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. 1990 Feb 1;265(3):731–734. doi: 10.1042/bj2650731

Thyroid-hormone control of state-3 respiration in isolated rat liver mitochondria.

R P Hafner 1, G C Brown 1, M D Brand 1
PMCID: PMC1133694  PMID: 2306210

Abstract

Oxidative phosphorylation can be treated as two groups of reactions; those that generate protonmotive force (dicarboxylate carrier, succinate dehydrogenase and the respiratory chain) and those that consume protonmotive force (adenine nucleotide and phosphate carriers. ATP synthase and proton leak). Mitochondria from hypothyroid rats have lower rates of respiration in the presence of ADP (state 3) than euthyroid controls. We show that the kinetics of the protonmotive-force generators are unchanged in mitochondria from hypothyroid animals, but the kinetics of the protonmotive-force consumers are altered, supporting proposals that the important effects of thyroid hormone on state 3 are on the ATP synthase or the adenine nucleotide translocator.

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Selected References

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  1. Babior B. M., Creagan S., Ingbar S. H., Kipnes R. S. Stimulation of mitochondrial adenosine diphosphate uptake by thyroid hormones. Proc Natl Acad Sci U S A. 1973 Jan;70(1):98–102. doi: 10.1073/pnas.70.1.98. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brand M. D., Hafner R. P., Brown G. C. Control of respiration in non-phosphorylating mitochondria is shared between the proton leak and the respiratory chain. Biochem J. 1988 Oct 15;255(2):535–539. [PMC free article] [PubMed] [Google Scholar]
  3. Brand M. D., Murphy M. P. Control of electron flux through the respiratory chain in mitochondria and cells. Biol Rev Camb Philos Soc. 1987 May;62(2):141–193. doi: 10.1111/j.1469-185x.1987.tb01265.x. [DOI] [PubMed] [Google Scholar]
  4. Bronk J. R. Thyroid hormone: effects on electron transport. Science. 1966 Aug 5;153(3736):638–639. doi: 10.1126/science.153.3736.638. [DOI] [PubMed] [Google Scholar]
  5. Brown G. C., Brand M. D. Proton/electron stoichiometry of mitochondrial complex I estimated from the equilibrium thermodynamic force ratio. Biochem J. 1988 Jun 1;252(2):473–479. doi: 10.1042/bj2520473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown G. C., Brand M. D. Thermodynamic control of electron flux through mitochondrial cytochrome bc1 complex. Biochem J. 1985 Jan 15;225(2):399–405. doi: 10.1042/bj2250399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. CHANCE B., WILLIAMS G. R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem. 1955 Nov;217(1):383–393. [PubMed] [Google Scholar]
  8. Clot J. P., Baudry M. Effect of thyroidectomy on oxidative phosphorylation mechanisms in rat liver mitochondria. Mol Cell Endocrinol. 1982 Nov-Dec;28(3):455–469. doi: 10.1016/0303-7207(82)90139-3. [DOI] [PubMed] [Google Scholar]
  9. Crabtree B., Newsholme E. A. The derivation and interpretation of control coefficients. Biochem J. 1987 Oct 1;247(1):113–120. doi: 10.1042/bj2470113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Groen A. K., Wanders R. J., Westerhoff H. V., van der Meer R., Tager J. M. Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem. 1982 Mar 25;257(6):2754–2757. [PubMed] [Google Scholar]
  11. Hafner R. P., Brand M. D. Hypothyroidism in rats does not lower mitochondrial ADP/O and H+/O ratios. Biochem J. 1988 Mar 1;250(2):477–484. doi: 10.1042/bj2500477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hafner R. P., Leake M. J., Brand M. D. Hypothyroidism in rats decreases mitochondrial inner membrane cation permeability. FEBS Lett. 1989 May 8;248(1-2):175–178. doi: 10.1016/0014-5793(89)80455-7. [DOI] [PubMed] [Google Scholar]
  13. Hafner R. P., Nobes C. D., McGown A. D., Brand M. D. 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 Dec 15;178(2):511–518. doi: 10.1111/j.1432-1033.1988.tb14477.x. [DOI] [PubMed] [Google Scholar]
  14. Hafner R. P. Thyroid hormone uptake into the cell and its subsequent localisation to the mitochondria. FEBS Lett. 1987 Nov 30;224(2):251–256. doi: 10.1016/0014-5793(87)80464-7. [DOI] [PubMed] [Google Scholar]
  15. Hoch F. L. Adenine nucleotide translocation in liver mitochondria of hypothyroid rats. Arch Biochem Biophys. 1977 Jan 30;178(2):535–545. doi: 10.1016/0003-9861(77)90224-7. [DOI] [PubMed] [Google Scholar]
