RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection

Journal of Immunology

Volumn 174, Issue 3, 2005, Pages 1171-1177

  Flodström Tullberg, Malin ^a,b   Hultcrantz, Monica ^b   Stotland, Alexandr ^a   Maday, Amy ^a   Tsai, Devin ^a   Fine, Cody ^a   Williams, Bryan ^c   Silverman, Robert ^c   Sarvetnick, Nora ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA INTERFERON; GAMMA INTERFERON; PROTEIN KINASE R; RIBONUCLEASE L;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; COXSACKIE VIRUS B4; COXSACKIE VIRUS INFECTION; IN VITRO STUDY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS INHIBITION; VIRUS REPLICATION;

EID: 12444252033     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.3.1171     Document Type: Article

References (55)

1. . Knip, M., and H. K. Akerblom. 1999. Environmental factors in the pathogenesis of type 1 diabetes mellitus. Exp Clin. Endocrinol. Diabetes. 107:S93.
2. Jaeckel, E., M. Manns, and M. Von Herrath. 2002. Viruses and diabetes. Ann. NY Acad. Sci. 958:7.
3. Gladisch, R., W. Hofmann, and R. Waldherr. 1976. [Myocarditis and insulitis following Coxsackie virus infection]. Z. Kardiol. 65:837.
4. Yoon, J. W., M. Austin, T. Onodera, and A. L. Notkins. 1979. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N. Engl. J. Med. 300:1173.
5. Jenson, A. B., H. S. Rosenberg, and A. L. Notkins. 1980. Pancreatic islet-cell damage in children with fatal viral infections. Lancet 2:354.
6. 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 β cells. Diabetologia 47:225.
7. 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. Diabetes Med. 6:314.
8. 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. Funct. 4:181.
9. 2+ response to glucose in mouse β-cells infected with Coxsackie B or Echo virus. Virus Res. 33:229.
10. Roivainen, M., S. Rasilainen, P. Ylipaasto, R. Nissinen, J. Ustinov, L. Bouwens, D. L. Eizirik, T. Hovi, and T. Otonkoski. 2000. Mechanisms of Coxsackievirus-induced damage to human pancreatic β-cells. J. Clin. Endocrinol. Metab. 85:432.
11. Flodstrom, M., A. Maday, D. Balakrishna, M. M. Cleary, A. Yoshimura, and N. Sarvetnick. 2002. Target cell defense prevents the development of diabetes after viral infection. Nat. Immunol. 3:373.
12. Roivainen, M., P. Ylipaasto, C. Savolainen, J. Galama, T. Hovi, and T. Otonkoski. 2002. Functional impairment and killing of human β 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.
13. Torres, A., J. Garib, and M. L. Recurt. 1984. Coxsackie virus: a review. Bol. Asoc. Med. P. R. 76:49.
14. Chehadeh, W., J. Kerr-Conte, F. Pattou, G. Alm, J. Lefebvre, P. Wattre, and D. Hober. 2000. Persistent infection of human pancreatic islets by Coxsackievirus B is associated with α interferon synthesis in β cells. J. Virol. 74:10153.
15. Flodstrom, M., D. Tsai, C. Fine, A. Maday, and N. Sarvetnick. 2003. Diabetogenic potential of human pathogens uncovered in experimentally permissive β-cells. Diabetes 52:2025.
16. Yoon, J. W., P. R. McClintock, T. Onodera, and A. L. Notkins. 1980. Virus-induced diabetes mellitus. XVIII. Inhibition by a nondiabetogenic variant of encephalomyocarditis virus. J. Exp. Med. 152:878.
17. Pozzetto, B., and I. Gresser. 1985. Role of sex and early interferon production in the susceptibility of mice to encephalomyocarditis virus. J. Gen. Virol. 66:701.
18. Nakayama, T., T. Urano, M. Osano, Y. Hayashi, S. Sekine, T. Ando, and S. Makinom. 1989. Outbreak of herpangina associated with Coxsackievirus B3 infection. Pediatr. Infect. Dis. J. 8:495.
