The structure and function of the brown fat uncoupling protein UCP1: Current status

BioFactors

Volumn 8, Issue 3-4, 1998, Pages 209-219

  Rial, Eduardo ^a   González Barroso, M Mar ^a   Fleury, Christophe ^b   Bouillaud, Frédéric ^b  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

UNCOUPLING PROTEIN;

BROWN ADIPOSE TISSUE; CATALYSIS; GENE EXPRESSION REGULATION; METABOLIC RATE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; RESPIRATORY CHAIN; REVIEW; TISSUE SPECIFICITY;

MAMMALIA;

EID: 2442753376     PISSN: 09516433     EISSN: None     Source Type: Journal    
DOI: 10.1002/biof.5520080307     Document Type: Review

References (88)

1. D.F.S. Rolfe and G.C. Brown, Cellular energy utilization and molecular origin of standard metabolic rate in mammals, Physiol. Rev. 77 (1997), 731-758.
2. D.G. Nicholls and R.M. Locke, Thermogenic mechanisms in brown fat, Physiol. Rev. 64 (1984), 1-64.
3. B. Cannon, D.G. Nicholls and O. Lindberg, Purine nucleotides and fatty acids in energy coupling of mitochondria from brown adipose tissue, in: Mechanisms in Bioenergetics, G.F. Azzone, L. Ernster, S. Papa, E. Quagliariello and N. Siliprandi, eds, Academic Press, New York, 1973, pp. 357-363.
4. C. Fleury, M. Neverova, S. Collins, S. Raimbault, O. Champigny, C. Levi-Meyrueis, F. Bouillaud, M.F. Seldin, R.S. Surwit, D. Ricquier and C.H. Warden, Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia, Nature Genetics 15 (1997), 269-272.
5. O. Boss, S. Samec, A. Paoloni-Giacobino, C. Rossier, A. Dulloo, J. Seydoux, P. Muzzin and J.P. Giacobino, Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression, FEBS Lett. 408 (1997), 39-42.
6. M. Laloi, M. Klein, J.W. Riesmeier, B. Müller-Röber, C. Fleury, F. Bouillaud and D. Ricquier, A plant cold-induced uncoupling protein, Nature 389 (1997), 135-136.
7. D. Ricquier, F. Bouillaud, P. Toumelin, G. Mory, R. Bazin, J. Arch and L. Penicaud, Expression of uncoupling protein mRNA in thermogenic or weakly thermogenic brown adipose tissue: evidence for a rapid β-adrenoreceptor-mediated and transcriptionally regulated step during activation of thermogenesis, J. Biol. Chem. 261 (1986), 13 905-13 910.
8. A.M. Cassard-Doulcier, M. Larose, J.C. Matamala, O. Champigny, F. Bouillaud and D. Ricquier, In vitro interactions between nuclear proteins and uncoupling protein gene promoter reveal several putative transactivating factors including Ets1, retinoid X receptor, thyroid hormone receptor, and a CACCC box-binding protein, J. Biol. Chem. 269 (1994), 24 335-24 342.
9. R. Alvarez, J. De Andrés, P. Yubero, O. Viñas, T. Mampel, R. Iglesias, M. Giralt and F. Villarroya, A novel regulatory pathway of brown fat thermogenesis. Retinoic acid is a transcriptional activator of the mitochondrial uncoupling protein gene, J. Biol. Chem. 270 (1995), 5666-5673.
10. J.E. Silva and R. Rabelo, Regulation of the uncoupling protein gene expression, Eur. J. Endocrin. 136 (1997), 251-264.
11. M. Larose, A.M. Cassard-Doulcier, C. Fleury, F. Serra, O. Champigny, F. Bouillaud and D. Ricquier, Essential cis-acting elements in rat uncoupling protein gene are in an enhancer containing a complex retinoic acid response domain, J. Biol. Chem. 271 (1996), 31 533-31 542.
12. D.G. Nicholls, Hamster brown-adipose-tissue mitochondria: purine nucleotide control of the ion conductance of the inner membrane, the nature of the nucleotide binding site, Eur. J. Biochemistry 62 (1976), 223-228.
13. E. Rial, A. Poustie and D.G. Nicholls, Brown adipose tissue mitochondria: the regulation of the 32000 Mr uncoupling protein by fatty acids and purine nucleotides, Eur. J. Biochem. 137 (1983), 197-203.
14. S. Cunningham, H. Wiesinger and D.G. Nicholls, Quantification of fatty acid activation of the uncoupling protein in adipocytes and mitochondria from guinea-pig, Eur. J. Biochem. 157 (1986), 415-420.
