MKK3 signalling plays an essential role in leukocyte-mediated pancreatic injury in the multiple low-dose streptozotocin model

Laboratory Investigation

Volumn 88, Issue 4, 2008, Pages 398-407

  Fukuda, Kyoichi ^a   Tesch, Greg H ^a,b   Yap, Felicia Y ^c   Forbes, Josephine M ^c   Flavell, Richard A ^d   Davis, Roger J ^e   Nikolic Paterson, David J ^a,b  

^a MONASH MEDICAL CENTRE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

cell; Apoptosis; Cytokine; Hyperglycaemia; Macrophage; p38 MAPK

Indexed keywords

CASPASE 3; CYTOKINE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE; MOUSE; NONHUMAN; PANCREAS INJURY; PANCREAS ISLET CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; APOPTOSIS; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; INSULIN-SECRETING CELLS; MALE; MAP KINASE KINASE 3; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PANCREATITIS; T-LYMPHOCYTES;

EID: 41149137721     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2008.10     Document Type: Article

References (54)

1. Hohmeier HE, Tran VV, Chen G, et al. Inflammatory mechanisms in diabetes: lessons from the beta-cell. Int J Obes Relat Metab Disord 2003;27(Suppl 3):S12-S16.
2. Kawasaki E, Abiru N, Eguchi K. Prevention of type 1 diabetes: from the view point of beta cell damage. Diabetes Res Clin Pract 2004;66(Suppl 1):S27-S32.
3. Bendtzen K, Mandrup-Poulsen T, Nerup J, et al. Cytotoxicity of human pI 7 interleukin-1 for pancreatic islets of Langerhans. Science 1986;232:1545-1547.
4. Mandrup-Poulsen T, Bendtzen K, Dinarello CA, et al. Human tumor necrosis factor potentiates human interleukin 1-mediated rat pancreatic beta-cell cytotoxicity. J Immunol 1987;139:4077-4082.
5. Eizirik DL, Sandler S, Welsh N, et al. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 1994;93:1968-1974.
6. Sandberg JO, Andersson A, Eizirik DL, et al. Interleukin-1 receptor antagonist prevents low dose streptozotocin induced diabetes in mice. Biochem Biophys Res Commun 1994;202:543-548.
7. Holstad M, Sandler S. A transcriptional inhibitor of TNF-alpha prevents diabetes induced by multiple low-dose streptozotocin injections in mice. J Autoimmunity 2001;16:441-447.
8. Sandberg JO, Eizirik DL, Sandler S, et al. Treatment with an interleukin-1 receptor antagonist protein prolongs mouse islet allograft survival. Diabetes 1993;42:1845-1851.
9. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007;356:1517-1526.
10. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001;81:807-869.
11. Welsh N. Interleukin-1 beta-induced ceramide and diacylglycerol generation may lead to activation of the c-Jun NH2-terminal kinase and the transcription factor ATF2 in the insulin-producing cell line RINm5F. J Biol Chem 1996;271:8307-8312.
12. Larsen CM, Wadt KA, Juhl LF, et al. Interleukin-1beta-induced rat pancreatic islet nitric oxide synthesis requires both the p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J Biol Chem 1998;273:15294-15300.
13. Ammendrup A, Maillard A, Nielsen K, et al. The c-Jun amino-terminal kinase pathway is preferentially activated by interleukin-1 and controls apoptosis in differentiating pancreatic beta-cells. Diabetes 2000;49:1468-1476.
14. Bonny C, Oberson A, Negri S, et al. Cell-permeable peptide inhibitors of JNK: novel blockers of beta-cell death. Diabetes 2001;50:77-82.
15. Saldeen J, Lee JC, Welsh N. Role of p38 mitogen-activated protein kinase (p38 MAPK) in cytokine-induced rat islet cell apoptosis. Biochem Pharmacol 2001;61:1561-1569.