19. Bogdan, C. 2000. The function of type I interferons in antimicrobial immunity. Curr. Opin. Immunol. 12:419.
20. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778.
21. Chesler, D. A., and C. S. Reiss. 2002. The role of IFN-γ in immune responses to viral infections of the central nervous system. Cytokine Growth Factor Rev. 13:441.
22. Barber, G. N. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8:113.
23. Chawla-Sarkar, M., D. J. Lindner, Y. F. Liu, B. R. Williams, G. C. Sen, R. H. Silverman, and E. C. Borden. 2003. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237.
24. Player, M. R., and P. F. Torrence. 1998. The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol. Ther. 78:55.
25. Saunders, L. R., and G. N. Barber. 2003. The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB J. 17:961.
26. 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.
27. Flodstrom, M., and D. L. Eizirik. 1997. Interferon-γ-induced interferon regulatory factor-1 (IRF-1) expression in rodent and human islet cells precedes nitric oxide production. Endocrinology 138:2747.
28. Deonarain, R., A. Alcami, M. Alexiou, M. J. Dallman, D. R. Gewert, and A. C. Porter. 2000. Impaired antiviral response and α/β interferon induction in mice lacking β interferon. J. Virol. 74:3404.
29. Stephens, L. A., H. E. Thomas, L. Ming, M. Grell, R. Darwiche, L. Volodin, and T. W. Kay. 1999. Tumor necrosis factor-α-activated cell death pathways in NIT-1 insulinoma cells and primary pancreatic β cells. Endocrinology 140:3219.
30. Horwitz, M. S., L. M. Bradley, J. Harbertson, T. Krahl, J. Lee, and N. Sarvetnick. 1998. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med. 4:781.
31. Blair, L. A., M. R. Heitmeier, A. L. Scarim, L. B. Maggi, Jr., and J. A. Corbett. 2001. Double-stranded RNA-dependent protein kinase is not required for double-stranded RNA-induced nitric oxide synthase expression or nuclear factor-κB activation by islets. Diabetes 50:283.
32. Zhou, A., J. Paranjape, T. L. Brown, H. Nie, S. Naik, B. Dong, A. Chang, B. Trapp, R. Fairchild, C. Colmenares, and R. H. Silverman. 1997. Interferon action and apoptosis are defective in mice devoid of 2′,5′- oligoadenylate-dependent RNase L. EMBO (Eur. Mol. Biol. Organ) J. 16:6355.
33. Flodstrom, M., M. S. Horwitz, A. Maday, D. Balakrishna, E. Rodriguez, and N. Sarvetnick. 2001. A critical role for inducible nitric oxide synthase in host survival following Coxsackievirus B4 infection. Virology 281:205.
34. Vella, C., and H. Festenstein. 1992. Coxsackievirus B4 infection of the mouse pancreas: the role of natural killer cells in the control of virus replication and resistance to infection. J. Gen. Virol. 73:1379.
35. Chebath, J., P. Benech, M. Revel, and M. Vigneron. 1987. Constitutive expression of (2′,5′)oligo A synthetase confers resistance to picornavirus infection. Nature 330:587.
36. Bonnevie-Nielsen, V., A. M. Gerdes, J. Fleckner, J. S. Petersen, B. Michelsen, and T. Dyrberg. 1991. Interferon stimulates the expression of 2′,5′-oligoadenylate synthetase and MHC class I antigens in insulin-producing cells. J. Interferon Res. 11:255.
37. Bonnevie-Nielsen, V., K. Buschard, and T. Dyrberg. 1996. Differential responsiveness to interferon-α in β-cells and non-β cells. Diabetes 45:818.
38. Li, X. L., J. A. Blackford, C. S. Judge, M. Liu, W. Xiao, D. V. Kalvakolanu, and B. A. Hassel. 2000. RNase-L-dependent destabilization of interferon-induced mRNAs: a role for the 2-5A system in attenuation of the interferon response. J. Biol. Chem. 275:8880.
