Interferon regulatory factors: Critical mediators of human lupus

Translational Research

Volumn 165, Issue 2, 2015, Pages 283-295

  Jensen, Mark A ^a   Niewold, Timothy B ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 5; INTERFERON REGULATORY FACTOR 7; NUCLEIC ACID; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR; ANTIGEN ANTIBODY COMPLEX; AUTOANTIBODY;

ANTIGEN ANTIBODY COMPLEX; AUTOIMMUNITY; B LYMPHOCYTE; CLINICAL FEATURE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; HUMORAL IMMUNITY; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; BIOSYNTHESIS; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; SIGNAL TRANSDUCTION; TRANSLATIONAL RESEARCH;

ANTIGEN-ANTIBODY COMPLEX; AUTOANTIBODIES; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; HUMANS; INTERFERON REGULATORY FACTORS; INTERFERON TYPE I; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84921334545     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2014.10.002     Document Type: Review

References (144)

1. F. Goldblatt, and S.G. O'Neill Clinical aspects of autoimmune rheumatic diseases Lancet 382 2013 797 808
2. A. Perniok, F. Wedekind, M. Herrmann, C. Specker, and M. Schneider High levels of circulating early apoptic peripheral blood mononuclear cells in systemic lupus erythematosus Lupus 7 1998 113 118
3. I.K. Poon, C.D. Lucas, A.G. Rossi, and K.S. Ravichandran Apoptotic cell clearance: basic biology and therapeutic potential Nat Rev Immunol 14 2014 166 180
4. L.A. Casciola-Rosen, G. Anhalt, and A. Rosen Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes J Exp Med 179 1994 1317 1330
5. D. Mevorach, J.O. Mascarenhas, D. Gershov, and K.B. Elkon Complement-dependent clearance of apoptotic cells by human macrophages J Exp Med 188 1998 2313 2320
6. L.C. Korb, and J.M. Ahearn C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited J Immunol 158 1997 4525 4528
7. I. Baumann, W. Kolowos, and R.E. Voll Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus Arthritis Rheum 46 2002 191 201
8. M. Botto, C. Dell'Agnola, and A.E. Bygrave Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies Nat Genet 19 1998 56 59
9. F. Wermeling, Y. Chen, and T. Pikkarainen Class A scavenger receptors regulate tolerance against apoptotic cells, and autoantibodies against these receptors are predictive of systemic lupus J Exp Med 204 2007 2259 2265
10. X.W. Chen, Y. Shen, C.Y. Sun, F.X. Wu, Y. Chen, and C.D. Yang Anti-class a scavenger receptor autoantibodies from systemic lupus erythematosus patients impair phagocytic clearance of apoptotic cells by macrophages in vitro Arthritis Res Ther 13 2011 R9
11. T.K. Means, E. Latz, F. Hayashi, M.R. Murali, D.T. Golenbock, and A.D. Luster Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9 J Clin Invest 115 2005 407 417
12. F.J. Barrat, T. Meeker, and J. Gregorio Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus J Exp Med 202 2005 1131 1139
13. T. Lovgren, M.L. Eloranta, U. Bave, G.V. Alm, and L. Ronnblom Induction of interferon-alpha production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG Arthritis Rheum 50 2004 1861 1872
14. K.M. Kelly, H. Zhuang, and D.C. Nacionales "Endogenous adjuvant" activity of the RNA components of lupus autoantigens Sm/RNP and Ro 60 Arthritis Rheum 54 2006 1557 1567
15. T. Taniguchi, M.S. Lamphier, and N. Tanaka IRF-1: the transcription factor linking the interferon response and oncogenesis Biochim Biophys Acta 1333 1997 M9 M17
16. T. Nakaya, M. Sato, and N. Hata Gene induction pathways mediated by distinct IRFs during viral infection Biochem Biophys Res Commun 283 2001 1150 1156
17. M. Sato, H. Suemori, and N. Hata Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction Immunity 13 2000 539 548
18. A. Paun, J.T. Reinert, and Z. Jiang Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response J Biol Chem 283 2008 14295 14308
19. A. Schoenemeyer, B.J. Barnes, and M.E. Mancl The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor 7 signaling J Biol Chem 280 2005 17005 17012
20. H.M. Lazear, A. Lancaster, and C. Wilkins IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling PLoS Pathog 9 2013 e1003118
21. P. Dai, H. Cao, and T. Merghoub Myxoma virus induces type I interferon production in murine plasmacytoid dendritic cells via a TLR9/MyD88-, IRF5/IRF7-, and IFNAR-dependent pathway J Virol 85 2011 10814 10825
22. J.J. Hooks, H.M. Moutsopoulos, S.A. Geis, N.I. Stahl, J.L. Decker, and A.L. Notkins Immune interferon in the circulation of patients with autoimmune disease N Engl J Med 301 1979 5 8
23. E.C. Baechler, F.M. Batliwalla, and G. Karypis Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus Proc Natl Acad Sci U S A 100 2003 2610 2615
24. L. Bennett, A.K. Palucka, and E. Arce Interferon and granulopoiesis signatures in systemic lupus erythematosus blood J Exp Med 197 2003 711 723
25. J. Hua, K. Kirou, C. Lee, and M.K. Crow Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies Arthritis Rheum 54 2006 1906 1916
26. T.B. Niewold, J. Hua, T.J. Lehman, J.B. Harley, and M.K. Crow High serum IFN-alpha activity is a heritable risk factor for systemic lupus erythematosus Genes Immun 8 2007 492 502
27. C.E. Weckerle, B.S. Franek, and J.A. Kelly Network analysis of associations between serum interferon-alpha activity, autoantibodies, and clinical features in systemic lupus erythematosus Arthritis Rheum 63 2011 1044 1053
28. T.B. Niewold, T.L. Rivera, J.P. Buyon, and M.K. Crow Serum type I interferon activity is dependent on maternal diagnosis in anti-SSA/Ro-positive mothers of children with neonatal lupus Arthritis Rheum 58 2008 541 546
29. T.B. Niewold, J.A. Kelly, M.H. Flesch, L.R. Espinoza, J.B. Harley, and M.K. Crow Association of the IRF5 risk haplotype with high serum interferon-alpha activity in systemic lupus erythematosus patients Arthritis Rheum 58 2008 2481 2487
30. T.B. Niewold, J.A. Kelly, and S.N. Kariuki IRF5 haplotypes demonstrate diverse serological associations which predict serum interferon alpha activity and explain the majority of the genetic association with systemic lupus erythematosus Ann Rheum Dis 71 2012 463 468
31. J.B. Harley, M.E. Alarcon-Riquelme, and L.A. Criswell Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci Nat Genet 40 2008 204 210
32. R. Salloum, B.S. Franek, and S.N. Kariuki Genetic variation at the IRF7/PHRF1 locus is associated with autoantibody profile and serum interferon-alpha activity in lupus patients Arthritis Rheum 62 2010 553 561
33. Q. Fu, J. Zhao, and X. Qian Association of a functional IRF7 variant with systemic lupus erythematosus Arthritis Rheum 63 2011 749 754
34. V. Gateva, J.K. Sandling, and G. Hom A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus Nat Genet 41 2009 1228 1233
35. C.J. Lessard, I. Adrianto, and J.A. Ice Identification of IRF8, TMEM39A, and IKZF3-ZPBP2 as susceptibility loci for systemic lupus erythematosus in a large-scale multiracial replication study Am J Hum Genet 90 2012 648 660
