Acute hypoxia produces a superoxide burst in cells

Free Radical Biology and Medicine

Volumn 71, Issue , 2014, Pages 146-156

  Hernansanz Agustín, Pablo ^a,b   Izquierdo Álvarez, Alicia ^a   Sánchez Gómez, Francisco J ^c,d,f   Ramos, Elena ^a   Villa Piña, Tamara ^a   Lamas, Santiago ^c,d   Bogdanova, Anna ^e   Martínez Ruiz, Antonio ^a  

^a HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c Section of Nephrology   (Spain)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Cell signaling; Free radicals; Hypoxia; Ischemia; Oxidative phosphorylation; Reactive oxygen species; Superoxide

Indexed keywords

OXYGEN; SUPEROXIDE;

ANIMAL; BOVINAE; CELL HYPOXIA; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; HELA CELL LINE; HUMAN; HYDROXYLATION; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; RESPIRATORY BURST; SIGNAL TRANSDUCTION; TIME;

ANIMALS; CATTLE; CELL HYPOXIA; ENDOTHELIAL CELLS; HELA CELLS; HUMANS; HYDROXYLATION; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; OXYGEN; OXYGEN CONSUMPTION; RESPIRATORY BURST; SIGNAL TRANSDUCTION; SUPEROXIDES; TIME FACTORS;

EID: 84898860936     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.03.011     Document Type: Article

References (39)

