Endoplasmic reticulum stress and protein quality control in diabetic cardiomyopathy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 2, 2015, Pages 209-218

  Yang, Lifang ^a,b   Zhao, Dajun ^a   Ren, Jun ^b   Yang, Jian ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WYOMING   (United States)

Author keywords

Diabetic cardiomyopathy; Endoplasmic reticulum stress; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ENZYME; FATTY ACID; INOSITOL REQUIRING ENZYME 1; PROTEIN KINASE RNA LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; PROTEIN;

APOPTOSIS; AUTOPHAGY; DIABETIC CARDIOMYOPATHY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPERLIPIDEMIA; INFLAMMATION; INSULIN RESISTANCE; NONHUMAN; PATHOGENESIS; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PATHOLOGY;

ANIMALS; DIABETIC CARDIOMYOPATHIES; ENDOPLASMIC RETICULUM STRESS; HUMANS; MODELS, BIOLOGICAL; PROTEINS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84919789614     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.05.006     Document Type: Review

References (129)

1. Neugebauer R., Fireman B., Roy J.A., O'Connor P.J. Impact of specific glucose-control strategies on microvascular and macrovascular outcomes in 58,000 adults with type 2 diabetes. Diabetes Care 2013, 36:3510-3516.
2. Hiebert L., Han J., Mandal A.K. Glycosaminoglycans, hyperglycemia and disease. Antioxid. Redox Signal. 2014 Feb 4, [Epub ahead of print].
3. Roger V.L., Go A.S., Lloyd-Jones D.M., Adams R.J., Berry J.D., Brown T.M., Carnethon M.R., Dai S., de Simone G., Ford E.S., Fox C.S., Fullerton H.J., Gillespie C., Greenlund K.J., Hailpern S.M., Heit J.A., Ho P.M., Howard V.J., Kissela B.M., Kittner S.J., Lackland D.T., Lichtman J.H., Lisabeth L.D., Makuc D.M., Marcus G.M., Marelli A., Matchar D.B., McDermott M.M., Meigs J.B., Moy C.S., Mozaffarian D., Mussolino M.E., Nichol G., Paynter N.P., Rosamond W.D., Sorlie P.D., Stafford R.S., Turan T.N., Turner M.B., Wong N.D., Wylie-Rosett J., American Heart C. Association statistics, s. stroke statistics, heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 2011, 123:e18-e209.
4. Preis S.R., Pencina M.J., Hwang S.J., D'Agostino R.B., Savage P.J., Levy D., Fox C.S. Trends in cardiovascular disease risk factors in individuals with and without diabetes mellitus in the Framingham Heart Study. Circulation 2009, 120:212-220.
5. Rubler S., Dlugash J., Yuceoglu Y.Z., Kumral T., Branwood A.W., Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am. J. Cardiol. 1972, 30:595-602.
6. Miki T., Yuda S., Kouzu H., Miura T. Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail. Rev. 2013, 18:149-166.
7. Pereira L., Matthes J., Schuster I., Valdivia H.H., Herzig S., Richard S., Gomez A.M. Mechanisms of [Ca2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes 2006, 55:608-615.
8. Wold L.E., Ceylan-Isik A.F., Ren J. Oxidative stress and stress signaling: menace of diabetic cardiomyopathy. Acta Pharmacol. Sin. 2005, 26:908-917.
9. Huynh K., Kiriazis H., Du X.J., Love J.E., Gray S.P., Jandeleit-Dahm K.A., McMullen J.R., Ritchie R.H. Targeting the upregulation of reactive oxygen species subsequent to hyperglycemia prevents type 1 diabetic cardiomyopathy in mice. Free Radic. Biol. Med. 2013, 60:307-317.
10. Groenendyk J., Sreenivasaiah P.K., Kim do H., Agellon L.B., Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ. Res. 2010, 107:1185-1197.
11. Xu J., Zhou Q., Xu W., Cai L. Endoplasmic reticulum stress and diabetic cardiomyopathy. Exp. Diabetes Res. 2012, 2012:827971.
12. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
13. van Meer G., Voelker D.R., Feigenson G.W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9:112-124.
14. Meusser B., Hirsch C., Jarosch E., Sommer T. ERAD: the long road to destruction. Nat. Cell Biol. 2005, 7:766-772.
15. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999, 286:1882-1888.
