Induction of the mitochondrial NDUFA4L2 protein by HIF-1α decreases oxygen consumption by inhibiting complex i activity

Cell Metabolism

Volumn 14, Issue 6, 2011, Pages 768-779

  Tello, Daniel ^a   Balsa, Eduardo ^a   Acosta Iborra, Bárbara ^a   Fuertes Yebra, Esther ^a   Elorza, Ainara ^a   Ordóñez, Ángel ^a   Corral Escariz, María ^a   Soro, Inés ^a   López Bernardo, Elia ^a   Perales Clemente, Ester ^b   Martínez Ruiz, Antonio ^a   Enríquez, José Antonio ^b,c   Aragonés, Julián ^a   Cadenas, Susana ^a,d   Landázuri, Manuel O ^a  

^a Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c UNIVERSITY OF ZARAGOZA   (Spain)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NADH DEHYDROGENASE(UBIQUINONE) 1 ALPHA SUBCOMPLEX, 4 LIKE 2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; MALE; MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL;

ANIMALS; ANOXIA; APOPTOSIS; CELL LINE; ELECTRON TRANSPORT COMPLEX I; ENZYME INDUCTION; FIBROBLASTS; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MITOCHONDRIA; OXYGEN CONSUMPTION; RATS; REACTIVE OXYGEN SPECIES; STATISTICS, NONPARAMETRIC;

MURINAE;

EID: 82955237531     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.10.008     Document Type: Article

References (45)

