Towards a molecular understanding of adaptive thermogenesis (original) (raw)

• Hart, J. S., Heroux, O. & Depocas, F. Cold acclimation and the electromyogram of unanesthetized rats. J. Appl. Physiol. 9, 404– 408 (1956).
  Article CAS PubMed Google Scholar
• Davis, T. R. A., Johnston, D. R., Bell, F. C. & Cremer, B. J. Regulation of shivering and nonshivering heat production during acclimation of rats. Am. J. Physiol. 198, 471– 475 (1960).
  Article CAS PubMed Google Scholar
• Foster, D. O. & Frydman, M. L. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can. J. Physiol. Pharmacol. 57, 257–270 (1979).
  Article CAS PubMed Google Scholar
• Dauncey, M. J. Influence of mild cold on 24 h energy expenditure, resting metabolism and diet-induced thermogenesis. Br. J. Nutr. 45, 257–267 (1981).
  Article CAS PubMed Google Scholar
• Blaxter, K. Energy Metabolism in Animals and Man (Cambridge Univ. Press, Cambridge, 1989).
  Google Scholar
• Leibel, R. L., Rosenbaum, M. & Hirsch, J. Changes in energy expenditure resulting from altered body weight. N. Engl. J. Med. 332, 621– 628 (1995).
  Article CAS PubMed Google Scholar
• Sims, E. A. & Danforth, E. Jr Expenditure and storage of energy in man. J. Clin. Invest. 79, 1019–1025 (1987).
  Article CAS PubMed PubMed Central Google Scholar
• Shibata, H. & Bukowiecki, L. J. Regulatory alterations of daily energy expenditure induced by fasting or overfeeding in unrestrained rats. J. Appl. Physiol. 63, 465– 470 (1987).
  Article CAS PubMed Google Scholar
• Levine, J. A., Eberhardt, N. L. & Jensen, M. D. Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science 283, 212– 214 (1999).
  Article CAS PubMed Google Scholar
• Bouchard, C. et al. The response to long-term overfeeding in identical twins. N. Engl. J. Med. 322, 1477–1482 (1990).
  Article CAS PubMed Google Scholar
• Kevonian, A. V., Vander Tuig, J. G. & Romsos, D. R. Consumption of a low protein diet increases norepinephrine turnover in brown adipose tissue of adult rats. J. Nutr. 114, 543–549 (1984).
  Article CAS PubMed Google Scholar
• Rothwell, N. J. & Stock, M. J. Effect of environmental temperature on energy balance and thermogenesis in rats fed normal or low protein diets. J. Nutr. 117, 833– 837 (1987).
  Article CAS PubMed Google Scholar
• Landsberg, L., Saville, M. E. & Young, J. B. Sympathoadrenal system and regulation of thermogenesis . Am. J. Physiol. 247, E181–E189 ( 1984).
• Thomas, S. A. & Palmiter, R. D. Thermoregulatory and metabolic phenotypes of mice lacking noradrenaline and adrenaline. Nature 387, 94–97 ( 1997).
  Article ADS CAS PubMed Google Scholar
• Elmquist, J. K., Elias, C. F. & Saper, C. B. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 22, 221– 232 (1999).
  Article CAS PubMed Google Scholar
• Himms-Hagen, J. Brown adipose tissue thermogenesis and obesity. Prog. Lipid Res. 28, 67–115 ( 1989).
  Article CAS PubMed Google Scholar
• al-Adsani, H., Hoffer, L. J. & Silva, J. E. Resting energy expenditure is sensitive to small dose changes in patients on chronic thyroid hormone replacement. J. Clin. Endocrinol. Metab. 82, 1118– 1125 (1997).
  CAS PubMed Google Scholar
• Brand, M. D. et al. The significance and mechanism of mitochondrial proton conductance . Int. J. Obes. Relat. Metab. Disord. 23( Suppl. 6), S4–S11 (1999 ).
  Article CAS PubMed Google Scholar
• Silva, J. E. Thyroid hormone control of thermogenesis and energy balance. Thyroid 5, 481–492 ( 1995).