15. + transport activity of the reconstituted uncoupling protein, J. Biol. Chem. 269 (1994), 2508-2515.
16. P. Jezek, D.E. Orosz, M. Modriansky and K.D. Garlid, Transport of anions and protons by the mitochondrial uncoupling protein and its regulation by nucleotides and fatty acids. A new look at old hypotheses, J. Biol. Chem. 269 (1994), 26 184-26 190.
17. M.M. González-Barroso, C. Fleury, I. Arechaga, P. Zaragoza, C. Levi-Meyrueis, S. Raimbault, D. Ricquier, F. Bouillaud and E. Rial, Activation of the uncoupling protein by fatty acids is modulated by mutations in the C-terminal region of the protein, Eur. J. Biochem. 239 (1996), 445-450.
18. K.D. Garlid, D.E. Orosz, M. Modriansky, S. Vassanelli and P. Jezek, On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein, J. Biol. Chem. 271 (1996), 2615-2620.
19. R.M. Locke, E. Rial and D.G. Nicholls, The acute regulation of mitochondrial proton conductance in cells and mitochondria from the brown fat of cold-adapted and warm-adapted guinea-pigs, Eur. J. Biochem. 129 (1982), 381-387.
20. R.M. Locke, E. Rial, I.D. Scott and D.G. Nicholls, Fatty acids as acute regulators of the proton conductance of hamster brown fat mitochondria, Eur. J. Biochem. 129 (1982), 373-380.
21. A.Y. Andreyev, T.O. Bondareva, V.I. Dedukhova, E.N. Mokhova, V.P. Skulachev and N.I. Volkov, Carboxyatractylate inhibits the uncoupling effect of free fatty acids, FEBS Lett. 226 (1988), 265-269.
22. A.Y. Andreyev, T.O. Bondareva, V.I. Dedukhova, E.N. Mokhova, V.P. Skulachev, L.M. Tsofina, N.I. Volkov and T.V. Vygodina, The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria, Eur. J. Biochem. 182 (1989), 585-592.
23. V.P. Skulachev, Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation, FEBS Lett. 294 (1991), 158-162.
24. M.R. Wiçckowski and L. Wojtczak, Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria, Biochem. Biophys. Res. Comm. 232 (1997), 414-417.
25. V.N. Samartsev, A.V. Smirnov, I.P. Zeldi, O.V. Markova, E.N. Mokhova and V.P. Skulachev, Involvement of aspartate/glutamate antiporter in fatty acid-induced uncoupling of liver mitochondria, Biochim. Biophys. Acta 1319 (1997), 251-257.
26. + transport by uncoupling protein (UCP-1) is dependent on a histidine pair, absent in UCP-2 and UCP-3, Biochemistry 37 (1998), 3-8.
27. M.M. González-Barroso, C. Fleury, F. Bouillaud, D.G. Nicholls and E. Rial, 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 (1998), 15 528-15 532.
28. M. Desautels, G. Zabor-Behrens and J. Himms-Hagen, Increased purine nucleotide binding, altered polypeptide composition, and thermogenesis in brown adipose tissue mitochondria of cold-acclimated rats, Can. J. Biochem. 56 (1978), 378-383.
29. M. Desautels and J. Himms-Hagen, Roles of noradrenaline and protein synthesis in the cold-induced increase in purine nucleotide binding by rat brown adipose tissue mitochondria, Can. J. Biochem. 51 (1979), 968-976.
30. M. Desautels and J. Himms-Hagen, Parallel regression of cold-induced changes in ultra-structure, composition, and properties of brown adipose tissue mitochondria during recovery of rats from acclimation to cold, Can. J. Biochem. 58 (1980), 1057-1068.
31. S.G. Huang and M. Klingenberg, Nature of the masking of nucleotide-binding sites in brown adipose tissue mitochondria: involvement of endogenous adenosine triphosphate, Eur. J. Biochem. 229 (1995), 718-725.
32. Y. Shinohara, A. Shima, M. Kamida and H. Terada, Uncoupling protein is expressed in liver mitochondria of cold-exposed and newborn rats, FEBS Lett. 293 (1991), 173-174.
33. D. Ricquier, S. Raimbault, O. Champigny, B. Miroux and F. Bouillaud, Comment to Shinohara et al., FEBS Lett. 293 (1991), 173-174; The uncoupling protein is not expressed in rat liver, FEBS Lett. 303 (1992), 103-106.