1. E. Aguirre, F. Rodríguez-Juárez, A. Bellelli, E. Gnaiger, and S. Cadenas Kinetic model of the inhibition of respiration by endogenous nitric oxide in intact cells Biochim. Biophys. Acta 1797 2010 557 565
2. M. Aldakkak, D.F. Stowe, Q. Chen, E.J. Lesnefsky, and A.K. Camara Inhibited mitochondrial respiration by amobarbital during cardiac ischaemia improves redox state and reduces matrix Ca2+ overload and ROS release Cardiovasc. Res. 77 2008 406 415 (Pubitemid 351197651)
3. K. Andreas, T. Häupl, C. Lübke, J. Ringe, L. Morawietz, A. Wachtel, M. Sittinger, and C. Kaps Antirheumatic drug response signatures in human chondrocytes: potential molecular targets to stimulate cartilage regeneration Arthritis Res. Ther. 11 2009 R15
4. J. Aragonés, M. Schneider, K. Van Geyte, P. Fraisl, T. Dresselaers, M. Mazzone, R. Dirkx, S. Zacchigna, H. Lemieux, and N.H. Jeoung Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism Nat. Genet. 40 2008 170 180 (Pubitemid 351171394)
5. J. Aragonés, P. Fraisl, M. Baes, and P. Carmeliet Oxygen sensors at the crossroad of metabolism Cell Metab. 9 2009 11 22
6. 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 (Pubitemid 43960624)
7. J. Carroll, I.M. Fearnley, J.M. Skehel, R.J. Shannon, J. Hirst, and J.E. Walker Bovine complex I is a complex of 45 different subunits J. Biol. Chem. 281 2006 32724 32727 (Pubitemid 46036828)
8. S.Y. Chan, Y.Y. Zhang, C. Hemann, C.E. Mahoney, J.L. Zweier, and J. Loscalzo MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2 Cell Metab. 10 2009 273 284
9. Q. Chen, C.L. Hoppel, and E.J. Lesnefsky Blockade of electron transport before cardiac ischemia with the reversible inhibitor amobarbital protects rat heart mitochondria J. Pharmacol. Exp. Ther. 316 2006 200 207 (Pubitemid 41832597)
10. Q. Chen, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion J. Pharmacol. Exp. Ther. 319 2006 1405 1412
11. Z. Chen, Y. Li, H. Zhang, P. Huang, and R. Luthra Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression Oncogene 29 2010 4362 4368
12. N. Driessens, S. Versteyhe, C. Ghaddhab, A. Burniat, X. De Deken, J. Van Sande, J.E. Dumont, F. Miot, and B. Corvilain Hydrogen peroxide induces DNA single- and double-strand breaks in thyroid cells and is therefore a potential mutagen for this organ Endocr. Relat. Cancer 16 2009 845 856
13. E. Favaro, A. Ramachandran, R. McCormick, H. Gee, C. Blancher, M. Crosby, C. Devlin, C. Blick, F. Buffa, and J.L. Li MicroRNA-210 regulates mitochondrial free radical response to hypoxia and krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU PLoS ONE 5 2010 e10345
14. J. Favier, J.J. Brire, N. Burnichon, J. Rivire, L. Vescovo, P. Benit, I. Giscos-Douriez, A. De Reynis, J. Bertherat, and C. Badoual The Warburg effect is genetically determined in inherited pheochromocytomas PLoS ONE 4 2009 e7094
15. E. Fredlund, M. Ovenberger, K. Borg, and S. Phlman Transcriptional adaptation of neuroblastoma cells to hypoxia Biochem. Biophys. Res. Commun. 366 2008 1054 1060
16. M.T. Frost, Q. Wang, S. Moncada, and M. Singer Hypoxia accelerates nitric oxide-dependent inhibition of mitochondrial complex I in activated macrophages Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 2005 R394 R400
17. R. Fukuda, H. Zhang, J.W. Kim, L. Shimoda, C.V. Dang, and G.L. Semenza HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells Cell 129 2007 111 122 (Pubitemid 46507584)
18. L.B. Gardner, Q. Li, M.S. Park, W.M. Flanagan, G.L. Semenza, and C.V. Dang Hypoxia inhibits G1/S transition through regulation of p27 expression J. Biol. Chem. 276 2001 7919 7926
19. E. Gnaiger, B. Lassnig, A.V. Kuznetsov, and R. Margreiter Mitochondrial respiration in the low oxygen environment of the cell. Effect of ADP on oxygen kinetics Biochim. Biophys. Acta 1365 1998 249 254 (Pubitemid 29359265)
20. N. Goda, H.E. Ryan, B. Khadivi, W. McNulty, R.C. Rickert, and R.S. Johnson Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia Mol. Cell. Biol. 23 2003 359 369 (Pubitemid 36008526)
21. 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 (Pubitemid 43960623)
22. N.V. Iyer, L.E. Kotch, F. Agani, S.W. Leung, E. Laughner, R.H. Wenger, M. Gassmann, J.D. Gearhart, A.M. Lawler, A.Y. Yu, and G.L. Semenza Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha Genes Dev. 12 1998 149 162 (Pubitemid 28060446)
23. 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 (Pubitemid 351681994)
24. J.W. Kim, I. Tchernyshyov, G.L. Semenza, and C.V. Dang HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia Cell Metab. 3 2006 177 185
25. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18 (Pubitemid 27470791)
26. S.E. Kruse, W.C. Watt, D.J. Marcinek, R.P. Kapur, K.A. Schenkman, and R.D. Palmiter Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy Cell Metab. 7 2008 312 320 (Pubitemid 351455216)
27. Y. Liu, G. Fiskum, and D. Schubert Generation of reactive oxygen species by the mitochondrial electron transport chain J. Neurochem. 80 2002 780 787 (Pubitemid 34809230)
28. C.W. Lu, S.C. Lin, K.F. Chen, Y.Y. Lai, and S.J. Tsai Induction of pyruvate dehydrogenase kinase-3 by hypoxia-inducible factor-1 promotes metabolic switch and drug resistance J. Biol. Chem. 283 2008 28106 28114
29. 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 (Pubitemid 43960625)
30. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
31. I. Papandreou, R.A. Cairns, L. Fontana, A.L. Lim, and N.C. Denko HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption Cell Metab. 3 2006 187 197
32. J.I. Piruat, and J. López-Barneo Oxygen tension regulates mitochondrial DNA-encoded complex I gene expression J. Biol. Chem. 280 2005 42676 42684 (Pubitemid 43049226)
33. S. Raha, and B.H. Robinson Mitochondria, oxygen free radicals, disease and ageing Trends Biochem. Sci. 25 2000 502 508
34. F. Rodríguez-Juárez, E. Aguirre, and S. Cadenas Relative sensitivity of soluble guanylate cyclase and mitochondrial respiration to endogenous nitric oxide at physiological oxygen concentration Biochem. J. 405 2007 223 231 (Pubitemid 47075157)
35. H. Schägger Native electrophoresis for isolation of mitochondrial oxidative phosphorylation protein complexes Methods Enzymol. 260 1995 190 202
36. C.J. Schofield, and P.J. Ratcliffe Oxygen sensing by HIF hydroxylases Nat. Rev. Mol. Cell Biol. 5 2004 343 354 (Pubitemid 38579472)
37. G.L. Semenza Hydroxylation of HIF-1: oxygen sensing at the molecular level Physiology (Bethesda) 19 2004 176 182 (Pubitemid 39481932)
38. G.L. Semenza Regulation of oxygen homeostasis by hypoxia-inducible factor 1 Physiology (Bethesda) 24 2009 97 106
39. R.T. Smolenski, J. Schrader, H. de Groot, and A. Deussen Oxygen partial pressure and free intracellular adenosine of isolated cardiomyocytes Am. J. Physiol. 260 1991 C708 C714
40. J. St-Pierre, J.A. Buckingham, S.J. Roebuck, and M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790 (Pubitemid 36159072)
41. T. Stumpe, and J. Schrader Phosphorylation potential, adenosine formation, and critical PO2 in stimulated rat cardiomyocytes Am. J. Physiol. 273 1997 H756 H766
42. R.O. Vogel, R.J. Janssen, C. Ugalde, M. Grovenstein, R.J. Huijbens, H.J. Visch, L.P. van den Heuvel, P.H. Willems, M. Zeviani, J.A. Smeitink, and L.G. Nijtmans Human mitochondrial complex I assembly is mediated by NDUFAF1 FEBS J. 272 2005 5317 5326 (Pubitemid 41503160)
43. T.V. Votyakova, and I.J. Reynolds DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria J. Neurochem. 79 2001 266 277 (Pubitemid 32988942)
44. J.E. Walker, J.M. Arizmendi, A. Dupuis, I.M. Fearnley, M. Finel, S.M. Medd, S.J. Pilkington, M.J. Runswick, and J.M. Skehel Sequences of 20 subunits of NADH:ubiquinone oxidoreductase from bovine heart mitochondria. Application of a novel strategy for sequencing proteins using the polymerase chain reaction J. Mol. Biol. 226 1992 1051 1072
45. W.W. Wheaton, and N.S. Chandel Hypoxia. 2. Hypoxia regulates cellular metabolism Am. J. Physiol. Cell Physiol. 300 2011 C385 C393