Glucose reintroduction triggers the activation of Nrf2 during experimental ischemia reperfusion

Molecular and Cellular Biochemistry

Volumn 366, Issue 1-2, 2012, Pages 231-238

  Crean, Daniel ^a   Felice, Luca ^a   Taylor, Cormac T ^a   Rabb, Hamid ^b   Jennings, Paul ^c   Leonard, Martin O ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b JOHNS HOPKINS HOSPITAL   (United States)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Glucose; Ischemia; NADPH; Nrf2; Reperfusion

Indexed keywords

GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LAMIN A; LAMIN C; MESSENGER RNA; NADPH DEHYDROGENASE QUINONE 1; OXIDOREDUCTASE; OXYGEN; PROTEIN AKR1C1-3; PROTEIN DHRS2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ARTICLE; CELL DAMAGE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; ISCHEMIA; KIDNEY EPITHELIUM; MICROARRAY ANALYSIS; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FAMILY; REGULATORY MECHANISM; REPERFUSION; TARGET CELL; UPREGULATION;

ALCOHOL OXIDOREDUCTASES; ANIMALS; CELL LINE; CELL NUCLEUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLUCOSE; HUMANS; ISCHEMIA; KIDNEY; MICE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; REPERFUSION INJURY;

MURINAE;

EID: 84862021685     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-012-1300-4     Document Type: Article

References (35)

