Anti-inflammatory action of exendin-4 in human islets is enhanced by phosphodiesterase inhibitors: Potential therapeutic benefits in diabetic patients

Diabetologia

Volumn 53, Issue 11, 2010, Pages 2357-2368

  Pugazhenthi, U ^b   Velmurugan, K ^a,b   Tran, A ^a   Mahaffey, G ^a   Pugazhenthi, S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Anti inflammatory; cAMP; CXCL10; Cytokines; Diabetes; Exendin 4; Interferon ; NF kB; STAT 1

Indexed keywords

ADENOSINE PHOSPHATE; BUCLADESINE; CHEMOKINE RECEPTOR CXCR3; CILOSTAMIDE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXENDIN 4; FORSKOLIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; ROLIPRAM; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MOUSE; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANTI-INFLAMMATORY AGENTS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CHEMOKINE CXCL10; CYCLIC AMP; DIABETES MELLITUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; ISLETS OF LANGERHANS; NF-KAPPA B; PEPTIDES; PHOSPHODIESTERASE INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA; VENOMS;

EID: 77957678974     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1849-y     Document Type: Article

References (50)

1. DJ Drucker 2006 The biology of incretin hormones Cell Metab 3 153 165 1:CAS:528:DC%2BD28Xislyhtr4%3D 10.1016/j.cmet.2006.01.004 16517403
2. DM Aronoff C Canetti CH Serezani M Luo M Peters-Golden 2005 Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase A and exchange protein directly activated by cAMP-1 J Immunol 174 595 599 1:CAS:528:DC%2BD2MXotV2l 15634874
3. TK Sengupta EM Schmitt LB Ivashkiv 1996 Inhibition of cytokines and JAK-STAT activation by distinct signaling pathways Proc Natl Acad Sci U S A 93 9499 9504 1:CAS:528:DyaK28XlsFeitro%3D 10.1073/pnas.93.18.9499 8790359 (Pubitemid 26296637)
4. WA Sands TM Palmer 2005 Inhibition of pro-inflammatory cytokine receptor signalling by cAMP in vascular endothelial cells Biochem Soc Trans 33 1126 1128 1:CAS:528:DC%2BD2MXhtFCqs7bP 10.1042/BST20051126 16246062 (Pubitemid 41659130)
5. N Kawada M Uoya S Seki T Kuroki K Kobayashi 1997 Regulation by cAMP of STAT1 activation in hepatic stellate cells Biochem Biophys Res Commun 233 464 469 1:CAS:528:DyaK2sXivVGru7c%3D 10.1006/bbrc.1997.6481 9144559 (Pubitemid 27226650)
6. L Liang E Beshay GJ Prud'homme 1998 The phosphodiesterase inhibitors pentoxifylline and rolipram prevent diabetes in NOD mice Diabetes 47 570 575 1:CAS:528:DyaK1cXit1Gns7g%3D 10.2337/diabetes.47.4.570 9568689 (Pubitemid 28160447)
7. A Rabinovitch WL Sumoski 1990 Theophylline protects against diabetes in BB rats and potentiates cyclosporine protection Diabetologia 33 506 508 1:CAS:528:DyaK3MXjtFY%3D 10.1007/BF00405114 2210124 (Pubitemid 20254875)
8. M Baggiolini 2001 Chemokines in pathology and medicine J Intern Med 250 91 104 1:CAS:528:DC%2BD3MXmsVOltrk%3D 10.1046/j.1365-2796.2001.00867.x 11489059 (Pubitemid 32868689)
9. AD Luster JV Ravetch 1987 Biochemical characterization of a gamma interferon-inducible cytokine (IP-10) J Exp Med 166 1084 1097 1:CAS:528:DyaL1cXitVartA%3D%3D 10.1084/jem.166.4.1084 2443596
10. AD Luster 1998 Chemokines-chemotactic cytokines that mediate inflammation N Engl J Med 338 436 445 1:CAS:528:DyaK1cXht1Wrsrc%3D 10.1056/ NEJM199802123380706 9459648 (Pubitemid 28135672)
