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Subsarcolemmal mitochondria and capillarization of soleus muscle fibers in young rats subjected to an endurance training

A morphometric study of semithin sections

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Summary

Rats, 6 weeks old, were subjected to a program of endurance running for 3, 6 and 12 weeks. 0.5 to 0.8 μm thick sections of Epon embedded soleus muscles were studied with morphometric methods.

In cross-sections the area occupied by subsarcolemmal mitochondria was independent of the age, but was 53% higher after 12 weeks of training. The mean depth of the zones with subsarcolemmal mitochondria increased only 15% to about 0.9 μm. Thus, the subsarcolemmal mitochondria showed a pronounced spreading at the muscle fiber surface in trained muscles. — The number of capillaries per fiber decreased slightly in controls and increased not significantly in trained muscles.

It is concluded that the subsarcolemmal mitochondria supply the energy for the active transport of metabolites through the sarcolemma in oxidative muscle fibers, and that they are the limiting factor for endurance performance of the soleus muscle fibers because the changes in the capillarization were only small. It is suggested that the subsarcolemmal and the interfibrillar mitochondria have different functions and may therefore represent different types of mitochondria which can be distinguished by their morphology as well as by their biochemical properties.

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References

  • Ariano, M.A., Armstrong, R.B., Edgerton, V.R.: Hindlimb muscle fiber populations of five mammals. J. Histochem. Cytochem. 21, 51–55 (1973)

    Google Scholar 

  • Ashmore, C.R., Tompkins, G., Doerr, L.: Comparative aspects of mitochondria isolated from αW, αR, and βR muscle fibers of the chick. Exp. Neurology 35, 413–420 (1972)

    Google Scholar 

  • Baldwin, K.M., Reitman, J.S., Terjung, R.L., Winder, W.W., Holloszy, J.O.: Substrate depletion in different types of muscle and in liver during prolonged running. Amer. J. Physiol. 225, 1045–1050 (1973)

    Google Scholar 

  • Benzi, G., Panceri, P., Bernardi, M. de, Villa, R., Arcelli, E., d'Agnelo, L., Arrigoni, E., Berté, F.: Mitochondrial enzymatic adaptation of skeletal muscle to endurance training. J. appl. Physiol. 38, 565–569 (1975)

    Google Scholar 

  • Berger, E.R.: Two morphologically different mitochondrial populations in the rat hepatocyte as determined by quantitative three-dimensional electron microscopy. J. Ultrastruct. Res. 45, 303–327 (1973)

    Google Scholar 

  • Bing, O.H.L., Brooks, W.W., Messer, J.V.: Prolongation of tension on reoxygenation following myocardial hypoxia: A possible role for mitochondria in muscle relaxation. J. molec. cell. Cardiol. 8, 205–215 (1976)

    Google Scholar 

  • Bloor, C.M., Leon, A.S.: Interaction of age and exercise on the heart and its blood supply. Lab. Invest. 22, 160–165 (1970)

    Google Scholar 

  • Borensztajn, J., Rone, M.S., Babirak, S.P., McGarr, J.A., Oscai, L.B.: Effect of exercise on lipoprotein lipase activity in rat heart and skeletal muscle. Amer. J. Physiol. 229, 394–397 (1975)

    Google Scholar 

  • Bullock, G.R., Carter, E.E., White, A.M.: The analysis of rat skeletal muscle mitochondria isolated by the method of tryptic lysis. Biochim. biophys. Acta (Amst.) 292, 350–359 (1973)

    Google Scholar 

  • Burri, P.H., Giger, H., Gnägi, H.R., Weibel, E.R.: Application of stereological methods to cytophysiologic experiments on polarized cells. 4th Europ. Regional Conf. Electron Microscopy, Vol. 1, 593–594 (1968)

    Google Scholar 

  • Carafoli, E.: Mitochondria, Ca2+ transport and the regulation of heart contraction and metabolism. J. molec. cell. Cardiol. 7, 83–89 (1975)

    Google Scholar 

  • Carrow, R.E., Brown, R.E., Van Huss, W.D.: Fiber sizes and capillary to fiber ratios in skeletal muscle of exercised rats. Anat. Rec. 159, 33–40 (1967)

