. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med. 1979;301:5–8.
  • Ytterberg SR, Schnitzer TJ. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum. 1982;25:401–6.
  • Bengtsson A, Sturfelt G, Truedsson L, Blomberg J, Alm G, Vallin H, Activation of type I interferon system in systemic lupus erythematosus correlates with disease activity but not antiretroviral antibodies. Lupus. 2000;9:664–71.
  • Preble OT, Rothko K, Klippel JH, Friedman RM, Johnston MI. Interferon-induced 2′-5′ adenylate synthetase in vivo and interferon production in vitro by lymphocytes from systemic lupus erythematosus patients with and without circulating interferon. J Exp Med. 1983;157:2140–6.
  • von Wussow P, Jakschies D, Hochkeppel H, Horisberger M, Hartung K, Deicher H. MX homologous protein in mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum. 1989;32:914–8.
  • Crow MK, Wohlgemuth J. Microarray analysis of gene expression in lupus. Arthritis Res Ther. 2003;5:279–87.
  • Han GM, Chen SL, Shen N, Ye S, Bao CD, Gu YY. Analysis of gene expression profiles in human systemic lupus erythematosus using oligonucleotide microarray. Genes Immun. 2003;4:177–86.
  • Hjelmervik TO, Petersen K, Jonassen I, Jonsson R, Bolstad AI. Gene expression profiling of minor salivary glands clearly distinguishes primary Sjogren's syndrome patients from healthy control subjects. Arthritis Rheum. 2005;52:1534–44.
  • Baechler EC, Batliwalla FM, Reed AM, Peterson EJ, Gaffney PM, Moser KL, Gene expression profiling in human autoimmunity. Immunol Rev. 2006;210:120–37.
  • Higgs BW, Liu Z, White B, Zhu W, White WI, Morehouse C, Patients with systemic lupus erythematosus, myositis, rheumatoid arthritis and scleroderma share activation of a common type I interferon pathway. Ann Rheum Dis. 2011 Jul 28 (Epub ahead of print).
  • Cederblad B, Blomberg S, Vallin H, Perers A, Alm GV, Rönnblom L. Patients with systemic lupus erythematosus have reduced numbers of circulating natural interferon-α-producing cells. J Autoimmun. 1998;11:465–70.
  • Blomberg S, Eloranta M-L, Magnusson M, Alm GV, Rönnblom L. Expression of the markers BDCA-2 and -4 and production of interferon-α by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Rheum. 2003;48:2524–32.
  • Blomberg S, Eloranta M-L, Cederblad B, Nordlind K, Alm GV, Rönnblom L. Presence of cutaneous interferon-α producing cells in patients with systemic lupus erythematosus. Lupus. 2001;10:484–90.
  • Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL. Plasmacytoid dendritic cells (natural interferon-α/β-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol. 2001;159:237–43.
  • Rönnblom L, Alm GV. The natural interferon-α producing cells in systemic lupus erythematosus. Hum Immunol.2002;63:1181–93.
  • Tucci M, Quatraro C, Lombardi L, Pellegrino C, Dammacco F, Silvestris F. Glomerular accumulation of plasmacytoid dendritic cells in active lupus nephritis: role of interleukin-18. Arthritis Rheum. 2008;58:251–62.
  • Båve U, Nordmark G, Lövgren T, Rönnelid J, Cajander S, Eloranta ML, Activation of the type I interferon system in primary Sjögren's syndrome: a possible etiopathogenic mechanism. Arthritis Rheum. 2005;52:1185–95.
  • Eloranta ML, Barbasso SH, Ulfgren AK, Rönnblom L, Alm GV, Lundberg IE. A possible mechanism for endogenous activation of the type I interferon system in myositis patients with anti-Jo-1 or anti-Ro52/Ro60 autoantibodies. Arthritis Rheum. 2007;56:3112–24.
  • Vallin H, Blomberg S, Alm GV, Cederblad B, Rönnblom L. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-alpha (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin Exp Immunol. 1999;115:196–202.
  • Vallin H, Perers A, Alm GV, Rönnblom L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J Immunol. 1999;163:6306–13.
  • Båve U, Magnusson M, Eloranta M-L, Perers A, Alm GV, Rönnblom L. FcγRIIa is expressed on natural IFN-α producing cells (plasmacytoid dendritic cells) and is required for the IFN-α production induced by apoptotic cells combined with lupus IgG. J Immunol. 2003;171:3296–302.
  • Rönnblom L, Eloranta ML, Alm GV. The type I interferon system in systemic lupus erythematosus. Arthritis Rheum. 2006;54:408–20.
  • Lövgren T, Eloranta ML, Båve U, Alm GV, Rönnblom L. Induction of interferon-α production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum. 2004;50:1861–72.
  • Munoz LE, van Bavel C, Franz S, Berden J, Herrmann M, van der Vlag J. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus. 2008;17:371–5.
  • Pisetsky DS, Rönnblom L. Systemic lupus erythematosus: a matter of life and death. Arthritis Rheum. 2009;60:1567–70.
  • Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, Gregorio J, Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med. 2011;3: 73ra19.
  • Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med. 2011;3: 73ra20.
  • Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Rönnblom L, C1q inhibits immune complex-induced interferon-a production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum. 2009;60:3081–90.
  • Santer DM, Hall BE, George TC, Tangsombatvisit S, Liu CL, Arkwright PD, C1q deficiency leads to the defective suppression of IFN-α in response to nucleoprotein containing immune complexes. J Immunol. 2010;185:4738–49.
  • Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology. 1998;199:265–85.
  • Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M, Forsbach A, Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med. 2005;202:1575–85.
  • Lövgren T, Eloranta ML, Kastner B, Wahren-Herlenius M, Alm GV, Rönnblom L. Induction of interferon-α by immune complexes or liposomes containing systemic lupus erythematosus autoantigen- and Sjögren's syndrome autoantigen-associated RNA. Arthritis Rheum. 2006;54:1917–27.
  • Hua J, Kirou K, Lee C, Crow MK. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 2006;54:1906–16.
  • Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349:1526–33.
  • McClain MT, Heinlen LD, Dennis GJ, Roebuck J, Harley JB, James JA. Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry. Nat Med. 2005;11:85–9.
  • Eloranta ML, Franck-Larsson K, Lovgren T, Kalamajski S, Rönnblom A, Rubin K, Type I interferon system activation and association with disease manifestations in systemic sclerosis. Ann Rheum Dis. 2010;69:1396–402.
  • Eloranta ML, Lövgren T, Finke D, Mathsson L, Rönnelid J, Kastner B, Regulation of the interferon-α production induced by RNA-containing immune complexes in plasmacytoid dendritic cells. Arthritis Rheum. 2009;60:2418–27.
  • Hagberg N, Berggren O, Leonard D, Weber G, Bryceson YT, Alm GV, IFN-α production by plasmacytoid dendritic cells stimulated with RNA-containing immune complexes is promoted by NK cells via MIP-1β and LFA-1. J Immunol. 2011;186:5085–94.
  • Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, Dai J, Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol. 2003;74:1125–38.
  • Sigurdsson S, Nordmark G, Göring HH, Lindroos K, Wiman AC, Sturfelt G, Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am J Hum Gen. 2005;76:528–37.
  • Sigurdsson S, Padyukov L, Kurreeman FAS, Liljedahl U, Wiman A-C, Alfredsson L, Association of a haplotype in the promotor region of the interferon regulatory factor 5 gene with rheumatoid arthritis. Arthritis Rheum. 2007;56:2202–10.
  • Nordmark G, Kristjansdottir G, Theander E, Eriksson P, Brun JG, Wang C, Additive effects of the major risk alleles of IRF5 and STAT4 in primary Sjogren's syndrome. Genes Immun. 2009;10:68–76.
  • Sigurdsson S, Göring HH, Kristjansdottir G, Milani L, Nordmark G, Sandling J, Comprehensive evaluation of the genetic variants of interferon regulatory factor 5 reveals a novel 5bp length polymorphism as strong risk factor for systemic lupus erythematosus. Hum Mol Genet. 2008;17:872–81.
  • Feng D, Stone RC, Eloranta ML, Sangster-Guity N, Nordmark G, Sigurdsson S, Genetic variants and disease-associated factors contribute to enhanced interferon regulatory factor 5 expression in blood cells of patients with systemic lupus erythematosus. Arthritis Rheum. 2010;62:562–73.
  • Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK. Association of the IRF5 risk haplotype with high serum interferon-α activity in systemic lupus erythematosus patients. Arthritis Rheum. 2008;58:2481–7.
  • Sandling JK, Garnier S, Sigurdsson S, Wang C, Nordmark G, Gunnarsson I, A candidate gene study of the type I interferon pathway implicates IKBKE and IL8 as risk loci for SLE. Eur J Hum Genet. 2011;19:479–84.
  • Tyler DR, Persky ME, Matthews LA, Chan S, Farrar JD. Pre-assembly of STAT4 with the human IFN-α/β?receptor-2 subunit is mediated by the STAT4 N-domain. Mol Immunol. 2007;44:1864–72.
  • Remmers EF, Plenge RM, Lee AT, Graham RR, Hom G, Behrens TW, STAT4 and the risk of rheumatoid arthritis and systemic lupus erythematosus. N Engl J Med. 2007;357:977–86.
  • Taylor KE, Remmers EF, Lee AT, Ortmann WA, Plenge RM, Tian C, Specificity of the STAT4 genetic association for severe disease manifestations of systemic lupus erythematosus. PLoS Genet. 2008;4:e1000084.
  • Sigurdsson S, Nordmark G, Garnier S, Grundberg E, Kwan T, Nilsson O, A risk haplotype of STAT4 for systemic lupus erythematosus is over-expressed, correlates with anti-dsDNA and shows additive effects with two risk alleles of IRF5. Hum Mol Genet. 2008;17:2868–76.
