Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1978 Jun 1;77(3):887–901. doi: 10.1083/jcb.77.3.887

Biochemical and stereological analysis of rat liver mitochondria in different thyroid states

PMCID: PMC2110148  PMID: 681456

Abstract

The concentrations of the inner mitochondrial membrane markers cardiolipin and cytochrome alpha have been measured in liver homogenates and in purified mitochondria after thyroxine administration to thyroidectomized and normal rats. The biochemical results have been correlated with stereological electron micrographic analyses of hepatocytes in liver sections, and of isolated mitochondrial pellets. There were progressive and parallel increases in homogenate and mitochondrial cardiolipin concentration, and in mitochondrial cytochrome alpha concentration, after administration of 20 microgram of thyroxine on alternate days to thyroidectomized rats, and of 300 microgram on alternate days to normal rats. Electron microscope measurements showed marked differences in the shape of the mitochondria and in the number of cristae in different thyroid states. Hypothyroid mitochondria were shorter and wider than controls, and hyperthyroid mitochondria longer but of similar width. Mitochondrial volume per unit cell volume was virtually unchanged in hypo- and hyperthyroid animals. The most striking changes were a decrease in the area of the inner membrane plus cristae in thyroidectomized rats, and a substantial increase in membrane area after thyroxine administration. The biochemical and electron micrographic results indicate that, in rat liver, thyroid hormone administration leads to a selective increase in the relative amount of mitochondrial inner membranes, with little or no change in the mitochondrial volume per unit cell volume, or in total mitochondrial protein per unit total cell protein.

Full Text

The Full Text of this article is available as a PDF (4.6 MB).

