Diabetes as a disease of endoplasmic reticulum stress

Diabetes/Metabolism Research and Reviews

Volumn 26, Issue 8, 2010, Pages 611-621

  Thomas, Sally E ^a   Dalton, Lucy E ^a   Daly, Marie Louise ^a   Malzer, Elke ^a   Marciniak, Stefan J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Diabetes; ER stress; PERK; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ENDOPLASMIC RETICULUM KINASE; INOSITOL REQUIRING ENZYME; PROTEIN KINASE; PROTEIN KINASE R; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW; TRANSLATION INITIATION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; DIABETES MELLITUS; DIABETES MELLITUS, TYPE 1; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; EPIPHYSES; GLYCOPROTEINS; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; OSTEOCHONDRODYSPLASIAS; PROTEIN-SERINE-THREONINE KINASES; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 78049485910     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.1132     Document Type: Review

References (181)

1. Marciniak SJ, Ron D. Endoplasmic reticulum signalling in disease. Physiol Rev 2006; 86: 1133-1149.
2. Pollard MG, Travers KJ, Weissman JS. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell 1998; 1: 171-182.
3. Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1998; 1: 161-170.
4. Cabibbo A, Pagani M, Fabbri M, et al. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem 2000; 275: 4827-4833.
5. Pagani M, Fabbri M, Benedetti C, et al. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J Biol Chem 2000; 275: 23685-23692.
6. Marciniak SJ, Yun CY, Oyadomari S, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 2004; 18: 3066-3077.
7. Dias-Gunasekara S, Gubbens J, van Lith M, et al. Tissue-specific expression and dimerization of the endoplasmic reticulum oxidoreductase Ero1beta. J Biol Chem 2005; 280: 33066-33075.
8. Mezghrani A, Fassio A, Benham A, Simmen T, Braakman I, Sitia R. Manipulation of oxidative protein folding and PDI redox state in mammalian cells. EMBO J 2001; 20: 6288-6296.
9. Jansens A, van Duijn E, Braakman I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 2002; 298: 2401-2403.
10. Haynes CM, Titus EA, Cooper AA. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol Cell 2004; 15: 767-776.
11. Brodsky JL. The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem J 2007; 404: 353-363.
12. Harding H, Zhang Y, Ron D. Translation and protein folding are coupled by an endoplasmic reticulum resident kinase. Nature 1999; 397: 271-274.
13. Sood R, Porter AC, Ma K, Quilliam LA, Wek RC. Pancreatic eukaryotic initiation factor-2alpha kinase (PEK) homologues in humans, Drosophila melanogaster and Caenorhabditis elegans that mediate translational control in response to endoplasmic reticulum stress. Biochem J 2000; 346(Pt 2): 281-293.
14. Harding H, 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.
15. Harding HP, Calfon M, Urano F, Novoa I, Ron D. Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol 2002; 18: 575-599.
16. Clemens M. Protein kinases that phosphorylate eIF2 and eIF2B, their role in eukaryotic cell translational control. In Translational Control, Hershey J, Mathews M, Sonenberg N (eds). Cold Spring Harbor Laboratory Press: Cold Spring Harbor, 1996; 139-172.
17. Harding H, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003; 11: 619-633.
18. Wolcott C, Rallison M. Infancy-onset diabetes mellitus and multiple epiphyseal dysplasia. J Pediatrics 1972; 80: 292-297.
19. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, Julier C. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 2000; 25: 406-409.
20. Harding H, Zeng H, Zhang Y, et al. Diabetes mellitus and excocrine pancreatic dysfunction in Perk - /- mice reveals a role for translational control in survival of secretory cells. Mol Cell 2001; 7: 1153-1163.
21. Liu M, Li Y, Cavener D, Arvan P. Proinsulin disulfide maturation and misfolding in the endoplasmic reticulum. J Biol Chem 2005; 280: 13209-13212.
22. Zhang W, Feng D, Li Y, Iida K, McGrath B, Cavener DR. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 2006; 4: 491-497.
23. Liu CY, Xu Z, Kaufman RJ. Structure and intermolecular interactions of the luminal dimerization domain of human IRE1alpha. J Biol Chem 2003; 278: 17680-17687.