1. Toledo-Pereyra LH, Toledo AH, Walsh J, Lopez-Neblina F (2004) Molecular signaling pathways in ischemia/reperfusion. Exp Clin Transplant 2:174-177
2. Erdogan H, Fadillioglu E, Yagmurca M, Uçar M, Irmak MK (2006) Protein oxidation and lipid peroxidation after renal ischemia-reperfusion injury: protective effects of erdosteine and N-acetylcysteine. Urol Res 34:41-46. doi:10.1007/s00240-005-0031-3 (Pubitemid 43234713)
3. Niture SK, Kaspar JW, Shen J, Jaiswal AK (2010) Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 244:37-42. doi:10.1016/j.taap.2009.06.009
4. Dinkova-Kostova AT, Talalay P (2010) NAD(P)H: quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Appl Biochem Biophys 501:116-123. doi:10.1016/j.abb. 2010.03.019
5. Webster KA, Discher DJ, Kaiser S, Hernandez O, Sato B, Bishopric NH (1999) Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J Clin Invest 104:239-252. doi:10.1172/JCI5871
6. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2006) Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion. J Pharmacol Exp Ther 319:1405-1412. doi:10.1124/jpet.106.110262
7. Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, Porter AG, O'Farrelly C, Rabb H, Taylor CT (2006) Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J 20:2624-2626. doi:10.1096/fj.06-5097fje
8. Leonard MO, Hannan K, Burne MJ, Lappin DW, Doran P, Coleman P, Stenson C, Taylor CT, Daniels F, Godson C, Petasis NA, Rabb H, Brady HR (2002) 15-Epi-16-(para-fluorophenoxy)-lipoxin A(4)-methyl ester, a synthetic analogue of 15-epi-lipoxin A(4), is protective in experimental ischemic acute renal failure. J Am Soc Nephrol 13:1657-1662. doi:10.1097/01.ASN.0000015795.74094.91 (Pubitemid 34579255)
9. Wilmes A, Crean D, Aydin S, Pfaller W, Jennings P, Leonard MO (2011) Identification and dissection of the Nrf2 mediated oxidative stress pathway in human renal proximal tubule toxicity. Toxicol In Vitro 25:613-622. doi:10.1016/j.tiv.2010.12.009
10. Leonard MO, Howell K, Madden SF, Costello CM, Higgins DG, Taylor CT, McLoughlin P (2008) Hypoxia selectively activates the CREB family of transcription factors in the in vivo lung. Am J Respir Crit Care Med 178:977-983. doi:10.1164/rccm.200712-1890OC
11. Venugopal R, Jaiswal AK (1996) Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H: quinone oxidoreductase 1 gene. Proc Natl Acad Sci USA 93:14960-14965 (Pubitemid 26419078)
12. McLeod AK, McMahon M, Plummer SM, Higgins LG, Penning TM, Igarashi K, Hayes JD (2009) Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes. Carcinogenesis 30:1571-1580. doi:10.1093/carcin/bgp176
13. Shen G, Xu C, Hu R, Jain MR, Gopalkrishnan A, Nair S, Huang MT, Chan JY, Kong AN (2006) Modulation of nuclear factor E2-related factor 2-mediated gene expression in mice liver and small intestine by cancer chemopreventive agent curcumin. Mol Cancer Ther 5:39-51. doi:10.1158/1535-7163.MCT-05-0293
14. Hübner RH, Schwartz JD, De Bishnu P, Ferris B, Omberg L, Mezey JG, Hackett NR, Crystal RG (2009) Coordinate control of expression of Nrf2-modulated genes in the human small airway epithelium is highly responsive to cigarette smoking. Mol Med 15:203-219. doi:10.2119/molmed.2008.00130
15. Abramov AY, Scorziello A, Duchen MR (2007) Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 27:1129-1138. doi:10.1523/JNEUROSCI.4468- 06.2007 (Pubitemid 46203321)
16. Loor G, Kondapalli J, Iwase H, Chandel NS, Waypa GB, Guzy RD, Vanden Hoek TL, Schumacker PT (2011) Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim Biophys Acta 1813:1382-1394. doi:10.1016/j.bbamcr.2010.12.008
17. Meischl C, Krijnen PA, Sipkens JA, Cillessen SA, Muñoz IG, Okroj M, Ramska M, Muller A, Visser CA, Musters RJ, Simonides WS, Hack CE, Roos D, Niessen HW (2006) Ischemia induces nuclear NOX2 expression in cardiomyocytes and subsequently activates apoptosis. Apoptosis 11:913-921. doi:10.1007/s10495-006- 6304-7 (Pubitemid 43876822)
18. Therade-Matharan S, Laemmel E, Duranteau J, Vicaut E (2004) Reoxygenation after hypoxia and glucose depletion causes reactive oxygen species production by mitochondria in HUVEC. Am J Physiol Regul Integr Comp Physiol 287:1037-1043. doi:10.1152/ajpregu.00048.2004