    Google Scholar 

  • Clark, B.J., Coburn, R.F.: Mean myoglobin oxygen tension during exercise at maximal oxygen uptake. J. appl. Physiol. 39, 135–144 (1975)

    Google Scholar 

  • Clausen, J.P.: Effects of physical conditioning. A hypothesis concerning circulatory adjustment to exercise. Scand. J. clin. Lab. Invest. 24, 305–313 (1969)

    Google Scholar 

  • Clausen, J.P., Klausen, K., Rasmussen, B., Trap-Jensen, J.: Central and peripheral circulatory changes after training of the arms or legs. Amer. J. Physiol. 225, 675–682 (1973)

    Google Scholar 

  • Close, R.I.: Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52, 129–197 (1972)

    Google Scholar 

  • Cotter, M., Hudlická, O., Pette, D., Staudte, H., Vrbová, G.: Changes of capillary density and enzyme pattern in fast rabbit muscles during long-term stimulation. J. Physiol. (Lond.) 230, 34–35P (1973)

    Google Scholar 

  • Dadoune, J.P.: Protein turnover in striated muscle as visualized by radioautography after (3H)leucine administration. Exp. Cell Res. 97, 31–41 (1976)

    Google Scholar 

  • Dölken, G., Pette, D.: Turnover of several glycolytic enzymes in rabbit heart, soleus muscle and liver. Hoppe-Seylers Z. physiol. Chem. 355, 289–299 (1974)

    Google Scholar 

  • Edgerton, V.R.: Morphology and histochemistry of the soleus muscle from normal and exercised rats. Amer. J. Anat. 127, 81–88 (1969)

    Google Scholar 

  • Eisenberg, B.R., Kuda, A.M., Peter, J.B.: Stereological analysis of mammalian skeletal muscle. J. Cell Biol. 60, 732–754 (1974)

    Google Scholar 

  • Eisenberg, B.R., Mobley, B.A.: Size changes in single muscle fibers during fixation and embedding. Tissue Cell 7, 383–387 (1975)

    Google Scholar 

  • Fitts, R.H., Booth, F.W., Winder, W.W., Holloszy, J.O.: Skeletal muscle respiratory capacity, endurance, and glycogen utilization. Amer. J. Physiol. 228, 1029–1033 (1975)

    Google Scholar 

  • Folkow, B., Halicka, H.D.: A comparison between “red” and “white” muscle with respect to blood supply, capillary surface area and oxygen uptake during rest and exercise. Microvasc. Res. 1, 1–14 (1968)

    Google Scholar 

  • Fronek, K., Zweifach, B.W.: Microvascular pressure distribution in skeletal muscle and the effect of vasodilation. Amer. J. Physiol. 228, 791–796 (1975)

    Google Scholar 

  • Fuchs, H.D.: Qualitative and quantitative elektronenmikroskopische Untersuchungen an Querschnitten des musculus soleus euthyreoter und hyperthyreoter Ratten. M.D. Thesis, University of Ulm, W.-Germany 1970

    Google Scholar 

  • Funderburk, C.F., Hipskind, S.G., Welton, R.C., Lind, A.R.: Development of and recovery from fatigue induced by static effort at various tensions. J. appl. Physiol. 37, 392–396 (1974)

    Google Scholar 

  • Galavazi, G., Szirmai, J.A.: Cytomorphometry of skeletal muscle: The influence of age and testosterone on the rat m. levator ani. Z. Zellforsch. 121, 507–530 (1971)

    Google Scholar 

  • Gauthier, G.F.: On the relationship of ultrastructural and cytochemical features to color in mammalian skeletal muscle. Z. Zellforsch. 95, 462–482 (1969)

    Google Scholar 

  • Gauthier, G.F.: Some ultrastructural and cytochemical features of fiber populations in the soleus muscle. Anat. Rec. 180, 551–564 (1974)

    Google Scholar 

  • Gauthier, G.F., Padykula, H.E.: Cytological studies of fiber types in skeletal muscle. J. Cell Biol. 28, 333–354 (1966)