16. Zhang S, Liu H, Liu J, et al. Activation of activating transcription factor 2 by p38 MAP kinase during apoptosis induced by human amylin in cultured pancreatic beta-cells. FEBS J 2006;273:3779-3791.
17. Matsuda T, Omori K, Vuong T, et al. Inhibition of p38 pathway suppresses human islet production of pro-inflammatory cytokines and improves islet graft function. Am J Transplant 2005;5:484-493.
18. Pavlovic D, Andersen NA, Mandrup-Poulsen T, et al. Activation of extracellular signal-regulated kinase (ERK)1/2 contributes to cytokine-induced apoptosis in purified rat pancreatic beta-cells. Eur Cytokine Netw 2000;11:267-274.
19. Kang YJ, Seit-Nebi A, Davis RJ, et al. Multiple activation mechanisms of p38alpha mitogen-activated protein kinase. J Biol Chem 2006;281:26225-26234.
20. Dong J, Ramachandiran S, Tikoo K, et al. EGFR-independent activation of p38 MAPK and EGFR-dependent activation of ERK1/2 are required for ROS-induced renal cell death. Am J Physiol Renal Physiol 2004;287:F1049-F1058.
21. de Graauw M, Tijdens I, Cramer R, et al. Heat shock protein 27 is the major differentially phosphorylated protein involved in renal epithelial cellular stress response and controls focal adhesion organization and apoptosis. J Biol Chem 2005;280:29885-29898.
22. Ando H, Kurita S, Takamura T. The specific p38 mitogen-activated protein kinase pathway inhibitor FR167653 keeps insulitis benign in nonobese diabetic mice. Life Sci 2004;74:1817-1827.
23. Jackson JR, Bolognese B, Hillegass L, et al. Pharmacological effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinase, in angiogenesis and chronic inflammatory disease models. J Pharmacol Exp Ther 1998;284:687-692.
24. Underwood DC, Osborn RR, Bochnowicz S, et al. SB 239063, a p38 MAPK inhibitor, reduces neutrophilia, inflammatory cytokines, MMP-9, and fibrosis in lung. Am J Physiol Lung Cell Mol Physiol 2000;279:L895-L902.
25. Behr TM, Nerurkar SS, Nelson AH, et al. Hypertensive end-organ damage and premature mortality are p38 mitogen-activated protein kinase-dependent in a rat model of cardiac hypertrophy and dysfunction. Circulation 2001;104:1292-1298.
26. Stambe C, Atkins RC, Tesch GH, et al. The role of p38alpha mitogen-activated protein kinase activation in renal fibrosis. J Am Soc Nephrol 2004;15:370-379.
27. Stambe C, Atkins RC, Tesch GH, et al. Blockade of p38alpha MAPK ameliorates acute inflammatory renal injury in rat anti-GBM glomerulonephritis. J Am Soc Nephrol 2003;14:338-351.
28. Kumar S, Boehm J, Lee JC. p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov 2003;2:717-726.
29. Inoue T, Boyle DL, Corr M, et al. Mitogen-activated protein kinase kinase 3 is a pivotal pathway regulating p38 activation in inflammatory arthritis. Proc Natl Acad Sci USA 2006;103:5484-5489.
30. Abdelli S, Ansite J, Roduit R, et al. Intracellular stress signaling pathways activated during human islet preparation and following acute cytokine exposure. Diabetes 2004;53:2815-2823.
31. Kim YT, Steinberg C. Immunologic studies on the induction of diabetes in experimental animals. Cellular basis for the induction of diabetes by streptozotocin. Diabetes 1984;33:771-777.
32. Herold KC, Vezys V, Sun Q, et al. Regulation of cytokine production during development of autoimmune diabetes induced with multiple low doses of streptozotocin. J Immunol 1996;156:3521-3527.
33. Muller A, Schott-Ohly P, Dohle C, et al. Differential regulation of Th1-type and Th2-type cytokine profiles in pancreatic islets of C57BL/6 and BALB/c mice by multiple low doses of streptozotocin. Immunobiology 2002;205:35-50.
