1887

Chapter 15 : The Possible Role of Enteroviruses in Diabetes Mellitus

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

The Possible Role of Enteroviruses in Diabetes Mellitus, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818326/9781555810924_Chap15-1.gif /docserver/preview/fulltext/10.1128/9781555818326/9781555810924_Chap15-2.gif

Abstract:

Insulin-dependent diabetes mellitus (IDDM) is the most common severe chronic childhood illness, affecting an estimated 123,000 children in the United States. Picornaviruses have long been examined for their role as the primary etiologic agent in the pathogenesis of IDDM. Encephalomyocarditis virus (EMCV), a murine picornavirus, produces acute lytic infection of pancreatic β cells and diabetes whose severity correlates with the degree of β-cell lysis. An alternative innocent bystander theory proposes that local inflammation in the peri-insular tissue may induce molecules on the surface of β-cells that enteroviruses could use as cellular receptors. Well-established models of persistent viral infection leading to IDDM include reovirus type 1-induced diabetes and lymphocytic choriomeningitis virus (LCMV)-induced diabetes in mice as well as congenital rubella syndrome (CRS) in humans. Much of what is known concerning tropism of enteroviruses to the human pancreas has been learned from autopsy studies of newborns and infants who died of fulminant enteroviral infection. A large prospective study of young children monitored for concurrent development of enteroviral infections and β-cell autoimmunity is needed to test the hypothesis that symptomatic and/or serologically detectable enteroviral infection is associated with development of IDDM or β-cell autoimmunity. At present, it is not known, whether a single pathogenic mechanism is responsible for diabetes induced by various picornaviruses or whether diabetes can result from a spectrum of picornavirus-induced lesions, e.g., acute β-cell lysis, chronic autoimmunity, or insulin secretion defect. The rate of spontaneous mutation for enteroviruses is as high as 10 .

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15

Key Concept Ranking

Tumor Necrosis Factor alpha
0.46185172
0.46185172
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Molecular homology between GAD and coxsackievirus P2-C. Solid lines enclose identical amino acid residues. Dashed lines enclose residues with similar charges, polarities, or hydrophobicities. Reproduced from the ( ), by copyright permission of the American Society for Clinical Investigation.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Incidences of IDDM (thin line) and enteroviral meningitis (EVM) (heavy line) in Wielkopolska, Poland, (a) Children aged 0 through 4 years; (b) children aged 5 through 9 years; (c) children aged 10 through 14 years.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Incidence of IDDM (thin line) and enteroviral meningitis (EVM) (thick line) in Wielkopolska, Poland, 1980 through 1988. The IDDM curve reflects 3-month moving averages. The dominant serotypes of enteroviruses cultured from or determined serologically in the meningitis cases are shown. E, echovirus; B5, CVB5.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Incidence of IDDM in the age group 0 through 14 years in Norway, Colorado, and Poland in 1978 through 1980, showing significant geographic differences in incidence rates.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Age distribution of enteroviral meningitis in Norway, Colorado, and Poland. The high incidence of enteroviral meningitis in the age group 0 through 14 years in Poland (low IDDM risk) compared to those in Colorado (moderate IDDM risk) and Norway (high IDDM .risk) supports the polio model of IDDM etiology.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Age distribution of enteroviral meningitis inWielkopolska, Poland. There was no evidence for a change in distribution during the epidemic year (1982) compared to that in the nonepidemic years (1979 through 1981 and 1983).

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7
FIGURE 7

Incidence of IDDM and enteroviral meningitis (AM) in Colorado, 1978 through 1988. The incidence of IDDM paralleled that of enteroviral meningitis in lower-income Hispanics but not in higher-income non-Hispanic white children.

