Summary
The disposition of transverse (T) tubules, sarcoplasmic reticulum (SR) and T-SR junctions (triads) and the width of Z lines are matched to contractile properties in adult muscle fibres. We have studied the development of the membrane systems in the slow anterior (ALD) and the fast posterior (PLD) latissimus dorsi of the chicken in ovo (E14–E21) and after hatching (D1–D30). T tubules, SR, triads and Z lines were visualized using DiIC16[3] labelling for confocal microscopy and either Ca-osmium-ferrocyanide or standard procedures for electron microscopy. Anterior latissimus dorsi and PLD have similar, slow twitches in early development (E14–E16), but PLD suddenly becomes faster starting at E17–E18. We find that in coincidence with the differentiation of faster contraction properties (starting at E18–E19) density of triads is significantly higher and width of Z lines is narrower in PLD. The SR also begins to acquire fibre-type specific characteristics at this time. Early development of T tubules, on the other hand, is quite similar in the two muscles. Peripherally-located, longitudinally-oriented T tubules, and the first T networks crossing the fibre center appear earlier in ALD (E14–E15 and E16) than in PLD (E14–E16 and E17), but have similar dispositions. The final fibre-type specific distribution of T tubules is achieved after hatching. Some T tubules-rich fibres in the ALD, presumably future fast fibres, develop extensive T tubule networks at early stages. Location of triads at the Z line in pectoralis occurs in three steps: an initial location of longitudinally oriented triads at the A-I junction; a subsequent move to the Z lines and finally a rotation to a transverse orientation.
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References
AKSTER, H. A., GRANZIER, H. L. M. & TER KEURS, H. E. D. J. (1985) A comparison of quantitative ultrastructural and contractile characteristics of muscle fibre type of the perch, Perca fluviatilis L. J. Comp. Physiol. (B) 155, 685–91.
APPELT, D., BUENVIAJE, B., CHAMP, C. & FRANZINI-ARMSTRONG, C. (1989) Quantitation of ‘junctional feet’ content in two types of muscle fiber from hind limb muscles of the rat. Tissue and Cell 21, 783–94.
APPELT, D., SHEN, V. & FRANZINI-ARMSTRONG, C. (1991) Quantitation of Ca ATPase, feet and mitochondria in superfast muscle fibres from the toadfish, Opsanus tau. J. Muscle Res. Cell Motil. 12, 543–52.
ARNDT, I. & PEPE, F. A. (1975) Antigen specificity of red and white muscle myosin. J. Histochem. Cytochem. 23, 159–68.
BANDMAN, E. & BENNETT, T. (1988) Diversity of fast myosin heavy chain expression during development of gastrocnemius, bicep brachii, and posterior latissimus dorsi muscles in normal and dystrophic chickens. Dev. Biol. 130, 220–31.
BANDMAN, E., MATSUDA, R. & STROHMAN, R. C. (1982) Developmental appearance of myosin heavy and light chain isoforms in vivo and in vitro in chicken skeletal muscle. Dev. Biol. 93, 508–18.
BAUMANN, O., KITAZAWA, T. & SOMLYO, A. P. (1990). Laser confocal scanning microscopy of the surface membrane/T-tubular system and the sarcoplasmic reticulum in insect striated muscle stained with DiIC18 (3). J. Structural Biol. 105, 154–61.
BRAY, D. F. & RAYNS, D. G. (1976) A comparative freeze-etch study of the sarcoplasmic reticulum of avian fast and slow muscle fibres. J. Ultrastruct. Res. 57, 251–62.
BUTLER, J. & COSMOS, E. (1981) Differentiation of the avian latissimus dorsi primordium: analysis of fiber type expression using the myosin ATPase histochemical reaction. J. Exp. Zool. 218, 219–32.
BUTLER, J., COSMOS, E. & BRIERLEY, J. (1982) Differentiation of muscle fiber types in aneurogenic brachial muscles of the chick embryo. J. Exp. Zool. 224, 65–80.
CLOSE, R. (1972) Dynamic properties of mammalian skeletal muscle. Physiol. Rev. 52, 129–97.
COSTANTIN, L. L., PODOLSKY, R. J. & TICE, L. W. (1967) Calcium activation of frog slow muscle fibres. J. Physiol. 188, 261–71.
DHOOT, G. K. (1988) Identification and distribution of the fast class of troponin T in the adult and developing avian skeletal muscle. J. Muscle Res. Cell Motil. 9, 446–55.
EISENBERG, B. R. (1983) Quantitative ultrastructure of mammalian skeletal muscle. In Handbook of Physiology, Section 10, Skeletal Muscle (edited by PEACHEY, L. D., ADRIAN, R. H. & GEIGER, S. R.) pp. 73–112. Bethesda: American Physiological Society.
EISENBERG, B. R., DIX, D. J., LIN, Z. W. & WENDEROTH, M. P. (1987) Relationship of membrane systems in muscle to isomyosin content. Can. J. Physiol. Pharmacol. 65, 598–605.
FORBES, M. S., PLANTHOLT, B. A. & SPERELAKIS, N. (1977) Cytochemical staining procedures selective for sarcotubular systems of muscle: modifications and applications. J. Ultrastruct. Res. 60, 306–27.
FLUCHER, B. E., TAKEKURA, H. & FRANZINI-ARMSTRONG, C. (1993) Association of sarcoplasmic reticulum and transverse tubules with myofibrils in developing muscle fibers. Dev. Biol., in press.
FRANZINI-ARMSTRONG, C. (1986) The sarcoplasmic reticulum and the transverse tubules. In Myology (Edited by ENGEL, A. G. & BANKER, B. Q.) pp. 125–54. New York: McGraw-Hill Book Co.
