Genetic and phenotypic diversity of echovirus 30 strains and pathogenesis of type 1 diabetes

Journal of Medical Virology

Volumn 79, Issue 7, 2007, Pages 945-955

  Paananen, A ^a   Savolainen Kopra, C ^a   Kaijalainen, S ^a   Vaarala, O ^a   Hovi, T ^a   Roivainen, M ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Antigenic clustering; E 30; Echovirus; Enterovirus; Field isolates; Full length infectious clone; Neutralizing antibodies; Sequence analyses; Type 1 diabetes; Virus specific antibody response

Indexed keywords

NEUTRALIZING ANTIBODY; STRUCTURAL PROTEIN;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CELL KILLING; CHILD; CONTROLLED STUDY; DIABETOGENESIS; ECHO VIRUS; ENTEROVIRUS; EVOLUTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS; SEROTYPE; VIRUS CAPSID; VIRUS GENOME; VIRUS STRAIN; VIRUS VIRULENCE;

ADOLESCENT; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; CROSS REACTIONS; DIABETES MELLITUS, TYPE 1; DNA, VIRAL; ECHOVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; FINLAND; HUMANS; INFANT; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PHENOTYPE; PHYLOGENY; SEROTYPING; VARIATION (GENETICS);

ECHOVIRUS; ENTEROVIRUS; HUMAN ECHOVIRUS 30; HUMAN ECHOVIRUS 9; HUMAN ENTEROVIRUS B; MIRIDAE;

EID: 34249889088     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.20922     Document Type: Article

References (44)

