Ischemic injury promotes Keap1 nitration and disturbance of antioxidative responses in endothelial cells: A potential vasoprotective effect of melatonin

Journal of Pineal Research

Volumn 54, Issue 3, 2013, Pages 271-281

  Tao, Rong Rong ^a   Huang, Ji Yun ^a   Shao, Xue Jing ^a   Ye, Wei Feng ^a,b   Tian, Yun ^a   Liao, Mei Hua ^a   Fukunaga, Kohji ^c   Lou, Yi Jia ^a   Han, Feng ^a   Lu, Ying Mei ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

endothelial cells; Keap1; melatonin; oxygen glucose deprivation; S nitrosylation; tyrosine nitration

Indexed keywords

BIOTIN; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MELATONIN; PEROXYNITRITE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; IN VITRO STUDY; ISCHEMIA; ISCHEMIC INJURY; MASS SPECTROMETRY; NITROSATIVE STRESS; NITROSYLATION; OXIDATIVE STRESS; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANTIOXIDANTS; CELL LINE; ENDOTHELIAL CELLS; GLUCOSE; HISTOCYTOCHEMISTRY; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISCHEMIA; MELATONIN; MICROSCOPY, FLUORESCENCE; NF-E2-RELATED FACTOR 2; NITRATES; OXYGEN; STRESS, PHYSIOLOGICAL; TYROSINE;

EID: 84874950225     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12009     Document Type: Article

References (50)