36. B.S. Chrabot, S.N. Kariuki, and M.I. Zervou Genetic variation near IRF8 is associated with serologic and cytokine profiles in systemic lupus erythematosus and multiple sclerosis Genes Immun 14 2013 471 478
37. R. Salloum, and T.B. Niewold Interferon regulatory factors in human lupus pathogenesis Transl Res 157 2011 326 331
38. T.B. Niewold Interferon alpha as a primary pathogenic factor in human lupus J Interferon Cytokine Res 31 2011 887 892
39. T.B. Niewold, J.E. Adler, S.B. Glenn, T.J. Lehman, J.B. Harley, and M.K. Crow Age- and sex-related patterns of serum interferon-alpha activity in lupus families Arthritis Rheum 58 2008 2113 2119
40. D. Mangale, S.N. Kariuki, and B.S. Chrabot Familial aggregation of high tumor necrosis factor alpha levels in systemic lupus erythematosus Clin Dev Immunol 2013 2013 267430
41. C.E. Weckerle, D. Mangale, and B.S. Franek Large-scale analysis of tumor necrosis factor alpha levels in systemic lupus erythematosus Arthritis Rheum 64 2012 2947 2952
42. Y. Ghodke-Puranik, and T.B. Niewold Genetics of the type I interferon pathway in systemic lupus erythematosus Int J Clin Rheumatol 8 2013 657 669
43. S.N. Kariuki, and T.B. Niewold Genetic regulation of serum cytokines in systemic lupus erythematosus Transl Res 155 2010 109 117
44. S. Agik, B.S. Franek, and A.A. Kumar The autoimmune disease risk allele of UBE2L3 in African American patients with systemic lupus erythematosus: a recessive effect upon subphenotypes J Rheumatol 39 2012 73 78
45. T. Robinson, S.N. Kariuki, and B.S. Franek Autoimmune disease risk variant of IFIH1 is associated with increased sensitivity to IFN-alpha and serologic autoimmunity in lupus patients J Immunol 187 2011 1298 1303
46. S.N. Kariuki, B.S. Franek, and A.A. Kumar 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 2010 R151
47. Y. Koldobskaya, K. Ko, and A.A. Kumar Gene-expression-guided selection of candidate loci and molecular phenotype analyses enhance genetic discovery in systemic lupus erythematosus Clin Dev Immunol 2012 2012 682018
48. L.E. Ronnblom, G.V. Alm, and K.E. Oberg Possible induction of systemic lupus erythematosus by interferon-alpha treatment in a patient with a malignant carcinoid tumour J Intern Med 227 1990 207 210
49. T.B. Niewold, and W.I. Swedler Systemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis C Clin Rheumatol 24 2005 178 181
50. K.A. Kirou, C. Lee, and S. George Coordinate overexpression of interferon-alpha-induced genes in systemic lupus erythematosus Arthritis Rheum 50 2004 3958 3967
51. T.B. Niewold, D.N. Clark, R. Salloum, and B.D. Poole Interferon alpha in systemic lupus erythematosus J Biomed Biotechnol 2010 2010 948364
52. Y. Qiao, E.G. Giannopoulou, and C.H. Chan Synergistic activation of inflammatory cytokine genes by interferon-gamma-induced chromatin remodeling and toll-like receptor signaling Immunity 39 2013 454 469
53. N.A. de Weerd, J.P. Vivian, and T.K. Nguyen Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1 Nat Immunol 14 2013 901 907
54. L.B. Ivashkiv, and L.T. Donlin Regulation of type I interferon responses Nat Rev Immunol 14 2014 36 49
55. G.R. Stark, and J.E. Darnell Jr. The JAK-STAT pathway at twenty Immunity 36 2012 503 514
56. I. Marie, J.E. Durbin, and D.E. Levy Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7 EMBO J 17 1998 6660 6669
57. M. Sato, N. Hata, M. Asagiri, T. Nakaya, T. Taniguchi, and N. Tanaka Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7 FEBS Lett 441 1998 106 110
58. K. Honda, H. Yanai, and H. Negishi IRF-7 is the master regulator of type-I interferon-dependent immune responses Nature 434 2005 772 777
