Cause and consequences of the activated type I interferon system in SLE

Journal of Molecular Medicine

Volumn 94, Issue 10, 2016, Pages 1103-1110

  Eloranta, Maija Leena ^a   Rönnblom, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Etiopathogenesis; Immune regulation; Plasmacytoid dendritic cells; Systemic lupus erythematosus; Type I interferon

Indexed keywords

INTERFERON; INTERFERON REGULATORY FACTOR 7; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; ALPHA BETA INTERFERON RECEPTOR;

CELLULAR DISTRIBUTION; DNA RNA HYBRIDIZATION; ENVIRONMENTAL FACTOR; EXTRACELLULAR TRAP; GENETIC BACKGROUND; GENETIC VARIABILITY; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INTERFERON PRODUCTION; NEGATIVE FEEDBACK; PLASMACYTOID DENDRITIC CELL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANTAGONISTS AND INHIBITORS; GENETICS; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC;

INTERFERON TYPE I; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTOR, INTERFERON ALPHA-BETA;

EID: 84964321086     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-016-1421-4     Document Type: Review

References (72)

1. Rönnblom L, Alm GV (2001) An etiopathogenic role for the type I IFN system in SLE. Trends Immunol 22:427–431
2. Rönnblom L, Alm GV, Eloranta ML (2011) The type I interferon system in the development of lupus. Semin Immunol 23:113–121
3. Smith PP, Gordon C (2010) Systemic lupus erythematosus: clinical presentations. Autoimmun Rev 10:43–45
4. Tsokos GC (2011) Systemic lupus erythematosus. N Engl J Med 365:2110–2121
5. Crow MK, Olferiev M, Kirou KA (2015) Targeting of type I interferon in systemic autoimmune diseases. Transl Res 165:296–305
6. Yaniv G, Twig G, Shor DB, Furer A, Sherer Y, Mozes O, Komisar O, Slonimsky E, Klang E, Lotan E et al (2015) A volcanic explosion of autoantibodies in systemic lupus erythematosus: a diversity of 180 different antibodies found in SLE patients. Autoimmun Rev 14:75–79
7. Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Harley JB (2003) Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 349:1526–1533
8. Agmon-Levin N, Mosca M, Petri M, Shoenfeld Y (2012) Systemic lupus erythematosus one disease or many? Autoimmun Rev 11:593–595
9. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V (2003) Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 197:711–723
10. Rönnblom L, Eloranta M-L (2013) The interferon signature in autoimmune diseases. Curr Opin Rheumatol 25:248–253
11. Crow MK (2014) Advances in understanding the role of type I interferons in systemic lupus erythematosus. Curr Opin Rheumatol 26:467–474
12. Gürtler C, Bowie AG (2013) Innate immune detection of microbial nucleic acids. Trends Microbiol 21:413–420
13. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373–384
14. Rigby RE, Webb LM, Mackenzie KJ, Li Y, Leitch A, Reijns MA, Lundie RJ, Revuelta A, Davidson DJ, Diebold S et al (2014) RNA:DNA hybrids are a novel molecular pattern sensed by TLR9. EMBO J 33:542–558
15. Fitzgerald-Bocarsly P, Feng D (2007) The role of type I interferon production by dendritic cells in host defense. Biochimie 89:843–855
16. Swiecki M, Colonna M (2015) The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol 15:471–485
17. Wu J, Chen ZJ (2014) Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461–488
18. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV et al (2015) Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 347(6227):aaa2630
19. Båve U, Magnusson M, Eloranta ML, Perers A, Alm GV, Rönnblom L (2003) FcgRIIa 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 171:3296–3302
20. Lövgren T, Eloranta ML, Kastner B, Wahren-Herlenius M, Alm GV, Rönnblom L (2006) Induction of interferon-α by immune complexes or liposomes containing systemic lupus erythematosus autoantigen- and Sjögren’s syndrome autoantigen-associated RNA. Arthritis Rheum 54:1917–1927
21. Pinegin B, Vorobjeva N, Pinegin V (2015) Neutrophil extracellular traps and their role in the development of chronic inflammation and autoimmunity. Autoimmun Rev 14:633–640
22. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A (2010) Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A 107:9813–9818
23. Leffler J, Ciacma K, Gullstrand B, Bengtsson AA, Martin M, Blom AM (2015) A subset of patients with systemic lupus erythematosus fails to degrade DNA from multiple clinically relevant sources. Arthritis Res Ther 17:205
