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. 1965 Aug 1;26(2):555–578. doi: 10.1083/jcb.26.2.555

THE RELATIONSHIP BETWEEN THE STRUCTURE AND ACTIVITY OF RAT SKELETAL MUSCLE MITOCHONDRIA AFTER THYROIDECTOMY AND THYROID HORMONE TREATMENT

R Gustafsson 1, J R Tata 1, O Lindberg 1, L Ernster 1
PMCID: PMC2106749  PMID: 5893687

Abstract

The fine structure of rat gastrocnemius muscle fibers has been studied after changes were induced in the basal metabolic rate (BMR) by thyroidectomy and L-thyroxine administration under anabolic conditions. Biochemical analysis of skeletal muscle mitochondrial respiration and phosphorylation from the same tissue preparations has been summarized, details having been published earlier (3). As estimated from electron micrographs, the total amount of mitochondria from thyroidectomized animals was enlarged 1.5 times over that from normal controls. The total amount of mitochondria from thyroidectomized or normal animals made hypermetabolic with thyroxine was increased 2.5 to 3.5 times over that from their corresponding controls. In all cases, there was an increase in the mitochondrial population and the profile ratio of cristae to matrix was also considerably increased, thus indicating both relative and absolute enlargements of the entire surface of the cristae per unit fiber. The major structural changes persisted for at least 3 weeks after the cessation of thyroxine treatment, by which time the elevated mitochondrial respiratory and phosphorylative activity had declined to normal values. The hypertrophy and increase in mitochondrial population was more prominent in the perinuclear and subsacrolemmic regions near blood vessels than in the interstices of the fibrils. The very long interfibrillar mitochondria found in both the hypo- and hypermetabolic tissues are more likely to be derived from outgrowths of the original mitochondria rather than from a fusion of smaller ones. These findings are compatible with the ideas expressed elsewhere (see 1, 3, 10) that, under conditions close to the physiological, thyroid hormones control mitochondrial metabolic activity by a subtle alteration in mitochondrial composition with respect to their respiratory and phosphorylative constituents. The possible application of using thyroid hormones in the study of biogenesis of mitochondria and the synthesis of mitochondrial constituents are discussed.

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Selected References

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  1. AZZONE G. F., EEG-OLOFSSON O., ERNSTER L., LUFT R., SZABOLCSI G. Studies on isolated human skeletal muscle mitochondria. Exp Cell Res. 1961 Jan;22:415–436. doi: 10.1016/0014-4827(61)90119-7. [DOI] [PubMed] [Google Scholar]
  2. BRONK J. R. THYROID HORMONES: CONTROL OF TERMINAL OXIDATION. Science. 1963 Aug 30;141(3583):816–818. doi: 10.1126/science.141.3583.816. [DOI] [PubMed] [Google Scholar]
  3. CHAPPELL J. B., PERRY S. V. Biochemical and osmotic properties of skeletal muscle mitochondria. Nature. 1954 Jun 5;173(4414):1094–1095. doi: 10.1038/1731094a0. [DOI] [PubMed] [Google Scholar]
  4. COOPER C., TAPLEY D. F. Effect of thyroxine on the swelling of mitochondria isolated from various tissues of the rat. Nature. 1956 Nov 17;178(4542):1119–1119. doi: 10.1038/1781119a0. [DOI] [PubMed] [Google Scholar]
  5. FLETCHER M. J., SANADI D. R. Turnover of rat-liver mitochondria. Biochim Biophys Acta. 1961 Aug 5;51:356–360. doi: 10.1016/0006-3002(61)90177-9. [DOI] [PubMed] [Google Scholar]
  6. FREEMAN K. B., ROODYN D. B., TATA J. R. Stimulation of amino acid incorporation into protein by isolated mitochondria from rats treated with thyroid hormones. Biochim Biophys Acta. 1963 May 28;72:129–132. [PubMed] [Google Scholar]
  7. HOCH F. L. Biochemical actions of thyroid hormones. Physiol Rev. 1962 Oct;42:605–673. doi: 10.1152/physrev.1962.42.4.605. [DOI] [PubMed] [Google Scholar]
  8. KARNOVSKY M. J. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. doi: 10.1083/jcb.11.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. LARDY H. A., LEE Y. P., TAKEMORI A. Enzyme responses to thyroid hormones. Ann N Y Acad Sci. 1960 Apr 23;86:506–511. doi: 10.1111/j.1749-6632.1960.tb42826.x. [DOI] [PubMed] [Google Scholar]
  10. LEHNINGER A. L. Water uptake and extrusion by mitochondria in relation to oxidative phosphorylation. Physiol Rev. 1962 Jul;42:467–517. doi: 10.1152/physrev.1962.42.3.467. [DOI] [PubMed] [Google Scholar]
  11. LUCK D. J. Genesis of mitochondria in neurospora crassa. Proc Natl Acad Sci U S A. 1963 Feb 15;49:233–240. doi: 10.1073/pnas.49.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. LUCK D. J. THE INFLUENCE OF PRECURSOR POOL SIZE ON MITOCHONDRIAL COMPOSITION IN NEUROSPORA CRASSA. J Cell Biol. 1965 Mar;24:445–460. doi: 10.1083/jcb.24.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LUFT R., IKKOS D., PALMIERI G., ERNSTER L., AFZELIUS B. A case of severe hypermetabolism of nonthyroid origin with a defect in the maintenance of mitochondrial respiratory control: a correlated clinical, biochemical, and morphological study. J Clin Invest. 1962 Sep;41:1776–1804. doi: 10.1172/JCI104637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. PORTER K. R., PALADE G. E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol. 1957 Mar 25;3(2):269–300. doi: 10.1083/jcb.3.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Parsons D. F. Mitochondrial Structure: Two Types of Subunits on Negatively Stained Mitochondrial Membranes. Science. 1963 May 31;140(3570):985–987. doi: 10.1126/science.140.3570.985. [DOI] [PubMed] [Google Scholar]
  17. ROODYN D. B., FREEMAN K. B., TATA J. R. THE STIMULATION BY TREATMENT IN VIVO WITH TRI-IODOTHYRONINE OF AMINO ACID INCORPORATION INTO PROTEIN BY ISOLATED RAT-LIVER MITOCHONDRIA. Biochem J. 1965 Mar;94:628–641. doi: 10.1042/bj0940628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. TATA J. R. ACCELERATED SYNTHESIS AND TURNOVER OF NUCLEAR AND CYTOPLASMIC RNA DURING THE LATENT PERIOD OF ACTION OF THYROID HORMONE. Biochim Biophys Acta. 1964 Jul 22;87:528–530. doi: 10.1016/0926-6550(64)90132-x. [DOI] [PubMed] [Google Scholar]
  19. TATA J. R., ERNSTER L., LINDBERG O., ARRHENIUS E., PEDERSEN S., HEDMAN R. The action of thyroid hormones at the cell level. Biochem J. 1963 Mar;86:408–428. doi: 10.1042/bj0860408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. TATA J. R., ERNSTER L., LINDBERG O. Control of basal metabolic rate by thyroid hormones and cellular function. Nature. 1962 Mar 17;193:1058–1060. doi: 10.1038/1931058a0. [DOI] [PubMed] [Google Scholar]
  21. WIDNELL C. C., TATA J. R. Stimulation of nuclear RNA polymerase during the latent period of action of thyroid hormones. Biochim Biophys Acta. 1963 Jul 30;72:506–508. [PubMed] [Google Scholar]

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