Insights into the genetic basis of systemic sclerosis: immunity in human disease and in mouse models

References

• Sapadin AN, Esser AC, Fleischmajer R. Immunopathogenesis of scleroderma – evolving concepts. Mt Sinai J Med. 2001;68(4–5):233–242.
   Google Scholar
• Barnes J, Mayes MD. Epidemiology of systemic sclerosis: incidence, prevalence, survival, risk factors, malignancy, and environmental triggers. Curr Opin Rheumatol. 2012;24(2):165–170.
   PubMed Web of Science ®Google Scholar
• Arnett FC, Cho M, Chatterjee S, Aguilar MB, Reveille JD, Mayes MD. Familial occurrence frequencies and relative risks for systemic sclerosis (scleroderma) in three United States cohorts. Arthritis Rheum. 2001;44(6):1359–1362.
   PubMedGoogle Scholar
• Zhou X, Tan FK, Xiong M, Arnett FC, Feghali-Bostwick CA. Monozygotic twins clinically discordant for scleroderma show concordance for fibroblast gene expression profiles. Arthritis Rheum. 2005;52(10):3305–3314.
   PubMedGoogle Scholar
• Frech T, Khanna D, Markewitz B, Mineau G, Pimentel R, Sawitzke A. Heritability of vasculopathy, autoimmune disease, and fibrosis in systemic sclerosis: a population-based study. Arthritis Rheum. 2010;62(7):2109–2116.
   Google Scholar
• Martín JE, Bossini-Castillo L, Martín J. Unraveling the genetic component of systemic sclerosis. Hum Genet. 2012;131(7):1023–1037.
   Web of Science ®Google Scholar
• Mayes MD. The genetics of scleroderma: looking into the postgenomic era. Curr Opin Rheumatol. 2012;24(6):677–684.
   Web of Science ®Google Scholar
• Radstake TR, Gorlova O, Rueda B, et al; Spanish Scleroderma Group. Genome-wide association study of systemic sclerosis identifies CD247 as a new susceptibility locus. Nat Genet. 2010;42(5):426–429.
   PubMed Web of Science ®Google Scholar
• Gorlova O, Martin JE, Rueda B, et al; Spanish Scleroderma Group. Identification of novel genetic markers associated with clinical phenotypes of systemic sclerosis through a genome-wide association strategy. PLoS Genet. 2011;7(7):e1002178.
   Web of Science ®Google Scholar
• Allanore Y, Saad M, Dieudé P, et al. Genome-wide scan identifies TNIP1, PSORS1C1, and RHOB as novel risk loci for systemic sclerosis. PLoS Genet. 2011;7(7):e1002091.
   Web of Science ®Google Scholar
• Bossini-Castillo L, Martin JE, Broen J, et al; Spanish Scleroderma Group. A GWAS follow-up study reveals the association of the IL12RB2 gene with systemic sclerosis in Caucasian populations. Hum Mol Genet. 2012;21(4):926–933.
   Web of Science ®Google Scholar
• Martin JE, Broen JC, Carmona FD, et al; Spanish Scleroderma Group. Identification of CSK as a systemic sclerosis genetic risk factor through Genome Wide Association Study follow-up. Hum Mol Genet. 2012;21(12):2825–2835.
   Web of Science ®Google Scholar
• López-Isac E, Bossini-Castillo L, Simeon CP, et al; Spanish Scleroderma Group. A genome-wide association study follow-up suggests a possible role for PPARG in systemic sclerosis susceptibility. Arthritis Res Ther. 2014;16(1):R6.
   PubMed Web of Science ®Google Scholar
• Mayes MD, Bossini-Castillo L, Gorlova O, et al; Spanish Scleroderma Group. Immunochip analysis identifies multiple susceptibility loci for systemic sclerosis. Am J Hum Genet. 2014;94(1):47–61.
   PubMed Web of Science ®Google Scholar
• Dieudé P, Bouaziz M, Guedj M, et al. Evidence of the contribution of the X chromosome to systemic sclerosis susceptibility: association with the functional IRAK1 196Phe/532Ser haplotype. Arthritis Rheum. 2011;63(12):3979–3987.
   PubMed Web of Science ®Google Scholar
• Carmona FD, Cénit MC, Diaz-Gallo LM, et al; Spanish Scleroderma Group. New insight on the Xq28 association with systemic sclerosis. Ann Rheum Dis. 2013;72(12):2032–2038.
   PubMed Web of Science ®Google Scholar
• Bossini-Castillo L, Martin JE, Broen J, et al; Spanish Scleroderma Group. Confirmation of TNIP1 but not RHOB and PSORS1C1 as systemic sclerosis risk factors in a large independent replication study. Ann Rheum Dis. 2013;72(4):602–607.
