Do viral infections protect from or enhance type 1 diabetes and how can we tell the difference?

Cellular and Molecular Immunology

Volumn 8, Issue 3, 2011, Pages 193-198

  Christen, Urs ^a   Von Herrath, Matthias G ^b  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

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

Author keywords

animal model; enterovirus; hygiene hypothesis; molecular mimicry; pathogens

Indexed keywords

DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; EPIDEMIOLOGICAL DATA; GENETIC PREDISPOSITION; HUMAN; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; REVIEW; RISK FACTOR; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS REPLICATION;

ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; ENVIRONMENTAL EXPOSURE; EPITOPES, T-LYMPHOCYTE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MOLECULAR MIMICRY; VIRUS DISEASES; VIRUS REPLICATION;

ANIMALIA; ENTEROVIRUS;

EID: 79955670895     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2010.71     Document Type: Review

References (66)

1. Todd JA. Etiology of type 1 diabetes. Immunity 2010; 32: 457-467.
2. Ziegler AG, Nepom GT. Prediction and pathogenesis in type 1 diabetes. Immunity 2010; 32: 468-478.
3. Redondo MJ, Rewers M, Yu L, Garg S, Pilcher CC, Elliott RB et al. Genetic determination of islet cell autoimmunity in monozygotic twin, dizygotic twin, and non-twin siblings of patients with type 1 diabetes: prospective twin study. BMJ 1999; 318: 698-702. (Pubitemid 29191993)
4. Bonifacio E, Hummel M, Walter M, Schmid S, Ziegler AG. IDDM1 and multiplefamily historyoftype 1 diabetescombineto identifyneonatesat high riskfortype 1 diabetes. Diabetes Care 2004; 27: 2695-700.
5. Christen U, Benke D, Wolfe T, Rodrigo E, Rhode A, Hughes AC et al. Cure of prediabetic mice byviral infections involves lymphocyte recruitment along an IP-10 gradient. JClin Invest 2004; 113: 74-84. (Pubitemid 38541634)
6. Filippi CM, Estes EA, Oldham JE, von Herrath MG. Immunoregulatory mechanisms triggered byviral infections protect from type 1 diabetes in mice. J Clin Invest 2009; 119:1515-1523.
7. Ehlers S, Kaufmann SH. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: lifestyle changes affecting the host-environment interface. Clin Exp Immunol 2010; 160: 10-14.
8. Filippi CM, von Herrath MG. 99th Dahlem conferenceon infection, inflammationand chronic inflammatorydisorders: viruses, autoimmunity and immunoregulation. Clin Exp Immunol 2010; 160: 113-119.
9. Chatenoud L, You S, Okada H, Kuhn C, Michaud B, Bach JF. 99th Dahlemconference on infection, inflammation and chronic inflammatorydisorders: immunetherapiesof type 1 diabetes: new opportunities based on the hygiene hypothesis. Clin Exp Immunol 2010; 160: 106-112.
10. Gamble DR, Kinsley ML, Fitz Gerald MG, Bolton R, Taylor KW. Viral antibodies in diabetes mellitus. Br Med J 1969; 3: 627-630.
11. Al-Hello H, Paananen A, Eskelinen M, Ylipaasto P, Hovi T, Salmela K et al. An enterovirus strain isolated from diabetic child belongs to a genetic subcluster of echovirus 11, but is also neutralised with monotypic antisera to coxsackievirus A9. J Gen Virol 2008; 89: 1949-1959.
12. Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S et al. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA2007; 104: 5115-5120. (Pubitemid 47186185)
13. Yoon JW, Austin M, Onodera T, Notkins AL. Virus-induceddiabetesmellitus: isolation of avirusfromthepancreasof a child withdiabetic ketoacidosis. NEngl JMed 1979; 300:1173-1179. (Pubitemid 9191515)
14. Honeyman MC, Coulson BS, Stone NL, Gellert SA, Goldwater PN, Steele CE et al. Associationbetweenrotavirus infectionand pancreatic isletautoimmunity inchildren at risk of developingtype 1 diabetes. Diabetes 2000; 49: 1319-1324.
15. Hyoty H, Leinikki P, Reunanen A, Ilonen J, Surcel HM, Rilva A et al. Mumps infections in the etiology of type 1 (insulin-dependent) diabetes. Diabetes Res 1988; 9: 111-116. (Pubitemid 19089947)
16. Gale EA. Congenital rubella: citation virus or viral cause of type 1 diabetes? Diabetologia 2008; 51: 1559-1566.
17. Pak CY, Eun HM, McArthur RG, Yoon JW. Association of cytomegalovirus infection with autoimmunetype 1 diabetes. Lancet 1988; 2: 1-4.
