Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1976 Feb;57(2):368–379. doi: 10.1172/JCI108288

Thyroid thermogenesis. Relationships between Na+-dependent respiration and Na+ + K+-adenosine triphosphatase activity in rat skeletal muscle.

Y Asano, U A Liberman, I S Edelman
PMCID: PMC436661  PMID: 130385

Abstract

The effect of thyroid status on QO2, QO2 (t) and NaK-ATPase activity was examined in rat skeletal muscle. QO2(t) (i.e. Na+-transport-dependent respiration) was estimated with ouabain or Na+-free media supplemented with K+. In contrast to the effects of ouabain on ion composition, intracellular K+ was maintained at about 125 meq/liter, and intracellular Na+ was almost nil in the Na+-free media. The estimates of QO2(t) were independent of the considerable differences in tissue ion concentrations. The increase in QO2(t) account for 47% of the increase in QO2 in the transition from the hypothyroid to the euthyroid state and 84% of the increase in the transition from the euthyroid to the hyperthyroid state. Surgical thyroidectomy lowered NaK-ATPase activity of the microsomal fraction (expressed per milligram protein) 32%; injections of triodothyronine (T3) increased this activity 75% in initially hypothyroid rats and 26% in initially euthyroid rats. Thyroidectomy was attended by significant falls in serum Ca and Pi concentrations. Administration of T3 resulted in further declines in serum Ca and marked increases in serum Ps concentrations. Similar effects were seen in 131I-treated rats, but the magnitude of the declines in serum Ca were less. The effects of T3 on QO2, QO2(t), and NaK-ATPase activity of skeletal muscle were indistinguishable in the 131I-ablated and surgically thyroidectomized rats. In thyroidectomized or euthyroid rats given repeated doses of T3, QO2(t) and NaA-ATPase activity increased proportionately. In thyroidectomized rats injected with single doses of T3, either 10, 50, or 250 mug/100 g body wt, QO2(t) increased linearly with NaK-ATPase activity. The kinetics of the NaK-ATPase activity was assessed with an ATP-generating system. T3 elicited a significant increase in Vmax with no change in Km for ATP.