11. LF Neville G Mathiak O Bagasra 1997 The immunobiology of interferon-gamma inducible protein 10 kD (IP-10): a novel, pleiotropic member of the C-X-C chemokine superfamily Cytokine Growth Factor Rev 8 207 219 1:CAS:528: DyaK1cXjsVWmtw%3D%3D 10.1016/S1359-6101(97)00015-4 9462486 (Pubitemid 28077928)
12. U Christen MG von Herrath 2004 IP-10 and type 1 diabetes: a question of time and location Autoimmunity 37 273 282 1:CAS:528:DC%2BD2cXnslans7w%3D 10.1080/08916930410001713124 (Pubitemid 39172911)
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 1:CAS:528:DC%2BD3sXhvVyrurw%3D 12627325
14. J Morimoto H Yoneyama A Shimada, et al. 2004 CXC chemokine ligand 10 neutralization suppresses the occurrence of diabetes in nonobese diabetic mice through enhanced beta cell proliferation without affecting insulitis J Immunol 173 7017 7024 1:CAS:528:DC%2BD2cXhtVShsbrI 15557199
15. F Nicoletti I Conget M Di Mauro, et al. 2002 Serum concentrations of the interferon-gamma-inducible chemokine IP-10/CXCL10 are augmented in both newly diagnosed type I diabetes mellitus patients and subjects at risk of developing the disease Diabetologia 45 1107 1110 1:CAS:528:DC%2BD38Xmt1Shsrk%3D 10.1007/s00125-002-0879-5 12189440 (Pubitemid 34985286)
16. FT Schulthess F Paroni NS Sauter, et al. 2009 CXCL10 impairs beta cell function and viability in diabetes through TLR4 signaling Cell Metab 9 125 139 1:CAS:528:DC%2BD1MXnt12qtbg%3D 10.1016/j.cmet.2009.01.003 19187771
17. BO Roep FS Kleijwegt AG van Halteren, et al. 2009 Islet inflammation and CXCL10 in recent-onset type 1 diabetes Clin Exp Immunol 159 338 343 10.1111/j.1365-2249.2009.04087.x
18. SA Sarkar B Kutlu K Velmurugan, et al. 2009 Cytokine-mediated induction of anti-apoptotic genes that are linked to nuclear factor kappa-B (NF-kappaB) signalling in human islets and in a mouse beta cell line Diabetologia 52 1092 1101 1:CAS:528:DC%2BD1MXlt1GqtL4%3D 10.1007/s00125-009-1331-x 19343319
19. SA Sarkar J Gunter R Bouchard, et al. 2007 Dominant negative mutant forms of the cAMP response element binding protein induce apoptosis and decrease the anti-apoptotic action of growth factors in human islets Diabetologia 50 1649 1659 1:CAS:528:DC%2BD2sXnt1Kis7s%3D 10.1007/s00125-007-0707-z 17593347 (Pubitemid 47036652)
20. J Miyazaki K Araki E Yamato, et al. 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 1:CAS:528:DyaK3cXltV2lsbo%3D 10.1210/endo-127-1-126 2163307
21. RE Schweppe JP Klopper C Korch, et al. 2008 Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification J Clin Endocrinol Metab 93 4331 4341 1:CAS:528:DC%2BD1cXhtlyqs7bP 10.1210/jc.2008-1102 18713817 (Pubitemid 352789529)
22. S Majumder LZ Zhou P Chaturvedi G Babcock S Aras RM Ransohoff 1998 p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha J Immunol 161 4736 4744 1:CAS:528:DyaK1cXntVWgsLk%3D 9794404
23. R Abdi TK Means AD Luster 2003 Chemokines in islet allograft rejection Diabetes Metab Res Rev 19 186 190 1:CAS:528:DC%2BD3sXltFGrtrw%3D 10.1002/dmrr.362 12789651 (Pubitemid 36675958)
24. DL Eizirik ML Colli F Ortis 2009 The role of inflammation in insulitis and beta-cell loss in type 1 diabetes Nat Rev Endocrinol 5 219 226 1:CAS:528:DC%2BD1MXjs1ymt7Y%3D 10.1038/nrendo.2009.21 19352320