24. Bertolotti A, Zhang Y, Hendershot L, Harding H, Ron D. Dynamic interaction of BiP and the ER stress transducers in the unfolded protein response. Nat Cell Biol 2000; 2: 326-332.
25. Su Q, Wang S, Gao HQ, et al. Modulation of the eukaryotic initiation factor 2 alpha-subunit kinase PERK by tyrosine phosphorylation. J Biol Chem 2008; 283: 469-475.
26. Marciniak SJ, Garcia-Bonilla L, Hu J, Harding HP, Ron D. Activation-dependent substrate recruitment by the eukaryotic translation initiation factor 2 kinase PERK. J Cell Biol 2006; 172: 201-209.
27. 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.
28. 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.
29. Jousse C, Oyadomari S, Novoa I, et al. Inhibition of a constitutive translation initiation factor 2a phosphatase, CReP, promotes survival of stressed cells. J Cell Biol 2003; 163: 767-775.
30. Novoa I, Zeng H, Harding H, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2a. J Cell Biol 2001; 153: 1011-1022.
31. Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 2003; 22: 1180-1187.
32. Lu PD, Harding HP, Ron D. Translation re-initiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 2004; 167: 27-33.
33. Mueller PP, Jackson BM, Miller PF, Hinnebusch AG. The first and fourth upstream open reading frames in GCN4 mRNA have similar initiation efficiencies but respond differently in translational control to change in length and sequence. Mol Cell Biol 1988; 8: 5439-5447.
34. Tzamarias D, Roussou I, Thireos G. Coupling of GCN4 mRNA translational activation with decreased rates of polypeptide chain initiation. Cell 1989; 57: 947-954.
35. Hinnebusch AG. Gene-specific translational control of the yeast GCN4 gene by phosphorylation of eukaryotic initiation factor 2. Mol Microbiol 1993; 10: 215-223.
36. Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci U S A 2004; 101: 11269-11274.
37. Wang X-Z, Lawson B, Brewer J, et al. Signals from the stressed endoplasmic reticulum induce C/EBP homologous protein (CHOP/GADD153). Mol Cell Biol 1996; 16: 4273-4280.
38. 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.
39. Jousse C, Bruhat A, Harding HP, Ferrara M, Ron D, Fafournoux P. Amino acid limitation regulates CHOP expression through a specific pathway independent of the unfolded protein response. FEBS Lett 1999; 448: 211-216.
40. 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.
41. Leroux L, Desbois P, Lamotte L, et al. Compensatory responses in mice carrying a null mutation for Ins1 or Ins2. Diabetes 2001; 50(Suppl. 1): S150-S153.
42. 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.
43. Izumi T, Yokota-Hashimoto H, Zhao S, Wang J, Halban PA, Takeuchi T. Dominant negative pathogenesis by mutant proinsulin in the Akita diabetic mouse. Diabetes 2003; 52: 409-416.
44. Nozaki J, Kubota H, Yoshida H, et al. The endoplasmic reticulum stress response is stimulated through the continuous activation of transcription factors ATF6 and XBP1 in Ins2 + /Akita pancreatic beta cells. Genes Cells 2004; 9: 261-270.
45. Allen JR, Nguyen LX, Sargent KE, Lipson KL, Hackett A, Urano F. High ER stress in beta-cells stimulates intracellular degradation of misfolded insulin. Biochem Biophys Res Commun 2004; 324: 166-170.
46. Liu M, Hodish I, Rhodes CJ, Arvan P. Proinsulin maturation, misfolding, and proteotoxicity. Proc Natl Acad Sci U S A 2007; 104: 15841-15846.
47. 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.
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. Oyadomari S, Takeda K, Takiguchi M, et al. Nitric oxide-induced apoptosis in pancreatic b-cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 2001; 98: 10845-10850.
50. Boyce M, Bryant KF, Jousse C, et al. A selective inhibitor of eIF2a dephosphorylation protects cells from ER stress. Science 2005; 307: 935-939.
51. Cnop M, Ladriere L, Hekerman P, et al. 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.
52. Adler HT, Chinery R, Wu DY, et al. Leukemic HRX fusion proteins inhibit GADD34-induced apoptosis and associate with the GADD34 and hSNF5/INI1 proteins. Mol Cell Biol 1999; 19: 7050-7060.
