A type I Interferon transcriptional signature precedes autoimmunity in children genetically at risk for type 1 diabetes

Diabetes

Volumn 63, Issue 7, 2014, Pages 2538-2550

  Ferreira, Ricardo C ^a   Guo, Hui ^a   Coulson, Richard M R ^a,b   Smyth, Deborah J ^a   Pekalski, Marcin L ^a   Burren, Oliver S ^a   Cutler, Antony J ^a   Doecke, James D ^a,c,d,e   Flint, Shaun ^b   McKinney, Eoin F ^b   Lyons, Paul A ^b   Smith, Kenneth G C ^b   Achenbach, Peter ^f   Beyerlein, Andreas ^f   Dunger, David B ^g   Clayton, David G ^a   Wicker, Linda S ^a   Todd, John A ^a   Bonifacio, Ezio ^h   Wallace, Chris ^a   Ziegler, Anette G ^f   more..

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^d CSIRO   (Australia)

^e MACQUARIE UNIVERSITY   (Australia)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD14 ANTIGEN; DNA; INTERFERON; INTERLEUKIN 1BETA; SIALOADHESIN; TYPE 1 INTERFERON; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; AUTOIMMUNITY; BIRTH; CHILD; CHILDHOOD DISEASE; COHORT ANALYSIS; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENE EXPRESSION; GENETIC PARAMETERS; GENETIC PREDISPOSITION; GENETICS; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; MEDICAL HISTORY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRESCHOOL CHILD; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; TRANSCRIPTIONAL SIGNATURE; UPPER RESPIRATORY TRACT INFECTION; UPREGULATION;

ADOLESCENT; ADULT; AUTOIMMUNITY; CHILD; COHORT STUDIES; DIABETES MELLITUS, TYPE 1; FEMALE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTERFERON TYPE I; MALE; MIDDLE AGED; RISK; TRANSCRIPTOME; YOUNG ADULT;

EID: 84903188015     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1777     Document Type: Article

References (55)

