Enterovirus infections and type 1 diabetes

References

• Zinkernagel RM. Cellular immune recognition and the biological role of major transplantaticn antigens. Scand J Immunol 1997; 46: 421–36.
   Google Scholar
• Atkinson MA, Madaren NK. The pathogenesis of insulin-dependent diabetes mellitus. N Engl J Med 1994; 331: 1428–36.
   PubMed Web of Science ®Google Scholar
• Kimpimäki T, Kulmala P, Savola K, Vähäsalo P, Reijonen H, llonen J, et al. Disease-associated autoantibodies as surrogate markers of type 1 diabetes in young children at increased genetic risk. J Clin Endocrinol Metab 2000; 85: 1126–32.
   Google Scholar
• Menser MA, Forrest JM, Bransby RD. Rubella infection and diabetes mellitus. Lancet 1978; i: 57–60.
   Google Scholar
• Yoon JW. A new look at viruses in type 1 diabetes. Diabetes Metab Rev 1995; 11: 83–107.
   Google Scholar
• Juhela S, Hytity H, Liinnrot M, Roivainen M, Simell 0, Ilonen J. Enterovirus infections and enterovirus specific T-cell responses in infancy. J Med Virol 1998; 54: 226–32.
   PubMedGoogle Scholar
• Melnick JL. Enteroviruses: Polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In: Fields BN, Knipe DM, Howley PM, eds. Virology 3rd edn. Philadelphia, PA: Lippincott-Raven Publishers 1996: 655–712.
   Google Scholar
• Gamble DR, Kinsley ML, Fitzgerald MG, Taylor KW. Viral antibodies in diabetes mellitus. BMJ 1969; 3: 627–30.
   PubMed Web of Science ®Google Scholar
• Gamble DR, Taylor KW. Seasonal incidence of diabetes mellitus. BMJ 1969; 3: 631–3.
   PubMedGoogle Scholar
• Green A, Patterson CC on behalf of the EURODIAB TIGER Study Group. Trends in the incidence of childhood-onset diabetes in Europe 1989-1998. Diabetologia 2001; 44 (Suppl 3): B3–8.
   PubMedGoogle Scholar
• Kimpimäki T, Kupila A, Hämäläinen AM, Kukko M, Kulmala P, Savola K, 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: 4782–8.
   PubMedGoogle Scholar
• Banatvala JE, Bryant J, Schernthaner G, Borkenstein M, Schober E, Brown D, et al. Coxsackie B, mumps, rubella, and cytomegalovirus specific IgM responses in patients with juvenile-onset insulin-dependent diabetes mellitus in Britain, Austria, and Australia. Lancet 1985; 1: 1409–12.
   PubMed Web of Science ®Google Scholar
• Frisk G, Friman G, Tuvemo T, Fohhnan J, Diderholm H. Coxsackie B virus IgM in children at onset of type 1 (insulin-dependent) diabetes mellitus: evidence for IgM induction by a recent or current infection. Diabetologia 1992; 35: 249–53.
   PubMed Web of Science ®Google Scholar
• Szopa TM, Titchener PA, Portwood ND, Taylor KW. Diabetes mellitus due to viruses-some recent developments. Diabetologia 1993; 36: 687–95.
   PubMed Web of Science ®Google Scholar
• Helfand RF, Gary HE, Freeman CY, Anderson LI, Pitts-burgh Diabetes Research Group, Pallansch MA. Serologic evidence of an association between enteroviruses and the onset of type 1 diabetes mellitus. J Infect Dis 1995; 172: 1206–11.
   Google Scholar
• Palmer JP, Cooney MK, Ward RH, Hansen JA, Brodsky JB, Ray CG, et al. Reduced coxsackie antibody titres in type 1 (insulin-dependent) diabetic patients presenting during an outbreak of coxsackie B3 and B4 infection. Diabetologia 1982; 22: 426–9.
   Google Scholar
• Bruserud O, Jervell J, Thorsby E. HLA-DR3 and -DR4 control T-lymphocyte responses to mumps and Coxsackie B4 virus: studies on patients with type 1 (insulin-dependent) diabetes and healthy subjects. Diabetologia 1985; 28: 420–6.
