Suppressor of cytokine signaling-1 inhibits caspase activation and protects from cytokine-induced beta cell death

Cellular and Molecular Life Sciences

Volumn 66, Issue 23, 2009, Pages 3787-3795

  Zaitseva, Irina I ^a   Hultcrantz, Monica ^a   Sharoyko, Vladimir ^a   Flodström Tullberg, Malin ^a   Zaitsev, Sergei V ^a,b   Berggren, Per Olof ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Apoptosis; Caspase; Cytokine; Interferon gamma; Islets of Langerhans; Pancreatic beta cell

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; GLUCOSE; INSULIN; NITRIC OXIDE; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 1BETA; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CELL DEATH; CELL PROTECTION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE OVEREXPRESSION; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CASPASES; CELL DEATH; CYTOKINES; ENZYME ACTIVATION; INSULIN; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; JANUS KINASES; MICE; MICE, INBRED C57BL; NITRIC OXIDE; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 70849110137     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0151-y     Document Type: Article

References (55)

1. J Chandra B Zhivotovsky S Zaitsev L Juntti-Berggren PO Berggren S Orrenius 2001 Role of apoptosis in pancreatic beta-cell death in diabetes Diabetes 50 Suppl 1 S44 S47 10.2337/diabetes.50.2007.S44 1:CAS:528: DC%2BD3MXhtVOgtrs%3D 11272200
2. T Mandrup-Poulsen 2003 Beta cell death and protection Ann N Y Acad Sci 1005 32 42 10.1196/annals.1288.005 14679038 (Pubitemid 38507732)
3. M Hultcrantz S Jacobson NJ Hill P Santamaria M Flodstrom-Tullberg 2009 The target cell response to cytokines governs the autoreactive T cell repertoire in the pancreas of NOD mice Diabetologia 52 299 305 10.1007/s00125-008-1193-7 1:CAS:528:DC%2BD1MXjvFGjtw%3D%3D 19031069
4. M Flodstrom-Tullberg D Yadav R Hagerkvist D Tsai P Secrest A Stotland N Sarvetnick 2003 Target cell expression of suppressor of cytokine signaling-1 prevents diabetes in the NOD mouse Diabetes 52 2696 2700 10.2337/diabetes.52.11. 2696 14578288 (Pubitemid 37339699)
5. MM Chong Y Chen R Darwiche NL Dudek W Irawaty P Santamaria J Allison TW Kay HE Thomas 2004 Suppressor of cytokine signaling-1 overexpression protects pancreatic beta cells from CD8 + T cell-mediated autoimmune destruction J Immunol 172 5714 5721 1:CAS:528:DC%2BD2cXjt1Ckurw%3D 15100317
6. AM Barral HE Thomas EM Ling R Darwiche E Rodrigo U Christen M Ejrnaes T Wolfe TW Kay MG von Herrath 2006 SOCS-1 protects from virally-induced CD8 T cell mediated type 1 diabetes J Autoimmun 27 166 173 10.1016/j.jaut.2006.08.002 1:CAS:528:DC%2BD28Xht1SjsrvL 17045460 (Pubitemid 46048591)
7. JA Corbett MA Sweetland JL Wang JR Lancaster Jr ML McDaniel 1993 Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans Proc Natl Acad Sci USA 90 1731 1735 10.1073/pnas.90.5.1731 1:CAS:528:DyaK3sXhs1Ogs7w%3D 8383325
8. C Southern D Schulster IC Green 1990 Inhibition of insulin secretion by interleukin-1 beta and tumour necrosis factor-alpha via an L-arginine-dependent nitric oxide generating mechanism FEBS Lett 276 42 44 10.1016/0014-5793(90) 80502-A 1:CAS:528:DyaK3MXktVOqtw%3D%3D 2265709
