Regulation and function of the cytosolic viral RNA sensor RIG-I in pancreatic beta cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 11, 2009, Pages 1768-1775

  García, Mónica ^a   Dogusan, Zeynep ^a   Moore, Fabrice ^a   Sato, Shintaro ^b   Hartmann, Gunther ^c   Eizirik, Decio L ^a   Rasschaert, Joanne ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b University of Tokyo   (Japan)

^c UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Apoptosis; Diabetes; RNA helicases; Toll like receptor 3

Indexed keywords

BETA INTERFERON; CYTOKINE; DOUBLE STRANDED RNA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; LIPOFECTAMINE; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; POLYINOSINIC POLYCYTIDYLIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL CULTURE; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; CYTOSOL; DENDRITIC CELL; DISEASE ASSOCIATION; ENTEROVIRUS; ENTEROVIRUS INFECTION; FLUORESCENCE ACTIVATED CELL SORTING; GENE ACTIVATION; GENE DELETION; GENETIC PREDISPOSITION; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; CYTOSOL; DEAD-BOX RNA HELICASES; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; GENE DELETION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSULIN-SECRETING CELLS; INTERFERON-BETA; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NF-KAPPA B; POLY I-C; PROMOTER REGIONS, GENETIC; RATS; RATS, WISTAR; RNA, DOUBLE-STRANDED; RNA, VIRAL; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

MUS; RATTUS;

EID: 71749111445     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.09.005     Document Type: Article

References (70)

