Mitochondrial uncoupling as a target for drug development for the treatment of obesity

Obesity Reviews

Volumn 2, Issue 4, 2001, Pages 255-265

  Harper, J A ^a,b   Dickinson, K ^c   Brand, M D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ABBOTT LABORATORIES   (United States)

Author keywords

Mitochondria; Obesity; Standard Metabolic Rate; Uncoupling

Indexed keywords

ANTIOBESITY AGENT; CARRIER PROTEIN; ION CHANNEL; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN;

BASAL METABOLIC RATE; DRUG EFFECT; ENERGY METABOLISM; HUMAN; METABOLISM; MITOCHONDRION; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; WEIGHT REDUCTION;

ANTI-OBESITY AGENTS; BASAL METABOLISM; CARRIER PROTEINS; ENERGY METABOLISM; HUMANS; ION CHANNELS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OBESITY; WEIGHT LOSS;

EID: 0035502402     PISSN: 14677881     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1467-789X.2001.00043.x     Document Type: Article

References (123)

1. Kopelman PG. Obesity as a medical problem. Nature 2000; 404: 635-643.
2. Wadden TA. Treatment of obesity by moderate and severe caloric restriction. Results of clinical research trials. Ann Intern Med 1993; 119: 688-693.
3. Bray GA, Blackburn GL, Ferguson JM, Greenway FL, Jain AK, Mendel CM, Mendels J, Ryan DH, Schwartz SL, Scheinbaum ML, Seaton TB. Sibutramine produces dose-related weight loss. Obes Res 1999; 7: 189-198.
4. James WP, Astrup A, Finer N, Hilsted J, Kopelman P, Rossner S, Saris WH, Van Gaal LF. Effect of sibutramine on weight maintenance after weight loss: a randomised trial. STORM Study Group. Sibutramine Trial of Obesity Reduction and Maintenance. Lancet 2000; 356: 2119-2125.
5. Ryan DH. Use of sibutramine and other noradrenergic and serotonergic drugs in the management of obesity. Endocrine 2000; 13: 193-199.
6. Sjostrom L, Rissanen A, Andersen T, Boldrin M, Golay A, Koppeschaar HP, Krempf M. Randomised placebo-controlled trial of orlistat for weight loss and prevention of weight regain in obese patients. European Multicentre Orlistat Study Group. Lancet 1998; 352: 167-172.
7. Hvizdos KM, Markham A. Orlistat: a review of its use in the management of obesity. Drugs 1999; 58: 743-760.
8. Connoley IP, Lui Y, Frost I, Reckless IP, Heal DJ, Stock MJ. Thermogenic effects of sibutramine and its metabolites. Br J Pharmacol 1999; 126: 1487-1495.
9. Danforth E Jr. Sibutramine and thermogenesis in humans. Int J Obes Relat Metab Disord 1999; 23: 1007-1008.
10. Ferro-Luzzi A, Martino L. The Origins and Consequences of Obesity. Wiley: Chichester, 1996.
11. Poehlman ET. A review: exercise and its influence on resting energy metabolism in man. Med Sci Sports Exerc 1989; 21: 515-525.
12. Parascandola J, Dinitrophenol and bioenergetics: a historical perspective. Mol Cell Biochem 1974; 5: 69-77.
13. 3-adrenoceptor agonists for the treatment of obesity and diabetes-an update. Diabetes Metab 1999; 25: 11-21.
14. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA, Beeley LJ, Godden RJ, Herrity N, Skehel M, Changani KK, Hockings PD, Reid DG, Squires SM, Hatcher J, Trail B, Latcham J, Rastan S, Harper AJ, Cadenas S, Buckingham JA, Brand MD, Abuin A. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 2000; 406: 415-48.
15. Rolfe DFS, Brand MD. Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol 1996; 271: C1380-C1389.
16. Rolfe DFS, Newman JM, Buckingham JA, Clark MG, Brand MD. Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 1999; 276: C692-C699.
17. Blaxter K. Energy Metabolism in Animals and Man. Cambridge University Press: Cambridge, 1989.
18. Li B, Nolte LA, Ju JS, Han DH, Coleman T, Holloszy JO, Semenkovich CF. Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 2000; 6: 1115-1120.
19. Brand MD. The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J Theor Biol 1990; 145: 267-286.
20. Hulbert AJ, Else PL. Mechanisms underlying the cost of living in animals. Annu Rev Physiol 2000; 62: 207-235.
21. Hemmingsen AM. Energy metabolism as related to body size and respiratory surfaces and its evolution. Rep Steno Mem Hosp Nord Insulinab 1960; 9: 1-110.
22. Kleiber M. Body size and metabolism. Hilgardia 1932; 6: 315-353.
23. Brody S, Procter RC. Relation between basal metabolism and mature body weight in different species of mammals and birds. Univ Miss Agric Exp Sta Res Bull 1932; 166: 89-101.
24. Nagy KA. Field metabolic rate and food requirement scaling in mammals and birds. Ecol Mono 1987; 57: 111-128.
25. Nagy KA. Field bioenergetics of mammals: what determines field metabolic rates. Aust J Zool 1994; 42: 43-53.
26. Rolfe DFS, Hulbert AJ, Brand MD. Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat. Biochim Biophys Acta 1994; 1188: 405-416.
27. Brody S. Bioenergetics and Growth. Hafner: Canada, 1945.
28. Calder WA. Size, Function and Life History. Harvard University Press: London, 1984.
29. Peters RH. The Ecological Implications of Body Size. Cambridge University Press: Cambridge, 1983.
30. + leak in mitochondria and its relevance to metabolic rate. Nature 1993; 362: 628-630.
31. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ. Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 1991; 275: 81-86.
32. Porter RK, Brand MD. Causes of differences in respiration rate of hepatocytes from mammals of different body mass. Am J Physiol 1995; 269: R1213-R1224.
33. Porter RK, Hulbert AJ, Brand MD. Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol 1996; 271: R1550-R1560.
34. Brookes PS, Hulbert AJ, Brand MD. The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim Biophys Acta 1997; 1330: 157-164.
35. Hulbert AJ, Else PL. Membranes as possible pacemakers of metabolism. J Theor Biol 1999; 199: 257-274.
36. Pehowich DJ. Thyroid hormone status and membrane n-3 fatty acid content influence mitochondrial proton leak. Biochim Biophys Acta 1999; 1411: 192-200.
37. Belzung F, Raclot T, Groscolas R. Fish oil n-3 fatty acids selectively limit the hypertrophy of abdominal fat depots in growing rats fed high-fat diets. Am J Physiol 1993; 264: R1111-R1118.
38. Hun CS, Hasegawa K, Kawabata T, Kato M, Shimokawa T, Kagawa Y. Increased uncoupling protein 2 mRNA in white adipose tissue, and decrease in leptin, visceral fat, blood glucose, and cholesterol in KK-Ay mice fed with eicosapentaenoic and docosahexaenoic acids in addition to linolenic acid. Biochem Biophys Res Commun 1999; 259: 85-90.
39. Erasmus U. (2001). Udo's Choice 3,6,9 Perfected Oil Blend [WWW document] URL http://www.udoerasmus.com/
40. Tainter ML, Cutting WC, Stockton AB. Use of dinitrophenol in nutritional disorders: a critical survey of clinical results. Am J Public Health 1934; 24: 1045-1053.
41. Cazeneuze P, Lepine R. Compt Rend Soc Biol 1885; 101: 1167-1169.
42. Magne H, Mayer A, Plantefol L. Studies on the action of dinitrophenol 1-2-4 (Thermol). Ann Physiol Physicochem Biol 1932; 8: 1-167.
43. Cutting WC, Tainter ML. Actions of dinitrophenol. Proc Soc Exper Biol & Med 1932; 29: 1268.
44. Tainter ML, Stockton AB, Cutting WC. Dinitrophenol in the treatment of obesity: Final report. J Am Med Assoc 1935; 101: 322-336.
45. Cutting WC, Mehrtens HG, Tainter ML. Actions and uses of dinitrophenol: Promising metabolic applications. J Am Med Assoc 1933; 101: 193-195.
46. Tainter ML, Stockton AB, Cutting WC. Use of dinitrophenol in obesity and related conditions: a progress report. J Am Med Assoc 1933; 101: 1472-1475.
47. Cutting WC, Tainter ML. Metabolic actions of dinitrophenol with the use of balanced and unbalanced diets. J Am Med Assoc 1933; 101: 2099-2102.
48. Simkins S. Dinitrophenol and desiccated thyroid in the treatment of obesity: a comprehensive clinical and laboratory study. J Am Med Assoc 1937; 108: 2110-2118.
49. Boardman WW. Rapidly developing cataract after dinitrophenol. J Am Med Assoc 1935; 105: 108.
50. Horner W, Jones R, Boardman WW. Cataracts following the use of dinitrophenol. J Am Med Assoc 1935; 105: 108-110.
51. Anthony DM, Dickinson K, Jones RB, Heal DJ. Metabolic actions of 2,4-dinitrophenol: - a re-evaluation of activity in-vitro and in-vivo. In: Obesity Regulation Energy Homeostasis Keystone Symposia. Keystone Symposia: Silverthorne, CO, 2001, p 218.
