Glucose amplifies fatty acid-induced endoplasmic reticulum stress in pancreatic β-cells via activation of mTORC1

PLoS ONE

Volumn 4, Issue 3, 2009, Pages

  Bachar, Etti ^a   Ariav, Yafa ^a   Ketzinel Gilad, Mali ^a   Cerasi, Erol ^a   Kaiser, Nurit ^a   Leibowitz, Gil ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; FATTY ACID; GLUCOSE; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MEMBRANE PROTEIN; PALMITIC ACID; PROINSULIN; PROTEIN MTORC1; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; CYCLOHEXIMIDE; ERN2 PROTEIN, MOUSE; MTORC1 PROTEIN, MOUSE; PALMITIC ACID DERIVATIVE; PROTEIN SYNTHESIS INHIBITOR; TORC1 PROTEIN, RAT; TRANSCRIPTION FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FIBROBLAST; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; GERBIL; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CELL LINE; CYCLOHEXIMIDE; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GERBILLINAE; GLUCOSE; INSULIN-SECRETING CELLS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MEMBRANE PROTEINS; MICE; OXIDATIVE STRESS; PALMITATES; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SIROLIMUS; TRANSCRIPTION FACTORS;

EID: 63349109171     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004954     Document Type: Article

References (53)

1. Poitout V, Robertson RP (2008) Glucolipotoxicity: Fuel excess and beta-cell dysfunction. Endocr Rev 29: 351-366.
2. Goh TT, Mason TM, Gupta N, So A, Lam TK, et al. (2007) Lipid-induced beta-cell dysfunction in vivo in models of progressive beta-cell failure. Am J Physiol Endocrinol Metab 292: E549-E560.
3. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, et al. (2001) Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 59: 69-76.
4. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY (2003) Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 52: 726-733.
5. Eitel K, Staiger H, Brendel MD, Brandhorst D, Bretzel RG, et al. (2002) Different role of saturated and unsaturated fatty acids in beta-cell apoptosis. Biochem Biophys Res Commun 299: 853-856.
6. Poitout V, Robertson RP (2002) Minireview: secondary beta-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 143: 339-342.
7. Prentki M, Joly E, El-Assaad W, Roduit R (2002) Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: role in beta-cell adaptation and failure in the etiology of diabetes. Diabetes 51(Suppl 3): S405-413.
8. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, et al. (2007) Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50: 752-563.
9. Lai E, Bikopoulos G, Wheeler MB, Rozakis-Adcock M, Volchuk A (2008) Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic beta-cells. Am J Physiol Endocrinol Metab 294: E540-550.
10. Karaskov E, Scott C, Zhang L, Teodoro T, Ravazzola M, et al. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147: 3398-3407.
11. Eizirik DL, Cardozo AK, Cnop M (2008) The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 29: 42-61.
12. Jeffrey KD, Alejandro EU, Luciani DS, Kalynyak TB, Hu X, et al. (2008) Carboxypeptidase E mediates palmitate-induced beta-cell ER stress and apoptosis. Proc Natl Acad Sci U S A 105: 8452-8457.
13. Fonseca SG, Lipson KL, Urano F (2007) Endoplasmic reticulum stress signaling in pancreatic beta-cells. Antioxid Redox Signal 9: 2335-2344.
14. Ortsäter H, Sjöholm A (2007) A busy cell-endoplasmic reticulum stress in the pancreatic beta-cell. Mol Cell Endocrinol 277: 1-5.
15. Patil C, Walter P (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13: 349-355.
16. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86: 1133-1149.
17. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
18. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
19. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
20. Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459.
21. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
22. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389.
23. Um SH, D'Alessio D, Thomas G (2006) Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 3: 393-402.
24. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124: 471-484.
25. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, et al. (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10: 457-468.
26. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
27. Sarbassov DD, Ali SM, Sabatini DM (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603.