34. D. Ricquier, S. Raimbault, O. Champigny, B. Miroux and F. Bouillaud, Comment to Shinohara et al., FEBS Lett. 293 (1991), 173-174; The uncoupling protein is not expressed in rat liver, FEBS Lett. 303 (1992), 103-106.
35. S. Enerback, A. Jacobsson, E.M. Simpson, C. Guerra, H. Yamashita, M.E. Harper and L.P. Kozak, Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese, Nature 387 (1997), 90-94.
36. T. Masaki, H. Yoshimatsu, T. Kakuma, S. Hidaka, M. Kurokawa and T. Sakata, Enhanced expression of uncoupling protein 2 gene in rat white adipose tissue and skeletal muscle following chronic treatment with thyroid hormone, FEBS Lett. 418 (1997), 323-326.
37. D.W. Gong, Y. He, M. Kara and M. Reitman, Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin, J. Biol. Chem. 272 (1997), 24 129-24 132.
38. O. Boss, S. Samec, D. Desplanches, M.H. Mayet, J. Seydoux, P. Muzzin and J.P. Giacobino, Effect of endurance training on mRNA expression of uncoupling proteins 1, 2, and 3 in the rat, FASEB J. 12 (1998), 335-339.
39. Y.T. Zhou, M. Shimabukuro, K. Koyama, Y. Lee, M.Y. Wang, F. Trieu, C.B. Newgard and R.H. Unger, Induction by leptin of uncoupling protein-2 and enzymes of fatty acid oxidation, Proc. Natl. Acad. Sci. USA 94 (1997), 6386-6390.
40. C. Bouchard, L. Pérusse, Y.C. Chagnon, C. Warden and D. Ricquier, Linkage between markers in the vicinity of the uncoupling protein 2 gene and resting metabolic rate in humans, Human Mol. Gen. 6 (1997), 1887-1889.
41. S.C. Elbein, M. Leppert and S. Hasstedt, Uncoupling protein 2 region on chromosome 11q13 is not linked to markers of obesity in familial type 2 diabetes, Diabetes 46 (1997), 2105-2107.
42. S. Larkin, E. Mull, W. Miao, R. Pittner, K. Albrandt, C. Moore, A. Young, M. Denaro and K. Beaumont, Regulation of the third member of the uncoupling protein family, UCP3, by cold and thyroid hormone, Biochem. Biophys. Res. Comm. 240 (1997), 222-227.
43. L. Millet, H. Vidal, F. Andreelli, D. Larrouy, J.P. Riou, D. Ricquier, M. Laville and D. Langin, Increased uncoupling protein-2 and -3 mRNA expression during fasting in obese and lean humans, J. Clin. Invest. 100 (1997), 2665-2670.
44. O. Boss, S. Samec, F. Kuhne, P. Bijlenga, F. Assimacopoulos-Jeannet, J. Seydoux, J.P. Giacobino and P. Muzzin, Uncoupling protein-3 expression in rodent skeletal muscle is modulated by food intake but not by change in environmental temperature, J. Biol. Chem. 273 (1998), 5-8.
45. D.S. Weigle, L.E. Selfridge, M.W. Schwartz, R.J. Seeley, D.E. Cummings, P.J. Havel, J.L. Kuijper and H. Beltran Río, Elevated free fatty acids induce uncoupling protein 3 expression in muscle: a potential explanation for the effect of fasting, Diabetes 47 (1998), 298-302.
46. H. Aquila, T.A. Link and M. Klingenberg, Solute carriers involved in energy transfer of mitochondria form a homologous protein family, FEBS Lett. 212 (1987), 1-9.
47. J.E. Walker and M.J. Runswick, The mitochondrial transport protein superfamily, J. Bioenerg. Biomembr. 25 (1993), 435-446.
48. J. Kuan and M.H. Saier, The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships, Crit. Rev. Biochem. Mol. Biol. 28 (1993), 209-223.
49. B. El Moualij, C. Duyckaerts, J. Lamotte-Brasseur and F.E. Sluse, Phylogenetic classification of the mitochondrial carrier family of Saccharomyces cerevisiae, Yeast 13 (1997), 573-581.
50. F. Palmieri, C. Indiveri, F. Bisaccia and R. Krämer, Functional properties of purified and reconstituted mitochondrial metabolite carriers, J. Bioenerg. Biomembr. 25 (1993), 525-535.
51. C. Indiveri, L. Palmieri and F. Palmieri, Characterization of the unidirectional transport of carnitine catalyzed by the reconstituted carnitine carrier from rat liver mitochondria, Biochim. Biophys. Acta 1069 (1991), 110-116.
