Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human β-cell apoptosis

Diabetes

Volumn 61, Issue 11, 2012, Pages 2763-2775

  Cunha, Daniel A ^a   Igoillo Esteve, Mariana ^a   Gurzov, Esteban N ^a   Germano, Carla M ^a   Naamane, Najib ^a   Marhfour, Ihsane ^a   Fukaya, Makiko ^a   Vanderwinden, Jean Marie ^a   Gysemans, Conny ^b   Mathieu, Chantal ^b   Marselli, Lorella ^c   Marchetti, Piero ^c   Harding, Heather P ^d   Ron, David ^d   Eizirik, Décio L ^a   Cnop, Miriam ^a,e  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF PISA   (Italy)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CASPASE 3; CASPASE 9; CYTOCHROME C; DEATH PROTEIN 5; DEATH RECEPTOR 5; PALMITIC ACID; PROTEIN IRE1; PROTEIN KINASE B; PUMA PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; LIPID DIET; LIPOTOXICITY; MALE; MICROARRAY ANALYSIS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SECRETION; RAT;

AGED; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; HUMANS; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MITOCHONDRIA; PALMITIC ACID; PROTO-ONCOGENE PROTEINS; RATS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84868013359     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-0123     Document Type: Article

References (52)

1. International Diabetes Federation. IDF Diabetes Atlas. 4th ed. Brussels, International Diabetes Federation Executive Office, 2009
2. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
3. Swinburn BA, Boyce VL, Bergman RN, Howard BV, Bogardus C. Deterioration in carbohydrate metabolism and lipoprotein changes induced by modern, high fat diet in Pima Indians and Caucasians. J Clin Endocrinol Metab 1991;73:156-165
4. Kaiyala KJ, Prigeon RL, Kahn SE, Woods SC, Porte D Jr, Schwartz MW. Reduced β-cell function contributes to impaired glucose tolerance in dogs made obese by high-fat feeding. Am J Physiol 1999;277:E659-E667
5. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001;50:1771-1777
6. Zhou YP, Grill VE. Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 1994;93:870-876
7. Kharroubi I, Ladrière L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL. Free fatty acids and cytokines induce pancreatic β-cell apoptosis by different mechanisms: role of nuclear factor-κB and endoplasmic reticulum stress. Endocrinology 2004;145:5087-5096
8. Karaskov E, Scott C, Zhang L, Teodoro T, Ravazzola M, Volchuk A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic β-cell apoptosis. Endocrinology 2006;147:3398-3407
9. Cunha DA, Hekerman P, Ladrière L, et al. Initiation and execution of lipotoxic ER stress in pancreatic β-cells. J Cell Sci 2008;121:2308-2318
10. Laybutt DR, Preston AM, Akerfeldt MC, et al. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007;50:752-763
11. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008;29:42-61
12. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529
13. Cunha DA, Ladrière L, Ortis F, et al. Glucagon-like peptide-1 agonists protect pancreatic β-cells from lipotoxic endoplasmic reticulum stress through upregulation of BiP and JunB. Diabetes 2009;58:2851-2862
14. Ladrière L, Igoillo-Esteve M, Cunha DA, et al. Enhanced signaling downstream of ribonucleic acid-activated protein kinase-like endoplasmic reticulum kinase potentiates lipotoxic endoplasmic reticulum stress in human islets. J Clin Endocrinol Metab 2010;95:1442-1449
15. Cnop M, Ladriere L, Hekerman P, et al. Selective inhibition of eukaryotic translation initiation factor 2 α dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic β-cell dysfunction and apoptosis. J Biol Chem 2007;282:3989-3997
16. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008;9:47-59
17. Kim H, Rafiuddin-Shah M, Tu HC, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006;8: 1348-1358
18. Tournier C, Hess P, Yang DD, et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000;288: 870-874
19. Kim BJ, Ryu SW, Song BJ. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 2006;281: 21256-21265
20. Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 2003; 100:2432-2437
21. Donovan N, Becker EB, Konishi Y, Bonni A. JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery. J Biol Chem 2002;277:40944-40949
22. Akazawa Y, Cazanave S, Mott JL, et al. Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis. J Hepatol 2010;52:586-593
23. Ma C, Ying C, Yuan Z, et al. dp5/HRK is a c-Jun target gene and required for apoptosis induced by potassium deprivation in cerebellar granule neurons. J Biol Chem 2007;282:30901-30909