19. Loukogeorgakis SP, Van den Berg MJ, Sofat R, Nitsch D, Charakida M, Haiyee B, de Groot E, MacAllister RJ, Kuijpers TW, Deanfield JE (2010) Role of NADPH oxidase in endothelial ischemia/reperfusion injury in humans. Circulation 121:2310-2316. doi:10.1161/CIRCULATIONAHA.108.814731
20. Suh SW, Shin BS, Ma H, Van Hoecke M, Brennan AM, Yenari MA, Swanson RA (2008) Glucose and NADPH oxidase drive neuronal superoxide formation in stroke. Ann Neurol 64:654-663. doi:10.1002/ana.21511
21. Amaral AL, Teixeira AP, Martens S, Bernal V, Sousa MF, Alves PM (2010) Metabolic alterations induced by ischemia in primary cultures of astrocytes: merging 13C NMR spectroscopy and metabolic flux analysis. J Neurochem 113:735-748. doi:10.1111/j.1471-4159.2010.06636.x
22. Jain M, Cui L, Brenner DA, Wang B, Handy DE, Leopold JA, Loscalzo J, Apstein CS, Liao R (2004) Increased myocardial dysfunction after ischemia-reperfusion in mice lacking glucose-6-phosphate dehydrogenase. Circulation 109:898-903. doi:10.1161/01.CIR.0000112605.43318.CA (Pubitemid 38252743)
23. Hill JR, Kwon G, Marshall CA, McDaniel ML (1998) Hyperglycemic levels of glucose inhibit interleukin 1 release from RAW 264.7 murine macrophages by activation of protein kinase C. J Biol Chem 273:3308-3313. doi:10.1074/jbc.273. 6.3308 (Pubitemid 28109744)
24. Li H, Wang F, Zhang L, Cao Y, Liu W, Hao J, Liu Q, Duan H (2011) Modulation of Nrf2 expression alters high glucose-nduced oxidative stress and antioxidant gene expression in mouse mesangial cells. Cell Signal 23:1625-1632. doi:10.1016/j.cellsig.2011.05.016
25. Gao L, Mann GE (2009) Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc Res 82:9-20. doi:10.1093/cvr/cvp031
26. Balteau M, Tajeddine N, de Meester C, Ginion A, Des Rosiers C, Brady NR, Sommereyns C, Horman S, Vanoverschelde JL, Gailly P, Hue L, Bertrand L, Beauloye C (2011) NADPH oxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1. Cardiovasc Res 92:237-246. doi:10.1093/cvr/cvr230
27. Wu KC, Cui JY, Klaassen CD (2011) Beneficial role of Nrf2 in regulating NADPH generation and consumption. Toxicol Sci 123:590-600. doi:10.1093/toxsci/ kfr183
28. Gaikwad A, Long DJ, Stringer JL, Jaiswal AK (2001) In vivo role of NAD(P)H: quinone oxidoreductase 1 (NQO1) in the regulation of intracellular redox state and accumulation of abdominal adipose tissue. J Biol Chem 276:22559-22564. doi:10.1074/jbc.M101053200
29. Shafqat N, Shafqat J, Eissner G, Marschall HU, Tryggvason K, Eriksson U, Gabrielli F, Lardy H, Jörnvall H, Oppermann U (2006) Hep27, a member of the short-chain dehydrogenase/reductase family, is an NADPH-dependent dicarbonyl reductase expressed in vascular endothelial tissue. Cell Mol Life Sci 63:1205-1213. doi:10.1007/s00018-006-6013-y (Pubitemid 43939006)
30. Oppermann U (2007) Carbonyl reductases: the complex relationships of mammalian carbonyl- and quinone-reducing enzymes and their role in physiology. Annu Rev Pharmacol Toxicol 47:293-322. doi:10.1146/annurev.pharmtox.47.120505. 105316
31. Monge M, Colas E, Doll A, Gil-Moreno A, Castellvi J, Diaz B, Gonzalez M, Lopez-Lopez R, Xercavins J, Carreras R, Alameda F, Canals F, Gabrielli F, Reventos J, Abal M (2009) Proteomic approach to ETV5 during endometrial carcinoma invasion reveals a link to oxidative stress. Carcinogenesis 30:1288-1297. doi:10.1093/carcin/bgp119
32. Eltzschig HK, Eckle T (2011) Ischemia and reperfusion-from mechanism to translation. Nat Med 17:1391-1401. doi:10.1038/nm.2507
33. Eltzschig HK, Carmeliet P (2011) Hypoxia and inflammation. N Engl J Med 364:656-665. doi:10.1056/NEJMra0910283
34. Grenz A, Bauerle JD, Dalton JH, Ridyard D, Badulak A, Tak E, McNamee EN, Clambey E, Moldovan R, Reyes G, Klawitter J, Ambler K, Magee K, Christians U, Brodsky KS, Ravid K, Choi DS, Wen J, Lukashev D, Blackburn MR, Osswald H, Coe IR, Nürnberg B, Haase VH, Xia Y, Sitkovsky M, Eltzschig HK (2012) Equilibrative nucleoside transporter 1 (ENT1) regulates postischemic blood flow during acute kidney injury in mice. J Clin Invest 122:693-710. doi:10.1172/JCI60214
35. Min KJ, Kim JH, Jou I, Joe EH (2008) Adenosine induces hemeoxygenase-1 expression in microglia through the activation of phosphatidylinositol 3-kinase and nuclear factor E2-related factor 2. Glia 56:1028-1037. doi:10.1002/glia. 20676