16. Kozutsumi Y., Segal M., Normington K., Gething M.J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 1988, 332:462-464.
17. Schroder M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 2008, 65:862-894.
18. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
19. Trombetta E.S., Parodi A.J. Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 2003, 19:649-676.
20. Otero J.H., Lizak B., Hendershot L.M. Life and death of a BiP substrate. Semin. Cell Dev. Biol. 2010, 21:472-478.
21. Chevet E., Smirle J., Cameron P.H., Thomas D.Y., Bergeron J.J. Calnexin phosphorylation: linking cytoplasmic signalling to endoplasmic reticulum lumenal functions. Semin. Cell Dev. Biol. 2010, 21:486-490.
22. Michalak M., Groenendyk J., Szabo E., Gold L.I., Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 2009, 417:651-666.
23. Chapman D.C., Williams D.B. ER quality control in the biogenesis of MHC class I molecules. Semin. Cell Dev. Biol. 2010, 21:512-519.
24. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
25. Patil C., Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 2001, 13:349-355.
26. Bravo R., Parra V., Gatica D., Rodriguez A.E., Torrealba N., Paredes F., Wang Z.V., Zorzano A., Hill J.A., Jaimovich E., Quest A.F., Lavandero S. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int. Rev. Cell Mol. Biol. 2013, 301:215-290.
27. Tirasophon W., Welihinda A.A., Kaufman R.J. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 1998, 12:1812-1824.
28. Iwawaki T., Hosoda A., Okuda T., Kamigori Y., Nomura-Furuwatari C., Kimata Y., Tsuru A., Kohno K. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol. 2001, 3:158-164.
29. Ozcan U., Ozcan L., Yilmaz E., Duvel K., Sahin M., Manning B.D., Hotamisligil G.S. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell 2008, 29:541-551.
30. Mao T., Shao M., Qiu Y., Huang J., Zhang Y., Song B., Wang Q., Jiang L., Liu Y., Han J.D., Cao P., Li J., Gao X., Rui L., Qi L., Li W., Liu Y. PKA phosphorylation couples hepatic inositol-requiring enzyme 1alpha to glucagon signaling in glucose metabolism. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:15852-15857.
31. Pfaffenbach K.T., Nivala A.M., Reese L., Ellis F., Wang D., Wei Y., Pagliassotti M.J. Rapamycin inhibits postprandial-mediated X-box-binding protein-1 splicing in rat liver. J. Nutr. 2010, 140:879-884.
32. Kato H., Nakajima S., Saito Y., Takahashi S., Katoh R., Kitamura M. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death Differ. 2012, 19:310-320.
33. Park S.W., Zhou Y., Lee J., Lu A., Sun C., Chung J., Ueki K., Ozcan U. The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation. Nat. Med. 2010, 16:429-437.
34. Shi Y., Vattem K.M., Sood R., An J., Liang J., Stramm L., Wek R.C. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 1998, 18:7499-7509.
35. 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.
36. Eizirik D.L., Cardozo A.K., Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 2008, 29:42-61.
37. Lu P.D., Jousse C., Marciniak S.J., Zhang Y., Novoa I., Scheuner D., Kaufman R.J., Ron D., Harding H.P. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 2004, 23:169-179.
38. Wek R.C., Cavener D.R. Translational control and the unfolded protein response. Antioxid. Redox Signal. 2007, 9:2357-2371.
39. Cullinan S.B., Zhang D., Hannink M., Arvisais E., Kaufman R.J., Diehl J.A. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 2003, 23:7198-7209.
40. Rouschop K.M., van den Beucken T., Dubois L., Niessen H., Bussink J., Savelkouls K., Keulers T., Mujcic H., Landuyt W., Voncken J.W., Lambin P., van der Kogel A.J., Koritzinsky M., Wouters B.G. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J. Clin. Invest. 2010, 120:127-141.
41. Rzymski T., Milani M., Pike L., Buffa F., Mellor H.R., Winchester L., Pires I., Hammond E., Ragoussis I., Harris A.L. Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 2010, 29:4424-4435.
42. 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.
43. Breckenridge D.G., Germain M., Mathai J.P., Nguyen M., Shore G.C. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22:8608-8618.