24. Lood C, Blanco LP, Purmalek MM, Carmona-Rivera C, De Ravin SS, Smith CK, Malech HL, Ledbetter JA, Elkon KB, Kaplan MJ (2016) Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med
25. Schneider WM, Chevillotte MD, Rice CM (2014) Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 32:513–545
26. Hoffmann H-HH, Schneider WM, Rice CM (2015) Interferons and viruses: an evolutionary arms race of molecular interactions. Trends Immunol 36:124–138
27. Platanias LC (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5:375–386
28. Barbhaiya M, Costenbader KH (2014) Ultraviolet radiation and systemic lupus erythematosus. Lupus 23:588–595
29. Kuhn A, Wenzel J, Bijl M (2016) Lupus erythematosus revisited. Semin Immunopathol 38:97–112
30. Wack A, Terczynska-Dyla E, Hartmann R (2015) Guarding the frontiers: the biology of type III interferons. Nat Immunol 16:802–809
31. Zahn S, Rehkamper C, Kummerer BM, Ferring-Schmidt S, Bieber T, Tuting T, Wenzel J (2011) Evidence for a pathophysiological role of keratinocyte-derived type III interferon (IFNlambda) in cutaneous lupus erythematosus. J Investig Dermatol 131:133–140
32. Kemp MG, Lindsey-Boltz LA, Sancar A (2015) UV light potentiates STING (Stimulator of Interferon Genes)-dependent innate immune signaling through deregulation of ULK1 (Unc51-like Kinase 1). J Biol Chem 290:12184–12194
33. Rubin RL (2015) Drug-induced lupus. Expert Opin Drug Saf 14:361–378
34. Biggar KK, Li SS (2015) Non-histone protein methylation as a regulator of cellular signalling and function. Nat Rev Mol Cell Biol 16:5–17
35. Deapen D, Escalante A, Weinrib L, Horwitz D, Bachman B, Roy-Burman P, Walker A, Mack TM (1992) A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis Rheum 35:311–318
36. Tsao BP, Deng Y (2011) Constitutive genes and lupus. In: Lahita RG (ed) Systemic lupus erythematosus, 5th edn. Elsevier, London
37. Cui Y, Sheng Y, Zhang X (2013) Genetic susceptibility to SLE: recent progress from GWAS. J Autoimmun 41:25–33
38. Deng Y, Tsao BP (2014) Advances in lupus genetics and epigenetics. Curr Opin Rheumatol 26:482–492
39. Bentham J, Morris DL, Cunninghame Graham DS, Pinder CL, Tombleson P, Behrens TW, Martin J, Fairfax BP, Knight JC, Chen L et al (2015) Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat Genet 47:1457–1464
40. Bronson PG, Chaivorapol C, Ortmann W, Behrens TW, Graham RR (2012) The genetics of type I interferon in systemic lupus erythematosus. Curr Opin Immunol 24:530–537
41. Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK (2008) Association of the IRF5 risk haplotype with high serum interferon-alpha activity in systemic lupus erythematosus patients. Arthritis Rheum 58:2481–2487
42. Berggren O, Alexsson A, Morris DL, Tandre K, Weber G, Vyse TJ, Syvänen A-CC, Rönnblom L, Eloranta M-L (2015) IFN-α production by plasmacytoid dendritic cell associations with polymorphisms in gene loci related to autoimmune and inflammatory diseases. Hum Mol Genet 24:3571–3581
43. Crow YJ (2011) Lupus: how much “complexity” is really (just) genetic heterogeneity? Arthritis Rheum 63:3661–3664
44. Elkon KB, Santer DM (2012) Complement, interferon and lupus. Curr Opin Immunol 24:665–670
45. Lee-Kirsch MA, Gong M, Chowdhury D, Senenko L, Engel K, Lee YA, de Silva U, Bailey SL, Witte T, Vyse TJ et al (2007) Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat Genet 39:1065–1067
46. Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Rönnblom L, Sturfelt G, Eloranta ML, Bengtsson AA (2009) C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 60:3081–3090
47. Santer DM, Hall BE, George TC, Tangsombatvisit S, Liu CL, Arkwright PD, Elkon KB (2010) C1q deficiency leads to the defective suppression of IFN-alpha in response to nucleoprotein containing immune complexes. J Immunol 185:4738–4749
48. Hertzog P, Forster S, Samarajiwa S (2011) Systems biology of interferon responses. J Interferon Cytokine Res 31:5–11
49. Gonzalez-Navajas JM, Lee J, David M, Raz E (2012) Immunomodulatory functions of type I interferons. Nat Rev Immunol 12:125–135
50. Schreiber G, Piehler J (2015) The molecular basis for functional plasticity in type I interferon signaling. Trends Immunol 36:139–149
