Glucagon-like peptide-1 agonists protect pancreatic β-cells from lipotoxic endoplasmic reticulum stress through upregulation of BIP and JunB

Diabetes

Volumn 58, Issue 12, 2009, Pages 2851-2862

  Cunha, Daniel A ^a   Ladrière, Laurence ^a   Ortis, Fernanda ^a   Igoillo Esteve, Mariana ^a   Gurzov, Esteban N ^a   Lupi, Roberto ^b   Marchetti, Piero ^b   Eizirik, Décio L ^a   Cnop, Miriam ^a,c  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF PISA   (Italy)

^c ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CASPASE 12; CASPASE 7; CCAAT ENHANCER BINDING PROTEIN; CYCLOPIAZONIC ACID; EXENDIN 4; FORSKOLIN; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; OLEIC ACID; PALMITIC ACID; PROTEIN BCL 2; TRANSCRIPTION FACTOR JUNB; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN TISSUE; MALE; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, DIFFERENTIATION; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; DIABETES MELLITUS, TYPE 2; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; FORSKOLIN; GLUCAGON-LIKE PEPTIDE 1; HEAT-SHOCK PROTEINS; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; LIPID METABOLISM; MALE; PEPTIDES; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RATS, WISTAR; RECEPTORS, GLUCAGON; RNA INTERFERENCE; TRANSCRIPTION FACTORS; UP-REGULATION; VENOMS;

EID: 73249116246     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0685     Document Type: Article

References (49)

