The binary switch that controls the life and death decisions of ER stressed β cells

Current Opinion in Cell Biology

Volumn 23, Issue 2, 2011, Pages 207-215

  Oslowski, Christine M ^a   Urano, Fumihiko ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPLASMIC RETICULUM; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; WOLFRAM SYNDROME;

ANIMALS; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; HUMANS; INSULIN-SECRETING CELLS; PROTEIN UNFOLDING; STRESS, PHYSIOLOGICAL;

EID: 79954421880     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.11.005     Document Type: Review

References (77)

1. Donath M.Y., Halban P.A. Decreased beta-cell mass in diabetes: significance, mechanisms and therapeutic implications. Diabetologia 2004, 47:581-589.
2. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
3. Oslowski C.M., Urano F. The binary switch between life and death of endoplasmic reticulum-stressed beta cells. Curr Opin Endocrinol Diabetes Obes 2010, 17:107-112.
4. Eizirik D.L., Cardozo A.K., Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008, 29:42-61.
5. Fonseca S.G., Ishigaki S., Oslowski C.M., Lu S., Lipson K.L., Ghosh R., Hayashi E., Ishihara H., Oka Y., Permutt M.A., et al. Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Invest 2010, 120:744-755.
6. Fonseca S.G., Burcin M., Gromada J., Urano F. Endoplasmic reticulum stress in beta-cells and development of diabetes. Curr Opin Pharmacol 2009, 9:763-770.
7. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
8. Lipson K.L., Fonseca S.G., Ishigaki S., Nguyen L.X., Foss E., Bortell R., Rossini A.A., Urano F. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 2006, 4:245-254.
9. Lipson K.L., Ghosh R., Urano F. The role of IRE1alpha in the degradation of insulin mRNA in pancreatic beta-cells. PLoS One 2008, 3:e1648.
10. 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 beta-cell apoptosis. Endocrinology 2006, 147:3398-3407.
11. Cnop M., Ladriere L., Hekerman P., Ortis F., Cardozo A.K., Dogusan Z., Flamez D., Boyce M., Yuan J., Eizirik D.L. Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J Biol Chem 2007, 282:3989-3997.
12. Kharroubi I., Ladriere L., Cardozo A.K., Dogusan Z., Cnop M., Eizirik D.L. Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 2004, 145:5087-5096.
13. Cardozo A.K., Ortis F., Storling J., Feng Y.M., Rasschaert J., Tonnesen M., Van Eylen F., Mandrup-Poulsen T., Herchuelz A., Eizirik D.L. 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.
14. Eizirik D.L., Flodstrom M., Karlsen A.E., Welsh N. The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic beta cells. Diabetologia 1996, 39:875-890.
15. Oyadomari S., Takeda K., Takiguchi M., Gotoh T., Matsumoto M., Wada I., Akira S., Araki E., Mori M. 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.
16. Cardozo A.K., Heimberg H., Heremans Y., Leeman R., Kutlu B., Kruhoffer M., Orntoft T., Eizirik D.L. A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta-cells. J Biol Chem 2001, 276:48879-48886.
17. Wang J., Takeuchi T., Tanaka S., Kubo S.K., Kayo T., Lu D., Takata K., Koizumi A., Izumi T. 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.
18. Yoshioka M., Kayo T., Ikeda T., Koizumi A. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes 1997, 46:887-894.
19. Kayo T., Koizumi A. Mapping of murine diabetogenic gene mody on chromosome 7 at D7Mit258 and its involvement in pancreatic islet and beta cell development during the perinatal period. J Clin Invest 1998, 101:2112-2118.
20. Stoy J., Edghill E.L., Flanagan S.E., Ye H., Paz V.P., Pluzhnikov A., Below J.E., Hayes M.G., Cox N.J., Lipkind G.M., et al. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A 2007, 104:15040-15044.
21. Ritzel R.A., Meier J.J., Lin C.Y., Veldhuis J.D., Butler P.C. Human islet amyloid polypeptide oligomers disrupt cell coupling, induce apoptosis, and impair insulin secretion in isolated human islets. Diabetes 2007, 56:65-71.
22. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., Apostol M.I., Thompson M.J., Balbirnie M., Wiltzius J.J., McFarlane H.T., et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 2007, 447:453-457.
23. Huang C.J., Haataja L., Gurlo T., Butler A.E., Wu X., Soeller W.C., Butler P.C. Induction of endoplasmic reticulum stress-induced beta-cell apoptosis and accumulation of polyubiquitinated proteins by human islet amyloid polypeptide. Am J Physiol Endocrinol Metab 2007, 293:E1656-E1662.
24. Matveyenko A.V., Gurlo T., Daval M., Butler A.E., Butler P.C. Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPP-induced beta-cell endoplasmic reticulum stress. Diabetes 2009, 58:906-916.
25. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. 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.
26. Shen X., Ellis R.E., Lee K., Liu C.Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D.M., Mori K., et al. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 2001, 107:893-903.
27. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415:92-96.
28. Yoshida H., Matsui T., Hosokawa N., Kaufman R.J., Nagata K., Mori K. A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 2003, 4:265-271.
29. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003, 23:7448-7459.
30. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
31. Nishitoh H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., Hori S., Kakizuka A., Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002, 16:1345-1355.
32. Maundrell K., Antonsson B., Magnenat E., Camps M., Muda M., Chabert C., Gillieron C., Boschert U., Vial-Knecht E., Martinou J.C., 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.
33. Park J., Kim I., Oh Y.J., Lee K., Han P.L., Choi E.J. Activation of c-Jun N-terminal kinase antagonizes an anti-apoptotic action of Bcl-2. J Biol Chem 1997, 272:16725-16728.
34. Han D., Lerner A.G., Vande Walle L., Upton J.P., Xu W., Hagen A., Backes B.J., Oakes S.A., Papa F.R. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009, 138:562-575.
35. Hollien J., Lin J.H., Li H., Stevens N., Walter P., Weissman J.S. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009, 186:323-331.
36. Hollien J., Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006, 313:104-107.
37. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
38. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K., Cavener D.R. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 2002, 22:3864-3874.
39. Zhang W., Feng D., Li Y., Iida K., McGrath B., Cavener D.R. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 2006, 4:491-497.
40. Harding H.P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., Sabatini D.D., Ron D. 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.
41. Harding H.P., Zhang Y., Bertolotti A., Zeng H., Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000, 5:897-904.
42. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000, 6:1099-1108.
43. Ishigaki S., Fonseca S.G., Oslowski C.M., Jurczyk A., Shearstone J.R., Zhu L.J., Permutt M.A., Greiner D.L., Bortell R., Urano F. AATF mediates an antiapoptotic effect of the unfolded protein response through transcriptional regulation of AKT1. Cell Death Differ 2010, 17:774-786.
44. Ron D., Habener J.F. 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.
45. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12:982-995.
46. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., Mori M. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 2002, 109:525-532.
47. Song B., Scheuner D., Ron D., Pennathur S., Kaufman R.J. 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.
48. Ye J., Rawson R.B., Komuro R., Chen X., Dave U.P., Prywes R., Brown M.S., Goldstein J.L. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 2000, 6:1355-1364.
49. Yoshida H., Okada T., Haze K., Yanagi H., Yura T., Negishi M., Mori K. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 2000, 20:6755-6767.
50. 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.
51. Seo H.Y., Kim Y.D., Lee K.M., Min A.K., Kim M.K., Kim H.S., Won K.C., Park J.Y., Lee K.U., Choi H.S., et al. Endoplasmic reticulum stress-induced activation of activating transcription factor 6 decreases insulin gene expression via up-regulation of orphan nuclear receptor small heterodimer partner. Endocrinology 2008, 149:3832-3841.
52. Rutkowski D.T., Arnold S.M., Miller C.N., Wu J., Li J., Gunnison K.M., Mori K., Sadighi Akha A.A., Raden D., Kaufman R.J. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 2006, 4:e374.
53. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000, 2:326-332.
54. Okamura K., Kimata Y., Higashio H., Tsuru A., Kohno K. 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.
55. 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.
56. Novoa I., Zeng H., Harding H.P., Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 2001, 153:1011-1022.
57. Yan W., Frank C.L., Korth M.J., Sopher B.L., Novoa I., Ron D., Katze M.G. Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci U S A 2002, 99:15920-15925.
58. Ladiges W.C., Knoblaugh S.E., Morton J.F., Korth M.J., Sopher B.L., Baskin C.R., MacAuley A., Goodman A.G., LeBoeuf R.C., Katze M.G. Pancreatic beta-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes 2005, 54:1074-1081.
59. Qiu Y., Mao T., Zhang Y., Shao M., You J., Ding Q., Chen Y., Wu D., Xie D., Lin X., et al. A crucial role for RACK1 in the regulation of glucose-stimulated IRE1alpha activation in pancreatic beta cells. Sci Signal 2010, 3:ra7.
60. Wolfram D.J., Wagener H.P. Diabetes mellitus and simple optic atrophy among siblings: report of four cases. May Clin Proc 1938, 1:715-718.
61. Barrett T.G., Bundey S.E. Wolfram (DIDMOAD) syndrome. J Med Genet 1997, 34:838-841.
62. Barrett T.G., Bundey S.E., Macleod A.F. Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet 1995, 346:1458-1463.
63. Karasik A., O'Hara C., Srikanta S., Swift M., Soeldner J.S., Kahn C.R., Herskowitz R.D. Genetically programmed selective islet beta-cell loss in diabetic subjects with Wolfram's syndrome. Diabetes Care 1989, 12:135-138.
64. Inoue H., Tanizawa Y., Wasson J., Behn P., Kalidas K., Bernal-Mizrachi E., Mueckler M., Marshall H., Donis-Keller H., Crock P., 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.
65. Strom T.M., Hortnagel K., Hofmann S., Gekeler F., Scharfe C., Rabl W., Gerbitz K.D., Meitinger T. 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.
66. Khanim F., Kirk J., Latif F., Barrett T.G. WFS1/wolframin mutations, Wolfram syndrome, and associated diseases. Hum Mutat 2001, 17:357-367.
67. Takeda K., Inoue H., Tanizawa Y., Matsuzaki Y., Oba J., Watanabe Y., Shinoda K., Oka Y. 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.
68. Hofmann S., Philbrook C., Gerbitz K.D., Bauer M.F. Wolfram syndrome: structural and functional analyses of mutant and wild-type wolframin, the WFS1 gene product. Hum Mol Genet 2003, 12:2003-2012.
69. Fonseca S.G., Fukuma M., Lipson K.L., Nguyen L.X., Allen J.R., Oka Y., Urano F. 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.
70. Ishihara H., Takeda S., Tamura A., Takahashi R., Yamaguchi S., Takei D., Yamada T., Inoue H., Soga H., Katagiri H., 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.
71. Riggs A.C., Bernal-Mizrachi E., Ohsugi M., Wasson J., Fatrai S., Welling C., Murray J., Schmidt R.E., Herrera P.L., Permutt M.A. 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.
72. Minton J.A., Hattersley A.T., Owen K., McCarthy M.I., Walker M., Latif F., Barrett T., Frayling T.M. Association studies of genetic variation in the WFS1 gene and type 2 diabetes in U.K. populations. Diabetes 2002, 51:1287-1290.
73. Sandhu M.S., Weedon M.N., Fawcett K.A., Wasson J., Debenham S.L., Daly A., Lango H., Frayling T.M., Neumann R.J., Sherva R., et al. Common variants in WFS1 confer risk of type 2 diabetes. Nat Genet 2007, 39:951-953.
74. Franks P.W., Rolandsson O., Debenham S.L., Fawcett K.A., Payne F., Dina C., Froguel P., Mohlke K.L., Willer C., Olsson T., et al. Replication of the association between variants in WFS1 and risk of type 2 diabetes in European populations. Diabetologia 2008, 51:458-463.
75. Florez J.C., Jablonski K.A., McAteer J., Sandhu M.S., Wareham N.J., Barroso I., Franks P.W., Altshuler D., Knowler W.C. Testing of diabetes-associated WFS1 polymorphisms in the Diabetes Prevention Program. Diabetologia 2008, 51:451-457.
76. Sparso T., Andersen G., Albrechtsen A., Jorgensen T., Borch-Johnsen K., Sandbaek A., Lauritzen T., Wasson J., Permutt M.A., Glaser B., et al. Impact of polymorphisms in WFS1 on prediabetic phenotypes in a population-based sample of middle-aged people with normal and abnormal glucose regulation. Diabetologia 2008, 51:1646-1652.
77. Schafer S.A., Mussig K., Staiger H., Machicao F., Stefan N., Gallwitz B., Haring H.U., Fritsche A. A common genetic variant in WFS1 determines impaired glucagon-like peptide-1-induced insulin secretion. Diabetologia 2009, 52:1075-1082.