The binary switch between life and death of endoplasmic reticulum-stressed β cells

Current Opinion in Endocrinology, Diabetes and Obesity

Volumn 17, Issue 2, 2010, Pages 107-112

  Oslowski, Christine M ^a   Urano, Fumihiko ^a,b  

^a Program in Gene Function and Expression   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

cell death; Diabetes; Endoplasmic reticulum stress; Unfolded protein response

Indexed keywords

CALCIUM ION; GLUCOSE; INSULIN;

CELL DEATH; CELL SURVIVAL; CELL TYPE; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; FEEDBACK SYSTEM; HOMEOSTASIS; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PROTEIN FOLDING; REVIEW;

ANIMALS; CELL DEATH; CELL SURVIVAL; ENDOPLASMIC RETICULUM; HUMANS; INSULIN-SECRETING CELLS; MODELS, BIOLOGICAL; PROTEIN FOLDING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 77749334709     PISSN: 1752296X     EISSN: None     Source Type: Journal    
DOI: 10.1097/MED.0b013e3283372843     Document Type: Review

References (69)

1. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008; 29:42-61.
2. Scheuner D, Kaufman RJ. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 2008; 29:317-333.
3. Fonseca SG, Burcin M, Gromada J, Urano F. Endoplasmic reticulum stress in beta-cells and development of diabetes. Curr Opin Pharmacol 2009; 9:763-770.
4. Rhodes CJ. Processing of the insulin molecule. In: LeRoith D, Taylor SI, Olefsky JM, editors. Diabetes Mellitus. Philadelphia, Pennsylvania: Lippincott Williams & Wilkins; 2004. pp. 27-50.
5. Rhodes CJ, Shoelson S, Halban PA. Insulin biosynthesis, processing, and chemistry. In: Kahn CR, Weir GC, King GL, et al., editors. Joslin's Diabetes Mellitus. Boston: Joslin Diabetes Center; 2005. pp. 65-82.
6. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519-529.
7. Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 2007; 32:469-476.
8. Ernst V, Levin DH, London IM. Inhibition of protein synthesis initiation by oxidized glutathione: activation of a protein kinase that phosphorylates the alpha subunit of eukaryotic initiation factor 2. Proc Natl Acad Sci U S A 1978; 75:4110-4114.
9. Munro S, Pelham HR. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 1986; 46:291-300.
10. Sorger PK, Pelham HR. The glucose-regulated protein grp94 is related to heat shock protein hsp90. J Mol Biol 1987; 194:341-344.
11. Kozutsumi Y, Segal M, Normington K, et al. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucoseregulated proteins. Nature 1988; 332:462-464.
12. Bulleid NJ, Freedman RB. Defective co-translational formation of disulphide bonds in protein disulphide-isomerase-deficient microsomes. Nature 1988; 335:649-651.
13. Gardner RG, Swarbrick GM, Bays NW, et al. Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J Cell Biol 2000; 151:69-82.
14. Friedlander R, Jarosch E, Urban J, et al. A regulatory link between ERassociated protein degradation and the unfolded-protein response. Nat Cell Biol 2000; 2:379-384.
15. Schuberth C, Buchberger A. Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 2005; 7:999-1006.
16. Okamura K, Kimata Y, Higashio H, et al. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem Biophys Res Commun 2000; 279:445-450.
17. Bertolotti A, Zhang Y, Hendershot LM, et al. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2:326-332.
18. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002; 3:99-111.
19. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 2001; 153:1011-1022.
20. Ron D, Habener JF. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 1992; 6:439-453.
21. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998; 12:982-995.
22. Oyadomari S, Koizumi A, Takeda K, et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 2002; 109:525-532.
23. Oyadomari S, Takeda K, Takiguchi M, et al. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 2001; 98:10845-10850.
24. McCullough KD, Martindale JL, Klotz LO, et al. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21:1249-1259.
25. Murphy KM, Ranganathan V, Farnsworth ML, et al. Bcl-2 inhibits Bax translocation from cytosol to mitochondria during drug-induced apoptosis of human tumor cells. Cell Death Differ 2000; 7:102-111.
26. Zong WX, Li C, Hatzivassiliou G, et al. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003; 162:59-69.
27. Zong WX, Lindsten T, Ross AJ, et al. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 2001; 15:1481-1486.
28. Ishigaki S, Fonseca SG, Oslowski CM, et al. AATF mediates anti-apoptotic effect of the unfolded protein response through transcriptional regulation of AKT1. Cell Death Differ 2010. [Epub ahead of print].
29. Harding HP, Zeng H, Zhang Y, et al. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell 2001; 7:1153-1163.
30. Zhang W, Feng D, Li Y, et al. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 2006; 4:491-497.
31. Scheuner D,Mierde DV, Song B, et al. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 2005; 11:757-764.
32. Scheuner D, Song B, McEwen E, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 2001; 7:1165-1176.
33. Lipson KL, Fonseca SG, Ishigaki S, et al. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 2006; 4:245-254.