53. Hasegawa T, Isobe K. Evidence for the interaction between Translin and GADD34 in mammalian cells. Biochim Biophys Acta 1999; 1428: 161-168.
54. Hasegawa T, Xiao H, Hamajima F, Isobe K. Interaction between DNA-damage protein GADD34 and a new member of the Hsp40 family of heat shock proteins that is induced by a DNA-damaging reagent. Biochem J 2000; 352: 795-800.
55. Hasegawa T, Yagi A, Isobe K. Interaction between GADD34 and kinesin superfamily, KIF3A. Biochem Biophys Res Commun 2000; 267: 593-596.
56. Grishin AV, Azhipa O, Semenov I, Corey SJ. Interaction between growth arrest-DNA damage protein 34 and Src kinase Lyn negatively regulates genotoxic apoptosis. Proc Natl Acad Sci U S A 2001; 98: 10172-10177.
57. Wu DY, Tkachuck DC, Roberson RS, Schubach WH. The human SNF5/INI1 protein facilitates the function of the growth arrest and DNA damage-inducible protein (GADD34) and modulates GADD34-bound protein phosphatase-1 activity. J Biol Chem 2002; 277: 27706-27715.
58. Hung WJ, Roberson RS, Taft J, Wu DY. Human BAG-1 proteins bind to the cellular stress response protein GADD34 and interfere with GADD34 functions. Mol Cell Biol 2003; 23: 3477-3486.
59. Shi W, Sun C, He B, et al. GADD34-PP1c recruited by Smad7 dephosphorylates TGF{beta} type I receptor. J Cell Biol 2004; 164: 291-300.
60. Vander Mierde D, Scheuner D, Quintens R, et al. Glucose activates a protein phosphatase-1-mediated signaling pathway to enhance overall translation in pancreatic beta-cells. Endocrinology 2007; 148: 609-617.
61. Drucker DJ. The biology of incretin hormones. Cell Metab 2006; 3: 153-165.
62. Drucker DJ. Glucagon-like peptide-1 and the islet beta-cell: augmentation of cell proliferation and inhibition of apoptosis. Endocrinology 2003; 144: 5145-5148.
63. Kim JG, Baggio LL, Bridon DP, et al. Development and characterization of a glucagon-like peptide 1-albumin conjugate: the ability to activate the glucagon-like peptide 1 receptor in vivo. Diabetes 2003; 52: 751-759.
64. Li Y, Hansotia T, Yusta B, Ris F, Halban PA, Drucker DJ. Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J Biol Chem 2003; 278: 471-478.
65. Yusta B, Baggio LL, Estall JL, et al. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006; 4: 391-406.
66. Tsunekawa S, Yamamoto N, Tsukamoto K, et al. Protection of pancreatic beta-cells by exendin-4 may involve the reduction of endoplasmic reticulum stress; in vivo and in vitro studies. J Endocrinol 2007; 193: 65-74.
67. Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 2005; 433: 477-480.
68. Yamaguchi S, Ishihara H, Yamada T, et al. ATF4-mediated induction of 4E-BP1 contributes to pancreatic beta cell survival under endoplasmic reticulum stress. Cell Metab 2008; 7: 269-276.
69. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. 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.
70. Back SH, Scheuner D, Han J, et al. Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab 2009; 10: 13-26.
71. Sigfrid LA, Cunningham JM, Beeharry N, et al. Antioxidant enzyme activity and mRNA expression in the islets of Langerhans from the BB/S rat model of type 1 diabetes and an insulin-producing cell line. J Mol Med 2004; 82: 325-335.
72. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med 1996; 20: 463-466.
73. Tanaka Y, Gleason CE, Tran PO, Harmon JS, Robertson RP. Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci U S A 1999; 96: 10857-10862.
74. Tanaka Y, Tran PO, Harmon J, Robertson RP. A role for glutathione peroxidase in protecting pancreatic beta cells against oxidative stress in a model of glucose toxicity. Proc Natl Acad Sci U S A 2002; 99: 12363-12368.
75. Kaneto H, Kajimoto Y, Miyagawa J, et al. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 1999; 48: 2398-2406.
76. Cox JS, Shamu CE, Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 1993; 73: 1197-1206.
77. 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.