44. Shen J., Prywes R. Dependence of site-2 protease cleavage of ATF6 on prior site-1 protease digestion is determined by the size of the luminal domain of ATF6. J. Biol. Chem. 2004, 279:43046-43051.
45. 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.
46. Bommiasamy H., Back S.H., Fagone P., Lee K., Meshinchi S., Vink E., Sriburi R., Frank M., Jackowski S., Kaufman R.J., Brewer J.W. ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J. Cell Sci. 2009, 122:1626-1636.
47. Liang G., Audas T.E., Li Y., Cockram G.P., Dean J.D., Martyn A.C., Kokame K., Lu R. Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein Herp through an ER stress response element. Mol. Cell. Biol. 2006, 26:7999-8010.
48. Cnop M., Foufelle F., Velloso L.A. Endoplasmic reticulum stress, obesity and diabetes. Trends Mol. Med. 2012, 18:59-68.
49. Morton G.J., Cummings D.E., Baskin D.G., Barsh G.S., Schwartz M.W. Central nervous system control of food intake and body weight. Nature 2006, 443:289-295.
50. Milanski M., Degasperi G., Coope A., Morari J., Denis R., Cintra D.E., Tsukumo D.M., Anhe G., Amaral M.E., Takahashi H.K., Curi R., Oliveira H.C., Carvalheira J.B., Bordin S., Saad M.J., Velloso L.A. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J. Neurosci. 2009, 29:359-370.
51. Coope A., Milanski M., Arruda A.P., Ignacio-Souza L.M., Saad M.J., Anhe G.F., Velloso L.A. Chaperone insufficiency links TLR4 protein signaling to endoplasmic reticulum stress. J. Biol. Chem. 2012, 287:15580-15589.
52. Denis R.G., Arruda A.P., Romanatto T., Milanski M., Coope A., Solon C., Razolli D.S., Velloso L.A. TNF-alpha transiently induces endoplasmic reticulum stress and an incomplete unfolded protein response in the hypothalamus. Neuroscience 2010, 170:1035-1044.
53. Cretenet G., Le Clech M., Gachon F. Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab. 2010, 11:47-57.
54. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., Tuncman G., Gorgun C., Glimcher L.H., Hotamisligil G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461.
55. Puri P., Mirshahi F., Cheung O., Natarajan R., Maher J.W., Kellum J.M., Sanyal A.J. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 2008, 134:568-576.
56. Xu L., Spinas G.A., Niessen M. ER stress in adipocytes inhibits insulin signaling, represses lipolysis, and alters the secretion of adipokines without inhibiting glucose transport. Horm. Metab. Res. 2010, 42:643-651.
57. Vendrell J., Maymo-Masip E., Tinahones F., Garcia-Espana A., Megia A., Caubet E., Garcia-Fuentes E., Chacon M.R. Tumor necrosis-like weak inducer of apoptosis as a proinflammatory cytokine in human adipocyte cells: up-regulation in severe obesity is mediated by inflammation but not hypoxia. J. Clin. Endocrinol. Metab. 2010, 95:2983-2992.
58. Liu M., Zhou L., Xu A., Lam K.S., Wetzel M.D., Xiang R., Zhang J., Xin X., Dong L.Q., Liu F. A disulfide-bond A oxidoreductase-like protein (DsbA-L) regulates adiponectin multimerization. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18302-18307.
59. Zhou L., Liu M., Zhang J., Chen H., Dong L.Q., Liu F. DsbA-L alleviates endoplasmic reticulum stress-induced adiponectin downregulation. Diabetes 2010, 59:2809-2816.
60. Lefterova M.I., Mullican S.E., Tomaru T., Qatanani M., Schupp M., Lazar M.A. Endoplasmic reticulum stress regulates adipocyte resistin expression. Diabetes 2009, 58:1879-1886.
61. Deldicque L., Cani P.D., Philp A., Raymackers J.M., Meakin P.J., Ashford M.L., Delzenne N.M., Francaux M., Baar K. The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the downregulation of protein synthesis. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E695-E705.
62. Colombo C., Porzio O., Liu M., Massa O., Vasta M., Salardi S., Beccaria L., Monciotti C., Toni S., Pedersen O., Hansen T., Federici L., Pesavento R., Cadario F., Federici G., Ghirri P., Arvan P., Iafusco D., Barbetti F. Seven mutations in the human insulin gene linked to permanent neonatal/infancy-onset diabetes mellitus. J. Clin. Invest. 2008, 118:2148-2156.
