Amino acids of Coxsackie B5 virus are critical for infection of the murine insulinoma cell line, MIN-6

Journal of Medical Virology

Volumn 81, Issue 2, 2009, Pages 296-304

  Al Hello, Haider ^a   Ylipaasto, Petri ^a   Smura, Teemu ^a   Rieder, Elisabeth ^b,c   Hovi, Tapani ^a   Roivainen, Merja ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b STONY BROOK UNIVERSITY   (United States)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

CBV 5 MPP; MIN 6; MIN 6 cell adapted and site directed mutagenesis; Mouse pancreas passaged CBV 5

Indexed keywords

AMINO ACID; CAPSID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; COXSACKIE VIRUS; COXSACKIE VIRUS B5; CYTOPATHOGENIC EFFECT; EXPERIMENTAL MOUSE; GENETIC TRAIT; IN VITRO STUDY; INSULINOMA; MALE; MOUSE; NONHUMAN; PROGENY; VIROGENESIS; VIRUS INFECTION; VIRUS STRAIN; ANIMAL; CHEMISTRY; COXSACKIE VIRUS INFECTION; ENTEROVIRUS; GENETICS; METABOLISM; PANCREAS; PANCREATITIS; PATHOLOGY; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE; VIROLOGY; VIRUS CULTURE; VIRUS GENOME; VIRUS REPLICATION;

AMINO ACIDS; ANIMALS; CAPSID PROTEINS; CELL LINE, TUMOR; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; GENOME, VIRAL; INSULINOMA; MALE; MICE; MUTAGENESIS, SITE-DIRECTED; PANCREAS; PANCREATITIS; SERIAL PASSAGE; VIRUS REPLICATION;

HUMAN ENTEROVIRUS B; MURINAE; MUS;

EID: 61749083673     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.21391     Document Type: Article

References (44)

1. Al-Hello H, Davydova B, Smura T, Kaialainen S, Ylipaasto P, Saario E, Hovi T, Rieder E, Roivainen M. 2005. Phenotypic and genetic changes in coxsackievirus B5 following repeated passage in mouse pancreas in vivo. J Med Virol 75:566-574.
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. Arola A, Kalimo H, Ruuskanen O, Hyypia T. 1995. Experimental myocarditis induced by two different coxsackievirus B3 variants: Aspects of pathogenesis and comparison of diagnostic methods. J Med Virol 47:251-259.
4. Bae YS, Yoon JW. 1993. Determination of diabetogenicity attributable to a single amino acid, Ala776, on the polyprotein of encephalomyocarditis virus. Diabetes 42:435-443.
5. Caggana M, Chan P, Ramsingh A. 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.
6. Chehadeh W, Kerr-Conte J, Pattou F, Alm G, Lefebvre J, Wattre P, Hober D. 2000. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J Virol 74:10153-10164.
7. Clements GB, Galbraith DN, Taylor KW. 1995. Coxsackie B virus infection and onset of childhood diabetes. Lancet 346:221-223.
8. Craig ME, Howard NJ, Silink M, Rawlinson WD. 2003. Reduced frequency of HLA DRB1*03-DQB1*02 in children with Type 1 diabetes associated with enterovirus RNA. J Infect Dis 187:1562-1570.
9. Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P. 2007. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA 104:5115-5120.
10. Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N. 2002a. Target cell defense prevents the development of diabetes after viral infection. Nat Immunol 3:373-382.
11. Flodstrom M, Shi FD, Sarvetnick N, Ljunggren HG. 2002b. The natural killer cell - friend or foe in autoimmune disease? Scand J Immunol 55:432-441.
12. Gerling I, Chatterjee NK. 1990. Autoantigen (64000-Mr) expression in coxsackievirus B4-induced experimental diabetes. Curr Top Microbiol Immunol 156:55-62.
13. Halim S, Ramsingh AI. 2000. Apoint mutation in VP1 of coxsackievirus B4 alters antigenicity. Virology 269:86-94.
14. 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.
15. Hiltunen M, Hyoty H, Karjalainen J, Leinikki P, Knip M, Lounamaa R, Akerblom HK. 1995. Serological evaluation of the role of cytomegalovirus in the pathogenesis of IDDM: A prospective study. The childhood diabetes in Finland study group. Diabetologia 38:705-710.
16. Hiltunen M, Hyoty H, Knip M, Ilonen J, Reijonen H, Vahasalo P, Roivainen M, Lonnrot M, Leinikki P, Hovi T, Akerblom HK. 1997. Islet cell antibody seroconversion in children is temporally associated with enterovirus infections. Childhood diabetes in Finland (DiMe) study group. J Infect Dis 175:554-560.
17. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. 1998. Diabetes induced by Coxsackie virus: Initiation by bystander damage and not molecular mimicry. Nat Med 4:781-785.
18. Hovi T, Roivainen M. 1993. Peptide antisera targeted to a conserved sequence in poliovirus capsid VP1 cross-react widely with members of the genus Enterovirus. J Clin Microbiol 31:1083-1087.
19. Hyoty H, Hiltunen M, Knip M, Laakkonen M, Vahasalo P, Karjalainen J, Koskela P, Roivainen M, Leinikki P, Hovi T, Akerblom H, The Childhood Diabetes in Finland (DiMe) Study Group. 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.
20. Hyttinen V, Kaprio J, Kinnunen L, Koskenvuo M, Tuomilehto J. 2003. Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: A nationwide follow-up study. Diabetes 52:1052-1055.
21. Jun HS, Kang Y, Notkins AL, Yoon JW. 1997. Gain or loss of diabetogenicity resulting from a single point mutation in recombinant encephalomyocarditis virus. J Virol 71:9782-9785.
22. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S. 1996. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J Virol 70:7811-7818.
23. 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. Clini Experiment Immunol 104:398-405.
24. Lonnrot M, Korpela K, Knip M, Ilonen J, Simell O, Korhonen S, Savola K, Muona P, Simell T, Koskela P, Hyoty H. 2000a. Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: The Finnish diabetes prediction and prevention study. Diabetes 49:1314-1318.
25. Lonnrot M, Salminen K, Knip M, Savola K, Kulmala P, Leinikki P, Hyypia T, Akerblom HK, Hyoty H. 2000b. Enterovirus RNA in serum is a risk factor for beta-cell autoimmunity and clinical type 1 diabetes: A prospective study. childhood diabetes in Finland (DiMe) study group. J Med Virol 61:214-220.
26. Miyazaki J, Araki K, Yamato E, Ikegami H, Asano T, Shibasaki Y, Oka Y, Yamamura K. 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.
27. Ramsingh AI, Chapman N, Tracy S. 1997a. Coxsackieviruses and diabetes. Bioessays 19:793-800.
28. Ramsingh AI, Lee WT, Collins DN, Armstrong LE. 1997b. Differential recruitment of B and T cells in coxsackievirus B4-induced pancreatitis is influenced by a capsid protein. J Virol 71:8690-8697.
29. Redondo MJ, Yu L, Hawa M, Mackenzie T, Pyke DA, Eisenbarth GS, Leslie RD. 2001. Heterogeneity of type I diabetes: Analysis of monozygotic twins in Great Britain and the United States. Diabetologia 44:354-362.
30. Roivainen M. 2006. Enteroviruses: New findings on the role of enteroviruses in type 1 diabetes. Int J Biochem Cell Biol 38:721-725.
31. Roivainen M, Alfthan G, Jousilahti P, Kimpimaki M, Hovi T, Tuomilehto J. 1998. Enterovirus infections as a possible risk factor for myocardial infarction. Circulation 98:2534-2537.
32. 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.
33. Ross ME, Hayashi K, Notkins AL. 1974. Virus-induced pancreatic disease: Alterations in concentration of glucose and amylase in blood. J Infect Dis 129:669-676.
34. Schloot NC, Willemen SJ, Duinkerken G, Drijfhout JW, de Vries RR, Roep BO. 2001. 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 62:299-309.
35. Schmidtke M, Selinka HC, Heim A, Jahn B, Tonew M, Kandolf R, Stelzner A, Zell R. 2000. Attachment of coxsackievirus B3 variants to various cell lines: Mapping of phenotypic differences to capsid protein VP1. Virology 275:77-88.
36. See DM, Tilles JG. 1995. Pathogenesis of virus-induced diabetes in mice. J Infect Dis 171:1131-1138.
37. Szopa TM, Dronfield DM, Ward T, Taylor KW. 1989. In vivo infection of mice with Coxsackie B4 virus induces long-term functional changes in pancreatic islets with minimal alteration in blood glucose. Diabet Med 6:314-319.
38. Toniolo A, Onodera T, Jordan G, Yoon JW, Notkins AL. 1982. Virus-induced diabetes mellitus. Glucose abnormalities produced in mice by the six members of the Coxsackie B virus group. Diabetes 31:496-499.
39. Vella C, Brown CL, McCarthy DA. 1992. Coxsackievirus B4 infection of the mouse pancreas: Acute and persistent infection. J Gen Virol 73:1387-1394.
40. Verdaguer N, Jimenez-Clavero MA, Fita I, Ley V. 2003. Structure of swine vesicular disease virus: Mapping of changes occurring during adaptation of human coxsackie B5 virus to infect swine. J Virol 77:9780-9789.
41. Vreugdenhil GR, Geluk A, Ottenhoff THM, Melchers WJG, Roep BP, Galama JMD. 1998. Molecular mimicry in diabetes mellitus: The homologous domain in coxsackie B virus protein. Diabetologia 41:40-46.
42. Vuorinen T, Kallajoki M, Hyypia T, Vainionpaa R. 1989. Coxsackievirus B3-induced acute pancreatitis: Analysis of histopathological and viral parameters in a mouse model. Br J Exp Pathol 70:395-403.
43. Ylipaasto P, Klingel K, Lindberg AM, Otonkoski T, Kandolf R, Hovi T, Roivainen M. 2004. Enterovirus infection in human pancreatic islet cells, islet tropismin vivo and receptor involvement in cultured islet beta cells. Diabetologia 47:225-239.
44. Yoon JW, Ihm SH, Kim KW. 1989. Viruses as a triggering factor of type 1 diabetes and genetic markers related to the susceptibility to the virus-associated diabetes. Diabetes Res Clin Pract 7:S47-S58.