78. Kimata Y, Kimata YI, Shimizu Y, et al. Genetic evidence for a role of BiP/Kar2 that regulates Ire1 in response to accumulation of unfolded proteins. Mol Biol Cell 2003; 14: 2559-2569.
79. Bertolotti A, Ron D. Alterations in an IRE1-RNA complex in the mammalian unfolded protein response. J Cell Sci 2001; 114: 3207-3212.
80. Lee KP, Dey M, Neculai D, Cao C, Dever TE, Sicheri F. Structure of the dual enzyme Ire1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 2008; 132: 89-100.
81. 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.
82. 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.
83. Calfon M, Zeng H, Urano F, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415: 92-96.
84. Lee K, Tirasophon W, Shen X, et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002; 16: 452-466.
85. Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K. A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 2003; 4: 265-271.
86. 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.
87. Lee AH, Chu GC, Iwakoshi NN, Glimcher LH. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J 2005; 24: 4368-4380.
88. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004; 21: 81-93.
89. Sriburi R, Jackowski S, Mori K, Brewer JW. XBP1: a link between the unfolded protein response, lipid biosynthesis and biogenesis of the endoplasmic reticulum. J Cell Biol 2004; 167: 35-41.
90. Iwakoshi NN, Lee AH, Glimcher LH. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol Rev 2003; 194: 29-38.
91. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003; 4: 321-329.
92. Reimold AM, Etkin A, Clauss I, et al. An essential role in liver development for transcription factor XBP-1. Genes Dev 2000; 14: 152-157.
93. Reimold AM, Iwakoshi NN, Manis J, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001; 412: 300-307.
94. Papa FR, Zhang C, Shokat K, Walter P. Bypassing a kinase activity with an ATP-competitive drug. Science 2003; 302: 1533-1537.
95. Han D, Upton JP, Hagen A, Callahan J, Oakes SA, Papa FR. A kinase inhibitor activates the IRE1alpha RNase to confer cytoprotection against ER stress. Biochem Biophys Res Commun 2008; 365: 777-783.
96. Lin JH, Li H, Yasumura D, et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007; 318: 944-949.
97. 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.
98. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006; 313: 104-107.
99. Iwawaki T, Hosoda A, Okuda T, et al. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat Cell Biol 2001; 3: 158-164.
100. Li WW, Alexandre S, Cao X, Lee AS. Transactivation of the grp78 promoter by Ca2 + depletion. A comparative analysis with A23187 and the endoplasmic reticulum Ca(2 + )-ATPase inhibitor thapsigargin. J Biol Chem 1993; 268: 12003-12009.
101. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the endoplasmic reticulum to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000; 287: 664-666.
102. 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.
103. Nishitoh H, Saitoh M, Mochida Y, et al. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 1998; 2: 389-395.
104. Ichijo H, Nishida E, Irie K, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997; 275: 90-94.
105. Saitoh M, Nishitoh H, Fujii M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998; 17: 2596-2606.
106. Hatai T, Matsuzawa A, Inoshita S, et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J Biol Chem 2000; 275: 26576-26581.
107. Fischer H, Koenig U, Eckhart L, Tschachler E. Human caspase 12 has acquired deleterious mutations. Biochem Biophys Res Commun 2002; 293: 722-726.
108. Yoneda T, Imaizumi K, Oono K, et al. 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.
109. Luo D, He Y, Zhang H, et al. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J Biol Chem 2008; 283: 11905-11912.
110. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
111. Tonnesen MF, Grunnet LG, Friberg J, et al. Inhibition of nuclear factor-kappaB or Bax prevents endoplasmic reticulum stress but not nitric oxide-mediated apoptosis in INS-1E cells. Endocrinology 2009; 150: 4094-4103.
112. Hetz C, Bernasconi P, Fisher J, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006; 312: 572-576.
113. Thirone AC, Huang C, Klip A. Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 2006; 17: 72-78.
114. Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306: 457-461.
115. Nakatani Y, Kaneto H, Kawamori D, et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 2005; 280: 847-851.
116. Ozawa K, Miyazaki M, Matsuhisa M, et al. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes 2005; 54: 657-663.
117. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006; 313: 1137-1140.
118. Gregor MF, Hotamisligil GS. Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 2007; 48: 1905-1914.
119. Xue X, Piao JH, Nakajima A, et al. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem 2005; 280: 33917-33925.
120. 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.
121. El-Assaad W, Buteau J, Peyot ML, et al. Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 2003; 144: 4154-4163.
122. Kharroubi I, Ladriere L, Cardozo AK, Dogusan Z, Cnop M, Eizirik DL. 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.
123. 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.
124. Wei Y, Wang D, Pagliassotti MJ. Saturated fatty acid-mediated endoplasmic reticulum stress and apoptosis are augmented by trans-10, cis-12-conjugated linoleic acid in liver cells. Mol Cell Biochem 2007; 303: 105-113.
125. Wang D, Wei Y, Pagliassotti MJ. Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis. Endocrinology 2006; 147: 943-951.
126. 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.
127. Guo W, Wong S, Xie W, Lei T, Luo Z. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 2007; 293: E576-E586.
128. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006; 291: E275-E281.
129. Moffitt JH, Fielding BA, Evershed R, Berstan R, Currie JM, Clark A. Adverse physicochemical properties of tripalmitin in beta cells lead to morphological changes and lipotoxicity in vitro. Diabetologia 2005; 48: 1819-1829.
130. Borradaile NM, Han X, Harp JD, Gale SE, Ory DS, Schaffer JE. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J Lipid Res 2006; 47: 2726-2737.
131. Preston AM, Gurisik E, Bartley C, Laybutt DR, Biden TJ. Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse beta cells by promoting protein overload. Diabetologia 2009; 52: 2369-2373.
132. Gwiazda KS, Yang TL, Lin Y, Johnson JD. Effects of palmitate on ER and cytosolic Ca2 + homeostasis in beta-cells. Am J Physiol Endocrinol Metab 2009; 296: E690-E701.
133. 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.
134. Kasibhatla B, Wos J, Peters KG. Targeting protein tyrosine phosphatase to enhance insulin action for the potential treatment of diabetes. Curr Opin Investig Drugs 2007; 8: 805-813.
135. Elchebly M, Payette P, Michaliszyn E, et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 1999; 283: 1544-1548.
136. Umezawa K, Kawakami M, Watanabe T. Molecular design and biological activities of protein-tyrosine phosphatase inhibitors. Pharmacol Ther 2003; 99: 15-24.
137. Xie L, Lee SY, Andersen JN, et al. Cellular effects of small molecule PTP1B inhibitors on insulin signaling. Biochemistry 2003; 42: 12792-12804.
138. Gu F, Nguyen DT, Stuible M, Dube N, Tremblay ML, Chevet E. Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J Biol Chem 2004; 279: 49689-49693.
139. Taniguchi CM, Aleman JO, Ueki K, et al. The p85alpha regulatory subunit of phosphoinositide 3-kinase potentiates c-Jun N-terminal kinase-mediated insulin resistance. Mol Cell Biol 2007; 27: 2830-2840.
140. Venable CL, Frevert EU, Kim YB, et al. Overexpression of protein-tyrosine phosphatase-1B in adipocytes inhibits insulin-stimulated phosphoinositide 3-kinase activity without altering glucose transport or Akt/protein kinase B activation. J Biol Chem 2000; 275: 18318-18326.
141. Li M, Baumeister P, Roy B, et al. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol Cell Biol 2000; 20: 5096-5106.
142. 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.
143. Chen X, Shen J, Prywes R. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J Biol Chem 2002; 277: 13045-13052.
144. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 and unmasking of Golgi localization signals. Dev Cell 2002; 3: 99-111.
145. Ye J, Rawson RB, Komuro R, et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 2000; 6: 1355-1364.
146. Raggo C, Rapin N, Stirling J, et al. Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol Cell Biol 2002; 22: 5639-5649.
147. Lu R, Misra V. Potential role for luman, the cellular homologue of herpes simplex virus VP16 (alpha gene trans-inducing factor), in herpesvirus latency. J Virol 2000; 74: 934-943.
148. DenBoer LM, Hardy-Smith PW, Hogan MR, Cockram GP, Audas TE, Lu R. Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem Biophys Res Commun 2005; 331: 113-119.
149. Kondo S, Murakami T, Tatsumi K, et al. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol 2005; 7: 186-194.
150. Zhang K, Shen X, Wu J, et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 2006; 124: 587-599.
151. Stirling J, O'Hare P. CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol Biol Cell 2006; 17: 413-426.
152. Babu DA, Deering TG, Mirmira RG. A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis. Mol Genet Metab 2007; 92: 43-55.