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818326.chap15
1. Ahmad, N.,, and A. A. Abraham. 1982. Pancreatic isleitis with coxsackie virus B5 infection. Hum. Pathol. 13: 661 662.
2. Allen, C.,, M. Paha,, and D. J. D'Alessio. 1991. Risk of diabetes in siblings and other relatives of IDDM subjects. Diabetes 40: 831 836.
3. Anderson, H. U.,, K. H. Jorgensen,, J. Egeberg,, T. Mandrup-Poulsen,, and J. Nerup. 1994. Nicotinamide prevents interleukin-1 effects on accumulated insulin release and nitric oxide production in rat islets of Langerhans. Diabetes 43: 770 777.
4. Anderson, O. O.,, M. Christy,, K. Arnung,, K. Buschard,, B. Christau,, H. Kromann,, J. Herup,, P. Platz,, L. P. Ryder,, A. Svejgaard,, and M. Thomsen,. 1977. Viruses and diabetes, p. 294 298. In J. S. Baja (ed.), Diabetes. Excerpta Medica, Amsterdam.
5. Archard, L. C.,, N. E. Bowles,, E. G. J. Olsen,, and P.J. Richardson. 1987. Detection of persistent coxsackie B virus RNA in dilated cardiomyopathy and myocarditis. Eur. Heart. J. 8( Suppl. J): 437 440.
6. Asplin, C. M.,, M. K. Cooney,, J. R. Crossley,, T. L. Dornan,, P. Raghu,, and J. P. Palmer. 1982. Coxsackie B4 infection and islet cell antibodies three years before overt diabetes. J. Pediatr. 101: 398 400.
6a. Atkinson, M. A., et al. Unpublished observations.
7. Atkinson, M. A.,, M. Bowman,, B. Darrow,,and D. Kaufman. 1994. Cellular immunity to an epitope common to glutamate decarboxylase (GAD) and coxsackie virus in insulin dependent diabetes (IDD). Diabetes 43( Suppl. 1): 93A.
8. Atkinson, M. A.,, D. L. Kaufman,, L. Campbell,, A. J. Tobin,, and N. K. Maclaren. 1993. Islet cell cytoplasmic autoantibody reactivity to glutamate decarboxylase in insulin dependent diabetes. J. Clin. Invest. 91: 350 356.
9. Bae, Y.-S.,, and J.-W. Yoon. 1993. Determination of diabetogenicity attributable to a single amino acid Ala776, on the polyprotein of encephalomyocarditis virus. Diabetes 42: 435 443.
10. Baekkeskov, S.,, M. Landin,, J. K. Kristensen,, S. Srikanta,, G. J. Bruining,, T. Mandrup-Poulsen,, C. De Beaufort,, J. S. Soeldner,, G. Eisenbarth,, E. Lindgren, et al. 1987. Antibodies to a 64,000 Mr human islet cell antigen precede the clinical onset of insulin-dependent diabetes. J. Clin. Invest. 79: 926 934.
10a. Baekkeskov, S.,, H. Jan-Aanstoot,, S. Christgau,, A. Reetz,, M. Solimena,, M. Cascalho,, E. Folli,, H. Richter-Olesen,, and P. De-Camilli. 1990. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature (London) 347: 151 156.
11. Baekkeskov, S.,, J. H. Nielsen,, B. T. Marner,, J. Bilde,, Ludvigsson,, and A. Lernmark. 1982. Autoantibodies in newly diagnosed diabetic children immunoprecipitate human pancreatic islet cell proteins. Nature (London) 298: 167 169.
12. Banatvala, J. E. 1987. Insulin-dependent (juvenile-onset, type 1) diabetes mellitus coxsackie B viruses revisited. Prog. Med. Virol. 34: 33 54.
13. Banatvala, J. E.,, J. Bryant,, G. Schernthaner,, M. Borkenstein,, E. Schober,, D. Brown,, L. M. DeSilva,, M. A. Menser,, and M. Silink. 1985. Coxsackie B, mumps, rubella, and cytomegalovirus specific IgM responses in patients with juvenile-onset insulin-dependent diabetes mellitus in Britain, Austria, and Australia. Lancet i: 1409 1412.
14. Barmeier, H.,, D. K. McCulloch,, J. L. Neifing,, G. Warnock,, R. V. Rajotte,, J. P. Palmer,, and A. Lernmark. 1991. Risk for developing type 1 (insulin-dependent) diabetes mellitus and the presence of islet 64K antibodies. Diabetologia 34: 727 733.
15. Barrett-Connor, E. 1985. Is insulin-dependent diabetes mellitus caused by coxsackie virus B infection? A review of the epidemiologic evidence. Rev. Infect. Dis. 7: 207 215.
16. Bell, G. I.,, S. Horita,, and J. H. Karam. 1984. A polymorphic locus near the human insulin gene is associated with insulin-dependent diabetes mellitus. Diabetes 33: 176 183.
17. Bertrams, J.,, and M. P. Baur,. 1984. Insulin-dependent diabetes mellitus, p. 348 358. In E. D. Albert (ed.), Histocompatibility Testing 1984. Springer-Verlag, Berlin.
18. Blom, L.,, L. Nystrom,, and G. Dahlquist. 1991. The Swedish childhood diabetes study. Vaccinations and infections as risk determinants for diabetes in childhood. Diabetologia 34: 176 181.
19. Bodansky, H. J.,, P. J. Grant,, B. M. Dean,, J. McNally,, G. E Bottazzo,, M. H. Hambling,, and J. K. Wales. 1986. Islet-cell antibodies and insulin autoantibodies in association with common viral infections. Lancet ii: 1351 1353.
20. Boehm, B. O.,, B. Manfras,, J. Seissler,, K. Schoffling,, M. Gluck,, G. Holzberger,, S. Seidl,, P. Kuhnl,, M. Trucco,, and W. A. Scherbaum. 1991. Epidemiology and immunogenetic background of islet cell antibody-positive nondiabetic schoolchildren. Ulm-Frankfurt population study. Diabetes 40: 1435 1439.
21. Bonifacio, E.,, P. J. Bingley,, M. Shattock,, B. M. Dean,, D. Dunger,, E. A. M. Gale,, and G. E Bottazzo. 1990. Quantification of islet-cell antibodies and prediction of insulin-dependent diabetes. Lancet 335: 147 149.
22. Bonnevie-Nielsen, V.,, M. L. Larsen,, J. J. Frifelt,, B. Michelsen,, and A. Lernmark. 1989. Association of IDDM and attenuated response of 2',5'-oligoadenylate synthetase to yellow fever vaccine. Diabetes 38: 1636 1642.
23. Boucher, D. W.,, K. Hayashi,, J. Rosenthal,, and A. L. Notkins. 1975. Virus-induced diabetes mellitus. III. Influence of sex and strain of the host. J. Infect. Dis. 131: 462 466.
24. Bouter, K. P.,, R. J. A. Diepersloot,, P. J. Wismans, et al. 1992. Humoral immune response to a yeast-derived hepatitis B vaccine in patients with type 1 diabetes mellitus. Diabetic Med. 9: 66 69.
25. Bruserud, O.,, J. Jervell,, and E. Thorsby. 1985. HOLA-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 28: 420 426.
26. Bruserud, O.,, and E. Thorsby. 1985. T lymphocyte responses to coxsackie B4 and mumps virus. I. Influence of HLA-DR restriction elements. Tissue Antigens 26: 41 50.
27. Bu, D. E.,, M. G. Erlander,, B. C. Hitz,, N. J. K. Tillakaratne,, D. L. Kaufman,, C. B. Wagner-McPherson,, G. A. Evans,, and A. J. Tobin. 1992. Two human glutamates decarboxylases, GAD 65 and GAD 67, are each en-coded by a single gene. Proc. Natl. Acad. Sci. USA 89: 2115 2119.
28. Buesa-Gomez, J.,, C. J. de la Torre,, T. Dyrberger,, M. Landin-Olsson,, R. S. Mauseth,, A. Lernmark,, and M. B. A. Oldstone. 1994. Failure to detect genomic viral sequences in pancreatic tissues from two children with acute-onset diabetes mellitus. J Med. Virol. 42: 193 197.
29. Burrows, R. 1966. Studies on the carrier state of cattle exposed to foot-and-mouth disease virus. J. Hyg. Camb. 64: 81 90.
30. Caggana, M.,, R. Chan,, and A. Ramsingh. 1993. Identification of a single amino acid residue in the capsid protein VP1 of coxsackievirus B4 that determines the virulent phenotype. J. Virol. 67: 4797 4803.
31. Campbell, I. L.,, A. Cutri,, D. Wilkinson,, A. W. Boyd,, and L. C. Harrison. 1989. Intracellular adhesion molecule 1 is induced on isolated endocrine islet cells by cytokines but not by reovirus infection. Proc. Natl. Acad. Sci. USA 86: 4282.
32. Cao, Y.,, and D. R Schnurr. 1988. Persistent infection ofYAC-1 cells by coxsackie virus B3. J. Gen. Virol. 69: 59 65.