52. Byrom FB. Nature of myxoedema. Clin Sc 1933; 1: 273-285.
53. Astrup A, Buemann B, Toubro S, Ranneries C, Raben A. Low resting metabolic rate in subjects predisposed to obesity: a role for thyroid status. Am J Clin Nutr 1996; 63: 879-883.
54. Stenlof K, Sjostrom L, Fagerberg B, Nystrom E, Lindstedt G. Thyroid hormones, procollagen III peptide, body composition and basal metabolic rate in euthyroid individuals. Scand J Clin Lab Invest 1993; 53: 793-803.
55. Harper ME, Brand MD. The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem 1993; 268: 14850-14860.
56. Hafner RP, Nobes CD, McGown AD, Brand MD. Altered relationship between protonmotive force and respiration rate in non-phosphorylating liver mitochondria isolated from rats of different thyroid hormone status. Eur J Biochem 1988; 178: 511-518.
57. Brand MD, Steverding D, Kadenbach B, Stevenson PM, Hafner RP. The mechanism of the increase in mitochondrial proton permeability induced by thyroid hormones. Eur J Biochem 1992; 206: 775-781.
58. Drabkin DL. Cytochrome c metabolism and liver regeneration. Influence of thyroid gland and thyroxine. J Biol Chem 1949; 182: 335-349.
59. Tata JR, Ernster L, Lindberg O, Arrhenius E, Pederson S, Hedman R. The action of thyroid hormones at the cell level. Biochem J 1963; 86: 408-428.
60. Hulbert AJ. Thyroid hormones and their effects: a new perspective. Biol Rev Camb Philos Soc 2000; 75: 519-631.
61. Hoch FL. Lipids and thyroid hormones. Prog Lipid Res 1988; 27: 199-270.
62. Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD. The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B Biochem Mol Biol 1998; 119: 325-334.
63. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Enhanced cytochrome oxidase activity and modification of lipids in heart mitochondria from hyperthyroid rats. Biochim Biophys Acta 1994; 1225: 165-170.
64. Soboll S. Thyroid hormone action on mitochondrial energy transfer. Biochim Biophys Acta 1993; 1144: 1-16.
65. Masaki T, Yoshimatsu H, Kakuma T, Hidaka S, Kurokawa M, Sakata T. Enhanced expression of uncoupling protein 2 gene in rat white adipose tissue and skeletal muscle following chronic treatment with thyroid hormone. FEBS Lett 1997; 418: 323-326.
66. Lanni A, Beneduce L, Lombardi A, Moreno M, Boss O, Muzzin P, Giacobino JP, Goglia F. Expression of uncoupling protein-3 and mitochondrial activity in the transition from hypothyroid to hyperthyroid state in rat skeletal muscle. FEBS Lett 1999; 444: 250-254.
67. Lanni A, De Felice M, Lombardi A, Moreno M, Fleury C, Ricquier D, Goglia F. Induction of UCP2 mRNA by thyroid hormones in rat heart. FEBS Lett 1997; 418: 171-174.
68. Gong DW, He Y, Karas M, Reitman M. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin. J Biol Chem 1997; 272: 24129-24132.
69. Larkin S, Mull E, Miao W, Pittner R, Albrandt K, Moore C, Young A, Denaro M, Beaumont K. Regulation of the third member of the uncoupling protein family, UCP3, by cold and thyroid hormone. Biochem Biophys Res Commun 1997; 240: 222-227.
70. Klein I, Levey GS. New perspectives on thyroid hormone, catecholamines, and the heart. Am J Med 1984; 76: 167-172.
71. Burgi U, Burgi-Saville ME, Burgherr J, Clement M, Lauber K. T3 plus high doses of beta-blockers: effects on energy intake, body composition, bat and heart in rats. Int J Obes 1990; 14: 1023-1038.
72. Mittleman RE, Goldberg RB, Nadji M. Severe thyroid atrophy due to prolonged ingestion of thyroid hormone for treatment of obesity. South Med J 1984; 77: 268-270.
73. Kyle LH, Ball MF, Doolan PD. Effect of thyroid hormone on body composition in myxedema and obesity. N Engl J Med 1966; 275: 12-17.
74. Abraham RR, Densem JW, Davies P, Davie MW, Wynn V. The effects of triiodothyronine on energy expenditure, nitrogen balance and rates of weight and fat loss in obese patients during prolonged caloric restriction. Int J Obes 1985; 9: 433-442.
75. Nicholls DG, Locke RM. Thermogenic mechanisms in brown fat. Physiol Rev 1984; 64: 1-64.
76. Nedergaard J, Golozoubova V, Matthias A, Asadi A, Jacobsson A, Cannon B. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim Biophys Acta 2001; 1504: 82-106.
77. Nicholls DG. The effective proton conductance of the inner membrane of mitochondria from brown adipose tissue. Dependency on proton electrochemical potential gradient. Eur J Biochem 1977; 77: 349-356.
78. Nicholls DG, Lindberg O. Brown-adipose-tissue mitochondria. The influence of albumin and nucleotides on passive ion permeabilities. Eur J Biochem 1973; 37: 523-530.
79. Nicholls DG. 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 Biochem 1976; 62: 223-228.
80. Heaton GM, Wagenvoord RJ, Kemp AJ, Nicholls DG. Brown-adipose-tissue mitochondria: photoaffinity labelling of the regulatory site of energy dissipation. Eur J Biochem 1978; 82: 515-521.
81. Lin CS, Hackenberg H, Klingenberg EM. The uncoupling protein from brown adipose tissue mitochondria is a dimer. A hydrodynamic study. FEBS Lett 1980; 113: 304-306.
82. Lin CS, Klingenberg M. Characteristics of the isolated purine nucleotide binding protein from brown fat mitochondria. Biochemistry 1982; 21: 2950-2956.
83. Bathgate B, Freebairn EM, Greenland AJ, Reid GA. Functional expression of the rat brown adipose tissue uncoupling protein in Saccharomyces cerevisiae. Mol Microbiol 1992; 6: 363-370.
84. Jezek P, Orosz DE, Garlid KD. Reconstitution of the uncoupling protein of brown adipose tissue mitochondria. Demonstration of GDP-sensitive halide anion uniport. J Biol Chem 1990; 265: 19296-19302.
85. Katiyar SS, Shrago E. Reconstitution of purified brown adipose tissue mitochondria uncoupling protein: demonstration of separate identity of nucleotide binding and proton translocation sites by chemical probes. Proc Natl Acad Sci USA 1989; 86: 2559-2562.
86. + translocator. EMBO J 1985; 4: 3087-3092.
87. Strieleman PJ, Schalinske KL, Shrago E. Fatty acid activation of the reconstituted brown adipose tissue mitochondria uncoupling protein. J Biol Chem 1985; 260: 13402-13405.
88. Harper ME, Himms-Hagen J. Mitochondrial efficiency: lessons learned from transgenic mice. Biochim Biophys Acta 2001; 1504: 159-172.
89. Enerbäck S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 1997; 387: 90-94.
90. Melnyk A, Harper ME, Himms-Hagen J. Raising at thermoneutrality prevents obesity and hyperphagia in BAT- ablated transgenic mice. Am J Physiol 1997; 272: R1088-R1093.
91. Kopecky J, Clarke G, Enerback S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 1995; 96: 2914-2923.
92. Strosberg AD, Pietri-Rouxel F. Function and regulation of the β3-adrenoceptor. Trends Pharmacol Sci 1996; 17: 373-381.
93. Ricquier D, Bouillaud F. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 2000; 345: 161-179.
94. Nicholls DG, Rial E. A history of the first uncoupling protein, UCP1. J Bioenerg Biomembr 1999; 31: 399-406.
95. Arch JR, Wilson S. Prospects for β3-adrenoceptor agonists in the treatment of obesity and diabetes. Int J Obes Relat Metab Disord 1996; 20: 191-199.
96. Henningfield MF, Swick RW. Immunochemical detection and quantitation of brown adipose tissue uncoupling protein. Biochem Cell Biol 1987; 65: 245-251.
97. Lean ME, Branch WJ, James WP, Jennings G, Ashwell M. Measurement of rat brown-adipose-tissue mitochondrial uncoupling protein by radioimmunoassay: increased concentration after cold acclimation. Biosci Rep 1983; 3: 61-71.
98. Ricquier D, Barlet JP, Garel JM, Combes-George M, Dubois MP. An immunological study of the uncoupling protein of brown adipose tissue mitochondria. Biochem J 1983; 210: 859-866.
99. Pecqueur C, Alves-Guerra MC, Gelly C, Levi-Meyrueis C, Couplan E, Collins S, Ricquier D, Bouillaud F, Miroux B. Uncoupling Protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 2001; 276: 8705-8712.
100. Sivitz WI, Fink BD, Donohoue PA. Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression. Endocrinology 1999; 140: 1511-1519.
101. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levi-Meyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 1997; 15: 269-272.