9. V Hadjivassiliou MH Green RF James SM Swift HA Clayton IC Green 1998 Insulin secretion, DNA damage, and apoptosis in human and rat islets of Langerhans following exposure to nitric oxide, peroxynitrite, and cytokines Nitric Oxide 2 429 441 10.1006/niox.1998.0203 1:CAS:528:DyaK1MXislWrsbg%3D 10342486 (Pubitemid 29231176)
10. DL Eizirik T Mandrup-Poulsen 2001 A choice of death-the signal-transduction of immune-mediated beta-cell apoptosis Diabetologia 44 2115 2133 10.1007/s001250100021 1:CAS:528:DC%2BD3MXovFWit7s%3D 11793013 (Pubitemid 34015464)
11. M Cetkovic-Cvrlje DL Eizirik 1994 TNF-alpha and IFN-gamma potentiate the deleterious effects of IL-1 beta on mouse pancreatic islets mainly via generation of nitric oxide Cytokine 6 399 406 10.1016/1043-4666(94)90064-7 1:CAS:528:DyaK2cXlsFClu78%3D 7948748 (Pubitemid 24263885)
12. SV Zaitsev IB Appelskog IL Kapelioukh SN Yang M Kohler S Efendic PO Berggren 2001 Imidazoline compounds protect against interleukin 1beta-induced beta-cell apoptosis Diabetes 50 Suppl 1 S70 S76 10.2337/diabetes.50.2007.S70 1:CAS:528:DC%2BD3MXhtVOgt74%3D 11272206
13. M Todaro F Di Gaudio M Lavitrano G Stassi G Papaccio 2003 Islet beta-cell apoptosis triggered in vivo by interleukin-1beta is not related to the inducible nitric oxide synthase pathway: evidence for mitochondrial function impairment and lipoperoxidation Endocrinology 144 4264 4271 10.1210/en.2003-0385 1:CAS:528:DC%2BD3sXns1Srt7Y%3D 12960105 (Pubitemid 37204822)
14. M Kohler SV Zaitsev II Zaitseva B Leibiger IB Leibiger M Turunen IL Kapelioukh L Bakkman IB Appelskog JB de Monvel G Imreh PO Berggren 2003 On-line monitoring of apoptosis in insulin-secreting cells Diabetes 52 2943 2950 10.2337/diabetes.52.12.2943 14633855 (Pubitemid 37466864)
15. P Augstein J Bahr G Wachlin P Heinke S Berg E Salzsieder LC Harrison 2004 Cytokines activate caspase-3 in insulinoma cells of diabetes-prone NOD mice directly and via upregulation of Fas J Autoimmun 23 301 309 10.1016/j.jaut.2004. 09.006 1:CAS:528:DC%2BD2cXhtVagsrfJ 15571924 (Pubitemid 39574805)
16. SJ Riedl Y Shi 2004 Molecular mechanisms of caspase regulation during apoptosis Nat Rev Mol Cell Biol 5 897 907 10.1038/nrm1496 1:CAS:528: DC%2BD2cXptFemsL0%3D 15520809 (Pubitemid 39486541)
17. II Zaitseva J Storling T Mandrup-Poulsen PO Berggren SV Zaitsev 2008 The imidazoline RX871024 induces death of proliferating insulin-secreting cells by activation of c-jun N-terminal kinase Cell Mol Life Sci 65 1248 1255 10.1007/s00018-008-7564-x 1:CAS:528:DC%2BD1cXkvFynsL0%3D 18278435
18. K Suk S Kim YH Kim KA Kim I Chang H Yagita M Shong MS Lee 2001 IFN-gamma/TNF-alpha synergism as the final effector in autoimmune diabetes: a key role for STAT1/IFN regulatory factor-1 pathway in pancreatic beta cell death J Immunol 166 4481 4489 1:CAS:528:DC%2BD3MXit1Okt78%3D 11254704
19. JL Contreras CA Smyth G Bilbao CJ Young JA Thompson DE Eckhoff 2002 17beta-Estradiol protects isolated human pancreatic islets against proinflammatory cytokine-induced cell death: molecular mechanisms and islet functionality Transplantation 74 1252 1259 10.1097/00007890-200211150-00010 1:CAS:528:DC%2BD38XptVShsr4%3D 12451262
