Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3

Cell Metabolism

Volumn 2, Issue 2, 2005, Pages 85-93

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

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A; FATTY ACID; FREE RADICAL; INSULIN; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; CARRIER PROTEIN; ION CHANNEL; ISOPROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; MITOCHONDRIAL UNCOUPLING PROTEIN 3;

AGING; ATTENUATION; CATALYSIS; CELL DAMAGE; CELL PROTECTION; DEGENERATIVE DISEASE; DIABETES MELLITUS; DRUG TARGETING; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; HUMAN; INSULIN RELEASE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; THERMOGENESIS; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SECRETION;

AGING; ANIMALS; CARRIER PROTEINS; FATTY ACIDS; INSULIN; ION CHANNELS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OBESITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN ISOFORMS; REACTIVE OXYGEN SPECIES; THERMOGENESIS;

EID: 25144476923     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2005.06.002     Document Type: Review

References (98)

1. D. Arsenijevic H. Onuma C. Pecqueur S. Raimbault B.S. Manning B. Miroux E. Couplan M.C. Alves-Guerra M. Goubern R. Surwit et. al. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production Nat. Genet. 26 2000 435-439
2. J. Blanc M.C. Alves-Guerra B. Esposito S. Rousset P. Gourdy D. Ricquier A. Tedgui B. Miroux Z. Mallat Protective role of uncoupling protein 2 in atherosclerosis Circulation 107 2003 388-390
3. O. Boss T. Hagen B.B. Lowell Uncoupling proteins 2 and 3: Potential regulators of mitochondrial energy metabolism Diabetes 49 2000 143-156
4. O. Boss S. Samec A. Dulloo J. Seydoux P. Muzzin J.P. Giacobino Tissue-dependent upregulation of rat uncoupling protein-2 expression in response to fasting or cold FEBS Lett. 412 1997 111-114
5. O. Boss S. Samec A. Paoloni-Giacobino C. Rossier A. Dulloo J. Seydoux P. Muzzin 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. O. Boss S. Samec F. Kuhne P. Bijlenga F. Assimacopoulos-Jeannet J. Seydoux J.P. Giacobino P. Muzzin Uncoupling protein-3 expression in rodent skeletal muscle is modulated by food intake but not by changes in environmental temperature J. Biol. Chem. 273 1998 5-8
7. M.D. Brand Uncoupling to survive? The role of mitochondrial inefficiency in ageing Exp. Gerontol. 35 2000 811-820
8. M.D. Brand R. Pamplona M. Portero-Otin J.R. Requena S.J. Roebuck J.A. Buckingham J.C. Clapham S. Cadenas Oxidative damage and phospholipid fatty acyl composition in skeletal muscle mitochondria from mice underexpressing or overexpressing uncoupling protein 3 Biochem. J. 368 2002 597-603
9. M.D. Brand C. Affourtit T.C. Esteves K. Green A.J. Lambert S. Miwa J.L. Pakay N. Parker Mitochondrial superoxide: Production, biological effects, and activation of uncoupling proteins Free Radic. Biol. Med. 37 2004 755-767
10. M.D. Brand J.A. Buckingham T.C. Esteves K. Green A.J. Lambert S. Miwa M.P. Murphy J.L. Pakay D.A. Talbot K.S. Echtay Mitochondrial superoxide and aging: Uncoupling-protein activity and superoxide production Biochem. Soc. Symp. 71 2004 203-213
11. S. Cadenas J.A. Buckingham S. Samec J. Seydoux N. Din A.G. Dulloo M.D. Brand UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged FEBS Lett. 462 1999 257-260
12. S. Cadenas K.S. Echtay J.A. Harper M.B. Jekabsons J.A. Buckingham E. Grau A. Abuin H. Chapman J.C. Clapham M.D. Brand The basal proton conductance of skeletal muscle mitochondria from transgenic mice overexpressing or lacking uncoupling protein-3 J. Biol. Chem. 277 2002 2773-2778