  • Cunninghame Graham DS, Akil M, Vyse TJ. Association of polymorphisms across the tyrosine kinase gene, TYK2 in UK SLE families. Rheumatology (Oxford). 2007;46:927–30.
  • Moser KL, Kelly JA, Lessard CJ, Harley JB. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun. 2009;10:373–9.
  • Fu Q, Chen X, Cui H, Guo Y, Chen J, Shen N, Association of elevated transcript levels of interferon-inducible chemokines with disease activity and organ damage in systemic lupus erythematosus patients. Arthritis Res Ther. 2008;10:R112.
  • Shiozawa S, Kuroki Y, Kim M, Hirohata S, Ogino T. Interferon-α in lupus psychosis. Arthritis Rheum. 1992;35:417–22.
  • Raison CL, Demetrashvili M, Capuron L, Miller AH. Neuropsychiatric adverse effects of interferon-alpha: recognition and management. CNS Drugs. 2005;19:105–23.
  • Santer DM, Yoshio T, Minota S, Moller T, Elkon KB. Potent induction of IFN-α and chemokines by autoantibodies in the cerebrospinal fluid of patients with neuropsychiatric lupus. J Immunol. 2009;182:1192–201.
  • Fairhurst AM, Mathian A, Connolly JE, Wang A, Gray HF, George TA, Systemic IFN-α drives kidney nephritis in B6. Sle123 mice. Eur J Immunol. 2008;38:1948–60.
  • Peterson KS, Huang JF, Zhu J, D'Agati V, Liu X, Miller N, Characterization of heterogeneity in the molecular pathogenesis of lupus nephritis from transcriptional profiles of laser-captured glomeruli. J Clin Invest. 2004;113:1722–33.
  • Kaplan MJ, Salmon JE. How does IFN-alpha insult the vasculature? let me count the ways. Arthritis Rheum. 2011;63:334–6.
  • Denny MF, Thacker S, Mehta H, Somers EC, Dodick T, Barrat FJ, Interferon-α promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis. Blood. 2007;110:2907–15.
  • Lood C, Amisten S, Gullstrand B, Jonsen A, Allhorn M, Truedsson L, Platelet transcriptional profile and protein expression in patients with systemic lupus erythematosus: up-regulation of the type I interferon system is strongly associated with vascular disease. Blood. 2010;116:1951–7.
  • Li J, Fu Q, Cui H, Qu B, Pan W, Shen N, Interferon-α priming promotes lipid uptake and macrophage-derived foam cell formation: a novel link between interferon-α and atherosclerosis in lupus. Arthritis Rheum. 2011;63:492–502.
  • Niessner A, Shin MS, Pryshchep O, Goronzy JJ, Chaikof EL, Weyand CM. Synergistic proinflammatory effects of the antiviral cytokine interferon-α and Toll-like receptor 4 ligands in the atherosclerotic plaque. Circulation. 2007;116:2043–52.
  • Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet. 2009;41:1228–33.
  • Rönnblom L, Alm GV, Eloranta ML. The type I interferon system in the development of lupus. Semin Immunol. 2011;23:113–21.
  • Santiago-Raber ML, Baccala R, Haraldsson KM, Choubey D, Stewart TA, Kono DH, Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med. 2003;197:777–88.
  • Braun D, Geraldes P, Demengeot J. Type I interferon controls the onset and severity of autoimmune manifestations in lpr mice. J Autoimmun. 2003;20:15–25.
  • Wallace DJ, Petri M, Olsen N, Kirou K, Dennis G, Yao Y, MEDI-545, an anti-interferon alpha monoclonal antibody, shows evidence of clinical activity in systemic lupus erythematosus. Arthritis Rheum. 2007;56:S562–3.
  • McBride JM, Wallace DJ, Yao Z, Morimoto A, Jiang J, Maciuca R, Dose-dependent modulation of interferon regulated genes with administration of single and repeat doses of rontalizumab in a phase I, placebo controlled, double blind, dose escalation study in SLE. ACR Annual Scientific Meeting 2009.
  • Yao Y, Richman L, Higgs BW, Morehouse CA, de los Reyes M, Brohawn P, Neutralization of interferon-α?β-inducible genes and downstream effect in a phase I trial of an anti-interferon-α monoclonal antibody in systemic lupus erythematosus. Arthritis Rheum. 2009;60:1785–96.
  • Rönnblom L, Alm GV. An etiopathogenic role for the type I IFN system in SLE. Trends Immunol. 2001;22:427–31.
  • Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol Rev. 2004;202:8–32.
  • Dzionek A, Sohma Y, Nagafune J, Cella M, Colonna M, Facchetti F, BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon α?β induction. J Exp Med. 2001;194:1823–34.
  • Barrat FJ, Coffman RL. Development of TLR inhibitors for the treatment of autoimmune diseases. Immunol Rev. 2008;223:271–83.
  • Rönnblom L. Potential role of IFNα in adult lupus. Arthritis Res Ther. 2010;12 1S3.