52. + translocator, EMBO J. 4 (1985), 3087-3092.
53. E. Rial, I. Aréchaga, E. Sainz-de-la-Maza and D.G. Nicholls, Effect of Hydrophobic sulphydryl reagents on the uncoupling protein and inner-membrane anion channel of brown-adipose-tissue mitochondria, Eur. J. Biochem. 182 (1989), 187-193.
54. T. Dierks, A. Salentin, C. Heberger and R. Krämer, The mitochondrial aspartate/glutamate and ADP/ATP carrier switch from obligate counterexchange to unidirectional transport after modification by SH-reagents, Biochim. Biophys. Acta 1028 (1990), 268-280.
55. T. Dierks, A. Salentin and R. Krämer, Pore-like and carrier-like properties of the mitochondrial aspartate/glutamte carrier after modification by SH-reagents: evidence for a preformed channel as a structural requirement of carrier-mediated transport, Biochim. Biophys. Acta 1028 (1990), 281-288.
56. C. Indiveri, A. Tonazzi, T. Dierks, R. Krämer and F. Palmieri, The mitochondrial carnitine carrier: characterization of SH-groups relevant for its transport function, Biochim. Biophys. Acta 1140 (1992), 53-58.
57. R. Stappen and R. Krämer, Functional properties of the reconstituted phosphate carrier from bovine heart mitochondria: evidence for asymmetric orientation and characterization of three different transport modes, Biochim. Biophys. Acta 1149 (1993), 40-48.
58. K. Herick and R. Krämer, Kinetic and energetic characterization of solute flux through the reconstituted aspartate/glutamate carrier from beef heart mitochondria after modification with mercurials, Biochim. Biophys. Acta 1238 (1995), 63-71.
59. T. Dierks, R. Stappen and R. Krämer, Channel properties of mitochondrial carriers, in: Molecular Biology of Mitochondrial Transport Systems, M. Forte and M. Colombini, eds, Springer-Verlag, Berlin, 1994, pp. 117-129.
60. R.M. Krupka, Interpreting the effects of specific protein modification on antiport coupling mechanism: the case of the aspartate/glutamate exchanger, Biochim. Biophys. Acta 1236 (1995), 1-9.
61. 2+, Biochemistry 35 (1996), 8483-8488.
62. K. Herick, R. Krämer and H. Lühring, Patch clamp investigation into the phosphate carrier from Saccharomyces cerevisiae mitochondria, Biochim. Biophys. Acta 1321 (1997), 207-220.
63. S.G. Huang and M. Klingenberg, Chloride channel properties of the uncoupling protein from brown adipose tissue mitochondria: a patch-clamp study, Biochemistry 35 (1996), 16 806-16 814.
64. M.M. González-Barroso, C. Fleury, C. Levi-Meyrueis, P. Zaragoza, F. Bouillaud and E. Rial, Deletion of amino acids 261-269 in the brown fat uncoupling protein converts the carrier into a pore, Biochemistry 36 (1997), 10 930-10 935.
65. V. Petronilli, C. Cola, S. Massari, R. Colonna and P. Bernardi, Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria, J. Biol. Chem. 268 (1993), 21 939-24 945.
66. G. Beutner, A. Rück, B. Riede, W. Weite and D. Brdiczka, Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore, FEBS Lett. 396 (1996), 189-195.
67. A.P. Halestrap, K.Y. Woodfield and C.P. Connern, Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase, J. Biol. Chem. 272 (1997), 3346-3354.
68. G. Kroemer, P. Petit, N. Zamzani, J.L. Vayssière and B. Mignotte, The biochemistry of programmed cell death, FASEB J. 9 (1995), 1277-1287.
69. F. Palmieri, Mitochondrial carrier proteins, FEBS Lett. 346 (1994), 48-54.
70. B. Miroux, V. Frossard, S. Raimbault, D. Ricquier and F. Bouillaud, The topology of the brown adipose tissue mitochondrial uncoupling protein determined with antibodies against its antigenic sites revealed by a library af fusion proteins, EMBO J. 12 (1993), 3739-3745.
71. C. Eckerskorn and M. Klingenberg, In the uncoupling protein from brown adipose tissue the C-terminus protudes to the c-side of the membrane as shown by tryptic cleavage, FEBS Lett. 226 (1987), 166-170.