28. Wang X, Beugnet A, Murakami M, Yamanaka S, Proud CG (2005) Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol Cell Biol 25: 2558-2572.
29. Kaiser N, Nesher R, Donath MY, Fraenkel M, Behar V, et al. (2005) Psammomys obesus, a model for environment-gene interactions in type 2 diabetes. Diabetes 54(Suppl 2): S137-144.
30. Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M, et al. (2003) Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell 11: 1457-1466.
31. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J (2003) Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 13: 1259-1268.
32. Cunha DA, Hekerman P, Ladriere L, Bazarra-Castro A, Ortis F, et al. (2008) Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J Cell Sci 121: 2308-2318.
33. Lipson KL, Ghosh R, Urano F (2008) The role of IRE1alpha in the degradation of insulin mRNA in pancreatic beta-cells. PLoS ONE 3: e1648.
34. Schuit FC, In't Veld PA, Pipeleers DG (1988) Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc Natl Acad Sci U S A 85: 3865-3869.
35. Elouil H, Bensellam M, Guiot Y, Vander Mierde D, Pascal SM, et al. (2007) Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 50: 1442-1452.
36. Lipson KL, Fonseca SG, Ishigaki S, Nguyen LX, Foss E, et al. (2006) Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 4: 245-254.
37. Briaud I, Dickson LM, Lingohr MK, McCuaig JF, Lawrence JC, et al. (2005) Insulin receptor substrate-2 proteasomal degradation mediated by a mammalian target of rapamycin (mTOR)-induced negative feedback down-regulates protein kinase B-mediated signaling pathway in beta-cells. J Biol Chem 280: 2282-2293.
38. Fraenkel M, Ketzinel-Gilad M, Ariav Y, Pappo O, Karaca M, et al. (2008) mTOR inhibition by rapamycin prevents -cell adaptation to hyperglycemia and exacerbates the metabolic state in type 2 diabetes. Diabetes 57: 945-957.
39. Ozcan U, Ozcan L, Yilmaz E, Duvel K, Sahin M, et al. (2008) Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol Cell 29: 541-551.
40. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633.
41. Serizawa M, Nabika T, Ochiai Y, Takahashi K, Yamaguchi S, et al. (2008) Association between PRKCH gene polymorphisms and subcortical silent brain infarction. Atherosclerosis 199: 340-345.
42. Trusina A, Papa FR, Tang C (2008) Rationalizing translation attenuation in the network architecture of the unfolded protein response. Proc Natl Acad Sci U S A 105: 20280-20285.
43. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev 6: 1402-1413.
44. Martinez SC, Tanabe K, Cras-Meneur C, Abumrad NA, Bernal-Mizrachi E, et al. (2008) Inhibition of Foxol protects pancreatic islet beta-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 57: 846-859.
45. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, et al. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140.
46. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, et al. (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205.
47. Tremblay F, Krebs M, Dombrowski L, Brehm A, Bernroider E, et al. (2005) Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54: 2674-2684.
48. Rachdi L, Balcazar N, Osorio-Duque F, Elghazi L, Weiss A, et al. (2008) Disruption of Tsc2 in pancreatic beta cells induces beta cell mass expansion and improved glucose tolerance in a TORC1-dependent manner. Proc Natl Acad Sci U S A 105: 9250-9255.
49. Shigeyama Y, Kobayashi T, Kido Y, Hashimoto N, Asahara S, et al. (2008) Biphasic response of pancreatic beta-cell mass to ablation of tuberous sclerosis complex 2 in mice. Mol Cell Biol 28: 2971-2979.
50. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, et al. (2007) mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450: 736-740.
51. Kaiser N, Corcos AP, Sarel I, Cerasi E (1991) Monolayer culture of adult rat pancreatic islets on extracellular matrix: Modulation of B-cell function by chronic exposure to high glucose. Endocrinology 129: 2067-2076.
52. Attali V, Parnes M, Ariav Y, Cerasi E, Kaiser N, et al. (2006) Regulation of insulin secretion and proinsulin biosynthesis by succinate. Endocrinology 147: 5110-5118.
53. Alarcon C, Lincoln B, Rhodes CJ (1993) The biosynthesis of the subtilisin-related proprotein convertase PC3, but no that of the PC2 convertase, is regulated by glucose in parallel to proinsulin biosynthesis in rat pancreatic islets. J Biol Chem 268: 4276-4280.