  Article CAS PubMed Google Scholar
• Almeida, N. G., Levitsky, D. A. & Strupp, B. Enhanced thermogenesis during recovery from diet-induced weight gain in the rat. Am. J. Physiol. 271, R1380–R1387 (1996).
  Article CAS PubMed Google Scholar
• Ahima, R. S. et al. Role of leptin in the neuroendocrine response to fasting. Nature 382, 250–252 ( 1996).
  Article ADS CAS PubMed Google Scholar
• Legradi, G., Emerson, C. H., Ahima, R. S., Flier, J. S. & Lechan, R. M. Leptin prevents fasting-induced suppression of prothyrotropin-releasing hormone messenger ribonucleic acid in neurons of the hypothalamic paraventricular nucleus. Endocrinology 138, 2569–2576 ( 1997).
  Article CAS PubMed Google Scholar
• Rolfe, D. F. & Brown, G. C. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731–758 ( 1997).
  Article CAS PubMed Google Scholar
• Kadenbach, B. et al. Regulation of energy transduction and electron transfer in cytochrome c oxidase by adenine nucleotides. J. Bioenerg. Biomembr. 30, 25–33 ( 1998).
  Article CAS PubMed Google Scholar
• Kozak, L. P., Kozak, U. C. & Clarke, G. T. Abnormal brown and white fat development in transgenic mice overexpressing glycerol 3-phosphate dehydrogenase. Genes Dev. 5, 2256–2264 ( 1991).
  Article Google Scholar
• Nicholls, D. G. & Locke, R. M. Thermogenic mechanisms in brown fat. Physiol. Rev. 64, 1– 64 (1984).
  Article CAS PubMed Google Scholar
• Klingenberg, M. & Huang, S. G. Structure and function of the uncoupling protein from brown adipose tissue. Biochim. Biophys. Acta 1415, 271–296 (1999).
  Article CAS PubMed Google Scholar
• Enerback, S. et al. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90– 94 (1997).
  Article ADS CAS PubMed Google Scholar
• Fleury, C. et al. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia . Nature Genet. 15, 269– 272 (1997).
  Article CAS PubMed Google Scholar
• Gimeno, R. E. et al. Cloning and characterization of an uncoupling protein homolog: a potential molecular mediator of human thermogenesis. Diabetes 46, 900–906 ( 1997).
  Article CAS PubMed Google Scholar
• Boss, O. et al. Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett. 408, 39–42 (1997).
  Article ADS CAS PubMed Google Scholar
• Vidal-Puig, A., Solanes, G., Grujic, D., Flier, J. S. & Lowell, B. B. UCP3: an uncoupling protein homologue expressed preferentially and abundantly in skeletal muscle and brown adipose tissue. Biochem. Biophys. Res. Commun. 235, 79–82 (1997).
  Article CAS PubMed Google Scholar
• Gong, D. W., 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. 272, 24129–24132 (1997).
  Article CAS PubMed Google Scholar
• Hinz, W., Faller, B., Gruninger, S., Gazzotti, P. & Chiesi, M. Recombinant human uncoupling protein-3 increases thermogenesis in yeast cells. FEBS Lett. 448, 57–61 (1999).
  Article CAS PubMed Google Scholar
• Zhang, C. Y., Hagen, T., Mootha, V. K., Slieker, L. J. & Lowell, B. B. Assessment of uncoupling activity of uncoupling protein 3 using a yeast heterologous expression system. FEBS Lett. 449, 129–134 (1999).
  Article CAS PubMed Google Scholar
• Jaburek, M. et al. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J. Biol. Chem. 274, 26003 –26007 (1999).
  Article CAS PubMed Google Scholar
• Sanchis, D. et al. BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J. Biol. Chem. 273, 34611–34615 (1998).
  Article CAS PubMed Google Scholar
• Mao, W. et al. UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett. 443 , 326–330 (1999).
  Article CAS PubMed Google Scholar
• Boss, O. et al. Tissue-dependent upregulation of rat uncoupling protein-2 expression in response to fasting or cold. FEBS Lett. 412, 111–114 (1997).