Selected References

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

  1. BAHR G. F., ZEITLER E. Study of mitochondria in rat liver. Quantitative electron microscopy. J Cell Biol. 1962 Dec;15:489–501. doi: 10.1083/jcb.15.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
  3. Barsano C. P., Degroot L. J., Getz G. S. The effect of thyroid hormone on in vitro rat liver mitochondrial RNA synthesis. Endocrinology. 1977 Jan;100(1):52–60. doi: 10.1210/endo-100-1-52. [DOI] [PubMed] [Google Scholar]
  4. Chen Y. D., Hoch F. L. Mitochondrial inner membrane in hypothyroidism. Arch Biochem Biophys. 1976 Feb;172(2):741–744. doi: 10.1016/0003-9861(76)90132-6. [DOI] [PubMed] [Google Scholar]
  5. DeGroot L. J., Torresani J. Triiodothyronine binding to isolated liver cell nuclei. Endocrinology. 1975 Feb;96(2):357–359. doi: 10.1210/endo-96-2-357. [DOI] [PubMed] [Google Scholar]
  6. Fleischer S., Rouser G., Fleischer B., Casu A., Kritchevsky G. Lipid composition of mitochondria from bovine heart, liver, and kidney. J Lipid Res. 1967 May;8(3):170–180. [PubMed] [Google Scholar]
  7. Gadaleta M. N., Barletta A., Caldarazzo M., De Leo T., Saccone C. Triiodothyronine action on RNA synthesis in rat-liver mitochondria. Eur J Biochem. 1972 Oct;30(2):376–381. doi: 10.1111/j.1432-1033.1972.tb02108.x. [DOI] [PubMed] [Google Scholar]
  8. Gadaleta M. N., Di Reda N., Bove G., Saccone C. Effects of triiodothyronine on rat-liver mitochondrial transcription process. Eur J Biochem. 1975 Feb 21;51(2):495–501. doi: 10.1111/j.1432-1033.1975.tb03949.x. [DOI] [PubMed] [Google Scholar]
  9. Getz G. S., Bartley W., Lurie D., Notton B. M. The phospholipids of various sheep organs, rat liver and of their subcellular fractions. Biochim Biophys Acta. 1968 Mar 4;152(2):325–339. doi: 10.1016/0005-2760(68)90040-4. [DOI] [PubMed] [Google Scholar]
  10. Getz G. S., Jakovcic S., Heywood J., Frank J., Rabinowitz M. A two-dimensional thin-layer chromatographic system for phospholipid separation. The analysis of yeast phospholipids. Biochim Biophys Acta. 1970 Dec 15;218(3):441–452. doi: 10.1016/0005-2760(70)90007-x. [DOI] [PubMed] [Google Scholar]
  11. Gross N. J. Control of mitochondrial turnover under the influence of thyroid hormone. J Cell Biol. 1971 Jan;48(1):29–40. doi: 10.1083/jcb.48.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gross N. J., Getz G. S., Rabinowitz M. Apparent turnover of mitochondrial deoxyribonucleic acid and mitochondrial phospholipids in the tissues of the rat. J Biol Chem. 1969 Mar 25;244(6):1552–1562. [PubMed] [Google Scholar]
  13. Gustafsson R., Tata J. R., Lindberg O., Ernster L. The relationship between the structure and activity of rat skeletal muscle mitochondria after thyroidectomy and thyroid hormone treatment. J Cell Biol. 1965 Aug;26(2):555–578. doi: 10.1083/jcb.26.2.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hulbert A. J., Augee M. L., Raison J. K. The influence of thyroid hormones on the structure and function of mitochondrial membranes. Biochim Biophys Acta. 1976 Dec 2;455(2):597–601. doi: 10.1016/0005-2736(76)90328-x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Jakovcic S., Haddock J., Getz G. S., Rabinowitz M., Swift H. Mitochondrial development in liver of foetal and newborn rats. Biochem J. 1971 Jan;121(2):341–347. doi: 10.1042/bj1210341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Loud A. V. A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J Cell Biol. 1968 Apr;37(1):27–46. doi: 10.1083/jcb.37.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MacLeod K. N., Baxter J. D. DNA binding of thyroid hormone receptors. Biochem Biophys Res Commun. 1975 Feb 3;62(3):577–583. doi: 10.1016/0006-291x(75)90437-4. [DOI] [PubMed] [Google Scholar]
  20. McCallister L. P., Page E. Effects of thyroxin on ultrastructure of rat myocardial cells: a stereological study. J Ultrastruct Res. 1973 Jan;42(1):136–155. doi: 10.1016/s0022-5320(73)80012-7. [DOI] [PubMed] [Google Scholar]
  21. McMurray W. C., Dawson R. M. Phospholipid exchange reactions within the liver cell. Biochem J. 1969 Mar;112(1):91–108. doi: 10.1042/bj1120091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Page E., McCallister L. P. Quantitative electron microscopic description of heart muscle cells. Application to normal, hypertrophied and thyroxin-stimulated hearts. Am J Cardiol. 1973 Feb;31(2):172–181. doi: 10.1016/0002-9149(73)91030-8. [DOI] [PubMed] [Google Scholar]
  23. RASCH E. M., SWIFT H., SCHWEIGERT B. S. Liver nucleoproteins in vitamin B12 deficiency. Proc Soc Exp Biol Med. 1955 Apr;88(4):637–640. doi: 10.3181/00379727-88-21678. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Samuels H. H., Tsai J. S., Casanova J., Stanley F. Thyroid hormone action: in vitro characterization of solubilized nuclear receptors from rat liver and cultured GH1 cells. J Clin Invest. 1974 Oct;54(4):853–865. doi: 10.1172/JCI107825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sottocasa G. L., Kuylenstierna B., Ernster L., Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol. 1967 Feb;32(2):415–438. doi: 10.1083/jcb.32.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sterling K., Milch P. O., Brenner M. A., Lazarus J. H. Thyroid hormone action: the mitochondrial pathway. Science. 1977 Sep 2;197(4307):996–999. doi: 10.1126/science.196334. [DOI] [PubMed] [Google Scholar]
  28. Sterling K., Milch P. O. Thyroid hormone binding by a component of mitochondrial membrane. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3225–3229. doi: 10.1073/pnas.72.8.3225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Surks M. I., Koerner D. H., Oppenheimer J. H. In vitro binding of L-triiodothyronine to receptors in rat liver nuclei. Kinectics of binding, extraction properties, and lack of requirement for cytosol proteins. J Clin Invest. 1975 Jan;55(1):50–60. doi: 10.1172/JCI107917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  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. Tandler B., Williamson D. L., Ehrman L. Unusual filamentous structures in the paragonia of male Drosophila. J Cell Biol. 1968 Aug;38(2):329–336. doi: 10.1083/jcb.38.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. WEIBEL E. R., GOMEZ D. M. A principle for counting tissue structures on random sections. J Appl Physiol. 1962 Mar;17:343–348. doi: 10.1152/jappl.1962.17.2.343. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. WILLIAMS J. N., Jr A METHOD FOR THE SIMULTANEOUS QUANTITATIVE ESTIMATION OF CYTOCHROMES A, B, C1, AND C IN MITOCHONDRIA. Arch Biochem Biophys. 1964 Sep;107:537–543. doi: 10.1016/0003-9861(64)90313-3. [DOI] [PubMed] [Google Scholar]
  37. Weibel E. R., Kistler G. S., Scherle W. F. Practical stereological methods for morphometric cytology. J Cell Biol. 1966 Jul;30(1):23–38. doi: 10.1083/jcb.30.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weibel E. R., Stäubli W., Gnägi H. R., Hess F. A. Correlated morphometric and biochemical studies on the liver cell. I. Morphometric model, stereologic methods, and normal morphometric data for rat liver. J Cell Biol. 1969 Jul;42(1):68–91. doi: 10.1083/jcb.42.1.68. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yago N., Seki M., Sekiyama S., Kobayashi S., Kurokawa H. Growth and differentiation of mitochondria in the regenerating rat adrenal cortex. J Cell Biol. 1972 Mar;52(3):503–513. doi: 10.1083/jcb.52.3.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zaimis E., Papadaki L., Ash A. S., Larbi E., Kakari S., Matthew M., Paradelis A. Cardiovascular effects of thyroxine. Cardiovasc Res. 1969 Apr;3(2):118–133. doi: 10.1093/cvr/3.2.118. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES