DJ-1 Mediates the Delayed Cardioprotection of Hypoxic Preconditioning Through Activation of Nrf2 and Subsequent Upregulation of Antioxidative Enzymes

Journal of Cardiovascular Pharmacology

Volumn 66, Issue 2, 2015, Pages 148-158

  Yan, Yu Feng ^a   Chen, He Ping ^a   Huang, Xiao Shan ^a   Qiu, Ling Yu ^a   Liao, Zhang Ping ^a   Huang, Qi Ren ^a  

^a NANCHANG UNIVERSITY   (China)

Author keywords

antioxidative enzymes; delayed cardioprotection; DJ 1; hypoxic preconditioning; Nrf2 pathway

Indexed keywords

DJ 1 PROTEIN; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MANGANESE SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; MICROTUBULE ASSOCIATED PROTEIN; NFE2L2 PROTEIN, RAT; SP22 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BINDING AFFINITY; CELL DAMAGE; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME MECHANISM; GENE EXPRESSION; GENETIC TRANSFECTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; HUMAN CELL; HYPOXIA; HYPOXIC PRECONDITIONING; ISCHEMIC PRECONDITIONING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; REOXYGENATION; REPERFUSION INJURY; UPREGULATION; ANIMAL; CARDIAC MUSCLE CELL; CELL HYPOXIA; CELL LINE; GENE SILENCING; HEART INFARCTION PREVENTION; METABOLISM; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; CELL HYPOXIA; CELL LINE; GENE KNOCKDOWN TECHNIQUES; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MICROTUBULE-ASSOCIATED PROTEINS; MYOCYTES, CARDIAC; NF-E2-RELATED FACTOR 2; RATS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84939618270     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0000000000000257     Document Type: Article

References (38)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124-1136.
2. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev. 2003;83:1113-1151.
3. Das DK, Maulik N. Cardiac genomic response following preconditioning stimulus. Cardiovasc Res. 2006;70:254-263.
4. Bolli R. The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol. 1996;91:57-63.
5. Rizvi A, Tang XL, Qiu Y, et al. Increased protein synthesis is necessary for the development of late preconditioning against myocardial stunning. Am J Physiol. 1999;277:H874-H884.
6. Vanden Hoek T, Becker LB, Shao ZH, et al. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res. 2000;86:541-548.
7. Morihira M, Hasebe N, Baljinnyam E, et al. Ischemic preconditioning enhances scavenging activity of reactive oxygen species and diminishes transmural difference of infarct size. Am J Physiol Heart Circ Physiol. 2006;290:H577-H583.
8. Nagakubo D, Taira T, Kitaura H, et al. DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem Biophys Res Commun. 1997;231:509-513.
9. Ishikawa S, Taira T, Takahashi-Niki K, et al. Human DJ-1-specific transcriptional activation of tyrosine hydroxylase gene. J Biol Chem. 2010; 285:39718-39731.
10. Shinbo Y, Taira T, Niki T, et al. DJ-1 restores p53 transcription activity inhibited by Topors/p53BP3. Int J Oncol. 2005;26:641-648.
11. Taira T, Saito Y, Niki T, et al. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep. 2004;5:213-218.
12. Shendelman S, Jonason A, Martinat C, et al. DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol. 2004;2:e362.
13. Honbou K, Suzuki NN, Horiuchi M, et al. The crystal structure of DJ-1, a protein related to male fertility and Parkinson's disease. J Biol Chem. 2003;278:31380-31384.
14. Lu HS, Chen HP, Wang S, et al. Hypoxic preconditioning up-regulates DJ-1 protein expression in rat heart-derived H9c2 cells through the activation of extracellular-regulated kinase 1/2 pathway. Mol Cell Biochem. 2012;370:231-240.
15. Kaspar JW, Niture SK, Jaiswal AK. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med. 2009;47:1304-1309.
16. Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem. 2009;284:13291-13295.
17. Keum YS, Choi BY. Molecular and chemical regulation of the Keap1-Nrf2 signaling pathway. Molecules. 2014;19:10074-10089.
18. Sun Z, Zhang S, Chan JY, et al. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol. 2007;27:6334-6349.
19. Howden R. Nrf2 and cardiovascular defense. Oxid Med Cell Longev. 2013;2013:104308.
20. Huang XS, Chen HP, Yu HH, et al. Nrf2-dependent upregulation of antioxidative enzymes: a novel pathway for hypoxic preconditioningmediated delayed cardioprotection. Mol Cell Biochem. 2014;385:33-41.
21. Clements CM, McNally RS, Conti BJ, et al. DJ-1, a cancer-and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci USA. 2006;103:15091-15096.
22. Zhu ZM, Li ZR, Huang Y, et al. DJ-1 is involved in the peritoneal metastasis of gastric cancer through activation of the Akt signaling pathway. Oncol Rep. 2014;31:1489-1497.
23. Yu HH, Xu Q, Chen HP, et al. Stable overexpression of DJ-1 protects H9c2 cells against oxidative stress under a hypoxia condition. Cell Biochem Funct. 2013;31:643-651.
24. Mizukami Y, Iwamatsu A, Aki T, et al. ERK1/2 regulates intracellular ATP levels through alpha-enolase expression in cardiomyocytes exposed to ischemic hypoxia and reoxygenation. J Biol Chem. 2004;279:50120-50131.
25. Jiao JD, Garg V, Yang B, et al. Novel functional role of heat shock protein 90 in ATP-sensitive K+ channel-mediated hypoxic preconditioning. Cardiovasc Res. 2008;77:126-133.
26. Kim JY, Cho HJ, Sir JJ, et al. Sulfasalazine induces haem oxygenase-1 via ROS-dependent Nrf2 signalling, leading to control of neointimal hyperplasia. Cardiovasc Res. 2009;82:550-560.
27. Li J, Ichikawa T, Jin Y, et al. An essential role of Nrf2 in American ginseng-mediated anti-oxidative actions in cardiomyocytes. J Ethnopharmacol. 2010;130:222-230.
28. Saeed SA, Waqar MA, Zubairi AJ, et al. Myocardial ischaemia and reperfusion injury: reactive oxygen species and the role of neutrophil. J Coll Physicians Surg Pak. 2005;15:507-514.
29. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res. 2006;70:181-190.
30. Park JL, Lucchesi BR. Mechanisms of myocardial reperfusion injury. Ann Thorac Surg. 1999;68:1905-1912.
31. Hoshida S, Yamashita N, Otsu K, et al. The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines. Cardiovasc Res. 2002;55: 495-505.
32. Zhou X, Zhai X, Ashraf M. Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocytes. Circulation. 1996;93: 1177-1184.
33. Yamashita N, Nishida M, Hoshida S, et al. Induction of manganese superoxide dismutase in rat cardiac myocytes increases tolerance to hypoxia 24 hours after preconditioning. J Clin Invest. 1994;94:2193-2199.
34. Jancso G, Cserepes B, Gasz B, et al. Expression and protective role of heme oxygenase-1 in delayed myocardial preconditioning. Ann N Y Acad Sci. 2007;1095:251-261.
35. Bolli R. The late phase of preconditioning. Circ Res. 2000;87:972-983.
36. Kim RH, Smith PD, Aleyasin H, et al. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc Natl Acad Sci USA. 2005;102:5215-5220.
37. Inden M, Taira T, Kitamura Y, et al. PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson's disease rat model. Neurobiol Dis. 2006;24:144-158.
38. Malhotra D, Thimmulappa R, Navas-Acien A, et al. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am J Respir Crit Care Med. 2008;178:592-604.