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Physiol. Rev. 77: 731-758, 1997;
0031-9333/97 $15.00
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Physiological Reviews, Vol 77, 731-758, Copyright © 1997 by American Physiological Society

JOURNAL ARTICLE

Cellular energy utilization and molecular origin of standard metabolic rate in mammals

D. F. Rolfe and G. C. Brown
Department of Biochemistry, University of Cambridge, United Kingdom.

The molecular origin of standard metabolic rate and thermogenesis in mammals is examined. It is pointed out that there are important differences and distinctions between the cellular reactions that 1) couple to oxygen consumption, 2) uncouple metabolism, 3) hydrolyze ATP, 4) control metabolic rate, 5) regulate metabolic rate, 6) produce heat, and 7) dissipate free energy. The quantitative contribution of different cellular reactions to these processes is assessed in mammals. We estimate that approximately 90% of mammalian oxygen consumption in the standard state is mitochondrial, of which approximately 20% is uncoupled by the mitochondrial proton leak and 80% is coupled to ATP synthesis. The consequences of the significant contribution of proton leak to standard metabolic rate for tissue P-to-O ratio, heat production, and free energy dissipation by oxidative phosphorylation and the estimated contribution of ATP-consuming processes to tissue oxygen consumption rate are discussed. Of the 80% of oxygen consumption coupled to ATP synthesis, approximately 25-30% is used by protein synthesis, 19-28% by the Na(+)-K(+)-ATPase, 4-8% by the Ca2(+)-ATPase, 2-8% by the actinomyosin ATPase, 7-10% by gluconeogenesis, and 3% by ureagenesis, with mRNA synthesis and substrate cycling also making significant contributions. The main cellular reactions that uncouple standard energy metabolism are the Na+, K+, H+, and Ca2+ channels and leaks of cell membranes and protein breakdown. Cellular metabolic rate is controlled by a number of processes including metabolic demand and substrate supply. The differences in standard metabolic rate between animals of different body mass and phylogeny appear to be due to proportionate changes in the whole of energy metabolism. Heat is produced by some reactions and taken up by others but is mainly produced by the reactions of mitochondrial respiration, oxidative phosphorylation, and proton leak on the inner mitochondrial membrane. Free energy is dissipated by all cellular reactions, but the major contributions are by the ATP-utilizing reactions and the uncoupling reactions. The functions and evolutionary significance of standard metabolic rate are discussed.