33. Champsaur, H. F.,, G. F. Bottazzo,, J. Bertrams,, R. Assan,, and C. Bach. 1982. Virologic, immunologic, and genetic factors in insulin-dependent diabetes mellitus. J. Pediatr. 100: 15 20.
34. Chase, H. R.,, M. A. Voss,, N. Butler-Simon,, S. Hoops,, D. O'Brien,, and M.J. Doberson. 1987. Diagnosis ofpre-type 1 diabetes. J. Pediatr. 111: 807 812.
35. Chatterjee, N. K.,, J. Hou,, R. Dockstader,, and T. Charbonneau. 1992. Coxsackievirus B4 infection alters thymic, splenic, and peripheral lymphocyte repertoire preceding onset of hyperglycemia in mice. J. Med. Virol. 38: 124 131.
36. Chatterjee, N. K.,, C. Nejman,, and I. Gerling. 1988. Purification and characterization of a strain of coxsackievirus B4 of human origin that induces diabetes in mice. J. Med. Virol. 26: 57 69.
37. Christau, B.,, and A. G. Molbak. 1984. Further epidemiological evidence of a higher incidence level for the insulin-dependent diabetes mellitus in the older age groups. Acta Endocrinol. 95( Suppl. 263): 18.
38. Craighead, J. E.,, S. A. Huber,, and S. Sriram. 1990. Animal models of picornavirus-induced autoimmune disease: their possible relevance to human disease. Lab. Invest. 63: 432 446.
39. Craighead, J. E.,, and M. F. McLane. 1968. Diabetes mellitus: induction in mice by encephalomyocarditis virus. Science 162: 913 915
40. Craighead, J. E.,, and J. Steinke. 1969. Temporary diabetes in mice caused by encephalomyocarditis virus. Clin. Res. 17: 380.
41. Craighead, J. E.,, and J. Steinke. 1971. Diabetes mellitus-hke syndrome in mice infected with encephalomyocarditis virus. Am. J. Pathol. 63: 119 134.
42. Cudworth, A. G.,, D. R. Gamble,, G. B. B. White,, R. Lendrum,, J. C. Woodrow,, and A. Bloom. 1977. Aetiology of juvenile-onset diabetes: a prospective study. Lancet i: 385 388.
42a. Dahlquist, G., et al. Unpublished data.
43. D'Alessio, D.J. 1992. A case-control study of group B coxsackievirus immunoglobulin M antibody prevalence and HLA-DR antigens in newly diagnosed cases of insulin-dependent diabetes mellitus. Am.J. Epidemiol. 135: 1331 1338.
44. D'Andrea, B. J.,, G. L. Wilson,, and J. E. Craighead. 1981. Effect of genetic obesity in mice on the induction of diabetes by encephalomyocarditis virus. Diabetes 30: 451.
45. delaTorre, J. C.,, M. Davila,, E. Sobrino,, J. Ortin,, and E. Domingo. 1985. Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 145: 24 35.
46. Diabetes Epidemiology Research International Group. 1988. Geographic patterns of childhood insulin-dependent diabetes mellitus. Diabetes 37: 11131119.
47. Diabetes Epidemiology Research International Group. 1990. Secular trends in incidence of childhood IDDM in 10 countries. Diabetes 39: 858864.
48. Diepersloot, R. J. A.,, K. R Bouter,, W. E. R Beyer,, J. L. B. Hoekstra,, and N. Masurel. 1987. Humoral immune response and delayed type hypersensitivity to influenza vaccine in patients with diabetes mellitus. Diabetologia 30: 97100.
49. Dippe, S. E.,, R. H. Bennett,, M. Miller,, J. E. Maynard,, and K. R. Berquist. 1975. Lack of causal association between coxsackie B4 virus infection and diabetes. Lancet i: 1314 1317.
49a. Dorman, J. S. 1993. Personal communication.
50. Dronfield, D. M. 1993. Changes in serum insulin and islet cell antibodies following an outbreak of echovirus 4 in Glasgow. Diabetic Med. 10( Suppl. 1): S41.
51. Durruty, O.,, E. Ruiz,, and M. Garcia de los Rios. 1979. Age at diagnosis and seasonal variation in the onset of insulin-dependent diabetes in Chile (southern hemisphere). Diabetologia 17: 357 360.
52. Eberhardt, M. S.,, D. K. Wagener,, T. J. Orchard,, R. E. LaPorte,, D. E. Cavender,, B. S. Rabin,, R. W. Atchison,, L. H. Kuller,, A. L. Drash,, and D. J. Becker. 1985. HLA heterogeneity of insulin-dependent diabetes mellitus at diagnosis. The Pittsburgh IDDM Study. Diabetes 34: 1247 1252.
53. Elias D.,, H. Prigozin,, N. Polak,, M. Rapoport,, A. W. Lohse,, and I. R. Cohen. 1994. Autoimmune diabetes induced by the β cell toxin STZ. Immunity to the 60-kDa heat shock protein and to insulin. Diabetes 43: 992 998.
54. Erdo, S. L.,, and J. R. Wolff. 1990. Gamma-aminobutyric acid outside the mammalian brain. J. Neurochem. 54: 363 372.
55. Fohlman, J.,, J. Bohme,, L. Rask,, G. Frisk,, H. Diderholm,, G. Friman,, and T. Tuvemo. 1987. Matching of host genotype and serotypes of coxsackie B virus in the development of juvenile diabetes. Scand.J. Immunol. 26: 105 110.
56. Forrest, J. M.,, M. A. Menser,, and J. A. Burgess. 1971. High frequency of diabetes mellitus in young adults with congenital rubella. Lancet ii: 332 334.
57. Foulis, A. K.,, M. A. Farquharson,, S. O. Cameron,, M. McGill, Schonke, and R. Kandolf. 1990. A search for the presence of the enteroviral capsid protein VP1 in pancreases of patients with type 1 (insulin-dependent) diabetes of coxsackieviral myocarditis. Diabetologia 33: 290 298.
58. Foulis, A. K.,, M. A. Farquharson,, and R. Hardman. 1987. Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 30: 333 343.
59. Foulis, A. K.,, M. A. Farquharson,, and A. Meager. 1987. Immunoreactive a-interferon in insulin-secreting β cells in type 1 diabetes mellitus. Lancet ii: 1423 1427.
60. Foulis, A. K.,, C. N. Liddle,, M. A. Farquharson,, J. A. Richmond,, and R. S. Weir. 1986. The histopathology of the pancreas in type 1 (insulin-dependent) diabetes mellitus: a 25-year review of death in patients under 20 years of age in the United Kingdom. Diabetologia 20: 267 274.
61. Foulis, A. K.,, N. D. Francis,, M. A. Farquaharson,, and A. Boylson. 1986. Massive synchronous B-cell necrosis causing type 1 (insulin-dependent) diabetes—a unique histopathological case report. Diabetologia 31: 46 50.
62. Friedman, A.,, and Y. Lorch. 1985. Theiler's virus infection: a model for multiple sclerosis. Prog. Med. Virol. 31: 43 48.
63. Friman, G.,, J. Fohlman,, G. Frisk,, H. Diderholm,, U. Ewald,, M. Kobbah,, and T. Tuvemo. 1985. An incidence peak of juvenile diabetes. Relation to coxsackie B virus immune response. Acta Paediatr. Scand. ( Suppl. 320): 14 19.
64. Frisk, G.,, J. Fohlman,, M. Kobbah,, U. Ewald,, T. Tuvemo,, H. Diderholm,, and G. Friman. 1985. High frequency of coxackie-B-virus specific IgM in children developing type I diabetes during a period of high diabetes morbidity. J Med. Virol. 17: 219 227.
65. Frisk, G.,, G. Friman,, T. Tuvemo,, J. Fohlman,, and H. Diderholm. 1992. 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 35: 249 253.
66. Froeschle, J. E.,, P. M. Feorino,, and H. M. Gelfand. 1966. A continuing surveillance of enterovirus infection in healthy children in six U.S. cities. II. Surveillance enterovirus isolates 1960-1963 and comparison with enterovirus isolates from cases of acute central nervous system disease. Am. J. Epidemiol. 83: 455 469.
67. Gamble, D. R. 1980. The epidemiology of insulin-dependent diabetes with particular reference to the relationship of virus infection to its etiology. Epidemiol. Rev. 2: 49 70.
68. Gamble, D.R.,, and H. Cumming. 1985. Coxsackie B virus and juvenile-onset insulin-dependent diabetes. Lancet ii: 455 456.
69. Gamble, D. R.,, M. L. Kingsley,, M. G. Fitzgerald,, R. Bolton,, and K. W. Taylor. 1969. Viral antibodies in diabetes mellitus. Br. Med. J. 3: 627 630.