   Google Scholar
• Yoon JW, Austin M, Onodera T, Notkins AL. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 1979; 300: 1173–9.
   PubMed Web of Science ®Google Scholar
• Foulis AK, Farquharson MA, Meager A. Immunoreactive alpha-interfercn in insulin-secreting beta cells in type 1 diabetes mellitus. Lancet 1987; 2: 1423–7.
   PubMed Web of Science ®Google Scholar
• Huang X, Yuang J, Goddard A. Interferon expression in the pancreases of patients with type 1 diabetes. Diabetes 1995; 44: 658–64.
   PubMed Web of Science ®Google Scholar
• Foulis AK, Farquharson MA, Cameron SO, McGill M, Schonke H, Kandolf R. A search for the presence of the enteroviral capsid protein VP1 in pancreases of patients with type 1 (insulin-dependent) diabetes and pancreases and hearts of infants who died of coxsackieviral myocarditis. Diabeto-logia 1990; 33: 290–8.
   Google Scholar
• Foulis AK, Macgill M, Farquharson MA, Hilton DA. A search for evidence of viral infection in pancreases of newly diagnosed patients with IDDM. Diabetologia 1997; 40: 53–61.
   PubMed Web of Science ®Google Scholar
• Buesa-Gomez J, de la Torre JC, Dyrberg T, Landin-Olsson
   Google Scholar
• M, Mauseth RS, Lermnark A, et al. Failure to detect genomic viral sequences in pancreatic tissues from two children with acute-onset diabetes mellitus. J Med Virol 1994; 42: 193–7.
   Google Scholar
• Chehadeh W, Weill J, Vantyghem MC, Alm G, Lefebvre J, Wattre P, et al. Increased level of interferon-a in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J Infect Dis 2000; 181: 1929–39.
   PubMed Web of Science ®Google Scholar
• Jones DB, Crosby L Proliferative lymphocyte responses to virus antigens homologous to GAD65 in IDDM. Diabetologia 1996; 39: 1318–24.
   PubMed Web of Science ®Google Scholar
• Juhela S, Hyöty H, Hinkkanen A, Elliott J, Roivainen M, Kulmala P, et al. T cell responses to enterovirus antigens and to beta-cell autoantigens in unaffected children positive for IDDM-associated autoantibodies. J Auto immun 1999; 12: 269–78.
   PubMed Web of Science ®Google Scholar
• Juhela S, Hyöty H, Roivainen M, Härkonen T, Putto-Laurila A, Simell 0, et al. T-cell responses to enterovirus antigens in children with type 1 diabetes. Diabetes 2000; 49: 1308–13.
   PubMed Web of Science ®Google Scholar
• Hyöty H, Hiltunen M, Knip M, Laakkonen M, Vähäsalo P, Karjalainen J, et al. A prospective study of the role of coxsackie B and other enterovirus infections in the pathogen-esis of IDDM. Diabetes 1995; 44: 652–7.
   PubMed Web of Science ®Google Scholar
• Hiltunen M, Hyöty H, Knip M, llonen J, Reijonen H, Vähäsalo P, et al. Islet cell antibody seroconversion in children is temporally associated with enterovirus infections: Child-hood Diabetes in Finland (DiMe) Study Group. J Infect Dis 1997; 175: 554–60.
   Google Scholar
• Roivainen M, Knip M, Hyöty H, Kulmala P, Hiltunen M, Vähäsalo P, 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: 74–8.
   Google Scholar
• Lönnrot M, Sahninen K, Knip M, Savola K, Kuhnala P, Leinikki P, et al. Enterovirus RNA in serum is a risk factor for beta-cell autoimmunity and clinical IDDM - a prospective study. J Med Virol 2000; 61: 214–20.
   Google Scholar
• Kupila A, Muona P, Simell T, Arvilommi P, Savolainen H, Hämäläinen AM, et al. Feasibility of genetic and immuno-logical prediction of type 1 diabetes in a population-based birth cohort. Diabetologia 2001; 44: 290–7.
   PubMed Web of Science ®Google Scholar
• Lönnrot M, Korpela K, Knip M, Ilonen J, Simell 0, Korhonen S, et al. Enterovirus infection as a risk factor for
   Google Scholar
• beta-cell autoimmunity in the prospective birth-cohort trial DIPP. Diabetes 2000; 49: 1314–8.
   Google Scholar
• Sadeharju K, Lönnrot M, Kimpimäki T, Savola K, Erkkild S, Kalliokoski T, et al. Enterovirus antibody levels during the first two years of life in prediabetic autoantibody-positiw children. Diabetologia 2001; 44: 818–23.
   Google Scholar
• Heino L, Lönnrot M, Knip M, Kupila A, Erkkilä S, Toivonen A, et al. No evidence of abnormal regulation of antibody response to coxsackievirus B4 antigen in prediabetic children. Clin Exp Immunol 2001; 126: 432–6.
   Google Scholar
• Honeyman MC, Coulson BS, Stone NIL, Gellert SA, Goldwater PN, Steele CE, et al. Association between rotavirus infections and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes 2000; 49: 1319–24.
   PubMed Web of Science ®Google Scholar
• Dahlquist GG, Ivarsson S, Lindberg B, Forsgren M. Maternal enteroviral infection during pregnancy as a risk factor for childhood IDDM: a population-based case-control study. Diabetes 1995; 44: 408–13.
   PubMed Web of Science ®Google Scholar
• Dahlquist GG, Frisk G, Ivarsson SA, Svanberg L, Forsgren M, Diderholm H. Indications that maternal coxsackie B virus infection during pregnancy is a risk factor for childhood-onset IDDM. Diabetologia 1995; 38: 1371–3.
   PubMed Web of Science ®Google Scholar
• Otonkoski T, Roivainen M, Vaarala 0, Dinesen B, Leipala JA, Hovi T, et al. Neonatal Type I diabetes associated with maternal echovirus 6 infection: a case report. Diabetologia 2000; 43: 1235–8.
   PubMedGoogle Scholar
• Viskari HR, Koskela P, Lönnrot M, Luonuansuu S, Reunanen A, Baer M, et al. Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 2000; 23: 414–6.
   Google Scholar
• Lönnrot M, Knip M, Marciulionyte D, Rahko J, Urbonaite B, Moore WP, et al. Enterovirus antibodies in relation to islet cell antibodies in two populations with high and low incidence of type 1 diabetes. Diabetes Care 1999; 22: 2086–8.
   PubMedGoogle Scholar
• Mulders MN, Salminen M, Kalkkinen N, Hovi T. Molecu-lar epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2A(pro) cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes. J Gen Virol 2000; 81: 803–12.
   PubMed Web of Science ®Google Scholar
• Blonde! B, Duncan G, Couderc T, Delpeyroux F, Pavio N, Colbere-Garapin F. Molecular aspects of poliovirus biology with a special focus on the interactions with nerve cells. J Neurovirol 1998; 4: 1–26.
   Google Scholar
• Klingel K, Selinka HC, Huber M, Sauter M, Leube M, Kandolf R. Molecular pathology and structural features of enteroviral replication. Towards understanding the pathogen-esis of viral heart disease. Herz 2000; 25: 216–20.
   Google Scholar
• Jun HS, Yoon JW. The role of viruses in type I diabetes: two distinct cellular and molecular pathogenic mechanisms of virus-induced diabetes in animals. Diabetologia 2001; 44: 271–85.
   PubMed Web of Science ®Google Scholar
• Sussman ML, Strauss L, Hodes UL. Fatal coxsackie B virus infections in the newborn. Report of case with necropsy findings and brief review of the literature. Am J Dis Child 1959; 97: 483–92.
   Google Scholar
• Jenson AB, Rosenberg HS, Notkins AL. Pancreatic islet-cell damage in children with fatal viral infections. Lancet 1980; 1: 354–8.
   Google Scholar
• Ujevich MM, Jaffe R. Pancreatic islet cell damage. Its occurrence in neonatal coxsackievirus encephalomyocarditis. Arch Pathol Lab Med 1980; 104: 438–41.
