Summary
The differentiation of Purkinje fibres and ordinary ventricular and atrial myocytes in bovine hearts was studied with specific antibodies against M-line proteins (MM-creatine kinase and myomesin) and with enzyme histochemistry (succinate dehydrogenase and mitochondrial glycerol-3-phosphate dehydrogenase). MM-creatine kinase was detected at an earlier stage in Purkinje fibres and atrial myocytes than in ordinary ventricular myocytes. The findings are in agreement with previous ultrastructural observations that an earlier appearance of a dense M-band occurs in Purkinje fibres than in ordinary ventricular myocytes. Myomesin was detected in all three cell types even at early foetal stages, in accordance with suggestions that it is an integral component of the myofibrillar structure. The activity of succinate dehydrogenase gradually increased in both ordinary ventricular and atrial myocytes, while the activity of mitochondrial glycerol-3-phosphate dehydrogenase was high at different stages of early foetal development in the two tissues, finally becoming low in the adult stage. The activity of succinate dehydrogenase and mitochondrial glycerol-3-phosphate dehydrogenase seemed to remain unchanged in the Purkinje fibres from early to late foetal stages. The present study shows that the Purkinje fibres are already different from ordinary ventricular myocytes at early foetal stages and that the two cell types differentiate in different ways. It is concluded that there are also developmental differences between ordinary ventricular and atrial myocytes.
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Allen, E. R. &Pepe, F. A. (1965) Ultrastructure of developing muscle cells in the chick embryo.Am. J. Anat. 116, 115–48.
Anversa, P., Olivetti, G., Bracchi, P.-G. &Loud, A. V. (1981) Postnatal development of the M-band in rat cardiac myofibrils.Circ. Res. 48, 561–8.
Cooper, W. G. (1955) Succinic dehydrogenase activity in the pre-natal and post-natal rat heart.Anat. Rec. 123, 103–24.
Davies, M. J. (1971)Pathology of Conducting Tissue of the Heart. pp. 20–28. London: Butterworth.
Dehaan, R. L. (1961) Differentiation of the atrioventricular conducting system of the heart.Circulation 24, 458–70.
Dubowitz, V. &Brooke, M. H. (1973) Muscle biopsy: A modern approach. pp. 20–33. London: Saunders.
Eppenberger, H. M., Perriard, J.-C., Rosenberg, U. B. &Strehler, E. E. (1981) The Mr 165,000 M-protein myomesin: A specific protein of cross-striated muscle cells.J. Cell Biol. 89, 185–93.
Eppenberger, H. M., Wallimann, T., Kuhn, H. J. &Turner, D. C. (1975) Localization of creatine kinase isoenzymes in muscle cells: Physiological significance. InIsozymes II (edited byMarkert, C.), pp. 409–24. New York: Academic Press.
Eriksson, A., Thornell, L.-E. &Stigbrand, T. (1979) Skeletin immunoreactivity in heart Purkinje fibers of several species.J. Histochem. Cytochem. 27, 1604–9.
Etlinger, J. D. &Fischman, D. A. (1973) M-and Z-band components and the assembly of myofibrils.Cold Spring Harb. Symp. quant. Biol. 37, 511–22.
Fischman, D. A. (1970) The synthesis and assembly of myofibrils in embryonic muscle.Curr. Topics Devl Biol. 5, 235–80.
Forsgren, S., Carlsson, E., Strehler, E. & Thornell, L.-E. (1982) Ultrastructural identification of human fetal Purkinje fibres—A comparative immunocytochemical and electron icroscopic study of composition and structure of myofibrillar M-regions.J. molec. Cell. Cardiol. (in press).
Forsgren, S. &Thornell, L.-E. (1981) The development of Purkinje fibres and ordinary myocytes in the bovine fetal heart. An ultrastructural study.Anat. Embryol. 162, 127–36.
Forsgren, S., Thornell, L.-E. &Eriksson, A. (1980) The development of the Purkinje fibre system in the bovine fetal heart.Anat. Embryol. 159, 125–35.
Gossrau, R. (1968) Über das Reizleitungssystem der Vögel. Histochemische und elektronenmikroskopische Untersuchungen.Histochemie 13, 111–59.
Greenfield, P. C. &Boell, E. J. (1968) Succinic dehydrogenase and cytochrome oxidase of mitochondria of chick liver, heart and skeletal muscle during embryonic development.J. exp. Zool. 168, 491–500.
Harary, I. (1979) Biochemistry of cardiac development:in vivo andin vitro studies. InHandbook of Physiology. The Cardiovascular System (edited byBerne, R. M., Sperelakis, N. andGeiger, S. R.), Vol. 1, pp. 43–60. Bethesda, Maryland: American Physiological Society.
Hirakow, R., Gotoh, T. &Watanabe, T. (1980) Quantitative studies on the ultrastructural differentiation and growth of mammalian cardiac muscle cells. I. The atria and ventricles of the rat.Acta Anat. 108, 144–52.
Kilarski, W. &Jakubowska, M. (1979) An electron microscope study of myofibril formation in embryonic rabbit skeletal muscle.Z. mikrosk.-anat. Forsch. 93, 1159–81.
Mackler, B., Grace, R. &Duncan, H. M. (1971) Studies of mitochondrial development during embryogenesis in the rat.Archs Biochem. Biophys. 144, 603–10.
Markwald, R. R. (1973) Distribution and relationship of precursor Z-material to organizing myofibrillar bundles in embryonic rat and hamster ventricular myocytes.J. molec. Cell. Cardiol. 5, 341–50.
Meijer, A. E. F. H. &Devries, G. P. (1978) Enzyme histochemical studies on the Purkinje fibres of the atrioventricular system of the bovine and porcine hearts.Histochem. J. 10, 399–408.
Nandy, K. &Bourne, G. H. (1963) A study of the morphology of the conduction tissue in mammalian hearts.Acta Anat. 53, 217–26.
Oliphant, L. W. &Loewen, R. D. (1976) Filament systems in Purkinje cells of the sheep heart: possible alterations of myofibrillogenesis.J. molec. Cell. Cardiol. 8, 679–88.
Page, E., Power, B., Fozzard, H. A. &Meddoff, D. A. (1969) Sarcolemmal evaginations with knob-like or stalked projections in Purkinje fibres of the sheep's heart.J. Ultrastruct. Res. 28, 288–300.
Peter, J. B., Barnard, R. J., Edgerton, V. R., Gillespie, C. A. &Stempel, K. E. (1972) Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits.Biochemistry 11, 2627–33.
Robb, J. S. (1965)Comparative Basic Cardiology. New York: Grune & Stratton.
Schifbler, T. H., Stark, M. &Caesar, R. (1956) Die Stoffwechsel-situation des Reizleitungssystems.Klin. Wschr. 34, 181–3.
Schiebler, T. H. (1961) Histochemische Untersuchungen am Reizleitungssystem tierischer Herzen.Naturwissenschaften 14, 502–3.
Skala, J., Drahota, Z. &Hahn, P. (1970) Succinate dehydrogenase activity of rat heart muscle mitochondria during development.Physiol. bohemoslov. 19, 15–7.
Smith, H. E. &Page, E. (1977) Ultrastructural changes in rabbit heart mitochondria during the perinatal period.Dev. Biol. 57, 109–17.
Snijder, J. &Meijer, A. E. F. H. (1970) Enzyme histochemical studies on the Purkinje fibres of canine, bovine and porcine hearts.Histochem. J. 2, 395–409.
Sordahl, L. A., Crow, C. A., Kraft, G. H. &Schwartz, A. (1972) Some ultrastructural and biochemical aspects of heart mitochondria associated with development: fetal and cardiomyopathic tissue.J. molec. Cell. Cardiol. 4, 1–10.
Strehler, E. E., Pelloni, G., Heizman, C. W. &Eppenberger, H. M. (1979) M-protein in chicken cardiac muscle.Expl Cell Res. 124, 39–45.
Strehler, E. E., Pelloni, G., Heizman, C. W. &Eppenberger, H. M. (1980) Biochemical and ultrastructural aspects of Mr 165,000 M-protein in cross-striated chicken muscle.J. Cell Biol. 86, 775–83.
Tanimura, T. &Shepard, T. H. (1970) Glucose metabolism by rat embryosin vitro.Proc. Soc. exp. Biol. Med. 135, 51–4.
Thornell, L.-E. (1974) Distinction of glycogen and ribosome particles in cow Purkinje fibres by enzymatic digestion en bloc and in sections.J. Ultrastruct. Res. 49, 157–66.
Toth, A. &Schiebler, T. H. (1967) Über die Entwicklung der Arbeits- und Erregungsleitungsmuskulatur des Herzens von Ratte und Meerschweinchen. Histologische, histochemische und elektrophysiologische Untersuchungen.Z. Zellforsch. 76, 543–67.
Truex, R. C. &Smythe, M. Q. (1965) Comparative morphology of the cardiac conduction tissue in animals.Ann. N.Y. Acad. Sci. 127, 19–33.
Turner, D. C., Wallimann, T. &Eppenberger, H. M. (1973) A protein that binds specifically to the M-line of skeletal muscle is identified as the muscle form of creatine kinase.Proc. natn. Acad. Sci., U.S.A. 70, 702–5.
Virách, S. &Challice, C. E. (1977) The development of the conduction system in the mouse embryo heart.Dev. Biol. 56, 397–411.
Wallimann, T., Pelloni, G., Turner, D. C. &Eppenberger, H. M. (1978) Monovalent antibodies against MM-creatine kinase remove the M-line from myofibrils.Proc. natn. Acad. Sci., U.S.A. 75, 4296–300.
Wallimann, T., Turner, D. C. &Eppenberger, H. M. (1977) Localization of creatine kinase isoenzymes in myofibrils. I. Chicken skeletal muscle.J. Cell Biol. 75, 297–317.
Wendler, D. (1967) Die morphologische und chemische Organisation des fetalen und reifen Myokards.Z. inn. Med. 22, 737–46.
Weidmann, S. (1971) The Purkyne fibres of ungulate hearts. InCentenary Symposium (edited byKruta, V.), p. 227. Brno: Universita Jana Evangelisty Purkyne.
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Forsgren, S., Strehler, E. & Thornell, LE. Differentiation of Purkinje fibres and ordinary ventricular and atrial myocytes in the bovine heart: an immuno-and enzyme histochemical study. Histochem J 14, 929–942 (1982). https://doi.org/10.1007/BF01005234
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DOI: https://doi.org/10.1007/BF01005234