Coxsackievirus b1 is associated with induction of β-cells autoimmunity that portends type 1 diabetes

Diabetes

Volumn 63, Issue 2, 2014, Pages 446-455

  Laitinen, Olli H ^a   Honkanen, Hanna ^b   Pakkanen, Outi ^a   Oikarinen, Sami ^b   Hankaniemi, Minna M ^a   Huhtala, Heini ^b   Ruokoranta, Tanja ^a   Lecouturier, Valérie ^c   André, Philippe ^c   Harju, Raimo ^a   Virtanen, Suvi M ^b,d,e,f   Lehtonen, Jussi ^a   Almond, Jeffrey W ^c   Simell, Tuula ^g   Simell, Olli ^g   Ilonen, Jorma ^h,i   Veijola, Riitta ^j   Knip, Mikael ^f,k,l,m   Hyöty, Heikki ^b,d  

^a Vactech Ltd   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c SANOFI PASTEUR   (France)

^d PIRKANMAA HOSPITAL DISTRICT   (Finland)

^e NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^f TAMPERE UNIVERSITY HOSPITAL   (Finland)

^g TURKU UNIVERSITY HOSPITAL   (Finland)

^h UNIVERSITY OF TURKU   (Finland)

ⁱ UNIVERSITY OF EASTERN FINLAND   (Finland)

^j OULU UNIVERSITY HOSPITAL   (Finland)

^k FOLKHÄLSAN RESEARCH CENTER   (Finland)

^l UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^m UNIVERSITY OF HELSINKI   (Finland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; MATERNAL ANTIBODY; NEUTRALIZING ANTIBODY;

ARTICLE; AUTOIMMUNITY; BREAST FEEDING; CASE CONTROL STUDY; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; COXSACKIE VIRUS; COXSACKIE VIRUS B1; COXSACKIE VIRUS B3; COXSACKIE VIRUS B6; COXSACKIE VIRUS INFECTION; CROSS PROTECTION; FEMALE; FOLLOW UP; HUMAN; INFANT; INFECTION RISK; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; PANCREAS ISLET BETA CELL; PHYLOGENY; PRIORITY JOURNAL; PROSPECTIVE STUDY; SEROPREVALENCE; SEROTYPE; UMBILICAL CORD BLOOD;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; CASE-CONTROL STUDIES; CELL LINE; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; GENE EXPRESSION REGULATION; GENOTYPE; HLA-DQ BETA-CHAINS; HUMANS; INSULIN-SECRETING CELLS; PHYLOGENY; RISK FACTORS;

EID: 84893048226     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0619     Document Type: Article

References (44)