  Article ADS PubMed Google Scholar
• Weigle, D. S. et al. Elevated free fatty acids induce uncoupling protein 3 expression in muscle: a potential explanation for the effect of fasting. Diabetes 47, 298–302 ( 1998).
  Article CAS PubMed Google Scholar
• Prusiner, S. B., Cannon, B., Ching, T. M. & Lindberg, O. Oxidative metabolism in cells isolated from brown adipose tissue. 2. Catecholamine regulated respiratory control. Eur. J. Biochem. 7, 51– 57 (1968).
  Article CAS PubMed Google Scholar
• Bukowiecki, L. J., Follea, N., Lupien, J. & Paradis, A. Metabolic relationships between lipolysis and respiration in rat brown adipocytes. The role of long chain fatty acids as regulators of mitochondrial respiration and feedback inhibitors of lipolysis. J. Biol. Chem. 256, 12840–12848 (1981).
  CAS PubMed Google Scholar
• Jezek, P. et al. Fatty acid cycling mechanism and mitochondrial uncoupling proteins . Biochim. Biophys. Acta 1365, 319– 327 (1998).
  Article CAS PubMed Google Scholar
• Arch, J. R. et al. Atypical β-adrenoceptor on brown adipocytes as target for anti-obesity drugs. Nature 309, 163– 165 (1984).
  Article ADS CAS PubMed Google Scholar
• Strosberg, A. D. & Pietri-Rouxel, F. Function and regulation of the beta 3-adrenoceptor. Trends Pharmacol. Sci. 17, 373–381 ( 1996).
  Article CAS PubMed Google Scholar
• Susulic, V. S. et al. Targeted disruption of the beta 3-adrenergic receptor gene . J. Biol. Chem. 270, 29483– 29492 (1995).
  Article CAS PubMed Google Scholar
• Champigny, O. et al. Beta 3-adrenergic receptor stimulation restores message and expression of brown-fat mitochondrial uncoupling protein in adult dogs. Proc. Natl Acad. Sci. USA 88, 10774– 10777 (1991).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Fisher, M.H. et al. A selective human beta3 adrenergic receptor agonist increases metabolic rate in rhesus monkeys. J. Clin. Invest. 101, 2387–2393 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Garruti, G. & Ricquier, D. Analysis of uncoupling protein and its mRNA in adipose tissue deposits of adult humans. Int. J. Obes. Relat. Metab. Disord. 16, 383– 390 (1992).
  CAS PubMed Google Scholar
• Himms-Hagen, J. et al. Effect of CL-316,243, a thermogenic beta 3-agonist, on energy balance and brown and white adipose tissues in rats. Am. J. Physiol. 266, R1371–1382 ( 1994).
  CAS PubMed Google Scholar
• Collins, S., Daniel, K. W., Petro, A. E. & Surwit, R. S. Strain-specific response to beta 3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology 138, 405–413 (1997).
  Article CAS PubMed Google Scholar
• Guerra, C., Koza, R. A., Yamashita, H., Walsh, K. & Kozak, L. P. Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity . J. Clin. Invest. 102, 412– 420 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Collins, S. et al. Role of leptin in fat regulation. Nature 380, 677 (1996).
  Article ADS CAS PubMed Google Scholar
• Haynes, W. G., Morgan, D. A., Walsh, S. A., Mark, A. L. & Sivitz, W. I. Receptor-mediated regional sympathetic nerve activation by leptin. J. Clin. Invest. 100, 270–278 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Scarpace, P. J., Matheny, M., Pollock, B. H. & Tumer, N. Leptin increases uncoupling protein expression and energy expenditure. Am. J. Physiol. 273, E226–E230 (1997).
  CAS PubMed Google Scholar
• Satoh, N. et al. Satiety effect and sympathetic activation of leptin are mediated by hypothalamic melanocortin system. Neurosci. Lett. 249, 107–110 (1998).
  CAS PubMed Google Scholar
• Cusin, I. et al. Chronic central leptin infusion enhances insulin-stimulated glucose metabolism and favors the expression of uncoupling proteins. Diabetes 47, 1014–1019 ( 1998).