153. Stoffers DA, Ferrer J, Clarke WL, Habener JF. Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat Genet 1997; 17: 138-139.
154. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 2004; 114: 828-836.
155. Brissova M, Blaha M, Spear C, et al. Reduced PDX-1 expression impairs islet response to insulin resistance and worsens glucose homeostasis. Am J Physiol Endocrinol Metab 2005; 288: E707-E714.
156. Sachdeva MM, Claiborn KC, Khoo C, et al. Pdx1 (MODY4) regulates pancreatic beta cell susceptibility to ER stress. Proc Natl Acad Sci U S A 2009; 106: 19090-19095.
157. Bonner-Weir S, Toschi E, Inada A, et al. The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Pediatr Diabetes 2004; 5(Suppl. 2): 16-22.
158. Gu D, Lee MS, Krahl T, Sarvetnick N. Transitional cells in the regenerating pancreas. Development 1994; 120: 1873-1881.
159. Lipsett M, Finegood DT. Beta-cell neogenesis during prolonged hyperglycemia in rats. Diabetes 2002; 51: 1834-1841.
160. Minami K, Okuno M, Miyawaki K, et al. Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc Natl Acad Sci U S A 2005; 102: 15116-15121.
161. Zulewski H, Abraham EJ, Gerlach MJ, et al. Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes 2001; 50: 521-533.
162. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429: 41-46.
163. Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest 2007; 117: 2553-2561.
164. Meier JJ, Lin JC, Butler AE, Galasso R, Martinez DS, Butler PC. Direct evidence of attempted beta cell regeneration in an 89-year-old patient with recent-onset type 1 diabetes. Diabetologia 2006; 49: 1838-1844.
165. Bi M, Naczki C, Koritzinsky M, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005; 24: 3470-3481.
166. Gupta S, McGrath B, Cavener DR. PERK regulates the proliferation and development of insulin-secreting beta-cell tumors in the endocrine pancreas of mice. PLoS ONE 2009; 4: e8008.
167. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell 2006; 21: 521-531.
168. Brewer JW, Hendershot LM, Sherr CJ, Diehl JA. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc Natl Acad Sci U S A 1999; 96: 8505-8510.
169. Brewer JW, Diehl JA. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci U S A 2000; 97: 12625-12630.
170. Raven JF, Baltzis D, Wang S, et al. PKR and PKR-like endoplasmic reticulum kinase induce the proteasome-dependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation. J Biol Chem 2008; 283: 3097-3108.
171. Zhang F, Hamanaka RB, Bobrovnikova-Marjon E, et al. Ribosomal stress couples the unfolded protein response to p53-dependent cell cycle arrest. J Biol Chem 2006; 281: 30036-30045.
172. Qu L, Huang S, Baltzis D, et al. Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3beta. Genes Dev 2004; 18: 261-277.
173. Pluquet O, Qu LK, Baltzis D, Koromilas AE. Endoplasmic reticulum stress accelerates p53 degradation by the cooperative actions of Hdm2 and glycogen synthase kinase 3beta. Mol Cell Biol 2005; 25: 9392-9405.
174. Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 2006; 281: 7260-7270.
175. Baltzis D, Pluquet O, Papadakis AI, Kazemi S, Qu LK, Koromilas AE. The eIF2alpha kinases PERK and PKR activate glycogen synthase kinase 3 to promote the proteasomal degradation of p53. J Biol Chem 2007; 282: 31675-31687.
176. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003; 3: 577-587.
177. Zhang Y, Wolf GW, Bhat K, et al. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 2003; 23: 8902-8912.
178. Dai MS, Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem 2004; 279: 44475-44482.
179. Dai MS, Zeng SX, Jin Y, Sun XX, David L, Lu H. Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol Cell Biol 2004; 24: 7654-7668.
180. Jin A, Itahana K, O'Keefe K, Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol 2004; 24: 7669-7680.
181. DuRose JB, Scheuner D, Kaufman RJ, Rothblum LI, Niwa M. Phosphorylation of eukaryotic translation initiation factor 2alpha coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol Cell Biol 2009; 29: 4295-4307.