1. Tauriainen S, Oikarinen S, Oikarinen M, Hyöty H. Enteroviruses in the pathogenesis of type 1 diabetes. Semin Immunopathol 2011;33:45-55
2. Yeung WC, Rawlinson WD, Craig ME. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 2011;342:d35
3. Smyth DJ, Cooper JD, Bailey R, et al. A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferoninduced helicase (IFIH1) region. Nat Genet 2006;38:617-619
4. Frisk G, Diderholm H. Tissue culture of isolated human pancreatic islets infected with different strains of coxsackievirus B4: assessment of virus replication and effects on islet morphology and insulin release. Int J Exp Diabetes Res 2000;1:165-175
5. Chehadeh W, Kerr-Conte J, Pattou F, et al. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J Virol 2000;74:10153-10164
6. Roivainen M, Rasilainen S, Ylipaasto P, et al. Mechanisms of coxsackievirus-induced damage to human pancreatic beta-cells. J Clin Endocrinol Metab 2000;85:432-440
7. Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T. 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 2002; 45:693-702
8. Shibasaki S, Imagawa A, Tauriainen S, et al. Expression of toll-like receptors in the pancreas of recent-onset fulminant type 1 diabetes. Endocr J 2010;57:211-219
9. Tanaka S, Nishida Y, Aida K, et al. Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated betacell failure in fulminant type 1 diabetes. Diabetes 2009;58:2285-2291
10. 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
11. Oikarinen M, Tauriainen S, Honkanen T, et al. Analysis of pancreas tissue in a child positive for islet cell antibodies. Diabetologia 2008;51:1796-1802
12. Green J, Casabonne D, Newton R. Coxsackie B virus serology and Type 1 diabetes mellitus: a systematic review of published case-control studies. Diabet Med 2004;21:507-514
13. Al-Hello H, Paananen A, Eskelinen M, 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
14. Näntö-Salonen K, Kupila A, Simell S, et al. Nasal insulin to prevent type 1 diabetes in children with HLA genotypes and autoantibodies conferring increased risk of disease: a double-blind, randomised controlled trial. Lancet 2008;372:1746-1755
15. Ilonen J, Reijonen H, Herva E, et al. Rapid HLA-DQB1 genotyping for four alleles in the assessment of risk for IDDM in the Finnish population. The Childhood Diabetes in Finland (DiMe) Study Group. Diabetes Care 1996;19: 795-800
16. Sjöroos M, Iitiä A, Ilonen J, Reijonen H, Lövgren T. Triple-label hybridization assay for type-1 diabetes-related HLA alleles. Biotechniques 1995;18: 870-877
17. Knip M, Virtanen SM, Seppä K, et al.; Finnish TRIGR Study Group. Dietary intervention in infancy and later signs of beta-cell autoimmunity. N Engl J Med 2010;363:1900-1908
18. Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 2006;44: 2698-2704
19. Roivainen M, Knip M, Hyöty H, et al. Several different enterovirus serotypes can be associated with prediabetic autoimmune episodes and onset of overt IDDM. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 1998;56:74-78
20. Kimpimäki T, Kupila A, Hämäläinen AM, et al. The first signs of beta-cell autoimmunity appear in infancy in genetically susceptible children from the general population: the Finnish Type 1 Diabetes Prediction and Prevention Study. J Clin Endocrinol Metab 2001;86:4782-4788
21. Ziegler AG, Hummel M, Schenker M, Bonifacio E. Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 1999;48:460-468
22. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA; Centers for Disease Control and Prevention. Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ 2006;55:1-20
23. Centers for Disease Control and Prevention (CDC). Nonpolio enterovirus and human parechovirus surveillance - United States, 2006-2008. MMWR Morb Mortal Wkly Rep 2010;59:1577-1580
24. Kim H, Kang B, Hwang S, et al. Molecular characteristics of human coxsackievirus B1 infection in Korea, 2008-2009. J Med Virol 2013;85:110-115
25. Kumar A, Shukla D, Kumar R, Idris MZ, Misra UK, Dhole TN. Molecular epidemiological study of enteroviruses associated with encephalitis in children from India. J Clin Microbiol 2012;50:3509-3512
26. Bahri O, Rezig D, Nejma-Oueslati BB, et al. Enteroviruses in Tunisia: virological surveillance over 12 years (1992-2003). J Med Microbiol 2005;54: 63-69
27. Roth B, Enders M, Arents A, Pfitzner A, Terletskaia-Ladwig E. Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000-2005. J Med Virol 2007;79:956-962
28. Klemola P, Kaijalainen S, Ylipaasto P, Roivainen M. Diabetogenic effects of the most prevalent enteroviruses in Finnish sewage. Ann N Y Acad Sci 2008;1150:210-212
29. Centers for Disease Control and Prevention (CDC). Increased detections and severe neonatal disease associated with coxsackievirus B1 infection- United States, 2007. MMWR Morb Mortal Wkly Rep 2008;57:553-556
30. Chiou CC, Liu WT, Chen SJ, et al. Coxsackievirus B1 infection in infants less than 2 months of age. Am J Perinatol 1998;15:155-159
31. Jenson AB, Rosenberg HS, Notkins AL. Pancreatic islet-cell damage in children with fatal viral infections. Lancet 1980;2:354-358
32. Tam PE, Schmidt AM, Ytterberg SR, Messner RP. Duration of virus persistence and its relationship to inflammation in the chronic phase of coxsackievirus B1-induced murine polymyositis. J Lab Clin Med 1994;123: 346-356
33. Cello J, Strannegård O, Svennerholm B. A study of the cellular immune response to enteroviruses in humans: identification of cross-reactive T cell epitopes on the structural proteins of enteroviruses. J Gen Virol 1996;77: 2097-2108
34. Bodian D. Differentiation of types of poliomyelitis viruses; reinfection experiments in monkeys (second attacks). Am J Hyg 1949;49:200-223
35. Marttila J, Hyöty H, Vilja P, et al. T cell epitopes in coxsackievirus B4 structural proteins concentrate in regions conserved between enteroviruses. Virology 2002;293:217-224
36. Luostarinen T, af Geijersstam V, Bjørge T, et al. No excess risk of cervical carcinoma among women seropositive for both HPV16 and HPV6/11. Int J Cancer 1999;80:818-822
37. Ward RL, McNeal MM, Sheridan JF. Evidence that active protection following oral immunization of mice with live rotavirus is not dependent on neutralizing antibody. Virology 1992;188:57-66
38. Landau BJ, Whittier PS, Finkelstein SD, et al. Induction of heterotypic virus resistance in adult inbred mice immunized with a variant of Coxsackievirus B3. Microb Pathog 1990;8:289-298
39. Drescher KM, Kono K, Bopegamage S, Carson SD, Tracy S. Coxsackievirus B3 infection and type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection. Virology 2004;329:381-394
40. Serreze DV, Wasserfall C, Ottendorfer EW, et al. Diabetes acceleration or prevention by a coxsackievirus B4 infection: critical requirements for both interleukin-4 and gamma interferon. J Virol 2005;79:1045-1052
41. Oikarinen S, Tauriainen S, Hober D, et al. Virus antibody survey in different European populations indicates risk association between coxsackievirus B1 and type 1 diabetes. Diabetes 2014;63:655-662
42. Oikarinen S, Martiskainen M, Tauriainen S, et al. Enterovirus RNA in blood is linked to the development of type 1 diabetes. Diabetes 2011;60:276-279
43. Gerling I, Chatterjee NK, Nejman C. Coxsackievirus B4-induced development of antibodies to 64,000-Mr islet autoantigen and hyperglycemia in mice. Autoimmunity 1991;10:49-56
44. Larsson PG, Lakshmikanth T, Svedin E, King C, Flodström-Tullberg M. Previous maternal infection protects offspring from enterovirus infection and prevents experimental diabetes development in mice. Diabetologia 2013;56:867-874