70. Gamble, D. R.,, and K.W. Taylor. 1969. Seasonal incidence of diabetes mellitus. Br. Med. J. 3: 631 633.
71. Garchon, H.-J.,, P. Bedossa,, L. Eloy,, and J. -E Bach. 1991. Identification and mapping to chromosome 1 of a susceptibility locus for periinsulitis in non-obese diabetic mice. Nature (London) 353: 260 262.
72. Garry, D. J.,, H. D. Coulter,, M. G. Garry,, and R. L. Sorenson. 1988. Immunoreactive immunolocalization of L-glutamate decarboxylase in rat pancreatic islets. J. Histochem. Cytochem. 36: 573 580.
73. Gepts, W. 1965. Pathologic anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 14: 619 633.
74. Gerling, I.,, and N. K. Chatterjee. 1993. Lack of 64,000-M t islet autoantigen overexpression and antibody development following coxsackievirus B4 infection in diabetes-resistant mice. Autoimmunity 14: 197 203.
75. Gerling, I.,, C. Nejman,, and N. K. Chatterjee. 1988. Effect of coxsackievirus B4 infection in mice on expression of 64,000-Mr autoantigen and glucose sensitivity of islets before development of hyperglycemia. Diabetes 37: 1419 1425.
76. Ginsberg-Fellner, F.,, M. E. Witt,, S. Yagihashi,, M. J. Dobersen,, F. Taub,, B. Fedun,, R. C. McEvoy,, S. H. Roman,, R. G. Davies,, L. Z. Cooper, et al. 1984. Congenital rubella syndrome as a model for type 1 (insulin-dependent) diabetes mellitus: increased prevalence of islet cell surface antibodies. Diabetologia 27( Suppl. l): 87 89.
77. Giron, D. J.,, and S. Yei. 1993. Interference by a non-interferon-inducing subvariant of benign encephalomyelitis virus-B with the ability of EMCV-D to produce insulin-dependent diabetes mellitus in IRC Swiss male mice. J. Interferon Res. 13: 363 368.
78. Gladish, R.,, W. Hofmann,, and R. Waldherr. 1976. Myocarditis and insulitis in coxsackievirus infection. Z. Kardiol. 65: 835 849.
79. Gleason, R. E.,, C. B. Kahn,, I. B. Funk,, and J. E. Craighead. 1982. Seasonal incidence of insulin-dependent diabetes in Massachusetts, 1964-1973. Int. J. Epidemiol. 11: 39 45.
80. Gould, C. L.,, K. G. McMannama,, N. J. Bigley,, and D. J. Giron. 1985. Virus-induced murine diabetes: enhancement by immunosuppression. Diabetes 34: 1217 1221.
81. Greve, J. M.,, G. Davis,, A. M. Meyer,, C. P. Forte,, S. C. Yost,, C. W. Marlor,, M. E. Kamarck,, and A. McClelland. 1989. The major human rhinovirus receptor is ICAM-1. Cell 56: 839.
82. Groop, L. C.,, F. B. Bottazzo,, and D. Doniach. 1986. Islet cell antibodies identify latent type I diabetes in patients aged 35-75 at diagnosis. Diabetes 35: 237 241.
83. Hagopian, W. A.,, S. McGrew,, S. B. Kaliappan,, A. E. Karlsen,, and D. J. D'Allessio. 1993. Recent coxsackie B virus infection associates with glutamic acid decarboxylase autoantibodies (GAD65 Ab) regardless of insulin-dependent diabetes (IDDM) status. Am. Diabetes Assoc. 12th Int. Immunol. Diabetes Workshop.
84. Hamby, B. B.,, M. A. Pallansch,, and O. M. Kew. 1987. Reemergence of an epidemic coxsackievirus B5 genotype. J. Infect. Dis. 156: 288 292.
85. Harrison, L. C.,, M. G. Honeymoon,, H. J. DeAizpurua,, R. S. Schmidli,, P. G. Colman,, B. D. Tait,, and D. S. Cram. 1993. Inverse relation between humoral and cellular immunity to glutamic acid decarboxylase in subjects at risk of insulin-dependent diabetes. Lancet 341: 1365 1369.
86. Hartig, P. C.,, G. E. Madge,, and S. R. Webb. 1983. Diversity within a human isolate of coxsackie B4: relationship to viral-induced diabetes. J. Med. Virol. 11: 23 30.
87. Haskins, K.,, and M. McDuffie. 1990. Acceleration of diabetes in young NOD mice with a CD4 + islet-specific T cell clone. Science 249: 1433 1436.
88. Hayashi, K.,, D. W. Boucher,, and A. L. Notkins. 1974. Virus-induced diabetes mellitus. II. Relationship between β-cell damage and hyperglycemia in mice infected with encephalomyocarditis virus. Am. J. Pathol. 75: 91 102.
89. Hay ward, J. C.,, S. M. Gillespie,, K. M. Kaplan,, R. Packer,, M. Pallansch,, S. Plotkin,, and L. B. Schonberger. 1989. Outbreak of poliomyelitis-like paralysis associated with enterovirus 71. Pediatr. Infect. Dis. 8: 611 616.
90. Helfand, R. E.,, H. Gary,, C. Freeman,, L. Anderson,, Pittsburgh Diabetes Research Group, and M. Pallansch. 1994. Association between enteroviruses and type 1 diabetes mellitus, Pittsburgh, Pennsylvania. Colo. Dis. Bull. 21: 4.
91. Hellqvist, L. N. B.,, K. W. Taylor,, and S. Zaluzny. 1981. Selective disorganisation of biochemical function in B cells of islets of Langerhans infected by EMC-M virus in tissue culture. FEBS Lett. 132: 215 218.
92. Helmke, K., 1987. In Y. Becker (ed.), Virus Infections and Diabetes Mellitus, p. 127 142. Matinus Nijhoff Publishing, Boston.
93. Hierholzer, J. C.,, and W. A. Farris. 1974. Follow-up of children infected in a coxsackievirus B3 and B4 outbreak: no evidence of diabetes mellitus. J. Infect. Dis. 129: 741 746.
94. Hou, J.,, S. Sheikh,, D. L. Martin,, and N. K. Chatterjee. 1993. Coxsackie virus B4 alters pancreatic glutamate decarboxylase expression in mice soon after infection. J. Autoimmun. 6: 529 542.
95. Huff, J. C.,, J. C. Hierholzer,, and W. A. Farris. 1974. An "outbreak" of juvenile diabetes mellitus: consideration of a viral etiology. Am. J. Epidemiol. 100: 277 287.
95a. Hyoty, H., et al. Unpublished data.
96. Hyoty, H.,, M. Hiltunen,, A. Reunanen, et al. 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. Diabetologia 36: 1303 1308.
97. Hyoty, H.,, L. Rasanen,, M. Hiltunen,, M. Lehtinen,, T. Huupponen,, and P. Leinikki. 1991. Decreased antibody reactivity to Epstein-Barr virus capsid antigen in type 1 (insulin-dependent) diabetes mellitus. APMIS 99: 359 363.
98. Ihm, S. H.,, K. U. Lee,, R. G. McArthur,, and J. W. Yoon. 1990. Predisposing effect of anti-?-cell autoimmune process in NOD mice on the induction of diabetes by environmental insults. Diabetologia 33: 709 712.
99. Japan, Poland, the Netherlands and Pittsburgh Childhood Diabetes Research Groups. 1990. How frequently do children die at the onset of insulin-dependent diabetes? Analyses of registry data from Japan, Poland, the Netherlands and Allegheny County, Pennsylvania. Diabetes Nutr. Metab. 3: 5762.
100. Jenson, A. B.,, H. S. Rosenberg,, and A. L. Notkins. 1980. Pancreatic islet-cell damage in children with fatal viral infections. Lancet ii: 354 358.
101. Johnston, C.,, B. A. Millward,, P. Hoskins,, R. D. Leslie,, G. F. Bottazzo,, and D. A. Pyke. 1989. Islet-cell antibodies as predictors of the later development of type 1 (insulin-dependent) diabetes. A study in identical twins. Diabetologia 32: 382 386.
102. Joner, G.,, and O. Sovik. 1991. The incidence of type 1 (insulin-dependent) diabetes mellitus 15-29 years in Norway 1978-1982. Diabetologia 34: 271 274.
103. Jones, D. B.,, P. J. McLaughlin,, N. Armstrong,, M. Yeung,, and A. Coulson. 1992. Does coxsackie B4 virus infection induce GAD and HSP65 autoreactivity in type 1 diabetes? Diabetic Med. 9( Suppl. 2): 524A.
104. Rang, Y.,, and J. W. Yoon. 1993. A genetically determined host factor controlling susceptibility to encephalomyocarditis virus-induced diabetes in mice. J Gen. Virol. 74: 1207 1213.
105. Kaptur, P. E.,, D. C. Thomas,, and D. J. Giron. 1989. Differing attachment of diabetogenic and nondiabetogenic variants of encephalomyocarditis virus to β-cells. Diabetes 38: 1103 1108.
