Interferon regulatory factor-1 is a key transcription factor in murine beta cells under immune attack

Diabetologia

Volumn 52, Issue 11, 2009, Pages 2374-2384

  Gysemans, C ^a   Callewaert, H ^a   Moore, F ^b   Nelson Holte, M ^a   Overbergh, L ^a   Eizirik, D L ^b   Mathieu, C ^a  

^a LEGENDO   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Beta cell death; Chemokines; IFN ; IRF 1; Nitric oxide; NOD mice; Type 1 diabetes

Indexed keywords

CD3 ANTIGEN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRITE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CELL DAMAGE; CELL DEATH; CELL FUNCTION; CELL STIMULATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETES MELLITUS; FEMALE; GENE DELETION; GENE EXPRESSION; GRAFT SURVIVAL; IMMUNOCOMPETENT CELL; IN VITRO GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SKIN GRAFT;

ANIMALS; CELL DEATH; CELL SURVIVAL; DNA PRIMERS; GLUCOSE; GRAFT SURVIVAL; INSULIN; INSULIN-SECRETING CELLS; INTERFERON REGULATORY FACTOR-1; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSPLANTATION, HOMOLOGOUS;

EID: 70349884094     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-009-1514-5     Document Type: Article

References (51)

1. NC Schloot S Willemen G Duinkerken RR de Vries BO Roep 1998 Cloned T cells from a recent onset IDDM patient reactive with insulin B-chain J Autoimmun 11 169 175 9650096 10.1006/jaut.1997.0183 1:STN:280:DyaK1czhtlOrsA%3D%3D (Pubitemid 28273013)
2. GG Pinkse OH Tysma CA Bergen, et al. 2005 Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes Proc Natl Acad Sci U S A 102 18425 18430 16339897 10.1073/pnas.0508621102 1:CAS:528:DC%2BD28Xpt1Gl (Pubitemid 43011242)
3. MD McKenzie NL Dudek L Mariana, et al. 2006 Perforin and Fas induced by IFN-gamma and TNF-alpha mediate beta cell death by OT-I CTL Int Immunol 18 837 846 16574667 10.1093/intimm/dxl020 1:CAS:528:DC%2BD28XmsVejtL8%3D (Pubitemid 43983279)
4. VR Sutton E Estella C Li, et al. 2006 A critical role for granzyme B, in addition to perforin and TNF-alpha, in alloreactive CTL-induced mouse pancreatic beta cell death Transplantation 81 146 154 16436955 10.1097/01.tp.0000191939. 68451.d9 1:CAS:528:DC%2BD28Xnt1GisA%3D%3D
5. NL Dudek HE Thomas L Mariana, et al. 2006 Cytotoxic T cells from T cell receptor transgenic NOD8.3 mice destroy beta-cells via the perforin and Fas pathways Diabetes 55 2412 2418 16936188 10.2337/db06-0109 1:CAS:528: DC%2BD28XpsVOrtrk%3D (Pubitemid 44871141)
6. T Mandrup-Poulsen 1996 The role of interleukin-1 in the pathogenesis of IDDM Diabetologia 39 1005 1029 8877284 10.1007/BF00400649 1:CAS:528: DyaK28XlslOgsL0%3D
7. DL Eizirik T Mandrup-Poulsen 2001 A choice of death-the signal-transduction of immune-mediated beta-cell apoptosis Diabetologia 44 2115 2133 11793013 10.1007/s001250100021 1:CAS:528:DC%2BD3MXovFWit7s%3D (Pubitemid 34015464)
8. DL Eizirik F Moore D Flamez F Ortis 2008 Use of a systems biology approach to understand pancreatic beta-cell death in type 1 diabetes Biochem Soc Trans 36 321 327 18481950 10.1042/BST0360321 1:CAS:528:DC%2BD1cXmtVKlsL4%3D (Pubitemid 351839324)
9. AK Cardozo H Heimberg Y Heremans, et al. 2001 A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta-cells J Biol Chem 276 48879 48886 11687580 10.1074/jbc. M108658200 1:CAS:528:DC%2BD38Xktlehsg%3D%3D
10. CA Gysemans L Ladriere H Callewaert, et al. 2005 Disruption of the gamma-interferon signalling pathway at the level of signal transducer and activator of transcription-1 prevents immune destruction of beta-cells Diabetes 54 2396 2403 16046307 10.2337/diabetes.54.8.2396 1:CAS:528:DC%2BD2MXnt1yntrc%3D (Pubitemid 41134268)