39. Silverman, R. H., J. J. Skehel, T. C. James, D. H. Wreschner, and I. M. Kerr. 1983. rRNA cleavage as an index of ppp(A2′p)nA activity in interferon-treated encephalomyocarditis virus-infected cells. J. Virol. 46:1051.
40. Behera, A. K., M. Kumar, R. F. Lockey, and S. S. Mohapatra. 2002. 2′,5′-Oligoadenylate synthetase plays a critical role in interferon-γ inhibition of respiratory syncytial virus infection of human epithelial cells. J. Biol. Chem. 277:25601.
41. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO (Eur. Mol. Biol. Organ) J. 14:6095.
42. Horwitz, M. S., A. La Cava, C. Fine, E. Rodriguez, A. Ilic, and N. Sarvetnick. 2000. Pancreatic expression of interferon-γ protects mice from lethal Coxsackievirus B3 infection and subsequent myocarditis. Nat. Med. 6:693.
43. Zhou, A., J. M. Paranjape, S. D. Der, B. R. Williams, and R. H. Silverman. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258:435.
44. Hui, D. J., C. R. Bhasker, W. C. Merrick, and G. C. Sen. 2003. Viral stress-inducible protein p56 inhibits translation by blocking the interaction of eIF3 with the ternary complex eIF2.GTP.Met-tRNAi. J. Biol. Chem. 278:39477.
45. Haller, O., M. Frese, and G. Kochs. 1998. Mx proteins: mediators of innate resistance to RNA viruses. Rev. Sci. Tech. 17:220.
46. Espert, L., G. Degols, C. Gongora, D. Blondel, B. R. Williams, R. H. Silverman, and N. Mechti. 2003. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. J. Biol. Chem. 278:16151.
47. Scarim, A. L., M. Arnush, L. A. Blair, J. Concepcion, M. R. Heitmeier, D. Scheuner, R. J. Kaufman, J. Ryerse, R. M. Buller, and J. A. Corbett. 2001. Mechanisms of β-cell death in response to double-stranded (ds) RNA and interferon-γ: dsRNA-dependent protein kinase apoptosis and nitric oxide-dependent necrosis. Am. J. Pathol. 159:273.
48. Hostens, K., D. Pavlovic, Y. Zambre, Z. Ling, C. Van Schravendijk, D. L. Eizirik, and D. G. Pipeleers. 1999. Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release. J. Clin. Invest. 104:67.
49. Al-khatib, K., B. R. Williams, R. H. Silverman, W. Halford, and D. J. Carr. 2003. The murine double-stranded RNA-dependent protein kinase PKR and the murine 2′,5′-oligoadenylate synthetase-dependent RNase L are required for IFN-β-mediated resistance against herpes simplex virus type 1 in primary trigeminal ganglion culture. Virology 313:126.
50. Wessely, R., K. Klingel, K. U. Knowlton, and R. Kandolf. 2001. Cardioselective infection with Coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 103:756.
51. Castelli, J. C., B. A. Hassel, K. A. Wood, X. L. Li, K. Amemiya, M. C. Dalakas, P. F. Torrence, and R. J. Youle. 1997. A study of the interferon antiviral mechanism: apoptosis activation by the 2-5A system. J. Exp. Med. 186:967.
52. Zhou, A., J. M. Paranjape, B. A. Hassel, H. Nie, S. Shah, B. Galinski, and R. H. Silverman. 1998. Impact of RNase L overexpression on viral and cellular growth and death. J. Interferon Cytokine Res. 18:953.
53. Zheng, X., R. H. Silverman, A. Zhou, T. Goto, B. S. Kwon, H. E. Kaufman, and J. M. Hill. 2001. Increased severity of HSV-1 keratitis and mortality in mice lacking the 2-5A-dependent RNase L gene. Invest. Ophthalmol. Vis. Sci. 42:120.
54. Flodstrom-Tullberg, M. 2003. Viral infections: their elusive role in regulating susceptibility to autoimmune disease. Microbes Infect. 5:911.
55. Yasukawa, H., T. Yajima, H. Duplain, M. Iwatate, M. Kido, M. Hoshijima, M. D. Weitzman, T. Nakamura, S. Woodard, D. Xiong, et al. 2003. The suppressor of cytokine signaling-1 (SOCS1) is a novel therapeutic target for enterovirus-induced cardiac injury. J. Clin. Invest. 111:469.