106. Karjalainen, J. K. 1990. Islet cell antibodies as predictive markers for IDDM in children with high background incidence of disease. Diabetes 39: 1144 1150.
107. Karounos, D. G.,, J. S. Wolinsky,, and J. W. Thomas. 1993. Monoclonal antibody to rubella virus capsid protein recognizes a beta-cell antigen. J. Immunol. 150: 3080 3085.
108. Kaufman, D. L.,, M. Clare-Salzler,, J. Tian,, T. Forsthuber,, G. S. P. Ting,, P. Robinson,, M. A. Atkinson,, E. E. Sercarz,, A. J. Tobin,, and P. V. Lehmann. 1993. Spontaneous loss of T cell self tolerance to glutamate decarboxylase is a key event in the pathogenesis of murine insulin-dependent diabetes. Nature (London) 366: 69 72.
109. Kaufman, D. L.,, M. G. Erlander,, M. Clare-Salzler,, M. A. Atkinson,, N. K. Maclaren,, and A. J. Tobin. 1992. Autoimmunity to two forms of glutamate decarboxylase in insulin dependent diabetes mellitus. J. Clin. Invest. 89: 283 292.
110. Khoury, M. J.,, W. D. Flanders,, S. Greenland,, and M.J. Adams. 1989. On the measurement of susceptibility in epidemiologic studies. Am. J. Epidemiol. 129: 183 190.
111. Kim, J. W.,, W. Richter,, H. J. Aanstoot,, Y. Shi,, Q. Fu,, R. Rajotte,, G. Warnock,, and S. Baekkeskov. 1993. Differential expression of GAD65 and GAD67 in human, rat, and mouse pancreatic islets. Diabetes 42: 1799 1808.
112. King, M. L.,, D. Bidwell,, A. Voller,, J. Bryant,, and J. E. Banatvala. 1983. Role of coxsackie B viruses in insulin-dependent diabetes mellitus. Lancet ii: 915 916.
113. Kogon, A.,, I. Spigland,, T. E. Frothingham,, L. Elveback,, C. Williams,, C. E. Hall,, and J. P. Fox. 1969. The virus watch program: a continuing surveillance of viral infections in metropolitan New York families. VII. Observations on viral excretion, seroimmunity, intrafamiliar spread and illness association in coxsackie and echovirus infections. Am. J. Epidemiol. 89: 51 61.
114. Kostraba, J. N.,, E. C. Gay,, Y. Cai,, K. J. Cruickshanks,, M. J. Rewers,, G. J. Klingensmith,, H. P. Chase,, and R. F. Hamman. 1992. Incidence of insulin-dependent diabetes mellitus in Colorado. Epidemiology 3: 232 238.
115. Lampeter, E. F.,, I. Seifert,, D. Lohmann,, J. W. Heise,, J. Bertrams,, M. R. Christie, V Kolb-Bachofen, and H. Kolb. 1994. Inflammatory islet damage in patients bearing HLA-DR3 and/or DR4 haplotypes does not lead to islet autoimmunity. Diabetologia 37: 471 475.
116. Landin-Olsson, M.,, A. Karlsson,, G. Dahlquist,, L. Blom,, A. Lernmark,, and G. Sundkvist. 1989. Islet cell and other organ specific autoantibodies in all children developing type 1 (insulin-dependent) diabetes mellitus in Sweden during one year and in matched control children. Diabetologia 32: 387 395.
117. Lederman, M. M.,, G. Schifman,, and H. M. Rodman. 1981. Pneumococcal immunisation in adult diabetics. Diabetes 30: 119 121.
118. Lemon, S. M.,, P. C. Murphy,, P. A. Shields,, L. Ping,, S. M. Feinstone,, T. Cromeans,,and R.W. Jansen. 1991. Antigenic and genetic variation in cy topathic hepatitis A virus variants arising during persistent infection: Evidence for genetic recombination. J. Virol. 65: 2056 2065.
119. Lennette, E. H.,, T. T. Shinomoto,, N. J. Schmidt,, and R. L. Magoffin. 1960. Observations on the neutralizing antibody response to group B coxsackie viruses in patients with central nervous system disease. J. Immunol. 86: 257 266.
120. Levy-Marchal, C.,, J. Tichet,, I. Fajardy,, E. Dubois,, and P. Czernichow. 1992. Follow-up of children from a background population with high ICA titres. Diabetologia 35( Suppl. 1): A32.
121. Libman, I.,, T. Songer,, and R. LaPorte. 1993. How many people in the U.S. have IDDM? Diabetes Care 16: 841 842.
122. Like, A. A.,, D. L. Guberski,, and L. Butler. 1991. Influence of environmental viral agents on frequency and tempo of diabetes mellitus in BB/Wor rats. Diabetes 40: 259 262.
123. Loria, R. M.,, L. B. Montgomery,, L. Corey,, and V. M. Chinchilli. 1984. Influence of diabetes mellitus heredity on susceptibility to Coxsackie virus B4. Arch. Virol. 81: 251 262.
124. Lowis, G. W. 1988. Ethnic factors in multiple sclerosis: a review and critique of the epidemiological literature. Int. J. Epidemiol. 17: 14 20.
125. Ludvigsson, J.,, and A. O. Afoke. 1989. Seasonality of type 1 (insulin-dependent) diabetes mellitus: values of C-peptide, insulin antibodies and haemoglobin A lc show evidence of a more rapid loss of insulin secretion in epidemic patients. Diabetologia 32: 84 91.
126. Maclaren, N.,, G. Home,, R. Spillar,, L. Brown,, J. Silverstein,, S. Shah,, J. Malone,, and W. Riley. 1990. The feasibility of using ICA to predict IDD in U.S. school children. Diabetes 39( Suppl. 1): 122A.
127. Maeda, T.,, T. Sumida,, K. Kurosawa,, H. Tomioka,, I. Itoh,, S. Yoshida,, and T. Koike. 1991. T-lymphocyte receptor repertoire of infiltrating T-lymphocytes into NOD mouse pancreas. Diabetes 40: 1580 1585.
128. Matteucci, D.,, M. Paglianti,, A. M. Giangregorio,, M. R. Capobianchi,, F. Dianzani,, and M. Bendinelli. 1985. Group B coxsackieviruses readily establish persistent infections in human lymphoid cell lines. J. Virol. 56: 651 654.
128a. McDevitt, H., et al. Unpublished observation.
129. McDuffie, M.,, and A. Ostrowska. 1993. Superantigen-like effects and incidence of diabetes in NOD mice. Diabetes 42: 1094 1098.
130. McKinney, R. E.,, S. L. Katz,, and C. M. Wilfert. 1987. Chronic enteroviral meningoencephalitis in agammaglobulinemic patients. Rev. Infect. Dis. 9: 334 356.
131. Melton, J. L., et al. 1983. Incidence of diabetes mellitus by clinical type. Diabetes Care 6: 75 86.
132. Mendelsohn, C. L.,, E. Wirtuner,, and V. R. Racaniello. 1989. Cellular receptor for polio-virus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56: 855.
133. Menser, M. A.,, J. M. Forrest,, and R.D. Bransby. 1978. Rubella infection and diabetes mellitus. Lancet i: 57 60.
134. Modlin, J. R.,, and M. Bowman. 1987. Perinatal transmission of coxsackievirus B3 in mice. J. Infect. Dis. 156: 21 25.
135. Monif, G. R. G.,, G. B. Avery,, S. B. Korones,, and J. L. Sever. 1965. Post-mortem isolation of rubella virus from three children with rubella-syndrome defects. Lancet i: 723 724.
136. Montgomery, L.,, D. Gordon,, K. George,, and E. Maratos-Flier. 1991. Coxsackie infection of insulinoma cells leads to viral latency and altered insulin and class I MHC expression. Diabetes 40( Suppl. 1): 150A.
137. Montgomery, L. B.,, R. M. Loria,, and V. M. Chinchilli. 1990. Immunodeficiency as primary phenotype of diabetes mutation db: studies with coxsackievirus B4. Diabetes 39: 675 682.
138. Morrow, P. L.,, A. Freedman,, and J. E. Craighead. 1980. Testosterone effect on experimental mellitus in encephalomyocarditis (EMC) virus-infected mice. Diabetologia 18: 247.
139. Nakano, N.,, H. Kikutani,, H. Nishimoto,, and T. Kishimoto. 1991. T cell receptor V gene usage of islet β cell-reactive T cells is not restricted in non-obese diabetic mice. J. Exp. Med. 173: 1091 1097.
140. Nathanson, N.,, and J. Martin. 1979. The epidemiology of poliomyelitis: enigmas surrounding its appearance, epidemicity and disappearance. Am. J. Epidemiol. 110: 672 692.