20. MMW Chong HE Thomas TWH Kay 2002 Suppressor of cytokine signaling-1 regulates the sensitivity of pancreatic beta cells to tumor necrosis factor J Biol Chem 277 27945 27952 10.1074/jbc.M110214200 1:CAS:528:DC%2BD38XlvFKgt7c%3D 12032139 (Pubitemid 34966742)
21. A Hoorens G Stange D Pavlovic D Pipeleers 2001 Distinction between interleukin-1-induced necrosis and apoptosis of islet cells Diabetes 50 551 557 10.2337/diabetes.50.3.551 1:CAS:528:DC%2BD3MXhslGhu7Y%3D 11246874
22. LA Stephens HE Thomas L Ming M Grell R Darwiche L Volodin TW Kay 1999 Tumor necrosis factor-alpha-activated cell death pathways in NIT-1 insulinoma cells and primary pancreatic beta cells Endocrinology 140 3219 3227 10.1210/en.140.7.3219 1:CAS:528:DyaK1MXktVensbo%3D 10385418
23. LC Platanias 2005 Mechanisms of type-I- and type-II-interferon-mediated signalling Nat Rev Immunol 5 375 386 10.1038/nri1604 1:CAS:528: DC%2BD2MXjs1OkurY%3D 15864272 (Pubitemid 40685987)
24. JJ O'Shea M Gadina RD Schreiber 2002 Cytokine signaling in 2002: new surprises in the Jak/Stat pathway Cell 109 Suppl S121 S131 10.1016/S0092- 8674(02)00701-8 11983158 (Pubitemid 34457857)
25. DR Wesemann H Qin N Kokorina EN Benveniste 2004 TRADD interacts with STAT1-alpha and influences interferon-gamma signaling Nat Immunol 5 199 207 10.1038/ni1025 1:CAS:528:DC%2BD2cXntFWntw%3D%3D 14730360 (Pubitemid 38208362)
26. Y Wang TR Wu S Cai T Welte YE Chin 2000 Stat1 as a component of tumor necrosis factor alpha receptor 1-TRADD signaling complex to inhibit NF-kappaB activation Mol Cell Biol 20 4505 4512 10.1128/MCB.20.13.4505-4512.2000 1:CAS:528:DC%2BD3cXksVOjtLg%3D 10848577 (Pubitemid 30396098)
27. H Nguyen M Chatterjee-Kishore Z Jiang Y Qing CV Ramana J Bayes M Commane X Li GR Stark 2003 IRAK-dependent phosphorylation of Stat1 on serine 727 in response to interleukin-1 and effects on gene expression J Interferon Cytokine Res 23 183 192 10.1089/107999003765027384 1:CAS:528:DC%2BD3sXjsFeisrk%3D 12856330 (Pubitemid 36528981)
28. S Wormald DJ Hilton 2004 Inhibitors of cytokine signal transduction J Biol Chem 279 821 824 10.1074/jbc.R300030200 1:CAS:528:DC%2BD2cXhtV2htw%3D%3D 14607831 (Pubitemid 38082600)
29. Y Qing AP Costa-Pereira D Watling GR Stark 2005 Role of tyrosine 441 of interferon-gamma receptor subunit 1 in SOCS-1-mediated attenuation of STAT1 activation J Biol Chem 280 1849 1853 10.1074/jbc.M409863200 1:CAS:528: DC%2BD2MXksVWjtA%3D%3D 15522878
30. GM Davey WR Heath R Starr 2006 SOCS1: a potent and multifaceted regulator of cytokines and cell-mediated inflammation Tissue Antigens 67 1 9 10.1111/j.1399-0039.2005.00532.x 1:CAS:528:DC%2BD28XitFOltrs%3D 16451196 (Pubitemid 43381210)
31. A Mansell R Smith SL Doyle P Gray JE Fenner PJ Crack SE Nicholson DJ Hilton LA O'Neill PJ Hertzog 2006 Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation Nat Immunol 7 148 155 10.1038/ni1299 1:CAS:528:DC%2BD28Xlt1ertg%3D%3D 16415872 (Pubitemid 43135880)
32. R Nakagawa T Naka H Tsutsui M Fujimoto A Kimura T Abe E Seki S Sato O Takeuchi K Takeda S Akira K Yamanishi I Kawase K Nakanishi T Kishimoto 2002 SOCS-1 participates in negative regulation of LPS responses Immunity 17 677 687 10.1016/S1074-7613(02)00449-1 1:CAS:528:DC%2BD38XovF2ls7w%3D 12433373 (Pubitemid 35351512)
33. I Kinjyo T Hanada K Inagaki-Ohara H Mori D Aki M Ohishi H Yoshida M Kubo A Yoshimura 2002 SOCS1/JAB is a negative regulator of LPS-induced macrophage activation Immunity 17 583 591 10.1016/S1074-7613(02)00446-6 1:CAS:528:DC%2BD38XovF2lsro%3D 12433365 (Pubitemid 35351504)
34. M Flodstrom A Maday D Balakrishna MM Cleary A Yoshimura N Sarvetnick 2002 Target cell defense prevents the development of diabetes after viral infection Nat Immunol 3 373 382 10.1038/ni771 1:CAS:528:DC%2BD38Xis1Kksbc%3D 11919579 (Pubitemid 34308626)
35. M Solomon M Flodstrom-Tullberg N Sarvetnick 2005 Differences in suppressor of cytokine signaling-1 (SOCS-1) expressing islet allograft destruction in normal BALB/c and spontaneously-diabetic NOD recipient mice Transplantation 79 1104 1109 10.1097/01.TP.0000162979.66954.53 1:CAS:528:DC%2BD2MXjvF2ht7c%3D 15880051 (Pubitemid 40664005)
36. A Lernmark 1974 The preparation of, and studies on, free cell suspensions from mouse pancreatic islets Diabetologia 10 431 438 10.1007/BF01221634 1:STN:280:DyaE2M7htlaqtg%3D%3D 4375640
37. CB Wollheim P Meda PA Halban 1990 Isolation of pancreatic islets and primary culture of the intact microorgans or of dispersed islet cells Methods Enzymol 192 188 223 10.1016/0076-6879(90)92071-K 1:STN:280:DyaK3M7mtlertg%3D%3D 1963663
38. II Zaitseva V Sharoyko J Storling S Efendic C Guerin T Mandrup-Poulsen P Nicotera PO Berggren SV Zaitsev 2006 RX871024 reduces NO production but does not protect against pancreatic beta-cell death induced by proinflammatory cytokines Biochem Biophys Res Commun 347 1121 1128 10.1016/j.bbrc.2006.06.197 1:CAS:528:DC%2BD28Xns1Gktb4%3D 16870144 (Pubitemid 44118230)
39. IB Efanova SV Zaitsev B Zhivotovsky M Kohler S Efendic S Orrenius PO Berggren 1998 Glucose and tolbutamide induce apoptosis in pancreatic beta-cells: A process dependent on intracellular Ca2+ concentration J Biol Chem 273 33501 33507 10.1074/jbc.273.50.33501 1:CAS:528:DyaK1MXms1U%3D 9837930 (Pubitemid 29005733)
40. SV Zaitsev AM Efanov IB Efanova O Larsson CG Ostenson G Gold PO Berggren S Efendic 1996 Imidazoline compounds stimulate insulin release by inhibition of K(ATP) channels and interaction with the exocytotic machinery Diabetes 45 1610 1618 10.2337/diabetes.45.11.1610 1:CAS:528:DyaK28XmsVyqsrk%3D 8866568
41. R Laffranchi GA Spinas 1997 Interferon-gamma inhibits insulin release and induces cell death in the pancreatic beta-cell line INS-1 independently of nitric oxide production Exp Cell Res 237 217 222 10.1006/excr.1997.3791 1:CAS:528:DyaK2sXnvFWlsrs%3D 9417885 (Pubitemid 27528047)
42. HE Thomas R Darwiche JA Corbett TWH Kay 2002 Interleukin-1 plus gamma-interferon-induced pancreatic beta-cell dysfunction is mediated by beta-cell nitric oxide production Diabetes 51 311 316 10.2337/diabetes.51.2.311 1:CAS:528:DC%2BD38XhtVaqur8%3D 11812737
43. S Piro R Lupi F Dotta G Patane MA Rabuazzo L Marselli C Santangelo M Realacci GS Del F Purrello P Marchetti 2001 Bovine islets are less susceptible than human islets to damage by human cytokines Transplantation (Baltimore) 71 21 26 1:CAS:528:DC%2BD3MXhtVartrg%3D