11. AK Cardozo M Kruhoffer R Leeman T Orntoft DL Eizirik 2001 Identification of novel cytokine-induced genes in pancreatic beta-cells by high-density oligonucleotide arrays Diabetes 50 909 920 11334433 10.2337/diabetes.50.5.909 1:CAS:528:DC%2BD3MXkvFSgtb4%3D
12. MC Chen P Proost C Gysemans C Mathieu DL Eizirik 2001 Monocyte chemoattractant protein-1 is expressed in pancreatic islets from prediabetic NOD mice and in interleukin-1 beta-exposed human and rat islet cells Diabetologia 44 325 332 11317664 10.1007/s001250051622 1:CAS:528:DC%2BD3MXhsFCmsrg%3D (Pubitemid 32234459)
13. AK Cardozo P Proost C Gysemans MC Chen C Mathieu DL Eizirik 2003 IL-1beta and IFN-gamma induce the expression of diverse chemokines and IL-15 in human and rat pancreatic islet cells, and in islets from pre-diabetic NOD mice Diabetologia 46 255 266 12627325 1:CAS:528:DC%2BD3sXhvVyrurw%3D
14. L Piemonti BE Leone R Nano, et al. 2002 Human pancreatic islets produce and secrete MCP-1/CCL2: relevance in human islet transplantation Diabetes 51 55 65 11756323 10.2337/diabetes.51.1.55 1:CAS:528:DC%2BD38Xlt1ejuw%3D%3D
15. S Merani WW Truong W Hancock CC Anderson AM Shapiro 2006 Chemokines and their receptors in islet allograft rejection and as targets for tolerance induction Cell Transplant 15 295 309 16898223 10.3727/000000006783981963
16. AP Martin S Rankin S Pitchford IF Charo GC Furtado SA Lira 2008 Increased expression of CCL2 in insulin-producing cells of transgenic mice promotes mobilization of myeloid cells from the bone marrow, marked insulitis and diabetes Diabetes 57 3025 3033 18633103 10.2337/db08-0625 1:CAS:528: DC%2BD1MXhsleisrY%3D
17. A Kroger M Koster K Schroeder H Hauser PP Mueller 2002 Activities of IRF-1 J Interferon Cytokine Res 22 5 14 11846971 10.1089/107999002753452610 1:CAS:528:DC%2BD38XhtlWksrs%3D (Pubitemid 34161278)
18. T Fujita LF Reis N Watanabe Y Kimura T Taniguchi J Vilcek 1989 Induction of the transcription factor IRF-1 and interferon-beta mRNAs by cytokines and activators of second-messenger pathways Proc Natl Acad Sci U S A 86 9936 9940 2557635 10.1073/pnas.86.24.9936 1:CAS:528:DyaK3cXhtlOju7c%3D (Pubitemid 20030749)
19. R Pine 1997 Convergence of TNF-alpha and IFN-gamma signalling pathways through synergistic induction of IRF-1/ISGF-2 is mediated by a composite GAS/kappaB promoter element Nucleic Acids Res 25 4346 4354 9336467 10.1093/nar/25.21.4346 1:CAS:528:DyaK2sXns1Gqsb0%3D (Pubitemid 27485215)
20. M Lohoff D Ferrick HW Mittrucker, et al. 1997 Interferon regulatory factor-1 is required for a T helper 1 immune response in vivo Immunity 6 681 689 9208841 10.1016/S1074-7613(00)80444-6 1:CAS:528:DyaK2sXktFCqt7o%3D (Pubitemid 27305731)
21. D Pavlovic MC Chen CA Gysemans C Mathieu DL Eizirik 1999 The role of interferon regulatory factor-1 in cytokine-induced mRNA expression and cell death in murine pancreatic beta-cells Eur Cytokine Netw 10 403 412 10477397 1:CAS:528:DyaK1MXms1ajt7Y%3D
22. T Matsuyama T Kimura M Kitagawa, et al. 1993 Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development Cell 75 83 97 8402903 1:CAS:528:DyaK3sXms1yktL4%3D
23. CA Gysemans M Waer D Valckx, et al. 2000 Early graft failure of xenogeneic islets in NOD mice is accompanied by high levels of interleukin-1 and low levels of transforming growth factor-beta mRNA in the grafts Diabetes 49 1992 1997 11117999 10.2337/diabetes.49.12.1992 1:CAS:528:DC%2BD3cXos1ejsrs%3D
24. DL Eizirik DE Tracey K Bendtzen S Sandler 1991 An interleukin-1 receptor antagonist protein protects insulin-producing beta cells against suppressive effects of interleukin-1 beta Diabetologia 34 445 448 1832112 10.1007/BF00403185 1:CAS:528:DyaK3MXmtVGktLo%3D
25. A Hoorens M Van de Casteele G Kloppel D Pipeleers 1996 Glucose promotes survival of rat pancreatic beta cells by activating synthesis of proteins which suppress a constitutive apoptotic program J Clin Invest 98 1568 1574 8833905 10.1172/JCI118950 1:CAS:528:DyaK28XmtVCmu7g%3D
26. D Liu D Pavlovic MC Chen M Flodstrom S Sandler DL Eizirik 2000 Cytokines induce apoptosis in beta-cells isolated from mice lacking the inducible isoform of nitric oxide synthase (iNOS-/-) Diabetes 49 1116 1122 10909967 10.2337/diabetes.49.7.1116 1:CAS:528:DC%2BD3cXkslOqtr8%3D
27. B De Klerck L Geboes S Hatse, et al. 2005 Pro-inflammatory properties of stromal cell-derived factor-1 (CXCL12) in collagen-induced arthritis Arthritis Res Ther 7 R1208 R1220 16277673 10.1186/ar1806
28. H Kelchtermans S Struyf B De Klerck, et al. 2007 Protective role of IFN-gamma in collagen-induced arthritis conferred by inhibition of mycobacteria-induced granulocyte chemotactic protein-2 production J Leukoc Biol 81 1044 1053 17200147 10.1189/jlb.0806486 1:CAS:528:DC%2BD2sXkt1Oit7c%3D (Pubitemid 46495653)
29. DA Cunha P Hekerman L Ladriere, et al. 2008 Initiation and execution of lipotoxic ER stress in pancreatic beta-cells J Cell Sci 121 2308 2318 18559892 10.1242/jcs.026062 1:CAS:528:DC%2BD1cXpvVKqsbg%3D
30. M Cnop L Ladriere P Hekerman, et al. 2007 Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis J Biol Chem 282 3989 3997 17158450 10.1074/jbc.M607627200 1:CAS:528:DC%2BD2sXht1OjsrY%3D (Pubitemid 47084497)
31. I Kharroubi L Ladriere AK Cardozo Z Dogusan M Cnop DL Eizirik 2004 Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress Endocrinology 145 5087 5096 15297438 10.1210/en.2004-0478 1:CAS:528: DC%2BD2cXptVyhurs%3D (Pubitemid 39551129)
32. L Overbergh D Valckx M Waer C Mathieu 1999 Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR Cytokine 11 305 312 10328870 10.1006/cyto.1998.0426 1:CAS:528:DyaK1MXislWktbk%3D (Pubitemid 29213178)
33. L Overbergh C Gysemans C Mathieu 2006 Quantification of chemokines by real-time reverse transcriptase PCR: applications in type 1 diabetes Expert Rev Mol Diagn 6 51 64 16359267 10.1586/14737159.6.1.51 1:CAS:528: DC%2BD28XhtFWlsb0%3D
34. C Gysemans K Stoffels A Giulietti, et al. 2003 Prevention of primary non-function of islet xenografts in autoimmune diabetic NOD mice by anti-inflammatory agents Diabetologia 46 1115 1123 12879250 10.1007/s00125-003- 1154-0 1:CAS:528:DC%2BD3sXmtFCqtb0%3D (Pubitemid 37041242)
35. HI Callewaert CA Gysemans L Ladriere, et al. 2007 Deletion of STAT-1 pancreatic islets protects against streptozotocin-induced diabetes and early graft failure but not against late rejection Diabetes 56 2169 2173 17473223 10.2337/db07-0052 1:CAS:528:DC%2BD2sXos12qsbs%3D (Pubitemid 47195839)
36. CA Gysemans D Pavlovic R Bouillon DL Eizirik C Mathieu 2001 Dual role of interferon-γ signalling pathway in sensitivity of pancreatic beta cells to immune destruction Diabetologia 44 567 574 11380074 10.1007/s001250051662 1:CAS:528:DC%2BD3MXivVSis74%3D (Pubitemid 32411272)
37. T Nakazawa J Satoh K Takahashi, et al. 2001 Complete suppression of insulitis and diabetes in NOD mice lacking interferon regulatory factor-1 J Autoimmun 17 119 125 11591120 10.1006/jaut.2001.0531 1:STN:280: DC%2BD3Mrktlegsg%3D%3D (Pubitemid 32928207)