1. Ferrannini E, Gastaldelli A, Miyazaki Y, Matsuda M, Mari A, DeFronzo RA. β-Cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. J Clin Endocrinol Metab 2005;90:493-500
2. Cnop M, Vidal J, Hull RL, Utzschneider KM, Carr DB, Schraw T, Scherer PE, Boyko EJ, Fujimoto WY, Kahn SE. Progressive loss of β-cell function leads to worsening glucose tolerance in first-degree relatives of subjects with type 2 diabetes. Diabetes Care 2007;30:677-682
3. Florez JC. Newly identified loci highlight beta cell dysfunction as a key cause of type 2 diabetes: where are the insulin resistance genes? Diabetologia 2008;51:1100-1110
4. 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
5. 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
6. Marchetti P, Bugliani M, Lupi R, Marselli L, Masini M, Boggi U, Filipponi F, Weir GC, Eizirik DL, Cnop M. The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 2007;50:2486-2494
7. Cnop M. Fatty acids and glucolipotoxicity in the pathogenesis of type 2 diabetes. Biochem Soc Trans 2008;36:348-352
8. Poitout V. Glucolipotoxicity of the pancreatic β-cell: myth or reality? Biochem Soc Trans 2008;36:901-904
9. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008;29:42-61
10. Kharroubi I, Ladriere 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
11. Cnop M, Ladriere L, Hekerman P, Ortis F, Cardozo AK, Dogusan Z, Flamez D, Boyce M, Yuan J, Eizirik DL. Selective inhibition of eukaryotic translation initiation factor 2α dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic β-cell dysfunction and apoptosis. J Biol Chem 2007;282:3989-3997
12. Cunha DA, Hekerman P, Ladriere L, Bazarra-Castro A, Ortis F, Wakeham MC, Moore F, Rasschaert J, Cardozo AK, Bellomo E, Overbergh L, Mathieu C, Lupi R, Hai T, Herchuelz A, Marchetti P, Rutter GA, Eizirik DL, Cnop M. Initiation and execution of lipotoxic ER stress in pancreatic β-cells. J Cell Sci 2008;121:2308-2318
13. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007;50:752-763
14. 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
15. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004;14:20-28
16. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529
17. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J Cell Biol 2001;153:1011-1022
18. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999;10:3787-3799
19. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003;23:7448-7459
20. Pirot P, Naamane N, Libert F, Magnusson NE, Orntoft TF, Cardozo AK, Eizirik DL. Global profiling of genes modified by endoplasmic reticulum stress in pancreatic beta cells reveals the early degradation of insulin mRNAs. Diabetologia 2007;50:1006-1014
21. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000;287:664-666
22. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001;276:13935-13940
23. Stoy J, Edghill EL, Flanagan SE, Ye H, Paz VP, Pluzhnikov A, Below JE, Hayes MG, Cox NJ, Lipkind GM, Lipton RB, Greeley SA, Patch AM, Ellard S, Steiner DF, Hattersley AT, Philipson LH, Bell GI. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A 2007;104:15040-15044
24. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, Julier C. EIF2AK3, encoding translation initiation factor 2-α kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 2000;25:406-409
25. Inoue H, Tanizawa Y, Wasson J, Behn P, Kalidas K, Bernal-Mizrachi E, Mueckler M, Marshall H, Donis-Keller H, Crock P, Rogers D, Mikuni M, Kumashiro H, Higashi K, Sobue G, Oka Y, Permutt MA. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet 1998;20:143-148
26. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 2005;307:935-939
27. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008;118:3378-3389
28. Salehi M, Aulinger BA, D'Alessio DA. Targeting β-cell mass in type 2 diabetes: promise and limitations of new drugs based on incretins. Endocr Rev 2008;29:367-379
29. Yusta B, Baggio LL, Estall JL, Koehler JA, Holland DP, Li H, Pipeleers D, Ling Z, Drucker DJ. GLP-1 receptor activation improves β cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006;4:391-406
30. Rasschaert J, Ladriere L, Urbain M, Dogusan Z, Katabua B, Sato S, Akira S, Gysemans C, Mathieu C, Eizirik DL. Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA + interferon-γ-induced apoptosis in primary pancreatic β-cells. J Biol Chem 2005;280:33984-33991
31. Ling Z, Hannaert JC, Pipeleers D. Effect of nutrients, hormones and serum on survival of rat islet beta cells in culture. Diabetologia 1994;37:15-21
32. Asfari M, Janjic D, Meda P, Li G, Halban PA, Wollheim CB. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 1992;130:167-178
33. 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
34. Buteau J, El-Assaad W, Rhodes CJ, Rosenberg L, Joly E, Prentki M. Glucagon-like peptide-1 prevents beta cell glucolipotoxicity. Diabetologia 2004;47:806-815
35. Kwon G, Pappan KL, Marshall CA, Schaffer JE, McDaniel ML. cAMP Dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in β-cells. J Biol Chem 2004;279:8938-8945
36. Quevedo C, Salinas M, Alcazar A. Initiation factor 2B activity is regulated by protein phosphatase 1, which is activated by the mitogen-activated protein kinase-dependent pathway in insulin-like growth factor 1-stimulated neuronal cells. J Biol Chem 2003;278:16579-16586
37. 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
38. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997;91:479-489
39. Holcik M, Korneluk RG. XIAP, the guardian angel. Nat Rev Mol Cell Biol 2001;2:550-556
40. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis: cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002;277:34287-34294
41. Gurzov EN, Ortis F, Bakiri L, Wagner EF, Eizirik DL. JunB inhibits ER stress and apoptosis in pancreatic β cells. PLoS ONE 2008;3:e3030
42. Drucker DJ. The biology of incretin hormones. Cell Metab 2006;3:153-165
43. Tsunekawa S, Yamamoto N, Tsukamoto K, Itoh Y, Kaneko Y, Kimura T, Ariyoshi Y, Miura Y, Oiso Y, Niki I. Protection of pancreatic β-cells by exendin-4 may involve the reduction of endoplasmic reticulum stress; in vivo and in vitro studies. J Endocrinol 2007;193:65-74
44. -/- mice reveals a role for translational control in secretory cell survival. Mol Cell 2001;7:1153-1163
45. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 2001;7:1165-1176
46. Lipson KL, Fonseca SG, Ishigaki S, Nguyen LX, Foss E, Bortell R, Rossini AA, Urano F. Regulation of insulin biosynthesis in pancreatic β cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 2006;4:245-254
47. Elouil H, Bensellam M, Guiot Y, Vander Mierde D, Pascal SM, Schuit FC, Jonas JC. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 2007;50:1442-1452
48. Egger L, Madden DT, Rheme C, Rao RV, Bredesen DE. Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death Differ 2007;14:1172-1180
49. Susini S, Roche E, Prentki M, Schlegel W. Glucose and glucoincretin peptides synergize to induce c-fos, c-jun, junB, zif-268, and nur-77 gene expression in pancreatic β (INS-1) cells. Faseb J 1998;12:1173-1182