1. Virgin HW, Todd JA. Metagenomics and personalized medicine. Cell 2011;147:44- 56
2. Ziegler AG, Rewers M, Simell O, et al. Seroconversion to multiple islet autoantibodies and risk of progression to diabetes in children. JAMA 2013;309:2473-2479
3. Barrett JC, Clayton DG, Concannon P, et al; Type 1 Diabetes Genetics Consortium. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 2009;41:703-707
4. Dotta F, Galleri L, Sebastiani G, Vendrame F. Virus infections: lessons from pancreas histology. Curr Diab Rep 2010;10:357-361
5. Beyerlein A, Wehweck F, Ziegler AG, Pflueger M. Respiratory infections in early life and the development of islet autoimmunity in children at increased type 1 diabetes risk: evidence from the BABYDIET study. JAMA Pediatr 2013;167:800-807
6. Foulis AK, Farquharson MA, Meager A. Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus. Lancet 1987;2:1423-1427 (Pubitemid 18010318)
7. Coppieters KT, Dotta F, Amirian N, et al. Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 2012;209:51-60
8. Li Q, Xu B, Michie SA, Rubins KH, Schreriber RD, McDevitt HO. Interferon-α initiates type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci U S A 2008;105:12439-12444
9. Diana J, Simoni Y, Furio L, et al. Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat Med 2013;19:65-73
10. Baechler EC, Batliwalla FM, Karypis G, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A 2003;100:2610-2615 (Pubitemid 36297546)
11. Bennett L, Palucka AK, Arce E, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003;197:711-723 (Pubitemid 36350866)
12. Chaussabel D, Quinn C, Shen J, et al. A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 2008;29:150-164 (Pubitemid 351952461)
13. Berry MPR, Graham CM, McNab FW, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010;466:973-977
14. Hummel S, Pflüger M, Hummel M, Bonifacio E, Ziegler AG. Primary dietary intervention study to reduce the risk of islet autoimmunity in children at increased risk for type 1 diabetes: the BABYDIET study. Diabetes Care 2011;34:1301-1305
15. Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-1277 (Pubitemid 13221242)
16. Ferreira RC, Freitag DF, Cutler AJ, et al. Functional IL6R 358Ala allele impairs classical IL-6 receptor signaling and influences risk of diverse inflammatory diseases. PLoS Genet 2013;9:e1003444
17. Huber W, von Heydebreck A, Sültmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 2002;18(Suppl. 1):S96-S104 (Pubitemid 41185642)
18. R Core Team. R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing, 2013
19. Stranger BE, Montgomery SB, Dimas AS, et al. Patterns of cis regulatory variation in diverse human populations. PLoS Genet 2012;8:e1002639
20. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3: Article3
21. Waddell SJ, Popper SJ, Rubins KH, et al. Dissecting interferon-induced transcriptional programs in human peripheral blood cells. PLoS One 2010;5:e9753
22. Nickles D, Chen HP, Li MM, et al. Blood RNA profiling in a large cohort of multiple sclerosis patients and healthy controls. Hum Mol Genet 2013;22:4194-4205
23. Franco LM, Bucasas KL, Wells JM, et al. Integrative genomic analysis of the human immune response to influenza vaccination. eLife 2013;2:e00299
24. Elo LL, Mykkänen J, Nikula T, et al. Early suppression of immune response pathways characterizes children with prediabetes in genome-wide gene expression profiling. J Autoimmun 2010;35:70-76
25. Kallionpää H, Elo LL, Laajala E, et al. Innate immune activity is detected prior to seroconversion in children with HLA-conferred type 1 diabetes susceptibility. Diabetes 2014;63:2402-2414
26. Kaizer EC, Glaser CL, Chaussabel D, Banchereau J, Pascual V, White PC. Gene expression in peripheral blood mononuclear cells from children with diabetes. J Clin Endocrinol Metab 2007;92:3705-3711 (Pubitemid 47435359)
27. Reynier F, Pachot A, Paye M, et al. Specific gene expression signature associated with development of autoimmune type-I diabetes using whole-blood microarray analysis. Genes Immun 2010;11:269-278
28. York MR, Nagai T, Mangini AJ, Lemaire R, van Seventer JM, Lafyatis R. A macrophage marker, Siglec-1, is increased on circulating monocytes in patients with systemic sclerosis and induced by type I interferons and toll-like receptor agonists. Arthritis Rheum 2007;56:1010-1020 (Pubitemid 46399451)
29. Biesen R, Demir C, Barkhudarova F, et al. Sialic acid-binding Ig-like lectin 1 expression in inflammatory and resident monocytes is a potential biomarker for monitoring disease activity and success of therapy in systemic lupus erythematosus. Arthritis Rheum 2008;58:1136-1145 (Pubitemid 351564017)
30. Malhotra S, Castilló J, Bustamante M, et al. SIGLEC1 and SIGLEC7 expression in circulating monocytes of patients with multiple sclerosis. Mult Scler 2013;19:524-531
31. Preble OT, Black RJ, Friedman RM, Klippel JH, Vilcek J. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon. Science 1982;216:429-431 (Pubitemid 12076067)
32. Hooks JJ, Jordan GW, Cupps T, Moutsopoulos HM, Fauci AS, Notkins AL. Multiple interferons in the circulation of patients with systemic lupus erythematosus and vasculitis. Arthritis Rheum 1982;25:396-400 (Pubitemid 12158947)
33. Morimoto AM, Flesher DT, Yang J, et al. Association of endogenous anti-interferon-α autoantibodies with decreased interferon-pathway and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2011;63:2407-2415
34. Comabella M, Lünemann JD, Río J, et al. A type I interferon signature in monocytes is associated with poor response to interferon-b in multiple sclerosis. Brain 2009;132:3353-3365
35. Le Bon A, Thompson C, Kamphuis E, et al. Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J Immunol 2006;176:2074-2078 (Pubitemid 43201653)
36. Ehlers M, Fukuyama H, McGaha TL, Aderem A, Ravetch JV. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med 2006;203:553-561
37. Bonifacio E, Scirpoli M, Kredel K, Füchtenbusch M, Ziegler AG. Early autoantibody responses in prediabetes are IgG1 dominated and suggest antigen-specific regulation. J Immunol 1999;163:525-532
38. von Herrath M, Sanda S, Herold K. Type 1 diabetes as a relapsing-remitting disease? Nat Rev Immunol 2007;7:988-994
39. Laitinen OH, Honkanen H, Pakkanen O, et al. Coxsackievirus B1 is associated with induction of b -cell autoimmunity that portends type 1 diabetes. Diabetes 2014;63:446-455
40. Mejias A, Dimo B, Suarez NM, et al. Whole blood gene expression profiles to assess pathogenesis and disease severity in infants with respiratory syncytial virus infection. PLoS Med 2013;10:e1001549
41. Heinig M, Petretto E, Wallace C, et al Cardiogenics Consortium. A transacting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 2010;467:460-464
42. Wang Y, Swiecki M, Cella M, et al. Timing and magnitude of type I interferon responses by distinct sensors impact CD8 T cell exhaustion and chronic viral infection. Cell Host Microbe 2012;11:631-642
43. Hervas-Stubbs S, Mancheño U, Riezu-Boj J-I, et al. CD8 T cell priming in the presence of IFN-α renders CTLs with improved responsiveness to homeostatic cytokines and recall antigens: important traits for adoptive T cell therapy. J Immunol 2012;189:3299-3310
44. Downes K, Pekalski M, Angus KL, et al. Reduced expression of IFIH1 is protective for type 1 diabetes. PLoS One 2010;5:e12646
45. Carrero JA, Calderon B, Towfic F, Artyomov MN, Unanue ER. Defining the transcriptional and cellular landscape of type 1 diabetes in the NOD mouse. PLoS One 2013;8:e59701
46. Fabris P, Betterle C, Greggio NA, et al. Insulin-dependent diabetes mellitus during alpha-interferon therapy for chronic viral hepatitis. J Hepatol 1998;28:514-517 (Pubitemid 28133558)
47. Crow MK. Type I interferon in organ-targeted autoimmune and inflammatory diseases. Arthritis Res Ther 2010;12(Suppl. 1):S5
48. Nakamura K, Kawasaki E, Imagawa A, et al; Research Committee on Type 1 Diabetes of the Japan Diabetes Society. Type 1 diabetes and interferon therapy: a nationwide survey in Japan. Diabetes Care 2011;34:2084-2089
49. Decker T, Müller M, Stockinger S. The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 2005;5:675-687 (Pubitemid 43086170)
50. Trinchieri G. Type I interferon: friend or foe? J Exp Med 2010;207:2053-2063
51. González-Navajas JM, Lee J, David M, Raz E. Immunomodulatory functions of type I interferons. Nat Rev Immunol 2012;12:125-135
52. Le Bon A, Etchart N, Rossmann C, et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003;4:1009-1015 (Pubitemid 37265922)
53. Bacher N, Raker V, Hofmann C, et al. Interferon-α suppresses cAMP to disarm human regulatory T cells. Cancer Res 2013;73:5647-5656
54. Tree TIM, Roep BO, Peakman M. A mini meta-analysis of studies on CD4+CD25+ T cells in human type 1 diabetes: report of the Immunology of Diabetes Society T Cell Workshop. Ann N Y Acad Sci 2006;1079:9-18 (Pubitemid 44968695)
55. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol 2013;14:36-49