25. S Yeruva G Ramadori D Raddatz 2008 NF-kappaB-dependent synergistic regulation of CXCL10 gene expression by IL-1beta and IFN-gamma in human intestinal epithelial cell lines Int J Colorectal Dis 23 305 317 10.1007/s00384-007-0396-6 18046562
26. RK Campbell S Miller 2009 New therapeutic horizons: mapping the future of glycemic control with incretin-based therapy Diabetes Educ 35 731 734 10.1177/0145721709342900 19783765
27. T Iwai S Ito K Tanimitsu S Udagawa J Oka 2006 Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes Neurosci Res 55 352 360 1:CAS:528:DC%2BD28XlsFKktrw%3D 10.1016/j.neures.2006.04.008 16720054 (Pubitemid 43866249)
28. S Kim M Moon S Park 2009 Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease J Endocrinol 202 431 439 1:CAS:528:DC%2BD1MXhtFahtLnF 10.1677/JOE-09-0132 19570816
29. I Hadjiyanni LL Baggio P Poussier DJ Drucker 2008 Exendin-4 modulates diabetes onset in nonobese diabetic mice Endocrinology 149 1338 1349 1:CAS:528:DC%2BD1cXisVaqtbw%3D 10.1210/en.2007-1137 18063685 (Pubitemid 351397945)
30. J Zhang Y Tokui K Yamagata, et al. 2007 Continuous stimulation of human glucagon-like peptide-1 (7-36) amide in a mouse model (NOD) delays onset of autoimmune type 1 diabetes Diabetologia 50 1900 1909 1:CAS:528: DC%2BD2sXos1Cjt70%3D 10.1007/s00125-007-0737-6 17632702 (Pubitemid 47222856)
31. Z Yang M Chen JD Carter, et al. 2006 Combined treatment with lisofylline and exendin-4 reverses autoimmune diabetes Biochem Biophys Res Commun 344 1017 1022 1:CAS:528:DC%2BD28XktVOqs7g%3D 10.1016/j.bbrc.2006.03.177 16643856
32. N Ogawa JF List JF Habener T Maki 2004 Cure of overt diabetes in NOD mice by transient treatment with anti-lymphocyte serum and exendin-4 Diabetes 53 1700 1705 1:CAS:528:DC%2BD2cXlslWgt70%3D 10.2337/diabetes.53.7.1700 15220193 (Pubitemid 38857027)
33. NA Sherry W Chen JA Kushner, et al. 2007 Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 monoclonal antibody by enhancing recovery of beta-cells Endocrinology 148 5136 5144 1:CAS:528:DC%2BD2sXht1aju7vK 10.1210/en.2007-0358 17673522 (Pubitemid 350012634)
34. SJ Kim C Nian DJ Doudet CH McIntosh 2009 Dipeptidyl peptidase IV inhibition with MK0431 improves islet graft survival in diabetic NOD mice partially via T cell modulation Diabetes 58 641 651 1:CAS:528: DC%2BD1MXjt1Wktrw%3D 10.2337/db08-1101 19073764
35. FM Couto AH Minn CA Pise-Masison, et al. 2007 Exenatide blocks JAK1-STAT1 in pancreatic beta cells Metabolism 56 915 918 1:CAS:528:DC%2BD2sXmsF2jsbY%3D 10.1016/j.metabol.2007.02.004 17570252 (Pubitemid 46890974)
36. U Christen DB McGavern AD Luster MG von Herrath MB Oldstone 2003 Among CXCR3 chemokines, IFN-gamma-inducible protein of 10 kDa (CXC chemokine ligand (CXCL) 10) but not monokine induced by IFN-gamma (CXCL9) imprints a pattern for the subsequent development of autoimmune disease J Immunol 171 6838 6845 1:CAS:528:DC%2BD3sXpsV2rtbk%3D 14662890
37. AK Berg O Korsgren G Frisk 2006 Induction of the chemokine interferon-gamma-inducible protein-10 in human pancreatic islets during enterovirus infection Diabetologia 49 2697 2703 1:CAS:528:DC%2BD28XhtFOqsrrP 10.1007/s00125-006-0429-7 16969644