    Google Scholar 

  • Goldberg, A.L.: Protein synthesis in tonic and phasic skeletal muscles. Nature (Lond.) 216, 1219–1220 (1967)

    Google Scholar 

  • Goldberg, A.L.: Mechanisms of growth and atrophy of skeletal muscle. In: Muscle biology, Vol. 1, pp. 89–115 (R.G. Cassens, ed.). New York: Marcel Dekker 1972

    Google Scholar 

  • Golisch, G., Pette, D., Pichlmaier, H.: Metabolic differentiation of rabbit skeletal muscle as induced by specific innervation. Europ. J. Biochem. 16, 110–116 (1970)

    Google Scholar 

  • Granger, H.J., Shepherd, A.P., Jr.: Intrinsic microvascular control of tissue oxygen delivery. Microvasc. Res. 5, 49–72 (1973)

    Google Scholar 

  • Gray, S.D.: Ontogenic development of vascular reactivity in fast and slow muscles of the neonatal rat hindlimb. Angiologica 9, 1–10 (1972)

    Google Scholar 

  • 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. 26, 555–578 (1965)

    Google Scholar 

  • Hall-Craggs, E.C.B.: The longitudinal division of fibres in overloaded rat skeletal muscle. J. Anat. (Lond.) 107, 459–470 (1970)

    Google Scholar 

  • Hall-Craggs, E.C.B., Lawrence, C.A.: Longitudinal fibre division in skeletal muscle: A light- and electronmicroscopic study. Z. Zellforsch. 109, 481–494 (1970)

    Google Scholar 

  • Hermansen, L., Wachtlova, M.: Capillary density of skeletal muscle in well-trained and untrained men. J. appl. Physiol. 30, 860–863 (1971)

    Google Scholar 

  • Holloszy, J.O.: Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. biol. Chem. 242, 2278–2282 (1967)

    Google Scholar 

  • Hoppeler, H., Lüthi, P., Claassen, H., Weibel, E.R., Howald, H.: The ultrastructure of the normal human skeletal muscle. Pflügers Arch. 344, 217–232 (1973)

    Google Scholar 

  • Hort, W.: Quantitative Untersuchungen über die Capillarisierung des Herzmuskels im Erwachsenen-und Greisenalter, bei Hypertrophie und Hyperplasie. Virchows Arch. path. Anat. 327, 560–576 (1955)

    Google Scholar 

  • Howells, K.F., Goldspink, G.: The effects of age and exercise on the succinic dehydrogenase content of individual muscle fibres from fast, slow and mixed hamster muscles. Histochemistry 38, 195–201 (1974)

    Google Scholar 

  • Hudlická, O., Pette, D., Staudte, H.: The relation between blood flow and enzymatic activities in slow and fast muscles during development. Pflügers Arch. 343, 341–356 (1973)

    Google Scholar 

  • James, N.T.: A study of the distribution of mitochondria in some oxidative muscle fibres of the pig. J. neurol. Sci. 23, 565–573 (1974)

    Google Scholar 

  • Karnovsky, M.J.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967)

    Google Scholar 

  • Keul, J., Haralambie, G., Trittin, G.: Intermittent exercise: arterial lipid substrates and arteriovenous differences. J. appl. Physiol. 36, 159–162 (1974)

    Google Scholar 

  • Kiessling, K.-H., Pilström, L., Bylund, A.-C., Saltin, B., Piehl, K.: Correlation between morphometrical and functional parameters in human skeletal muscle. J. Ultrastruct. Res. 44, 439 (1973a)

    Google Scholar 

  • Kiessling, K.-H., Pilström, L., Karlssön, J., Piehl, K.: Mitochondrial volume in skeletal muscle from young and old physically untrained and trained healthy men and from alcoholics. Clin. Sci. 44, 547–554 (1973b)

    Google Scholar 

  • Kistler, A., Weber, R.: A morphometric analysis of inner membranes related to biochemical characteristics of mitochondria from heart muscle and liver in mice. Exp. Cell Res. 91, 326–332 (1975)