102. Gonzalez-Barroso MM, Fleury C, Arechaga I, Zaragoza P, Levi-Meyrueis C, Raimbault S, Ricquier D, Bouillaud F, Rial E. Activation of the uncoupling protein by fatty acids is modulated by mutations in the C-terminal region of the protein. Eur J Biochem 1996; 239: 445-450.
103. Hinz W, Faller B, Gruninger S, Gazzotti P, Chiesi M. Recombinant human uncoupling protein-3 increases thermogenesis in yeast cells. FEBS Lett 1999; 448: 57-61.
104. Stuart JA, Harper JA, Brindle KM, Jekabsons MB, Brand MD. Physiological levels of mammalian uncoupling protein 2 do not uncouple yeast mitochondria. J Biol Chem 2001; 22: 22.
105. Stuart JA, Brand MD, Brindle KM, Jekabsons MB, Harper JA. Evidence that the uncoupling observed with UCP2 and UCP3 in yeast mitochondria is an artefact. Obesity Regulation Energy Homeostasis Keystone Symposia. Keystone Symposia: Silverthorne, CO, 2001, pp 218.
106. Stuart JA, Harper JA, Jekabsons MB, Brindle KM, Brand MD. A mitochondrial uncoupling artefact can be caused by expression of uncoupling protein 1 in yeast. Biochem J 2001; 356: 779-789.
107. Echtay KS, Liu Q, Caskey T, Winkler E, Frischmuth K, Bienengraber M, Klingenberg M. Regulation of UCP3 by nucleotides is different from regulation of UCP1. FEBS Lett 1999; 450: 8-12.
108. Jaburek M, Varecha M, Gimeno RE, Dembski M, Jezek P, Zhang M, Burn P, Tartaglia LA, Garlid KD. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J Biol Chem 1999; 274: 26003-26007.
109. Echtay KS, Winkler E, Bienengraeber M, Klingenberg M. Site-directed mutagenesis identifies residues in uncoupling protein (UCP1) involved in three different functions. Biochemistry 2000; 39: 3311-3317.
110. Klingenberg M, Echtay KS. Uncoupling proteins: the issues from a biochemist point of view. Biochim Biophys Acta 2001; 1504: 128-143.
111. Echtay KS, Winkler E, Klingenberg M. Coenzyme Q is an obligatory cofactor for uncoupling protein function. Nature 2000; 408: 609-613.
112. + transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc Natl Acad Sci USA 2001; 98: 1416-1421.
113. Matthias A, Jacobsson A, Cannon B, Nedergaard J. The bioenergetics of brown fat mitochondria from UCP1-ablated mice. UCP1 is not involved in fatty acid-induced de-energization ('uncoupling'). J Biol Chem 1999; 274: 28150-28160.
114. Monemdjou S, Kozak LP, Harper ME. Mitochondrial proton leak in brown adipose tissue mitochondria of Ucp1- deficient mice is GDP insensitive. Am J Physiol 1999; 276: E1073-E1082.
115. Gong DW, Monemdjou S, Gavrilova O, Leon LR, Marcus-Samuels B, Chou CJ, Everett C, Kozak LP, Li C, Deng C, Harper ME, Reitman ML. Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3. J Biol Chem 2000; 275: 16251-16257.
116. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, Muoio DM, Lowell BB. Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 2000; 275: 16258-16266.
117. Samec S, Seydoux J, Dulloo AG. Role of UCP homologues in skeletal muscles and brown adipose tissue: mediators of thermogenesis or regulators of lipids as fuel substrate? FASEB J 1998; 12: 715-724.
118. Ma SW, Foster DO. Starvation-induced changes in metabolic rate, blood flow, and regional energy expenditure in rats. Can J Physiol Pharmacol 1986; 64: 1252-1258.
119. Cadenas S, Buckingham JA, Samec S, Seydoux J, Din N, Dulloo AG, Brand MD. UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 1999; 462: 257-260.
120. Andreyev A, Bondareva TO, Dedukhova VI, Mokhova EN, Skulachev VP, Volkov NI. Carboxyatractylate inhibits the uncoupling effect of free fatty acids. FEBS Lett 1988; 226: 265-269.
121. Skulachev VP. Uncoupling: new approaches to an old problem of bioenergetics. Biochim Biophys Acta 1998; 1363: 100-124.
122. Cadenas S, Buckingham JA, St-Pierre J, Dickinson K, Jones RB, Brand MD. AMP decreases the efficiency of skeletal-muscle mitochondria. Biochem J 2000; 351: 307-311.
123. Hafner RP, Brown GC, Brand MD. Thyroid-hormone control of state-3 respiration in isolated rat liver mitochondria. Biochem J 1990; 265: 731-734.