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. 1971 Nov 1;51(2):369–383. doi: 10.1083/jcb.51.2.369

CHANGES IN THE SARCOPLASMIC RETICULUM AND TRANSVERSE TUBULAR SYSTEM OF FAST AND SLOW SKELETAL MUSCLES OF THE MOUSE DURING POSTNATAL DEVELOPMENT

A R Luff 1, H L Atwood 1
PMCID: PMC2108137  PMID: 5112650

Abstract

The sarcoplasmic reticulum (SR) and transverse tubular system (TTS) of a fast-twitch muscle (extensor digitorum longus-EDL) and a slow-twitch muscle (soleus-SOL) of the mouse were examined during postnatal development. Muscles of animals newborn to 60 days old were fixed in glutaraldehyde and osmium tetroxide and examined with an electron microscope. At birth the few T tubules were often oriented longitudinally, but at the age of 10 days most of them had a transverse orientation. In the EDL, the estimated volume of the TTS increased from 0.08% at birth to 0.4% in the adult; corresponding values for the SOL were 0.04% at birth and 0.22% in the adult. A similar relative change was observed in surface area of the TTS during development. Calculated on the basis of a 30 µm diameter fiber, the surface area of the TTS in the EDL increased from 0.60 cm2 TTS/cm2 fiber surface in the newborn to 3.1 cm2/cm2 in the adult, compared with 0.15 cm2/cm2 at birth to 1.80 cm2/cm2 in the adult for the SOL. The SR in the newborn muscles occurred as a loose network of tubules that developed rapidly within the subsequent 20 days, especially at the I band level. The volume of the SR increased in the EDL from 1.1% of fiber volume at birth to 5.5% in the adult. In the SOL the change was from 1.7% to 2.9%. The SOL approached the adult values more rapidly than the EDL, although the EDL had more SR and T tubules. Fibers of both EDL and SOL muscles showed variation in Z line thickness, mitochondrial content, and diameter, but over-all differences between the two muscles in amount of SR and TTS were significant. It is considered that the differing amounts of SR and TTS are closely related to the differing speeds of contraction that have been demonstrated for these two muscles.