   PubMed Web of Science ®Google Scholar
• Graham RR, Kyogoku C, Sigurdsson S, et al. Three functional variants of IFN regulatory factor 5 (IRF5) define risk and protective haplotypes for human lupus. Proc Natl Acad Sci U S A. 2007;104(16):6758–6763.
   PubMed Web of Science ®Google Scholar
• Graham RR, Kozyrev SV, Baechler EC, et al; Argentine and Spanish Collaborative Groups. 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. 2006;38(5):550–555.
   PubMed Web of Science ®Google Scholar
• Sigurdsson S, Nordmark G, Göring 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. 2005;76(3):528–537.
   PubMed Web of Science ®Google Scholar
• Martin JE, Assassi S, Diaz-Gallo LM, et al; Spanish Scleroderma Group; SLEGEN consortium; US Scleroderma GWAS group; BIOLUPUS. A systemic sclerosis and systemic lupus erythematosus pan-meta-GWAS reveals new shared susceptibility loci. Hum Mol Genet. 2013;22(19):4021–4029.
   Web of Science ®Google Scholar
• Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008;26:535–584.
   PubMed Web of Science ®Google Scholar
• Lim CP, Cao X. Structure, function, and regulation of STAT proteins. Mol Biosyst. 2006;2(11):536–550.
   PubMedGoogle Scholar
• Kaplan MH. STAT4: a critical regulator of inflammation in vivo. Immunol Res. 2005;31(3):231–242.
   Web of Science ®Google Scholar
• Rueda B, Broen J, Simeon C, et al. The STAT4 gene influences the genetic predisposition to systemic sclerosis phenotype. Hum Mol Genet. 2009;18(11):2071–2077.
   PubMed Web of Science ®Google Scholar
• Dieudé P, Guedj M, Wipff J, et al. STAT4 is a genetic risk factor for systemic sclerosis having additive effects with IRF5 on disease susceptibility and related pulmonary fibrosis. Arthritis Rheum. 2009;60(8):2472–2479.
   PubMedGoogle Scholar
• Kaplan MH, Sun YL, Hoey T, Grusby MJ. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature. 1996;382(6587):174–177.
   Web of Science ®Google Scholar
• Avouac J, Fürnrohr BG, Tomcik M, et al. Inactivation of the transcription factor STAT-4 prevents inflammation-driven fibrosis in animal models of systemic sclerosis. Arthritis Rheum. 2011;63(3):800–809.
   Google Scholar
• Barnes BJ, Richards J, Mancl M, Hanash S, Beretta L, Pitha PM. Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J Biol Chem. 2004;279(43):45194–45207.
   PubMed Web of Science ®Google Scholar
• Barnes BJ, Kellum MJ, Pinder KE, Frisancho JA, Pitha PM. Interferon regulatory factor 5, a novel mediator of cell cycle arrest and cell death. Cancer Res. 2003;63(19):6424–6431.
   PubMed Web of Science ®Google Scholar
• Dieudé P, Wipff J, Guedj M, et al. BANK1 is a genetic risk factor for diffuse cutaneous systemic sclerosis and has additive effects with IRF5 and STAT4. Arthritis Rheum. 2009;60(11):3447–3454.
   PubMedGoogle Scholar
• Dieudé P, Guedj M, Wipff J, et al. Association between the IRF5 rs2004640 functional polymorphism and systemic sclerosis: a new perspective for pulmonary fibrosis. Arthritis Rheum. 2009;60(1):225–233.
   PubMedGoogle Scholar
• Ito I, Kawaguchi Y, Kawasaki A, et al. Association of a functional polymorphism in the IRF5 region with systemic sclerosis in a Japanese population. Arthritis Rheum. 2009;60(6):1845–1850.
   PubMed Web of Science ®Google Scholar
• Carmona FD, Martin JE, Beretta L, et al; Spanish Scleroderma Group. The systemic lupus erythematosus IRF5 risk haplotype is associated with systemic sclerosis. PLoS One. 2013;8(1):e54419.
   Web of Science ®Google Scholar
• Sharif R, Mayes MD, Tan FK, et al. IRF5 polymorphism predicts prognosis in patients with systemic sclerosis. Ann Rheum Dis. 2012;71(7):1197–1202.
   Web of Science ®Google Scholar
• Takaoka A, Yanai H, Kondo S, et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature. 2005;434(7030):243–249.
   PubMed Web of Science ®Google Scholar
• Terao C, Ohmura K, Kawaguchi Y, et al. PLD4 as a novel susceptibility gene for systemic sclerosis in a Japanese population. Arthritis Rheum. 2013;65(2):472–480.
   Google Scholar
• Turcotte K, Gauthier S, Tuite A, Mullick A, Malo D, Gros P. A mutation in the Icsbp1 gene causes susceptibility to infection and a chronic myeloid leukemia-like syndrome in BXH-2 mice. J Exp Med. 2005;201(6):881–890.
