Group B coxsackievirus diabetogenic phenotype correlates with replication efficiency

Journal of Virology

Volumn 80, Issue 11, 2006, Pages 5637-5643

  Kanno, Toru ^a   Kim, Kisoon ^a   Kono, Ken ^a,c   Drescher, Kristen M ^b   Chapman, Nora M ^a   Tracy, Steven ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCAGON; INSULIN; PANCREAS POLYPEPTIDE; SOMATOSTATIN; VIRUS PROTEIN;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS B; COXSACKIE VIRUS B3; DIABETOGENESIS; DOSE RESPONSE; DRUG MEGADOSE; FEMALE; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PHENOTYPE; PRIORITY JOURNAL; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; COXSACKIEVIRUS INFECTIONS; DIABETES MELLITUS, TYPE 1; ENTEROVIRUS B, HUMAN; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; PHENOTYPE; VIRUS REPLICATION;

COXSACKIEVIRUS;

EID: 33646754514     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02361-05     Document Type: Article

References (61)

1. Akerblom, H. K., O. Vaarala, H. Hyoty, J. Ilonen, and M. Knip. 2002. Environmental factors in the etiology of type 1 diabetes. Am. J. Med. Genet. 115:18-29.
2. Anonymous. 2000. Enterovirus surveillance, United States, 1997-1999. Morb. Mortal. Wkly. Rep. 49:913-916.
3. Anonymous. 2006. Enterovirus surveillance, United States, 2002-2004. Morb. Mortal. Wkly. Rep. 55:153-156.
4. Atkinson, M. A., and E. H. Leiter. 1999. The NOD mouse model of type 1 diabetes: as good as it gets? Nat. Med. 5:601-604.
5. Atkinson, M. A., and N. Maclaren. 1994. The pathogenesis of insulin-dependent diabetes mellitus. N. Engl. J. Med. 331:1428-1436.
6. Baekkeskov, S., and B. Hansen. 1990. Human diabetes: genetic, environmental, and autoimmune etiology. Curr. Top. Microbiol. Immunol. 164:143-168.
7. Barnett, A. H., C. Eff, R. Leslie, and D. Pyke. 1981. Diabetes in identical twins: a study of 200 pairs. Diabetologia 20:87-93.
8. Cabrera-Rode, E., L. Sarmiento, G. Molina, C. Perez, C. Arranz, J. A. Galvan, M. Prieto, J, Barrios, R. Palomera, M. Fonseca, P. Mas, O. Diaz-Diaz, and O. Diaz-Horta. 2005. Islet cell related antibodies and type 1 diabetes associated with echovirus 30 epidemic: a case report. J. Med. Virol. 76:373-377.
9. Cabrera-Rode, E., L. Sarmiento, C. Tiberti, G. Molina, J. Barrios, D. Hernandez, O. Diaz-Horta, and U. Di Mario. 2003. Type 1 diabetes islet associated antibodies in subjects infected by echovirus 16. Diabetologia 46:1348-1353.
10. Chehadeh, W., J. Kerr-Conte, F. Pattou, G. Alm, J. Lefebvre, N. Waugh, and D. Hober. 2000. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J. Virol. 74:10153-10164.
11. Control, C. F. D. 2000. Non-polio enterovirus surveillance, United States, 1993-1996. Morbid. Mortal. Wkly. Rep. 46:748-750.
12. Craighead, J. E. 1975. The role of viruses in the pathogenesis of pancreatic disease and diabetes mellitus. Prog. Med. Virol. 19:161-214.
13. Diaz-Horta, O., M. Bello, E. Cabrera-Rode, J. Suarez, P. Mas, I. Garcia, I. Abalos, R. Jofra, G. Molina, O. Diaz-Diaz, and U. Di Mario. 2001. Echovirus 4 and type 1 diabetes mellitus. Autoimmunity 34:275-281.
14. Drescher, K. M., K. Kono, S. Bopegamage, S. D. Carson, and S. Tracy. 2004. Coxsackievirus B3 infection and type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection. Virology 329:381-394.
15. Dunn, G., S. Bradrick, N. Chapman, S. Tracy, and J. Romero. 2003. The stem loop II within the 5′ nontranslated region of clinical coxsackievirus B3 genomes determines cardiovirulence phenotype in a murine model. J. Infect. Dis. 15:1552-1561.
16. Dunn, J. J., N. M. Chapman, S. Tracy, and J. R. Romero. 2000. Natural genetics of cardiovirulence in coxsackievirus B3 clinical isolates: localization to the 5′ nontranslated region. J. Virol. 74:4787-4794.
17. Flodstrom, M., A. Maday, B. Balakrishna, M. Cleary, A. Yoshimura, and N. Sarvetnick. 2002. Target cell defense prevents the development of diabetes after viral replication. Nat. Immunol. 3:373-382.
18. Foulis, A. K., M. Farquharson, S. Cameron, M. McGill, H. Schoenke, and R. Kandolf. 1990. A search for the presence of enteroviral capsid protein VP1 in pancreases of patients with type 1 diabetes and pancreases and hearts of infants who died of coxsackieviral myocarditis. Diabetologia 33:290-298.