1. Abraham G, Colonno RJ. 1984. Many rhinovirus serotypes share the same cellular receptor. J Virol 51:340-345.
2. Andreoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyghem MC, Lefebvre J, Wattre P. 1997. Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of type I diabetes mellitus. J Med Virol 52:121-127.
3. Beyer WE, Masurel N. 1985. Antigenic heterogeneity among influenza A(H3N2) field isolates during an outbreak in 1982/83, estimated by methods of numerical taxonomy. J Hyg (Lond) 94:97-109.
4. CDC. 2006. Enterovirus surveillance. United States, 1970-2005. MMWR 55:1-20.
5. Chehadeh W, Weill J, Vantyghem MC, Alm G, Lefebvre J, Wattre P, Hober D. 2000. Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: Relationship with coxsackievirus B infection. J Infect Dis 181:1929-1939.
6. Clements GB, Galbraith DN, Taylor KW. 1995. Coxsackie B virus infection and onset of childhood diabetes. Lancet 346:221-223.
7. Dussart P, Cartet G, Huguet P, Leveque N, Hajjar C, Morvan J, Vanderkerckhove J, Ferret K, Lina B, Chomel JJ, Norder H. 2005. Outbreak of acute hemorrhagic conjunctivitis in French Guiana and West Indies caused by coxsackievirus A24 variant: Phylogenetic analysis reveals Asian import. J Med Virol 75:559-565.
8. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) and documentation 3.65, Department of Genetics, University of Washington, Seattle.
9. Gerling I, Chatterjee NK. 1990. Autoantigen (64000-Mr) expression in coxsackievirus B4-induced experimental diabetes. Curr Top Microbiol Immunol 156:55-62.
10. Harkonen T, Puolakkainen M, Sarvas M, Airaksinen U, Hovi T, Roivainen M. 2000. Picornavirus proteins share antigenic determinants with heat shock proteins 60/65. J Med Virol 62:383-391.
11. Harkonen T, Lankinen H, Davydova B, Hovi T, Roivainen M. 2002. Enterovirus infection can induce immune responses that cross-react with beta-cell autoantigen tyrosine phosphatase IA-2/IAR. J Med Virol 66:340-350.
12. Harkonen T, Paananen A, Lankinen H, Hovi T, Vaarala O, Roivainen M. 2003. Enterovirus infection may induce humoral immune response reacting with islet cell autoantigens in humans. J Med Virol 69:426-440.
13. Hovi T, Stenvik M, Rosenlew M. 1996. Relative abundance of enterovirus serotypes in sewage differs from that in patients: Clinical and epidemiological implications. Epidemiol Infect 116:91-97.
14. Hyoty H, Hiltunen M, Knip M, Laakkonen M, Vahasalo P, Karjalainen J, Koskela P, Roivainen M, Leinikki P, Hovi T, et al. 1995. A prospective study of the role of coxsackie B and other enterovirus infections in the pathogenesis of IDDM. Childhood Diabetes in Finland (DiMe) Study Group. Diabetes 44:652-657.
15. Karttunen A, Poyry T, Vaarala O, Ilonen J, Hovi T, Roivainen M, Hyypia T. 2003. Variation in enterovirus receptor genes. J Med Virol 70:99-108.
16. Kaufman DL, Erlander MG, Clare-Salzler M, Atkinson MA, Maclaren NK, Tobin AJ. 1992. Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. J Clin Invest 89:283-292.
17. Kew OM, Mulders MN, Lipskaya GY, da Silva EE, Pallansch MA. 1995. Molecular epidemiology of polioviruses. Semin Virol 6:401-414.
18. Kew OM, Sutter RW, de Gourville EM, Dowdle WR, Pallansch MA. 2005. Vaccine-derived polioviruses and the endgame strategy for global polio eradication (*). Annu Rev Microbiol 59:587-635.
19. Lindberg AM, Andersson P, Savolainen C, Mulders MN, Hovi T. 2003. Evolution of the genome of Human enterovirus B: Incongruence between phytogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J Gen Virol 84:1223-1235.
20. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC. 1999. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152-160.
21. Lonnrot M, Hyoty H, Knip M, Roivainen M, Kulmala P, Leinikki P, Akerblom HK. 1996. Antibody cross-reactivity induced by the homologous regions in glutamic acid decarboxylase (GAD65) and 2C protein of coxsackievirus B4. Childhood Diabetes in Finland Study Group. Clin Experiment Immunol 104:398-405.
22. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J. 2005. Recombination in circulating human enterovirus B: Independent evolution of structural and non-structural genome regions. J Gen Virol 86:3281-3290.
23. Mulders MN, Salminen M, Kalkkinen N, Hovi T. 2000. Molecular 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 81:803-812.
24. Oberste MS, Maher K, Kennett ML, Campbell JJ, Carpenter MS, Schnurr D, Pallansch MA. 1999. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): Genotypes correlate with temporal dynamics of E30 isolation. J Clin Microbiol 37:3928-3933.
25. Oberste MS, Nix WA, Kilpatrick DR, Flemister MR, Pallansch MA. 2003. Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Res 91:241-248.
26. Oberste MS, Maher K, Pallansch MA. 2004. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78:855-867.
27. Onkamo P, Vaananen S, Karvonen M, Tuomilehto J. 1999. Worldwide increase in incidence of Type I diabetes - The analysis of the data on published incidence trends. Diabetologia 42:1395-1403.
28. Paananen A, Ylipaasto P, Rieder E, Hovi T, Galama J, Roivainen M. 2003. Molecular and biological analysis of echovirus 9 strain isolated from a diabetic child. J Med Virol 69:529-537.
29. Palacios G, Casas I, Cisterna D, Trallero G, Tenorio A, Freire C. 2002. Molecular epidemiology of echovirus 30: Temporal circulation and prevalence of single lineages. J Virol 76:4940-4949.
30. Perriere G, Gouy M. 1996. WWW-query: An on-line retrieval system for biological sequence banks. Biochimie 78:364-369.
31. Roivainen M, Knip M, Hyoty H, Kulmala P, Hiltunen M, Vahasalo P, Hovi T, Akerblom HK. 1998. 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 56:74-78.
32. Roivainen M, Rasilainen S, Ylipaasto P, Nissinen R, Ustinov J, Bouwens L, Eizirik DL, Hovi T, Otonkoski T. 2000. Mechanisms of coxsackievirus-induced damage to human pancreatic beta-cells. J Clin Endocrinol Metab 85:432-440.
33. Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T. 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.
34. Sadeharju K, Knip M, Hiltunen M, Akerblom HK, Hyoty H. 2003. The HLA-DR phenotype modulates the humoral immune response to enterovirus antigens. Diabetologia 46:1100-1105.
35. Santti J, Harvala H, Kinnunen L, Hyypia T. 2000. Molecular epidemiology and evolution of coxsackievirus A9. J Gen Virol 81:1361-1372.
36. Savolainen C, Hovi T, Mulders MN. 2001. Molecular epidemiology of echovirus 30 in Europe: Succession of dominant sublineages within a single major genotype. Arch Virol 146:521-537.
37. See DM, Tilles JG. 1995. Pathogenesis of virus-induced diabetes in mice. J Infect Dis 171:1131-1138.
38. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
39. Varela-Calvino R, Peakman M. 2003. Enteroviruses and type 1 diabetes. Diabetes Metab Res Rev 19:431-441.
40. Varela-Calvino R, Sgarbi G, Arif S, Peakman M. 2000. T-Cell reactivity to the P2C nonstructural protein of a diabetogenic strain of coxsackievirus B4. Virology 274:56-64.
41. Vreugdenhil GR, Geluk A, Ottenhoff TH, Melchers WJ, Roep BO, Galama JM. 1998. Molecular mimicry in diabetes mellitus: The homologous domain in coxsackie B virus protein 2C and islet autoantigen GAD65 is highly conserved in the coxsackie B-like enteroviruses and binds to the diabetes associated HLA-DR3 molecule. Diabelologia 41:40-46.
42. Vreugdenhil GR, Schloot NC, Hoorens A, Rongen C, Pipeleers DG, Melchers WJ, Roep BO, Galama JM. 2000. Acute onset of type I diabetes mellitus after severe echovirus 9 infection: Putative pathogenic pathways. Clin Infect Dis 31:1025-1031.
43. Ylipaasto P, Klingel K, Lindberg AM, Otonkoski T, Kandolf R, Hovi T, Roivainen M. 2004. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabctolngia 47:225-239.
44. Yoon JW, Austin M, Onodera T, Notkins AL. 1979. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 300:1173-1179.