Advertisement

Cellular and Molecular Life Sciences

, Volume 70, Issue 2, pp 239–255 | Cite as

Prevention or acceleration of type 1 diabetes by viruses

  • Liana Ghazarian
  • Julien Diana
  • Yannick Simoni
  • Lucie Beaudoin
  • Agnès Lehuen
Review

Abstract

Type 1 diabetes is an autoimmune disease characterized by the destruction of insulin-producing pancreatic β-cells. Even though extensive scientific research has yielded important insights into the immune mechanisms involved in pancreatic β-cell destruction, little is known about the events that trigger the autoimmune process. Recent epidemiological and experimental data suggest that environmental factors are involved in this process. In this review, we discuss the role of viruses as an environmental factor on the development of type 1 diabetes, and the immune mechanisms by which they can trigger or protect against this pathology.

Keywords

Diabetes Environment Virus Coxsackievirus 

Notes

Acknowledgments

We apologize to all the authors whose work we could not cite owing to space constrictions. This work was supported by funds from the Institut National de la Santé et de la Recherche Médicale and the Centre National pour la Recherche Scientifique, grant from ANR-09-GENO-023 and LABEX INFLAMEX to AL. Liana Ghazarian and Yannick Simoni were supported by doctoral fellowships from the Ministère de l'Education Nationale et de la Recherche et Technique and from Région Île-de-France.

Competing interests statement

The authors declare no competing financial interests.

