Inactivation of pyruvate dehydrogenase kinase 2 by mitochondrial reactive oxygen species

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35153-35160

  Hurd, Thomas R ^a,b   Collins, Yvonne ^a   Abakumova, Irina ^a,c   Chouchani, Edward T ^a   Baranowski, Bartlomiej ^a,d   Fearnley, Ian M ^a   Prime, Tracy A ^a   Murphy, Michael P ^a   James, Andrew M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITASE; CYSTEINE RESIDUES; FEEDBACK SIGNAL; LOW LEVEL; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL METABOLISM; MITOCHONDRIAL RESPIRATION; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATE DEHYDROGENASE KINASE; REACTIVE OXYGEN SPECIES; RESPIRATORY CHAINS; REVERSIBLE OXIDATION; SUPEROXIDES; TCA CYCLE; TRICARBOXYLIC ACIDS;

AMINO ACIDS; BYPRODUCTS; CARBOHYDRATES; ENZYME ACTIVITY; HYDROGEN PEROXIDE;

OXYGEN;

ACONITATE HYDRATASE; CYSTEINE; HYDROGEN PEROXIDE; PYRUVATE DEHYDROGENASE KINASE 2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; MITOCHONDRION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN;

ADENOSINE TRIPHOSPHATE; ANIMALS; CITRIC ACID CYCLE; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PYRUVATE DEHYDROGENASE COMPLEX; RATS; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84867407574     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.400002     Document Type: Article

References (31)