51. McNab F, Mayer-Barber K, Sher A, Wack A, O’Garra A (2015) Type I interferons in infectious disease. Nat Rev Immunol 15:87–103
52. Grammatikos AP, Tsokos GC (2012) Immunodeficiency and autoimmunity: lessons from systemic lupus erythematosus. Trends Mol Med 18:101–108
53. Swiecki M, Colonna M (2010) Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 234:142–162
54. Alunno A, Bartoloni E, Bistoni O, Nocentini G, Ronchetti S, Caterbi S, Valentini V, Riccardi C, Gerli R (2012) Balance between regulatory T and Th17 cells in systemic lupus erythematosus: the old and the new. Clin Dev Immunol 2012:823085
55. Lopez P, Rodriguez-Carrio J, Caminal-Montero L, Mozo L, Suarez A (2016) A pathogenic IFNalpha, BLyS and IL-17 axis in systemic lupus erythematosus patients. Sci Rep 6:1–9
56. Vazquez MI, Catalan-Dibene J, Zlotnik A (2015) B cells responses and cytokine production are regulated by their immune microenvironment. Cytokine 74:318–326
57. Jackson SW, Kolhatkar NS, Rawlings DJ (2015) B cells take the front seat: dysregulated B cell signals orchestrate loss of tolerance and autoantibody production. Curr Opin Immunol 33:70–77
58. Thacker SG, Zhao W, Smith CK, Luo W, Wang H, Vivekanandan-Giri A, Rabquer BJ, Koch AE, Pennathur S, Davidson A et al (2012) Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum 64:2975–2985
59. Knight JS, Kaplan MJ (2013) Cardiovascular disease in lupus: insights and updates. Curr Opin Rheumatol 25:597–605
60. Eloranta M, Alm GV, Rönnblom L (2013) Disease mechanisms in rheumatology—tools and pathways: plasmacytoid dendritic cells and their role in autoimmune rheumatic diseases. Arthritis Rheum 65:853–863
61. Savan R (2014) Post-transcriptional regulation of interferons and their signaling pathways. J Interferon Cytokine Res 34:318–329
62. Eloranta ML, Lövgren T, Finke D, Mathsson L, Rönnelid J, Kastner B, Alm GV, Rönnblom L (2009) Regulation of the interferon-alpha production induced by RNA-containing immune complexes in plasmacytoid dendritic cells. Arthritis Rheum 60:2418–2427
63. Berggren O, Hagberg N, Weber G, Alm GV, Rönnblom L, Eloranta ML (2012) B lymphocytes enhance the interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum 64:3409–3419
64. Leonard D, Eloranta ML, Hagberg N, Berggren O, Tandre K, Alm G, Ronnblom L (2015) Activated T cells enhance interferon-alpha production by plasmacytoid dendritic cells stimulated with RNA-containing immune complexes. Ann Rheum Dis. doi:10.1136/annrheumdis-2015-208055
65. Hagberg N, Berggren O, Leonard D, Weber G, Bryceson YT, Alm GV, Eloranta ML, Ronnblom L (2011) IFN-alpha production by plasmacytoid dendritic cells stimulated with RNA-containing immune complexes is promoted by NK cells via MIP-1beta and LFA-1. J Immunol 186:5085–5094
66. Privratsky JR, Newman DK, Newman PJ (2010) PECAM-1: conflicts of interest in inflammation. Life Sci 87:69–82
67. Clement M, Fornasa G, Loyau S, Morvan M, Andreata F, Guedj K, Khallou-Laschet J, Larghi P, Le Roux D, Bismuth G et al (2015) Upholding the T cell immune-regulatory function of CD31 inhibits the formation of T/B immunological synapses in vitro and attenuates the development of experimental autoimmune arthritis in vivo. J Autoimmun 56:23–33
68. Furie R, Merrill JT, Werth VP, Khamashta M, Kalunian K, Brohawn P, Illei G, Drappa J, Wang L, Yoo S (2015) Anifrolumab, an anti-interferon alpha receptor monoclonal antibody, in moderate to severe systemic lupus erythematosus (SLE). Arthritis Rheumatol 67(S10)
69. Sun X, Wiedeman A, Agrawal N, Teal TH, Tanaka L, Hudkins KL, Alpers CE, Bolland S, Buechler MB, Hamerman JA et al (2013) Increased ribonuclease expression reduces inflammation and prolongs survival in TLR7 transgenic mice. J Immunol 190:2536–2543
70. Pellerin A, Otero K, Czerkowicz JM, Kerns HM, Shapiro RI, Ranger AM, Otipoby KL, Taylor FR, Cameron TO, Viney JL et al (2015) Anti-BDCA2 monoclonal antibody inhibits plasmacytoid dendritic cell activation through Fc-dependent and Fc-independent mechanisms. EMBO Mol Med 7:464–476
71. Ichikawa HT, Conley T, Muchamuel T, Jiang J, Lee S, Owen T, Barnard J, Nevarez S, Goldman BI, Kirk CJ et al (2012) Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. Arthritis Rheum 64:493–503
72. Volkman HE, Stetson DB (2014) The enemy within: endogenous retroelements and autoimmune disease. Nat Immunol 15:415–422