1. Gillespie K.M. Type 1 diabetes: pathogenesis and prevention. CMAJ 175 (2006) 165-170
2. Honeyman M. How robust is the evidence for viruses in the induction of type 1 diabetes?. Curr. Opin. Immunol. 17 (2005) 616-623
3. Drescher K.M., and Tracy S.M. The CVB and etiology of type 1 diabetes. Curr. Top. Microbiol. Immunol. 323 (2008) 259-274
4. Nairn C., Galbraith D.N., Taylor K.W., and Clements G.B. Enterovirus variants in the serum of children at the onset of type 1 diabetes mellitus. Diabet. Med. 16 (1999) 509-513
5. Chehadeh W., Weill J., Vantyghem M.C., Alm G., Lefebvre J., Wattre P., and Hober D. Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J. Infect. Dis. 181 (2000) 1929-1939
6. Dotta F., Censini S., van Halteren A.G., Marselli L., Masini M., Dionisi S., Mosca F., Boggi U., Muda A.O., Prato S.D., Elliott J.F., Covacci A., Rappuoli R., Roep B.O., and Marchetti P. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5115-5120
7. Richardson S.J., Willcox A., Bone A.J., Foulis A.K., and Morgan N.G. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52 (2009) 1143-1151
8. Muir P., Singh N.B., and Banatvala J.E. Enterovirus-specific serum IgA antibody responses in patients with acute infections, chronic cardiac disease, and recently diagnosed insulin-dependent diabetes mellitus. J. Med. Virol. 32 (1990) 236-242
9. Elfaitouri A., Berg A.K., Frisk G., Yin H., Tuvemo T., and Blomberg J. Recent enterovirus infection in type 1 diabetes: evidence with a novel IgM method. J. Med. Virol. 79 (2007) 1861-1867
10. Andreoletti L., Hober D., Hober-Vandenberghe C., Fajardy I., Belaich S., Lambert V., Vantyghem M.C., Lefebvre J., Wattre P., and Coxsackie B. Virus infection and beta cell autoantibodies in newly diagnosed IDDM adult patients. Clin. Diagn. Virol. 9 (1998) 125-133
11. Frisk G., and Tuvemo T. 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 (2004) 450-459
12. Meylan E., Tschopp J., and Karin M. Intracellular pattern recognition receptors in the host response. Nature 442 (2006) 39-44
13. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
14. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses, Nat. Immunol. 5 (2004) 730-737
15. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.S., Reis e Sousa C., Matsuura Y., Fujita T., and Akira S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
16. Ahlquist P. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 4 (2006) 371-382
17. Jacobs B.L., and Langland J.O. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219 (1996) 339-349
18. Majde J.A., Guha-Thakurta N., Chen Z., Bredow S., and Krueger J.M. Spontaneous release of stable viral double-stranded RNA into the extracellular medium by influenza virus-infected MDCK epithelial cells: implications for the viral acute phase response. Arch. Virol. 143 (1998) 2371-2380
19. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int. Immunol. 17 (2005) 1-14
20. Heitmeier M.R., Scarim A.L., and Corbett J.A. Double-stranded RNA inhibits beta-cell function and induces islet damage by stimulating beta-cell production of nitric oxide. J. Biol. Chem. 274 (1999) 12531-12536
21. Sobel D.O., Newsome J., Ewel C.H., Bellanti J.A., Abbassi V., Creswell K., and Blair O. Poly I:C induces development of diabetes mellitus in BB rat. Diabetes 41 (1992) 515-520
22. Liu D., Cardozo A.K., Darville M.I., and Eizirik D.L. Double-stranded RNA cooperates with interferon-gamma and IL-1 beta to induce both chemokine expression and nuclear factor-kappa B-dependent apoptosis in pancreatic beta-cells: potential mechanisms for viral-induced insulitis and beta-cell death in type 1 diabetes mellitus. Endocrinology 143 (2002) 1225-1234
23. Rasschaert J., Ladriere L., Urbain M., Dogusan Z., Katabua B., Sato S., Akira S., Gysemans C., Mathieu C., and Eizirik D.L. Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA+ interferon-gamma-induced apoptosis in primary pancreatic beta-cells. J. Biol. Chem. 280 (2005) 33984-33991
24. Ylipaasto P., Kutlu B., Rasilainen S., Rasschaert J., Salmela K., Teerijoki H., Korsgren O., Lahesmaa R., Hovi T., Eizirik D.L., Otonkoski T., and Roivainen M. Global profiling of coxsackievirus- and cytokine-induced gene expression in human pancreatic islets. Diabetologia 48 (2005) 1510-1522
25. Hultcrantz M., Huhn M.H., Wolf M., Olsson A., Jacobson S., Williams B.R., Korsgren O., and Flodstrom-Tullberg M. Interferons induce an antiviral state in human pancreatic islet cells. Virology 367 (2007) 92-101
26. Sen G.C., and Sarkar S.N. Transcriptional signaling by double-stranded RNA: role of TLR3. Cytokine Growth Factor Rev. 16 (2005) 1-14
27. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O., and Akira S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23 (2005) 19-28
28. Dogusan Z., Garcia M., Flamez D., Alexopoulou L., Goldman M., Gysemans C., Mathieu C., Libert C., Eizirik D.L., and Rasschaert J. Double-stranded RNA induces pancreatic beta-cell apoptosis by activation of the toll-like receptor 3 and interferon regulatory factor 3 pathways. Diabetes 57 (2008) 1236-1245
29. Creagh E.M., and O'Neill L.A. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 27 (2006) 352-357
30. Yoneyama M., and Fujita T. RIG-I family RNA helicases: cytoplasmic sensor for antiviral innate immunity. Cytokine Growth Factor Rev. 18 (2007) 545-551
31. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., and Reis e Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314 (2006) 997-1001
32. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., Endres S., and Hartmann G. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006) 994-997
33. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z., and Shu H.B. VISA is an adapter protein required for virus-triggered IFN-beta signalling. Mol. Cell 19 (2005) 727-740
34. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale Jr. M., Akira S., Yonehara S., Kato A., and Fujita T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175 (2005) 2851-2858
35. Johnson C.L., and Gale Jr. M. CARD games between virus and host get a new player. Trends Immunol. 27 (2006) 1-4
36. Cardozo A.K., Kruhoffer M., Leeman R., Orntoft T., and Eizirik D.L. Identification of novel cytokine-induced genes in pancreatic beta-cells by high-density oligonucleotide arrays. Diabetes 50 (2001) 909-920
37. Giulietti A., Overbergh L., Valckx D., Decallonne B., Bouillon R., and Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25 (2001) 386-401