13. B. Cannon J. Nedergaard Brown adipose tissue: Function and physiological significance Physiol. Rev. 84 2004 277-359
14. C. Carlsson L.A. Borg N. Welsh Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro Endocrinology 140 1999 3422-3428
15. L. Casteilla M. Rigoulet L. Penicaud Mitochondrial ROS metabolism: modulation by uncoupling proteins IUBMB Life 52 2001 181-188
16. C.B. Chan P.E. MacDonald M.C. Saleh D.C. Johns E. Marban M.B. Wheeler Overexpression of uncoupling protein 2 inhibits glucose-stimulated insulin secretion from rat islets Diabetes 48 1999 1482-1486
17. C.B. Chan D. De Leo J.W. Joseph T.S. McQuaid X.F. Ha F. Xu R.G. Tsushima P.S. Pennefather A.M. Salapatek M.B. Wheeler Increased uncoupling protein-2 levels in beta-cells are associated with impaired glucose-stimulated insulin secretion: Mechanism of action Diabetes 50 2001 1302-1310
18. J.C. Clapham J.R. Arch H. Chapman A. Haynes C. Lister G.B. Moore V. Piercy S.A. Carter I. Lehner S.A. Smith et. al. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean Nature 406 2000 415-418
19. M.J. Considine M. Goodman K.S. Echtay M. Laloi J. Whelan M.D. Brand L.J. Sweetlove Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein J. Biol. Chem. 278 2003 22298-22302
20. H. Cortez-Pinto H. Zhi Lin S. Qi Yang S. Odwin Da Costa A.M. Diehl Lipids up-regulate uncoupling protein 2 expression in rat hepatocytes Gastroenterology 116 1999 1184-1193
21. E. Couplan M. del Mar Gonzalez-Barroso M.C. Alves-Guerra D. Ricquier M. Goubern F. Bouillaud No evidence for a basal, retinoic, or superoxide-induced uncoupling activity of the uncoupling protein 2 present in spleen or lung mitochondria J. Biol. Chem. 277 2002 26268-26275
22. A.G. Dulloo S. Samec Uncoupling proteins: Their roles in adaptive thermogenesis and substrate metabolism reconsidered Br. J. Nutr. 86 2001 123-139
23. C. Duval A. Negre-Salvayre A. Dogilo R. Salvayre L. Penicaud L. Casteilla Increased reactive oxygen species production with antisense oligonucleotides directed against uncoupling protein 2 in murine endothelial cells Biochem. Cell Biol. 80 2002 757-764
24. K.S. Echtay Q. Liu T. Caskey E. Winkler K. Frischmuth M. Bienengraber M. Klingenberg Regulation of UCP3 by nucleotides is different from regulation of UCP1 FEBS Lett. 450 1999 8-12
25. + transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone) Proc. Natl. Acad. Sci. USA 98 2001 1416-1421
26. K.S. Echtay M.P. Murphy R.A. Smith D.A. Talbot M.D. Brand Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants J. Biol. Chem. 277 2002 47129-47135
27. K.S. Echtay D. Roussel J. St-Pierre M.B. Jekabsons S. Cadenas J.A. Stuart J.A. Harper S.J. Roebuck A. Morrison S. Pickering et. al. Superoxide activates mitochondrial uncoupling proteins Nature 415 2002 96-99
28. K.S. Echtay T.C. Esteves J.L. Pakay M.B. Jekabsons A.J. Lambert M. Portero-Otin R. Pamplona A. Vidal-Puig S. Wang S.J. Roebuck M.D. Brand A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling EMBO J. 22 2003 4103-4110
29. Esteves, T.C., and Brand, M.D. (2005). The reactions catalyzed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim. Biophys. Acta. Published online June 27, 2005. doi:10.1016/j.bbabio.2005.06.002
30. C. Fleury M. Neverova S. Collins S. Raimbault O. Champigny C. Levi-Meyrueis F. Bouillaud M.F. Seldin R.S. Surwit D. Ricquier C.H. Warden Uncoupling protein-2: A novel gene linked to obesity and hyperinsulinemia Nat. Genet. 15 1997 269-272
31. K.D. Garlid M. Jaburek P. Jezek Mechanism of uncoupling protein action Biochem. Soc. Trans. 29 2001 803-806
32. R.E. Gimeno M. Dembski X. Weng N. Deng A.W. Shyjan C.J. Gimeno F. Iris S.J. Ellis E.A. Woolf L.A. Tartaglia Cloning and characterization of an uncoupling protein homolog: A potential molecular mediator of human thermogenesis Diabetes 46 1997 900-906