72. E. Rial, A. Muga, J.M. Valpuesta, J.L.R. Arrondo and P.M. Goñi, Infrared spectroscopic studies of detergent-solubilized uncoupling protein from brown-adipose-tissue mitochondria, Eur. J. Biochem. 188 (1990), 83-89.
73. + transport inhibition of the uncoupling protein from brown adipose tissue mitochondrial, Biochemistry 35 (1996), 7846-7854.
74. P. Mayinger and M. Klingenberg, Labeling of two different regions of the nucleotide binding site of the uncoupling protein from brown adipose tissue mitochondria with two ATP analogs, Biochemistry 31 (1992), 10 536-10 543.
75. E. Winkler and M. Klingenberg, Photoaffinity labeling of the nucleotide-binding site of the uncoupling protein from hamster brown adipose tissue, Eur. J. Biochem. 203 (1992), 295-304.
76. F. Bouillaud, I. Arechaga, P.X. Petit, S. Raimbault, C. Levi-Meyrueis, L. Casteilla, M. Laurent, E. Rial and D. Ricquier, A sequence related to a DNA recognition element is essential for the inhibition by nucleotides of proton transport throug the mitochondrial uncoupling protein, EMBO J. 13 (1994), 1990-1997.
77. B. Miroux, L. Casteilla, S. Klaus, S. Raimbault, S. Grandin, J.M. Clément, D. Ricquier and F. Bouillaud, Antibodies selected from whole antiserum by fusion proteins as tools for the study of the topology of mitochondrial membrane proteins, J. Biol. Chem. 267 (1992), 13 603-13 609.
78. F. Bouillaud, L. Casteilla and D. Ricquier, A conserved domain in mitochondrial transporters is homologous to a zinc-finger knuckle of nuclear hormone receptors, Mol. Biol. Evolut. 9 (1992), 970-975.
79. E. Majima, H. Koike, Y.M. Hong, Y. Shinohara and H. Terada, Characterization of cysteine residues of mitochondrial ADP/ATP carrier with the SH-reagents eosin-5-maleimide and N-ethylmaleimide, J. Biol. Chem. 268 (1993), 22 181-22 187.
80. L. Capobianco, F. Bisaccia, M. Mazzeo and F. Palmieri, The mitochondrial oxoglutarate carrier: sulfhydryl reagents bind to cysteine-184, and this interaction is enhanced by substrate binding, Biochemistry 35 (1996), 8974-8980.
81. E. Majima, Y. Shinohara, N. Yamaguchi, Y.M. Hong and H. Terada, Importance of loops of mitochondrial ADP/ATP carrier for its transport activity deduced from reactivities of its cysteine residues with the sulfhydryl reagent eosin-5-maleimide, Biochemistry 33 (1994), 9530-9536.
82. E. Majima, K. Ikawa, M. Takeda, M. Hashimoto, Y. Shinohara and H. Terada, Translocation of loops regulates transport activity of mitochondrial ADP-ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenanthroline, J. Biol. Chem. 270 (1995), 29 548-29 554.
83. E. Majima, N. Yamaguchi, H. Chuman, Y. Shinohara, M. Ishida, S. Goto and H. Terada, Binding of the fluorescein derivative eosin Y to the mitochondrial ADP/ATP carrier: characterization of the adenine nucleotide binding site, Biochemistry 37 (1998), 424-432.
84. + transport, J. Biol. Chem. 269 (1994), 7435-7438.
85. M. Modrianský, D. Murdza-Inglis, H.V. Patel, K.B. Freeman and K.D. Garlid, Identification by site-directed mutagenesis of three arginines in uncoupling protein that are essential for nucleotide binding and inhibition, J. Biol. Chem. 272 (1997), 24 759-24 762.
86. E. Winkler, E. Wachter and M. Klingenberg, Identification of the pH sensor for nucleotide binding in the uncoupling protein from brown adipose tissue, Biochemistry 36 (1997), 148-155.
87. K.S. Echtay, M. Bienengraeber and M. Klingenberg, Mutagenesis of the uncoupling protein of brown adipose tissue. Neutralization of E190 largely abolishes pH control of nucleotide binding, Biochemistry 36 (1997), 8253-8260.
88. P. Jezek, M. Modrianský and K.D. Garlid, A structure-activity study of fatty acid interaction with mitochondrial uncoupling protein, FEBS Lett. 408 (1997), 166-170.