   Web of Science ®Google Scholar
• Ozato K, Tailor P, Kubota T. The interferon regulatory factor family in host defense: mechanism of action. J Biol Chem. 2007;282(28):20065–20069.
   PubMed Web of Science ®Google Scholar
• Levi BZ, Hashmueli S, Gleit-Kielmanowicz M, Azriel A, Meraro D. ICSBP/IRF-8 transactivation: a tale of protein-protein interaction. J Interferon Cytokine Res. 2002;22(1):153–160.
   Web of Science ®Google Scholar
• Tailor P, Tamura T, Morse HC, Ozato K. The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood. 2008;111(4):1942–1945.
   Web of Science ®Google Scholar
• Valdes AM, Thomson G; Type 1 Diabetes Genetics Consortium. Several loci in the HLA class III region are associated with T1D risk after adjusting for DRB1-DQB1. Diabetes Obes Metab. 2009;11 Suppl 1:46–52.
   Google Scholar
• AlFadhli S, Nanda A. Genetic evidence for the involvement of NOTCH4 in rheumatoid arthritis and alopecia areata. Immunol Lett. 2013; 150(1–2):130–133.
   Web of Science ®Google Scholar
• Rioux JD, Goyette P, Vyse TJ, et al; International MHC and Autoimmunity Genetics Network. Mapping of multiple susceptibility variants within the MHC region for 7 immune-mediated diseases. Proc Natl Acad Sci U S A. 2009;106(44):18680–18685.
   Google Scholar
• Morris DL, Taylor KE, Fernando MM, et al; International MHC and Autoimmunity Genetics Network; Systemic Lupus Erythematosus Genetics Consortium. Unraveling multiple MHC gene associations with systemic lupus erythematosus: model choice indicates a role for HLA alleles and non-HLA genes in Europeans. Am J Hum Genet. 2012;91(5):778–793.
   Google Scholar
• Villa N, Walker L, Lindsell CE, Gasson J, Iruela-Arispe ML, Weinmaster G. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech Dev. 2001;108(1–2):161–164.
   PubMed Web of Science ®Google Scholar
• Krebs LT, Xue Y, Norton CR, et al. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 2000;14(11):1343–1352.
   PubMed Web of Science ®Google Scholar
• Uyttendaele H, Ho J, Rossant J, Kitajewski J. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc Natl Acad Sci U S A. 2001;98(10):5643–5648.
   PubMed Web of Science ®Google Scholar
• Begovich AB, Carlton VE, Honigberg LA, et al. A missense single-nucleotide polymorphism in a gene encoding a protein tyrosine phosphatase (PTPN22) is associated with rheumatoid arthritis. Am J Hum Genet. 2004;75(2):330–337.
   PubMed Web of Science ®Google Scholar
• Kyogoku C, Langefeld CD, Ortmann WA, et al. Genetic association of the R620W polymorphism of protein tyrosine phosphatase PTPN22 with human SLE. Am J Hum Genet. 2004;75(3):504–507.
   PubMed Web of Science ®Google Scholar
• Bottini N, Musumeci L, Alonso A, et al. A functional variant of lymphoid tyrosine phosphatase is associated with type I diabetes. Nat Genet. 2004;36(4):337–338.
   PubMed Web of Science ®Google Scholar
• Gourh P, Tan FK, Assassi S, et al. Association of the PTPN22 R620W polymorphism with anti-topoisomerase I- and anticentromere antibody-positive systemic sclerosis. Arthritis Rheum. 2006;54(12):3945–3953.
   PubMedGoogle Scholar
• Dieudé P, Guedj M, Wipff J, et al. The PTPN22 620W allele confers susceptibility to systemic sclerosis: findings of a large case-control study of European Caucasians and a meta-analysis. Arthritis Rheum. 2008;58(7):2183–2188.
   PubMed Web of Science ®Google Scholar
• Bottini N, Vang T, Cucca F, Mustelin T. Role of PTPN22 in type 1 diabetes and other autoimmune diseases. Semin Immunol. 2006;18(4):207–213.
   PubMed Web of Science ®Google Scholar
• Cohen S, Dadi H, Shaoul E, Sharfe N, Roifman CM. Cloning and characterization of a lymphoid-specific, inducible human protein tyrosine phosphatase, Lyp. Blood. 1999;93(6):2013–2024.
   PubMed Web of Science ®Google Scholar
• Matthews RJ, Bowne DB, Flores E, Thomas ML. Characterization of hematopoietic intracellular protein tyrosine phosphatases: description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences. Mol Cell Biol. 1992;12(5):2396–2405.
   PubMed Web of Science ®Google Scholar
• Cloutier JF, Veillette A. Cooperative inhibition of T-cell antigen receptor signaling by a complex between a kinase and a phosphatase. J Exp Med. 1999;189(1):111–121.