33. F. Goglia V.P. Skulachev A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet FASEB J. 17 2003 1585-1591
34. D.W. Gong Y. He M. Karas M. Reitman Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin J. Biol. Chem. 272 1997 24129-24132
35. D.W. Gong S. Monemdjou O. Gavrilova L.R. Leon B. Marcus-Samuels C.J. Chou C. Everett L.P. Kozak C. Li C. Deng et. al. Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3 J. Biol. Chem. 275 2000 16251-16257
36. M.M. Gonzalez-Barroso C. Fleury F. Bouillaud D.G. Nicholls 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 15528-15532
37. Green, K., Brand, M.D., and Murphy, M.P. (2004). Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 53, Suppl. 1, S110-S118.
38. B. Halliwell J.M.C. Gutteridge Free radicals in biology and medicine 1999 Oxford University Press Oxford
39. J.A. Harper K. Dickinson M.D. Brand Mitochondrial uncoupling as a target for drug development for the treatment of obesity Obes. Rev. 2 2001 255-265
40. J.A. Harper J.A. Stuart M.B. Jekabsons D. Roussel K.M. Brindle K. Dickinson R.B. Jones M.D. Brand Artifactual uncoupling by uncoupling protein 3 in yeast mitochondria at the concentrations found in mouse and rat skeletal-muscle mitochondria Biochem. J. 361 2002 49-56
41. M.E. Harper J. Himms-Hagen Mitochondrial efficiency: Lessons learned from transgenic mice Biochim. Biophys. Acta 1504 2001 159-172
42. M.E. Harper R.M. Dent V. Bezaire A. Antoniou A. Gauthier S. Monemdjou R. McPherson UCP3 and its putative function: Consistencies and controversies Biochem. Soc. Trans. 29 2001 768-773
43. J. Himms-Hagen M.E. Harper Physiological role of UCP3 may be export of fatty acids from mitochondria when fatty acid oxidation predominates: An hypothesis Exp. Biol. Med. (Maywood) 226 2001 78-84
44. Y. Hong B.D. Fink J.S. Dillon W.I. Sivitz Effects of adenoviral overexpression of uncoupling protein-2 and -3 on mitochondrial respiration in insulinoma cells Endocrinology 142 2001 249-256
45. M. Horimoto P. Fulop Z. Derdak J.R. Wands G. Baffy Uncoupling protein-2 deficiency promotes oxidant stress and delays liver regeneration in mice Hepatology 39 2004 386-392
46. T.L. Horvath S. Diano C. Barnstable Mitochondrial uncoupling protein 2 in the central nervous system: Neuromodulator and neuroprotector Biochem. Pharmacol. 65 2003 1917-1921
47. M. Jaburek K.D. Garlid Reconstitution of recombinant uncoupling proteins: UCP1, -2, and -3 have similar affinities for ATP and are unaffected by coenzyme Q10 J. Biol. Chem. 278 2003 25825-25831
48. M. Jaburek M. Varecha R.E. Gimeno M. Dembski P. Jezek M. Zhang P. Burn L.A. Tartaglia K.D. Garlid Transport function and regulation of mitochondrial uncoupling proteins 2 and 3 J. Biol. Chem. 274 1999 26003-26007
49. + translocation by UCP1 is not necessary for uncoupling J. Biol. Chem. 276 2001 31897-31905
50. M. Jaburek S. Miyamoto P. Di Mascio K.D. Garlid P. Jezek Hydroperoxy fatty acid cycling mediated by mitochondrial uncoupling protein UCP2 J. Biol. Chem. 279 2004 53097-53102
51. Jezek, P., Zackova, M., Ruzicka, M., Skobisova, E., and Jaburek, M. (2004). Mitochondrial uncoupling proteins-facts and fantasies. Physiol. Res. 53, Suppl. 1, S199-S211.
52. J.W. Joseph V. Koshkin C.Y. Zhang J. Wang B.B. Lowell C.B. Chan M.B. Wheeler Uncoupling protein 2 knockout mice have enhanced insulin secretory capacity after a high-fat diet Diabetes 51 2002 3211-3219
53. J.W. Joseph V. Koshkin M.C. Saleh W.I. Sivitz C.Y. Zhang B.B. Lowell C.B. Chan M.B. Wheeler Free fatty acid-induced beta-cell defects are dependent on uncoupling protein 2 expression J. Biol. Chem. 279 2004 51049-51056