59. K. Honda, and T. Taniguchi IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors Nat Rev Immunol 6 2006 644 658
60. H. Kono, and K.L. Rock How dying cells alert the immune system to danger Nat Rev Immunol 8 2008 279 289
61. P. Broz, and D.M. Monack Newly described pattern recognition receptors team up against intracellular pathogens Nat Rev Immunol 13 2013 551 565
62. M. Shrivastav, and T.B. Niewold Nucleic acid sensors and type I interferon production in systemic lupus erythematosus Front Immunol 4 2013 319
63. T. Tamura, H. Yanai, D. Savitsky, and T. Taniguchi The IRF family transcription factors in immunity and oncogenesis Annu Rev Immunol 26 2008 535 584
64. A.L. Blasius, and B. Beutler Intracellular toll-like receptors Immunity 32 2010 305 315
65. K. Yasuda, P. Yu, and C.J. Kirschning Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways J Immunol 174 2005 6129 6136
66. K. Yasuda, M. Rutz, and B. Schlatter CpG motif-independent activation of TLR9 upon endosomal translocation of "natural" phosphodiester DNA Eur J Immunol 36 2006 431 436
67. T. Haas, J. Metzger, and F. Schmitz The DNA sugar backbone 2′ deoxyribose determines toll-like receptor 9 activation Immunity 28 2008 315 323
68. M. Schlee, A. Roth, and V. Hornung Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus Immunity 31 2009 25 34
69. H. Kato, O. Takeuchi, and E. Mikamo-Satoh Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 J Exp Med 205 2008 1601 1610
70. K. Matsui, Y. Kumagai, and H. Kato Cutting edge: role of TANK-binding kinase 1 and inducible IkappaB kinase in IFN responses against viruses in innate immune cells J Immunol 177 2006 5785 5789
71. D. Goubau, S. Deddouche, and C. Reis e Sousa Cytosolic sensing of viruses Immunity 38 2013 855 869
72. H. Takaki, K. Honda, and K. Atarashi MAVS-dependent IRF3/7 bypass of interferon beta-induction restricts the response to measles infection in CD150Tg mouse bone marrow-derived dendritic cells Mol Immunol 57 2014 100 110
73. M. Funabiki, H. Kato, and Y. Miyachi Autoimmune disorders associated with gain of function of the intracellular sensor MDA5 Immunity 40 2014 199 212
74. J.E. Molineros, A.K. Maiti, and C. Sun Admixture mapping in lupus identifies multiple functional variants within IFIH1 associated with apoptosis, inflammation, and autoantibody production PLoS Genet 9 2013 e1003222
75. J. Pothlichet, T.B. Niewold, D. Vitour, B. Solhonne, M.K. Crow, and M. Si-Tahar A loss-of-function variant of the antiviral molecule MAVS is associated with a subset of systemic lupus patients EMBO Mol Med 3 2011 142 152
76. Z. Zhang, B. Yuan, M. Bao, N. Lu, T. Kim, and Y.J. Liu The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells Nat Immunol 12 2011 959 965
77. K. Parvatiyar, Z. Zhang, and R.M. Teles The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response Nat Immunol 13 2012 1155 1161
78. L. Unterholzner, S.E. Keating, and M. Baran IFI16 is an innate immune sensor for intracellular DNA Nat Immunol 11 2010 997 1004
79. M.H. Orzalli, N.A. DeLuca, and D.M. Knipe Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein Proc Natl Acad Sci U S A 109 2012 E3008 E3017
80. L. Sun, J. Wu, F. Du, X. Chen, and Z.J. Chen Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway Science 339 2013 786 791
81. J. Wu, L. Sun, and X. Chen Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA Science 339 2013 826 830
82. T. Kondo, J. Kobayashi, and T. Saitoh DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking Proc Natl Acad Sci U S A 110 2013 2969 2974