   PubMed Web of Science ®Google Scholar
• Gjörloff-Wingren A, Saxena M, Williams S, Hammi D, Mustelin T. Characterization of TCR-induced receptor-proximal signaling events negatively regulated by the protein tyrosine phosphatase PEP. Eur J Immunol. 1999;29(12):3845–3854.
   PubMed Web of Science ®Google Scholar
• Brownlie RJ, Miosge LA, Vassilakos D, Svensson LM, Cope A, Zamoyska R. Lack of the phosphatase PTPN22 increases adhesion of murine regulatory T cells to improve their immunosuppressive function. Sci Signal. 2012;5(252):ra87.
   Web of Science ®Google Scholar
• Dai X, James RG, Habib T, et al. A disease-associated PTPN22 variant promotes systemic autoimmunity in murine models. J Clin Invest. 2013;123(5):2024–2036.
   PubMed Web of Science ®Google Scholar
• Zhang J, Zahir N, Jiang Q, et al. The autoimmune disease-associated PTPN22 variant promotes calpain-mediated Lyp/Pep degradation associated with lymphocyte and dendritic cell hyperresponsiveness. Nat Genet. 2011;43(9):902–907.
   PubMed Web of Science ®Google Scholar
• Zheng P, Kissler S. PTPN22 silencing in the NOD model indicates the type 1 diabetes-associated allele is not a loss-of-function variant. Diabetes. 2013;62(3):896–904.
   PubMed Web of Science ®Google Scholar
• Zheng J, Petersen F, Yu X. The role of PTPN22 in autoimmunity: learning from mice. Autoimmun Rev. 2014;13(3):266–271.
   Web of Science ®Google Scholar
• Baron WF, Pan CQ, Spencer SA, Ryan AM, Lazarus RA, Baker KP. Cloning and characterization of an actin-resistant DNase I-like endonuclease secreted by macrophages. Gene. 1998;215(2):291–301.
   Web of Science ®Google Scholar
• Ueki M, Takeshita H, Fujihara J, et al. Caucasian-specific allele in non-synonymous single nucleotide polymorphisms of the gene encoding deoxyribonuclease I-like 3, potentially relevant to autoimmunity, produces an inactive enzyme. Clin Chim Acta. 2009;407(1–2):20–24.
   Web of Science ®Google Scholar
• Al-Mayouf SM, Sunker A, Abdwani R, et al. Loss-of-function variant in DNASE1L3 causes a familial form of systemic lupus erythematosus. Nat Genet. 2011;43(12):1186–1188.
   PubMed Web of Science ®Google Scholar
• Eyre S, Bowes J, Diogo D, et al; Biologics in Rheumatoid Arthritis Genetics and Genomics Study Syndicate; Wellcome Trust Case Control Consortium. High-density genetic mapping identifies new susceptibility loci for rheumatoid arthritis. Nat Genet. 2012;44(12):1336–1340.
   PubMed Web of Science ®Google Scholar
• Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG, Möröy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet. 2000;25(2):177–181.
   PubMed Web of Science ®Google Scholar
• Martin JE, Broen JC, Carmona FD, et al; Spanish Scleroderma Group. Identification of CSK as a systemic sclerosis genetic risk factor through Genome Wide Association Study follow-up. Hum Mol Genet. 2012;21(12):2825–2835.
   Web of Science ®Google Scholar
• Dieudé P, Guedj M, Wipff J, et al. Association of the TNFAIP3 rs5029939 variant with systemic sclerosis in the European Caucasian population. Ann Rheum Dis. 2010;69(11):1958–1964.
   PubMed Web of Science ®Google Scholar
• Yamamoto T, Takagawa S, Katayama I, et al. Animal model of sclerotic skin. I: Local injections of bleomycin induce sclerotic skin mimicking scleroderma. J Invest Dermatol. 1999;112(4):456–462.
   PubMed Web of Science ®Google Scholar
• Manne J, Markova M, Siracusa LD, Jimenez SA. Collagen content in skin and internal organs of the tight skin mouse: an animal model of scleroderma. Biochem Res Int. 2013;2013:436053.
   Google Scholar
• Christner PJ, Peters J, Hawkins D, Siracusa LD, Jiménez SA. The tight skin 2 mouse. An animal model of scleroderma displaying cutaneous fibrosis and mononuclear cell infiltration. Arthritis Rheum. 1995;38(12):1791–1798.
   Google Scholar
• Ruzek MC, Jha S, Ledbetter S, Richards SM, Garman RD. A modified model of graft-versus-host-induced systemic sclerosis (scleroderma) exhibits all major aspects of the human disease. Arthritis Rheum. 2004;50(4):1319–1331.
   Google Scholar