38. Liu D., Darville M., and Eizirik D.L. Double-stranded ribonucleic acid (RNA) induces beta-cell Fas messenger RNA expression and increases cytokine-induced beta-cell apoptosis. Endocrinology 142 (2001) 2593-2599
39. Hoorens A., Van de Casteele M., Kloppel G., and Pipeleers D. Glucose promotes survival of rat pancreatic beta cells by activating synthesis of proteins which suppress a constitutive apoptotic program. J. Clin. Invest. 98 (1996) 1568-1574
40. Kharroubi I., Ladriere L., Cardozo A.K., Dogusan Z., Cnop M., and Eizirik D.L. Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 145 (2004) 5087-5096
41. Ling Z., Van de Casteele M., Eizirik D.L., and Pipeleers D.G. Interleukin-1beta-induced alteration in a beta-cell phenotype can reduce cellular sensitivity to conditions that cause necrosis but not to cytokine-induced apoptosis. Diabetes 49 (2000) 340-345
42. Eizirik D.L., Moore F., Flamez D., and Ortis F. Use of a systems biology approach to understand pancreatic beta-cell death in type 1 diabetes. Biochem. Soc. Trans. 36 (2008) 321-327
43. Pavlovic D., Andersen N.A., Mandrup-Poulsen T., and Eizirik D.L. Activation of extracellular signal-regulated kinase (ERK)1/2 contributes to cytokine-induced apoptosis in purified rat pancreatic beta-cells. Eur. Cytokine Netw. 11 (2000) 267-274
44. Liu D., Pavlovic D., Chen M.C., Flodstrom M., Sandler S., and Eizirik D.L. Cytokines induce apoptosis in beta-cells isolated from mice lacking the inducible isoform of nitric oxide synthase (iNOS-/-). Diabetes 49 (2000) 1116-1122
45. Delaney C.A., Pavlovic D., Hoorens A., Pipeleers D.G., and Eizirik D.L. Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells. Endocrinology 138 (1997) 2610-2614
46. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., and Akira S. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301 (2003) 640-643
47. Jun H.S., and Yoon J.W. The role of viruses in type I diabetes: two distinct cellular and molecular pathogenic mechanisms of virus-induced diabetes in animals. Diabetologia 44 (2001) 271-285
48. Eizirik D.L., Colli M.L., and Ortis F. The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat. Rev. Endocrinol. 5 (2009) 219-226
49. Taniguchi T., and Takaoka A. The interferon-alpha/beta system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors. Curr. Opin. Immunol. 14 (2002) 111-116
50. Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., Garcia-Sastre A., Katze M.G., and Gale Jr. M. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol 82 (2008) 335-345
51. Liu P., Jamaluddin M., Li K., Garofalo R.P., Casola A., and Brasier A.R. Retinoic acid-inducible gene I mediates early antiviral response and Toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J. Virol. 81 (2007) 1401-1411
52. Gee P., Chua P.K., Gevorkyan J., Klumpp K., Najera I., Swinney D.C., and Deval J. Essential role of the N-terminal domain in the regulation of RIG-I ATPase activity. J. Biol. Chem. 283 (2008) 9488-9496
53. Yoneyama M., Onomoto K., and Fujita T. Cytoplasmic recognition of RNA. Adv. Drug Deliv. Rev. 60 (2008) 841-846
54. Rintahaka J., Wiik D., Kovanen P.E., Alenius H., and Matikainen S. Cytosolic antiviral RNA recognition pathway activates caspases 1 and 3. J. Immunol. 180 (2008) 1749-1757
55. Heimberg H., Heremans Y., Jobin C., Leemans R., Cardozo A.K., Darville M., and Eizirik D.L. Inhibition of cytokine-induced NF-kappaB activation by adenovirus-mediated expression of a NF-kappaB super-repressor prevents beta-cell apoptosis. Diabetes 50 (2001) 2219-2224
56. Colli M.L., Moore F., Gurzov E.N., Ortis F., and Eizirik D.L. PTPN2 and MDA5, two candidate genes for type 1 diabetes, modify beta cell responses to double-stranded RNA. Diabetologia 52 Suppl.1 (2009) S 153
57. Nallagatla S.R., Hwang J., Toroney R., Zheng X., Cameron C.E., and Bevilacqua P.C. 5′-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318 (2007) 1455-1458
58. Li K., Chen Z., Kato N., Gale Jr. M., and Lemon S.M. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J. Biol. Chem. 280 (2005) 16739-16747
59. Andersen J.M., Al-Khairy D., and Ingalls R.R. Innate immunity at the mucosal surface: role of toll-like receptor 3 and toll-like receptor 9 in cervical epithelial cell responses to microbial pathogens. Biol. Reprod. 74 (2006) 824-831
60. Kawai T., and Akira S. Antiviral signaling through pattern recognition receptors. J. Biochem. (Tokyo) 141 (2007) 137-145
61. Malmgaard L. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24 (2004) 439-454
62. Kalali B.N., Kollisch G., Mages J., Muller T., Bauer S., Wagner H., Ring J., Lang R., Mempel M., and Ollert M. Double-stranded RNA induces an antiviral defense status in epidermal keratinocytes through TLR3-, PKR-, and MDA5/RIG-I-mediated differential signalling. J. Immunol. 181 (2008) 2694-2704
63. Uehara A., Fujimoto Y., Fukase K., and Takada H. Various human epithelial cells express functional Toll-like receptors, NOD1 and NOD2 to produce anti-microbial peptides, but not proinflammatory cytokines. Mol. Immunol. 44 (2007) 3100-3111
64. Rasschaert J., Liu D., Kutlu B., Cardozo A.K., Kruhoffer M., ORntoft T.F., and Eizirik D.L. Global profiling of double stranded RNA- and IFN-gamma-induced genes in rat pancreatic beta cells. Diabetologia 46 (2003) 1641-1657
65. Chehadeh W., Kerr-Conte J., Pattou F., Alm G., Lefebvre J., Wattré P., and Hober D. Persistent infection of human pancreatic islets by coxsackievirus B is associated with alpha interferon synthesis in beta cells. J. Virol. 74 (2000) 10153-10164
66. Foulis A.K., Farquharson M.A., and Meager A. Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus. Lancet 2 (1987) 1423-1427
67. Huang X., Yuang J., Goddard A., Foulis A., James R.F., Lernmark A., Pujol-Borrell R., Rabinovitch A., Somoza N., and Stewart T.A. Interferon expression in the pancreases of patients with type I diabetes. Diabetes 44 (1995) 658-664
68. Devendra D., and Eisenbarth G.S. Interferon alpha-a potential link in the pathogenesis of viral-induced type 1 diabetes and autoimmunity. Clin. Immunol. 111 (2004) 225-233
69. Lang K.S., Recher M., Junt T., Navarini A.A., Harris N.L., Freigang S., Odermatt B., Conrad C., Ittner L.M., Bauer S., Luther S.A., Uematsu S., Akira S., Hengartner H., and Zinkernagel R.M. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat. Med. 11 (2005) 138-145
70. Wen L., Peng J., Li Z., and Wong F.S. The effect of innate immunity on autoimmune diabetes and the expression of Toll-like receptors on pancreatic islets. J. Immunol. 172 (2004) 3173-3180