Autoimmune disease risk variant of IFIH1 is associated with increased sensitivity to IFN-α and serologic autoimmunity in lupus patients

Journal of Immunology

Volumn 187, Issue 3, 2011, Pages 1298-1303

  Robinson, Talin ^a,b   Kariuki, Silvia N ^a,b   Franek, Beverly S ^a,b   Kumabe, Marissa ^a,b   Kumar, Akaash A ^a,b   Badaracco, Maria ^a,b   Mikolaitis, Rachel A ^c   Guerrero, Galen ^d   Utset, Tammy O ^a,b   Drevlow, Barbara E ^d   Zaacks, Laura S ^d   Grober, James S ^d   Cohen, Lewis M ^d   Kirou, Kyriakos A ^e   Crow, Mary K ^e   Jolly, Meenakshi ^c   Niewold, Timothy B ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c RUSH UNIVERSITY   (United States)

^d NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^e HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; DEAD BOX PROTEIN; DOUBLE STRANDED DNA ANTIBODY; INTERFERON INDUCED WITH HELICASE C DOMAIN 1; LA ANTIBODY; RIBONUCLEOPROTEIN ANTIBODY; RO ANTIBODY; SM ANTIBODY; STAT4 PROTEIN; UNCLASSIFIED DRUG;

AFRICAN AMERICAN; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; EUROPEAN AMERICAN; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC RISK; GENOTYPE; HISPANIC; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS;

ALLELES; AUTOANTIBODIES; CELL LINE; DEAD-BOX RNA HELICASES; DNA; GENETIC VARIATION; HUMANS; INTERFERON-ALPHA; LUPUS ERYTHEMATOSUS, SYSTEMIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS; SIGNAL TRANSDUCTION;

EID: 80051619284     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100857     Document Type: Article

References (44)