44. JC Reed 2000 Mechanisms of apoptosis Am J Pathol 157 1415 1430 1:CAS:528:DC%2BD3cXosFyiu7w%3D 11073801
45. P Cattan T Berney S Schena RD Molano A Pileggi C Vizzardelli C Ricordi L Inverardi 2001 Early assessment of apoptosis in isolated islets of Langerhans Transplantation 71 857 862 10.1097/00007890-200104150-00006 1:CAS:528: DC%2BD3MXjvVOhtrw%3D 11349716 (Pubitemid 32417343)
46. Z Jin WS El-Deiry 2005 Overview of cell death signaling pathways Cancer Biol Ther 4 139 163 1:CAS:528:DC%2BD28XhvFKgs7k%3D 15725726
47. S Fulda KM Debatin 2002 IFNgamma sensitizes for apoptosis by upregulating caspase-8 expression through the Stat1 pathway Oncogene 21 2295 2308 10.1038/sj.onc.1205255 1:CAS:528:DC%2BD38XivFykur8%3D 11948413
48. S Paraskevas R Aikin D Vlaysinger JRT Lakey TJ Cavanagh D Agapitos R Wang L Rosenberg 2001 Modulation of JNK and p38 stress activated protein kinases in isolated islets of Langerhans: Insulin as an autocrine survival signal Ann Surg 233 124 133 10.1097/00000658-200101000-00018 1:STN:280:DC%2BD3M3pvFCktg%3D%3D 11141234 (Pubitemid 32042782)
49. I Herr KM Debatin 2001 Cellular stress response and apoptosis in cancer therapy Blood 98 2603 2614 10.1182/blood.V98.9.2603 1:CAS:528: DC%2BD3MXotVegs7o%3D 11675328
50. Y He W Zhang R Zhang H Zhang W Min 2006 SOCS1 inhibits tumor necrosis factor-induced activation of ASK1-JNK inflammatory signaling by mediating ASK1 degradation J Biol Chem 281 5559 5566 10.1074/jbc.M512338200 1:CAS:528:DC%2BD28XhvVejtrg%3D 16407264 (Pubitemid 43847652)
51. A Kimura T Naka S Nagata I Kawase T Kishimoto 2004 SOCS-1 suppresses TNF-alpha-induced apoptosis through the regulation of Jak activation Int Immunol 16 991 999 10.1093/intimm/dxh102 1:CAS:528:DC%2BD2cXltVWntLw%3D 15173123 (Pubitemid 38960877)
52. Y Morita T Naka Y Kawazoe M Fujimoto M Narazaki R Nakagawa H Fukuyama S Nagata T Kishimoto 2000 Signals transducers and activators of transcription (STAT)-induced STAT inhibitor-1 (SSI-1)/suppressor of cytokine signaling-1 (SOCS-1) suppresses tumor necrosis factor alpha-induced cell death in fibroblasts Proc Natl Acad Sci USA 97 5405 5410 10.1073/pnas.090084797 1:CAS:528:DC%2BD3cXjsVWnu7s%3D 10792035 (Pubitemid 30313731)
53. NA Andersen CM Larsen T Mandrup-Poulsen 2000 TNFalpha and IFNgamma potentiate IL-1beta induced mitogen activated protein kinase activity in rat pancreatic islets of Langerhans Diabetologia 43 1389 1396 10.1007/s001250051544 1:CAS:528:DC%2BD3cXnsFWhsr8%3D 11126408 (Pubitemid 30816007)
54. WH Kim JW Lee B Gao MH Jung 2005 Synergistic activation of JNK/SAPK induced by TNF-alpha and IFN-gamma: apoptosis of pancreatic beta-cells via the p53 and ROS pathway Cell Signal 17 1516 1532 10.1016/j.cellsig.2005.03.020 1:CAS:528:DC%2BD2MXpvV2lsbs%3D 15908180 (Pubitemid 41253991)
55. CA Gysemans L Ladriere H Callewaert J Rasschaert D Flamez DE Levy P Matthys DL Eizirik C Mathieu 2005 Disruption of the gamma-interferon signaling pathway at the level of signal transducer and activator of transcription-1 prevents immune destruction of beta-cells Diabetes 54 2396 2403 10.2337/diabetes.54.8.2396 1:CAS:528:DC%2BD2MXnt1yntrc%3D 16046307 (Pubitemid 41134268)