Full text

PDF
368

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Armstrong W. M., Lurie D., Burt M. R., High J. R. Extracellular volume and ionic content of frog ventricle. Am J Physiol. 1969 Oct;217(4):1230–1235. doi: 10.1152/ajplegacy.1969.217.4.1230. [DOI] [PubMed] [Google Scholar]
  2. Ash A. S., Besch H. R., Jr, Harigaya S., Zaimis E. Changes in the activity of sarcoplasmic reticulum fragments and actomyosin isolated from skeletal muscle of thyroxine-treated cats. J Physiol. 1972 Jul;224(1):1–19. doi: 10.1113/jphysiol.1972.sp009878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BARKER S. B., KLITGAARD H. M. Metabolism of tissues excised from thyroxine-injected rats. Am J Physiol. 1952 Jul;170(1):81–86. doi: 10.1152/ajplegacy.1952.170.1.81. [DOI] [PubMed] [Google Scholar]
  4. BARKER S. B. Mechanism of action of the thyroid hormone. Physiol Rev. 1951 Jul;31(3):205–243. doi: 10.1152/physrev.1951.31.3.205. [DOI] [PubMed] [Google Scholar]
  5. BROZEK J., GRANDE F. Body composition and basal metabolism in man: correlation analysis versus physiological approach. Hum Biol. 1955 Feb;27(1):22–31. [PubMed] [Google Scholar]
  6. 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]
  7. ELSHOVE A., VAN ROSSUMG NET MOVEMENTS OF SODIUM AND POTASSIUM, AND THEIR RELATION TO RESPIRATION, IN SLICES OF RAT LIVER INCUBATED IN VITRO. J Physiol. 1963 Oct;168:531–553. doi: 10.1113/jphysiol.1963.sp007206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frazer A., Hess M. E., Shanfeld J. The effects of thyroxine on rat heart adenosine 3',5'-monophosphate, phosphorylase b kinase and phosphorylase a activity. J Pharmacol Exp Ther. 1969 Nov;170(1):10–16. [PubMed] [Google Scholar]
  9. Hassinen I. E., Ylikahri R. H., Kähönen M. T. Regulation of cellular respiration by thyroid hormone. Spectroscopic evidence of mitochondrial control in intact rat liver. Arch Biochem Biophys. 1971 Nov;147(1):255–261. doi: 10.1016/0003-9861(71)90333-x. [DOI] [PubMed] [Google Scholar]
  10. Hoch F. L. Early action of injected L-thyroxine on mitochondrial oxidative phosphorylation. Proc Natl Acad Sci U S A. 1967 Aug;58(2):506–512. doi: 10.1073/pnas.58.2.506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ismail-Beigi F., Edelman I. S. Effects of thyroid status on electrolyte distribution in rat tissues. Am J Physiol. 1973 Nov;225(5):1172–1177. doi: 10.1152/ajplegacy.1973.225.5.1172. [DOI] [PubMed] [Google Scholar]
  12. Ismail-Beigi F., Edelman I. S. The mechanism of the calorigenic action of thyroid hormone. Stimulation of Na plus + K plus-activated adenosinetriphosphatase activity. J Gen Physiol. 1971 Jun;57(6):710–722. doi: 10.1085/jgp.57.6.710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ismail-Beigi F., Edelman I. S. Time-course of the effects of thyroid hormone on respiration and Na+ + K+-ATPase activity in rat liver. Proc Soc Exp Biol Med. 1974 Sep;146(4):983–988. doi: 10.3181/00379727-146-38232. [DOI] [PubMed] [Google Scholar]
  14. Izmail-Beigi F., Edelman I. S. Mechanism of thyroid calorigenesis: role of active sodium transport. Proc Natl Acad Sci U S A. 1970 Oct;67(2):1071–1078. doi: 10.1073/pnas.67.2.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson R. B., Jr A new fluorometric method for the estimation or detection of total and fractionated alkaline phosphatase. Clin Chem. 1969 Feb;15(2):108–123. [PubMed] [Google Scholar]
  16. Jones J. K., Ismail-Beigi F., Edelman I. S. Rat liver adenyl cyclase activity in various thyroid states. J Clin Invest. 1972 Sep;51(9):2498–2501. doi: 10.1172/JCI107064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KLEINZELLER A., KNOTKOVA A. THE EFFECT OF OUABAIN ON THE ELECTROLYTE AND WATER TRANSPORT IN KIDNEY CORTEX AND LIVER SLICES. J Physiol. 1964 Dec;175:172–192. doi: 10.1113/jphysiol.1964.sp007510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Katz A. I., Lindheimer M. D. Renal sodium- and potassium-activated adenosine triphosphatase and sodium reabsorption in the hypothyroid rat. J Clin Invest. 1973 Apr;52(4):796–804. doi: 10.1172/JCI107243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kubista V., Kubistová J., Pette D. Thyroid hormone induced changes in the enzyme activity pattern of energy-supplying metabolism of fast (white), slow (red), and heart muscle of the rat. Eur J Biochem. 1971 Feb;18(4):553–560. doi: 10.1111/j.1432-1033.1971.tb01276.x. [DOI] [PubMed] [Google Scholar]