24. Santin I, Moore F, Colli ML, et al. PTPN2, a candidate gene for type 1 diabetes, modulates pancreatic β-cell apoptosis via regulation of the BH3-only protein Bim. Diabetes 2011;60:3279-3288
25. Cross BC, Bond PJ, Sadowski PG, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci USA 2012;109:E869-E878
26. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic β-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008;10(Suppl. 4):32-42
27. Sempoux C, Guiot Y, Lefevre A, et al. Neonatal hyperinsulinemic hypoglycemia: heterogeneity of the syndrome and keys for differential diagnosis. J Clin Endocrinol Metab 1998;83:1455-1461
28. Ortis F, Naamane N, Flamez D, et al. Cytokines interleukin-1β and tumor necrosis factor-α regulate different transcriptional and alternative splicing networks in primary β-cells. Diabetes 2010;59:358-374
29. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001;7:683-694
30. Wang P, Qiu W, Dudgeon C, et al. PUMA is directly activated by NF-kB and contributes to TNF-α-induced apoptosis. Cell Death Differ 2009;16:1192-1202
31. Gurzov EN, Germano CM, Cunha DA, et al. p53 up-regulated modulator of apoptosis (PUMA) activation contributes to pancreatic β-cell apoptosis induced by proinflammatory cytokines and endoplasmic reticulum stress. J Biol Chem 2010;285:19910-19920
32. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001;21:1249-1259
33. Qian B, Wang H, Men X, et al. TRIB3 is implicated in glucotoxicity- and endoplasmic reticulum stress-induced β-cell apoptosis [published correction appears in J Endocrinol 2009;200:243 and 2009;203:399].
34. J Endocrinol 2008;199:407-416
35. Cnop M, Igoillo-Esteve M, Cunha DA, Ladrière L, Eizirik DL. An update on lipotoxic endoplasmic reticulum stress in pancreatic β-cells. Biochem Soc Trans 2008;36:909-915
36. Poitout V. Glucolipotoxicity of the pancreatic beta-cell: myth or reality? Biochem Soc Trans 2008;36:901-904
37. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, Donath MY. Distinct effects of saturated and monounsaturated fatty acids on β-cell turnover and function. Diabetes 2001;50:69-76
38. Maestre I, Jordán J, Calvo S, et al. Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the β-cell line INS-1. Endocrinology 2003;144:335-345
39. Kuwana T, Bouchier-Hayes L, Chipuk JE, et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 2005;17:525-535
40. Ren D, Tu HC, Kim H, et al. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 2010; 330:1390-1393
41. Allagnat F, Cunha D, Moore F, Vanderwinden JM, Eizirik DL, Cardozo AK. Mcl-1 downregulation by pro-inflammatory cytokines and palmitate is an early event contributing to β-cell apoptosis. Cell Death Differ 2011;18:328-337
42. Gurzov EN, Ortis F, Cunha DA, et al. Signaling by IL-1b+IFN-g and ER stress converge on DP5/Hrk activation: a novel mechanism for pancreatic β-cell apoptosis. Cell Death Differ 2009;16:1539-1550
43. Pierucci D, Cicconi S, Bonini P, et al. NGF-withdrawal induces apoptosis in pancreatic beta cells in vitro. Diabetologia 2001;44:1281-1295
44. Harris CA, Johnson EM Jr. BH3-only Bcl-2 family members are co-ordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J Biol Chem 2001;276:37754-37760
45. Cazanave SC, Mott JL, Elmi NA, et al. JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J Biol Chem 2009;284:26591-26602
46. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves b cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008;118:3378-3389
47. Hartman MG, Lu D, Kim ML, et al. Role for activating transcription factor 3 in stress-induced β-cell apoptosis. Mol Cell Biol 2004;24:5721-5732
48. Li D, Yin X, Zmuda EJ, et al. The repression of IRS2 gene by ATF3, a stress-inducible gene, contributes to pancreatic β-cell apoptosis. Diabetes 2008; 57:635-644
49. Zmuda EJ, Qi L, Zhu MX, Mirmira RG, Montminy MR, Hai T. The roles of ATF3, an adaptive-response gene, in high-fat-diet-induced diabetes and pancreatic β-cell dysfunction. Mol Endocrinol 2010;24:1423-1433
50. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 2005;24:1243-1255
51. Liew CW, Bochenski J, Kawamori D, et al. The pseudokinase tribbles homolog 3 interacts with ATF4 to negatively regulate insulin exocytosis in human and mouse b cells. J Clin Invest 2010;120:2876-2888
52. You H, Pellegrini M, Tsuchihara K, et al. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med 2006; 203:1657-1663