141. Nicoletti, E.,, G. Scalia,, M. Lunetta,, F. Concorelli,, M. Di Mauro,, W. Barcellini,, S. Stracuzzi,, M. Pagano,, and P. L. Meroni. 1990. Correlation between islet cell antibodies and anti-cytomegalovirus IgM and IgG antibodies in healthy first-degree relatives of type 1 (insulin-dependent) diabetic patients. Clin. Immunol. Immunopathol. 55: 139 147.
142. Niklasson, B. S.,, M. J. Dobersen,, C. J. Peters,, W. H. Ennis,, and E. Mdller. 1985. An outbreak of coxsackievirus B infection followed by one case of diabetes mellitus. Scand. J. Infect. Dis. 17: 15 18.
142a. Norris, J. M., et al. Unpublished observations.
143. Notkins, A. L.,, T. Onodera,, and B. S. Prabhakar,. 1984. Virus-induced autoimmunity, p. 210 215. In A. L. Notkins (ed.), Concepts in Viral Pathogenesis. Springer, New York.
144. Notkins, A. L.,, and J. W. Yoon. 1982. Virus-induced diabetes in mice prevented by a live attenuated vaccine. N. Engl. J. Med. 1: 486.
145. Nystrom, L.,, G. Dahlquist,, M. Rewers,, and S. Wall. 1990. The Swedish Childhood Diabetes Study: an analysis of the temporal variation in diabetes incidence 1978-1987. Int. J. Epidemiol. 19: 141 146.
146. Ohashi, P. S.,, S. Oehen,, P. Aichele,, H. Pricher,, B. Odermatt,, P. Herrera,, Y. Higuchi,, K. Buerki,, H. Hengartner,, and R. M. Zinkernagel. 1993. Induction of diabetes is influenced by the infectious virus and local expression of MHC class I and tumor necrosis factor-a J. Immunol. 150: 5185 5194.
147. Ohashi, P. S.,, S. Oehen,, K. Buerki,, H. Pircher,, C. T. Ohashi,, B. Odermatt,, B. Malissen,, R. M. Zinkernagel,, and H. Hengartner. 1991. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65: 305 317.
148. Oksenberg, J. R.,, S. Stuart,, A. B. Begovich,, R. B. Bell,, H. A. Erlich,, L. Steinman,, and C. C. A. Bernard. 1990. Limited heterogeneity of rearranged T-cell receptor Va transcripts in brains of multiple sclerosis patients. Nature (London) 345: 344 346.
149. Oldstone, M. B. A. 1987. Molecular mimicry and autoimmune disease. Cell 50: 819 820.
150. Oldstone, M. B. A. 1988. Prevention of type 1 diabetes in nonobese diabetic mice by virus infection. Science 239: 500 502.
151. Oldstone, M. B. A. 1990. Viruses as therapeutic agents. I. Treatment of nonobese insulin-dependent diabetes mice with virus prevents insulin-dependent diabetes mellitus while maintaining general immune competence. J. Exp. Med. 171: 2077 2089.
152. Oldstone, M. B. A.,, M. Nerenberg,, P. Southern,, J. Price,, and H. Lewicki. 1991. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 65: 319 331.
153. Oldstone, M. B. A.,, P. Southern,, M. Rodriguez,, and P. W. Lampert. 1984. Virus persists in beta-cells and islets of Langerhans and is associated with chemical manifestation of diabetes. Science 224: 1440 1444.
154. O'Leary, L. A.,, J. S. Dorman,, R. E. LaPorte,, T. J. Orchard,, D. J. Becker,, L. H. Kuller,, M. S. Eberhardt,, D. E. Cavender,, B. S. Rabin,, and A. L. Drash. 1991. Familial and sporadic insulin-dependent diabetes: evidence for heterogeneous etiologies? Diabetes Res. Clin. Pract. 14: 183 190.
155. Onodera, T.,, A. Toniolo,, U. R. Ray,, A. A. Jenson,, R. A. Knazek,, and A. L. Notkins. 1981. Virus-induced diabetes mellitus. XX. Polyendocrinopathy and autoimmunity. J. Exp. Med. 153: 1547 1573.
156. Onodera, T.,, J. W. Yoon,, K. K. Brown,, and A. L. Notkins. 1978. Evidence for a single locus controlling susceptibility to virus-induced diabetes mellitus. Nature (London) 274: 693 696.
157. Orchard, T. J.,, R. W. Atchison,, D. Becker,, B. Rabin,, M. Eberhardt,, L. H. Kuller,, R. E. LaPorte,, and D. Cavender. 1983. Coxsackie infection and diabetes. Lancet ii: 631. ( Letter.)
158. Orchard, T. J.,, D. J. Becker,, R. W. Atchison,, R. E. LaPorte,, D. K. Wagener,, B. S. Rabin,, L. H. Kuller,, and A. L. Drash. 1983. The development of type 1 (insulin-dependent) diabetes mellitus: two contrasting presentations. Diabetologia 25: 89 92.
159. Owerbach, D.,, and K. H. Gabbay. 1993. Localization of a type 1 diabetes susceptibility locus to the variable tandem repeat region flanking the insulin gene. Diabetes 42: 1708 1714.
160. Pacsa, S.,, and J. Werblinska. 1971. Natural immunity of Ghanaian children to polio and coxsackievirus: brief report. Arch. Gesamte Virusforsch. 33: 192 193.
161. Pak, C. Y.,, E. Hyone-Myong,, R. G. McArthur,, and J. W. Yoon. 1988. Association of cytomegalovirus infection with autoimmune type 1 diabetes. Lancet ii: 1 3.
162. Paliard, X.,, S. G. West,, J. A. Lafferty,, J. R. Clements,, J. W. Kappler,, P. Marrack,, and B. L. Kotzin. 1991. Evidence for the effects of a superantigen in rheumatoid arthritis. Science 253: 325 329.
163. Palmer, J. P.,, M. K. Cooney,, R. H. Ward,, J. A. Hansen,, J. B. Brodsky,, C. G. Ray,, J. R. Crossley,, C. M. Asplin,, and R. H. Williams. 1982. Reduced coxsackie antibody titres in type I (insulin-dependent) diabetic patients presenting during an outbreak of coxsackie B3 and B4 infection. Diabetologia 22: 426 429.
164. Petersen, K.-G.,, P. Heilmeyer,, and L. Kerp. 1975. Synthesis of proinsulin and large glucagon immunoreactivity in isolated islets of Langerhans from EMC virus infected mice. Diabetologia 11: 21 25.
165. Peterson, J. S.,, S. Russel,, M. O. Marshall,, H. Kofod,, K. Buschard,, A. E. Cambon,, A. E. Karlsen,, E. Boel,, W. A. Hagopian,, K. R. Hejnaes,, A. Moody,, T. Dyrberg,, A. E. Lernmark,, O. D. Madsen,, and B. K. Michelsen. 1993. Differential expression of glutamate decarboxylase in rat and human islets. Diabetes 42: 484 495.
166. Pietropaolo, M.,, and G. S. Eisenbarth. 1994. Biochemical determination of antibodies to three recombinant human autoantigens: high predictive value and stability of patterns. Diabetes 43( Suppl. 1): 153A.
167. Pilcher, C. C.,, K. Dickens,, and R. B. Elliott. 1991. ICA only develop in early childhood. Diabetes Res. Clin. Pract. 14( Suppl. I): s82.
168. Pipeleers, D.,, and Z. Ling. 1992. Pancreatic beta cells in insulin-dependent diabetes. Diabetes Metab. Rev. 8: 209 227.
169. Pociot, E.,, R. Bergholdt,, J. Johannsen,, and J. Nerup. 1994. Genetic susceptibility to IDDM: chromosome 6p versus chromosome 2q. Diabetologia 37( Suppl. 1): A6.
170. Portwood, N. D.,, and K. W. Taylor. 1990. Coxsackie B4 virus-induced changes in mouse pancreatic β-cell mRNAs. Biochem. Soc. Trans. 18: 1264.
171. Pozzilli, P.,, P. Arduini,, N. Visalli, et al. 1987. Reduced protection against hepatitis B virus following vaccination in patients with type I (insulin dependent) diabetes. Diabetologia 30: 817 819.
172. Prabhakar, B. S.,, M. V. Haspel,, P. R. McClintock,, and A. L. Notkins. 1982. High frequency of antigenic variants among naturally occurring human coxsackie B4 virus isolates identified by monoclonal antibodies. Nature (London) 300: 374 376.
173. Prather, S. L.,, R. Dagan,, J. A. Jenista,, and M. A. Menegus. 1984. The isolation of enteroviruses from blood: a comparison of four processing methods. J. Med. Virol. 14: 221 227.
174. Ramsingh, A.,, J. Slack,, J. Silkworth,, and A. Hixson. 1989. Severity of disease induced by a pancreatropic coxsackie B4 virus correlates with the H-2Kq locus of the major histocompatibility complex. Virus Res. 14: 347 358.