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J. Exp. Biol., December 15, 2004; 207(26): 4525 - 4533.
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S. Iossa, M. P. Mollica, L. Lionetti, R. Crescenzo, R. Tasso, and G. Liverini
A Possible Link Between Skeletal Muscle Mitochondrial Efficiency and Age-Induced Insulin Resistance
Diabetes, November 1, 2004; 53(11): 2861 - 2866.
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R. McNulty, H. Wang, R. T. Mathias, B. J. Ortwerth, R. J W. Truscott, and S. Bassnett
Regulation of tissue oxygen levels in the mammalian lens
J. Physiol., September 15, 2004; 559(3): 883 - 898.
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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
B. J. Wu, A. J. Hulbert, L. H. Storlien, and P. L. Else
Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2004; 287(3): R633 - R641.
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F. van Breukelen, N. Sonenberg, and S. L. Martin
Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2004; 287(2): R349 - R353.
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C. Michiels
Physiological and Pathological Responses to Hypoxia
Am. J. Pathol., June 1, 2004; 164(6): 1875 - 1882.
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 Am. J. Physiol. Endocrinol. Metab.Home page
L. Bevilacqua, J. J. Ramsey, K. Hagopian, R. Weindruch, and M.-E. Harper
Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production
Am J Physiol Endocrinol Metab, June 1, 2004; 286(5): E852 - E861.
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 DiabetesHome page
D. R. Seals and C. Bell
Chronic Sympathetic Activation: Consequence and Cause of Age-Associated Obesity?
Diabetes, February 1, 2004; 53(2): 276 - 284.
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S. C. R. de Souza, J. E. de Carvalho, A. S. Abe, J. E. P. W. Bicudo, and M. S. C. Bianconcini
Seasonal metabolic depression, substrate utilisation and changes in scaling patterns during the first year cycle of tegu lizards (Tupinambis merianae)
J. Exp. Biol., January 15, 2004; 207(2): 307 - 318.
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D. Julian and C. Leeuwenburgh
Linkage between insulin and the free radical theory of aging
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2004; 286(1): R20 - R21.
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B. B. Lowell and E. S. Bachman
{beta}-Adrenergic Receptors, Diet-induced Thermogenesis, and Obesity
J. Biol. Chem., August 8, 2003; 278(32): 29385 - 29388.
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 ANN INTERN MEDHome page
J. E. Silva
The Thermogenic Effect of Thyroid Hormone and Its Clinical Implications
Ann Intern Med, August 5, 2003; 139(3): 205 - 213.
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A. J. Hulbert
Life, death and membrane bilayers
J. Exp. Biol., July 15, 2003; 206(14): 2303 - 2311.
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J. St-Pierre, J. Lin, S. Krauss, P. T. Tarr, R. Yang, C. B. Newgard, and B. M. Spiegelman
Bioenergetic Analysis of Peroxisome Proliferator-activated Receptor {gamma} Coactivators 1{alpha} and 1{beta} (PGC-1{alpha} and PGC-1{beta}) in Muscle Cells
J. Biol. Chem., July 11, 2003; 278(29): 26597 - 26603.
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R. guzman-marin, N. Suntsova, D. R Stewart, H. Gong, R. Szymusiak, and D. McGinty
Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats
J. Physiol., June 1, 2003; 549(2): 563 - 571.
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I. Pinz and H.-O. Portner
Metabolic costs induced by lactate in the toad Bufo marinus: new mechanism behind oxygen debt?
J Appl Physiol, March 1, 2003; 94(3): 1177 - 1185.
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 DiabetesHome page
H. Pilegaard, B. Saltin, and P. D. Neufer
Effect of Short-Term Fasting and Refeeding on Transcriptional Regulation of Metabolic Genes in Human Skeletal Muscle
Diabetes, March 1, 2003; 52(3): 657 - 662.
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B. D. Eads and S. C. Hand
Transcriptional initiation under conditions of anoxia-induced quiescence in mitochondria from Artemia franciscana embryos
J. Exp. Biol., February 1, 2003; 206(3): 577 - 589.
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 Ann Rheum DisHome page
A Kuhnke, G-R Burmester, S Krauss, and F Buttgereit
Bioenergetics of immune cells to assess rheumatic disease activity and efficacy of glucocorticoid treatment
Ann Rheum Dis, February 1, 2003; 62(2): 133 - 139.
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P. E. Bickler and P. H. Donohoe
Adaptive responses of vertebrate neurons to hypoxia
J. Exp. Biol., December 1, 2002; 205(23): 3579 - 3586.
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Z. Xia, A. D. Sniderman, and K. Cianflone
Acylation-stimulating Protein (ASP) Deficiency Induces Obesity Resistance and Increased Energy Expenditure in ob/ob Mice
J. Biol. Chem., November 22, 2002; 277(48): 45874 - 45879.
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A. J. Hulbert, S. Faulks, W. A. Buttemer, and P. L. Else
Acyl composition of muscle membranes varies with body size in birds
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M.-E. HARPER, A. ANTONIOU, E. VILLALOBOS-MENUEY, A. RUSSO, R. TRAUGER, M. VENDEMELIO, A. GEORGE, R. BARTHOLOMEW, D. CARLO, A. SHAIKH, et al.
Characterization of a novel metabolic strategy used by drug-resistant tumor cells
FASEB J, October 1, 2002; 16(12): 1550 - 1557.
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J. van Milgen
Modeling Biochemical Aspects of Energy Metabolism in Mammals
J. Nutr., October 1, 2002; 132(10): 3195 - 3202.
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H. Guderley and J. St-Pierre
Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change
J. Exp. Biol., August 1, 2002; 205(15): 2237 - 2249.
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R. G. Boutilier and J. St-Pierre
Adaptive plasticity of skeletal muscle energetics in hibernating frogs: mitochondrial proton leak during metabolic depression
J. Exp. Biol., August 1, 2002; 205(15): 2287 - 2296.
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G. Argyropoulos and M.-E. Harper
Molecular Biology of Thermoregulation: Invited Review: Uncoupling proteins and thermoregulation
J Appl Physiol, May 1, 2002; 92(5): 2187 - 2198.
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C. E. Ford, A. B. Scholey, G. Ayre, and K. Wesnes
The effect of glucose administration and the emotional content of words on heart rate and memory
J Psychopharmacol, May 1, 2002; 16(3): 241 - 244.
[Abstract] [PDF]


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