  16. Holness M., Crespo-Armas A., Mowbray J. The influence of thyroid hormone on the degree of control of oxidative phosphorylation exerted by the adenine nucleotide translocator. FEBS Lett. 1984 Nov 19;177(2):231–235. doi: 10.1016/0014-5793(84)81289-2. [DOI] [PubMed] [Google Scholar]
  17. Horrum M. A., Tobin R. B., Ecklund R. E. Thyroxine-induced changes in rat liver mitochondrial cytochromes. Mol Cell Endocrinol. 1985 Jul;41(2-3):163–169. doi: 10.1016/0303-7207(85)90019-x. [DOI] [PubMed] [Google Scholar]
  18. Horrum M. A., Tobin R. B., Ecklund R. E. Thyroxine-induced changes in rat liver mitochondrial ubiquinone. Biochem Biophys Res Commun. 1986 Jul 16;138(1):381–386. doi: 10.1016/0006-291x(86)90292-5. [DOI] [PubMed] [Google Scholar]
  19. Ida Chen Y. D., Hoch F. L. Thryoid control over biomembranes. Rat liver mitochondrial inner membranes. Arch Biochem Biophys. 1977 Jun;181(2):470–483. doi: 10.1016/0003-9861(77)90253-3. [DOI] [PubMed] [Google Scholar]
  20. Kunz W., Gellerich F. N., Schild L., Schönfeld P. Kinetic limitations in the overall reaction of mitochondrial oxidative phosphorylation accounting for flux-dependent changes in the apparent delta GexP/delta mu H+ ratio. FEBS Lett. 1988 Jun 6;233(1):17–21. doi: 10.1016/0014-5793(88)81347-4. [DOI] [PubMed] [Google Scholar]
  21. LEE Y. P., LARDY H. A. INFLUENCE OF THYROID HORMONES ON L-ALPHA-GLYCEROPHOSPHATE DEHYDROGENASES AND OTHER DEHYDROGENASES IN VARIOUS ORGANS OF THE RAT. J Biol Chem. 1965 Mar;240:1427–1436. [PubMed] [Google Scholar]
  22. Maddaiah V. T., Clejan S., Palekar A. G., Collipp P. J. Hormones and liver mitochondria: effects of growth hormone and thyroxine on respiration, fluorescence of 1-anilino-8-naphthalene sulfonate and enzyme activities of complex I and II of submitochondrial particles. Arch Biochem Biophys. 1981 Sep;210(2):666–677. doi: 10.1016/0003-9861(81)90234-4. [DOI] [PubMed] [Google Scholar]
  23. Mak I. T., Shrago E., Elson C. E. Effect of thyroidectomy on the kinetics of ADP-ATP translocation in liver mitochondria. Arch Biochem Biophys. 1983 Oct 1;226(1):317–323. doi: 10.1016/0003-9861(83)90298-9. [DOI] [PubMed] [Google Scholar]
  24. Mowbray J., Corrigall J. Short-term control of mitochondrial adenine nucleotide translocator by thyroid hormone. Eur J Biochem. 1984 Feb 15;139(1):95–99. doi: 10.1111/j.1432-1033.1984.tb07981.x. [DOI] [PubMed] [Google Scholar]
  25. Murphy M. P., Brand M. D. The control of electron flux through cytochrome oxidase. Biochem J. 1987 Apr 15;243(2):499–505. doi: 10.1042/bj2430499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Palacios-Romero R., Mowbray J. Evidence for the rapid direct control both in vivo and in vitro of the efficiency of oxidative phosphorylation by 3,5,3'-tri-iodo-L-thyronine in rats. Biochem J. 1979 Dec 15;184(3):527–538. doi: 10.1042/bj1840527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Protnay G. I., McClendon F. D., Bush J. E., Braverman L. E., Babior B. M. The effect of physiological doses of thyroxine on carrier-mediated ADP uptake by liver mitochondria from thyroidectomized rats. Biochem Biophys Res Commun. 1973 Nov 1;55(1):17–21. doi: 10.1016/s0006-291x(73)80053-1. [DOI] [PubMed] [Google Scholar]
  28. Reynafarje B., Costa L. E., Lehninger A. L. O2 solubility in aqueous media determined by a kinetic method. Anal Biochem. 1985 Mar;145(2):406–418. doi: 10.1016/0003-2697(85)90381-1. [DOI] [PubMed] [Google Scholar]
  29. Seitz H. J., Müller M. J., Soboll S. Rapid thyroid-hormone effect on mitochondrial and cytosolic ATP/ADP ratios in the intact liver cell. Biochem J. 1985 Apr 1;227(1):149–153. doi: 10.1042/bj2270149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shears S. B., Bronk J. R. The influence of thyroxine administered in vivo on the transmembrane protonic electrochemical potential difference in rat liver mitochondria. Biochem J. 1979 Feb 15;178(2):505–507. doi: 10.1042/bj1780505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Verhoeven A. J., Kamer P., Groen A. K., Tager J. M. Effects of thyroid hormone on mitochondrial oxidative phosphorylation. Biochem J. 1985 Feb 15;226(1):183–192. doi: 10.1042/bj2260183. [DOI] [PMC free article] [PubMed] [Google Scholar]

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