175. Ratzmann, K. P.,, J. Strese,, S. Witt,, H. Berling,, H. Kielacker,, and D. Michaelis. 1984. Mumps infection and insulin-dependent diabetes mellitus (IDDM). Diabetes Care 7: 170 173.
176. Rayfield, E. J.,, and K. Ishimura. 1987. Environmental factors and insulin dependent diabetes mellitus. Diabetes Metab. Rev. 3: 925 957.
177. Rewers, M.,, R. E. LaPorte,, H. King,, and J. Tuomilehto. 1988. Trends in the prevalence and incidence of diabetes: insulin-dependent diabetes mellitus in childhood. World Health Stat. Q. 41: 179 189.
178. Rewers, M.,, R. LaPorte,, M. Walczak,, K. Dmochowski,, and E. Bogaczynska. 1987. Apparent epidemic of insulin-dependent diabetes mellitus in midwestern Poland. Diabetes 36: 106 113.
179. Rewers, M.,, M. A. Pallansch,, E. Bogaczynska,, S. L. Patrick,, L. A. Anderson,, M. Walczak,, and R. E. LaPorte. 1990. Conflicting evidence for enterovirus as the cause of childhood diabetes epidemic in Poland. Diabetologia 33( Suppl. 1): A198.
180. Richter, W.,, T. Mertens,, B. Schoel,, S. Wolfahrt,, P. Muir,, W. A. Scherbaum,, and B. O. Boehm. 1994. Autoantibodies to glutamate decarboxylase detect no molecular mimicry to viral antigens or heat shock protein 60. Diabetologia 37( Suppl. 1): A63.
181. Riley, W. J.,, N. K. MacLaren,, J. Krischer,, R. P. Spillar,, J. H. Silverstein,, D. A. Schatz,, S. Schwartz,, J. Malone,, S. Shah,, C. Vadheim,, and J. I. Rotter. 1990. A prospective study of the development of diabetes in relatives of patients with insulin-dependent diabetes. N. Engl. J. Med. 323: 1167 1172.
182. Rose, N. R.,, and D. E. Griffin,. 1991. Virus-induced autoimmunity, p. 247 272. In N. Talal (ed.), Molecular Autoimmunity. Academic Press Ltd., London.
183. Rossmann, M. G.,, and A. C. Palmenberg. 1988. Conservation of the putative receptor attachment site in picornaviruses. Virology 164: 373 382.
184. Rotbart, H. A. 1991. Nucleic acid detection systems for enteroviruses. Clin. Microbiol. Rev. 4: 156 168.
185. Sairenji, T.,, M. Daibata,, C. H. Sorli, et al. 1991. Relating homology between the Epstein-Barr virus BOLF1 and HLA-DQw8 beta chain to recent onset type 1-dependent diabetes mellitus. Diabetologia 34: 33 39.
186. Salvato, M.,, P. Borrow,, E. Shimomaye,, and M. B. A. Oldstone. 1991. Molecular basis of viral persistence: a single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic T-lymphocytep response and establishment of persistence. J Virol. 65: 1863 1869.
187. Santamaria, P.,, C. Lewis,, J. Jessurun,, D. E. Sutherland,, and J.J. Barbosa. 1994. Skewed T-cell receptor usage junctional and heterogeneity among isletitis αβ and γσ T-cells in human IDDM. Diabetes 43: 599 606.
188. Santamaria, P.,, R. E. Nakhleh,, D. E. Sutherland,, and J. J. Barbosa. 1992. Char-acterization of T lymphocytes infiltrating human pancreas allograft affected by isletitis and recurrent diabetes. Diabetes 41: 53 61.
189. Scherbaum, W. A.,, W. Hampl,, P. Muir,, M. Gluck,, J. SeiBler,, H. Egle,, H. Hauner,, B. O. Boehm,, E. Heinze,, J. E. Banatvala,, and E. E Pfeiffer. 1991. No association between islet cell antibodies and coxsackie B, mumps, rubella and cytomegalovirus antibodies in non-diabetic individuals aged 7-19 years. Diabetologia 34: 835 838.
190. Schernthaner, G.,, J. E. Banatvala,, W. Scherbaum,, J. Bryant,, M. Borkenstein,, E. Schober,, and W. R. Mayr. 1985. Coxsackie B virus specific IgM responses, complement-fixing islet cell antibodies, HLA DR antigens, and C-peptide secretion in insulin-dependent diabetes mellitus. Lancet ii: 630 632.
191. See, D. M.,, and J. G. Tilles. 1993. WIN 54954 treatment of mice infected with a diabetogenic strain of group B coxsackievirus. Antimicrob. Agents Chemother. 37: 1593 1598.
192. Sharief, M. K.,, R. Hentges,, and M. Ciardi. 1991. Intrathecal immune response in patients with the post-polio syndrome. N. Engl. J. Med. 325: 749 755.
193. Songer, T. J. 1990. Health services and costing in diabetes. Med.J.Aust. 152: 115 117.
194. Spinas, G. A.,, L. Matter,, T. Wilkin,, O. StafFelbach,, and W. Berger. 1988. Islet-cell and insulin autoantibodies in first-degree relatives of type I diabetics: a 5-year follow-up study in a Swiss population. Adv. Exp. Med. Biol. 246: 209 214.
195. Stanway, G. 1990. Structure, function and evolution of picornaviruses. J. Gen. Virol. 71: 2483 2501.
196. Staunton, D. E.,, V. J. Merluzzi,, R. Rothlein,, R. Barton,, S. D. Martin,, and T. A. Springer. 1989. A cell adhesion molecule, IAMC-1, is the major surface receptor for rhinoviruses. Cell 56: 849.
197. Suenaga, K.,, and J. W. Yoon. 1988. Association of beta-cell-specific expression of endogenous retrovirus with development of insulitis and diabetes in NOD mouse. Diabetes 37: 1722 1726.
198. Sussman, M. L.,, L. Stauss,, and U. L. Hodes. 1959. Fatal coxsackie B virus infections in the newborn. Report of case with necropsy findings and brief review of the literature. Am. J. Dis. Child. 97: 483 492.
199. Szopa, T. M.,, D. M. Dronfield,, T. Ward,, and K.W. Taylor. 1989. In vivo infection of mice with coxsackie B4 virus induces long-term functional changes in pancreatic islets with minimal alteration in blood glucose. Diabetic Med. 6: 314 319.
200. Szopa, T. M.,, D. R. Gamble,, and K. W. Taylor. 1986. Coxsackie B4 virus induces short-term changes in the metabolic functions of mouse pancreatic islets in vitro. Cell Biochem. Fund. 4: 181 189.
201. Szopa, T. M.,, P. A. Titchener,, N. D. Portwood,, and K. W. Taylor. 1993. Diabetes mellitus due to viruses—some recent developments. Diabetologia 36: 687 695.
202. Szopa, T. M.,, T. Ward,, D. M. Dronfield,, N. D. Portwood,, and K. W. Taylor. 1990. Coxsackie B4 viruses with the potential to damage β-cells of the islets are present in clinical isolates. Diabetologia 33: 325 328.
203. Szopa, T. M.,, T. Ward,, and K. W. Taylor. 1992. Disturbance of mouse pancreatic β-cell function following echo 4 virus infection. Biochem. Soc. Trans. 20: 3155.
204. Thivolet, C.,, B. Beaufrere,, H. Betuel,, L. Gebuhrer,, P. Chatelain,, A. Durand,, J. Tourniaire,, and R. Francois. 1988. Islet cell and insulin autoantibodies in subjects at high risk for development of type 1 (insulin-dependent) diabetes mellitus: the Lyon family study. Diabetologia 31: 741 746.
204a. Tian, J., et al. Submitted for publication.
205. Tilzey, A. J.,, M. Signy,, and J. E. Banatvala. 1986. Persistent coxsackie B virus specific IgM response in patients with recurrent pericarditis. Lancet i: 1491.
206. Tisch, R.,, X. D. Yang,, S. M. Singer,, R. S. Liblau,, L. Fugger,, and H. McDevitt. 1993. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature (London) 366: 72 75.
207. Todd, J. A. 1990. The role of MHC class II genes in susceptibility to insulin-dependent diabetes mellitus. Curr. Top. Microbiol. Immunol. 164: 17 40.
208. Tolbert, M.,, and D.J. Giron. 1994. Persistence of the D variant of encephalomyocarditis virus in the ICR-Swiss mouse. Proc. Soc. Exp. Biol. Med. 205: 124 131.
209. Toniolo, A.,, T. Onodera,, G. Jordan,, J. W. Yoon,, and A. L. Notkins. 1982. Virus-induced diabetes mellitus. Glucose abnormalities produced in mice by the six members of the coxsackie B virus group. Diabetes 31: 496 499.