  20. LAMBERG B. A., GRASBECK R. The serum protein pattern in disorders of thyroid function. Acta Endocrinol (Copenh) 1955 May;19(1):91–100. doi: 10.1530/acta.0.0190091. [DOI] [PubMed] [Google Scholar]
  21. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  22. Levey G. S., Skelton C. L., Epstein S. E. Influence of hyperthyroidism on the effects of norepinephrine on myocardial adenyl cyclase activity and contractile state. Endocrinology. 1969 Dec;85(6):1004–1009. doi: 10.1210/endo-85-6-1004. [DOI] [PubMed] [Google Scholar]
  23. Matsui H., Schwartz A. Purification and properties of a highly active ouabain-sensitive Na+, K+-dependent adenosinetriphosphatase from cardiac tissue. Biochim Biophys Acta. 1966 Nov 15;128(2):380–390. doi: 10.1016/0926-6593(66)90185-8. [DOI] [PubMed] [Google Scholar]
  24. McNeill J. H., Muschek L. D., Brody T. M. The effect of triiodothyronine on cyclic AMP, phosphorylase, and adenyl cyclase in rat heart. Can J Physiol Pharmacol. 1969 Nov;47(11):913–916. doi: 10.1139/y69-149. [DOI] [PubMed] [Google Scholar]
  25. PAGE E., SOLOMON A. K. Cat heart muscle in vitro. I. Cell volumes and intracellular concentrations in papillary muscle. J Gen Physiol. 1960 Nov;44:327–344. doi: 10.1085/jgp.44.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rogus E., Price T., Zierler K. L. Sodium plus potassium-activated, ouabain-inhibited adenosine triphosphatase from a fraction of rat skeletal muscle, and lack of insulin effect on it. J Gen Physiol. 1969 Aug;54(2):188–202. doi: 10.1085/jgp.54.2.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SKOU J. C. ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. Physiol Rev. 1965 Jul;45:596–617. doi: 10.1152/physrev.1965.45.3.596. [DOI] [PubMed] [Google Scholar]
  28. Schwartz A., Allen J. C., Harigaya S. Possible involvement of cardiac Na+, K+-adenosine triphosphatase in the mechanism of action of cardiac glycosides. J Pharmacol Exp Ther. 1969 Jul;168(1):31–41. [PubMed] [Google Scholar]
  29. Skelton C. L., Pool P. E., Seagren S. C., Braunwald E. Mechanochemistry of cardiac muscle. V. Influence of thyroid state on energy utilization. J Clin Invest. 1971 Mar;50(3):463–473. doi: 10.1172/JCI106514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sperelakis N., Lee E. C. Characterization of (Na + ,K + )-ATPase isolated from embryonic chick hearts and cultured chick heart cells. Biochim Biophys Acta. 1971 Jun 1;233(3):562–579. doi: 10.1016/0005-2736(71)90155-6. [DOI] [PubMed] [Google Scholar]
  31. Suko J. Alterations of Ca 2 uptake and Ca 2+ activated ATPase of cardiac sarcoplasmic reticulum in hyper- and hypothyroidism. Biochim Biophys Acta. 1971 Nov 12;252(2):324–327. doi: 10.1016/0304-4165(71)90013-4. [DOI] [PubMed] [Google Scholar]
  32. TATA J. R. Inhibition of the biological action of thyroid hormones by actinomycin D and puromycin. Nature. 1963 Mar 23;197:1167–1168. doi: 10.1038/1971167a0. [DOI] [PubMed] [Google Scholar]
  33. Van Rossum G. D. On the coupling of respiration to cation transport in slices of rat liver. Biochim Biophys Acta. 1970 Apr 7;205(1):7–17. doi: 10.1016/0005-2728(70)90056-3. [DOI] [PubMed] [Google Scholar]
  34. Werner H. V., Berry M. N. Stimulatory effects of thyroxine administration on reducing-equivalent transfer from substrate to oxygen during hepatic metabolism of sorbitol and glycerol. Eur J Biochem. 1974 Mar 1;42(2):315–324. doi: 10.1111/j.1432-1033.1974.tb03342.x. [DOI] [PubMed] [Google Scholar]
  35. Westgard J. O., Poquette M. A. Determination of serum albumin with the "SMA 12-60" by a bromcresol green dye-binding method. Clin Chem. 1972 Jul;18(7):647–653. [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES