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Expert Review of Clinical Immunology Volume 3, 2007 - Issue 4
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Review

Activation of type I interferon in systemic lupus erythematosus

Kyriakos A Kirou Assistant Professor of Clinical Medicine and Assistant Scientist, Mary Kirkland Center for Lupus Research, Department of Medicine, Hospital for Special Surgery and Weill Medical College of Cornell University, 535 East 70th Street, New York, NY 10021, USA. [email protected]
,
Clio P Mavragani Post Doctoral Research Fellow, Mary Kirkland Center for Lupus Research, Department of Medicine, Hospital for Special Surgery and Weill Medical College of Cornell University, 535 East 70th Street, New York, NY 10021, USA. [email protected]
&
Mary K Crow Professor of Medicine and Senior Scientist, Mary Kirkland Center for Lupus Research, Department of Medicine, Hospital for Special Surgery and Weill Medical College of Cornell University, 535 East 70th Street, New York, NY 10021, USA. [email protected]
Pages 579-588 | Published online: 10 Jan 2014

References

  • Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc. R. Soc. Lond. B Biol. Sci.147(927), 258–267 (1957).
  • Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev.202, 8–32 (2004).
  • Jaks E, Gavutis M, Uze G, Martal J, Piehler J. Differential receptor subunit affinities of type I interferons govern differential signal activation. J. Mol. Biol.366(2), 525–539 (2007).
  • Jaitin DA, Roisman LC, Jaks E et al. Inquiring into the differential action of interferons (IFNs): an IFN-α2 mutant with enhanced affinity to IFNAR1 is functionally similar to IFN-β. Mol. Cell. Biol.26(5), 1888–1897 (2006).
  • Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-γ: an overview of signals, mechanisms and functions. J. Leukoc. Biol.75(2), 163–189 (2004).
  • Kotenko SV, Gallagher G, Baurin VV et al. IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol.4(1), 69–77 (2003).
  • Sheppard P, Kindsvogel W, Xu W et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol.4(1), 63–68 (2003).
  • Cella M, Jarrossay D, Facchetti F et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med.5(8), 919–923 (1999).
  • Siegal FP, Kadowaki N, Shodell M et al. The nature of the principal type 1 interferon-producing cells in human blood. Science284(5421), 1835–1837 (1999).
  • Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity25(3), 373–381 (2006).
  • Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell124(4), 783–801 (2006).
  • Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci. STKE2006(357), re13 (2006).
  • Honda K, Ohba Y, Yanai H et al. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature434(7036), 1035–1040 (2005).
  • Honda K, Yanai H, Negishi H et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature434(7034), 772–777 (2005).
  • Hoshino K, Sugiyama T, Matsumoto M et al. IκB kinase-α is critical for interferon-α production induced by Toll-like receptors 7 and 9. Nature440(7086), 949–953 (2006).
  • Honda K, Takaoka A, Taniguchi T. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity25(3), 349–360 (2006).
  • Vallin H, Blomberg S, Alm GV, Cederblad B, Ronnblom L. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-α (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin. Exp. Immunol.115(1), 196–202 (1999).
  • Vallin H, Perers A, Alm GV, Ronnblom L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J. Immunol.163(11), 6306–6313 (1999).
  • Lovgren T, Eloranta ML, Bave U, Alm GV, Ronnblom 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.50(6), 1861–1872 (2004).
  • Bave U, Alm GV, Ronnblom L. The combination of apoptotic U937 cells and lupus IgG is a potent IFN-α inducer. J. Immunol.165(6), 3519–3526 (2000).
  • Bave U, Magnusson M, Eloranta ML, Perers A, Alm GV, Ronnblom L. Fc γ RIIa 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.171(6), 3296–3302 (2003).
  • Means TK, Latz E, Hayashi F, Murali MR, Golenbock DT, Luster AD. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest.115(2), 407–417 (2005).
  • Vollmer J, Tluk S, Schmitz C et al. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med.202(11), 1575–1585 (2005).
  • Savarese E, Chae OW, Trowitzsch S et al. U1 small nuclear ribonucleoprotein immune complexes induce type I interferon in plasmacytoid dendritic cells through TLR7. Blood107(8), 3229–3234 (2006).
  • Lovgren T, Eloranta ML, Kastner B, Wahren-Herlenius M, Alm GV, Ronnblom L. Induction of interferon-α by immune complexes or liposomes containing systemic lupus erythematosus autoantigen- and Sjogren’s syndrome autoantigen-associated RNA. Arthritis Rheum.54(6), 1917–1927 (2006).
  • Kelly KM, Zhuang H, Nacionales DC et al. “Endogenous adjuvant” activity of the RNA components of lupus autoantigens Sm/RNP and Ro 60. Arthritis Rheum.54(5), 1557–1567 (2006).
  • Rice G, Newman WG, Dean J et al. Heterozygous mutations in TREX1 cause familial chilblain lupus and dominant Aicardi–Goutieres syndrome. Am. J. Hum. Genet.80(4), 811–815 (2007).
  • Crow YJ, Leitch A, Hayward BE et al. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi–Goutieres syndrome and mimic congenital viral brain infection. Nat. Genet.38(8), 910–916 (2006).
  • Crow YJ, Hayward BE, Parmar R et al. Mutations in the gene encoding the 3´-5´ DNA exonuclease TREX1 cause Aicardi–Goutieres syndrome at the AGS1 locus. Nat. Genet.38(8), 917–920 (2006).
  • 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.54(6), 1906–1916 (2006).
  • Kirou KA, Lee C, George S, Louca K, Peterson MG, Crow MK. Activation of the interferon-α pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum.52(5), 1491–1503 (2005).
  • Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science312(5780), 1669–1672 (2006).
  • Subramanian S, Tus K, Li QZ et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc. Natl Acad. Sci. USA103(26), 9970–9975 (2006).
  • Christensen SR, Shupe J, Nickerson K, Kashgarian M, Flavell RA, Shlomchik MJ. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity25(3), 417–428 (2006).
  • Bekeredjian-Ding IB, Wagner M, Hornung V et al. Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN. J. Immunol.174(7), 4043–4050 (2005).
  • Moseman EA, Liang X, Dawson AJ et al. Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J. Immunol.173(7), 4433–4442 (2004).
  • Sato K, Hida S, Takayanagi H et al. Antiviral response by natural killer cells through TRAIL gene induction by IFN-α/β. Eur. J. Immunol.31(11), 3138–3146 (2001).
  • Kirou KA, Vakkalanka RK, Butler MJ, Crow MK. Induction of Fas ligand-mediated apoptosis by interferon-α. Clin. Immunol.95(3), 218–226 (2000).
  • Nguyen KB, Salazar-Mather TP, Dalod MY et al. Coordinated and distinct roles for IFN-α β, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol.169(8), 4279–4287 (2002).
  • Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity8(5), 591–599 (1998).
  • Carrero JA, Calderon B, Unanue ER. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med.200(4), 535–540 (2004).
  • O’Connell RM, Saha SK, Vaidya SA et al. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med.200(4), 437–445 (2004).
  • Mancuso G, Midiri A, Biondo C et al. Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J. Immunol.178(5), 3126–3133 (2007).
  • Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-α in systemic lupus erythematosus. Science294(5546), 1540–1543 (2001).
  • Theofilopoulos AN, Baccala R, Beutler B, Kono DH. Type I interferons (α/β) in immunity and autoimmunity. Annu. Rev. Immunol.23, 307–336 (2005).
  • Havenar-Daughton C, Kolumam GA, Murali-Krishna K. Cutting edge: the direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J. Immunol.176(6), 3315–3319 (2006).
  • Tough DF, Borrow P, Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science272(5270), 1947–1950 (1996).
  • Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J. Exp. Med.189(3), 521–530 (1999).
  • 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. Immunity19(2), 225–234 (2003).
  • Le Bon A, Schiavoni G, D’Agostino G, Gresser I, Belardelli F, Tough DF. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity14(4), 461–470 (2001).
  • Lau CM, Broughton C, Tabor AS et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med.202(9), 1171–1177 (2005).
  • Sharif MN, Tassiulas I, Hu Y, Mecklenbrauker I, Tarakhovsky A, Ivashkiv LB. IFN-α priming results in a gain of proinflammatory function by IL-10: implications for systemic lupus erythematosus pathogenesis. J. Immunol.172(10), 6476–6481 (2004).
  • Bauer JW, Baechler EC, Petri M et al. Elevated serum levels of interferon-regulated chemokines are biomarkers for active human systemic lupus erythematosus. PLoS Med.3(12), E491 (2006).
  • Meller S, Winterberg F, Gilliet M et al. Ultraviolet radiation-induced injury, chemokines, and leukocyte recruitment: an amplification cycle triggering cutaneous lupus erythematosus. Arthritis Rheum.52(5), 1504–1516 (2005).
  • Yarilina A, DiCarlo E, Ivashkiv LB. Suppression of the effector phase of inflammatory arthritis by double-stranded RNA is mediated by type I IFNs. J. Immunol.178(4), 2204–2211 (2007).
  • Biron CA. Interferons α and β as immune regulators – a new look. Immunity14(6), 661–4 (2001).
  • Santiago-Raber ML, Baccala R, Haraldsson KM et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J. Exp. Med.197(6), 777–788 (2003).
  • Braun D, Geraldes P, Demengeot J. Type I interferon controls the onset and severity of autoimmune manifestations in lpr mice. J. Autoimmun.20(1), 15–25 (2003).
  • Jorgensen TN, Thurman J, Izui S et al. Genetic susceptibility to polyI:C-induced IFNα/β-dependent accelerated disease in lupus-prone mice. Genes Immun.7(7), 555–567 (2006).
  • Mathian A, Weinberg A, Gallegos M, Banchereau J, Koutouzov S. IFN-α induces early lethal lupus in preautoimmune (New Zealand Black × New Zealand White) F1 but not in BALB/c mice. J. Immunol.174(5), 2499–2506 (2005).
  • Hron JD, Peng SL. Type I IFN protects against murine lupus. J. Immunol.173(3), 2134–2142 (2004).
  • Schwarting A, Paul K, Tschirner S et al. Interferon-β: a therapeutic for autoimmune lupus in MRL-Faslpr mice. J. Am. Soc. Nephrol.16(11), 3264–3272 (2005).
  • von Wussow P, Jakschies D, Hartung K, Deicher H. Presence of interferon and anti-interferon in patients with systemic lupus erythematosus. Rheumatol. Int.8(5), 225–230 (1988).
  • Sibbitt WL Jr, Gibbs DL, Kenny C, Bankhurst AD, Searles RP, Ley KD. Relationship between circulating interferon and anti-interferon antibodies and impaired natural killer cell activity in systemic lupus erythematosus. Arthritis Rheum.28(6), 624–629 (1985).
  • Ytterberg SR, Schnitzer TJ. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum.25(4), 401–406 (1982).
  • Panem S, Ordonez N, Vilcek J. Renal deposition of α interferon in systemic lupus erythematosus. Infect. Immun.42(1), 368–373 (1983).
  • Shiozawa S, Kuroki Y, Kim M, Hirohata S, Ogino T. Interferon-α in lupus psychosis. Arthritis Rheum.35(4), 417–422 (1992).
  • Ronnblom LE, Alm GV, Oberg KE. Autoimmunity after α-interferon therapy for malignant carcinoid tumors. Ann. Intern. Med.115(3), 178–183 (1991).
  • Ronnblom LE, Alm GV, Oberg KE. Possible induction of systemic lupus erythematosus by interferon-α treatment in a patient with a malignant carcinoid tumour. J. Intern. Med.227(3), 207–210 (1990).
  • Bennett L, Palucka AK, Arce E et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med.197(6), 711–723 (2003).
  • Baechler EC, Batliwalla FM, Karypis G et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl Acad. Sci. USA100(5), 2610–2615 (2003).
  • Kirou KA, Lee C, George S et al. Coordinate overexpression of interferon-α-induced genes in systemic lupus erythematosus. Arthritis Rheum.50(12), 3958–3967 (2004).
  • Zhuang H, Narain S, Sobel E et al. Association of anti-nucleoprotein autoantibodies with upregulation of type I interferon-inducible gene transcripts and dendritic cell maturation in systemic lupus erythematosus. Clin. Immunol.117(3), 238–250 (2005).
  • Peterson KS, Huang JF, Zhu J et al. Characterization of heterogeneity in the molecular pathogenesis of lupus nephritis from transcriptional profiles of laser-captured glomeruli. J. Clin. Invest.113(12), 1722–1733 (2004).
  • Barrat FJ, Meeker T, Gregorio J et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med.202(8), 1131–1139 (2005).
  • Blomberg S, Eloranta ML, Cederblad B, Nordlin K, Alm GV, Ronnblom L. Presence of cutaneous interferon-α producing cells in patients with systemic lupus erythematosus. Lupus10(7), 484–490 (2001).
  • 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.159(1), 237–243 (2001).
  • Graham DS, Manku H, Wagner S et al. Association of IRF5 in UK SLE families identifies a variant involved in polyadenylation. Hum. Mol. Genet.16(6), 579–591 (2006).
  • Graham RR, Kozyrev SV, Baechler EC et al. A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat. Genet.38(5), 550–555 (2006).
  • Sigurdsson S, Nordmark G, Goring HH et al. Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am. J. Hum. Genet.76(3), 528–537 (2005).
  • Zhuang H, Kosboth M, Lee P et al. Lupus-like disease and high interferon levels corresponding to trisomy of the type I interferon cluster on chromosome 9p. Arthritis Rheum.54(5), 1573–1579 (2006).
  • Bave U, Nordmark G, Lovgren T et al. Activation of the type I interferon system in primary Sjogren’s syndrome: a possible etiopathogenic mechanism. Arthritis Rheum.52(4), 1185–1195 (2005).
  • Gottenberg JE, Cagnard N, Lucchesi C et al. Activation of IFN pathways and plasmacytoid dendritic cell recruitment in target organs of primary Sjogren’s syndrome. Proc. Natl Acad. Sci. USA103(8), 2770–2775 (2006).
  • James JA, Harley JB, Scofield RH. Role of viruses in systemic lupus erythematosus and Sjogren syndrome. Curr. Opin. Rheumatol.13(5), 370–376 (2001).
  • Triantafyllopoulou A, Tapinos N, Moutsopoulos HM. Evidence for coxsackievirus infection in primary Sjogren’s syndrome. Arthritis Rheum.50(9), 2897–2902 (2004).
  • 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.52(5), 1534–1544 (2005).
  • Wenzel J, Scheler M, Bieber T, Tuting T. Evidence for a role of type I interferons in the pathogenesis of dermatomyositis. Br. J. Dermatol.153(2), 462–463; author reply 463–464 (2005).
  • Zhou X, Dimachkie MM, Xiong M, Tan FK, Arnett FC. cDNA microarrays reveal distinct gene expression clusters in idiopathic inflammatory myopathies. Med. Sci. Monit.10(7), BR191–BR197 (2004).
  • Tan FK, Zhou X, Mayes MD et al. Signatures of differentially regulated interferon gene expression and vasculotrophism in the peripheral blood cells of systemic sclerosis patients. Rheumatology (Oxf.)45(6), 694–702 (2006).
  • Dong L, Ito S, Ishii KJ, Klinman DM. Suppressive oligodeoxynucleotides delay the onset of glomerulonephritis and prolong survival in lupus-prone NZB × NZW mice. Arthritis Rheum.52(2), 651–658 (2005).
  • Lenert PS. Targeting Toll-like receptor signaling in plasmacytoid dendritic cells and autoreactive B cells as a therapy for lupus. Arthritis Res. Ther.8(1), 203 (2006).
  • Patole PS, Zecher D, Pawar RD, Grone HJ, Schlondorff D, Anders HJ. G-rich DNA suppresses systemic lupus. J. Am. Soc. Nephrol.16(11), 3273–3280 (2005).
  • Davis JC Jr, Manzi S, Yarboro C et al. Recombinant human Dnase I (rhDNase) in patients with lupus nephritis. Lupus8(1), 68–76 (1999).
  • Blomberg S, Eloranta ML, Magnusson M, Alm GV, Ronnblom L. Expression of the markers BDCA-2 and BDCA-4 and production of interferon-α by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Rheum.48(9), 2524–32 (2003).
  • Abe M, Thomson AW. Dexamethasone preferentially suppresses plasmacytoid dendritic cell differentiation and enhances their apoptotic death. Clin. Immunol.118(2–3), 300–306 (2006).
  • Lebon P. Inhibition of herpes simplex virus type 1-induced interferon synthesis by monoclonal antibodies against viral glycoprotein D and by lysosomotropic drugs. J. Gen. Virol.66 (Pt 12), 2781–2786 (1985).
  • Mishra N, Reilly CM, Brown DR, Ruiz P, Gilkeson GS. Histone deacetylase inhibitors modulate renal disease in the MRL-lpr/lpr mouse. J. Clin. Invest.111(4), 539–552 (2003).
  • Chang HM, Paulson M, Holko M et al. Induction of interferon-stimulated gene expression and antiviral responses require protein deacetylase activity. Proc. Natl Acad. Sci. USA101(26), 9578–9583 (2004).
  • Mbow ML, Sarisky RT. What is disrupting IFN-α’s antiviral activity? Trends Biotechnol.22(8), 395–399 (2004).

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