    Google Scholar 

  • Kowalski, K., Gordon, E.E., Martinez, A., Adamek, J.: Changes in enzyme activities of various muscle fiber types in rat induced by different exercises. J. Histochem. Cytochem. 17, 601–607 (1969)

    Google Scholar 

  • Kraus, H., Kirsten, R., Wolff, J.R.: Die Wirkung von Schwimm- und Lauftraining auf die celluläre Funktion und Struktur des Muskels. Pflügers Arch. ges. Physiol. 308, 57–79 (1969)

    Google Scholar 

  • Kubišta, V., Kubištová, 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. Europ. J. Biochem. 18, 553–560 (1971)

    Google Scholar 

  • Lie, H.R.: A quantitative identification of three muscle fiber types in the body muscles of Lampetra fluviatilis, and their relation to blood capillaries. Cell Tiss. Res. 154, 109–119 (1974)

    Google Scholar 

  • Lišková, Z., Strunecká, A., Drahota, Z.: The metabolic activity and equipment of the mitochondrial membranes of different tissues. Physiol. Bohemoslov. 23, 229–234 (1974)

    Google Scholar 

  • Mai, J.V., Edgerton, V.R., Barnard, R.J.: Capillarity of red, white and intermediate muscle fibers in trained and untrained guinea-pigs. Experientia (Basel) 26, 1222–1223 (1970)

    Google Scholar 

  • Maxwell, L.C., Faulkner, J.A., Lieberman, D.A.: Histochemical manifestations of age and endurance training in skeletal muscle fibers. Amer. J. Physiol. 224, 356–361 (1973)

    Google Scholar 

  • McCallister, L.P., Page, E.: Effects of thyroxin on ultrastructure of rat myocardial cells: A stereological study. J. Ultrastruct. Res. 42, 136–155 (1973)

    Google Scholar 

  • Müller, W.: Temporal progress of muscle adaptation to endurance training in hind limb muscles of young rats. Cell Tiss. Res. 156, 61–87 (1974)

    Google Scholar 

  • Müller, W.: Isometric training of young rats — effects upon hind limb muscles. Cell Tiss. Res. 161, 225–237 (1975a)

    Google Scholar 

  • Müller, W.: A method for the comparison of morphometrical data on skeletal muscles in young rats of different ages and body weights. Histochemistry 43, 241–248 (1975b)

    Google Scholar 

  • Munn, E.A.: Ultrastructure of mitochondria. In: Handbook of molecular cytology, pp. 875–913 (A. Lima-de-Faria, ed.). Amsterdam-London: North-Holland Publ. Co. 1969

    Google Scholar 

  • Pařizková, J., Wachtlová, M., Soukupová, M.: The impact of different motor activity on body composition, density of capillaries and fibers in the heart and soleus muscles, and cell's migration in vitro in male rats. Int. Z. angew. Physiol. 30, 207–216 (1972)

    Google Scholar 

  • Peter, J.B., Barnard, R.J., Edgerton, V.R., Gillespie, C.A., Stempel, K.E.: Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633 (1972)

    Google Scholar 

  • Pette, D.: Mitochondrial enzyme activities. In: Regulation of metabolic processes in mitochondria, pp. 28–50 (J.M. Tager, S. Papa, E. Quagliariello, E.C. Slater, eds.). Amsterdam: Elsevier Publ. Co. 1966

    Google Scholar 

  • Pette, D., Müller, W., Leisner, E., Vrbová, G.: Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism. Pflügers Arch, (in press)

  • Plyley, M.J., Groom, A.G.: Geometrical distribution of capillaries in mammalian striated muscle. Amer. J. Physiol. 228, 1376–1383 (1975)

    Google Scholar 

  • Price, H.M., Howes, E.L., Sheldon, D.B., Hutson, O.D., Fitzgerald, R.T., Blumberg, J.M., Pearson, C.M.: An improved biopsy technique for light and electron microscopic studies of human skeletal muscle. Lab. Invest. 14, 194–199 (1965)

    Google Scholar 

  • Rakušan, K., Ošt'ádal, B., Wachtlová, M.: The influence of muscular work on the capillary density in the heart and skeletal muscle of pigeon (Columbia livia dom.). Canad. J. Physiol. Pharmacol. 49, 167–170 (1971)