19. Frisk, G., and T. Tuvemo. 2004. Enterovirus infections with beta-cell tropic strains are frequent in siblings of children diagnosed with type 1 diabetes children and in association with elevated levels of GAD65 antibodies. J. Med. Virol. 73:450-459.
20. Froeschle, J., P. Feorino, and H. M. Gelfand. 1966. A continuing surveillance of enterovirus infection in healthy children in six United States 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.
21. Fuchtenbusch, M., A. Irnstetter, G. Jager, and A.-G. Ziegler. 2001. No evidence for an association of coxsackievirus infections during pregnancy and early childhood with development of islet autoantibodies in offspring of mothers or fathers with type 1 diabetes. J. Autoimmun. 17:333-340.
22. Gamble, D. R. 1976. A possible virus etiology for juvenile diabetes, p. 95-105. In W. Kreutzfeld, J. Kobberling, and J. Neel (ed.), The genetics of diabetes mellitus. Springer Verlag, Berlin, Germany.
23. Gauntt, C. J. 1997. Roles of the humoral response in coxsackievirus B-induced disease. Curr. Top. Microbiol. Immunol. 223:259-282.
24. Hierholzer, J. C., and W. 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.
25. Huber, S. H. 1988. The role of immune mechanisms in pathogenesis, p. 103-116. In M. Bendinelli and H. Friedman (ed.), Coxsackieviruses: a general update. Plenum Press, New York, N.Y.
26. Huff, J. C., J. C. Hierholzer, and W. Farris. 1974. An "outbreak" of juvenile diabetes mellitus: consideration of a viral etiology. Am. J. Epidemiol. 100:277-287.
27. Hyoty, H., M. Hiltunen, and M. Lonnrot. 1998. Enterovirus infections and insulin dependent diabetes mellitus-evidence for causality. Clin. Diagn. Virol. 9:77-84.
28. Iwasaki, T., N. Monma, R. Satodate, R. Kawana, and T. Kurata. 1985. An immunofluorescent study of generalized coxsackie virus B3 infection in a newborn infant. Acta Pathol. Jpn. 35:741-748.
29. Jenkins, O., J. D. Booth, P. D. Minor, and J. W. Almond. 1987. The complete nucleotide sequence of coxsackievirus B4 and its comparison to other members of the picornaviridae. J. Gen. Virol. 68:1835-1848.
30. Kang, J., N. Chatterjee, M. Nodwell, and J. Yoon. 1994. Complete nucleotide sequence of a strain of coxsackie B4 virus of human origin that induces diabetes in mice and its comparison with nondiabetogenic coxsackie B4 JBV strain. J. Med. Virol. 44:353-361.
31. Kanno, T., D. Mackay, G. Wilsden, and P. Kitching. 2001. Virulence of swine vesicular disease virus is determined at two amino acids in capsid protein VP1 and 2A protease. Virus Res. 80:107.
32. Knip, M., and H. K. Akerblom. 1999. Environmental factors in the pathogenesis of type 1 diabetes mellitus. Exp. Clin. Endocrinol. Diabetes 107(Suppl. 3):S93-S100.
33. Lee, C.-K., K. Kono, E. Haas, K.-S. Kim, K. M. Drescher, N. M. Chapman, and S. Tracy. 2005. Characterization of an infectious cDNA copy of the genome of a naturally-occurring, avirulent coxsackievirus B3 clinical isolate. J. Gen. Virol. 86:197-210.
34. Lindberg, A., P. Andersoon, C. Savolainen, M. N. Mulders, and T. Hovi. 2003. Evolution of the genome of human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J. Gen. Virol. 84:1223-1235.
35. Lo, S., R. Tun, M. Hawa, and R. Leslie. 1991. Studies of diabetic twins. Diabetes Metab. Rev. 7:223-228.
36. Lukashev, A. N., V. A. Lashkevich, O. E. Ivanova, G. A. Koroleva, A. E. Hinkkanen, and J. Ilonen. 2005. Recombination in circulating human enterovirus B: independent evolution of structural and non-structural genome regions. J. Gen. Virol. 86:3281-3290.
37. Maria, H., A. Elshebani, O. Anders, T. Torsten, and K. Gun. 2005. Simultaneous type 1 diabetes onset in mother and son coincident with an enteroviral infection. J. Clin. Virol. 33:158-167.
38. Miyazaki, J., K. Araki, E. Yamato, H. Ikegami, T. Asano, Y. Shibasaki, Y. Oka, and K. Yamamura. 1990. Establishment of a pancreatic beta cell line that retains glucose inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127:126-132.
39. Moya-Suri, V., M. Schlosser, K. Zimmermann, I. Rjasanowski, L. Gurtler, and R. Mentel. 2005. Enterovirus RNA sequences in sera of schoolchildren in the general population and their association with type 1-diabetes-associated autoantibodies. J. Med. Microbiol. 54:879-883.
