Potential viral pathogenic mechanism in human type 1 diabetes

Diabetologia

Volumn 57, Issue 10, 2014, Pages 2009-2018

  Schneider, Darius A ^a,b   von Herrath, Matthias G ^a,c  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c NOVO NORDISK INC   (United States)

Author keywords

Autoimmune; Enterovirus; Environmental factors; Humans; Insulitis; Type 1 diabetes; Viruses

Indexed keywords

COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR;

ARTICLE; AUTOIMMUNITY; ENDOGENOUS RETROVIRUS; ENTEROVIRUS; HUMAN; INFECTION; INFECTION RISK; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; INTESTINE CELL; NERVE CELL; PANCREAS CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS TRANSFORMATION; CD8+ T LYMPHOCYTE; COMPLICATION; DIABETES MELLITUS, TYPE 1; IMMUNOLOGY; VIROLOGY;

AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; HUMANS; VIRUS DISEASES;

EID: 84926648661     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3340-7     Document Type: Article

References (108)

1. KarvonenM, Viik-KajanderM, Moltchanova E, Libman I, LaPorte R, Tuomilehto J (2000) Incidence of childhood type 1 diabetes worldwide. DiabetesMondiale (DiaMond) Project Group. Diabetes Care 23: 1516-1526.
2. Kondrashova A, Reunanen A, Romanov A et al (2005) A six-fold gradient in the incidence of type 1 diabetes at the eastern border of Finland. Ann Med 37: 67-72.
3. Bodansky HJ, Staines A, Stephenson C, Haigh D, Cartwright R (1992) Evidence for an environmental effect in the aetiology of insulin dependent diabetes in a transmigratory population. BMJ 304: 1020-1022.
4. Delli AJ, Lindblad B, Carlsson A et al (2010) Type 1 diabetes patients born to immigrants to Sweden increase their native diabetes risk and differ from Swedish patients in HLA types and islet autoantibodies. Pediatr Diabetes 11: 513-520.
5. Lang KS, Recher M, Junt T et al (2005) Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med 11: 138-145.
6. Rhode A, Pauza ME, Barral AM et al (2005) Islet-specific expression of CXCL10 causes spontaneous islet infiltration and accelerates diabetes development. J Immunol 175: 3516-3524.
7. Frigerio S, Junt T, Lu B et al (2002) Beta cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nat Med 8: 1414-1420.
8. von Herrath M, Holz A (1997) Pathological changes in the islet milieu precede infiltration of islets and destruction of beta-cells by autoreactive lymphocytes in a transgenic model of virus-induced IDDM. J Autoimmun 10: 231-238.
9. Wolter TR, Wong R, Sarkar SA, Zipris D (2009) DNA microarray analysis for the identification of innate immune pathways implicated in virus-induced autoimmune diabetes. Clin Immunol 132: 103-115.
10. Nair A, Wolter TR, Meyers AJ, Zipris D (2008) Innate immune pathways in virus-induced autoimmune diabetes. AnnN YAcad Sci 1150: 139-142.
11. Foulis AK (2008) Pancreatic pathology in type 1 diabetes in human. Novartis Found Symp 292: 2-13, discussion 13-18, 122-129, 202-203.
12. Roep BO, Kleijwegt FS, van Halteren AG et al (2010) Islet inflammation and CXCL10 in recent-onset type 1 diabetes. Clin Exp Immunol 159: 338-343.
13. Kallionpää H, Elo LL, Laajala E et al (2014) Innate immune activity is detected prior to seroconversion in children with HLA-conferred type 1 diabetes susceptibility. Diabetes 63: 2402-2414.
14. Foulis AK, Liddle CN, Farquharson MA, Richmond JA, Weir RS (1986) The histopathology of the pancreas in type 1 (insulindependent) diabetes mellitus: a 25-year review of deaths in patients under 20 years of age in the United Kingdom. Diabetologia 29: 267-274.
15. Coppieters KT, Dotta F, Amirian N et al (2012) Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 209: 51-60.
16. + T cells. J Exp Med 197: 643-656.
17. + T-cells encounter their cognate antigen and acquire capacity to destroy target hepatocytes. J Autoimmun 42: 19-28.
18. Gepts W (1965) Pathologic anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 14: 619-633.
19. Eisenbarth GS (1986) Type I diabetes mellitus. A chronic autoimmune disease. N Engl J Med 314: 1360-1368.
20. Campbell-Thompson ML, Atkinson MA, Butler AE et al (2013) The diagnosis of insulitis in human type 1 diabetes. Diabetologia 56: 2541-2543.
21. Pipeleers D, Ling Z (1992) Pancreatic beta cells in insulindependent diabetes. Diabetes Metab Rev 8: 209-227.
22. In't Veld P (2011) Insulitis in human type 1 diabetes: the quest for an elusive lesion. Islets 3: 131-138.
23. In't Veld P, Lievens D, De Grijse J et al (2007) Screening for insulitis in adult autoantibody-positive organ donors. Diabetes 56: 2400-2404.
24. Gepts W, De Mey J (1978) Islet cell survival determined by morphology. An immunocytochemical study of the islets of Langerhans in juvenile diabetes mellitus. Diabetes 27(Suppl 1): 251-261.
25. Gianani R, Campbell-Thompson M, Sarkar SA et al (2010) Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53: 690-698.
26. Schneider D, Von Herrath M (2014) Studies of the cytokine milieu of pancreatic islets and its role in the ontology of immune mediated diabetes. In: Annual Conference of the Network for Pancreatic Organ Donors, nPOD, Jacksonville (Abstract).
27. Fonseca V, Berger LA, Beckett AG, Dandona P (1985) Size of pancreas in diabetes mellitus: a study based on ultrasound. Br Med J (Clin Res Ed) 291: 1240-1241.
28. Campbell-Thompson M, Wasserfall C, Montgomery EL, AtkinsonMA, Kaddis JS (2012) Pancreas organ weight in individuals with disease-associated autoantibodies at risk for type 1 diabetes. JAMA 308: 2337-2339.
29. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG (2009) Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 155: 173-181.
30. AtkinsonMA, Eisenbarth GS (2001) Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 358: 221-229.
31. Ziegler AG, Nepom GT (2010) Prediction and pathogenesis in type 1 diabetes. Immunity 32: 468-478.
32. von Herrath MG, Fujinami RS, Whitton JL (2003) Microorganisms and autoimmunity: making the barren field fertile? Nat RevMicrobiol 1: 151-157.
33. von Herrath M, Sanda S, Herold K (2007) Type 1 diabetes as a relapsing-remitting disease? Nat Rev Immunol 7: 988-994.
34. Fujinami RS, von Herrath MG, Christen U, Whitton JL (2006) Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 19: 80-94.
35. Skog O, Korsgren S, Melhus A, Korsgren O (2013) Revisiting the notion of type 1 diabetes being a T-cell-mediated autoimmune disease. Curr Opin Endocrinol Diabetes Obes 20: 118-123.
36. Jenson AB, Rosenberg HS, Notkins AL (1980) Pancreatic islet-cell damage in children with fatal viral infections. Lancet 2: 354-358.
37. Oikarinen M, Tauriainen S, Honkanen T et al (2008) Analysis of pancreas tissue in a child positive for islet cell antibodies. Diabetologia 51: 1796-1802.
38. Skog O, Korsgren O, Frisk G (2011) Modulation of innate immunity in human pancreatic islets infected with enterovirus in vitro. J Med Virol 83: 658-664.
39. Alidjinou EK, Sané F, Engelmann I, Hober D (2013) Serumdependent enhancement of coxsackievirus B4-induced production of IFNα, IL-6 and TNFα by peripheral blood mononuclear cells. J Mol Biol 425: 5020-5031.
40. Parks GD, Alexander-Miller MA Paramyxovirus activation and inhibition of innate immune responses. J Mol Biol 425: 4872-4892.
41. Koma T, Huang C, Kolokoltsova OA, Brasier AR, Paessler S (2013) Innate immune response to arenaviral infection: a focus on the highly pathogenic New World hemorrhagic arenaviruses. J Mol Biol 425: 4893-4903.
42. Turley SJ, Lee JW, Dutton-Swain N, Mathis D, Benoist C (2005) Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc Natl Acad Sci U S A 102: 17729-17733.
43. Akatsuka H, Yano Y, Gabazza EC et al (2009) A case of fulminant type 1 diabeteswith coxsackie B4 virus infection diagnosed by elevated serum levels of neutralizing antibody. Diabetes Res Clin Pract 84: e50-e52.
44. Barboni E, Manocchio I, Asdrubali G (1966) Observations on diabetes in cattle due to experimental epizootic aphthae (Preliminary note). Nuovi Ann Ig Microbiol 17: 223-226 [Article in Italian].
45. Niklasson B, Heller KE, Schonecker B et al (2003) Development of type 1 diabetes in wild bank voles associated with islet autoantibodies and the novel Ljungan virus. Int J Exp Diabesity Res 4: 35-44.
46. Ellerman KE, Richards CA, Guberski DL, Shek WR, Like AA (1996) Kilham rat triggers T-cell-dependent autoimmune diabetes in multiple strains of rat. Diabetes 45: 557-562.
47. Yoon JW, London WT, Curfman BL, Brown RL, Notkins AL (1986) Coxsackie virus B4 produces transient diabetes in nonhuman primates. Diabetes 35: 712-716.
48. Yang C, Diiorio P, Jurczyk A, O'Sullivan-Murphy B, Urano F, Bortell R (2013) Pathological endoplasmic reticulum stress mediated by the IRE1 pathway contributes to pre-insulitic beta cell apoptosis in a virus-induced rat model of type 1 diabetes. Diabetologia 56: 2638-2646.
49. ChehadehW, Kerr-Conte J, Pattou F et al (2000) Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J Virol 74: 10153-10164.
50. Prchal-Murphy M, Semper C, Lassnig C et al (2012) TYK2 kinase activity is required for functional type I interferon responses in vivo. PLoS One 7: e39141.
51. Richer MJ, Horwitz MS (2008) Viral infections in the pathogenesis of autoimmune diseases: focus on type 1 diabetes. Front Biosci 13: 4241-4257.
52. Capua I, Mercalli A, Pizzuto MS et al (2012) Influenza A viruses grow in human pancreatic cells and cause pancreatitis and diabetes in an animal model. J Virol 87: 597-610.
53. Sano H, Terasaki J, Tsutsumi C, Imagawa A, Hanafusa T (2008) A case of fulminant type 1 diabetes mellitus after influenza B infection. Diabetes Res Clin Pract 79: e8-e9.
54. Bonifacio E, Krumsiek J, Winkler C, Theis FJ, ZieglerAG (2013) A strategy to find gene combinations that identify children who progress rapidly to type 1 diabetes after islet autoantibody seroconversion. Acta Diabetol 51: 403-411.
55. + sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 127: 1123-1135.
56. Shen Z, He H, Wu Y, Li J (2013) Cyclosporin a inhibits rotavirus replication and restores interferon-beta signaling pathway in vitro and in vivo. PLoS One 8: e71815.
57. Lakhan SE, Kirchgessner A (2010) Gut inflammation in chronic fatigue syndrome. Nutr Metab (Lond) 7: 79.
58. Coppieters KT, von Herrath MG (2010) Viruses and cytotoxic T lymphocytes in type 1 diabetes. Clin Rev Allergy Immunol 41: 169-178.
59. Vreugdenhil GR, Geluk A, Ottenhoff TH, Melchers WJ, Roep BO, Galama JM (1998) Molecular mimicry in diabetes mellitus: the homologous domain in coxsackie B virus protein 2C and islet autoantigen GAD65 is highly conserved in the coxsackie B-like enteroviruses and binds to the diabetes associated HLA-DR3 molecule. Diabetologia 41: 40-46.
60. Wucherpfennig KW, Strominger JL (1995) Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 80: 695-705.
61. Oikarinen S, Tauriainen S, Hober D et al (2014) Virus antibody survey in different european populations indicates risk association between coxsackievirus B1 and type 1 diabetes. Diabetes 63: 655-662.
62. Laitinen OH, Honkanen H, Pakkanen O et al (2014) Coxsackievirus B1 is associated with induction of beta-cell autoimmunity that portends type 1 diabetes. Diabetes 63: 446-455.
63. Yoon JW, Austin M, Onodera T, Notkins AL (1979) Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 300: 1173-1179.
64. Ramondetti F, Sacco S, Comelli M et al (2011) Type 1 diabetes and measles, mumps and rubella childhood infections within the Italian Insulin-dependent Diabetes Registry. Diabet Med 29: 761-766.
65. Stene LC, Oikarinen S, Hyoty H et al (2010) Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: the Diabetes andAutoimmunity Study in the Young (DAISY). Diabetes 59: 3174-3180.
66. Sarmiento L, Frisk G, Anagandula M, Cabrera-Rode E, Roivainen M, Cilio CM (2013) Expression of innate immunity genes and damage of primary human pancreatic islets by epidemic strains of echovirus: implication for post-virus islet autoimmunity. PLoS One 8: e77850.
67. Honke N, Shaabani N, Zhang DE et al (2013) Usp18 driven enforced viral replication in dendritic cells contributes to break of immunological tolerance in autoimmune diabetes. PLoS Pathog 9: e1003650.
68. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD (2013) Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A 110: 12450-12455.
69. Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453: 620-625.
70. Balada E, Vilardell-Tarres M, Ordi-Ros J (2010) Implication of human endogenous retroviruses in the development of autoimmune diseases. Int Rev Immunol 29: 351-370.
71. Schneider D, Chodaczek G, Coppieters K, Von Herrath M (2013) Antigen-specificity requirements for T cell invasion of pancreatic islets in a virus-induced autoimmune diabetes model. In: Annual Conference of the Federation of Clinical Immunology Societies, Boston, No. F. 38 (Abstract).
72. Pane JA, Webster NL, Graham KL, Holloway G, Zufferey C, Coulson BS (2012) Rotavirus acceleration of murine type 1 diabetes is associated with a T helper 1-dependent specific serum antibody response and virus effects in regional lymph nodes. Diabetologia 56: 573-582.
73. Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302: 575-581.
74. Goodnow CC, Sprent J, Fazekas de St Groth B, Vinuesa CG (2005) Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435: 590-597.
75. Zandman-Goddard G, Shoenfeld Y (2002) HIVand autoimmunity. Autoimmun Rev 1: 329-337.
76. Niller HH, Wolf H, Minarovits J (2008) Regulation and dysregulation of Epstein-Barr virus latency: implications for the development of autoimmune diseases. Autoimmunity 41: 298-328.
77. Vento S, McFarlane BM, McSorley CG et al (1988) Liver autoreactivity in acute virus A, B and non-A, non-B hepatitis. J Clin Lab Immunol 25: 1-7.
78. Cassani F, Cataleta M, Valentini P et al (1997) Serum autoantibodies in chronic hepatitis C: comparison with autoimmune hepatitis and impact on the disease profile. Hepatology 26: 561-566.
79. Ahmed R, Byrne JA, Oldstone MB (1984) Virus specificity of cytotoxic T lymphocytes generated during acute lymphocytic choriomeningitis virus infection: role of the H-2 region in determining cross-reactivity for different lymphocytic choriomeningitis virus strains. J Virol 51: 34-41.
80. Hunziker L, Recher M, Macpherson AJ et al (2003) Hypergammaglobulinemia and autoantibody induction mechanisms in viral infections. Nat Immunol 4: 343-349.
81. Mouquet H, Nussenzweig MC (2011) Polyreactive antibodies in adaptive immune responses to viruses. Cell Mol Life Sci 69: 1435-1445.
82. Filippi CM, Estes EA, Oldham JE, von Herrath MG (2009) Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice. J Clin Invest 119: 1515-1523.
83. Filippi CM, Ehrhardt K, Estes EA, Larsson P, Oldham JE, von Herrath MG (2011) TLR2 signaling improves immunoregulation to prevent type 1 diabetes. Eur J Immunol 41: 1399-1409.
84. Kanno T, Kim K, Kono K, Drescher KM, Chapman NM, Tracy S (2006) Group B coxsackievirus diabetogenic phenotype correlates with replication efficiency. J Virol 80: 5637-5643.
85. Willcox A, Richardson SJ, BoneAJ, Foulis AK, Morgan NG (2011) Immunohistochemical analysis of the relationship between islet cell proliferation and the production of the enteroviral capsid protein, VP1, in the islets of patients with recent-onset type 1 diabetes. Diabetologia 54: 2417-2420.
86. Hansson SF, Korsgren S, Ponten F, Korsgren O (2013) Enteroviruses and the pathogenesis of type 1 diabetes revisited: cross-reactivity of enterovirus capsid protein (VP1) antibodies with human mitochondrial proteins. J Pathol 229: 719-728.
87. Pugliese A, Yang M, Kusmarteva I et al (2014) The Juvenile Diabetes Research Foundation Network for Pancreatic Organ Donors with Diabetes (nPOD) Program: goals, operational model and emerging findings. Pediatr Diabetes 15: 1-9.
88. Korsgren S, MolinY, SalmelaK, LundgrenT, MelhusA, KorsgrenO (2012) On the etiology of type 1 diabetes: a new animal model signifying a decisive role for bacteria eliciting an adverse innate immunity response. Am J Pathol 181: 1735-1748.
89. Temajo NO, Howard N (2014) The mosaic of environment involvement in autoimmunity: the abrogation of viral latency by stress, a non-infectious environmental agent, is an intrinsic prerequisite prelude before viruses can rank as infectious environmental agents that trigger autoimmune diseases. Autoimmun Rev 13: 653-658.
90. Rasmussen T, Witso E, Tapia G, Stene LC, Ronningen KS (2011) Self-reported lower respiratory tract infections and development of islet autoimmunity in children with the type 1 diabetes highrisk HLA genotype: the MIDIA study. Diabetes Metab Res Rev 27: 834-837.
91. Beyerlein A, Wehweck F, Ziegler AG, Pflueger M (2013) 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 167: 800-807.
92. Gale EA (2008) Congenital rubella: citation virus or viral cause of type 1 diabetes? Diabetologia 51: 1559-1566.
93. Viskari H, Paronen J, Keskinen P et al (2003) Humoral beta-cell autoimmunity is rare in patients with the congenital rubella syndrome. Clin Exp Immunol 133: 378-383.
94. Green J, Casabonne D, Newton R (2004) Coxsackie B virus serology and type 1 diabetes mellitus: a systematic review of published case-control studies. Diabet Med 21: 507-514.
95. Tapia G, Cinek O, Rasmussen T et al (2010) Human enterovirus RNA in monthly fecal samples and islet autoimmunity in Norwegian children with high genetic risk for type 1 diabetes: the MIDIA study. Diabetes Care 34: 151-155.
96. YeungWC, RawlinsonWD, Craig ME (2011) Enterovirus infection and type 1 diabetes mellitus: systematic reviewandmeta-analysis of observational molecular studies. BMJ 342: d35.
97. Salur L, Oikarinen S, Tauriainen S, Mandel M, Hyoty H, Uibo R (2011) Enterovirus infections in young infants: are children still protected by maternal antibodies? Hum Vaccin 7: 966-971.
98. OikarinenM, Tauriainen S, Oikarinen S et al (2012) Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 61: 687-691.
99. Mercalli A, Lampasona V, Klingel K et al (2012) No evidence of enteroviruses in the intestine of patients with type 1 diabetes. Diabetologia 55: 2479-2488.
100. Viskari HR, Koskela P, Lonnrot M et al (2000) Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 23: 414-416.
101. Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T (2002) Functional impairment and killing of human beta cells by enteroviruses: the capacity is shared by a wide range of serotypes, but the extent is a characteristic of individual virus strains. Diabetologia 45: 693-702.
102. Viskari H, Ludvigsson J, Uibo R et al (2004) Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: results from the EPIVIR project. J Med Virol 72: 610-617.
103. Viskari H, Ludvigsson J, Uibo R et al (2005) Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation. Diabetologia 48: 1280-1287.
104. Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG (2009) The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52: 1143-1151.
105. GambleDR, Taylor KW, CummingH (1973) Coxsackie viruses and diabetes mellitus. Br Med J 4: 260-262.
106. Gamble DR, Kinsley ML, FitzGerald MG, Bolton R, Taylor KW (1969) Viral antibodies in diabetes mellitus. Br Med J 3: 627-630.
107. Dotta F, Censini S, van Halteren AG et al (2007) Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recentonset type 1 diabetic patients. Proc Natl Acad Sci U S A 104: 5115-5120.
108. Cabrera-Rode E, Sarmiento L, Tiberti C et al (2003) Type 1 diabetes islet associated antibodies in subjects infected by echovirus 16. Diabetologia 46: 1348-1353.