63. 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., Lipton R.B., Greeley S.A., Patch A.M., Ellard S., Steiner D.F., Hattersley A.T., Philipson L.H., Bell G.I. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:15040-15044.
64. Yin J.J., Li Y.B., Wang Y., Liu G.D., Wang J., Zhu X.O., Pan S.H. The role of autophagy in endoplasmic reticulum stress-induced pancreatic beta cell death. Autophagy 2012, 8:158-164.
65. Dickhout J.G., Carlisle R.E., Austin R.C. Interrelationship between cardiac hypertrophy, heart failure, and chronic kidney disease: endoplasmic reticulum stress as a mediator of pathogenesis. Circ. Res. 2011, 108:629-642.
66. Sari F.R., Widyantoro B., Thandavarayan R.A., Harima M., Lakshmanan A.P., Zhang S., Muslin A.J., Suzuki K., Kodama M., Watanabe K. Attenuation of CHOP-mediated myocardial apoptosis in pressure-overloaded dominant negative p38alpha mitogen-activated protein kinase mice. Cell. Physiol. Biochem. 2011, 27:487-496.
67. Mao W., Fukuoka S., Iwai C., Liu J., Sharma V.K., Sheu S.S., Fu M., Liang C.S. Cardiomyocyte apoptosis in autoimmune cardiomyopathy: mediated via endoplasmic reticulum stress and exaggerated by norepinephrine. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H1636-H1645.
68. Minamino T., Komuro I., Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ. Res. 2010, 107:1071-1082.
69. Hamada H., Suzuki M., Yuasa S., Mimura N., Shinozuka N., Takada Y., Suzuki M., Nishino T., Nakaya H., Koseki H., Aoe T. Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice. Mol. Cell. Biol. 2004, 24:8007-8017.
70. Toko H., Takahashi H., Kayama Y., Okada S., Minamino T., Terasaki F., Kitaura Y., Komuro I. ATF6 is important under both pathological and physiological states in the heart. J. Mol. Cell. Cardiol. 2010, 49:113-120.
71. Dally S., Monceau V., Corvazier E., Bredoux R., Raies A., Bobe R., del Monte F., Enouf J. Compartmentalized expression of three novel sarco/endoplasmic reticulum Ca2+ATPase 3 isoforms including the switch to ER stress, SERCA3f, in non-failing and failing human heart. Cell Calcium 2009, 45:144-154.
72. Okada K., Minamino T., Tsukamoto Y., Liao Y., Tsukamoto O., Takashima S., Hirata A., Fujita M., Nagamachi Y., Nakatani T., Yutani C., Ozawa K., Ogawa S., Tomoike H., Hori M., Kitakaze M. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 2004, 110:705-712.
73. Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ. Res. 2010, 107:839-850.
74. Lakshmanan A.P., Harima M., Suzuki K., Soetikno V., Nagata M., Nakamura T., Takahashi T., Sone H., Kawachi H., Watanabe K. The hyperglycemia stimulated myocardial endoplasmic reticulum (ER) stress contributes to diabetic cardiomyopathy in the transgenic non-obese type 2 diabetic rats: a differential role of unfolded protein response (UPR) signaling proteins. Int. J. Biochem. Cell Biol. 2013, 45:438-447.
75. 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.
76. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
77. Buchanan J., Mazumder P.K., Hu P., Chakrabarti G., Roberts M.W., Yun U.J., Cooksey R.C., Litwin S.E., Abel E.D. Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology 2005, 146:5341-5349.
78. Li Y., Ge M., Ciani L., Kuriakose G., Westover E.J., Dura M., Covey D.F., Freed J.H., Maxfield F.R., Lytton J., Tabas I. Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages. J. Biol. Chem. 2004, 279:37030-37039.
79. Boslem E., MacIntosh G., Preston A.M., Bartley C., Busch A.K., Fuller M., Laybutt D.R., Meikle P.J., Biden T.J. A lipidomic screen of palmitate-treated MIN6 beta-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem. J. 2011, 435:267-276.