40. Nigro, G., M. E. Pacella, E. Patane, and M. Midulla. 1986. Multi-system coxsackievirus B-6 infection with findings suggestive of diabetes mellitus. Eur. J. Pediatr. 145:557-559.
41. Oberste, M. S., S. Penaranda, and M. Pallansch. 2004. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J. Virol. 78:2948-2955.
42. Otonkoski, T., M. Roivainen, O. Vaarala, B. Dinesen, J. Leipala, L. Hix, and M. Knip. 2000. Neonatal type I diabetes associated with maternal echovirus 6 infection: a case report. Diabetologia 43:1235-1238.
43. Pallansch, M., and R. P. Roos. 2001. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses, p. 723-776. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams and Wilkins, Philadelphia, Pa.
44. Ramsingh, A., A. Hixson, B. Duceman, and J. Slack. 1990. Evidence suggesting that virulence maps to the P1 region of the coxsackievirus B4 genome. J. Virol. 64:3078-3081.
45. Redondo, M., L. Yu, M. Hawa, T. Mackenzie, D. Pyke, G. Eisenbarth, and R. Leslie. 2001. Heterogeneity of type I diabetes: analysis of monozygotic twins in Great Britain and the United States. Diabetologia 44:354-362.
46. Roep, B., M. A. Atkinson, and M. G. von Herrath. 2004. Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes. Nat. Rev. Immunol. 4:989-997.
47. Roivainen, M., S. Rasilainen, P. Ylipaasto, R. Nissinen, J. Ustinov, L. Bouwens, D. Eizirik, T. Hovi, and T. Otonkoski. 2000. Mechanism of coxsackievirus-induced damage to human pancreatic beta cells. J. Clin. Endocrinol. Metab. 85:432-440.
48. Roivainen, M., P. Ylipaasto, C. Savolainen, J. M. Galama, T. Hovi, and T. Otonkoski. 2002. Functional impairment and killing of human beta cells by enteroviruses: the capacity is shared by a wide range of serotypes, but the extent is a characteristic of individual virus strains. Diabetologia 45:693-702.
49. Rose, N. R., D. A. Neumann, and A. Herskowitz. 1988. Genetics of susceptibility to viral myocarditis in mice. Pathol. Immunopathol. Res. 7:266-278.
50. Schwimmbeck, P. L., S. A. Huber, and H. P. Schultheiss. 1997. Roles of T cells in coxsackievirus B-induced disease. Curr. Top. Microbiol. Immunol. 223:283-303.
51. Serreze, D. V., E. W. Ottendorfer, T. M. Ellis, C. J. Gauntt, and M. A. Atkinson. 2000. Acceleration of type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T-cells in pancreatic islets. Diabetes 49:708-711.
52. Smith, C., G. Clements, M. Riding, P. Collins, G. Bottazo, and K. Taylor. 1998. Simultaneous onset of type 1 diabetes mellitus in identical infant twins with enterovirus infection. Diabet. Med. 15:515-517.
53. 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. Function 4:181-187.
54. Thomson, A. B. R., and E. A. Shaffer. 1992. The first principles of gastroenterology. University of Toronto Press, Toronto, Canada.
55. Tracy, S., K. M. Drescher, N. M. Chapman, K.-S. Kim, S. D. Carson, S. Pirruccello, P. H. Lane, J. R. Romero, and J. S. Leser. 2002. Toward testing the hypothesis that group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic mice with CVB markedly lowers diabetes incidence. J. Virol. 76:12097-12111.
56. Tracy, S., K. Hofling, S. Pirruccello, P. H. Lane, S. M. Reyna, and C. Gauntt. 2000. Group B coxsackievirus myocarditis and pancreatitis in mice: connection between viral virulence phenotypes. J. Med. Virol. 62:70-81.
57. Verge, C., N. Howard, L. Irwig, J. Simpson, D. Mackerras, and M. Silink. 1994. Environmental factors in childhood IDDM: a population-based, case-control study. Diabetes Care 17:1381-1389.
58. Wadsworth, E., J. Shield, L. Hunt, and J. Baum. 1997. A case control study of environmental factors associated with diabetes in the under 5s. Diabet. Med. 14:390-396.
59. Ylipaasto, P., K. Klingel, A. M. Lindberg, T. Otonkoski, R. Kandolf, T. Hovi, and M. Roivainen. 2004. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47:225-239.
60. Yoon, J., M. Austin, T. Onodera, and A. Notkins. 1979. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N. Engl. J. Med. 300:1173-1179.
61. Yoon, J., T. Onodera, A. Jenson, and A. Notkins. 1978. Virus induced diabetes mellitus. XI. Replication of coxsackie B3 virus in human pancreatic beta cell cultures. Diabetes 27:778-781.