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Selected References

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  1. ALLEN E. R., PEPE F. A. ULTRASTRUCTURE OF DEVELOPING MUSCLE CELLS IN THE CHICK EMBRYO. Am J Anat. 1965 Jan;116:115–147. doi: 10.1002/aja.1001160107. [DOI] [PubMed] [Google Scholar]
  2. Barnard R. J., Edgerton V. R., Furukawa T., Peter J. B. Histochemical, biochemical, and contractile properties of red, white, and intermediate fibers. Am J Physiol. 1971 Feb;220(2):410–414. doi: 10.1152/ajplegacy.1971.220.2.410. [DOI] [PubMed] [Google Scholar]
  3. Bubenzer H. J. Die dünnen und die dicken Muskelfasern des Zwerchfells der Ratte. Z Zellforsch Mikrosk Anat. 1966;69:520–550. [PubMed] [Google Scholar]
  4. Bárány M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 1967 Jul;50(6 Suppl):197–218. doi: 10.1085/jgp.50.6.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DESSOUKY D. A., HIBBS R. G. AN ELECTRON MICROSCOPE STUDY OF THE DEVELOPMENT OF THE SOMATIC MUSCLE OF THE CHICK EMBRYO. Am J Anat. 1965 May;116:523–565. doi: 10.1002/aja.1001160305. [DOI] [PubMed] [Google Scholar]
  6. DUBOWITZ V., PEARSE A. G. A comparative histochemical study of oxidative enzyme and phosphorylase activity in skeletal muscle. Z Zellforch Microsk Anat Histochem. 1960;2:105–117. doi: 10.1007/BF00744575. [DOI] [PubMed] [Google Scholar]
  7. Edgerton V. R., Simpson D. R. Dynamic and metabolic relationships in the rat extensor digitorum longus muscle. Exp Neurol. 1971 Feb;30(2):374–376. doi: 10.1016/s0014-4886(71)80016-x. [DOI] [PubMed] [Google Scholar]
  8. Edgerton V. R., Simpson D. R. The intermediate muscle fiber of rats and guinea pigs. J Histochem Cytochem. 1969 Dec;17(12):828–838. doi: 10.1177/17.12.828. [DOI] [PubMed] [Google Scholar]
  9. Eisenberg B., Eisenberg R. S. Selective disruption of the sarcotubular system in frog sartorius muscle. A quantitative study with exogenous peroxidase as a marker. J Cell Biol. 1968 Nov;39(2):451–467. doi: 10.1083/jcb.39.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ezerman E. B., Ishikawa H. Differentiation of the sarcoplasmic reticulum and T system in developing chick skeletal muscle in vitro. J Cell Biol. 1967 Nov 1;35(2):405–420. doi: 10.1083/jcb.35.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gauthier G. F. On the relationship of ultrastructural and cytochemical features of color in mammalian skeletal muscle. Z Zellforsch Mikrosk Anat. 1969;95(3):462–482. doi: 10.1007/BF00995217. [DOI] [PubMed] [Google Scholar]
  12. Gauthier G. F., Padykula H. A. Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J Cell Biol. 1966 Feb;28(2):333–354. doi: 10.1083/jcb.28.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HUXLEY A. F. MUSCLE. Annu Rev Physiol. 1964;26:131–152. doi: 10.1146/annurev.ph.26.030164.001023. [DOI] [PubMed] [Google Scholar]
  14. Howse H. D., Ferrans V. J., Hibbs R. G. A light and electron microscopic study of he heart of a crayfish, Procambarus clarkii (Giraud). II. Fine structure. J Morphol. 1971 Mar;133(3):353–373. doi: 10.1002/jmor.1051330308. [DOI] [PubMed] [Google Scholar]
  15. PEACHEY L. D. Structure of the longitudinal body muscles of amphioxus. J Biophys Biochem Cytol. 1961 Aug;10(4):159–176. doi: 10.1083/jcb.10.4.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Peachey L. D., Schild R. F. The distribution of the T-system along the sarcomeres of frog and toad sartorius muscles. J Physiol. 1968 Jan;194(1):249–258. doi: 10.1113/jphysiol.1968.sp008405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  19. Pellegrino C., Franzini C. AN ELECTRON MICROSCOPE STUDY OF DENERVATION ATROPHY IN RED AND WHITE SKELETAL MUSCLE FIBERS. J Cell Biol. 1963 May 1;17(2):327–349. doi: 10.1083/jcb.17.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. REVEL J. P. The sarcoplasmic reticulum of the bat cricothroid muscle. J Cell Biol. 1962 Mar;12:571–588. doi: 10.1083/jcb.12.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. ROMANUL F. C. ENZYMES IN MUSCLE. I. HISTOCHEMICAL STUDIES OF ENZYMES IN INDIVIDUAL MUSCLE FIBERS. Arch Neurol. 1964 Oct;11:355–358. doi: 10.1001/archneur.1964.00460220017003. [DOI] [PubMed] [Google Scholar]
  22. Rayns D. G., Simpson F. O., Bertaud W. S. Surface features of striated muscle. II. Guinea-pig skeletal muscle. J Cell Sci. 1968 Dec;3(4):475–482. doi: 10.1242/jcs.3.4.475. [DOI] [PubMed] [Google Scholar]
  23. STEIN J. M., PADYKULA H. A. Histochemical classification of individual skeletal muscle fibers of the rat. Am J Anat. 1962 Mar;110:103–123. doi: 10.1002/aja.1001100203. [DOI] [PubMed] [Google Scholar]
  24. Schiaffino S., Hanzlíková V., Pierobon S. Relations between structure and function in rat skeletal muscle fibers. J Cell Biol. 1970 Oct;47(1):107–119. doi: 10.1083/jcb.47.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schiaffino S., Margreth A. Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J Cell Biol. 1969 Jun;41(3):855–875. doi: 10.1083/jcb.41.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shafiq S. A., Gorycki M. A., Milhorat A. T. An electron microscope study of fibre types in normal and dystrophic muscles of the mouse. J Anat. 1969 Mar;104(Pt 2):281–293. [PMC free article] [PubMed] [Google Scholar]
  27. Shimada Y., Fischman D. A., Moscona A. A. The fine structure of embryonic chick skeletal muscle cells differentiated in vitro. J Cell Biol. 1967 Nov;35(2):445–453. doi: 10.1083/jcb.35.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tice L. W., Engel A. G. The effects of glucocorticoids on red and white muscles in the rat. Am J Pathol. 1967 Feb;50(2):311–333. [PMC free article] [PubMed] [Google Scholar]
  29. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walker S. M., Schrodt G. R., Bingham M. Electron microscope study of the sarcoplasmic reticulum at the Z line level in skeletal muscle fibers of fetal and newborn rats. J Cell Biol. 1968 Nov;39(2):469–475. doi: 10.1083/jcb.39.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Walker S. M., Schrodt G. R. Triads in foetal skeletal muscle. Nature. 1967 Dec 9;216(5119):985–988. doi: 10.1038/216985a0. [DOI] [PubMed] [Google Scholar]

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