18. Jenson AB, Rosenberg HS, Notkins AL. Pancreaticislet- celldamageinchildrenwith fatalviral infections. Lancet 1980; 2: 354-358.
19. Tracy S, Drescher KM, Jackson JD, Kim K, Kono K. Enteroviruses, type 1 diabetesand hygiene: a complex relationship. Rev Med Virol 2010; 20: 106-116.
20. Andreoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyghem MC, Lefebvre J et al. Detectionof coxsackieBvirus RNAsequences inwholebloodsamplesfromadult patients atthe onset oftype I diabetes mellitus. J Med Virol 1997; 52: 121-127.
21. Schulte BM, Bakkers J, Lanke KH, Melchers WJ, Westerlaken C, Allebes W et al. Detection of enterovirus RNA in peripheral blood mononuclear cells of type 1 diabetic patients beyond the stage of acute infection. Viral Immunol 2010; 23: 99-104.
22. Clements GB, Galbraith DN, Taylor KW. Coxsackie B virus infection and onset of childhood diabetes. Lancet 1995; 346: 221-223.
23. Lonnrot M, Salminen K, Knip M, Savola K, Kulmala P, Leinikki P et al. Enterovirus RNAinserum isa riskfactorforbeta-cell autoimmunityandclinicaltype 1 diabetes: a prospective study. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 2000; 61: 214-220.
24. Stene LC, Oikarinen S, Hyöty H, Barriga KJ, Norris JM, Klingensmith G et al. Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: The Diabetes and Autoimmunity Study in the Young (DAISY). Diabetes 2010; 59: 3174-3180.
25. Yoon JW, Austin M, Onodera T, Notkins AL. Isolation of avirusfrom thepancreasof a child with diabetic ketoacidosis. N Engl J Med 1979; 300: 1173-1179.
26. Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 2009; 52: 1143-1151.
27. Richardson SJ, Willcox A, Hilton DA, Tauriainen S, Hyoty H, Bone AJ et al. Use of antisera directed against dsRNA to detect viral infections in formalin-fixed paraffin-embedded tissue. J Clin Virol 2010; 49: 180-185.
28. Chatterjee NK, Nejman C, Gerling I. Purification and characterization of a strain of coxsackievirus B4 of human origin that induces diabetes in mice. J Med Virol 1988; 26: 57-69.
29. Elshebani A, Olsson A, Westman J, Tuvemo T, Korsgren O, Frisk G. Effectson isolated human pancreatic islet cells after infection with strains of enterovirus isolated at clinical presentation of type 1 diabetes. Virus Res 2007; 124: 193-203. (Pubitemid 46216572)
30. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002; 347: 911-920.
31. Dunne DW, Cooke A. A worm's eye view of the immune system: consequences for evolution of human autoimmunedisease. Nat Rev Immunol 2005; 5: 420-426. (Pubitemid 40685991)
32. Schubert C. News feature: the worm hasturned. Nat Med 2004; 10: 1271-1272.
33. Kurtzke JF. Epidemiologic evidence for multiple sclerosis as an infection. Clin Microbiol Rev 1993; 6: 382-427. (Pubitemid 23306593)
34. Fujinami RS, von Herrath MG, Christen U, Whitton JL. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 2006; 19: 80-94. (Pubitemid 43157648)
35. Zaccone P, Fehervari Z, Phillips JM, Dunne DW, Cooke A. Parasitic worms and inflammatory diseases. Parasite Immunol 2006; 28: 515-523. (Pubitemid 44370857)
36. Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R et al. Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation. Diabetologia 2005; 48: 1280-1287. (Pubitemid 41186091)
37. Viskari H, Ludvigsson J, Uibo R, Salur L, Marciulionyte D, Hermann R et al. Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: results from the EPIVIR project. J Med Virol 2004; 72:610-617. (Pubitemid 38296072)
38. Seiskari T, Kondrashova A, Viskari H, Kaila M, Haapala AM, Aittoniemi J et al. Allergic sensitizationand microbial load\acomparisonbetween Finlandand Russian Karelia. Clin Exp Immunol 2007; 148: 47-52. (Pubitemid 46365000)
39. Bodansky HJ, Staines A, Stephenson C, Haigh D, Cartwright R. Evidence for an environmental effect in the aetiology of insulin dependent diabetes in a transmigratory population. BMJ1992;304: 1020-1022.
40. Cantorna MT, Mahon BD. Mountingevidenceforvitamin Dasanenvironmental factor affecting autoimmune disease prevalence. Exp Biol Med (Maywood) 2004; 229: 1136-1142. (Pubitemid 39602256)