38. K Bendtzen T Mandrup-Poulsen J Nerup JH Nielsen CA Dinarello M Svenson 1986 Cytotoxicity of human pI 7 interleukin-1 for pancreatic islets of Langerhans Science 232 1545 1547 3086977 10.1126/science.3086977 1:STN:280:DyaL283jsFCnuw%3D%3D (Pubitemid 16061563)
39. MD Dayer-Metroz CB Wollheim P Seckinger JM Dayer 1989 A natural interleukin 1 (IL-1) inhibitor counteracts the inhibitory effect of IL-1 on insulin production in cultured rat pancreatic islets J Autoimmun 2 163 171 2527507 10.1016/0896-8411(89)90152-2 1:STN:280:DyaL1MzltFaltg%3D%3D
40. JO Sandberg DL Eizirik S Sandler DE Tracey A Andersson 1993 Treatment with an interleukin-1 receptor antagonist protein prolongs mouse islet allograft survival Diabetes 42 1845 1851 8243831 10.2337/diabetes.42.12.1845 1:CAS:528:DyaK2cXivFagsw%3D%3D
41. JO Sandberg DL Eizirik S Sandler 1997 IL-1 receptor antagonist inhibits recurrence of disease after syngeneic pancreatic islet transplantation to spontaneously diabetic non-obese diabetic (NOD) mice Clin Exp Immunol 108 314 317 9158104 10.1046/j.1365-2249.1997.3771275.x 1:CAS:528:DyaK2sXjsFGnt7Y%3D
42. MY Donath T Mandrup-Poulsen 2008 The use of interleukin-1-receptor antagonists in the treatment of diabetes mellitus Nat Clin Pract Endocrinol Metab 4 240 241 18317479 10.1038/ncpendmet0783 1:CAS:528:DC%2BD1cXkvFWmt74%3D (Pubitemid 351571135)
43. M Montolio M Biarnes N Tellez J Escoriza J Soler E Montanya 2007 Interleukin-1beta and inducible form of nitric oxide synthase expression in early syngeneic islet transplantation J Endocrinol 192 169 177 17210754 10.1677/joe.1.06968 1:CAS:528:DC%2BD2sXktlKqtbY%3D (Pubitemid 46444407)
44. HE Thomas R Darwiche JA Corbett TW Kay 2002 Interleukin-1 plus gamma-interferon-induced pancreatic beta-cell dysfunction is mediated by beta-cell nitric oxide production Diabetes 51 311 316 11812737 10.2337/diabetes.51.2.311 1:CAS:528:DC%2BD38XhtVaqur8%3D
45. DB Kaufman JL Platt FL Rabe DL Dunn FH Bach DE Sutherland 1990 Differential roles of Mac-1+ cells, and CD4+ and CD8+ T lymphocytes in primary non-function and classic rejection of islet allografts J Exp Med 172 291 302 2113565 10.1084/jem.172.1.291 1:STN:280:DyaK3c3ptlKqsA%3D%3D (Pubitemid 20217271)
46. MS Baker X Chen AR Rotramel JJ Nelson DB Kaufman 2003 Interferon regulatory factor-1 down-regulates cytokine-induced IP-10 expression in pancreatic islets Surgery 134 134 141 12947309 10.1067/msy.2003.236 (Pubitemid 37070330)
47. R Kamijo H Harada T Matsuyama, et al. 1994 Requirement for transcription factor IRF-1 in NO synthase induction in macrophages Science 263 1612 1615 7510419 10.1126/science.7510419 1:CAS:528:DyaK2cXitFemu7w%3D
48. M Fujimura T Tominaga I Kato, et al. 1997 Attenuation of nitric oxide synthase induction in IRF-1-deficient glial cells Brain Res 759 247 250 9221944 10.1016/S0006-8993(97)00264-3 1:CAS:528:DyaK2sXjslKnur0%3D (Pubitemid 27286702)
49. X Teng H Zhang C Snead JD Catravas 2002 Molecular mechanisms of iNOS induction by IL-1 beta and IFN-gamma in rat aortic smooth muscle cells Am J Physiol Cell Physiol 282 C144 C152 11742807 1:CAS:528:DC%2BD38XlsVKnug%3D%3D
50. LA Blair LB Maggi Jr AL Scarim JA Corbett 2002 Role of interferon regulatory factor-1 in double-stranded RNA-induced iNOS expression by mouse islets J Biol Chem 277 359 365 11694524 10.1074/jbc.M109819200 1:CAS:528:DC%2BD38XjslGiug%3D%3D (Pubitemid 34952066)
51. MI Darville DL Eizirik 1998 Regulation by cytokines of the inducible nitric oxide synthase promoter in insulin-producing cells Diabetologia 41 1101 1108 9754830 10.1007/s001250051036 1:CAS:528:DyaK1cXls12hsr4%3D (Pubitemid 28394417)