References

  1. 1.
    Hanafusa T, Imagawa A (2007) Fulminant type 1 diabetes: a novel clinical entity requiring special attention by all medical practitioners. Nat Clin Pract Endocrinol Metab 3(1):36–45. doi: 10.1038/ncpendmet0351 (quiz 32p following 69)PubMedCrossRefGoogle Scholar
  2. 2.
    Knip M (2002) Natural course of preclinical type 1 diabetes. Horm Res 57(Suppl 1):6–11 [pii:53305]PubMedCrossRefGoogle Scholar
  3. 3.
    Ziegler AG, Nepom GT (2010) Prediction and pathogenesis in type 1 diabetes. Immunity 32(4):468–478. doi: 10.1016/j.immuni.2010.03.018 PubMedCrossRefGoogle Scholar
  4. 4.
    Mallone R, Brezar V, Boitard C (2011) T cell recognition of autoantigens in human type 1 diabetes: clinical perspectives. Clin Dev Immunol 2011:513210. doi: 10.1155/2011/513210 PubMedCrossRefGoogle Scholar
  5. 5.
    Wadonda-Kabondo N, Sterne JA, Golding J, Kennedy CT, Archer CB, Dunnill MG (2003) A prospective study of the prevalence and incidence of atopic dermatitis in children aged 0–42 months. Br J Dermatol 149(5):1023–1028. doi: 5605 PubMedCrossRefGoogle Scholar
  6. 6.
    Williams HC (1992) Is the prevalence of atopic dermatitis increasing? Clin Exp Dermatol 17(6):385–391PubMedCrossRefGoogle Scholar
  7. 7.
    Ma RC, Chan JC (2009) Diabetes: incidence of childhood type 1 diabetes: a worrying trend. Nat Rev Endocrinol 5(10):529–530. doi: 10.1038/nrendo.2009.180 PubMedCrossRefGoogle Scholar
  8. 8.
    Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G (2009) Incidence trends for childhood type 1 diabetes in Europe during 1989–2003 and predicted new cases 2005–20: a multicentre prospective registration study. Lancet 373(9680):2027–2033. doi: 10.1016/S0140-6736(09)60568-7 PubMedCrossRefGoogle Scholar
  9. 9.
    Sellner J, Kraus J, Awad A, Milo R, Hemmer B, Stuve O (2011) The increasing incidence and prevalence of female multiple sclerosis—a critical analysis of potential environmental factors. Autoimmun Rev 10(8):495–502. doi: 10.1016/j.autrev.2011.02.006 PubMedCrossRefGoogle Scholar
  10. 10.
    Gismera CS, Aladren BS (2008) Inflammatory bowel diseases: a disease(s) of modern times? Is incidence still increasing? World J Gastroenterol 14(36):5491–5498PubMedCrossRefGoogle Scholar
  11. 11.
    Karvonen M, Viik-Kajander M, Moltchanova E, Libman I, LaPorte R, Tuomilehto J (2000) Incidence of childhood type 1 diabetes worldwide. Diabetes Mondiale (DiaMond) Project Group. Diabetes Care 23(10):1516–1526PubMedCrossRefGoogle Scholar
  12. 12.
    Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347(12):911–920. doi: 10.1056/NEJMra020100347/12/911 PubMedCrossRefGoogle Scholar
  13. 13.
    Hernan MA, Olek MJ, Ascherio A (1999) Geographic variation of MS incidence in two prospective studies of US women. Neurology 53(8):1711–1718PubMedCrossRefGoogle Scholar
  14. 14.
    McLeod JG, Hammond SR, Hallpike JF (1994) Epidemiology of multiple sclerosis in Australia. With NSW and SA survey results. Med J Aust 160(3):117–122PubMedGoogle Scholar
  15. 15.
    Newhook LA, Grant M, Sloka S, Hoque M, Paterson AD, Hagerty D, Curtis J (2008) Very high and increasing incidence of type 1 diabetes mellitus in Newfoundland and Labrador Canada. Pediatr Diabetes 9(3 Pt 2):62–68. doi: 10.1111/j.1399-5448.2007.00315.x PubMedCrossRefGoogle Scholar
  16. 16.
    Green A, Patterson CC (2001) Trends in the incidence of childhood-onset diabetes in Europe 1989–1998. Diabetologia 44(Suppl 3):B3–B8PubMedCrossRefGoogle Scholar
  17. 17.
    Daimond Project Group (2006) Incidence and trends of childhood type 1 diabetes worldwide 1990–1999. Diabet Med 23(8):857–866. doi: 10.1111/j.1464-5491.2006.01925.x CrossRefGoogle Scholar
  18. 18.
    The Eurodiab Ace Study Group, The Eurodiab Ace Substudy 2 Study Group (1998) Familial risk of type I diabetes in European children. Diabetologia 41(10):1151–1156CrossRefGoogle Scholar
  19. 19.
    Redondo MJ, Jeffrey J, Fain PR, Eisenbarth GS, Orban T (2008) Concordance for islet autoimmunity among monozygotic twins. N Engl J Med 359(26):2849–2850. doi: 10.1056/NEJMc0805398 PubMedCrossRefGoogle Scholar
  20. 20.
    Hyttinen V, Kaprio J, Kinnunen L, Koskenvuo M, Tuomilehto J (2003) Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: a nationwide follow-up study. Diabetes 52(4):1052–1055PubMedCrossRefGoogle Scholar
  21. 21.
    Barrett JC, Clayton DG, Concannon P, Akolkar B, Cooper JD, Erlich HA, Julier C, Morahan G, Nerup J, Nierras C, Plagnol V, Pociot F, Schuilenburg H, Smyth DJ, Stevens H, Todd JA, Walker NM, Rich SS (2009) Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 41(6):703–707. doi: 10.1038/ng.381 PubMedCrossRefGoogle Scholar
  22. 22.
    Ronningen KS, Keiding N, Green A (2001) Correlations between the incidence of childhood-onset type I diabetes in Europe and HLA genotypes. Diabetologia 44(Suppl 3):B51–B59PubMedCrossRefGoogle Scholar
  23. 23.
    Almawi WY, Busson M, Tamim H, Al-Harbi EM, Finan RR, Wakim-Ghorayeb SF, Motala AA (2004) HLA class II profile and distribution of HLA-DRB1 and HLA-DQB1 alleles and haplotypes among Lebanese and Bahraini Arabs. Clin Diagn Lab Immunol 11(4):770–774. doi: 10.1128/CDLI.11.4.770-774.2004 PubMedGoogle Scholar
  24. 24.
    Park Y, Eisenbarth GS (2001) Genetic susceptibility factors of type 1 diabetes in Asians. Diabetes Metab Res Rev 17(1):2–11. doi: 10.1002/1520-7560(2000)9999:9999<:AID-DMRR164>3.0.CO;2-M PubMedCrossRefGoogle Scholar
  25. 25.
    Kondrashova A, Reunanen A, Romanov A, Karvonen A, Viskari H, Vesikari T, Ilonen J, Knip M, Hyoty H (2005) A sixfold gradient in the incidence of type 1 diabetes at the eastern border of Finland. Ann Med 37(1):67–72PubMedCrossRefGoogle Scholar
  26. 26.
    Skrodeniene E, Marciulionyte D, Padaiga Z, Jasinskiene E, Sadauskaite-Kuehne V, Sanjeevi CB, Ludvigsson J (2010) HLA class II alleles and haplotypes in Lithuanian children with type 1 diabetes and healthy children (HLA and type 1 diabetes). Medicina (Kaunas) 46(8):505–510 [pii:1008-01e]Google Scholar
  27. 27.
    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(6833):1020–1022PubMedCrossRefGoogle Scholar
  28. 28.
    Delli AJ, Lindblad B, Carlsson A, Forsander G, Ivarsson SA, Ludvigsson J, Marcus C, Lernmark A (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(8):513–520. doi: 10.1111/j.1399-5448.2010.00637.x PubMedCrossRefGoogle Scholar
  29. 29.
    Bruno G, Pagano G, Faggiano F, De Salvia A, Merletti F (2000) Effect of Sardinian heritage on risk and age at onset of type 1 diabetes: a demographic case-control study of Sardinian migrants. Int J Epidemiol 29(3):532–535PubMedCrossRefGoogle Scholar
  30. 30.
