Proinflammatory cytokines activate the intrinsic apoptotic pathway in β-cells

Diabetes

Volumn 58, Issue 8, 2009, Pages 1807-1815

  Grunnet, Lars G ^a,b   Aikin, Reid ^c   Tonnesen, Morten F ^a   Paraskevas, Steven ^c   Blaabjerg, Lykke ^a   Størling, Joachim ^a   Rosenberg, Lawrence ^c   Billestrup, Nils ^a   Maysinger, Dusica ^c   Mandrup Poulsen, Thomas ^a,b  

^a STENO DIABETES CENTER   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; CYTOCHROME C; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; SERINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; GRAFT FAILURE; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RAT;

ANIMALS; APOPTOSIS; CADAVER; CASPASE 9; CELL DEATH; CYTOKINES; HUMANS; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; RATS; RATS, WISTAR; TISSUE DONORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 68049143316     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db08-0178     Document Type: Article

References (50)

1. Eizirik DL, Mandrup-Poulsen T. A choice of death: the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 2001;44:2115-2133
2. Hengartner MO. The biochemistry of apoptosis. Nature (London) 2000;407:770-776
3. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004;116:205-219
4. Tibbetts MD, Zheng L, Lenardo MJ. The death effector domain protein family: regulators of cellular homeostasis. Nat Immunol 2003;4:404-409
5. Scorrano L, Korsmeyer SJ. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 2003;304:437-444
6. Adams JM. Ways of dying: multiple pathways to apoptosis. Genes Dev 2003;17:2481-2495
7. Wei MC, Zong WX, Cheng EHY, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-730
8. Zha J, Harada H, Yang E, et al. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell 1996;87:619-628
9. Yang E, Zha J, et al. Bad, a heterodimeric partner for Bcl-x(L), and Bcl-2, displaces Bax and promotes cell death. Cell 1995;80:285-291
10. Peso LD, Gonzalez-Garcia M, Page C, et al. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997;278:687-689
11. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999;284:339-343
12. Sunayama J, Tsuruta F, Masuyama N, et al. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 2005;170:295-304
13. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999;13:2905-2927
14. Barbu A, Welsh N, Saldeen J. Cytokine-induced apoptosis and necrosis are preceded by disruption of the mitochondrial membrane potential (Δψ(m)) in pancreatic R1Nm5F cells: prevention by Bcl-2. Mol Cell Endocrinol 2002;190:75-82
15. Papaccio G, Graziano A, Valiante S, et al. Interleukin (IL)-1β toxicity to islet β cells: efaroxan exerts a complete protection. J Cell Physiol 2005;203:94-102
16. Chang I, Cho N, Kim S, et al. Role of calcium in pancreatic islet cell death by IFN-gamma/TNF-alpha. J Immunol 2004;172:7008-7014
17. Kutlu B, Cardozo AK, Darville MI, et al. Discovery of gene networks regulating cytokine-induced dysfunction and apoptosis in insulin-producing INS-1 cells. Diabetes 2003;52:2701-2719
18. Saldeen J. Cytokines induce both necrosis and apoptosis via a common Bcl-2-inhibitable pathway in rat insulin-producing cells. Endocrinology 2000;141:2003-2010
19. Klein D, Ribeiro MM, Mendoza V, et al. Delivery of Bcl-XL or its BH4 domain by protein transduction inhibits apoptosis in human islets. Biochem Biophys Res Commun 2004;323:473-478
20. Liu Y, Rabinovitch A, Suarez-Pinzon W, et al. Expression of the bcl-2 gene from a defective HSV-1 amplicon vector protects pancreatic beta-cells from apoptosis. Human Gene Ther 1996;7:1719-1726
21. Iwahashi H, Hanafusa T, Eguchi Y, et al. Cytokine-induced apoptotic cell death in a mouse pancreatic beta-cell line: inhibition by Bcl-2. Diabetologia 1996;39:530-536
22. Rabinovitch A, Suarez-Pinzon W, Strynadka K, et al. Transfection of human pancreatic islets with an anti-apoptotic gene (bcl-2) protects β-cells from cytokine-induced destruction. Diabetes 1999;48:1223-1229
23. Dupraz P, Rinsch C, Pralong WF, et al. Lentivirus-mediated Bcl-2 expression in betaTC-tet cells improves resistance to hypoxia and cytokineinduced apoptosis while preserving in vitro and in vivo control of insulin secretion. Gene Ther 1999;6:1160-1169
24. Petersen L, Størling J, Heding P, et al. IL-1beta-induced pro-apoptotic signalling is facilitated by NCAM/FGF receptor signalling and inhibited by the C3d ligand in the INS-1E rat beta cell line. Diabetologia 2006;49:1864-1875