83. V. Hornung, A. Ablasser, and M. Charrel-Dennis AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC Nature 458 2009 514 518
84. T. Burckstummer, C. Baumann, and S. Bluml An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome Nat Immunol 10 2009 266 272
85. T.L. Roberts, A. Idris, and J.A. Dunn HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA Science 323 2009 1057 1060
86. T. Fernandes-Alnemri, J.W. Yu, and C. Juliana The AIM2 inflammasome is critical for innate immunity to Francisella tularensis Nat Immunol 11 2010 385 393
87. A. Takaoka, Z. Wang, and M.K. Choi DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response Nature 448 2007 501 505
88. S.R. Paludan, and A.G. Bowie Immune sensing of DNA Immunity 38 2013 870 880
89. Y.H. Chiu, J.B. Macmillan, and Z.J. Chen RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway Cell 138 2009 576 591
90. H. Ishikawa, Z. Ma, and G.N. Barber STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity Nature 461 2009 788 792
91. T. Lindahl, J.A. Gally, and G.M. Edelman Properties of deoxyribonuclease 3 from mammalian tissues J Biol Chem 244 1969 5014 5019
92. D.B. Stetson, J.S. Ko, T. Heidmann, and R. Medzhitov Trex1 prevents cell-intrinsic initiation of autoimmunity Cell 134 2008 587 598
93. Y.J. Crow, B.E. Hayward, and R. Parmar Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus Nat Genet 38 2006 917 920
94. M.A. Lee-Kirsch, D. Chowdhury, and S. Harvey A mutation in TREX1 that impairs susceptibility to granzyme A-mediated cell death underlies familial chilblain lupus J Mol Med (Berl) 85 2007 531 537
95. M.A. Lee-Kirsch, M. Gong, and D. Chowdhury Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus Nat Genet 39 2007 1065 1067
96. B. de Vries, G.M. Steup-Beekman, and J. Haan TREX1 gene variant in neuropsychiatric systemic lupus erythematosus Ann Rheum Dis 69 2010 1886 1887
97. B. Namjou, P.H. Kothari, and J.A. Kelly Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort Genes Immun 12 2011 270 279
98. A. Gall, P. Treuting, and K.B. Elkon Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease Immunity 36 2012 120 131
99. G.N. Zhao, D.S. Jiang, and H. Li Interferon regulatory factors: at the crossroads of immunity, metabolism, and disease Biochim Biophys Acta 2014 [Epub ahead of print]
100. C.R. Escalante, J. Yie, D. Thanos, and A.K. Aggarwal Structure of IRF-1 with bound DNA reveals determinants of interferon regulation Nature 391 1998 103 106
101. M. Kusumoto, Y. Fujii, and Y. Tsukuda Crystallographic characterization of the DNA-binding domain of interferon regulatory factor-2 complexed with DNA J Struct Biol 121 1998 363 366
102. Y. Fujii, T. Shimizu, M. Kusumoto, Y. Kyogoku, T. Taniguchi, and T. Hakoshima Crystal structure of an IRF-DNA complex reveals novel DNA recognition and cooperative binding to a tandem repeat of core sequences EMBO J 18 1999 5028 5041
103. W. Chen, S.S. Lam, and H. Srinath Insights into interferon regulatory factor activation from the crystal structure of dimeric IRF5 Nat Struct Mol Biol 15 2008 1213 1220
104. B.J. Barnes, M.J. Kellum, A.E. Field, and P.M. Pitha Multiple regulatory domains of IRF-5 control activation, cellular localization, and induction of chemokines that mediate recruitment of T lymphocytes Mol Cell Biol 22 2002 5721 5740
105. R. Lin, Y. Mamane, and J. Hiscott Structural and functional analysis of interferon regulatory factor 3: localization of the transactivation and autoinhibitory domains Mol Cell Biol 19 1999 2465 2474
106. R. Lin, Y. Mamane, and J. Hiscott Multiple regulatory domains control IRF-7 activity in response to virus infection J Biol Chem 275 2000 34320 34327
107. R.R. Graham, C. Cotsapas, and L. Davies Genetic variants near TNFAIP3 on 6q23 are associated with systemic lupus erythematosus Nat Genet 40 2008 1059 1061
108. I. Adrianto, F. Wen, and A. Templeton Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus Nat Genet 43 2011 253 258
109. I. Adrianto, S. Wang, and G.B. Wiley Association of two independent functional risk haplotypes in TNIP1 with systemic lupus erythematosus Arthritis Rheum 64 2012 3695 3705
110. S. Uematsu, S. Sato, and M. Yamamoto Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7- and TLR9-mediated interferon-{alpha} induction J Exp Med 201 2005 915 923
111. K.M. Kaufman, J. Zhao, and J.A. Kelly Fine mapping of Xq28: both MECP2 and IRAK1 contribute to risk for systemic lupus erythematosus in multiple ancestral groups Ann Rheum Dis 72 2013 437 444
112. B. Namjou, A.L. Sestak, and D.L. Armstrong High-density genotyping of STAT4 reveals multiple haplotypic associations with systemic lupus erythematosus in different racial groups Arthritis Rheum 60 2009 1085 1095
113. S.N. Kariuki, K.A. Kirou, E.J. MacDermott, L. Barillas-Arias, M.K. Crow, and T.B. Niewold Cutting edge: autoimmune disease risk variant of STAT4 confers increased sensitivity to IFN-alpha in lupus patients in vivo J Immunol 182 2009 34 38
114. E. Svenungsson, J. Gustafsson, and D. Leonard A STAT4 risk allele is associated with ischaemic cerebrovascular events and anti-phospholipid antibodies in systemic lupus erythematosus Ann Rheum Dis 69 2010 834 840
115. S.A. Chung, K.E. Taylor, and R.R. Graham Differential genetic associations for systemic lupus erythematosus based on anti-dsDNA autoantibody production PLoS Genet 7 2011 e1001323
116. R.C. Ferreira, Q. Pan-Hammarstrom, and R.R. Graham Association of IFIH1 and other autoimmunity risk alleles with selective IgA deficiency Nat Genet 42 2010 777 780
117. C. Kyogoku, C.D. Langefeld, and W.A. Ortmann Genetic association of the R620W polymorphism of protein tyrosine phosphatase PTPN22 with human SLE Am J Hum Genet 75 2004 504 507
118. S.N. Kariuki, M.K. Crow, and T.B. Niewold 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 2008 2818 2823
119. R.B. Seth, L. Sun, C.K. Ea, and Z.J. Chen Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 Cell 122 2005 669 682
120. A.H. Sawalha, R. Webb, and S. Han Common variants within MECP2 confer risk of systemic lupus erythematosus PLoS One 3 2008 e1727
121. R. Webb, J.D. Wren, and M. Jeffries Variants within MECP2, a key transcription regulator, are associated with increased susceptibility to lupus and differential gene expression in patients with systemic lupus erythematosus Arthritis Rheum 60 2009 1076 1084
122. A. Takaoka, H. Yanai, and S. Kondo Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors Nature 434 2005 243 249
123. T. Krausgruber, K. Blazek, and T. Smallie IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses Nat Immunol 12 2011 231 238
124. B.J. Barnes, J. Richards, M. Mancl, S. Hanash, L. Beretta, and P.M. Pitha Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection J Biol Chem 279 2004 45194 45207
125. K. Yasuda, A.A. Watkins, and G.S. Kochar Interferon regulatory factor-5 deficiency ameliorates disease severity in the MRL/lpr mouse model of lupus in the absence of a mutation in DOCK2 PLoS One 9 2014 e103478
126. A. Couzinet, K. Tamura, and H.M. Chen A cell-type-specific requirement for IFN regulatory factor 5 (IRF5) in Fas-induced apoptosis Proc Natl Acad Sci U S A 105 2008 2556 2561
127. C. Lien, C.M. Fang, D. Huso, F. Livak, R. Lu, and P.M. Pitha Critical role of IRF-5 in regulation of B-cell differentiation Proc Natl Acad Sci U S A 107 2010 4664 4668
128. C.M. Fang, S. Roy, and E. Nielsen Unique contribution of IRF-5-Ikaros axis to the B-cell IgG2a response Genes Immun 13 2012 421 430
129. C.M. Cham, K. Ko, and T.B. Niewold Interferon regulatory factor 5 in the pathogenesis of systemic lupus erythematosus Clin Dev Immunol 2012 2012 780436
130. E. Lazzari, and C.A. Jefferies IRF5-mediated signaling and implications for SLE Clin Immunol 153 2014 343 352
131. M.E. Mancl, G. Hu, and N. Sangster-Guity Two discrete promoters regulate the alternatively spliced human interferon regulatory factor-5 isoforms. Multiple isoforms with distinct cell type-specific expression, localization, regulation, and function J Biol Chem 280 2005 21078 21090
132. S. Sigurdsson, H.H. Goring, and G. Kristjansdottir Comprehensive evaluation of the genetic variants of interferon regulatory factor 5 (IRF5) reveals a novel 5 bp length polymorphism as strong risk factor for systemic lupus erythematosus Hum Mol Genet 17 2008 872 881
133. R.R. Graham, C. Kyogoku, and S. Sigurdsson Three functional variants of IFN regulatory factor 5 (IRF5) define risk and protective haplotypes for human lupus Proc Natl Acad Sci U S A 104 2007 6758 6763
134. R.R. Graham, S.V. Kozyrev, and E.C. Baechler 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 2006 550 555
135. S. Sigurdsson, G. Nordmark, and H.H. Goring Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus Am J Hum Genet 76 2005 528 537
136. E. Lazzari, J. Korczeniewska, J. Ni Gabhann, S. Smith, B.J. Barnes, and C.A. Jefferies TRIpartite Motif 21 (TRIM21) differentially regulates the stability of interferon regulatory factor 5 (IRF5) isoforms PLoS One 9 2014 e103609
137. T.S. Cherian, S.N. Kariuki, B.S. Franek, J.P. Buyon, R.M. Clancy, and T.B. Niewold Brief report: IRF5 systemic lupus erythematosus risk haplotype is associated with asymptomatic serologic autoimmunity and progression to clinical autoimmunity in mothers of children with neonatal lupus Arthritis Rheum 64 2012 3383 3387
138. S. Ning, J.S. Pagano, and G.N. Barber IRF7: activation, regulation, modification and function Genes Immun 12 2011 399 414
139. H. Tsujimura, T. Tamura, and H.J. Kong Toll-like receptor 9 signaling activates NF-kappaB through IFN regulatory factor-8/IFN consensus sequence binding protein in dendritic cells J Immunol 172 2004 6820 6827
140. S. Hambleton, S. Salem, and J. Bustamante IRF8 mutations and human dendritic-cell immunodeficiency N Engl J Med 365 2011 127 138
141. P.L. De Jager, X. Jia, and J. Wang Meta-analysis of genome scans and replication identify CD6, IRF8 and TNFRSF1A as new multiple sclerosis susceptibility loci Nat Genet 41 2009 776 782
142. X. Feng, N.P. Reder, and M. Yanamandala Type I interferon signature is high in lupus and neuromyelitis optica but low in multiple sclerosis J Neurol Sci 313 2012 48 53
143. X. Feng, D. Han, B.K. Kilaru, B.S. Franek, T.B. Niewold, and A.T. Reder Inhibition of interferon-beta responses in multiple sclerosis immune cells associated with high-dose statins Arch Neurol 69 2012 1303 1309
144. A.T. Reder, and X. Feng Aberrant type I interferon regulation in autoimmunity: opposite directions in MS and SLE, shaped by evolution and body ecology Front Immunol 4 2013 281