80. Pulinilkunnil T., Kienesberger P.C., Nagendran J., Waller T.J., Young M.E., Kershaw E.E., Korbutt G., Haemmerle G., Zechner R., Dyck J.R. Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes 2013, 62:1464-1477.
81. Hohensinner P.J., Niessner A., Huber K., Weyand C.M., Wojta J. Inflammation and cardiac outcome. Curr. Opin. Infect. Dis. 2011, 24:259-264.
82. Linde A., Mosier D., Blecha F., Melgarejo T. Innate immunity and inflammation-new frontiers in comparative cardiovascular pathology. Cardiovasc. Res. 2007, 73:26-36.
83. Niu J., Azfer A., Kolattukudy P.E. Protection against lipopolysaccharide-induced myocardial dysfunction in mice by cardiac-specific expression of soluble Fas. J. Mol. Cell. Cardiol. 2008, 44:160-169.
84. de Lemos J.A., Morrow D.A., Sabatine M.S., Murphy S.A., Gibson C.M., Antman E.M., McCabe C.H., Cannon C.P., Braunwald E. Association between plasma levels of monocyte chemoattractant protein-1 and long-term clinical outcomes in patients with acute coronary syndromes. Circulation 2003, 107:690-695.
85. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454:455-462.
86. Gotoh T., Endo M., Oike Y. Endoplasmic reticulum stress-related inflammation and cardiovascular diseases. Int. J. Inflamm. 2011, 2011:259462.
87. Younce C.W., Wang K., Kolattukudy P.E. Hyperglycaemia-induced cardiomyocyte death is mediated via MCP-1 production and induction of a novel zinc-finger protein MCPIP. Cardiovasc. Res. 2010, 87:665-674.
88. Martinon F., Chen X., Lee A.H., Glimcher L.H. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 2010, 11:411-418.
89. Kolattukudy P.E., Niu J. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway. Circ. Res. 2012, 110:174-189.
90. Martindale J.J., Fernandez R., Thuerauf D., Whittaker R., Gude N., Sussman M.A., Glembotski C.C. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ. Res. 2006, 98:1186-1193.
91. Tian F., Zhou X., Wikstrom J., Karlsson H., Sjoland H., Gan L.M., Boren J., Akyurek L.M. Protein disulfide isomerase increases in myocardial endothelial cells in mice exposed to chronic hypoxia: a stimulatory role in angiogenesis. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1078-H1086.
92. De Meyer G.R., Martinet W. Autophagy in the cardiovascular system. Biochim. Biophys. Acta 2009, 1793:1485-1495.
93. Takagi H., Matsui Y., Sadoshima J. The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid. Redox Signal. 2007, 9:1373-1381.
94. Hoyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., Bianchi K., Fehrenbacher N., Elling F., Rizzuto R., Mathiasen I.S., Jaattela M. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 2007, 25:193-205.
95. Hara T., Mizushima N. Role of ULK-FIP200 complex in mammalian autophagy: FIP200, a counterpart of yeast Atg17?. Autophagy 2009, 5:85-87.
96. Chang Y.Y., Neufeld T.P. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol. Biol. Cell 2009, 20:2004-2014.
97. Jung C.H., Jun C.B., Ro S.H., Kim Y.M., Otto N.M., Cao J., Kundu M., Kim D.H. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 2009, 20:1992-2003.
98. Wei Y., Sinha S., Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 2008, 4:949-951.
99. Pattingre S., Bauvy C., Carpentier S., Levade T., Levine B., Codogno P. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem. 2009, 284:2719-2728.
100. Kouroku Y., Fujita E., Tanida I., Ueno T., Isoai A., Kumagai H., Ogawa S., Kaufman R.J., Kominami E., Momoi T. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007, 14:230-239.
101. Zhang B., Zhang Y., La Cour K.H., Richmond K.L., Wang X.M., Ren J. Mitochondrial aldehyde dehydrogenase obliterates endoplasmic reticulum stress-induced cardiac contractile dysfunction via correction of autophagy. Biochim. Biophys. Acta 2013, 1832:574-584.
102. Yang L., Hu N., Jiang S., Zou Y., Yang J., Xiong L., Ren J. Heavy metal scavenger metallothionein attenuates ER stress-induced myocardial contractile anomalies: role of autophagy. Toxicol. Lett. 2014, 225:333-341.
103. Appenzeller-Herzog C., Hall M.N. Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol. 2012, 22:274-282.
104. 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.