54. M. Klingenberg K.S. Echtay Uncoupling proteins: The issues from a biochemist point of view Biochim. Biophys. Acta 1504 2001 128-143
55. M. Klingenberg S.G. Huang Structure and function of the uncoupling protein from brown adipose tissue Biochim. Biophys. Acta 1415 1999 271-296
56. S.S. Korshunov V.P. Skulachev A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15-18
57. V. Koshkin X. Wang P.E. Scherer C.B. Chan M.B. Wheeler Mitochondrial functional state in clonal pancreatic beta-cells exposed to free fatty acids J. Biol. Chem. 278 2003 19709-19715
58. A.J. Kowaltowski A.D. Costa A.E. Vercesi Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain FEBS Lett. 425 1998 213-216
59. L.P. Kozak M.E. Harper Mitochondrial uncoupling proteins in energy expenditure Annu. Rev. Nutr. 20 2000 339-363
60. S. Krauss C.Y. Zhang L. Scorrano L.T. Dalgaard J. St-Pierre S.T. Grey B.B. Lowell Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction J. Clin. Invest. 112 2003 1831-1842
61. M. Laloi M. Klein J.W. Riesmeier B. Muller-Rober C. Fleury F. Bouillaud D. Ricquier A plant cold-induced uncoupling protein Nature 389 1997 135-136
62. A.J. Lambert M.D. Brand Superoxide production by NADH:uBiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane Biochem. J. 382 2004 511-517
63. N. Lameloise P. Muzzin M. Prentki F. Assimacopoulos-Jeannet Uncoupling protein 2: A possible link between fatty acid excess and impaired glucose-induced insulin secretion? Diabetes 50 2001 803-809
64. L.X. Li F. Skorpen K. Egeberg I.H. Jorgensen V. Grill Uncoupling protein-2 participates in cellular defense against oxidative stress in clonal beta-cells Biochem. Biophys. Res. Commun. 282 2001 273-277
65. S.S. Liu Generating, partitioning, targeting and functioning of superoxide in mitochondria Biosci. Rep. 17 1997 259-272
66. E.M. Mills M.L. Banks J.E. Sprague T. Finkel Pharmacology: Uncoupling the agony from ecstasy Nature 426 2003 403-404
67. I. Miwa N. Ichimura M. Sugiura Y. Hamada S. Taniguchi Inhibition of glucose-induced insulin secretion by 4-hydroxy-2-nonenal and other lipid peroxidation products Endocrinology 141 2000 2767-2772
68. S. Miwa J. St-Pierre L. Partridge M.D. Brand Superoxide and hydrogen peroxide production by Drosophila mitochondria Free Radic. Biol. Med. 35 2003 938-948
69. M.P. Murphy K.S. Echtay F.H. Blaikie J. Asin-Cayuela H.M. Cocheme K. Green J.A. Buckingham E.R. Taylor F. Hurrell G. Hughes et. al. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation J. Biol. Chem. 278 2003 48534-48545
70. J. Nedergaard B. Cannon The 'nove' 'uncoupling' proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions Exp. Physiol. 88 2003 65-84
71. A. Negre-Salvayre C. Hirtz G. Carrera R. Cazenave M. Troly R. Salvayre L. Penicaud L. Casteilla A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation FASEB J. 11 1997 809-815
72. D.G. Nicholls S.L. Budd Mitochondria and neuronal survival Physiol. Rev. 80 2000 315-360
73. S. Papa V.P. Skulachev Reactive oxygen species, mitochondria, apoptosis and aging Mol. Cell. Biochem. 174 1997 305-319
74. C. Pecqueur M.C. Alves-Guerra C. Gelly C. Levi-Meyrueis E. Couplan S. Collins D. Ricquier F. Bouillaud B. Miroux Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation J. Biol. Chem. 276 2001 8705-8712
75. S. Raimbault S. Dridi F. Denjean J. Lachuer E. Couplan F. Bouillaud A. Bordas C. Duchamp M. Taouis D. Ricquier An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds Biochem. J. 353 2001 441-444
76. E. Rial E. Aguirregoitia J. Jimenez-Jimenez A. Ledesma Alkylsulfonates activate the uncoupling protein UCP1: Implications for the transport mechanism Biochim. Biophys. Acta 1608 2004 122-130
