Endoplasmic reticulum stress in cardiometabolic disorders

Current Atherosclerosis Reports

Volumn 14, Issue 5, 2012, Pages 469-475

  Ozcan, Lale ^a  

^a Columbia University ^*  (United States)

Author keywords

Atherosclerosis; Diabetes; ER Stress; NAFLD; Obesity; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; APOPTOSIS SIGNAL REGULATING KINASE 1; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; PROTEIN IRE1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT1 PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NRF2; X BOX BINDING PROTEIN 1;

ATHEROGENESIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CELL ACTIVATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; INSULIN RESISTANCE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; OBESITY; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CARDIOVASCULAR DISEASES; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84870484663     PISSN: 15233804     EISSN: 15346242     Source Type: Journal    
DOI: 10.1007/s11883-012-0270-z     Document Type: Review

References (65)

1. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA: J Am Med Assoc. 2010;303(3):242-9. Epub 2010/01/15.
2. Ozcan L, Tabas I. Role of endoplasmic reticulum stress in metabolic disease and other disorders. Ann Rev Med. 2012;63:317-28. Epub 2012/01/18.
3. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010;140(6):900-17. Epub 2010/03/23.
4. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334(6059):1081-6. Epub 2011/11/26.
5. Hetz C, Martinon F, Rodriguez D, Glimcher LH. The unfolded protein response: integrating stress signals through the stress sensor IRE1alpha. Physiol Rev. 2011;91(4):1219-43. Epub 2011/10/21.
6. Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol. 2007;18(6):716-31. Epub 2007/11/21.
7. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8(7):519-29. Epub 2007/06/15.
8. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol. 2004;14(1):20-8. Epub 2004/01/20.
9. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol. 2001;21(4):1249-59. Epub 2001/02/07.
10. 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(5):1011-22. Epub 2001/05/31.
11. Li G, Mongillo M, Chin KT, Harding H, Ron D, Marks AR, et al. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stressinduced apoptosis. J Cell Biol. 2009;186(6):783-92. Epub 2009/09/16.
12. Timmins JM, Ozcan L, Seimon TA, Li G, Malagelada C, Backs J, et al. Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways. J Clin Invest. 2009;119(10):2925-41. Epub 2009/09/11.
13. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. Nrf2 is a direct PERK substrate and effector of PERKdependent cell survival. Mol Cell Biol. 2003;23(20):7198-209. Epub 2003/10/01.
14. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, et al. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol. 2003;23 (16):5651-63. Epub 2003/08/05.
15. Glimcher LH. XBP1: the last two decades. Ann Rheum Dis. 2010;69 Suppl 1:i67-71. Epub 2010/01/09.
16. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. 2006;313 (5783):104-7. Epub 2006/07/11.
17. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287(5453):664-6. Epub 2000/01/29.
18. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403(6765):98-103. Epub 2000/01/19.
19. 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 (15):13045-52. Epub 2002/02/01.
20. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145(3):341-55. Epub 2011/05/03.
21. Tabas I. Pulling down the plug on atherosclerosis: finding the culprit in your heart. Nature Med. 2011;17(7):791-3. Epub 2011/07/09.
22. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10(1):36-46. Epub 2009/12/05.
23. Thorp E, Iwawaki T, Miura M, Tabas I. A reporter for tracking the UPR in vivo reveals patterns of temporal and cellular stress during atherosclerotic progression. J Lipid Res. 2011;52(5):1033-8. Epub 2011/03/02.
24. Thorp E, Li G, Seimon TA, Kuriakose G, Ron D, Tabas I. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab. 2009;9(5):474-81. Epub 2009/05/07.
25. Tsukano H, Gotoh T, Endo M, Miyata K, Tazume H, Kadomatsu T, et al. The endoplasmic reticulum stress-C/EBP homologous protein pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2010;30(10):1925-32. Epub 2010/07/24.
26. Myoishi M, Hao H, Minamino T, Watanabe K, Nishihira K, Hatakeyama K, et al. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation. 2007;116(11):1226-33. Epub 2007/08/22.
27. Dickhout JG, Lhotak S, Hilditch BA, Basseri S, Colgan SM, Lynn EG, et al. Induction of the unfolded protein response after monocyte to macrophage differentiation augments cell survival in early atherosclerotic lesions. FASEB J: Off Publ Fed Am Soc Exp Biol. 2011;25(2):576-89. Epub 2010/10/23.
28. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ. 2005;12 Suppl 2:1542-52. Epub 2005/10/26.
29. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, et al. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab. 2012;15(4):545-53. Epub 2012/03/27.
30. Civelek M, Manduchi E, Riley RJ, Stoeckert Jr CJ, Davies PF. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circ Res. 2009;105(5):453-61. Epub 2009/08/08.
31. Matsushita E, Asai N, Enomoto A, Kawamoto Y, Kato T, Mii S, et al. Protective role of Gipie, a Girdin family protein, in endoplasmic reticulum stress responses in endothelial cells. Mol Biol Cell. 2011;22(6):736-47. Epub 2011/02/04.
32. Zeng L, Zampetaki A, Margariti A, Pepe AE, Alam S, Martin D, et al. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc Natl Acad Sci U S A. 2009;106(20):8326-31. Epub 2009/05/07.
33. Sanson M, Auge N, Vindis C, Muller C, Bando Y, Thiers JC, et al. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circ Res. 2009;104(3):328-36. Epub 2008/12/25.
34. Gao J, Ishigaki Y, Yamada T, Kondo K, Yamaguchi S, Imai J, et al. Involvement of endoplasmic stress protein C/EBP homologous protein in arteriosclerosis acceleration with augmented biological stress responses. Circulation. 2011;124(7):830-9. Epub 2011/08/04.
35. Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res. 2010;107(7):839-50. Epub 2010/10/05.
36. Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, Prunet C, et al. NAD[P]H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol. 2004;24(24):10703-17. Epub 2004/12/02.
37. Fu S, Yang L, Li P, Hofmann O, Dicker L, Hide W, et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature. 2011;473(7348):528-31. Epub 2011/05/03.
38. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306(5695):457-61. Epub 2004/10/16.
39. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, Nie D, et al. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 2009;9(1):35-51. Epub 2009/01/02.
40. Boden G, Duan X, Homko C, Molina EJ, Song W, Perez O, et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes. 2008;57(9):2438-44. Epub 2008/06/24.
41. Gregor MF, Yang L, Fabbrini E, Mohammed BS, Eagon JC, Hotamisligil GS, et al. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes. 2009;58 (3):693-700. Epub 2008/12/11.
42. Boden G, Merali S. Measurement of the increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Methods Enzymol. 2011;489:67-82. Epub 2011/01/27.
43. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T, et al. GRP78 expression inhibits insulin and ER stressinduced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest. 2009;119(5):1201-15. Epub 2009/04/14.
44. Zhou Y, Lee J, Reno CM, Sun C, Park SW, Chung J, et al. Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction. Nature Med. 2011;17(3):356-65. Epub 2011/02/15.
45. Oyadomari S, Harding HP, Zhang Y, Oyadomari M, Ron D. Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab. 2008;7(6):520-32. Epub 2008/06/05.
46. Birkenfeld AL, Lee HY, Majumdar S, Jurczak MJ, Camporez JP, Jornayvaz FR, et al. Influence of the hepatic eukaryotic initiation factor 2alpha [eIF2alpha] endoplasmic reticulum [ER] stress response pathway on insulin-mediated ER stress and hepatic and peripheral glucose metabolism. J Biol Chem. 2011;286(42):36163-70. Epub 2011/08/13.
47. Wang Y, Vera L, Fischer WH, Montminy M. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature. 2009;460(7254):534-7. Epub 2009/06/23.
48. Kimura K, Yamada T, Matsumoto M, Kido Y, Hosooka T, Asahara S, et al. Endoplasmic reticulum stress inhibits STAT3-dependent suppression of hepatic gluconeogenesis via dephosphorylation and deacetylation. Diabetes. 2012;61(1):61-73. Epub 2011/11/30.
49. 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(4):406-9. Epub 2011/11/30.
50. Lee AH, Heidtman K, Hotamisligil GS, Glimcher LH. Dual and opposing roles of the unfolded protein response regulated by IRE1-alpha and XBP1 in proinsulin processing and insulin secretion. Proc Natl Acad Sci U S A. 2011;108(21):8885-90. Epub 2011/05/11.
51. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, et al. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia. 2007;50(4):752-63. Epub 2007/02/03.
52. 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(10):3378-89. Epub 2008/09/09.
53. Back SH, Scheuner D, Han J, Song B, Ribick M, Wang J, et al. Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab. 2009;10(1):13-26. Epub 2009/07/09.
54. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell. 2012;148(5):852-71. Epub 2012/03/06.
55. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science. 2008;320(5882):1492-6. Epub 2008/06/17.
56. Rutkowski DT, Wu J, Back SH, Callaghan MU, Ferris SP, Iqbal J, et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell. 2008;15(6):829-40. Epub 2008/12/17.
57. Ota T, Gayet C, Ginsberg HN. Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents. J Clin Invest. 2008;118(1):316-32. Epub 2007/12/07.
58. Qiu W, Su Q, Rutledge AC, Zhang J, Adeli K. Glucosamine-induced endoplasmic reticulum stress attenuates apolipoprotein B100 synthesis via PERK signaling. J Lipid Res. 2009;50(9):1814-23. Epub 2009/04/23.
59. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006;313(5790):1137-40. Epub 2006/08/26.
60. Erbay E, Babaev VR, Mayers JR, Makowski L, Charles KN, Snitow ME, et al. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nature Med. 2009;15(12):1383-91. Epub 2009/12/08.
61. Xiao C, Giacca A, Lewis GF. Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and beta-cell dysfunction in humans. Diabetes. 2011;60(3):918-24. Epub 2011/01/29.
62. Kars M, Yang L, Gregor MF, Mohammed BS, Pietka TA, Finck BN, et al. Tauroursodeoxycholic Acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes. 2010;59(8):1899-905. Epub 2010/06/05.
63. Breder I, Coope A, Arruda AP, Razolli D, Milanski M, Dorighello Gde G, et al. Reduction of endoplasmic reticulum stress - a novel mechanism of action of statins in the protection against atherosclerosis. Atherosclerosis. 2010;212(1):30-1. Epub 2010/06/12.
64. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM, et al. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res Treat. 2000;59(1):15-26. Epub 2000/04/07.
65. Lee AS. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res. 2007;67(8):3496-9. Epub 2007/04/19.