   Google Scholar
• Alunad N, Abraham AA. Pancreatic isleitis with coxsackie-virus B5 infection. Hum Pathol 1982; 13: 661–2.
   Google Scholar
• Yoon J-W, Onodera T, Jenson AB, Notkins AL. Virus induced diabetes mellitus. XI. Replication of coxsackie B3 in human pancreatic beta cell cultures. Diabetes 1978; 27: 778–81.
   PubMed Web of Science ®Google Scholar
• Roivainen M, Rasilainen S, Ylipaasto P, Nissinen R
   Google Scholar
• Ustinov J, Bouwens L, et al. Mechanisms of coxsackievirus-induced damage to human pancreatic beta-cells. J Clin Endocrinol Metab 2000; 85: 432–40.
   Google Scholar
• Szopa TM, Gamble DR, Taylor KW. Coxsackie B4 virus induces short-term changes in the metabolic function of mouse pancreatic islets in vitro. Cell Biochem Funct 1986; 4: 181–7.
   Google Scholar
• Frisk G, Diderholm H. Tissue culture of isolated human pancreatic islets infected with different strains of coxsackie-virus B4: assessment of virus replication and effects on islet morphology and insulin release. Int J Exp Diabetes Res 2000; 1: 165–75.
   Google Scholar
• Parkkonen P, Hyöty H, Koskinen L, Leinikki P. Mumps virus infects beta cells in human fetal islet cell cultures upregulating the expression of HLA class I molecules. Diabetologia 1992; 35: 63–9.
   PubMedGoogle Scholar
• Chehadeh W, Kerr-Conte J, Pattou F, Alm G, Lefebvre J, Wattre P, et al. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J Virol 2000; 74: 10153–64.
   PubMed Web of Science ®Google Scholar
• See TM, Tilles JG. Pathogenesis of virus-induced diabetes in mice. J Infect Dis 1995; 171: 1131–8.
   PubMed Web of Science ®Google Scholar
• Paronen J, Klemetti P, Kantele JM, Savilahti E, Perheentupa J, ikkerblom HK, et al. Glutamate decarboxylase-reactive peripheral blood lymphocytes from patients with IDDM express gut-specific homing receptor alpha4beta7-integrin Diabetes 1997; 46: 583–8.
   Google Scholar
• Hänninen A, Salmi M, Simell 0, Jallcanen S. Endothelial cell-binding properties of lymphocytes infiltrated into human diabetic pancreas. Implications for pathogenesis of IDDM. Diabetes 1993; 42:1656–62.
   PubMed Web of Science ®Google Scholar
• Graham S, Wang EC, Jenkins 0, Borysiewicz LK. Analysis of the human T-cell response to picornaviruses: identification of T-cell epitopes close to B-cell epitopes in poliovirus. J Virol 1993; 67: 1627–37.
   PubMedGoogle Scholar
• Cello J, Strannegard 0, Svennerholm B. A study of the cellular immune response to enteroviruses in humans: identi-fication of cross-reactive T cell epitopes on the structural proteins of enteroviruses. J Gen Virol 1996; 77: 2097–108.
   Google Scholar
• 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: 319–31.
   PubMed Web of Science ®Google Scholar
• Atkinson MA, Bowman MA, Campbell L, Darrow BL, Kaufman DL, Maclaren NK. Cellular immunity to a determinant common to glutamate decarboxylase and cox-sackie virus in insulin-dependent diabetes. J Clin Invest 1994; 94: 2125–9.
   PubMed Web of Science ®Google Scholar
• Kaufman DL, Erlander MG, Clare-Salzler M, Atkinson MA, Maclaren NK, Tobin AJ. Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. J Clin Invest 1992; 89: 283–92.
   PubMed Web of Science ®Google Scholar
• Marttila J, Juhela S, Vaarala 0, Hyöty H, Roivainen M, Hinkkanen A, et al. Responses of coxsackievirus B4-specific T-cell lines to 2C protein-characterizaticn of epitopes with special reference to the GAD65 homology region. Virology 2001; 284: 131–41.