41. 3 analog enhances regulatory T-cells and arrests autoimmune diabetes in NOD mice. Diabetes 2002; 51: 1367-1374. (Pubitemid 34826601)
42. 3 restores thymocyte apoptosis sensitivity in non-obese diabetic (NOD) micethrough dendritic cells. JAutoimmun 2005; 24: 281-289. (Pubitemid 40775852)
43. Fisman DN. Seasonality of infectious diseases. Annu Rev Public Health 2007; 28: 127-143. (Pubitemid 46833337)
44. Christen U, Hintermann E, Holdener M, von Herrath MG. Viral triggers for autoimmunity: isthe'glassof molecular mimicry' halffull orhalfempty?JAutoimmun 2010; 34: 38-44.
45. Christen U, von Herrath MG. Induction, accelerationorpreventionof autoimmunityby molecular mimicry. Mol Immunol 2004; 40: 1113-1120. (Pubitemid 38221193)
46. Damian RT. Molecular mimicry: antigen sharing by parasite and host and its consequences. Am Nat 1964; 98: 129-149.
47. Oldstone MB. Molecular mimicry as a mechanism for the cause and as a probe uncovering etiologic agent(s) of autoimmune disease. Curr Top Microbiol Immunol 1989; 145: 127-136.
48. von Herrath MG, Fujinami RS, Whitton JL. Microorganismsandautoimmunity: making the barren field fertile. Nat Rev Microbiol 2003; 1: 151-157.
49. Rhode A, Pauza ME, Barral AM, Rodrigo E, Oldstone MB, von Herrath MG et al. Islet-specific expression of CXCL10 causes spontaneous islet infiltration and accelerates diabetes development. J Immunol 2005; 175: 3516-3524. (Pubitemid 41292009)
50. Eizirik DL, Colli ML, Ortis F. The roleof inflammation in insulitisand beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 2009; 5: 219-226.
51. D'Alise AM, Auyeung V, Feuerer M, Nishio J, Fontenot J, Benoist C et al. Thedefect in T-cell regulation in NOD mice is an effect on theT-cell effectors. Proc Natl Acad Sci USA2008; 105: 19857-19862.
52. Freimuth P, Philipson L, Carson SD. The coxsackie virus and adeno virus receptor. Curr Top Microbiol Immunol 2008; 323: 67-87.
53. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 1998; 4: 781-785. (Pubitemid 28331018)
54. Horwitz MS, Ilic A, Fine C, Balasa B, Sarvetnick N. Coxsackieviral- mediateddiabetes: induction requires antigen-presenting cells and is accompanied by phagocytosis of betacells. Clin Immunol 2004; 110: 134-144. (Pubitemid 38296703)
55. Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA. Accelerationoftype 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactiveT-cells in pancreatic islets. Diabetes 2000; 49: 708-711. (Pubitemid 30339984)
56. Coleman TJ, Gamble DR, Taylor KW. Diabetes in mice after Coxsackie B4 virus infection. Br Med J 1973; 3: 25-27.
57. Tracy S, Drescher KM, Chapman NM, Kim KS, Carson SD, Pirruccello S et al. Toward testingthehypothesisthat group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic micewith CVB markedly lowers diabetes incidence. J Virol 2002; 76: 12097-12111. (Pubitemid 35304309)
58. Kanno T, Kim K, Kono K, Drescher KM, Chapman NM, Tracy S. Group B coxsackievirus diabetogenic phenotype correlates with replication efficiency. J Virol 2006; 80: 5637-5643.
59. Schulte BM, Kramer M, Ansems M, Lanke KH, van Doremalen N, Piganelli JD et al. Phagocytosis of enterovirus-infected pancreatic beta-cells triggers innate immune responsesinhumandendriticcells. Diabetes 2010; 59: 1182-1191.
60. Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: Role of anti-self (virus) immune response. Cell 1991; 65: 319-331. (Pubitemid 121006061)
61. von Herrath MG, Dockter J, Oldstone MB. How virus induces a rapid or slow onset insulin-dependentdiabetes mellitus inatransgenic model. Immunity 1994; 1: 231-242.
62. Oldstone MB. Prevention of type I diabetes in nonobese diabetic mice by virus infection. Science 1988; 239: 500-502. (Pubitemid 18084314)
63. Christen U, von Herrath MG. Infections and autoimmunity\good or bad? J Immunol 2005; 174: 7481-7486.
64. Selin LK, Welsh RM. Plasticityof Tcell memoryresponsestoviruses. Immunity 2004; 20: 5-16.
65. Christen U, Edelmann KH, McGavern DB, Wolfe T, Coon B, Teague MK et al. Aviral epitope that mimics a self antigen can accelerate but not initiate autoimmune diabetes. JClin Invest 2004; 114: 1290-1298. (Pubitemid 40385300)
66. Homepage TEDDYStudy. Availablefrom: http://teddy.epi.usf.edu/