    Muntoni S, Fonte MT, Stoduto S, Marietti G, Bizzarri C, Crino A, Ciampalini P, Multari G, Suppa MA, Matteoli MC, Lucentini L, Sebastiani LM, Visalli N, Pozzilli P, Boscherini B (1997) Incidence of insulin-dependent diabetes mellitus among Sardinian-heritage children born in Lazio region Italy. Lancet 349(9046):160–162 [pii:S0140673696042419]PubMedCrossRefGoogle Scholar
  31. 31.
    Borchers AT, Uibo R, Gershwin ME (2010) The geoepidemiology of type 1 diabetes. Autoimmun Rev 9(5):A355–A365. doi: 10.1016/j.autrev.2009.12.003 PubMedCrossRefGoogle Scholar
  32. 32.
    Gillespie KM, Bain SC, Barnett AH, Bingley PJ, Christie MR, Gill GV, Gale EA (2004) The rising incidence of childhood type 1 diabetes and reduced contribution of high-risk HLA haplotypes. Lancet 364(9446):1699–1700. doi: 10.1016/S0140-6736(04)17357-1 PubMedCrossRefGoogle Scholar
  33. 33.
    Hermann R, Knip M, Veijola R, Simell O, Laine AP, Akerblom HK, Groop PH, Forsblom C, Pettersson-Fernholm K, Ilonen J (2003) Temporal changes in the frequencies of HLA genotypes in patients with type 1 diabetes—indication of an increased environmental pressure? Diabetologia 46(3):420–425. doi: 10.1007/s00125-003-1045-4 PubMedGoogle Scholar
  34. 34.
    Patterson CC, Dahlquist G, Soltesz G, Green A (2001) Is childhood-onset type I diabetes a wealth-related disease? An ecological analysis of European incidence rates. Diabetologia 44(Suppl 3):B9–B16PubMedCrossRefGoogle Scholar
  35. 35.
    Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299(6710):1259–1260PubMedCrossRefGoogle Scholar
  36. 36.
    Lehuen A, Diana J, Zaccone P, Cooke A (2010) Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol 10(7):501–513. doi: 10.1038/nri2787 PubMedCrossRefGoogle Scholar
  37. 37.
    Cooke A, Tonks P, Jones FM, O’Shea H, Hutchings P, Fulford AJ, Dunne DW (1999) Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 21(4):169–176PubMedCrossRefGoogle Scholar
  38. 38.
    Zaccone P, Burton OT, Gibbs S, Miller N, Jones FM, Dunne DW, Cooke A (2010) Immune modulation by Schistosoma mansoni antigens in NOD mice: effects on both innate and adaptive immune systems. J Biomed Biotechnol 2010:795210. doi: 10.1155/2010/795210 PubMedCrossRefGoogle Scholar
  39. 39.
    Saunders KA, Raine T, Cooke A, Lawrence CE (2007) Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun 75(1):397–407. doi: 10.1128/IAI.00664-06 PubMedCrossRefGoogle Scholar
  40. 40.
    Liu Q, Sundar K, Mishra PK, Mousavi G, Liu Z, Gaydo A, Alem F, Lagunoff D, Bleich D, Gause WC (2009) Helminth infection can reduce insulitis and type 1 diabetes through CD25- and IL-10-independent mechanisms. Infect Immun 77(12):5347–5358. doi: 10.1128/IAI.01170-08 PubMedCrossRefGoogle Scholar
  41. 41.
    Hubner MP, Stocker JT, Mitre E (2009) Inhibition of type 1 diabetes in filaria-infected non-obese diabetic mice is associated with a T helper type 2 shift and induction of FoxP3+ regulatory T cells. Immunology 127(4):512–522. doi: 10.1111/j.1365-2567.2008.02958.x PubMedCrossRefGoogle Scholar
  42. 42.
    Newland SA, Phillips JM, Mastroeni P, Azuma M, Zaccone P, Cooke A (2011) PD-L1 blockade overrides Salmonella typhimurium-mediated diabetes prevention in NOD mice: no role for Tregs. Eur J Immunol 41(10):2966–2976. doi: 10.1002/eji.201141544 PubMedCrossRefGoogle Scholar
  43. 43.
    Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV (2008) Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455(7216):1109–1113. doi: 10.1038/nature07336 PubMedCrossRefGoogle Scholar
  44. 44.
    Bras A, Aguas AP (1996) Diabetes-prone NOD mice are resistant to Mycobacterium avium and the infection prevents autoimmune disease. Immunology 89(1):20–25PubMedCrossRefGoogle Scholar
  45. 45.
    Martins TC, Aguas AP (1999) Mechanisms of Mycobacterium avium-induced resistance against insulin-dependent diabetes mellitus (IDDM) in non-obese diabetic (NOD) mice: role of Fas and Th1 cells. Clin Exp Immunol 115(2):248–254PubMedCrossRefGoogle Scholar
  46. 46.
    Rosu V, Ahmed N, Paccagnini D, Gerlach G, Fadda G, Hasnain SE, Zanetti S, Sechi LA (2009) Specific immunoassays confirm association of Mycobacterium avium Subsp. paratuberculosis with type-1 but not type-2 diabetes mellitus. PLoS ONE 4(2):e4386. doi: 10.1371/journal.pone.0004386 PubMedCrossRefGoogle Scholar
  47. 47.
    Sechi LA, Paccagnini D, Salza S, Pacifico A, Ahmed N, Zanetti S (2008) Mycobacterium avium subspecies paratuberculosis bacteremia in type 1 diabetes mellitus: an infectious trigger? Clin Infect Dis 46(1):148–149. doi: 10.1086/524084 PubMedCrossRefGoogle Scholar
  48. 48.
    Rani PS, Sechi LA, Ahmed N (2010) Mycobacterium avium subsp. paratuberculosis as a trigger of type-1 diabetes: destination Sardinia, or beyond? Gut Pathog 2(1):1. doi: 10.1186/1757-4749-2-1 PubMedCrossRefGoogle Scholar
  49. 49.
    Luopajarvi K, Savilahti E, Virtanen SM, Ilonen J, Knip M, Akerblom HK, Vaarala O (2008) Enhanced levels of cow’s milk antibodies in infancy in children who develop type 1 diabetes later in childhood. Pediatr Diabetes 9(5):434–441. doi: 10.1111/j.1399-5448.2008.00413.x PubMedCrossRefGoogle Scholar
  50. 50.
    Elliott RB, Harris DP, Hill JP, Bibby NJ, Wasmuth HE (1999) Type I (insulin-dependent) diabetes mellitus and cow milk: casein variant consumption. Diabetologia 42(3):292–296. doi: 10.1007/s001250051153 PubMedCrossRefGoogle Scholar
  51. 51.
    Birgisdottir BE, Hill JP, Harris DP, Thorsdottir I (2002) Variation in consumption of cow milk proteins and lower incidence of type 1 diabetes in Iceland vs the other 4 Nordic countries. Diabetes Nutr Metab 15(4):240–245PubMedGoogle Scholar
  52. 52.
    Birgisdottir BE, Hill JP, Thorsson AV, Thorsdottir I (2006) Lower consumption of cow milk protein A1 beta-casein at 2 years of age, rather than consumption among 11- to 14-year-old adolescents, may explain the lower incidence of type 1 diabetes in Iceland than in Scandinavia. Ann Nutr Metab 50(3):177–183. doi: 10.1159/000090738 PubMedCrossRefGoogle Scholar
  53. 53.
    Smyth DJ, Plagnol V, Walker NM, Cooper JD, Downes K, Yang JH, Howson JM, Stevens H, McManus R, Wijmenga C, Heap GA, Dubois PC, Clayton DG, Hunt KA, van Heel DA, Todd JA (2008) Shared and distinct genetic variants in type 1 diabetes and celiac disease. N Engl J Med 359(26):2767–2777. doi: 10.1056/NEJMoa0807917 PubMedCrossRefGoogle Scholar
  54. 54.
    Maki M, Mustalahti K, Kokkonen J, Kulmala P, Haapalahti M, Karttunen T, Ilonen J, Laurila K, Dahlbom I, Hansson T, Hopfl P, Knip M (2003) Prevalence of Celiac disease among children in Finland. N Engl J Med 348(25):2517–2524. doi: 10.1056/NEJMoa021687348/25/2517 PubMedCrossRefGoogle Scholar
  55. 55.
    Ziegler AG, Schmid S, Huber D, Hummel M, Bonifacio E (2003) Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 290(13):1721–1728. doi: 10.1001/jama.290.13.1721290/13/1721 PubMedCrossRefGoogle Scholar
