C/EBP homologous protein deficiency attenuates myocardial reperfusion injury by inhibiting myocardial apoptosis and inflammation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 5, 2011, Pages 1124-1132

  Miyazaki, Yuji ^a   Kaikita, Koichi ^a   Endo, Motoyoshi ^a   Horio, Eiji ^a   Miura, Mitsutoshi ^a   Tsujita, Kenichi ^a   Hokimoto, Seiji ^a   Yamamuro, Megumi ^a   Iwawaki, Takao ^b   Gotoh, Tomomi ^a   Ogawa, Hisao ^a   Oike, Yuichi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b Japan Science and Technology Agency   (Japan)

Author keywords

CHOP; ER stress; ischemic heart disease; reactive oxygen species; reperfusion injury

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NORPHENAZONE; SUPEROXIDE; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA; X BOX BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CCAAT ENHANCER BINDING PROTEIN DEFICIENCY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; INFLAMMATORY INFILTRATE; LEFT CORONARY ARTERY; MALE; MOUSE; MYOCARDITIS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REPERFUSION INJURY; RNA SPLICING; WILD TYPE;

ANIMALS; ANTIPYRINE; APOPTOSIS; CELLS, CULTURED; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; RNA SPLICING; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; SUPEROXIDES; THAPSIGARGIN; TIME FACTORS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

EID: 79955597257     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.224519     Document Type: Article

References (42)

1. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature. 2008;454:455-462.
2. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest. 2005;115:2656-2664. (Pubitemid 41434389)
3. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11:381-389. (Pubitemid 38489416)
4. Myoishi M, Hao H, Minamino T, Watanabe K, Nishihira K, Hatakeyama K, Asada Y, Okada K, Ishibashi-Ueda H, Gabbiani G, Bochaton-Piallat ML, Mochizuki N, Kitakaze M. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation. 2007;116:1226-1233. (Pubitemid 47517533)
5. Fu HY, Okada K, Liao Y, Tsukamoto O, Isomura T, Asai M, Sawada T, Okuda K, Asano Y, Sanada S, Asanuma H, Asakura M, Takashima S, Komuro I, Kitakaze M, Minamino T. Ablation of C/EBP homologous protein attenuates endoplasmic reticulum-mediated apoptosis and cardiac dysfunction induced by pressure overload. Circulation. 2010;122: 361-369.
6. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135.
7. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal. 2007;9:2277-2293. (Pubitemid 350059010)
8. Verkhratsky A, Petersen OH. The endoplasmic reticulum as an integrating signalling organelle: from neuronal signalling to neuronal death. Eur J Pharmacol. 2002;447:141-154. (Pubitemid 34874448)
9. Martindale JJ, Fernandez R, Thuerauf D, Whittaker R, Gude N, Sussman MA, Glembotski CC. 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. (Pubitemid 43948105)
10. Natarajan R, Salloum FN, Fisher BJ, Smithson L, Almenara J, Fowler AA, III. Prolyl hydroxylase inhibition attenuates post-ischemic cardiac injury via induction of endoplasmic reticulum stress genes. Vascul Pharmacol. 2009;51:110-118.
11. Qi X, Vallentin A, Churchill E, Mochly-Rosen D. δPKC participates in the endoplasmic reticulum stress-induced response in cultured cardiac myocytes and ischemic heart. J Mol Cell Cardiol. 2007;43:420-428. (Pubitemid 47451430)
12. Zhang GG, Teng X, Liu Y, Cai Y, Zhou YB, Duan XH, Song JQ, Shi Y, Tang CS, Yin XH, Qi YF. Inhibition of endoplasm reticulum stress by ghrelin protects against ischemia/reperfusion injury in rat heart. Peptides. 2009;30:1109-1116.
13. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M. Nitric oxide-induced apoptosis in pancreatic cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA. 2001;98:10845-10850. (Pubitemid 32878707)
14. Geoghegan-Morphet N, Burger D, Lu X, Sathish V, Peng T, Sims SM, Feng Q. Role of neuronal nitric oxide synthase in lipopolysaccharideinduced tumor necrosis factor expression in neonatal mouse cardiomyocytes. Cardiovasc Res. 2007;75:408-416. (Pubitemid 46961921)
15. 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. (Pubitemid 34084979)
16. Nakagawa O, Ogawa Y, Itoh H, Suga S, Komatsu Y, Kishimoto I, Nishino K, Yoshimasa T, Nakao K. Rapid transcriptional activation and early mRNA turnover of brain natriuretic peptide in cardiocyte hypertrophy. Evidence for brain natriuretic peptide as an "emergency" cardiac hormone against ventricular overload. J Clin Invest. 1995;96:1280-1287.
17. 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;21:1249-1259. (Pubitemid 32114973)
18. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 1993;74:609-619. (Pubitemid 23259742)
19. Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol. 2001;2:63-67. (Pubitemid 33676963)
20. Li Y, Schwabe RF, DeVries-Seimon T, Yao PM, Gerbod-Giannone MC, Tall AR, Davis RJ, Flavell R, Brenner DA, Tabas I. Free cholesterolloaded macrophages are an abundant source of tumor necrosis factor and interleukin-6: model of NF-B-and map kinase-dependent inflammation in advanced atherosclerosis. J Biol Chem. 2005;280: 21763-21772. (Pubitemid 40827824)
21. Endo M, Mori M, Akira S, Gotoh T. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J Immunol. 2006;176: 6245-6253.
22. Namba T, Tanaka K, Ito Y, Ishihara T, Hoshino T, Gotoh T, Endo M, Sato K, Mizushima T. Positive role of CCAAT/enhancer-binding protein homologous protein, a transcription factor involved in the endoplasmic reticulum stress response in the development of colitis. Am J Pathol. 2009;174:1786-1798.
23. Zweier JL. Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem. 1988;263:1353-1357. (Pubitemid 18039938)
24. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev. 2008;88:581-609. (Pubitemid 351520088)
25. Ermak G, Davies KJ. Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol. 2002;38:713-721. (Pubitemid 34158874)
26. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal. 2006;8:1391-1418. (Pubitemid 44726319)
27. van der Vlies D, Makkinje M, Jansens A, Braakman I, Verkleij AJ, Wirtz KW, Post JA. Oxidation of ER resident proteins upon oxidative stress: effects of altering cellular redox/antioxidant status and implications for protein maturation. Antioxid Redox Signal. 2003;5:381-387. (Pubitemid 37087397)
28. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Nishi T, Maier CM, Kinouchi H, Chan PH. Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J Cereb Blood Flow Metab. 2003;23:1117-1128. (Pubitemid 37229515)
29. Edaravone Acute Infarction Study Group. Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction: randomized, placebo-controlled, double-blind study at multicenters. Cerebrovasc Dis. 2003;15:222-229.
30. Terai K, Hiramoto Y, Masaki M, Sugiyama S, Kuroda T, Hori M, Kawase I, Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol Cell Biol. 2005;25:9554-9575. (Pubitemid 41507855)
31. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest. 1994;94:1621-1628. (Pubitemid 24309885)
32. Saraste A, Pulkki K, Kallajoki M, Henriksen K, Parvinen M, Voipio-Pulkki LM. Apoptosis in human acute myocardial infarction. Circulation. 1997;95:320-323. (Pubitemid 27056193)
33. Freude B, Masters TN, Robicsek F, Fokin A, Kostin S, Zimmermann R, Ullmann C, Lorenz-Meyer S, Schaper J. Apoptosis is initiated by myocardial ischemia and executed during reperfusion. J Mol Cell Cardiol. 2000;32:197-208. (Pubitemid 30670343)
34. Kaiser RA, Liang Q, Bueno O, Huang Y, Lackey T, Klevitsky R, Hewett TE, Molkentin JD. Genetic inhibition or activation of JNK1/2 protects the myocardium from ischemia-reperfusion-induced cell death in vivo. J Biol Chem. 2005;280:32602-32608. (Pubitemid 41368302)
35. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, 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. (Pubitemid 46962086)
36. Gotoh T, Terada K, Oyadomari S, Mori M. hsp70-DnaJ chaperone pair prevents nitric oxide-and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ. 2004;11:390-402. (Pubitemid 38489417)
37. Goodall JC, Wu C, Zhang Y, McNeill L, Ellis L, Saudek V, Gaston JS. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc Natl Acad Sci USA. 2010;107:17698-17703.
38. Hattori T, Ohoka N, Hayashi H, Onozaki K. C/EBP homologous protein (CHOP) up-regulates IL-6 transcription by trapping negative regulating NF-IL6 isoform. FEBS Lett. 2003;541:33-39. (Pubitemid 36428913)
39. Prasad A, Stone GW, Holmes DR, Gersh B. Reperfusion injury, microvascular dysfunction, and cardioprotection: the "dark side" of reperfusion. Circulation. 2009;120:2105-2112.
40. Tsujita K, Shimomura H, Kawano H, Hokamaki J, Fukuda M, Yamashita T, Hida S, Nakamura Y, Nagayoshi Y, Sakamoto T, Yoshimura M, Arai H, Ogawa H. Effects of edaravone on reperfusion injury in patients with acute myocardial infarction. Am J Cardiol. 2004;94:481-484. (Pubitemid 39120000)
41. Nakamura Y, Yamada Y, Shimomura H, Nagayoshi Y, Tsujita K, Yamashita T, Fukuda M, Ohba K, Nako H, Ogura Y, Chitose T, Yamaguchi M, Nagata T, Soejima H, Kaikita K, Sugiyama S, Ogawa H. The effect of edaravone on plasma monocyte chemoattractant protein-1 levels in patients with acute myocardial infarction. J Cardiol. 2009;54: 416-424.
42. Qi X, Okuma Y, Hosoi T, Nomura Y. Edaravone protects against hypoxia/ ischemia-induced endoplasmic reticulum dysfunction. J Pharmacol Exp Ther. 2004;311:388-393. (Pubitemid 39287820)