Synergy of fatty acid and reactive alkenal activation of proton conductance through uncoupling protein 1 in mitochondria

Biochemical Journal

Volumn 395, Issue 3, 2006, Pages 619-628

  Esteves, Telma C ^a   Parker, Nadeene ^a   Brand, Martin D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

4 hydroxy 2 nonenal (4 HNE); Fatty acid; Mitochondria; Proton leak; Saccharomyces cerevisiae; Uncoupling protein 1 (UCP1)

Indexed keywords

BIOCHEMISTRY; BIODIVERSITY; PHYSIOLOGICAL MODELS; PROTEINS; TISSUE; YEAST;

4-HYDROXY-2-NONENAL (4-HNE; MITOCHONDRIA; PROTON LEAK; SACCHAROMYCES CEREVISIAE; UNCOUPLING PROTEIN 1 (UCP1);

FATTY ACIDS;

4 HYDROXYNONENAL; CINNAMIC ACID; FATTY ACID DERIVATIVE; GUANOSINE DIPHOSPHATE; PALMITIC ACID; PLASMID VECTOR; PROTON; UNCOUPLING PROTEIN 1;

ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; FEMALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON TRANSPORT; RAT; SACCHAROMYCES CEREVISIAE; YEAST;

ADIPOSE TISSUE, BROWN; ALDEHYDES; ALKENES; ANIMALS; CARRIER PROTEINS; CATTLE; ELECTRIC CONDUCTIVITY; FATTY ACIDS; ION CHANNELS; KINETICS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PLANT OILS; PROTEIN BINDING; PROTONS; RATS; SACCHAROMYCES CEREVISIAE; SERUM ALBUMIN, BOVINE;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 33646251863     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20052004     Document Type: Article

References (35)