38. S Tanaka Y Nishida K Aida, et al. 2009 Enterovirus infection, CXC chemokine ligand 10 (CXCL10), and CXCR3 circuit: a mechanism of accelerated beta-cell failure in fulminant type 1 diabetes Diabetes 58 2285 2291 1:CAS:528:DC%2BD1MXht1yku7bJ 10.2337/db09-0091 19641142
39. HS Jun JW Yoon 2001 The role of viruses in type I diabetes: two distinct cellular and molecular pathogenic mechanisms of virus-induced diabetes in animals Diabetologia 44 271 285 1:CAS:528:DC%2BD3MXhsFCnu7Y%3D 10.1007/s001250051614 11317656 (Pubitemid 32234451)
40. M Roivainen S Rasilainen P Ylipaasto, et al. 2000 Mechanisms of coxsackievirus-induced damage to human pancreatic beta-cells J Clin Endocrinol Metab 85 432 440 1:CAS:528:DC%2BD3cXjtl2ktA%3D%3D 10.1210/jc.85.1.432 10634421 (Pubitemid 32268847)
41. D Liu AK Cardozo MI Darville DL Eizirik 2002 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 1225 1234 1:CAS:528: DC%2BD38XisFGisrk%3D 10.1210/en.143.4.1225 11897677 (Pubitemid 34274351)
42. MY Donath J Storling K Maedler T Mandrup-Poulsen 2003 Inflammatory mediators and islet beta-cell failure: a link between type 1 and type 2 diabetes J Mol Med 81 455 470 1:CAS:528:DC%2BD3sXmsV2jtLw%3D 10.1007/s00109-003-0450-y 12879149 (Pubitemid 37070198)
43. MY Donath DM Schumann M Faulenbach H Ellingsgaard A Perren JA Ehses 2008 Islet inflammation in type 2 diabetes: from metabolic stress to therapy Diabetes Care 31 Suppl 2 S161 S164 1:CAS:528:DC%2BD1cXis1ajt70%3D 10.2337/dc08-s243 18227479
44. JA Ehses A Perren E Eppler, et al. 2007 Increased number of islet-associated macrophages in type 2 diabetes Diabetes 56 2356 2370 1:CAS:528:DC%2BD2sXhtV2gs7fE 10.2337/db06-1650 17579207 (Pubitemid 47358243)
45. M von Herrath A Holz 1997 Pathological changes in the islet milieu precede infiltration of islets and destruction of beta-cells by autoreactive lymphocytes in a transgenic model of virus-induced IDDM J Autoimmun 10 231 238 10.1006/jaut.1997.0131 (Pubitemid 27286528)
46. S Frigerio T Junt B Lu, et al. 2002 Beta cells are responsible for CXCR3-mediated T cell infiltration in insulitis Nat Med 8 1414 1420 1:CAS:528:DC%2BD38XptVSgsbw%3D 10.1038/nm792 12415259 (Pubitemid 36024137)
47. K Omori J Kotera 2007 Overview of PDEs and their regulation Circ Res 100 309 327 1:CAS:528:DC%2BD2sXhsF2kurY%3D 10.1161/01.RES.0000256354.95791.f1 17307970
48. JC Parker MA VanVolkenburg RJ Ketchum KL Brayman KM Andrews 1995 Cyclic AMP phosphodiesterases of human and rat islets of Langerhans: contributions of types III and IV to the modulation of insulin secretion Biochem Biophys Res Commun 217 916 923 1:CAS:528:DyaK28XhsVSrtQ%3D%3D 10.1006/bbrc.1995.2858 8554616 (Pubitemid 26019742)
49. MJ MacDonald NT Shahidi DB Allen RH Lustig TL Mitchell ST Cornwell 1994 Pentoxifylline in the treatment of children with new-onset type I diabetes mellitus JAMA 271 27 28 1:STN:280:DyaK2c%2FotFGmsQ%3D%3D 10.1001/jama.271.1.27 8258882 (Pubitemid 24020573)
50. S Stosic-Grujicic D Maksimovic V Badovinac, et al. 2001 Antidiabetogenic effect of pentoxifylline is associated with systemic and target tissue modulation of cytokines and nitric oxide production J Autoimmun 16 47 58 1:STN:280:DC%2BD3Mzitlarsw%3D%3D 10.1006/jaut.2000.0456 11221996 (Pubitemid 32174174)