Role of endoplasmic reticulum stress in metabolic disease and other disorders

Annual Review of Medicine

Volumn 63, Issue , 2012, Pages 317-328

  Ozcan, Lale ^a   Tabas, Ira ^a,b  

^a Columbia University ^*  (United States)

^b Department of Medicine   (United States)

Author keywords

Atherosclerosis; Cancer; Diabetes; ER stress; Liver disease; Neurodegenerative disease; Unfolded protein response (UPR)

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; AMYLOID BETA PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INSULIN RECEPTOR SUBSTRATE 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; VASCULAR CELL ADHESION MOLECULE 1; X BOX BINDING PROTEIN 1;

ALCOHOL LIVER DISEASE; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ATHEROSCLEROSIS; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HEPATITIS B; HEPATITIS C; HUMAN; METABOLIC DISORDER; NEOPLASM; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UNFOLDED PROTEIN RESPONSE;

APOPTOSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; METABOLIC DISEASES;

EID: 84855966721     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-043010-144749     Document Type: Review

References (66)

1. Rutkowski DT, Kaufman RJ. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20-28 (Pubitemid 38076857)
2. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8:519-29 (Pubitemid 46985379)
3. Tabas I, Ron D. 2011. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13:184-90
4. Marciniak SJ, Ron D. 2006. Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86:1133-49 (Pubitemid 44521649)
5. Wu J, Kaufman RJ. 2006. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13:374-84
6. Oikawa D, Kimata Y, Kohno K. 2007. Self-association and BiP dissociation are not sufficient for activation of the ER stress sensor Ire1. J. Cell Sci. 120:1681-88 (Pubitemid 46831798)
7. Glimcher LH. 2010. XBP1: the last two decades. Ann. Rheum. Dis. 69(Suppl. 1):i67-i71
8. Hollien J, Weissman JS. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104-7 (Pubitemid 44051264)
9. Urano F, Wang X, Bertolotti A, et al. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-66 (Pubitemid 30070916)
10. Nakagawa T, Zhu H, Morishima N, et al. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103 (Pubitemid 30038529)
11. Ittner LM, Gotz J. 2011. Amyloid-beta and tau-a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 12:65-72
12. Katayama T, Imaizumi K, Sato N, et al. 1999. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat. Cell Biol. 1:479-85 (Pubitemid 129503667)
13. Milhavet O, Martindale JL, Camandola S, et al. 2002. Involvement of Gadd153 in the pathogenic action of presenilin-1 mutations. J. Neurochem. 83:673-81 (Pubitemid 35231821)
14. Hoozemans JJ, Veerhuis R, van Haastert ES, et al. 2005. The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol. 110:165-72 (Pubitemid 41245205)
15. Unterberger U, Hoftberger R, Gelpi E, et al. 2006. Endoplasmic reticulum stress features are prominent in Alzheimer disease but not in prion diseases in vivo. J. Neuropathol. Exp. Neurol. 65:348-57 (Pubitemid 44264832)
16. Healy DG, bou-Sleiman PM, Wood NW. 2004. P INK, P ANK, or PARK? A clinicians' guide to familial parkinsonism. Lancet Neurol. 3:652-62 (Pubitemid 39370635)
17. Shimura H, Hattori N, Kubo S, et al. 2000. Familial Parkinson disease gene product, parkin, is a ubiquitinprotein ligase. Nat. Genet. 25:302-5 (Pubitemid 30437317)
18. Imai Y, Soda M, Takahashi R. 2000. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 275:35661-64
19. Atkin JD, Farg MA, Walker AK, et al. 2008. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol. Dis. 30:400-7
20. Saxena S, Cabuy E, Caroni P. 2009. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 12:627-36
21. Lee YH, White MF. 2004. Insulin receptor substrate proteins and diabetes. Arch. Pharm. Res. 27:361-70 (Pubitemid 43073729)
22. Ozcan U, Cao Q, Yilmaz E, et al. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-61 (Pubitemid 39372439)
23. Boden G, Duan X, Homko C, et al. 2008. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 57:2438-44
24. Gregor MF, Yang L, Fabbrini E, et al. 2009. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 58:693-700
25. Wang Y, Vera L, Fischer WH, et al. 2009. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 460:534-37
26. Cnop M, Welsh N, Jonas JC, et al. 2005. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54(Suppl. 2):S97-107 (Pubitemid 43343337)
27. Laybutt DR, Preston AM, Akerfeldt MC, et al. 2007. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50:752-63 (Pubitemid 46355827)
28. Oyadomari S, Koizumi A, Takeda K, et al. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109:525-32 (Pubitemid 34171784)
29. Song B, Scheuner D, Ron D, et al. 2008. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J. Clin. Invest. 118:3378-89
30. Lee AH, Heidtman K, Hotamisligil GS, et al. 2011. Dual and opposing roles of the unfolded protein response regulated by IRE1αand XBP1 in proinsulin processing and insulin secretion. Proc. Natl. Acad. Sci. USA 108:8885-90
31. Williams KJ, Tabas I. 1998. The response-to-retention hypothesis of atherogenesis reinforced. Curr. Opin. Lipidol. 9:471-74 (Pubitemid 28495557)