1. Halliwell, B. and Gutteridge, J. M. C. (1999) Free Radicals in Biology and Medicine, Oxford University Press, Oxford, U.K.
2. Allen, R. G. and Tresini, M. (2000) Oxidative stress and gene regulation. Free Radical Biol. Med. 28, 463-499
3. Echtay, K. S., Esteves, T. C., Pakay, J. L., Jekabsons, M. B., Lambert, A. J., Portero-Otin, M., Pamplona, R., Vidal-Puig, A., Wang, S., Roebuck, S. J. et al. (2003) A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22, 4103-4110
4. Skulachev, V. P. (1998) Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta 1363, 100-124
5. Brand, M. D. and Esteves, T. C. (2005) Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2, 85-93
6. Cannon, B. and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359
7. Echtay, K. S., Roussel, D., St-Pierre, J., Jekabsons, M. B., Cadenas, S., Stuart, J. A., Harper, J. A., Roebuck, S. J., Morrison, A., Pickering, S. et al. (2002) Superoxide activates mitochondrial uncoupling proteins. Nature (London) 415, 96-99
8. Echtay, K. S., Winkler, E. and Klingenberg, M. (2000) Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature (London) 408, 609-613
9. + transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc. Natl. Acad. Sci. U.S.A. 98, 1416-1421
10. Murphy, M. P., Echtay, K. S., Blaikie, F. H., Asin-Cayuela, J., Cocheme, H. M., Green, K., Buckingham, J. A., Taylor, E. R., Hurrell, F., Hughes, G. et al. (2003) Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation. J. Biol. Chem. 278, 48534-48545
11. Esteves, T. C., Echtay, K. S., Jonassen, T., Clarke, C. F. and Brand, M. D. (2004) Ubiquinone is not required for proton conductance by uncoupling protein 1 in yeast mitochondria. Biochem. J. 379, 309-315
12. Esteves, T. C. and Brand, M. D. (2005) The reactions catalysed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim. Biophys. Acta 1709, 35-44
13. Rial, E., González-Barroso, M., Fleury, C., Iturrizaga, S., Sanchis, D., Jimenez-Jimenez, J., Ricquier, D., Goubern, M. and Bouillaud, F. (1999) Retinoids activate proton transport by the uncoupling proteins UCP1 and UCP2. EMBO J. 18, 5827-5833
14. Krauss, S., Zhang, C. Y. and Lowell, B. B. (2002) A significant portion of mitochondrial proton leak in intact thymocytes depends on expression of UCP2. Proc. Natl. Acad. Sci. U.S.A. 99, 118-122
15. Proft, M., Kotter, P., Hedges, D., Bojunga, N. and Entian, K. D. (1995) CAT5, a new gene necessary for derepression of gluconeogenic enzymes in Saccharomyces cerevisiae. EMBO J. 14, 6116-6126
16. Harper, A. J. (2002) Expression and characterization of the uncoupling proteins in yeast. Ph.D. thesis, University of Cambridge, Cambridge, U.K., p. 76
17. Stuart, J. A., Harper, J. A., Brindle, K. M., Jekabsons, M. B. and Brand, M. D. (2001) A mitochondrial uncoupling artifact can be caused by expression of uncoupling protein 1 in yeast. Biochem. J. 356, 779-789
18. Brand, M. D. (1995) Measurement of mitochondrial proton motive force. In Bioenergetics - A Practical Approach (Brown, G. C. and Cooper, C. E., eds.), pp. 39-62, IRL Press, Oxford, U.K.
19. 2 solubility in aqueous media determined by a kinetic method. Anal. Biochem. 145, 406-418
20. Cornwall, E. J. (2004) The role of the adenine nucleotide translocase in mitochondrial proton leak. Ph.D. thesis, University of Cambridge, Cambridge, U.K., pp. 100-104
21. Richieri, G. V., Ogata, R. T. and Kleinfeld, A. M. (1992) A fluorescently labeled intestinal fatty acid binding protein. Interactions with fatty acids and its use in monitoring free fatty acids. J. Biol. Chem. 267, 23495-23501
22. Rolfe, D. F. S., Hulbert, A. J. and Brand, M. D. (1994) Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat. Biochim. Biophys. Acta 1188, 405-416
23. González-Barroso, M. M., Fleury, C., Bouillaud, F., Nicholls, D. G. and Rial, E. (1998) The uncoupling protein UCP1 does not increase the proton conductance of the inner mitochondrial membrane by functioning as a fatty acid anion transporter. J. Biol. Chem. 273, 15528-15532
24. Arechaga, I., Raimbault, S., Prieto, S., Levi-Meyrueis, C., Zaragoza, P., Miroux, B., Ricquier, D., Bouillaud, F. and Rial, E. (1993) Cysteine residues are not essential for uncoupling protein function. Biochem. J. 296, 693-700
25. Tomás, P., Jimenez-Jimenez, J., Zaragoza, P., Vuligonda, V., Chandraratna, R. A. and Rial, E. (2004) Activation by retinoids of the uncoupling protein UCP1. Biochim. Biophys. Acta 1658, 157-164
26. Garlid, K. D., Orosz, D. E., Modriansky, M., Vassanelli, S. and Jezek, P. (1996) On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein. J. Biol. Chem. 271, 2615-2620
27. Skulachev, V. P. (1999) Anion carriers in fatty acid-mediated physiological uncoupling. J. Bioenerg. Biomembr. 31, 431-445
28. + transport activity of the reconstituted uncoupling protein. J. Biol. Chem. 269, 2508-2515
29. Klingenberg, M. and Echtay, K. S. (2001) Uncoupling proteins: the issues from a biochemist point of view. Biochim. Biophys. Acta 1504, 128-143
30. Huang, S. G. (2003) Binding of fatty acids to the uncoupling protein from brown adipose tissue mitochondria. Arch. Biochem. Biophys. 412, 142-146
31. Shabalina, I. G., Jacobsson, A., Cannon, B. and Nedergaard, J. (2004) Native UCP1 displays simple competitive kinetics between the regulators purine nucleotides and fatty acids. J. Biol. Chem. 279, 38236-38248
32. Rial, E., Aguirregoitia, E., Jimenez-Jimenez, J. and Ledesma, A. (2004) Alkylsulfonates activate the uncoupling protein UCP1: implications for the transport mechanism. Biochim. Biophys. Acta 1608, 122-130
33. Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L. and Parker, N. (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radical Biol. Med. 37, 755-767
34. St-Pierre, J., Buckingham, J. A., Roebuck, S. J. and Brand, M. D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790
35. Silva, J. P., Shabalina, I. G., Dufour, E., Petrovic, N., Backlund, E. C., Hultenby, K., Wibom, R., Nedergaard, J., Cannon, B. and Larsson, N. G. (2005) SOD2 overexpression: enhanced mitochondrial tolerance but absence of effect on UCP activity. EMBO J. 24, 4061-4070