210. Toniolo, A.,, T. Onodera,, J. W. Yoon,, and A. L. Notkins. 1980. Induction of diabetes by cumulative environmental insults from viruses and chemicals. Nature (London) 288: 383 385.
210a. Trucco, M. Unpublished observations.
211. Trucco, M.,, C. Ricordi,, E. Weidmann,, H. Rodriquez-Rio,, G. Trucco,, and D. Finegold. 1993. Involvement of superantigensin the etiology of IDDM. Diabetes 42( Suppl. 1): 4A.
212. Tuomi, T.,, L. C. Groop,, P. Z. Zimmet,, M. J. Rowley,, W. Knowles,, and I. R. Mackay. 1993. Antibodies to glutamic acid decarboxylase reveal latent autoimmune diabetes mellitus in adults with a non-insulin-dependent onset of disease. Diabetes 42: 359 362.
213. Tuvemo, T.,, G. Dahlquist,, G. Frisk,, L. Blom,, G. Friman,, M. Landin-Olsson,, and H. Dierholm. 1989. The Swedish childhood diabetes study. III. IgM against coxsackie B viruses in newly diagnosed type 1 (insulin-dependent) diabetic children—no evidence of increased antibody frequency. Diabetologia 32: 745 747.
214. Tuvemo, T.,, G. Frisk,, G. Friman,, J. Ludvigsson,, and H. Diderholm. 1988. IgM against coxsackie B viruses in children developing type I diabetes mellitus—a seven year retrospective study. Diabetes Res. 9: 125 129.
215. Ujevich, M. M.,, and R. Jane. 1980. Pancreatic cell damage. Its occurrence in neonatal coxsackie virus encephalomyocarditis. Arch. Pathol. Lab. Med. 104: 438 441.
216. Uriarte, A.,, E. Cabrera,, R. Ventura,, and J. Vargas. 1987. Islet cell antibodies and ECHO-4 virus infection. Diabetologia 30( Suppl. 1): 590A.
217. Vadheim, C. M.,, A. Zeidler,, J. I. Rotter,, M. Langbaum,, I. A. Shulman,, M. R. Spencer,, G. Costin,, W. J. Riley,, and N. K. MacLaren. 1989. Different HLA haplotypes in Mexican Americans with IDDM. Diabetes Care 12: 497 500.
218. Vella, C.,, A. J. Easton,, P. R. Eglin,, C. L. Brown,, and L. Perry. 1991. Coxsackie virus B4 infection of the mouse pancreas. I. Detection of virus-specific RNA in the pancreas by in situ hybridization. J. Med. Virol. 35: 46 49.
219. Vento, S.,, T. Garofano,, G. DiPerri,, L. Dolci,, E. Concia,, and D. Bassetti. 1991. Identification of hepatitis A virus as a trigger for autoimmune chronic hepatitis type 1 in susceptible individuals. Lancet 337: 1181 1187.
220. Vialettes, B.,, P. Demicco,, C. Badier,, J. Niccoline, and V Lassmann-Vague. 1987. Anti-coxsackie B IgG and IgM antibodies in first degree relatives of type 1 (insulin-dependent) diabetic patients: lack of association with islet cell antibodies. Diabetologia 30( Suppl. 1): 594A.
221. Wagener, D. K.,, J. M. Sacks,, R. E. LaPorte,, and J. M. MacGregor. 1982. The Pittsburgh study of insulin-dependent diabetes mellitus. Risk for diabetes among relatives of IDDM. Diabetes 31: 136 144.
222. Wagenknecht, L. E.,, J. M. Roseman,, and W. H. Herman. 1991. Increased incidence of insulin-dependent diabetes mellitus following an epidemic of coxsackievirus B5. Am. J. Epidemiol. 133: 1024 1031.
223. Ward, T.,, J. Clemens,, and K. W. Taylor. 1990. Effects of a diabetogenic strain of encephalomyocarditis virus on protein synthesis in mouse islets of langerhans. Biochem.J. 270: 777 781.
224. Warram, J. H.,, B. C. Martin,, and A. S. Krolewski. 1991. Risk of IDDM in children of diabetic mothers decreases with increasing maternal age at pregnancy. Diabetes 40: 1679 1984.
225. Waters, S. H.,, J. J. O'Neil,, D. T. Melican,, and M. C. Appel. 1992. Multiple TCR VB usage by infiltrates of young NOD mouse islets of Langerhans. Diabetes 41: 308 312.
226. Webb, S. R.,, R. M. Loria,, G. E. Madge,, and S. Kibrick. 1976. Susceptibility of mice to group B coxsackie virus is influenced by diabetic gene. J. Exp. Med. 143: 1239 1248.
227. Wegner, V.,, A. Kewitsch,, M. Madauss,, L. Dohner,, and H. Ziihlke. 1985. Hyperglycemia in BALB/c mice after pretreatment with one subdiabetogenic dose of streptozotocin and subsequent infection with a coxsackie B4 strain. Biomed. Biochem. Acta 44: 21 27.
228. Weinberg, C. R.,, T. L. Dornan,, J. A. Hansen,, R. K. Raghu,, and J. P. Palmer. 1984. HLA-related heterogeneity in seasonal patterns of diagnosis in type 1 (insulin-dependent) diabetes. Diabetologia 26: 199 202.
229. Werner, S.,, W. M. Klump,, H. Schdnke,, P. H. Hofscheider,, and R. Kandolf. 1988. Expression of coxsackievirus B 3 capsid proteins in Escherichia coli and generation of virus-specific antisera. DNA 7: 307 316.
230. WHOS tudy Group. 1985. Diabetes Mellitus. Technical Report Series 727. World Health Organization, Geneva.
231. Wilberz, S.,, H. J. Partke,, F. Dagnaes-Hansen,, and L. Herberg. 1991. Persistent MHV (mouse hepatitis virus) infection reduces the incidence of diabetes mellitus in non-obese diabetic mice. Diabetologia 34: 2 5.
232. Wilfert, C. M.,, R. H. Buckley,, T. Mohanakumar,, J. K. Griffiths,, S. L. Katz,, J. K. Whisnant,, and P. A. Eggleston. 1977. Persistent and fatal central system echovirus infection in agammaglobulinaemia. N. Engl. J. Med. 296: 1485.
233. Wyatt, H. V. 1973. Poliomyelitis in hypogammaglobuhnemics. J. Infect. Dis. 128: 802 806.
234. Yagi, S.,, D. Schnurr,, and J. Lin. 1992. Spectrum of monoclonal antibodies to coxsackievirus B-3 includes type- and group-specific antibodies J. Clin. Microbiol. 30: 2498 2501.
235. Yoon, J.W. 1990. The role of viruses and environmental factors in the induction of diabetes. Curt Top. Microbiol. Immunol. 164: 95 123.
236. Yoon, J. W.,, M. Austin,, T. Onodera,, and A. L. Notkins. 1979. Virus-induced diabetes mellitus: isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N. Engl. J. Med. 300: 1173 1179.
237. Yoon, J. W.,, T. L. London,, L. Curfman,, R. L. Brown,, and A. L. Notkins. 1986. Coxsackie virus B4 produces transient diabetes in nonhuman primates. Diabetes 35: 712 716.
238. Yoon, J. W.,, P. R. McClintock,, C. J. Bachurski,, J. D. Longstreth,, and A. L. Notkins. 1985. Virus-induced diabetes mellitus: no evidence for immune mechanisms in the destruction of p-cells by the D-variant of encephalomyocarditis virus. Diabetes 34: 922 925.
239. Yoon, J. W.,, P. R. McClintock,, T. Onodera,, and A. L. Notkins. 1980. Virus-induced diabetes mellitus. XVIII. Inhibition by a non-diabetogenic variant of encephalomyocarditis virus J. Exp. Med. 152: 878 892.
240. Yoon, J. W.,, T. Onodera,, and A. L. Notkins. 1978. Virus-induced diabetes. XV. Beta-cell damage and insulin-dependent hyperglycemia in mice infected with coxsackie B4J. Exp. Med. 148: 1060 1080.
241. Zibert, A.,, and E. Wimmer,. 1993. Receptor for poliovirus and other picornaviruses, p. 325 345. In K.W. Adolph (ed.), Genome Research in Molecular Medicine and Virology. Academic Press, San Diego, Calif.

Tables

Generic image for table
TABLE 1

Associations between HLA phenotype and elevated CVB IgM levels in newly diagnosed IDDM patients

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15
Generic image for table
TABLE 2

Problems in relating viruses to IDDM etiology

Citation: Rewers M, Atkinson M. 1995. The Possible Role of Enteroviruses in Diabetes Mellitus, p 353-385. In Rotbart H (ed), Human Enterovirus Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818326.ch15

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error