1. Quaegebeur A, Lange C, Carmeliet P,. The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 2011; 71: 406-424.
2. del Zoppo GJ,. The neurovascular unit, matrix proteases, and innate inflammation. Ann N Y Acad Sci 2010; 1207: 46-49.
3. Rizzo MT, Leaver HA,. Brain endothelial cell death: modes, signaling pathways, and relevance to neural development, homeostasis, and disease. Mol Neurobiol 2010; 42: 52-63.
4. Leblanc GG, Golanov E, Awad IA, et al. Biology of Vascular Malformations of the Brain NINDS Workshop Collaborators. Biology of vascular malformations of the brain. Stroke 2009; 40: e694-e702.
5. Girouard H, Park L, Anrather J, et al. Cerebrovascular nitrosative stress mediates neurovascular and endothelial dysfunction induced by angiotensin II. Arterioscler Thromb Vasc Biol 2007; 27: 303-309. (Pubitemid 46143044)
6. Wassmann S, Wassmann K, Nickenig G,. Modulation of oxidant and antioxidant enzyme expression and function in vascular cells. Hypertension 2004; 44: 381-386. (Pubitemid 39281479)
7. Liu QB, Liu LL, Lu YM, et al. The induction of reactive oxygen species and loss of mitochondrial Omi/HtrA2 is associated with S-nitrosoglutathione- induced apoptosis in human endothelial cells. Toxicol Appl Pharmacol 2010; 244: 374-384.
8. Han F, Chen YX, Lu YM, et al. Regulation of the ischemia-induced autophagy-lysosome processes by nitrosative stress in endothelial cells. J Pineal Res 2011; 51: 124-135.
9. Han F, Shirasaki Y, Fukunaga K,. Microsphere embolism-induced endothelial nitric oxide synthase expression mediates disruption of the blood-brain barrier in rat brain. J Neurochem 2006; 99: 97-106. (Pubitemid 44395133)
10. Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999; 13: 76-86. (Pubitemid 29045117)
11. Shih AY, Johnson DA, Wong G, et al. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 2003; 23: 3394-3406. (Pubitemid 36531981)
12. Copple IM, Lister A, Obeng AD, et al. Physical and functional interaction of sequestosome 1 with Keap1 regulates the Keap1-Nrf2 cell defense pathway. J Biol Chem 2010; 285: 16782-16788.
13. Lee JM, Shih AY, Murphy TH, et al. NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J Biol Chem 2003; 278: 37948-37956. (Pubitemid 37175325)
14. Seng S, Avraham HK, Birrane G, et al. Nuclear matrix protein (NRP/B) modulates the nuclear factor (Erythroid-derived 2)-related 2 (NRF2)-dependent oxidative stress response. J Biol Chem 2010; 285: 26190-26198.
15. Calkins MJ, Johnson DA, Townsend JA, et al. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal 2009; 11: 497-508.
16. Han F, Tao RR, Zhang GS, et al. Melatonin ameliorates ischemic-like injury-evoked nitrosative stress: involvement of HtrA2/PED pathways in endothelial cells. J Pineal Res 2011; 50: 281-291.
17. Tao RR, Ji YL, Lu YM, et al. Targeting nitrosative stress for neurovascular protection: new implications in brain diseases. Curr Drug Targets 2012; 13: 272-284.
18. Forrester MT, Foster MW, Benhar M, et al. Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic Biol Med 2009; 46: 119-126.
19. Chakrabarti S, Lekontseva O, Peters A, et al. 17beta-Estradiol induces protein S-nitrosylation in the endothelium. Cardiovasc Res 2010; 85: 796-805.
20. Shioda N, Han F, Moriguchi S, et al. Constitutively active calcineurin mediates delayed neuronal death through Fas-ligand expression via activation of NFAT and FKHR transcriptional activities in mouse brain ischemia. J Neurochem 2007; 102: 1506-1517. (Pubitemid 47256193)
21. Han F, Ali Raie A, Shioda N, et al. Accumulation of beta-amyloid in the brain microvessels accompanies increased hyperphosphorylated tau proteins following microsphere embolism in aged rats. Neuroscience 2008; 153: 414-427.
22. 2+ overload. Neuroscience 2008; 154: 473-481.
23. Liu B, Tewari AK, Zhang L, et al. Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: mitochondria as the major target. Biochim Biophys Acta 2009; 1794: 476-485.
24. Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 2010; 12: 213-223.
25. Velichkova M, Hasson T,. Keap1 regulates the oxidation-sensitive shuttling of Nrf2 into and out of the nucleus via a Crm1-dependent nuclear export mechanism. Mol Cell Biol 2005; 25: 4501-4513. (Pubitemid 40705756)
26. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, et al. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci USA 2004; 101: 2040-2045. (Pubitemid 38229011)
27. Tan DX, Chen LD, Poeggeler B, et al. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocrine J 1993; 1: 57-60.
28. Reiter RJ, Paredes SD, Manchester LC, et al. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit Rev Biochem Mol Biol 2009; 44: 175-200.
29. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
30. Tsai MC, Chen WJ, Tsai MS, et al. Melatonin attenuates brain contusion-induced oxidative insult, inactivation of signal transducers and activators of transcription 1, and upregulation of suppressor of cytokine signaling-3 in rats. J Pineal Res 2011; 51: 233-245.
31. Nair SM, Rahman RM, Clarkson AN, et al. Melatonin treatment following stroke induction modulates L-arginine metabolism. J Pineal Res 2011; 51: 313-323.
32. Kweon MH, Adhami VM, Lee JS, et al. Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem 2006; 281: 33761-33772. (Pubitemid 46036754)
33. Pozo D, Reiter RJ, Calvo JR, et al. Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin. J Cell Biochem 1997; 65: 430-442. (Pubitemid 27190697)
34. Cuzzocrea S, Costantino G, Gitto E, et al. Protective effects of melatonin in ischemic brain injury. J Pineal Res 2000; 29: 217-227.
35. Tai SH, Hung YC, Lee EJ, et al. Melatonin protects against transient focal cerebral ischemia in bothreproductively active and estrogen-deficient female rats: the impact of circulating estrogen on its hormetic dose-response. J Pineal Res 2011; 50: 292-303.
36. Kilic U, Yilmaz B, Ugur M, et al. Evidence that membrane-bound G protein-coupled melatonin receptors MT1 and MT2 are not involved in the neuroprotective effects of melatonin in focal cerebral ischemia. J Pineal Res 2012; 52: 228-135.
37. Koh PO,. Melatonin attenuates decrease of protein phosphatase 2A subunit B in ischemic brain injury. J Pineal Res 2012; 52: 57-61.
38. Kilic E, Kilic U, Reiter RJ, et al. Tissue-plasminogen activator-induced ischemic brain injury is reversed by melatonin: role of iNOS and Akt. J Pineal Res 2005; 39: 151-155. (Pubitemid 41140753)
39. Wakabayashi N, Itoh K, Wakabayashi J, et al. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 2003; 35: 238-245. (Pubitemid 37363177)
40. 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. (Pubitemid 47435741)
41. Satoh T, Kosaka K, Itoh K, et al. Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J Neurochem 2008; 104: 1116-1131. (Pubitemid 351143643)
42. Buckley BJ, Li S, Whorton AR,. Keap1 modification and nuclear accumulation in response to S-nitrosocysteine. Free Radic Biol Med 2008; 44: 692-698.
43. Silva CL, Tamura EK, Macedo SM, et al. Melatonin inhibits nitric oxide production by microvascular endothelial cells in vivo and in vitro. Br J Pharmacol 2007; 151: 195-205. (Pubitemid 46763046)
44. Gilad E, Cuzzocrea S, Zingarelli B, et al. Melatonin is a scavenger of peroxynitrite. Life Sci 1997; 60: PL169-PL174. (Pubitemid 27087273)
45. Reiter RJ,. Melatonin: lowering the high price of free radicals. News Physiol Sci 2000; 15: 246-250.
46. Wang B, Cao W, Biswal S, et al. Carbon monoxide-activated Nrf2 pathway leads to protection against permanent focal cerebral ischemia. Stroke 2011; 42: 2605-2610.
47. Kaspar JW, Niture SK, Jaiswal AK,. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009; 47: 1304-1309.
48. Um HC, Jang JH, Kim DH, et al. Nitric oxide activates Nrf2 through S-nitrosylation of Keap1 in PC12 cells. Nitric Oxide 2011; 25: 161-168.
49. Rada P, Rojo AI, Chowdhry S, et al. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011; 31: 1121-1133.
50. Rojo AI, Medina-Campos ON, Rada P, et al. Signaling pathways activated by the phytochemical nordihydroguaiaretic acid contribute to a Keap1-independent regulation of Nrf2 stability: role of glycogen synthase kinase-3. Free Radic Biol Med 2012; 52: 473-487.