1. Murphy, M. P. (2009) How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13
2. Janssen-Heininger, Y. M., Mossman, B. T., Heintz, N. H., Forman, H. J., Kalyanaraman, B., Finkel, T., Stamler, J. S., Rhee, S. G., and van der Vliet, A. (2008) Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic. Biol. Med. 45, 1-17
3. Hurd, T. R., Prime, T. A., Harbour, M. E., Lilley, K. S., and Murphy, M. P. (2007) Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J. Biol. Chem. 282, 22040-22051 (Pubitemid 47195755)
4. Rhee, S. G. (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883
5. D'Autréaux, B., and Toledano, M. B. (2007) ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813-824 (Pubitemid 47462134)
6. 2 for platelet-derived growth factor signal transduction. Science 270, 296-299
7. Veal, E. A., Day, A. M., and Morgan, B. A. (2007) Hydrogen peroxide sensing and signaling. Mol. Cell 26, 1-14 (Pubitemid 46578115)
8. Patel, M. S., and Korotchkina, L. G. (2006) Regulation of the pyruvate dehydrogenase complex. Biochem. Soc. Trans. 34, 217-222
9. Randle, P. J. (1995) Metabolic fuel selection: general integration at the whole-body level. Proc. Nutr. Soc. 54, 317-327
10. Yeaman, S. J., Hutcheson, E. T., Roche, T. E., Pettit, F. H., Brown, J. R., Reed, L. J., Watson, D. C., and Dixon, G. H. (1978) Sites of phosphorylation on pyruvate dehydrogenase from bovine kidney and heart. Biochemistry 17, 2364-2370 (Pubitemid 8365757)
11. Roche, T. E., Baker, J. C., Yan, X., Hiromasa, Y., Gong, X., Peng, T., Dong, J., Turkan, A., and Kasten, S. A. (2001) Distinct regulatory properties of pyruvate dehydrogenase kinase and phosphatase isoforms. Prog. Nucleic Acid Res. Mol. Biol. 70, 33-75
12. Bowker-Kinley, M. M., Davis, W. I., Wu, P., Harris, R. A., and Popov, K. M. (1998) Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem. J. 329, 191-196 (Pubitemid 28022308)
13. Makmura, L., Hamann, M., Areopagita, A., Furuta, S., Muñoz, A., and Momand, J. (2001) Development of a sensitive assay to detect reversibly oxidized protein cysteine sulfhydryl groups. Antioxid. Redox Signal. 3, 1105-1118 (Pubitemid 34027366)
14. Rardin, M. J., Wiley, S. E., Naviaux, R. K., Murphy, A. N., and Dixon, J. E. (2009) Monitoring phosphorylation of the pyruvate dehydrogenase complex. Anal. Biochem. 389, 157-164
15. Cochemé, H. M., and Murphy, M. P. (2008) Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283, 1786-1798
16. Thor, H., Smith, M. T., Hartzell, P., Bellomo, G., Jewell, S. A., and Orrenius, S. (1982) The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes: a study of the implications of oxidative stress in intact cells. J. Biol. Chem. 257, 12419-12425 (Pubitemid 13180138)
17. Cox, A. G., Pullar, J. M., Hughes, G., Ledgerwood, E. C., and Hampton, M. B. (2008) Oxidation of mitochondrial peroxiredoxin 3 during the initiation of receptor-mediated apoptosis. Free Radic. Biol. Med. 44, 1001-1009
18. Popp, D. A., Kiechle, F. L., Kotagal, N., and Jarett, L. (1980) Insulin stimulation of pyruvate dehydrogenase in an isolated plasma membrane- mitochondrial mixture occurs by activation of pyruvate dehydrogenase phosphatase. J. Biol. Chem. 255, 7540-7543
19. Knoechel, T. R., Tucker, A. D., Robinson, C. M., Phillips, C., Taylor, W., Bungay, P. J., Kasten, S. A., Roche, T. E., and Brown, D. G. (2006) Regulatory roles of the N-terminal domain based on crystal structures of human pyruvate dehydrogenase kinase 2 containing physiological and synthetic ligands. Biochemistry 45, 402-415 (Pubitemid 43100407)
20. Whitehouse, S., Cooper, R. H., and Randle, P. J. (1974) Mechanism of activation of pyruvate dehydrogenase by dichloroacetate and other halogenated carboxylic acids. Biochem. J. 141, 761-774
21. Popov, K. M., Kedishvili, N. Y., Zhao, Y., Gudi, R., and Harris, R. A. (1994) Molecular cloning of the p45 subunit of pyruvate dehydrogenase kinase. J. Biol. Chem. 269, 29720-29724 (Pubitemid 24365131)
22. Hausladen, A., and Fridovich, I. (1994) Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J. Biol. Chem. 269, 29405-29408 (Pubitemid 24365084)
23. Green, T., Grigorian, A., Klyuyeva, A., Tuganova, A., Luo, M., and Popov, K. M. (2008) Structural and functional insights into the molecular mechanisms responsible for the regulation of pyruvate dehydrogenase kinase 2. J. Biol. Chem. 283, 15789-15798
24. Kato, M., Chuang, J. L., Tso, S. C., Wynn, R. M., and Chuang, D. T. (2005) Crystal structure of pyruvate dehydrogenase kinase 3 bound to lipoyl domain 2 of human pyruvate dehydrogenase complex. EMBO J. 24, 1763-1774 (Pubitemid 40769496)
25. Wynn, R. M., Kato, M., Chuang, J. L., Tso, S. C., Li, J., and Chuang, D. T. (2008) Pyruvate dehydrogenase kinase-4 structures reveal a metastable open conformation fostering robust core-free basal activity. J. Biol. Chem. 283, 25305-25315
26. Li, J., Kato, M., and Chuang, D. T. (2009) Pivotal role of the C-terminal DW-motif in mediating inhibition of pyruvate dehydrogenase kinase 2 by dichloroacetate. J. Biol. Chem. 284, 34458-34467
27. Steussy, C. N., Popov, K. M., Bowker-Kinley, M. M., Sloan, R. B., Jr., Harris, R. A., and Hamilton, J. A. (2001) Structure of pyruvate dehydrogenase kinase: novel folding pattern for a serine protein kinase. J. Biol. Chem. 276, 37443-37450
28. James, A. M., Collins, Y., Logan, A., and Murphy, M. P. (2012) Mitochondrial oxidative stress and the metabolic syndrome. Trends Endocrinol. Metab. 23, 429-434
29. Li, Y., Huang, T. T., Carlson, E. J., Melov, S., Ursell, P. C., Olson, J. L., Noble, L. J., Yoshimura, M. P., Berger, C., Chan, P. H., Wallace, D. C., and Epstein, C. J. (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376-381
30. Hoehn, K. L., Salmon, A. B., Hohnen-Behrens, C., Turner, N., Hoy, A. J., Maghzal, G. J., Stocker, R., Van Remmen, H., Kraegen, E. W., Cooney, G. J., Richardson, A. R., and James, D. E. (2009) Insulin resistance is a cellular antioxidant defense mechanism. Proc. Natl. Acad. Sci. U.S.A. 106, 17787-17792
31. Rodriguez-Cuenca, S., Cochemé, H. M., Logan, A., Abakumova, I., Prime, T. A., Rose, C., Vidal-Puig, A., Smith, A. C., Rubinsztein, D. C., Fearnley, I. M., Jones, B. A., Pope, S., Heales, S. J., Lam, B. Y., Neogi, S. G., McFarlane, I., James, A. M., Smith, R. A., and Murphy, M. P. (2010) Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice. Free Radic. Biol. Med. 48, 161-172