  56. 56.
    Mohr SB, Garland CF, Gorham ED, Garland FC (2008) The association between ultraviolet B irradiance, vitamin D status and incidence rates of type 1 diabetes in 51 regions worldwide. Diabetologia 51(8):1391–1398. doi: 10.1007/s00125-008-1061-5 PubMedCrossRefGoogle Scholar
  57. 57.
    Sloka S, Grant M, Newhook LA (2010) The geospatial relation between UV solar radiation and type 1 diabetes in Newfoundland. Acta Diabetol 47(1):73–78. doi: 10.1007/s00592-009-0100-0 PubMedCrossRefGoogle Scholar
  58. 58.
    Griffin MD, Lutz WH, Phan VA, Bachman LA, McKean DJ, Kumar R (2000) Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochem Biophys Res Commun 270(3):701–708. doi: 10.1006/bbrc.2000.2490 PubMedCrossRefGoogle Scholar
  59. 59.
    van Halteren AG, van Etten E, de Jong EC, Bouillon R, Roep BO, Mathieu C (2002) Redirection of human autoreactive T cells upon interaction with dendritic cells modulated by TX527, an analog of 1,25 dihydroxyvitamin D(3). Diabetes 51(7):2119–2125PubMedCrossRefGoogle Scholar
  60. 60.
    Mohr SB, Garland FC, Garland CF, Gorham ED, Ricordi C (2010) Is there a role of vitamin D deficiency in type 1 diabetes of children? Am J Prev Med 39(2):189–190. doi: 10.1016/j.amepre.2010.03.023 PubMedCrossRefGoogle Scholar
  61. 61.
    Hypponen E, Laara E, Reunanen A, Jarvelin MR, Virtanen SM (2001) Intake of vitamin D and risk of type 1 diabetes: a birth-cohort study. Lancet 358(9292):1500–1503. doi: 10.1016/S0140-6736(01)06580-1 PubMedCrossRefGoogle Scholar
  62. 62.
    Fronczak CM, Baron AE, Chase HP, Ross C, Brady HL, Hoffman M, Eisenbarth GS, Rewers M, Norris JM (2003) In utero dietary exposures and risk of islet autoimmunity in children. Diabetes Care 26(12):3237–3242PubMedCrossRefGoogle Scholar
  63. 63.
    The Eurodiab Substudy 2 Study Group (1999) Vitamin D supplement in early childhood and risk for type I (insulin-dependent) diabetes mellitus. Diabetologia 42(1):51–54CrossRefGoogle Scholar
  64. 64.
    Simpson M, Brady H, Yin X, Seifert J, Barriga K, Hoffman M, Bugawan T, Baron AE, Sokol RJ, Eisenbarth G, Erlich H, Rewers M, Norris JM (2011) No association of vitamin D intake or 25-hydroxyvitamin D levels in childhood with risk of islet autoimmunity and type 1 diabetes: the diabetes autoimmunity study in the young (DAISY). Diabetologia 54(11):2779–2788. doi: 10.1007/s00125-011-2278-2 PubMedCrossRefGoogle Scholar
  65. 65.
    Marjamaki L, Niinisto S, Kenward MG, Uusitalo L, Uusitalo U, Ovaskainen ML, Kronberg-Kippila C, Simell O, Veijola R, Ilonen J, Knip M, Virtanen SM (2010) Maternal intake of vitamin D during pregnancy and risk of advanced beta cell autoimmunity and type 1 diabetes in offspring. Diabetologia 53(8):1599–1607. doi: 10.1007/s00125-010-1734-8 PubMedCrossRefGoogle Scholar
  66. 66.
    Lehmann PV, Forsthuber T, Miller A, Sercarz EE (1992) Spreading of T cell autoimmunity to cryptic determinants of an autoantigen. Nature 358(6382):155–157. doi: 10.1038/358155a0 PubMedCrossRefGoogle Scholar
  67. 67.
    Liacopoulos P, Ben-Efraim S (1975) Antigenic competition. Prog Allergy 18:97–204PubMedGoogle Scholar
  68. 68.
    Pross HF, Eidinger D (1974) Antigenic competition: a review of nonspecific antigen-induced suppression. Adv Immunol 18:133–168PubMedCrossRefGoogle Scholar
  69. 69.
    Smith KA, Efstathiou S, Cooke A (2007) Murine gammaherpesvirus-68 infection alters self-antigen presentation and type 1 diabetes onset in NOD mice. J Immunol 179(11):7325–7333 [pii:179/11/7325]PubMedGoogle Scholar
  70. 70.
    Takei I, Asaba Y, Kasatani T, Maruyama T, Watanabe K, Yanagawa T, Saruta T, Ishii T (1992) Suppression of development of diabetes in NOD mice by lactate dehydrogenase virus infection. J Autoimmun 5(6):665–673. doi: 10.1016/0896-8411(92)90184-R PubMedCrossRefGoogle Scholar
  71. 71.
    Diana J, Brezar V, Beaudoin L, Dalod M, Mellor A, Tafuri A, von Herrath M, Boitard C, Mallone R, Lehuen A (2011) Viral infection prevents diabetes by inducing regulatory T cells through NKT cell-plasmacytoid dendritic cell interplay. J Exp Med 208(4):729–745. doi: 10.1084/jem.20101692 PubMedCrossRefGoogle Scholar
  72. 72.
    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(6):1515–1523. doi: 10.1172/JCI3850338503 PubMedGoogle Scholar
  73. 73.
    Menser MA, Forrest JM, Bransby RD (1978) Rubella infection and diabetes mellitus. Lancet 1(8055):57–60PubMedCrossRefGoogle Scholar
  74. 74.
    Rayfield EJ, Kelly KJ, Yoon JW (1986) Rubella virus-induced diabetes in the hamster. Diabetes 35(11):1278–1281PubMedCrossRefGoogle Scholar
  75. 75.
    McEvoy RC, Fedun B, Cooper LZ, Thomas NM, Rodriguez de Cordoba S, Rubinstein P, Ginsberg-Fellner F (1988) Children at high risk of diabetes mellitus: New York studies of families with diabetes and of children with congenital rubella syndrome. Adv Exp Med Biol 246:221–227PubMedCrossRefGoogle Scholar
  76. 76.
    Ou D, Mitchell LA, Metzger DL, Gillam S, Tingle AJ (2000) Cross-reactive rubella virus and glutamic acid decarboxylase (65 and 67) protein determinants recognised by T cells of patients with type I diabetes mellitus. Diabetologia 43(6):750–762. doi: 10.1007/s001250051373 PubMedCrossRefGoogle Scholar
  77. 77.
    Gale EA (2008) Congenital rubella: citation virus or viral cause of type 1 diabetes? Diabetologia 51(9):1559–1566. doi: 10.1007/s00125-008-1099-4 PubMedCrossRefGoogle Scholar
  78. 78.
    Lindberg B, Ahlfors K, Carlsson A, Ericsson UB, Landin-Olsson M, Lernmark A, Ludvigsson J, Sundkvist G, Ivarsson SA (1999) Previous exposure to measles, mumps, and rubella—but not vaccination during adolescence—correlates to the prevalence of pancreatic and thyroid autoantibodies. Pediatrics 104(1):e12PubMedCrossRefGoogle Scholar
  79. 79.
    Hyoty H, Hiltunen M, Reunanen A, Leinikki P, Vesikari T, Lounamaa R, Tuomilehto J, Akerblom HK (1993) Decline of mumps antibodies in type 1 (insulin-dependent) diabetic children and a plateau in the rising incidence of type 1 diabetes after introduction of the mumps–measles–rubella vaccine in Finland. Childhood Diabetes in Finland Study Group. Diabetologia 36(12):1303–1308PubMedCrossRefGoogle Scholar
  80. 80.
    Honeyman MC, Coulson BS, Stone NL, Gellert SA, Goldwater PN, Steele CE, Couper JJ, Tait BD, Colman PG, Harrison LC (2000) Association between rotavirus infection and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes 49(8):1319–1324PubMedCrossRefGoogle Scholar
  81. 81.
    Coulson BS, Witterick PD, Tan Y, Hewish MJ, Mountford JN, Harrison LC, Honeyman MC (2002) Growth of rotaviruses in primary pancreatic cells. J Virol 76(18):9537–9544PubMedCrossRefGoogle Scholar
  82. 82.
    Honeyman MC, Stone NL, Falk BA, Nepom G, Harrison LC (2010) Evidence for molecular mimicry between human T cell epitopes in rotavirus and pancreatic islet autoantigens. J Immunol 184(4):2204–2210. doi: 10.4049/jimmunol.0900709 PubMedCrossRefGoogle Scholar
  83. 83.
    Blomqvist M, Juhela S, Erkkila S, Korhonen S, Simell T, Kupila A, Vaarala O, Simell O, Knip M, Ilonen J (2002) Rotavirus infections and development of diabetes-associated autoantibodies during the first 2 years of life. Clin Exp Immunol 128(3):511–515 [pii:1842]PubMedCrossRefGoogle Scholar
  84. 84.
    Graham KL, O’Donnell JA, Tan Y, Sanders N, Carrington EM, Allison J, Coulson BS (2007) Rotavirus infection of infant and young adult nonobese diabetic mice involves extraintestinal spread and delays diabetes onset. J Virol 81(12):6446–6458. doi: 10.1128/JVI.00205-07 PubMedCrossRefGoogle Scholar
  85. 85.
    Pak CY, Eun HM, McArthur RG, Yoon JW (1988) Association of cytomegalovirus infection with autoimmune type 1 diabetes. Lancet 2(8601):1–4PubMedCrossRefGoogle Scholar
  86. 86.
    Roep BO, Hiemstra HS, Schloot NC, De Vries RR, Chaudhuri A, Behan PO, Drijfhout JW (2002) Molecular mimicry in type 1 diabetes: immune cross-reactivity between islet autoantigen and human cytomegalovirus but not coxsackie virus. Ann NY Acad Sci 958:163–165PubMedCrossRefGoogle Scholar
  87. 87.
    Ivarsson SA, Lindberg B, Nilsson KO, Ahlfors K, Svanberg L (1993) The prevalence of type 1 diabetes mellitus at follow-up of Swedish infants congenitally infected with cytomegalovirus. Diabet Med 10(6):521–523PubMedCrossRefGoogle Scholar
  88. 88.
    Hiltunen M, Hyoty H, Karjalainen J, Leinikki P, Knip M, Lounamaa R, Akerblom HK (1995) Serological evaluation of the role of cytomegalovirus in the pathogenesis of IDDM: a prospective study. The Childhood Diabetes in Finland Study Group. Diabetologia 38(6):705–710PubMedCrossRefGoogle Scholar
  89. 89.
    Aarnisalo J, Veijola R, Vainionpaa R, Simell O, Knip M, Ilonen J (2008) Cytomegalovirus infection in early infancy: risk of induction and progression of autoimmunity associated with type 1 diabetes. Diabetologia 51(5):769–772. doi: 10.1007/s00125-008-0945-8 PubMedCrossRefGoogle Scholar
  90. 90.
    Tirabassi RS, Guberski DL, Blankenhorn EP, Leif JH, Woda BA, Liu Z, Winans D, Greiner DL, Mordes JP (2010) Infection with viruses from several families triggers autoimmune diabetes in LEW*1WR1 rats: prevention of diabetes by maternal immunization. Diabetes 59(1):110–118. doi: 10.2337/db09-0255 PubMedCrossRefGoogle Scholar
  91. 91.
    Hillebrands JL, van der Werf N, Klatter FA, Bruggeman CA, Rozing J (2003) Role of peritoneal macrophages in cytomegalovirus-induced acceleration of autoimmune diabetes in BB-rats. Clin Dev Immunol 10(2–4):133–139PubMedCrossRefGoogle Scholar
  92. 92.
    Smelt MJ, Faas MM, de Haan BJ, Draijer C, Hugenholtz GC, de Haan A, Engelse MA, de Koning EJ, de Vos P (2012) Susceptibility of human pancreatic beta cells for cytomegalovirus infection and the effects on cellular immunogenicity. Pancreas 41(1):39–49. doi: 10.1097/MPA.0b013e31821fc90c PubMedCrossRefGoogle Scholar
  93. 93.
    Hirasawa K, Jun HS, Maeda K, Kawaguchi Y, Itagaki S, Mikami T, Baek HS, Doi K, Yoon JW (1997) Possible role of macrophage-derived soluble mediators in the pathogenesis of encephalomyocarditis virus-induced diabetes in mice. J Virol 71(5):4024–4031PubMedGoogle Scholar
  94. 94.
    Chung YH, Jun HS, Son M, Bao M, Bae HY, Kang Y, Yoon JW (2000) Cellular and molecular mechanism for Kilham rat virus-induced autoimmune diabetes in DR-BB rats. J Immunol 165(5):2866–2876 [pii:ji_v165n5p2866]PubMedGoogle Scholar
  95. 95.
    Zipris D, Lien E, Nair A, Xie JX, Greiner DL, Mordes JP, Rossini AA (2007) TLR9-signaling pathways are involved in Kilham rat virus-induced autoimmune diabetes in the biobreeding diabetes-resistant rat. J Immunol 178(2):693–701 [pii:178/2/693]PubMedGoogle Scholar
  96. 96.
    Harada M, Kishimoto Y, Makino S (1990) Prevention of overt diabetes and insulitis in NOD mice by a single BCG vaccination. Diabetes Res Clin Pract 8(2):85–89PubMedCrossRefGoogle Scholar
  97. 97.
    Niu X, Zhou Z, Jiang T, Su H (2002) The effects of complete Freund’s adjuvant on prevention of pancrentitis and diabetes mellitus in non-obese diabetic mice. Zhonghua Nei Ke Za Zhi 41(4):229–232PubMedGoogle Scholar
  98. 98.
    Liddi R, Beales PE, Rosignoli G, Pozzilli P (2000) Incomplete Freund’s adjuvant reduces diabetes in the non-obese diabetic mouse. Horm Metab Res 32(6):201–206. doi: 10.1055/s-2007-978622 PubMedCrossRefGoogle Scholar
  99. 99.
    Dyrberg T, Schwimmbeck P, Oldstone M (1988) The incidence of diabetes in BB rats is decreased following acute LCMV infection. Adv Exp Med Biol 246:397–402PubMedCrossRefGoogle Scholar
  100. 100.
    Oldstone MB (1988) Prevention of type I diabetes in nonobese diabetic mice by virus infection. Science 239(4839):500–502PubMedCrossRefGoogle Scholar
  101. 101.
    Christen U, Benke D, Wolfe T, Rodrigo E, Rhode A, Hughes AC, Oldstone MB, von Herrath MG (2004) Cure of prediabetic mice by viral infections involves lymphocyte recruitment along an IP-10 gradient. J Clin Invest 113(1):74–84. doi: 10.1172/JCI17005 PubMedGoogle Scholar
  102. 102.
    Novak J, Griseri T, Beaudoin L, Lehuen A (2007) Regulation of type 1 diabetes by NKT cells. Int Rev Immunol 26(1–2):49–72. doi: 10.1080/08830180601070229 PubMedCrossRefGoogle Scholar
  103. 103.
    Beaudoin L, Laloux V, Novak J, Lucas B, Lehuen A (2002) NKT cells inhibit the onset of diabetes by impairing the development of pathogenic T cells specific for pancreatic beta cells. Immunity 17(6):725–736 [pii:S1074761302004739]PubMedCrossRefGoogle Scholar
  104. 104.
    Laloux V, Beaudoin L, Jeske D, Carnaud C, Lehuen A (2001) NK T cell-induced protection against diabetes in V alpha 14-J alpha 281 transgenic nonobese diabetic mice is associated with a Th2 shift circumscribed regionally to the islets and functionally to islet autoantigen. J Immunol 166(6):3749–3756PubMedGoogle Scholar
  105. 105.
    Diana J, Griseri T, Lagaye S, Beaudoin L, Autrusseau E, Gautron AS, Tomkiewicz C, Herbelin A, Barouki R, von Herrath M, Dalod M, Lehuen A (2009) NKT cell-plasmacytoid dendritic cell cooperation via OX40 controls viral infection in a tissue-specific manner. Immunity 30(2):289–299. doi: 10.1016/j.immuni.2008.12.017 PubMedCrossRefGoogle Scholar
  106. 106.
    Wetzel JD, Barton ES, Chappell JD, Baer GS, Mochow-Grundy M, Rodgers SE, Shyr Y, Powers AC, Thomas JW, Dermody TS (2006) Reovirus delays diabetes onset but does not prevent insulitis in nonobese diabetic mice. J Virol 80(6):3078–3082. doi: 10.1128/JVI.80.6.3078-3082.2006 PubMedCrossRefGoogle Scholar
  107. 107.
    Wilberz S, Partke HJ, Dagnaes-Hansen F, Herberg L (1991) Persistent MHV (mouse hepatitis virus) infection reduces the incidence of diabetes mellitus in non-obese diabetic mice. Diabetologia 34(1):2–5PubMedCrossRefGoogle Scholar
  108. 108.
    Cook-Mills JM, Munshi HG, Perlman RL, Chambers DA (1992) Mouse hepatitis virus infection suppresses modulation of mouse spleen T cell activation. Immunology 75(3):542–545PubMedGoogle Scholar
  109. 109.
    de Souza MS, Smith AL (1991) Characterization of accessory cell function during acute infection of BALB/cByJ mice with mouse hepatitis virus (MHV), strain JHM. Lab Anim Sci 41(2):112–118PubMedGoogle Scholar
  110. 110.
    Viskari HR, Koskela P, Lonnrot M, Luonuansuu S, Reunanen A, Baer M, Hyoty H (2000) Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 23(3):414–416PubMedCrossRefGoogle Scholar
  111. 111.
    Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R, Soltesz G, Fuchtenbusch M, Ziegler AG, Kondrashova A, Romanov A, Kaplan B, Laron Z, Koskela P, Vesikari T, Huhtala H, Knip M, Hyoty H (2005) Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation. Diabetologia 48(7):1280–1287. doi: 10.1007/s00125-005-1780-9 PubMedCrossRefGoogle Scholar
  112. 112.
    Gamble DR, Kinsley ML, FitzGerald MG, Bolton R, Taylor KW (1969) Viral antibodies in diabetes mellitus. Br Med J 3(5671):627–630PubMedCrossRefGoogle Scholar
  113. 113.
    Gamble DR, Taylor KW (1969) Seasonal incidence of diabetes mellitus. Br Med J 3(5671):631–633PubMedCrossRefGoogle Scholar
  114. 114.
    Hierholzer JC, Farris WA (1974) Follow-up of children infected in a coxsackievirus B-3 and B-4 outbreak: no evidence of diabetes mellitus. J Infect Dis 129(6):741–746PubMedCrossRefGoogle Scholar
  115. 115.
    Fuchtenbusch M, Irnstetter A, Jager G, Ziegler AG (2001) No evidence for an association of coxsackie virus infections during pregnancy and early childhood with development of islet autoantibodies in offspring of mothers or fathers with type 1 diabetes. J Autoimmun 17(4):333–340. doi: 10.1006/jaut.2001.0550 PubMedCrossRefGoogle Scholar
  116. 116.
    Yeung WC, Rawlinson WD, Craig ME (2011) Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342:d35. doi: 10.1136/bmj.d35 PubMedCrossRefGoogle Scholar
  117. 117.
    Hyoty H, Hiltunen M, Knip M, Laakkonen M, Vahasalo P, Karjalainen J, Koskela P, Roivainen M, Leinikki P, Hovi T et al (1995) A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. Childhood Diabetes in Finland (DiMe) Study Group. Diabetes 44(6):652–657PubMedCrossRefGoogle Scholar
  118. 118.
    Lonnrot M, Korpela K, Knip M, Ilonen J, Simell O, Korhonen S, Savola K, Muona P, Simell T, Koskela P, Hyoty H (2000) Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study. Diabetes 49(8):1314–1318PubMedCrossRefGoogle Scholar
  119. 119.
    Sadeharju K, Hamalainen AM, Knip M, Lonnrot M, Koskela P, Virtanen SM, Ilonen J, Akerblom HK, Hyoty H (2003) Enterovirus infections as a risk factor for type I diabetes: virus analyses in a dietary intervention trial. Clin Exp Immunol 132(2):271–277 [pii:2147]PubMedCrossRefGoogle Scholar
  120. 120.
    Stene LC, Oikarinen S, Hyoty H, Barriga KJ, Norris JM, Klingensmith G, Hutton JC, Erlich HA, Eisenbarth GS, Rewers M (2010) Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: the diabetes and autoimmunity study in the young (DAISY). Diabetes 59(12):3174–3180. doi: 10.2337/db10-0866 PubMedCrossRefGoogle Scholar
  121. 121.
    Sarmiento L, Cabrera-Rode E, Lekuleni L, Cuba I, Molina G, Fonseca M, Heng-Hung L, Borroto AD, Gonzalez P, Mas-Lago P, Diaz-Horta O (2007) Occurrence of enterovirus RNA in serum of children with newly diagnosed type 1 diabetes and islet cell autoantibody-positive subjects in a population with a low incidence of type 1 diabetes. Autoimmunity 40(7):540–545. doi: 10.1080/08916930701523429 PubMedCrossRefGoogle Scholar
  122. 122.
    Nairn C, Galbraith DN, Taylor KW, Clements GB (1999) Enterovirus variants in the serum of children at the onset of type 1 diabetes mellitus. Diabet Med 16(6):509–513PubMedCrossRefGoogle Scholar
  123. 123.
    Schulte BM, Bakkers J, Lanke KH, Melchers WJ, Westerlaken C, Allebes W, Aanstoot HJ, Bruining GJ, Adema GJ, Van Kuppeveld FJ, Galama JM (2010) Detection of enterovirus RNA in peripheral blood mononuclear cells of type 1 diabetic patients beyond the stage of acute infection. Viral Immunol 23(1):99–104. doi: 10.1089/vim.2009.0072 PubMedCrossRefGoogle Scholar
  124. 124.
    Frisk G, Tuvemo T (2004) Enterovirus infections with beta-cell tropic strains are frequent in siblings of children diagnosed with type 1 diabetes children and in association with elevated levels of GAD65 antibodies. J Med Virol 73(3):450–459. doi: 10.1002/jmv.20111 PubMedCrossRefGoogle Scholar
  125. 125.
    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(21):1173–1179. doi: 10.1056/NEJM197905243002102 PubMedCrossRefGoogle Scholar
  126. 126.
    Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P (2007) Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA 104(12):5115–5120. doi: 10.1073/pnas.0700442104 PubMedCrossRefGoogle Scholar
  127. 127.
    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(6):1143–1151. doi: 10.1007/s00125-009-1276-0 PubMedCrossRefGoogle Scholar
  128. 128.
    Ylipaasto P, Klingel K, Lindberg AM, Otonkoski T, Kandolf R, Hovi T, Roivainen M (2004) Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47(2):225–239. doi: 10.1007/s00125-003-1297-z PubMedCrossRefGoogle Scholar
  129. 129.
    Foulis AK, Farquharson MA, Meager A (1987) Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus. Lancet 2(8573):1423–1427PubMedCrossRefGoogle Scholar
  130. 130.
    Huang X, Yuang J, Goddard A, Foulis A, James RF, Lernmark A, Pujol-Borrell R, Rabinovitch A, Somoza N, Stewart TA (1995) Interferon expression in the pancreases of patients with type I diabetes. Diabetes 44(6):658–664PubMedCrossRefGoogle Scholar
  131. 131.
    Otonkoski T, Roivainen M, Vaarala O, Dinesen B, Leipala JA, Hovi T, Knip M (2000) Neonatal type I diabetes associated with maternal echovirus six infection: a case report. Diabetologia 43(10):1235–1238. doi: 10.1007/s001250051518 PubMedCrossRefGoogle Scholar
  132. 132.
    Vreugdenhil GR, Schloot NC, Hoorens A, Rongen C, Pipeleers DG, Melchers WJ, Roep BO, Galama JM (2000) Acute onset of type I diabetes mellitus after severe echovirus nine infection: putative pathogenic pathways. Clin Infect Dis 31(4):1025–1031. doi: 10.1086/318159 PubMedCrossRefGoogle Scholar
  133. 133.
    Diaz-Horta O, Bello M, Cabrera-Rode E, Suarez J, Mas P, Garcia I, Abalos I, Jofra R, Molina G, Diaz–Diaz O, Dimario U (2001) Echovirus four and type 1 diabetes mellitus. Autoimmunity 34(4):275–281PubMedCrossRefGoogle Scholar
  134. 134.
