Physiological evidence for diversification of IFNaα- and IFNβ-mediated response programs in different autoimmune diseases

Arthritis Research and Therapy

Volumn 18, Issue 1, 2016, Pages

  de Jong, Tamarah D ^a   Vosslamber, Saskia ^a   Mantel, Elise ^a   de Ridder, Sander ^a   Wesseling, John G ^a   van der Pouw Kraan, Tineke C T M ^a   Leurs, Cyra ^a   Hegen, Harald ^b   Deisenhammer, Florian ^b   Killestein, Joep ^a   Lundberg, Ingrid E ^c   Vencovsky, Jiri ^d   Nurmohamed, Mike T ^e   van Schaardenburg, Dirkjan ^e   Bultink, Irene E M ^a   Voskuyl, Alexandre E ^a   Pegtel, D Michiel ^a   van der Laken, Conny J ^a   Bijlsma, Johannes W J ^a,e   Verweij, Cornelis L ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d INSTITUTE OF RHEUMATOLOGY   (Czech Republic)

^e Reade ^*  (Netherlands)

Author keywords

Autoimmune diseases; Gene expression profiling; Multiple sclerosis; Rheumatic diseases; Type I interferons

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON;

ADULT; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; FEMALE; GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MULTIPLE SCLEROSIS; MYOSITIS; RHEUMATOID ARTHRITIS; SCORING SYSTEM; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION REGULATION; TREATMENT RESPONSE; TYPE I IFN RESPONSE GENE; UPREGULATION; VALIDATION STUDY; AGED; AUTOIMMUNE DISEASES; BLOOD; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MIDDLE AGED; TREATMENT OUTCOME;

ADULT; AGED; AUTOIMMUNE DISEASES; FEMALE; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; TREATMENT OUTCOME;

EID: 84958012909     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-016-0946-9     Document Type: Article

References (52)

1. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-64.
2. Takaoka A, Taniguchi T. New aspects of IFN-alpha/beta signalling in immunity, oncogenesis and bone metabolism. Cancer Sci. 2003;94:405-11.
3. Ghislain JJ, Fish EN. Application of genomic DNA affinity chromatography identifies multiple interferon-alpha-regulated Stat2 complexes. J Biol Chem. 1996;271:12408-13.
4. Li X, Leung S, Qureshi S, Darnell Jr. JE, Stark GR. Formation of STAT1-STAT2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-alpha. J Biol Chem. 1996;271:5790-4.
5. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, et al. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov. 2007;6:975-90.
6. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol. 2008;89:1-47.
7. Higgs BW, Liu Z, White B, Zhu W, White WI, Morehouse C, et al. Patients with systemic lupus erythematosus, myositis, rheumatoid arthritis and scleroderma share activation of a common type I interferon pathway. Ann Rheum Dis. 2011;70:2029-36.
8. Bave U, Nordmark G, Lovgren T, Ronnelid J, Cajander S, Eloranta ML, et al. Activation of the type I interferon system in primary Sjogren's syndrome: a possible etiopathogenic mechanism. Arthritis Rheum. 2005;52:1185-95.
9. van Baarsen LG, van der Pouw Kraan TC, Kragt JJ, Baggen JM, Rustenburg F, Hooper T, et al. A subtype of multiple sclerosis defined by an activated immune defense program. Genes Immun. 2006;7:522-31.
10. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001;294:1540-3.
11. Kirou KA, Lee C, George S, Louca K, Peterson MG, Crow MK. Activation of the interferon-alpha pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 2005;52:1491-503.
12. Ronnblom L, Alm GV, Eloranta ML. The type I interferon system in the development of lupus. Semin Immunol. 2011;23:113-21.
13. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197:711-23.
14. Dall'era MC, Cardarelli PM, Preston BT, Witte A, Davis Jr. JC. Type I interferon correlates with serological and clinical manifestations of SLE. Ann Rheum Dis. 2005;64:1692-7.
15. Ronnblom LE, Alm GV, Oberg KE. Possible induction of systemic lupus erythematosus by interferon-alpha treatment in a patient with a malignant carcinoid tumour. J Intern Med. 1990;227:207-10.
16. Ho V, Mclean A, Terry S. Severe systemic lupus erythematosus induced by antiviral treatment for hepatitis C. J Clin Rheumatol. 2008;14:166-8.
17. Hafler DA, Slavik JM, Anderson DE, O'Connor KC, de Jager P, Baecher-Allan C. Multiple sclerosis. Immunol Rev. 2005;204:208-31.
18. Interferon beta-1b in the treatment of multiple sclerosis: final outcome of the randomized controlled trial. The IFNB Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. Neurology. 1995; 45:1277-85.
19. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, et al. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis. 2003;8:237-49.
20. Taniguchi T, Mantei N, Schwarzstein M, Nagata S, Muramatsu M, Weissmann C. Human leukocyte and fibroblast interferons are structurally related. Nature. 1980;285:547-9.
21. Jaitin DA, Roisman LC, Jaks E, Gavutis M, Piehler J, Van der Heyden J, et al. Inquiring into the differential action of interferons (IFNs): an IFN-alpha2 mutant with enhanced affinity to IFNAR1 is functionally similar to IFN-beta. Mol Cell Biol. 2006;26:1888-97.
22. Lewerenz M, Mogensen KE, Uze G. Shared receptor components but distinct complexes for alpha and beta interferons. J Mol Biol. 1998;282:585-99.
23. Platanias LC, Uddin S, Domanski P, Colamonici OR. Differences in interferon alpha and beta signaling. Interferon beta selectively induces the interaction of the alpha and betaL subunits of the type I interferon receptor. J Biol Chem. 1996;271:23630-3.
24. Johns TG, Mackay IR, Callister KA, Hertzog PJ, Devenish RJ, Linnane AW. Antiproliferative potencies of interferons on melanoma cell lines and xenografts: higher efficacy of interferon beta. J Natl Cancer Inst. 1992;84:1185-90.
25. Hegen H, Millonig A, Bertolotto A, Comabella M, Giovanonni G, Guger M, et al. Early detection of neutralizing antibodies to interferon-beta in multiple sclerosis patients: binding antibodies predict neutralizing antibody development. Mult Scler. 2014;20:577-87.
26. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA. 2003;100:2610-5.
27. van Baarsen LG, Vosslamber S, Tijssen M, Baggen JM, van der Voort LF, Killestein J, et al. Pharmacogenomics of interferon-beta therapy in multiple sclerosis: baseline IFN signature determines pharmacological differences between patients. PLoS One. 2008;3:e1927.
28. van der Pouw Kraan TC, Wijbrandts CA, van Baarsen LG, Voskuyl AE, Rustenburg F, Baggen JM, et al. Rheumatoid arthritis subtypes identified by genomic profiling of peripheral blood cells: assignment of a type I interferon signature in a subpopulation of patients. Ann Rheum Dis. 2007;66:1008-14.
29. Raterman HG, Vosslamber S, de Ridder S, Nurmohamed MT, Lems WF, Boers M, et al. The interferon type I signature towards prediction of non-response to rituximab in rheumatoid arthritis patients. Arthritis Res Ther. 2012;14:R95.
30. Greenberg SA, Higgs BW, Morehouse C, Walsh RJ, Kong SW, Brohawn P, et al. Relationship between disease activity and type 1 interferon- and other cytokine-inducible gene expression in blood in dermatomyositis and polymyositis. Genes Immun. 2012;13:207-13.
31. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998;95:14863-8.
32. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207-10.
33. Lee HM, Sugino H, Aoki C, Nishimoto N. Underexpression of mitochondrial-DNA encoded ATP synthesis-related genes and DNA repair genes in systemic lupus erythematosus. Arthritis Res Ther. 2011;13:R63.
34. Nickles D, Chen HP, Li MM, Khankhanian P, Madireddy L, Caillier SJ, et al. Blood RNA profiling in a large cohort of multiple sclerosis patients and healthy controls. Hum Mol Genet. 2013;22:4194-205.
35. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Cumming H, et al. Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res. 2013;41:D1040-6.
36. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004;32:W273-9.
37. Eloranta ML, Barbasso HS, Ulfgren AK, Ronnblom 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-Ro 52/anti-Ro 60 autoantibodies. Arthritis Rheum. 2007;56:3112-24.
38. Mavragani CP, La DT, Stohl W, Crow MK. Association of the response to tumor necrosis factor antagonists with plasma type I interferon activity and interferon-beta/alpha ratios in rheumatoid arthritis patients: a post hoc analysis of a predominantly Hispanic cohort. Arthritis Rheum. 2010;62:392-401.
39. Platanias LC, Uddin S, Colamonici OR. Tyrosine phosphorylation of the alpha and beta subunits of the type I interferon receptor. Interferon-beta selectively induces tyrosine phosphorylation of an alpha subunit-associated protein. J Biol Chem. 1994;269:17761-4.
40. Deonarain R, Verma A, Porter AC, Gewert DR, Platanias LC, Fish EN. Critical roles for IFN-beta in lymphoid development, myelopoiesis, and tumor development: links to tumor necrosis factor alpha. Proc Natl Acad Sci USA. 2003;100:13453-8.
41. Marijanovic Z, Ragimbeau J, Van der Heyden J, Uze G, Pellegrini S. Comparable potency of IFNalpha2 and IFNbeta on immediate JAK/STAT activation but differential down-regulation of IFNAR2. Biochem J. 2007;407:141-51.
42. de Weerd NA, Vivian JP, Nguyen TK, Mangan NE, Gould JA, Braniff SJ, et al. Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1. Nat Immunol. 2013;14:901-7.
43. Moraga I, Harari D, Schreiber G, Uze G, Pellegrini S. Receptor density is key to the alpha2/beta interferon differential activities. Mol Cell Biol. 2009;29:4778-87.
44. 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. 2007;366:525-39.
45. Piehler J, Thomas C, Garcia KC, Schreiber G. Structural and dynamic determinants of type I interferon receptor assembly and their functional interpretation. Immunol Rev. 2012;250:317-34.
46. 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.
47. Dhib-Jalbut S, Marks S. Interferon-beta mechanisms of action in multiple sclerosis. Neurology. 2010;74 Suppl 1:S17-24.
48. Der SD, Zhou A, Williams BR, Silverman RH. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA. 1998;95:15623-8.
49. van Boxel-Dezaire AH, Zula JA, Xu Y, Ransohoff RM, Jacobberger JW, Stark GR. Major differences in the responses of primary human leukocyte subsets to IFN-beta. J Immunol. 2010;185:5888-99.
50. Ghislain JJ, Wong T, Nguyen M, Fish EN. The interferon-inducible Stat2:Stat1 heterodimer preferentially binds in vitro to a consensus element found in the promoters of a subset of interferon-stimulated genes. J Interferon Cytokine Res. 2001;21:379-88.
51. Brierley MM, Fish EN. Functional relevance of the conserved DNA-binding domain of STAT2. J Biol Chem. 2005;280:13029-36.
52. Meraro D, Gleit-Kielmanowicz M, Hauser H, Levi BZ. IFN-stimulated gene 15 is synergistically activated through interactions between the myelocyte/lymphocyte-specific transcription factors, PU.1, IFN regulatory factor-8/IFN consensus sequence binding protein, and IFN regulatory factor-4: characterization of a new subtype of IFN-stimulated response element. J Immunol. 2002;168:6224-31.