Mitochondrial oxidative phosphorylation thermodynamic efficiencies reflect physiological organ roles.

Mitochondria cannot maximize energy production, efficiency, and the cellular ATP phosphorylation potential all at the same time. The theoretical and observed determinations of coupling of oxidative phosphorylation in mitochondria from rat liver, heart, and brain were compared using classical and nonequilibrium thermodynamic measures. Additionally, the optimal thermodynamic efficiency and flow ratios were determined for control of the two energy-converting complexes of the respiratory chain: complex I (NADH), which reflects the integrated cellular pathway, and complex II (FADH2), the predominantly tricarboxylic acid (TCA) cycle pathway. For all three organs, the cellular respiratory pathway was more tightly coupled than the TCA pathway and resulted in a greater optimal efficiency. Liver mitochondria are the most thermodynamically efficient at ATP production using oxidative phosphorylation. Heart and brain mitochondrial systems utilize more oxygen, but can produce ATP at a faster rate than liver systems. Per the theory of economic degrees of coupling, isolated rat liver mitochondrial systems are designed for the economic production of ATP for use in cellular processes. In the brain, the mitochondrial TCA cycle pathway promotes the maximal maintenance of the cellular energy state for cellular viability, whereas in the heart the TCA cycle pathway maximizes the production of ATP. The coupling of oxidative phosphorylation not only can be expected to change with substrate availability but may also reflect an ontogenetic response of mitochondria to fit specific organ roles in the rat.

[1]  J. Lemasters,et al.  Thermodynamic limits to the ATP/site stoichiometries of oxidative phosphorylation by rat liver mitochondria. , 1984, The Journal of biological chemistry.

[2]  R. Hansford,et al.  4 – PREPARATION OF MITOCHONDRIA FROM ANIMAL TISSUES AND YEASTS , 1972 .

[3]  G. Babcock,et al.  Oxygen activation and the conservation of energy in cell respiration , 1992, Nature.

[4]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[5]  J. Lemasters The ATP-to-oxygen stoichiometries of oxidative phosphorylation by rat liver mitochondria. An analysis of ADP-induced oxygen jumps by linear nonequilibrium thermodynamics. , 1984, The Journal of biological chemistry.

[6]  M. Wilson,et al.  Mitochondria: a practical approach. , 1987 .

[7]  B CHANCE,et al.  The respiratory chain and oxidative phosphorylation. , 1956, Advances in enzymology and related subjects of biochemistry.

[8]  R. Rosenthal,et al.  Cerebral Ischemia and Reperfusion: Prevention of Brain Mitochondrial Injury by Lidoflazine , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  J. Exton,et al.  Stable changes to calcium fluxes in mitochondria isolated from rat livers perfused with alpha-adrenergic agonists and with glucagon. , 1980, The Biochemical journal.

[10]  R. Capaldi,et al.  Mitochondrial myopathies and respiratory chain proteins. , 1988, Trends in biochemical sciences.

[11]  H. Rottenberg,et al.  Non-equilibrium thermodynamics of energy conversion in bioenergetics. , 1979, Biochimica et biophysica acta.

[12]  L. Mela,et al.  Isolation of mitochondria with emphasis on heart mitochondria from small amounts of tissue. , 1979, Methods in enzymology.

[13]  J. Stucki The optimal efficiency and the economic degrees of coupling of oxidative phosphorylation. , 1980, European journal of biochemistry.

[14]  P. Tummino,et al.  A comparative study of succinate-supported respiration and ATP/ADP translocation in liver mitochondria from adult and old rats , 1991, Mechanisms of Ageing and Development.

[15]  G. Fiskum,et al.  Differential sensitivity of AS-30D rat hepatoma cells and normal hepatocytes to anoxic cell damage. , 1992, American Journal of Physiology.

[16]  Grégoire Nicolis,et al.  Self-Organization in nonequilibrium systems , 1977 .

[17]  M. Gutman,et al.  Control of the rate of reverse electron transport in submitochondrial particles by the free energy. , 1977, Biochemistry.

[18]  D. Wallace,et al.  Diseases of the mitochondrial DNA. , 1992, Annual review of biochemistry.

[19]  A. Katchalsky,et al.  Nonequilibrium Thermodynamics in Biophysics , 1965 .

[20]  N. Sims Rapid Isolation of Metabolically Active Mitochondria from Rat Brain and Subregions Using Percoll Density Gradient Centrifugation , 1990, Journal of neurochemistry.

[21]  J. Stucki,et al.  Regulation of the degree of coupling of oxidative phosphorylation in intact rat liver. , 1985, Biochimica et biophysica acta.

[22]  P. Reinhart,et al.  A procedure for the rapid preparation of mitochondria from rat liver. , 1982, The Biochemical journal.

[23]  S. Caplan,et al.  Degree of coupling and its relation to efficiency of energy conversion , 1965 .