25. Paraskevas S, Aikin R, Maysinger D, et al. Modulation of JNK and p38 stress activated protein kinases in isolated islets of Langerhans: insulin as an autocrine survival signal. Ann Surg 2001;233:124-133
26. 2+ current mediates cytokine-induced pancreatic beta-cell death. Endocrinology 1999;140:1200-1204
27. Størling J, Binzer J, Andersson A, et al. Nitric oxide contributes to cytokine-induced apoptosis in pancreatic beta cells via potentiation of JNK activity and inhibition of Akt. Diabetologia 2005;48:2039-2050
28. Aikin R, Maysinger D, Rosenberg L. Cross-talk between phosphatidylinositol 3-kinase/AKT and c-jun NH2-terminal kinase mediates survival of isolated human islets. Endocrinology 2004;145:4522-4531
29. Nielsen K, Karlsen AE, Deckert M, et al. β-Cell maturation leads to in vitro sensitivity to cytotoxins. Diabetes 1999;48:2324-2332
30. Gomez JA, Gama V, Yoshida T, et al. Bax-inhibiting peptides derived from Ku70 and cell-penetrating pentapeptides. Biochem Soc Trans 2007;35:797-801
31. Cohen HY, Lavu S, Bitterman KJ, et al. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol Cell 2004;13:627-638
32. Subramanian C, Opipari AW Jr, Bian X, et al. Ku70 acetylation mediates neuroblastoma cell death induced by histone deacetylase inhibitors. Proc Nat Acad Sci U S A 2005;102:4842-4847
33. Yoshida T, Tomioka I, Nagahara T, et al. Bax-inhibiting peptide derived from mouse and rat Ku70. Biochem Biophys Res Commun 2004;321:961-966
34. Maechler P, Wollheim CB. Mitochondrial function in normal and diabetic beta-cells. Nature 2001;414:807-812
35. Zhou YP, Pena JC, Roe MW, et al. Overexpression of Bcl-xL in beta -cells prevents cell death but impairs mitochondrial signal for insulin secretion. Am J Physiol Endocrinol Metab 2000;278:E340-E351
36. Doyle ME, Egan JM: Pharmacological agents that directly modulate insulin secretion. Pharmacol Rev 2003;55:105-131
37. Mao Z, Wiedmann M. Calcineurin enhances MEF2 DNA binding activity in calcium-dependent survival of cerebellar granule neurons. J Biol Chem 1999;274:31102-31107
38. Matsuda S, Shibasaki F, Takehana K, et al. Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T-cell activation. Embo Rep 2000;1:428-434
39. Collier JJ, Fueger PT, Hohmeier HE, et al. Pro- and antiapoptotic proteins regulate apoptosis but do not protect against cytokine-mediated cytotoxicity in rat islets and β-cell lines. Diabetes 2006;55:1398-1406
40. + channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 2000;49:424-430
41. Chen G, Hohmeier HE, Gasa R, et al. Selection of insulinoma cell lines with resistance to interleukin-1β- and γ-interferon-induced cytotoxicity. Diabetes 2000;49:562-570
42. Cottet S, Dupraz P, Hamburger F, et al. cFLIP protein prevents tumor necrosis factor-α-mediated induction of caspase-8-dependent apoptosis in insulin-secreting βTc-Tet cells. Diabetes 2002;51:1805-1814
43. McKenzie MD, Carrington EM, Kaufmann T, et al. Proapoptotic BH3-only protein Bid is essential for death receptor-induced apoptosis of pancreatic β-cells. Diabetes 2008;57:1284-1292
44. Tunon MJ, Sanchez-Campos S, Gutierrez B, et al. Effects of FK506 and rapamycin on generation of reactive oxygen species, nitric oxide production and nuclear factor kappa B activation in rat hepatocytes. Biochem Pharmacol 2003;66:439-445
45. Strasser S, Alejandro R, Shapiro ET, et al. Effect of FK506 on insulin secretion in normal dogs. Metabolism 1992;41:64-67
46. Redmon JB, Olson LK, Armstrong MB, et al. Effects of Tacrolimus (FK506) on human insulin gene expression, insulin mRNA levels, and insulin secretion in HIT-T15 cells. J Clin Invest 1996;98:2786-2793
47. Polastri L, Galbiati F, Bertuzzi F, et al. Secretory defects induced by immunosuppressive agents on human pancreatic beta-cells. Acta Diabetologica 2002;39:229-233
48. Drachenberg CB, Klassen DK, Weir MR, et al. Islet cell damage associated with tacrolimus and cyclosporine: morphological features in pancreas allograft biopsies and clinical correlation. Transplantation (Baltimore) 1999;68:396-402
49. Lawrence MC, Bhatt HS, Watterson JM, et al. Regulation of insulin gene transcription by a Ca2+-responsive pathway involving calcineurin and nuclear factor of activated T cells. Mol Endocrinol 2001;15:1758-1767
50. Aikin R, Hanley S, Maysinger D, et al. Autocrine insulin action activates Akt and increases survival of isolated human islets. Diabetologia 2006;49:2900-2909