  Article CAS PubMed Google Scholar
• Champigny, O. & Ricquier, D. Effects of fasting and refeeding on the level of uncoupling protein mRNA in rat brown adipose tissue: evidence for diet-induced and cold-induced responses. J. Nutr. 120, 1730–1736 (1990).
  Article CAS PubMed Google Scholar
• Lowell, B. B. et al. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature 366, 740 –742 (1993).
  Article ADS CAS PubMed Google Scholar
• Melnyk, A. & Himms-Hagen, J. Temperature-dependent feeding: lack of role for leptin and defect in brown adipose tissue-ablated obese mice . Am. J. Physiol. 274, R1131– 1135 (1998).
  CAS PubMed Google Scholar
• Ravussin, E. et al. Reduced rate of energy expenditure as a risk factor for body-weight gain. N. Engl. J. Med. 318, 467– 472 (1988).
  Article CAS PubMed Google Scholar
• Roberts, S. B., Savage, J., Coward, W. A., Chew, B. & Lucas, A. Energy expenditure and intake in infants born to lean and overweight mothers. N. Engl. J. Med. 318, 461–466 (1988).
  Article CAS PubMed Google Scholar
• Zurlo, F., Larson, K., Bogardus, C. & Ravussin, E. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J. Clin. Invest. 86, 1423–1427 (1990).
  Article CAS PubMed PubMed Central Google Scholar
• Simonsen, L., Bulow, J., Madsen, J. & Christensen, N. J. Thermogenic response to epinephrine in the forearm and abdominal subcutaneous adipose tissue. Am. J. Physiol. 263, E850– E855 (1992).
  CAS PubMed Google Scholar
• Gugneja, S., Virbasius, C. M. & Scarpulla, R. C. Nuclear respiratory factors 1 and 2 utilize similar glutamine-containing clusters of hydrophobic residues to activate transcription . Mol. Cell. Biol. 16, 5708– 5716 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Virbasius, J. V. & Scarpulla, R. C. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl. Acad. Sci. USA 91, 1309–1313 ( 1994).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Villena, J. A. et al. Regulation of mitochondrial biogenesis in brown adipose tissue: nuclear respiratory factor-2/GA-binding protein is responsible for the transcriptional regulation of the gene for the mitochondrial ATP synthase beta subunit. Biochem. J. 331, 121–127 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Demonacos, C. V. et al. Mitochondrial genes as sites of primary action of steroid hormones. Steroids 61, 226– 232 (1996).
  Article CAS PubMed Google Scholar
• Cassard-Doulcier, A. M. et al. Tissue-specific and beta-adrenergic regulation of the mitochondrial uncoupling protein gene: control by cis-acting elements in the 5′-flanking region. Mol. Endocrinol. 7, 497– 506 (1993).
  CAS PubMed Google Scholar
• Kozak, U. C. et al. An upstream enhancer regulating brown-fat-specific expression of the mitochondrial uncoupling protein gene. Mol. Cell. Biol. 14, 59–67 ( 1994).
  Article CAS PubMed PubMed Central Google Scholar
• Cummings, D. E. et al. Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A. Nature 382, 622–626 (1996).
  Article ADS CAS PubMed Google Scholar
• Sears, I. B., MacGinnitie, M. A., Kovacs, L. G. & Graves, R. A. Differentiation-dependent expression of the brown adipocyte uncoupling protein gene: regulation by peroxisome proliferator-activated receptor gamma. Mol. Cell. Biol. 16, 3410–3419 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Foellmi-Adams, L. A., Wyse, B. M., Herron, D., Nedergaard, J. & Kletzien, R. F. Induction of uncoupling protein in brown adipose tissue. Synergy between norepinephrine and pioglitazone, an insulin-sensitizing agent. Biochem. Pharmacol. 52, 693– 701 (1996).
  Article CAS PubMed Google Scholar
• Tai, T. A. C. et al. Activation of the nuclear receptor peroxisome proliferator-activated receptor gamma promotes brown adipocyte differentiation. J. Biol. Chem. 271, 29909–29914 ( 1996).