   PubMedGoogle Scholar
• Schloot NC, Willemen SJ, Duinkerken G, Drijfhout JW, de Vries RR, Roep BO. 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 2001; 62: 299–309.
   PubMedGoogle Scholar
• Lönnrot M, Hyöty H, Knip M, Roivainen M, Kulmala P, Leinikki P, et al. Antibody cross-reactivity induced by the homologous regions in glutamic acid decarboxylase (GAD65) and 2C protein of Coxsackievirus B4. Clin Exp Immunol 1996; 104: 398–402.
   PubMed Web of Science ®Google Scholar
• Richter W, Mertens T, Schoel B, Muir P, Ritzkowsky A, Scherbaum WA, et al. Sequence homology of the diabetes-associated autoantigen glutamate decarboxylase with cox-sackie B4-2C protein and heat shock protein 60 mediates no molecular mimicry of autoantibodies. J Exp Med 1994;180: 721–6.
   PubMed Web of Science ®Google Scholar
• Härkonen T, Puolakkainen M, Sarvas M, Airaksinen U, Hovi T, Roivainen M. Picornavirus proteins share antigenic determinants with heat shock proteins 60/65. J Med Virol 2000; 62: 383–91.
   Google Scholar
• Luppi P, Zanone MM, Hyöty H, Rudert WA, Haluszczak C, Alexander A, et al. Restricted TCR VI3 gene usage and enterovirus infection in Type 1 diabetes. Diabetologia 2000; 43: 1484–97.
   PubMed Web of Science ®Google Scholar
• Yoon J-W, Onodera T, Nodcins AL. Virus induced diabetes mellitus: beta cell damage and insulin dependent hyperglycae-mia in mice infected with coxsackie B4. J Exp Med 1978; 148: 1068–80.
   PubMed Web of Science ®Google Scholar
• Jun HS, Yoon JW. The role of viruses in type I diabetes: two distinct cellular and molecular pathogenic mechanisms of virus-induced diabetes in animals. Diabetologia 2001; 44: 271–85.
   PubMed Web of Science ®Google Scholar
• Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by coxsackievirus: Initiaticn by bystander damage and not molecular mimicry. Nat Med 1998; 4: 781–5.
   PubMed Web of Science ®Google Scholar
• Horwitz MS, Fine C, flic A, Sarvetnick N. Requirements for viral-mediated autoimmune diabetes: beta-cell damage and immune infiltration. J Autoimmun 2001; 16: 211–7.
   PubMedGoogle Scholar
• Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA. Acceleration of type 1 diabetes by a cox-sackievirus infection requires preexisting critical mass of autoreactive T-cells in pancreatic islets. Diabetes 2000; 49: 708–11.
   PubMedGoogle Scholar
• Clements GB, Galbraith DN, Taylor KW. Coxsackie B virus infection and onset of childhood diabetes. Lancet 1995; 346: 221–3.
   PubMed Web of Science ®Google Scholar
• Nairn C, Galbraith DN, Taylor KW, Clements GB. Enterovirus variants in the serum of children at the onset of type 1 diabetes mellitus. Diabet Med 1999; 16: 509–13.
   PubMedGoogle Scholar
• Andreoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyghem M-C, Lefebvre J, et al. Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of type 1 diabetes mellitus. J Med Virol 1997; 52: 121–7.
   PubMedGoogle Scholar
• Yin H, Tuvemo T, Frisk G. High frequency of enterovirus RNA in lymphocytes from IDDM children at onset. Diabeto-logia 2000; 43 (Suppl. 1): A96.
   Google Scholar
• Craig ME, Silink M, Howard NJ, Rawlinson WD. Genotyping of enteroviruses in children at diagnosis of type 1 diabetes (abstract). 26th Annual meeting of the International Society for pediatric and adolescent diabetes (ISPAD), Los Angeles, USA, 2000.
   Google Scholar
• Gerling I, Chatterjee NK, Neiman C. Coxsackievirus B4-induced development of antibodies to 64,000-Mr islet auto-antigen and hyperglycemia in mice. Autoimmunity 1991; 10: 49–56.
   PubMed Web of Science ®Google Scholar