    Google Scholar 

  • Rakušan, K., Poupa, O.: Changes in the diffusion distance in the rat heart muscle during development. Physiol. Bohemoslov. 12, 220–227 (1963)

    Google Scholar 

  • Rakušan, K., Poupa, O.: The relationship between the capillaries and protein nitrogen in the myocardium of the rat during postnatal development. Physiol. Bohemoslov. 14, 320–323 (1965)

    Google Scholar 

  • Reis, D.J., Wooten, G.F.: The relationship of blood flow to myoglobin, capillary density, and twitch characteristics in red and white skeletal muscle in cat. J. Physiol. (Lond.) 210, 121–135 (1970)

    Google Scholar 

  • Reitsma, W.: Some structural changes in skeletal muscles of the rat after intensive training. Acta morph. neerl.-scand. 7, 229–246 (1970)

    Google Scholar 

  • Reitsma, W.: Formation of new capillaries in hypertrophie skeletal muscle. Angiology 24, 45–57 (1973)

    Google Scholar 

  • Romanul, F.C.A.: Capillary supply and metabolism of muscle fibers. Arch. Neurol. 12, 497–509 (1965)

    Google Scholar 

  • Romanul, F.C.A.: Reversal of enzymatic profiles and capillary supply of muscle fibers in fast and slow muscles after cross innervation. In: Muscle metabolism during exercise, pp. 21–32 (B. Pernow and B. Saltin, eds.). New York: Plenum Press 1971

    Google Scholar 

  • Schmalbruch, H.: “Rote” Muskelfasern. Z. Zellforsch. 119, 120–146 (1971)

    Google Scholar 

  • Schmidt-Nielsen, K., Pennycuik, P.: Capillary density in mammals in relation to body size and oxygen consumption. Amer. J. Physiol. 200, 746–750 (1961)

    Google Scholar 

  • Staudte, H.W., Exner, G.U., Pette, D.: Effects of short-term, high intensity (sprint) training on some contractile and metabolic characteristics of fast and slow muscle of the rat. Pflügers Arch. 344, 159–168 (1973)

    Google Scholar 

  • Tomanek, R.J., Asmundson, C.R., Cooper, R.R., Barnard, R.J.: Fine structure of fast-twitch and slow-twitch guinea pig muscle fibers. J. Morph. 139, 47–66 (1973)

    Google Scholar 

  • Turto, H., Lindy, S., Halme, J.: Protocollagen proline hydroxylase activity in work-induced hypertrophy of rat muscle. Amer. J. Physiol. 226, 63–65 (1974)

    Google Scholar 

  • Vaughan, H.S., Ullah, A., Goldspink, G., Nowell, N.W.: Sex and stock differences in the histochemical myofibrillar adenosine triphosphatase reaction in the soleus muscle of the mouse. J. Histochem. Cytochem. 22, 155–159 (1974)

    Google Scholar 

  • Wachtlová, M., Pařízková, J.: Comparison of capillary density in skeletal muscles of animals differing in respect of their physical activity — the hare (Lepus europaeus), the domestic rabbit (Oryctolagus domesticus), the brown rat (Rattus norvegicus) and the trained and untrained rat. Physiol. Bohemoslov. 21, 489–495 (1972)

    Google Scholar 

  • Weibel, E.R.: Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 26, 235–302 (1969)

    Google Scholar 

  • Wootton, G.S., Goodford, P.J.: The ratio of smooth muscle cell volume to cell surface area measured by electron microscopy with corrections for shrinkage. Cell Tiss. Res. 162, 75–82 (1975)

    Google Scholar 

  • Zíka, K., Lojda, Z., Kučera, M.: Activities of some oxidative and hydrolytic enzymes in musculus biceps brachii of rats after tonic stress. Histochemie 35, 153–164 (1973)

    Google Scholar 

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Müller, W. Subsarcolemmal mitochondria and capillarization of soleus muscle fibers in young rats subjected to an endurance training. Cell Tissue Res. 174, 367–389 (1976). https://doi.org/10.1007/BF00220682

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