1. Harley, J. B., J. A. Kelly, and K. M. Kaufman. 2006. Unraveling the genetics of systemic lupus erythematosus. Springer Semin. Immunopathol. 28: 119-130. (Pubitemid 44526313)
2. Niewold, T. B., D. N. Clark, R. Salloum, and B. D. Poole. 2010. Interferon alpha in systemic lupus erythematosus. J. Biomed. Biotechnol. 2010: 948364.
3. Kariuki, S. N., and T. B. Niewold. 2010. Genetic regulation of serum cytokines in systemic lupus erythematosus. Transl. Res. 155: 109-117.
4. Rönnblom, L. E., G. V. Alm, and K. E. Oberg. 1990. Possible induction of systemic lupus erythematosus by interferon-alpha treatment in a patient with a malignant carcinoid tumour. J. Intern. Med. 227: 207-210. (Pubitemid 20075945)
5. Niewold, T. B., and W. I. Swedler. 2005. Systemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis C. Clin. Rheumatol. 24: 178-181. (Pubitemid 40552976)
6. Niewold, T. B. 2008. Interferon alpha-induced lupus: proof of principle. J. Clin. Rheumatol. 14: 131-132.
7. Weckerle, C. E., B. S. Franek, J. A. Kelly, M. Kumabe, R. A. Mikolaitis, S. L. Green, T. O. Utset, M. Jolly, J. A. James, J. B. Harley, and T. B. Niewold. 2011. Network analysis of associations between serum interferon-a activity, autoantibodies, and clinical features in systemic lupus erythematosus. Arthritis Rheum. 63: 1044-1053.
8. Niewold, T. B., J. Hua, T. J. Lehman, J. B. Harley, and M. K. Crow. 2007. High serum IFN-alpha activity is a heritable risk factor for systemic lupus erythematosus. Genes Immun. 8: 492-502. (Pubitemid 47365615)
9. Niewold, T. B., J. E. Adler, S. B. Glenn, T. J. Lehman, J. B. Harley, and M. K. Crow. 2008. Age- and sex-related patterns of serum interferon-alpha activity in lupus families. Arthritis Rheum. 58: 2113-2119. (Pubitemid 351988103)
10. Kariuki, S. N., J. G. Moore, K. A. Kirou, M. K. Crow, T. O. Utset, and T. B. Niewold. 2009. Age- and gender-specific modulation of serum osteopontin and interferon-alpha by osteopontin genotype in systemic lupus erythematosus. Genes Immun. 10: 487-494.
11. Salloum, R., B. S. Franek, S. N. Kariuki, L. Rhee, R. A. Mikolaitis, M. Jolly, T. O. Utset, and T. B. Niewold. 2010. Genetic variation at the IRF7/PHRF1 locus is associated with autoantibody profile and serum interferon-alpha activity in lupus patients. Arthritis Rheum. 62: 553-561.
12. Niewold, T. B., J. A. Kelly, M. H. Flesch, L. R. Espinoza, J. B. Harley, and M. K. Crow. 2008. Association of the IRF5 risk haplotype with high serum interferon-alpha activity in systemic lupus erythematosus patients. Arthritis Rheum. 58: 2481-2487.
13. Kariuki, S. N., K. A. Kirou, E. J. MacDermott, L. Barillas-Arias, M. K. Crow, and T. B. Niewold. 2009. Cutting edge: autoimmune disease risk variant of STAT4 confers increased sensitivity to IFN-alpha in lupus patients in vivo. J. Immunol. 182: 34-38.
14. Harley, I. T. W., T. B. Niewold, R. M. Stormont, K. M. Kaufman, S. B. Glenn, B. S. Franek, J. A. Kelly, J. R. Kilpatrick, D. Hutchings, J. Divers, et al. 2010. The role of genetic variation near interferon-kappa in systemic lupus erythematosus. J. Biomed. Biotechnol. 2010: 706825.
15. Kariuki, S. N., M. K. Crow, and T. B. Niewold. 2008. The PTPN22 C1858T polymorphism is associated with skewing of cytokine profiles toward high interferon-alpha activity and low tumor necrosis factor alpha levels in patients with lupus. Arthritis Rheum. 58: 2818-2823.
16. Wilkins, C., and M. Gale Jr. 2010. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 22: 41-47.
17. Smyth, D. J., J. D. Cooper, R. Bailey, S. Field, O. Burren, L. J. Smink, C. Guja, C. Ionescu-Tirgoviste, B. Widmer, D. B. Dunger, et al. 2006. A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferon-induced helicase (IFIH1) region. Nat. Genet. 38: 617-619. (Pubitemid 43927300)
18. Sutherland, A., J. Davies, C. J. Owen, S. Vaikkakara, C. Walker, T. D. Cheetham, R. A. James, P. Perros, P. T. Donaldson, H. J. Cordell, et al. 2007. Genomic polymorphism at the interferon-induced helicase (IFIH1) locus contributes to Graves' disease susceptibility. J. Clin. Endocrinol. Metab. 92: 3338-3341. (Pubitemid 47236412)
19. Strange, A., F. Capon, C. C. Spencer, J. Knight, M. E. Weale, M. H. Allen, A. Barton, G. Band, C. Bellenguez, J. G. Bergboer, et al; Genetic Analysis of Psoriasis Consortium & the Wellcome Trust Case Control Consortium 2. 2010. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat. Genet. 42: 985-990.
20. Harley, J. B., M. E. Alarcón-Riquelme, L. A. Criswell, C. O. Jacob, R. P. Kimberly, K. L. Moser, B. P. Tsao, T. J. Vyse, C. D. Langefeld, S. K. Nath, et al International Consortium for Systemic Lupus Erythematosus Genetics (SLEGEN). 2008. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 40: 204-210. (Pubitemid 351171405)
21. Gateva, V., J. K. Sandling, G. Hom, K. E. Taylor, S. A. Chung, X. Sun, W. Ortmann, R. Kosoy, R. C. Ferreira, G. Nordmark, et al. 2009. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat. Genet. 41: 1228-1233.
22. Nejentsev, S., N. Walker, D. Riches, M. Egholm, and J. A. Todd. 2009. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324: 387-389.
23. Downes, K., M. Pekalski, K. L. Angus, M. Hardy, S. Nutland, D. J. Smyth, N. M. Walker, C. Wallace, and J. A. Todd. 2010. Reduced expression of IFIH1 is protective for type 1 diabetes. PLoS One 5: e12646.
24. Zouk, H., L. Marchand, and C. Polychronakos. 2010. Study of transcriptional effects in Cis at the IFIH1 locus. PLoS One 5: e11564.
25. Kariuki, S. N., B. S. Franek, R. A. Mikolaitis, T. O. Utset, M. Jolly, A. D. Skol, and T. B. Niewold. 2010. Promoter variant of PIK3C3 is associated with autoimmunity against Ro and Sm epitopes in African-American lupus patients. J. Biomed. Biotechnol. 2010: 826434.
26. Kariuki, S. N., B. S. Franek, A. A. Kumar, J. Arrington, R. A. Mikolaitis, T. O. Utset, M. Jolly, M. K. Crow, A. D. Skol, and T. B. Niewold. 2010. Trait-stratified genome-wide association study identifies novel and diverse genetic associations with serologic and cytokine phenotypes in systemic lupus erythematosus. Arthritis Res. Ther. 12: R151.
27. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25: 1271-1277. (Pubitemid 13221242)
28. Hua, J., K. Kirou, C. Lee, and M. K. Crow. 2006. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 54: 1906-1916. (Pubitemid 43877940)
29. Kirou, K. A., C. Lee, S. George, K. Louca, I. G. Papagiannis, M. G. Peterson, N. Ly, R. N. Woodward, K. E. Fry, A. Y. Lau, et al. 2004. Coordinate overexpression of interferon-alpha-induced genes in systemic lupus erythematosus. Arthritis Rheum. 50: 3958-3967. (Pubitemid 39643944)
30. Niewold, T. B., T. L. Rivera, J. P. Buyon, and M. K. Crow. 2008. Serum type I interferon activity is dependent on maternal diagnosis in anti-SSA/Ro-positive mothers of children with neonatal lupus. Arthritis Rheum. 58: 541-546. (Pubitemid 351294888)
31. Niewold, T. B., S. N. Kariuki, G. A. Morgan, S. Shrestha, and L. M. Pachman. 2009. Elevated serum interferon-alpha activity in juvenile dermatomyositis: associations with disease activity at diagnosis and after thirty-six months of therapy. Arthritis Rheum. 60: 1815-1824.
32. Purcell, S., B. Neale, K. Todd-Brown, L. Thomas, M. A. Ferreira, D. Bender, J. Maller, P. Sklar, P. I. de Bakker, M. J. Daly, and P. C. Sham. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81: 559-575. (Pubitemid 47330214)
33. Pothlichet, J., T. B. Niewold, D. Vitour, B. Solhonne, M. K. Crow, and M. Si-Tahar. 2011. A loss-of-function variant of the antiviral molecule MAVS is associated with a subset of systemic lupus patients. EMBO Mol. Med. 3: 142-152.
34. Chistiakov, D. A., N. V. Voronova, K. V. Savost'Anov, and R. I. Turakulov. 2010. Loss-of-function mutations E6 27X and I923V of IFIH1 are associated with lower poly(I:C)-induced interferon-β production in peripheral blood mononuclear cells of type 1 diabetes patients. Hum. Immunol. 71: 1128-1134.
35. James, J. A., K. M. Kaufman, A. D. Farris, E. Taylor-Albert, T. J. Lehman, and J. B. Harley. 1997. An increased prevalence of Epstein-Barr virus infection in young patients suggests a possible etiology for systemic lupus erythematosus. J. Clin. Invest. 100: 3019-3026. (Pubitemid 28022839)
36. Samanta, M., D. Iwakiri, T. Kanda, T. Imaizumi, and K. Takada. 2006. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J. 25: 4207-4214. (Pubitemid 44435218)
37. Poole, B. D., R. H. Scofield, J. B. Harley, and J. A. James. 2006. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity 39: 63-70. (Pubitemid 43878521)
38. Crow, M. K. 2010. Long interspersed nuclear elements (LINE-1): potential triggers of systemic autoimmune disease. Autoimmunity 43: 7-16.
39. Bauernfeind, F., A. Ablasser, S. Kim, E. Bartok, and V. Hornung. 2010. An unexpected role for RNA in the recognition of DNA by the innate immune system. RNA Biol. 7: 151-157.
40. Atamaniuk, J., Y. Y. Hsiao, M. Mustak, D. Bernhard, L. Erlacher, M. Fodinger, B. Tiran, and K. M. Stuhlmeier. 2011. Analysing cell-free plasma DNA and SLE disease activity. Eur. J. Clin. Invest. 41: 579-583.
41. Ioannou, Y., and D. A. Isenberg. 2000. Current evidence for the induction of autoimmune rheumatic manifestations by cytokine therapy. Arthritis Rheum. 43: 1431-1442. (Pubitemid 30452458)
42. Cantaert, T., L. De Rycke, C. P. Mavragani, C. A. Wijbrandts, T. B. Niewold, T. Niers, B. Vandooren, E. M. Veys, D. Richel, P. P. Tak, et al. 2009. Exposure to nuclear antigens contributes to the induction of humoral autoimmunity during tumour necrosis factor alpha blockade. Ann. Rheum. Dis. 68: 1022-1029.
43. Båve, U., G. Nordmark, T. Lövgren, J. Rönnelid, S. Cajander, M. L. Eloranta, G. V. Alm, and L. Rönnblom. 2005. Activation of the type I interferon system in primary Sjögren's syndrome: a possible etiopathogenic mechanism. Arthritis Rheum. 52: 1185-1195. (Pubitemid 40530126)
44. Devendra, D., and G. S. Eisenbarth. 2004. Interferon alpha - a potential link in the pathogenesis of viral-induced type 1 diabetes and autoimmunity. Clin. Immunol. 111: 225-233. (Pubitemid 38739316)