    Cabrera-Rode E, Sarmiento L, Molina G, Perez C, Arranz C, Galvan JA, Prieto M, Barrios J, Palomera R, Fonseca M, Mas P, Diaz–Diaz O, Diaz-Horta O (2005) Islet cell related antibodies and type 1 diabetes associated with echovirus 30 epidemic: a case report. J Med Virol 76(3):373–377. doi: 10.1002/jmv.20368 PubMedCrossRefGoogle Scholar
  135. 135.
    Paananen A, Savolainen-Kopra C, Kaijalainen S, Vaarala O, Hovi T, Roivainen M (2007) Genetic and phenotypic diversity of echovirus 30 strains and pathogenesis of type 1 diabetes. J Med Virol 79(7):945–955. doi: 10.1002/jmv.20922 PubMedCrossRefGoogle Scholar
  136. 136.
    Cabrera-Rode E, Sarmiento L, Tiberti C, Molina G, Barrios J, Hernandez D, Diaz-Horta O, Di Mario U (2003) Type 1 diabetes islet associated antibodies in subjects infected by echovirus 16. Diabetologia 46(10):1348–1353. doi: 10.1007/s00125-003-1179-4 PubMedCrossRefGoogle Scholar
  137. 137.
    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(5):693–702. doi: 10.1007/s00125-002-0805-x PubMedCrossRefGoogle Scholar
  138. 138.
    Atkinson MA, Bowman MA, Campbell L, Darrow BL, Kaufman DL, Maclaren NK (1994) Cellular immunity to a determinant common to glutamate decarboxylase and coxsackie virus in insulin-dependent diabetes. J Clin Invest 94(5):2125–2129. doi: 10.1172/JCI117567 PubMedCrossRefGoogle Scholar
  139. 139.
    Schloot NC, Willemen SJ, Duinkerken G, Drijfhout JW, de Vries RR, Roep BO (2001) Molecular mimicry in type 1 diabetes mellitus revisited: T cell clones to GAD65 peptides with sequence homology to Coxsackie or proinsulin peptides do not crossreact with homologous counterpart. Hum Immunol 62(4):299–309 [pii:S0198-8859(01)00223-3]PubMedCrossRefGoogle Scholar
  140. 140.
    Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N (1998) Diabetes induced by coxsackievirus: initiation by bystander damage and not molecular mimicry. Nat Med 4(7):781–785PubMedCrossRefGoogle Scholar
  141. 141.
    Tracy S, Drescher KM, Chapman NM, Kim KS, Carson SD, Pirruccello S, Lane PH, Romero JR, Leser JS (2002) Toward testing the hypothesis that group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic mice with CVB markedly lowers diabetes incidence. J Virol 76(23):12097–12111PubMedCrossRefGoogle Scholar
  142. 142.
    Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA (2000) Acceleration of type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T cells in pancreatic islets. Diabetes 49(5):708–711PubMedCrossRefGoogle Scholar
  143. 143.
    Horwitz MS, Fine C, Ilic A, Sarvetnick N (2001) Requirements for viral-mediated autoimmune diabetes: beta-cell damage and immune infiltration. J Autoimmun 16(3):211–217. doi: 10.1006/jaut.2000.0486 PubMedCrossRefGoogle Scholar
  144. 144.
    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(11):5637–5643. doi: 10.1128/JVI.02361-05 PubMedCrossRefGoogle Scholar
  145. 145.
    Szopa TM, Gamble DR, Taylor KW (1986) Coxsackie B4 virus induces short-term changes in the metabolic functions of mouse pancreatic islets in vitro. Cell Biochem Funct 4(3):181–187. doi: 10.1002/cbf.290040304 PubMedCrossRefGoogle Scholar
  146. 146.
    Roivainen M, Rasilainen S, Ylipaasto P, Nissinen R, Ustinov J, Bouwens L, Eizirik DL, Hovi T, Otonkoski T (2000) Mechanisms of coxsackievirus-induced damage to human pancreatic beta-cells. J Clin Endocrinol Metab 85(1):432–440PubMedCrossRefGoogle Scholar
  147. 147.
    Flodstrom M, Horwitz MS, Maday A, Balakrishna D, Rodriguez E, Sarvetnick N (2001) A critical role for inducible nitric oxide synthase in host survival following coxsackievirus B4 infection. Virology 281(2):205–215. doi: 10.1006/viro.2000.0801 PubMedCrossRefGoogle Scholar
  148. 148.
    Bergelson JM, Krithivas A, Celi L, Droguett G, Horwitz MS, Wickham T, Crowell RL, Finberg RW (1998) The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. J Virol 72(1):415–419PubMedGoogle Scholar
  149. 149.
    Mena I, Fischer C, Gebhard JR, Perry CM, Harkins S, Whitton JL (2000) Coxsackievirus infection of the pancreas: evaluation of receptor expression, pathogenesis, and immunopathology. Virology 271(2):276–288. doi: 10.1006/viro.2000.0332 PubMedCrossRefGoogle Scholar
  150. 150.
    Yap IS, Giddings G, Pocock E, Chantler JK (2003) Lack of islet neogenesis plays a key role in beta-cell depletion in mice infected with a diabetogenic variant of coxsackievirus B4. J Gen Virol 84(Pt 11):3051–3068PubMedCrossRefGoogle Scholar
  151. 151.
    Horwitz MS, Ilic A, Fine C, Balasa B, Sarvetnick N (2004) Coxsackieviral-mediated diabetes: induction requires antigen-presenting cells and is accompanied by phagocytosis of beta cells. Clin Immunol 110(2):134–144. doi: 10.1016/j.clim.2003.09.014 PubMedCrossRefGoogle Scholar
  152. 152.
    Drescher KM, Kono K, Bopegamage S, Carson SD, Tracy S (2004) Coxsackievirus B3 infection and type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection. Virology 329(2):381–394. doi: 10.1016/j.virol.2004.06.049 PubMedCrossRefGoogle Scholar
  153. 153.
    Horwitz MS, Krahl T, Fine C, Lee J, Sarvetnick N (1999) Protection from lethal coxsackievirus-induced pancreatitis by expression of gamma interferon. J Virol 73(3):1756–1766PubMedGoogle Scholar
  154. 154.
    Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N (2002) Target cell defense prevents the development of diabetes after viral infection. Nat Immunol 3(4):373–382. doi: 10.1038/ni771 PubMedCrossRefGoogle Scholar
  155. 155.
    Flodstrom-Tullberg M, Hultcrantz M, Stotland A, Maday A, Tsai D, Fine C, Williams B, Silverman R, Sarvetnick N (2005) RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J Immunol 174(3):1171–1177 [pii:174/3/1171]PubMedGoogle Scholar
  156. 156.
    In’t Veld P (2011) Insulitis in the human endocrine pancreas: does a viral infection lead to inflammation and beta cell replication? Diabetologia. doi: 10.1007/s00125-011-2224-3 PubMedGoogle Scholar
  157. 157.
    Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R, Soltesz G, Fuchtenbusch M, Ziegler AG, Kondrashova A, Romanov A, Knip M, Hyoty H (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(4):610–617. doi: 10.1002/jmv.20033 PubMedCrossRefGoogle Scholar
  158. 158.
    Sadeharju K, Knip M, Virtanen SM, Savilahti E, Tauriainen S, Koskela P, Akerblom HK, Hyoty H (2007) Maternal antibodies in breast milk protect the child from enterovirus infections. Pediatrics 119(5):941–946. doi: 10.1542/peds.2006-0780 PubMedCrossRefGoogle Scholar
  159. 159.
    Nathanson N, Kew OM (2010) From emergence to eradication: the epidemiology of poliomyelitis deconstructed. Am J Epidemiol 172(11):1213–1229. doi: 10.1093/aje/kwq320 PubMedCrossRefGoogle Scholar
  160. 160.
    Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441(7089):101–105. doi: 10.1038/nature04734 PubMedCrossRefGoogle Scholar
  161. 161.
    Nejentsev S, Walker N, Riches D, Egholm M, Todd JA (2009) Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324(5925):387–389. doi: 10.1126/science.1167728 PubMedCrossRefGoogle Scholar
  162. 162.
    Shigemoto T, Kageyama M, Hirai R, Zheng J, Yoneyama M, Fujita T (2009) Identification of loss of function mutations in human genes encoding RIG-I and MDA5: implications for resistance to type I diabetes. J Biol Chem 284(20):13348–13354. doi: 10.1074/jbc.M809449200 PubMedCrossRefGoogle Scholar
  163. 163.
    Smyth DJ, Cooper JD, Bailey R, Field S, Burren O, Smink LJ, Guja C, Ionescu-Tirgoviste C, Widmer B, Dunger DB, Savage DA, Walker NM, Clayton DG, Todd JA (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(6):617–619. doi: 10.1038/ng1800 PubMedCrossRefGoogle Scholar
  164. 164.
    Chehadeh W, Weill J, Vantyghem MC, Alm G, Lefebvre J, Wattre P, Hober D (2000) Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J Infect Dis 181(6):1929–1939. doi: 10.1086/315516 PubMedCrossRefGoogle Scholar
  165. 165.
    Alba A, Puertas MC, Carrillo J, Planas R, Ampudia R, Pastor X, Bosch F, Pujol-Borrell R, Verdaguer J, Vives-Pi M (2004) IFN beta accelerates autoimmune type 1 diabetes in nonobese diabetic mice and breaks the tolerance to beta-cells in nondiabetes-prone mice. J Immunol 173(11):6667–6675 [pii:173/11/6667]PubMedGoogle Scholar
  166. 166.
    Li Q, Xu B, Michie SA, Rubins KH, Schreriber RD, McDevitt HO (2008) Interferon-alpha initiates type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci USA 105(34):12439–12444. doi: 10.1073/pnas.0806439105 PubMedCrossRefGoogle Scholar
  167. 167.
    Li Q, McDevitt HO (2011) The role of interferon alpha in initiation of type I diabetes in the NOD mouse. Clin Immunol 140(1):3–7. doi: 10.1016/j.clim.2011.04.010 PubMedCrossRefGoogle Scholar
  168. 168.
    Cooper JD, Walker NM, Smyth DJ, Downes K, Healy BC, Todd JA (2009) Follow-up of 1715 SNPs from the Wellcome Trust Case Control Consortium genome-wide association study in type I diabetes families. Genes Immun 10(Suppl 1):S85–S94. doi: 10.1038/gene.2009.97 PubMedCrossRefGoogle Scholar
  169. 169.
    Wang JP, Asher DR, Chan M, Kurt-Jones EA, Finberg RW (2007) Cutting edge: antibody-mediated TLR7-dependent recognition of viral RNA. J Immunol 178(6):3363–3367 [pii:178/6/3363]PubMedGoogle Scholar
  170. 170.
    Lee AS, Ghoreishi M, Cheng WK, Chang TY, Zhang YQ, Dutz JP (2011) Toll-like receptor 7 stimulation promotes autoimmune diabetes in the NOD mouse. Diabetologia 54(6):1407–1416. doi: 10.1007/s00125-011-2083-y PubMedCrossRefGoogle Scholar
  171. 171.
    Colonna M (2006) Toll-like receptors and IFN-alpha: partners in autoimmunity. J Clin Invest 116(9):2319–2322. doi: 10.1172/JCI29879 PubMedCrossRefGoogle Scholar
  172. 172.
    McCartney SA, Vermi W, Lonardi S, Rossini C, Otero K, Calderon B, Gilfillan S, Diamond MS, Unanue ER, Colonna M (2011) RNA sensor-induced type I IFN prevents diabetes caused by a beta cell-tropic virus in mice. J Clin Invest 121(4):1497–1507. doi: 10.1172/JCI44005 PubMedCrossRefGoogle Scholar
  173. 173.
    Via CS, Nguyen P, Niculescu F, Papadimitriou J, Hoover D, Silbergeld EK (2003) Low-dose exposure to inorganic mercury accelerates disease and mortality in acquired murine lupus. Environ Health Perspect 111(10):1273–1277PubMedCrossRefGoogle Scholar
  174. 174.
    Havarinasab S, Hultman P (2006) Alteration of the spontaneous systemic autoimmune disease in (NZB × NZW)F1 mice by treatment with thimerosal (ethyl mercury). Toxicol Appl Pharmacol 214(1):43–54. doi: 10.1016/j.taap.2005.12.004 PubMedCrossRefGoogle Scholar
  175. 175.
    Leffel EK, Wolf C, Poklis A, White KL Jr (2003) Drinking water exposure to cadmium, an environmental contaminant, results in the exacerbation of autoimmune disease in the murine model. Toxicology 188(2–3):233–250 [pii:S0300483X03000921]PubMedCrossRefGoogle Scholar
  176. 176.
    Rahman M, Tondel M, Ahmad SA, Axelson O (1998) Diabetes mellitus associated with arsenic exposure in Bangladesh. Am J Epidemiol 148(2):198–203PubMedCrossRefGoogle Scholar
  177. 177.
    Lai MS, Hsueh YM, Chen CJ, Shyu MP, Chen SY, Kuo TL, Wu MM, Tai TY (1994) Ingested inorganic arsenic and prevalence of diabetes mellitus. Am J Epidemiol 139(5):484–492PubMedGoogle Scholar
  178. 178.
    Kolachi NF, Kazi TG, Afridi HI, Kazi N, Khan S, Kandhro GA, Shah AQ, Baig JA, Wadhwa SK, Shah F, Jamali MK, Arain MB (2011) Status of toxic metals in biological samples of diabetic mothers and their neonates. Biol Trace Elem Res 143(1):196–212. doi: 10.1007/s12011-010-8879-7 PubMedCrossRefGoogle Scholar
  179. 179.
    Chen YW, Huang CF, Tsai KS, Yang RS, Yen CC, Yang CY, Lin-Shiau SY, Liu SH (2006) Methylmercury induces pancreatic beta-cell apoptosis and dysfunction. Chem Res Toxicol 19(8):1080–1085. doi: 10.1021/tx0600705 PubMedCrossRefGoogle Scholar
  180. 180.
    Chen YW, Huang CF, Tsai KS, Yang RS, Yen CC, Yang CY, Lin-Shiau SY, Liu SH (2006) The role of phosphoinositide 3-kinase/Akt signaling in low-dose mercury-induced mouse pancreatic beta-cell dysfunction in vitro and in vivo. Diabetes 55(6):1614–1624. doi: 10.2337/db06-0029 PubMedCrossRefGoogle Scholar
  181. 181.
    Chen Y, Ahsan H, Slavkovich V, Peltier GL, Gluskin RT, Parvez F, Liu X, Graziano JH (2010) No association between arsenic exposure from drinking water and diabetes mellitus: a cross-sectional study in Bangladesh. Environ Health Perspect 118(9):1299–1305. doi: 10.1289/ehp.0901559 PubMedCrossRefGoogle Scholar
  182. 182.
    Steinmaus C, Yuan Y, Liaw J, Smith AH (2009) Low-level population exposure to inorganic arsenic in the United States and diabetes mellitus: a reanalysis. Epidemiology 20(6):807–815. doi: 10.1097/EDE.0b013e3181b0fd29 PubMedCrossRefGoogle Scholar
  183. 183.
    Brenden N, Rabbani H, Abedi-Valugerdi M (2001) Analysis of mercury-induced immune activation in nonobese diabetic (NOD) mice. Clin Exp Immunol 125(2):202–210 [pii:cei1580]PubMedCrossRefGoogle Scholar
  184. 184.
    Abedi-Valugerdi M, Nilsson C, Zargari A, Gharibdoost F, DePierre JW, Hassan M (2005) Bacterial lipopolysaccharide both renders resistant mice susceptible to mercury-induced autoimmunity and exacerbates such autoimmunity in susceptible mice. Clin Exp Immunol 141(2):238–247. doi: 10.1111/j.1365-2249.2005.02849.x PubMedCrossRefGoogle Scholar
  185. 185.
    Funseth E, Wicklund-Glynn A, Friman G, Ilback N (2000) Redistribution of accumulated 2,3,7,8-tetrachlorodibenzo-p-dioxin during coxsackievirus B3 infection in the mouse. Toxicol Lett 116(1–2):131–141 [pii:S0378427400002174]PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2012

Authors and Affiliations

  1. 1.Hôpital Saint Vincent de Paul/CochinParisFrance

Personalised recommendations