  Article CAS PubMed Google Scholar
• Brun, S. et al. Activators of peroxisome proliferator-activated receptor-alpha induce the expression of the uncoupling protein-3 gene in skeletal muscle: a potential mechanism for the lipid intake-dependent activation of uncoupling protein-3 gene expression at birth. Diabetes 48, 1217–1222 (1999).
  Article CAS PubMed Google Scholar
• Aubert, J. et al. Up-regulation of UCP-2 gene expression by PPAR agonists in preadipose and adipose cells. Biochem. Biophys. Res. Commun. 238, 606–611 (1997).
  Article CAS PubMed Google Scholar
• Puigserver, P. et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829– 839 (1998).
  Article CAS PubMed Google Scholar
• Boss, O. et al. Role of the beta(3)-adrenergic receptor and/or a putative beta(4)-adrenergic receptor on the expression of uncoupling proteins and peroxisome proliferator-activated receptor-gamma coactivator-1. Biochem. Biophys. Res. Commun. 261, 870–876 (1999).
  Article CAS PubMed Google Scholar
• Wu, Z. et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115–124 (1999).
  Article CAS PubMed Google Scholar
• Hosoi, Y. et al. Expression and regulation of type II iodothyronine deiodinase in cultured human skeletal muscle cells. J. Clin. Endocrinol. Metab. 84, 3293–3300 ( 1999).
  CAS PubMed Google Scholar
• Encke, D., Ely, M., Heldmaier, G. & Klaus, S. Physiological approach to maturation of brown adipocytes in primary cell culture. Biochim. Biophys. Acta 1357, 339–347 (1997).
  Article CAS PubMed Google Scholar
• Bartha, T. et al. Characterization of the 5′-flanking and 5′-untranslated regions of the cyclic adenosine 3′,5′-monophosphate-responsive human type 2 iodothyronine deiodinase gene. Endocrinology 141, 229–237 (2000).
  Article CAS PubMed Google Scholar
• Porter, R. K. & Brand, M. D. Body mass dependence of H+ leak in mitochondria and its relevance to metabolic rate. Nature 362, 628–630 ( 1993).
  Article ADS CAS PubMed Google Scholar
• Chance, B. & Williams, C. M. J. Biol. Chem. 217, 405–427 (1955).
  Google Scholar
• Mitchell, P. Keilin's respiratory chain concept and its chemiosmotic consequences. Science 206, 1148–1159 ( 1979).
  Article ADS CAS PubMed Google Scholar
• Balaban, R. S. Regulation of oxidative phosphorylation in the mammalian cell. Am. J. Physiol. 258, C377–C389 (1990).
  Article CAS PubMed Google Scholar
• Hochachka, P. W. The metabolic implications of intracellular circulation. Proc. Natl Acad. Sci. USA 96, 12233–12239 (1999).
  Article ADS CAS PubMed PubMed Central Google Scholar
• McCormack, J. G., Halestrap, A. P. & Denton, R. M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70, 391– 425 (1990).
  Article CAS PubMed Google Scholar
• Brown, G. C. Control of respiration and ATP synthesis in mammalian mitochondria and cells . Biochem. J. 284, 1–13 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Block, B. A. Thermogenesis in muscle. Annu. Rev. Physiol. 56, 535–577 (1994).
  Article CAS PubMed Google Scholar
• O'Brien, J. & Block, B. A. Effects of Ca2+ on oxidative phosphorylation in mitochondria from the thermogenic organ of marlin. J. Exp. Biol. 199, 2679– 2687 (1996).
  CAS PubMed Google Scholar
• Denborough, M. Malignant hyperthermia. Lancet 352, 1131 –1136 (1998).
  Article CAS PubMed Google Scholar
• Dumonteil, E., Barre, H. & Meissner, G. Expression of sarcoplasmic reticulum Ca2+ transport proteins in cold-acclimating ducklings. Am. J. Physiol. 269, C955–C960 ( 1995).
  Article CAS PubMed Google Scholar