34. Wolfram DJ, Wagener HP. Diabetes mellitus and simple optic atrophy among siblings: report of four cases. May Clin Proc 1938; 1:715-718.
35. Barrett TG, Bundey SE. Wolfram (DIDMOAD) syndrome. J Med Genet 1997; 34:838-841.
36. Barrett TG, Bundey SE, Macleod AF. Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet 1995; 346:1458-1463.
37. Karasik A, O'Hara C, Srikanta S, et al. Genetically programmed selective islet beta-cell loss in diabetic subjects with Wolfram's syndrome. Diabetes Care 1989; 12:135-138.
38. Inoue H, Tanizawa Y, Wasson J, et al. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet 1998; 20:143-148.
39. Strom TM, Hortnagel K, Hofmann S, et al. Diabetes insipidus, diabetes mellitus, optic atrophy and deafness (DIDMOAD) caused by mutations in a novel gene (wolframin) coding for a predicted transmembrane protein. Hum Mol Genet 1998; 7:2021-2028.
40. Khanim F, Kirk J, Latif F, Barrett TG. WFS1/wolframin mutations, Wolfram syndrome, and associated diseases. Hum Mutat 2001; 17:357-367.
41. Takeda K, Inoue H, Tanizawa Y, et al. WFS1 (Wolfram syndrome 1) gene product: predominant subcellular localization to endoplasmic reticulum in cultured cells and neuronal expression in rat brain. Hum Mol Genet 2001; 10:477-484.
42. Hofmann S, Philbrook C, Gerbitz KD, Bauer MF. Wolfram syndrome: structural and functional analyses of mutant and wild-type wolframin, the WFS1 gene product. Hum Mol Genet 2003; 12:2003-2012.
43. Fonseca SG, Fukuma M, Lipson KL, et al. WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic {beta}-cells. J Biol Chem 2005; 280: 39609-39615.
44. Ishihara H, Takeda S, Tamura A, et al. Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion. Hum Mol Genet 2004; 13:1159-1170.
45. Riggs AC, Bernal-Mizrachi E, Ohsugi M, et al. Mice conditionally lacking the Wolfram gene in pancreatic islet beta cells exhibit diabetes as a result of enhanced endoplasmic reticulum stress and apoptosis. Diabetologia 2005; 48:2313-2321.
46. Stoy J, Edghill EL, Flanagan SE, et al. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A 2007; 104:15040-15044.
47. Wang J, Takeuchi T, Tanaka S, et al. A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J Clin Invest 1999; 103:27-37.
48. Herbach N, Rathkolb B, Kemter E, et al. Dominant-negative effects of a novel mutated Ins2 allele causes early-onset diabetes and severe beta-cell loss in Munich Ins2C95S mutant mice. Diabetes 2007; 56:1268-1276.
49. Karaskov E, Scott C, Zhang L, et al. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 2006; 147:3398-3407.
50. Cnop M, Ladriere L, Hekerman P, et al. Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acidinduced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J Biol Chem 2007; 282:3989-3997.
51. Cunha DA, Hekerman P, Ladriere L, et al. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J Cell Sci 2008; 121:2308-2318.
52. Pirot P, Eizirik DL, Cardozo AK. Interferon-gamma potentiates endoplasmic reticulum stress-induced death by reducing pancreatic beta cell defence mechanisms. Diabetologia 2006; 49:1229-1236.
53. Cardozo AK, Ortis F, Storling J, et al. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 2005; 54:452-461.
54. Yoshida H, Matsui T, Yamamoto A, et al. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001; 107:881-891.
55. Shen X, Ellis RE, Lee K, et al. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 2001; 107:893-903.
56. Calfon M, Zeng H, Urano F, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing theXBP-1mRNA. Nature 2002; 415:92-96.
57. Yoshida H, Matsui T, Hosokawa N, et al. A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 2003; 4:265-271.
58. 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.
59. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000; 287:664-666.
60. Nishitoh H, Matsuzawa A, Tobiume K, et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002; 16:1345-1355.
61. Maundrell K, Antonsson B, Magnenat E, et al. Bcl-2 undergoes phosphorylation by c-Jun N-terminal kinase/stress-activated protein kinases in the presence of the constitutively active GTP-binding protein Rac1. J Biol Chem 1997; 272:25238-25242.
62. Park J, Kim I, Oh YJ, et al. Activation of c-Jun N-terminal kinase antagonizes an antiapoptotic action of Bcl-2. J Biol Chem 1997; 272:16725-16728.
63. Lipson KL, Ghosh R, Urano F. The Role of IRE1alpha in the degradation of insulin mRNA in pancreatic beta-cells. PLoS One 2008; 3:e1648.
64. Han D, Lerner AG, Vande Walle L, et al. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009; 138:562-575.
65. Hollien J, Lin JH, Li H, et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009; 186:323-331.
66. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006; 313:104-107.
67. Harding HP, Zhang Y, Bertolotti A, et al. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000; 5:897-904.
68. Song B, Scheuner D, Ron D, et al. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008; 118:3378-3389.
69. Rutkowski DT, Arnold SM, Miller CN, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 2006; 4:e374.