34. Wysk M, Yang DD, Lu HT, et al. Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for tumor necrosis factor-induced cytokine expression. Proc Natl Acad Sci USA 1999;96:3763-3768.
35. Peterson JD, Pike B, McDuffie M, et al. Islet-specific T cell clones transfer diabetes to nonobese diabetic (NOD) F1 mice. J Immunol (Baltimore, MD, USA) 1994;153:2800-2806.
36. Schnedl WJ, Ferber S, Johnson JH, et al. STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 1994;43:1326-1333.
37. Wang Z, Gleichmann H. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 1998;47:50-56.
38. O'Brien BA, Harmon BV, Cameron DP, et al. Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J Pathol 1996;178:176-181.
39. Herold KC, Montag AG, Fitch FW. Treatment with anti-T-lymphocyte antibodies prevents induction of insulitis in mice given multiple doses of streptozocin. Diabetes 1987;36:796-801.
40. Herold KC, Montag AG, Buckingham F. Induction of tolerance to autoimmune diabetes with islet antigens. J Exp Med 1992;176:1107-1114.
41. Herold KC, Bloch TN, Vezys V, et al. Diabetes induced with low doses of streptozotocin is mediated by V beta 8.2+ T-cells. Diabetes 1995;44:354-359.
42. Ihm SH, Lee KU, Rhee BD, et al. Initial role of macrophage in the development of anti-beta-cell cellular autoimmunity in multiple lowdose streptozotocin-induced diabetes in mice. Diabetes Res Clin Pract 1990;10:123-126.
43. Mensah-Brown E, Shahin A, Parekh K, et al. Functional capacity of macrophages determines the induction of type 1 diabetes. Ann N Y Acad Sci 2006;1084:49-57.
44. Cockfield SM, Ramassar V, Urmson J, et al. Multiple low dose streptozotocin induces systemic MHC expression in mice by triggering T cells to release IFN-gamma. J Immunol 1989;142:1120-1128.
45. Chen MC, Proost P, Gysemans C, et al. 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 2001;44:325-332.
46. Welsh N, Cnop M, Kharroubi I, et al. Is there a role for locally produced interleukin-1 in the deleterious effects of high glucose or the type 2 diabetes milieu to human pancreatic islets? Diabetes 2005;54:3238-3244.
47. Eizirik DL, Pavlovic D. Is there a role for nitric oxide in beta-cell dysfunction and damage in IDDM? Diabetes Metab Rev 1997;13:293-307.
48. Holstad M, Sandler S. Aminoguanidine, an inhibitor of nitric oxide formation, fails to protect against insulitis and hyperglycemia induced by multiple low dose streptozotocin injections in mice. Autoimmunity 1993;15:311-314.
49. Sternesjo J, Welsh N, Sandler S. S-methyl-L-thiocitrulline counteracts interleukin 1 beta induced suppression of pancreatic islet function in vitro, but does not protect against multiple low-dose streptozotocin-induced diabetes in vivo. Cytokine 1997;9:352-359.
50. Flodstrom M, Tyrberg B, Eizirik DL, et al. Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes. Diabetes 1999;48:706-713.
51. Tamura K, Sudo T, Senftleben U, et al. Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 2000;102:221-231.
52. van den Blink B, Juffermans NP, ten Hove T, et al. p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages in vitro and during infection in vivo. J Immunol 2001;166:582-587.
53. Ohashi R, Nakagawa T, Watanabe S, et al. Inhibition of p38 mitogenactivated protein kinase augments progression of remnant kidney model by activating the ERK pathway. Am J Pathol 2004;164:477-485.
54. Aoudjit L, Stanciu M, Li H, et al. p38 mitogen-activated protein kinase protects glomerular epithelial cells from complement-mediated cell injury. Am J Physiol Renal Physiol 2003;285:F765-F774.