32. Tabas I. 2010. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10:36-46
33. Moore KJ, Tabas I. 2011. Macrophages in the pathogenesis of atherosclerosis. Cell 145:341-55
34. Kedi X, Ming Y, Yongping W, et al. 2009. Free cholesterol overloading induced smooth muscle cells death and activated both ER-and mitochondrial- dependent death pathway. Atherosclerosis 207:123-30
35. Nakano T, Watanabe H, Ozeki M, et al. 2006. Endoplasmic reticulumCa2+ depletion induces endothelial cell apoptosis independently of caspase-12. Cardiovasc. Res. 69:908-15 (Pubitemid 43227989)
36. Tsukano H, Gotoh T, Endo M, et al. 2010. The endoplasmic reticulum stress-CHOP pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques. Arterioscler. Thromb. Vasc. Biol. 30:1925-32
37. Thorp E, Li G, Seimon TA, et al. 2009. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/-and Ldlr-/-mice lacking CHO P. Cell Metab. 9:474-81
38. Myoishi M, Hao H, Minamino T, et al. 2007. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation 116:1226-33 (Pubitemid 47517533)
39. Erbay E, Babaev VR, Mayers JR, et al. 2009. Reducing endoplasmic reticulum stress through amacrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 15:1383-91
40. Sanson M, Auge N, Vindis C, et al. 2009. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circ. Res. 104:328-36
41. Civelek M, Manduchi E, Riley RJ, et al. 2009. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circ. Res. 105:453-61
42. Geng YJ, Libby P. 2002. Progression of atheroma: a struggle between death and procreation. Arterioscler. Thromb. Vasc. Biol. 22:1370-80
43. Werstuck GH, Khan MI, Femia G, et al. 2006. Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model. Diabetes 55:93-101 (Pubitemid 43343303)
44. Pedruzzi E, Guichard C, Ollivier V, et al. 2004. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterolinduced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol. Cell Biol. 24:10703-17 (Pubitemid 39603128)
45. Diraison F, Dusserre E, Vidal H, et al. 2002. Increased hepatic lipogenesis but decreased expression of lipogenic gene in adipose tissue in human obesity. Am. J. Physiol. Endocrinol. Metab. 282:E46-E51 (Pubitemid 34654105)
46. Kammoun HL, Chabanon H, Hainault I, et al. 2009. GRP78 expression inhibits insulin and ER stressinduced SREBP-1c activation and reduces hepatic steatosis in mice. J. Clin. Invest. 119:1201-15
47. Lee AH, Scapa EF, Cohen DE, et al. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320:1492-96 (Pubitemid 351929428)
48. Oyadomari S, Harding HP, Zhang Y, et al. 2008. Dephosphorylation of translation initiation factor 2α enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab. 7:520-32 (Pubitemid 351729207)
49. Tardif KD, Mori K, Kaufman RJ, et al. 2004. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 279:17158-64 (Pubitemid 38560472)
50. Xu Z, Jensen G, Yen TS. 1997. Activation of hepatitis B virus S promoter by the viral large surface protein via induction of stress in the endoplasmic reticulum. J. Virol. 71:7387-92 (Pubitemid 27391678)
51. Asselah T, Bieche I, Mansouri A, et al. 2010. In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C. J. Pathol. 221:264-74
52. Ji C, Kaplowitz N. 2006. ER stress: Can the liver cope?. J. Hepatol. 45:321-33
53. Ji C, Mehrian-Shai R, Chan C, et al. 2005. Role of CHOP in hepatic apoptosis in the murine model of intragastric ethanol feeding. Alcohol. Clin. Exp. Res. 29:1496-503 (Pubitemid 41243375)
54. Ji C, Kaplowitz N. 2003. Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 124:1488-99 (Pubitemid 36531821)
55. Fernandez PM, Tabbara SO, Jacobs LK, et al. 2000. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res. Treat. 59:15-26 (Pubitemid 30153894)
56. Lee AS. 2007. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res. 67:3496-99 (Pubitemid 46762126)
57. Carrasco DR, Sukhdeo K, Protopopova M, et al. 2007. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 11:349-60 (Pubitemid 46518314)
58. So AY, de la FE, Walter P, et al. 2009. The unfolded protein response during prostate cancer development. Cancer Metastasis Rev. 28:219-23
59. Ozcan U, Yilmaz E, Ozcan L, et al. 2006. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:1137-40 (Pubitemid 44300242)
60. Ozcan L, Ergin AS, Lu A, et al. 2009. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 9:35-51
61. Bown CD, Wang JF, Chen B, et al. 2002. Regulation of ER stress proteins by valproate: therapeutic implications. Bipolar. Disord. 4:145-51 (Pubitemid 34411277)
62. Kudo T, Kanemoto S, Hara H, et al. 2008. A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ. 15:364-75
63. Smith WW, Jiang H, Pei Z, et al. 2005. Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum. Mol. Genet. 14:3801-11 (Pubitemid 43020082)
64. Nakka VP, Gusain A, Raghubir R. 2010. Endoplasmic reticulum stress plays critical role in brain damage after cerebral ischemia/reperfusion in rats. Neurotox. Res. 17:189-202
65. SanMiguel JF, Schlag R, Khuageva NK, et al. 2008. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N. Engl. J. Med. 359:906-17
66. Nawrocki ST, Carew JS, Pino MS, et al. 2005. Bortezomib sensitizes pancreatic cancer cells to endoplasmic reticulum stress-mediated apoptosis. Cancer Res. 65:11658-66 (Pubitemid 41821726)