1. G.L. Semenza Life with oxygen Science 318 2007 62 64
2. W.G. Kaelin Jr, and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol. Cell 30 2008 393 402
3. N.S. Chandel, E. Maltepe, E. Goldwasser, C.E. Mathieu, M.C. Simon, and P.T. Schumacker Mitochondrial reactive oxygen species trigger hypoxia-induced transcription Proc. Natl. Acad. Sci. USA 95 1998 11715 11720
4. 2 sensor in rat pulmonary vasculature Circ. Res. 73 1993 1100 1112
5. J.R. Desireddi, K.N. Farrow, J.D. Marks, G.B. Waypa, and P.T. Schumacker Hypoxia increases ROS signaling and cytosolic Ca(2+) in pulmonary artery smooth muscle cells of mouse lungs slices Antioxid. Redox Signaling 12 2010 595 602
6. S. Yakushev, M. Band, M.C. Tissot van Patot, M. Gassmann, A. Avivi, and A. Bogdanova Cross talk between S-nitrosylation and S-glutathionylation in control of the Na,K-ATPase regulation in hypoxic heart Am. J. Physiol. Heart Circ. Physiol. 303 2012 H1332 H1343
7. I.Y. Petrushanko, S. Yakushev, V.A. Mitkevich, Y.V. Kamanina, R.H. Ziganshin, X. Meng, A.A. Anashkina, A. Makhro, O.D. Lopina, M. Gassmann, A.A. Makarov, and A. Bogdanova S-glutathionylation of the Na,K-ATPase catalytic alpha subunit is a determinant of the enzyme redox sensitivity J. Biol. Chem. 287 2012 32195 32205
8. A. Izquierdo-Álvarez, E. Ramos, J. Villanueva, P. Hernansanz-Agustín, R. Fernández-Rodríguez, D. Tello, M. Carrascal, and A. Martínez-Ruiz Differential redox proteomics allows identification of proteins reversibly oxidized at cysteine residues in endothelial cells in response to acute hypoxia J. Proteomics 75 2012 5449 5462
9. R.D. Guzy, B. Hoyos, E. Robin, H. Chen, L. Liu, K.D. Mansfield, M.C. Simon, U. Hammerling, and P.T. Schumacker Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing Cell Metab. 1 2005 401 408
10. K.D. Mansfield, R.D. Guzy, Y. Pan, R.M. Young, T.P. Cash, P.T. Schumacker, and M.C. Simon Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-[alpha] activation Cell Metab. 1 2005 393 399
11. J.K. Brunelle, E.L. Bell, N.M. Quesada, K. Vercauteren, V. Tiranti, M. Zeviani, R.C. Scarpulla, and N.S. Chandel Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation Cell Metab. 1 2005 409 414
12. E.L. Bell, B.M. Emerling, S.J. Ricoult, and L. Guarente SirT3 suppresses hypoxia inducible factor 1alpha and tumor growth by inhibiting mitochondrial ROS production Oncogene 30 2011 2986 2996
13. R.D. Guzy, and P.T. Schumacker Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia Exp. Physiol. 91 2006 807 819
14. R.B. Hamanaka, and N.S. Chandel Mitochondrial reactive oxygen species regulate hypoxic signaling Curr. Opin. Cell Biol. 21 2009 894 899
15. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
16. E.C. Vaux, E. Metzen, K.M. Yeates, and P.J. Ratcliffe Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain Blood 98 2001 296 302
17. Y.L. Chua, E. Dufour, E.P. Dassa, P. Rustin, H.T. Jacobs, C.T. Taylor, and T. Hagen Stabilization of hypoxia-inducible factor-1alpha protein in hypoxia occurs independently of mitochondrial reactive oxygen species production J. Biol. Chem. 285 2010 31277 31284
18. T. Hagen Oxygen versus reactive oxygen in the regulation of HIF-1alpha: the balance tips Biochem. Res. Int. 2012 2012 436981
19. C. Schroedl, D.S. McClintock, G.R.S. Budinger, and N.S. Chandel Hypoxic but not anoxic stabilization of HIF-1alpha requires mitochondrial reactive oxygen species Am. J. Physiol. Lung Cell. Mol. Physiol. 283 2002 L922 L931
20. M. Quintero, S.L. Colombo, A. Godfrey, and S. Moncada Mitochondria as signaling organelles in the vascular endothelium Proc. Natl. Acad. Sci. USA 103 2006 5379 5384
21. E. Robin, R.D. Guzy, G. Loor, H. Iwase, G.B. Waypa, J.D. Marks, T.L.V. Hoek, and P.T. Schumacker Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion J. Biol. Chem. 282 2007 19133 19143
22. H. Iwase, E. Robin, R.D. Guzy, P.T. Mungai, T.L. Vanden Hoek, N.S. Chandel, J. Levraut, and P.T. Schumacker Nitric oxide during ischemia attenuates oxidant stress and cell death during ischemia and reperfusion in cardiomyocytes Free Radic. Biol. Med. 43 2007 590 599
23. G.B. Waypa, J.D. Marks, R. Guzy, P.T. Mungai, J. Schriewer, D. Dokic, and P.T. Schumacker Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells Circ. Res. 106 2010 526 535
24. P.T. Schumacker Lung cell hypoxia: role of mitochondrial reactive oxygen species signaling in triggering responses Proc. Am. Thorac. Soc. 8 2011 477 484
25. W. Yang, and E.R. Block Effect of hypoxia and reoxygenation on the formation and release of reactive oxygen species by porcine pulmonary artery endothelial cells J. Cell. Physiol. 164 1995 414 423
26. J. Navarro-Antolín, J. Rey-Campos, and S. Lamas Transcriptional induction of endothelial nitric oxide gene by cyclosporine A: a role for activator protein-1 J. Biol. Chem. 275 2000 3075 3080
27. R. Moreno-Loshuertos, R. Acín-Pérez, P. Fernández-Silva, N. Movilla, A. Pérez-Martos, S. Rodríguez de Córdoba, M.E. Gallardo, and J.A. Enríquez Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants Nat. Genet. 38 2006 1261 1268
28. B.M. Rothen-Rutishauser, E. Ehler, E. Perriard, J.M. Messerli, and J.C. Perriard Different behaviour of the non-sarcomeric cytoskeleton in neonatal and adult rat cardiomyocytes J. Mol. Cell. Cardiol. 30 1998 19 31
29. P. Armitage, G. Berry, and J. Matthews Statistical Methods in Medical Research 2002 Blackwell Sci. Oxford
30. J.W. Hardin, and J.M. Hilbe Generalized Estimating Equations 2002 Chapman & Hall/CRC Press Boca Raton, FL
31. J.F. Turrens Mitochondrial formation of reactive oxygen species J. Physiol. 552 2003 335 344
32. C.J. Edgell, C.C. McDonald, and J.B. Graham Permanent cell line expressing human factor VIII-related antigen established by hybridization Proc. Natl. Acad. Sci. USA 80 1983 3734 3737
33. H. Zhao, J. Joseph, H.M. Fales, E.A. Sokoloski, R.L. Levine, J. Vasquez-Vivar, and B. Kalyanaraman Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence Proc. Natl. Acad. Sci. USA 102 2005 5727 5732
34. M. Redondo-Horcajo, N. Romero, P. Martínez-Acedo, A. Martínez-Ruiz, C. Quijano, C.F. Lourenço, N. Movilla, J.A. Enríquez, F. Rodríguez-Pascual, E. Rial, R. Radi, J. Vázquez, and S. Lamas Cyclosporine A-induced nitration of tyrosine 34 MnSOD in endothelial cells: role of mitochondrial superoxide Cardiovasc. Res. 87 2010 356 365
35. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, L.J. Roberts 2nd, and H. Ischiropoulos Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic. Biol. Med. 52 2012 1 6
36. M. Calvani, G. Comito, E. Giannoni, and P. Chiarugi Time-dependent stabilization of hypoxia inducible factor-1alpha by different intracellular sources of reactive oxygen species PLoS One 7 2012 e38388
37. L.G. Nijtmans, L. de Jong, M. Artal Sanz, P.J. Coates, J.A. Berden, J.W. Back, A.O. Muijsers, H. van der Spek, and L.A. Grivell Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins EMBO J. 19 2000 2444 2451
38. S.W. Perry, J.P. Norman, J. Barbieri, E.B. Brown, and H.A. Gelbard Mitochondrial membrane potential probes and the proton gradient: a practical usage guide Biotechniques 50 2011 98 115
39. L.B. Becker, T.L. vanden Hoek, Z.H. Shao, C.Q. Li, and P.T. Schumacker Generation of superoxide in cardiomyocytes during ischemia before reperfusion Am. J. Physiol. 277 1999 H2240 H2246