105. Thuerauf D.J., Marcinko M., Gude N., Rubio M., Sussman M.A., Glembotski C.C. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ. Res. 2006, 99:275-282.
106. Hetz C., Bernasconi P., Fisher J., Lee A.H., Bassik M.C., Antonsson B., Brandt G.S., Iwakoshi N.N., Schinzel A., Glimcher L.H., Korsmeyer S.J. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006, 312:572-576.
107. 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.
108. Lei K., Davis R.J. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2432-2437.
109. Yamamoto K., Ichijo H., Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 1999, 19:8469-8478.
110. Yamaguchi H., Wang H.G. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J. Biol. Chem. 2004, 279:45495-45502.
111. Ohoka N., Yoshii S., Hattori T., Onozaki K., Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005, 24:1243-1255.
112. 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.
113. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., Hughes P.D., Michalak E.M., McKimm-Breschkin J., Motoyama N., Gotoh T., Akira S., Bouillet P., Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
114. 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.
115. Dorn G.W., Maack C. SR and mitochondria: calcium cross-talk between kissing cousins. J. Mol. Cell. Cardiol. 2013, 55:42-49.
116. Kranstuber A.L., Del Rio C., Biesiadecki B.J., Hamlin R.L., Ottobre J., Gyorke S., Lacombe V.A. Advanced glycation end product cross-link breaker attenuates diabetes-induced cardiac dysfunction by improving sarcoplasmic reticulum calcium handling. Front. Physiol. 2012, 3:292.
117. Lu F.H., Fu S.B., Leng X., Zhang X., Dong S., Zhao Y.J., Ren H., Li H., Zhong X., Xu C.Q., Zhang W.H. Role of the calcium-sensing receptor in cardiomyocyte apoptosis via the sarcoplasmic reticulum and mitochondrial death pathway in cardiac hypertrophy and heart failure. Cell. Physiol. Biochem. 2013, 31:728-743.
118. Younce C.W., Burmeister M.A., Ayala J.E. Exendin-4 attenuates high glucose-induced cardiomyocyte apoptosis via inhibition of endoplasmic reticulum stress and activation of SERCA2a. Am. J. Physiol. Cell Physiol. 2013, 304:C508-C518.
119. Gray S., Kim J.K. New insights into insulin resistance in the diabetic heart. Trends Endocrinol. Metab. 2011, 22:394-403.
120. Flamment M., Hajduch E., Ferre P., Foufelle F. New insights into ER stress-induced insulin resistance. Trends Endocrinol. Metab. 2012, 23:381-390.
121. Saltiel A.R., Pessin J.E. Insulin signaling pathways in time and space. Trends Cell Biol. 2002, 12:65-71.
122. Hirosumi J., Tuncman G., Chang L., Gorgun C.Z., Uysal K.T., Maeda K., Karin M., Hotamisligil G.S. A central role for JNK in obesity and insulin resistance. Nature 2002, 420:333-336.
123. Weston C.R., Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 2007, 19:142-149.
124. Hu P., Han Z., Couvillon A.D., Kaufman R.J., Exton J.H. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol. Cell. Biol. 2006, 26:3071-3084.
125. Dong F., Ren J. Adiponectin improves cardiomyocyte contractile function in db/dB diabetic obese mice. Obesity (Silver Spring) 2009, 17:262-268.
126. Rieusset J., Chauvin M.A., Durand A., Bravard A., Laugerette F., Michalski M.C., Vidal H. Reduction of endoplasmic reticulum stress using chemical chaperones or Grp78 overexpression does not protect muscle cells from palmitate-induced insulin resistance. Biochem. Biophys. Res. Commun. 2012, 417:439-445.
127. Peng G., Li L., Liu Y., Pu J., Zhang S., Yu J., Zhao J., Liu P. Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 2011, 152:2206-2218.
128. Hwang S.L., Li X., Lee J.Y., Chang H.W. Improved insulin sensitivity by rapamycin is associated with reduction of mTOR and S6K1 activities in L6 myotubes. Biochem. Biophys. Res. Commun. 2012, 418:402-407.
129. Kaufman R.J., Scheuner D., Schroder M., Shen X., Lee K., Liu C.Y., Arnold S.M. The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell Biol. 2002, 3:411-421.