77. D. Richard S. Clavel Q. Huang D. Sanchis D. Ricquier Uncoupling protein 2 in the brain: Distribution and function Biochem. Soc. Trans. 29 2001 812-817
78. D. Ricquier F. Bouillaud Mitochondrial uncoupling proteins: From mitochondria to the regulation of energy balance J. Physiol. 529 2000 3-10
79. D. Ricquier F. Bouillaud The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP Biochem. J. 345 2000 161-179
80. D.F.S. Rolfe M.D. Brand The physiological significance of mitochondrial proton leak in animal cells and tissues Biosci. Rep. 17 1997 9-16
81. G.A. Rutter Nutrient-secretion coupling in the pancreatic islet beta-cell: Recent advances Mol. Aspects Med. 22 2001 247-284
82. K. Sakai K. Matsumoto T. Nishikawa M. Suefuji K. Nakamaru Y. Hirashima J. Kawashima T. Shirotani K. Ichinose M. Brownlee E. Araki Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic beta-cells Biochem. Biophys. Res. Commun. 300 2003 216-222
83. M.C. Saleh M.B. Wheeler C.B. Chan Uncoupling protein-2: Evidence for its function as a metabolic regulator Diabetologia 45 2002 174-187
84. S. Samec J. Seydoux A.G. Dulloo Role of UCP homologues in skeletal muscles and brown adipose tissue: Mediators of thermogenesis or regulators of lipids as fuel substrate? FASEB J. 12 1998 715-724
85. P. Schrauwen M.K. Hesselink The role of uncoupling protein 3 in fatty acid metabolism: Protection against lipotoxicity? Proc. Nutr. Soc. 63 2004 287-292
86. V.P. Skulachev Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants Q. Rev. Biophys. 29 1996 169-202
87. V.P. Skulachev Uncoupling: New approaches to an old problem of bioenergetics Biochim. Biophys. Acta 1363 1998 100-124
88. J. St-Pierre J.A. Buckingham S.J. Roebuck M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784-44790
89. J.A. Stuart J.A. Harper K.M. Brindle M.D. Brand Uncoupling protein 2 from carp and zebrafish, ectothermic vertebrates Biochim. Biophys. Acta 1413 1999 50-54
90. D.A. Talbot N. Hanuise B. Rey J.-L. Rouanet C. Duchamp M.D. Brand Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus) Biochem. Biophys. Res. Commun. 312 2003 983-988
91. D.A. Talbot C. Duchamp B. Rey N. Hanuise J.L. Rouanet B. Sibille M.D. Brand Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins J. Physiol. 558 2004 123-135
92. D.A. Talbot A.J. Lambert M.D. Brand Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3 FEBS Lett. 556 2004 111-115
93. M. Toyomizu M. Ueda S. Sato Y. Seki K. Sato Y. Akiba Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle FEBS Lett. 529 2002 313-318
94. C.R. Vianna T. Hagen C.Y. Zhang E. Bachman O. Boss B. Gereben A.S. Moriscot B.B. Lowell J.E. Bicudo A.C. Bianco Cloning and functional characterization of an uncoupling protein homolog in hummingbirds Physiol. Genomics 5 2001 137-145
95. A. Vidal-Puig G. Solanes D. Grujic J.S. Flier B.B. Lowell UCP3: An uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue Biochem. Biophys. Res. Commun. 235 1997 79-82
96. A.J. Vidal-Puig D. Grujic C.Y. Zhang T. Hagen O. Boss Y. Ido A. Szczepanik J. Wade V. Mootha R. Cortright et. al. Energy metabolism in uncoupling protein 3 gene knockout mice J. Biol. Chem. 275 2000 16258-16266
97. C.Y. Zhang G. Baffy P. Perret S. Krauss O. Peroni D. Grujic T. Hagen A.J. Vidal-Puig O. Boss Y.B. Kim et. al. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes Cell 105 2001 745-755
98. Y.T. Zhou M. Shimabukuro K. Koyama Y. Lee M.Y. Wang F.Trieu C.B. Newgard and R.H. Unger (1997) Induction by leptin of uncoupling protein-2 and enzymes of fatty acid oxidation. Proc. Natl. Acad. Sci. USA 94, 6386-6390