FRANZINI-ARMSTRONG, C. (1991) Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Develop. Biol. 146, 353–63.
FRANZINI-ARMSTRONG, C., GILLY, W. F., ALADJEM, E. & APPELT, D. (1987) Golgi stain identifies three types of fibres in fish muscle. J. Muscle Res. Cell Motil. 8, 418–27.
FRANZINI-ARMSTRONG, C., FERGUSON, D. G. & CHAMP, C. (1988) Discrimination between fast and slow twitch fibres in guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J. Muscle Res. Cell Motil. 9, 403–14.
GARDAHAUT, M.-F., ROUAUD, T., RENAUD, D. & LEDOUARIN, G. (1988) Developmental changes in myosin isoforms from slow and fast latissimus dorsi muscles in the chicken. Differentiation 37, 81–5.
GAUTHIER, G. F. & HOBBS, A. W. (1986) Freeze-fractured sarcoplasmic reticulum in adult and embryonic fast and slow muscles. J. Muscle Res. Cell Motil. 7, 122–32.
GAUTHIER, G. F. & LOWEY, S. (1977) Polymorphism of myosin among skeletal muscle fiber types. J. Cell Biol. 74, 760–79.
GINSBORG, B. C. (1960) Some properties of avian skeletal muscle fibres with multiple neuromuscular junctions. J. Physiol. 154, 581–98.
GORDON, T. & VRBOVA, G. (1975) The influence of innervation on the differentiation of contractile speeds of developing chick muscles. Pflugers Arch. 360, 199–218.
GORDON, T., PURVES, R. D. & VRBOVA, G. (1977) Differentiation of electrical and contractile properties of slow and fast muscle fibres. J. Physiol. 269, 535–47.
KAPRIELIAN, Z. & FAMBROUGH, D. M. (1987) Expression of fast and slow isoforms of the Ca2+-ATPase in developing chick skeletal muscle. Dev. Biol. 124, 490–503.
KIDD, P. M. & YASUMURA, T. (1982) T system abnormalities in differentiating skeletal fibers of dystrophic chickens. Muscle and Nerve 5, 471–8.
MARTONOSI, A., ROUL, D., HA, B. & BOLAND, R. (1980) The biosynthesis of sarcoplasmic reticulum. Fed. Proc. 39, 2415–21.
MCLENNAN, L. S. (1983) Differentiation of muscle fiber types in the chicken hindlimb. Dev. Biol. 97, 222–8.
NUNZI, G. & FRANZINI-ARMSTRONG, C. (1980) Trabecular network in adult skeletal muscle. J. Ultrastruct. Res. 73, 21–6.
OGATA, T. (1988) Morphological and cytochemical features of fiber types in vertebrate skeletal muscle. CRC Critical Rev. Anat. Cell Biol. 1, 229–75.
PAGE, S. G. (1965) A comparison of the fine structure of frog slow and twitch fibers. J. Cell Biol. 26, 477–97.
PAGE, S. G. (1969) Structure and some contractile properties of fast and slow muscle of the chicken. J. Physiol. 205, 131–45.
PETTE, D., VRBOVA, G. & WHALES, R. C. (1979) Independent development of contractile properties and myosin light chains in embryonic chick fast and slow muscle. Pflugers Arch. 378, 251–7.
REID, S. K., KENNEDY, J. M., SHIMIZU, N., STEWART, A., VRBOVA, G. & ZAK, R. (1989) Regulation of expression of avian slow myosin heavy-chain isoforms. Biochem. J. 260, 449–54.
REISER, P. J. & STOKES, B. T. (1982) Development of contractile properties in avian embryonic skeletal muscle. Am. J. Physiol. 242 (Cell Physiol. 12), C52–8.
REISER, P. J., STOKES, B. T. & RALL, J. A. (1982) Isometric contractile properties and velocity of shortening during avian myogenesis. Am. J. Physiol. 243 (Cell Physiol. 12), C177–83.
REISER, P. J., GREASER, M. L. & MOSS, R. L. (1988) Myosin heavy chain composition of single cells from avian slow skeletal muscle is strongly correlated with velocity of shortening during development. Dev. Biol. 129, 400–7.
REISER, P. J., GREASER, M. L. & MOSS, R. L. (1992) Developmental changes in troponin T isoform expression and tension production in chicken single skeletal muscle fibres. J. Physiol. 449, 573–88.
RYAN, D. M. & SHAFIQ, S. A. (1980) A freeze-fracture of the anterior and posterior latissimus dorsi muscles of the chicken. Anat. Rec. 198, 147–61.
SCHMALBRUCH, H. (1979) The membrane systems in different fibre types of the triceps surae of cat. Cell Tissue Res. 204, 187–200.
SOMMER, J. R. & WAUGH, R. A. (1976) The ultrastructure of the mammalian cardiac muscle cell with special emphasis on the tubular membrane system. Am. J. Pathol. 82, 192–232.
STOCKDALE, F. & MILLER, J. B. (1987) The cellular basis of myosin heavy chain isoform expression during development of avian skeletal muscles. Dev. Biol. 123, 1–9.
WALKER, S. M., SCHRODT, G. R. & BINGHAM, M. (1969) Evidence for connections of the sarcoplasmic reticulum with the sarcolemma and with the Z line in skeletal muscle fibers of fetal and newborn rats. Am. J. Phys. Med. 48, 63–77.
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Takekura, H., Shuman, H. & Franzini-Armstrong, C. Differentiation of membrane systems during development of slow and fast skeletal muscle fibres in chicken. J Muscle Res Cell Motil 14, 633–645 (1993). https://doi.org/10.1007/BF00141560
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DOI: https://doi.org/10.1007/BF00141560