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Ultrastructure of muscle fibers and cells synthesizing DNA in lymph hearts of developing frogs and chick embryos

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The ultrastructure of striated muscle fibers and 3H-thymidine (3HTdr)-labeled cells adjacent to them in the lymph hearts of larvae of Rana temporaria, yearling frogs, and 9- to 13-day-old chick embryos was studied by use of electron-microscopic autoradiography. A comparatively high level of differentiation of lymph-heart muscle fibers was observed not only in yearling frogs but also in larvae. Myosatellites occurred at all stages of development. No mitoses were found in muscle fibers. In 9- to 13-day-old chick embryos the myofibers of lymph hearts were somewhat less differentiated than those of the larvae and yearling frogs. Differentiating sarcomeres were often seen in the sarcoplasm of myofibers of chick embryos. The analysis of the ultrastructure of 3HTdr-incorporating cells shows that 2–4 h after the single 3HTdr administration only mononucleated cells devoid of myofilaments are commonly labeled both in tadpoles and chick embryos. When fixation is postponed by 48–70 h, myonuclei frequently become labeled. Thus, the data obtained support the evidence that proliferation and differentiation processes in the developing muscle tissue of the lymph heart of both species studied are mutually exclusive, similar to the situation in differentiating vertebrate skeletal muscle.

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  1. Bencosme SA, Berger JM (1971) Specific granules in mammalian and nonmammalian vertebrate cardiomyocytes. In: Bajusz E, Jasmin G (eds) Methods and achievements in experimental pathology, Vol 5, Functional morphology of the heart. Karger, Basel New York, pp 173–213

  2. Berens von Rautenfeld D, Budras KD (1981) TEM and SEM investigations of lymph heart in birds. Lymphology 14:186–190

  3. Brodsky WYa, Arefyeva AM, Uryvaeva IV (1980) Mitotic polyploidization of mouse heart myocytes during the first postnatal week. Cell Tissue Res 210:133–144

  4. Budge A (1882) Über Lymphherzen bei Hühnerembryonen. Müllers Arch Anat Physiol (cited by Kampmeier 1969)

  5. Cantin M, Tautu C, Ballak M, Yunge L, Benchimol S, Beuzeron J (1980) Ultrastructural cytochemistry of atrial muscle cells. IX. Reactivity of specific granules in cultured cardiocytes. J Mol Cell Cardiol 12:1033–1051

  6. Cheredeeva EA (1951) Histological features of lymph-heart muscle in the frog (in Russian). Dokl Akad Nauk SSSR 76:897–900

  7. Cheredeeva EA (1953) Regeneration of lymph hearts of the frog (in Russian). Dokl Akad Nauk SSSR 92:847–850

  8. Cobb JL, Bennett T (1970) An ultrastructural study of mitotic division in differentiated gastric smooth muscle cell. Z Zellforsch 108:177–189

  9. Dabagyan NV, Sleptsova LA (1975) The frog — Rana temporaria. (in Russian). In: Detlaf TA, Astaurov BL (eds) Experimental animals in developmental biology. Nauka, Moskva, pp 442–462

  10. Del Castillo J, Sanchez V (1961) The electrical activity of the amphibian lymph heart. J Cell Comp Physiol 57:29–45

  11. Fedorowicz S (1913) Untersuchungen über die Entwicklung der Lymphgefäße bei Anurenlarven. Bull Int Acad Sci Pol Cracovie, (Ser B):290–297

  12. Fischman DA (1972) Development of striated muscle. In: Bourne GH (ed) The structure and function of muscle, Vol 1, Part 1. Academic Press, New York London, pp 75–142

  13. Gräbner W, Pfitzer P (1974) Number of nuclei in isolated myocardial cells of pigs. Virchows Arch (Cell Pathol) 15:279–294

  14. Hamburger W, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–93

  15. Hanak H, Böck P (1971) Die Feinstruktur der Muskel-Sehnenverbindung von Skelett- und Herzmuskel. J Ultrastruct Res 36:68–85

  16. Heine H (1979) Funktionelle Morphologie und Ultrazytochemie der spezifischen Granula der Vorhofmuskelzellen bei Säugetieren. Acta Anat 105:86–93

  17. Hoyer MH (1908) Untersuchungen über das Lymphgefäßsystem der Froschlarven. II Teil. Bull Int Acad Sci Pol Cracovie (MathNat Kl), 451–464

  18. Iosifov GM (1904) On the concept of the lymphatic system in the tadpole, frog and lizard (in Russian). Zap Imper Akad. Nauk 15, 11:1–17

  19. Ishikawa H, Bischoff R, Holtzer H (1968) Mitosis and intermediate-sized filaments in developing skeletal muscle. J Cell Biol 38:538–555

  20. Itina NA (1959) Functional properties of nerve-muscle devices of lower vertebrates (in Russian). Izd Akad Nauk SSSR, Moskva Leningrad

  21. Jolly J, Lieure C (1934) Formation des myofibrilles dans les coeurs lymphatiques des larves d'Anoures. C R Soc Biol (Paris) 115:124–127

  22. Kampmeier OF (1969) Evolution and comparative morphology of the lymphatic system. Charles C Thomas, Springfield Illinois

  23. Karrer HE (1959) The striated musculature of blood vessels. I. General cell morphology. J Biophys Biochem Cytol 6:383–392

  24. Katzberg AA, Farmer BB, Harris RA (1977) The predominance of binucleation in isolated rat heart myocytes. Am J Anat 149:489–500

  25. Kawaguti S (1967) Electron microscopic study on the cross striated muscle in the frog lymph heart. Biol J Okayama Univ 13:13–22

  26. Klika E, Jarkovskà D (1976) The myocardium of the intrapulmonary veins in mammals. Academia, Praha

  27. Kühn H, Richards JG, Tranzer JP (1975) The nature of rat “specific heart granules” with regard to catecholamines: an investigation by ultrastructural cytochemistry. J Ultrastruct Res 50:159–166

  28. Larra F, Droz B (1970) Techniques radioautographiques et leur application a l'étude du renouvellement des constituants cellulaires. J Microsc 9:845–880

  29. Lentz TL (1973) Myogenesis: differentiation of skeletal muscle fibers. In: Coward SJ (ed) Developmental regulation. Aspects of cell differentiation. Academic Press, New York London, pp 169–192

  30. Lindner E, Schaumburg G (1968) Zytoplasmatische Filamente in den quergestreiften Muskelzellen des kaudalen Lymphherzens von Rana temporaria. I. Untersuchungen von Lymphherzen. Z Zellforsch 84:549–562

  31. Ludatscher RM (1968) Fine structure of the muscular wall of rat pulmonary veins. J Anat 103:345–357

  32. Manasek FJ (1968) Mitosis in developing cardiac muscle. J Cell Biol 37:191–196

  33. Manasek FJ (1973) Some comparative aspects of cardiac and skeletal myogenesis. In: Coward SJ (ed) Developmental regulation. Aspects of cell differentiation. Academic Press, New York London, pp 193–218

  34. Markozashvili MI, Rumyantsev PP (1983) Muscle tissue histogenesis in chick embryo lymph heart (in Russian, English summary). Tsitologiya 25:1120–1127

  35. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–497

  36. Mauro A (ed) (1979) Muscle regeneration. Raven Press, New York

  37. McNutt NS (1970) Ultrastructure of intercellular junction in adult and developing cardiac muscle. Am J Cardiol 25:169–183

  38. Müller J (1834) Über die Existenz von 4 getrennten, regelmäßig pulsierenden Herzen, welche mit dem lymphatischen System in Verbindung stehen. Arch Anat Physiol Wiss Med 296–299

  39. Myklebust R, Engedal H, Saetersdal TS, Ulstein M (1977) Primary 9 + 0 cilia in the embryonic and adult human heart. Anat Embryol 151:127–139

  40. Nakao T (1976) Some observations on the fine structure of the myotendinous junction in myotomal muscles of the tadpole tail. Cell Tissue Res 166:241–254

  41. Przybylski R (1971) Occurrence of centrioles during skeletal and cardiac myogenesis. J Cell Biol 49:214–220

  42. Ragozina MN (1975) The domestic fowl — Gallus domesticus. In: Detlaf TA, Astaurov BL (eds) Experimental animals in developmental biology (in Russian). Nauka, Moskva, pp 463–503

  43. Rash JE, Shay IW, Biesele JJ (1969) Cilia in cardiac differentiation. J Ultrastruct Res 29:470–484

  44. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electronmicroscopy. J Cell Biol 17:208–212

  45. Rumyantsev PP (1977) Interrelations of the proliferation and differentiation processes during cardiac myogenesis and regeneration. Int Rev Cytol 51:187–273

  46. Rumyantsev PP, Shmantsar IA (1967) Ultrastructure of lymph heart muscle fibers of the frog (in Russian, English summary). Tsitologiya 11:1129–1136

  47. Salamon A, Hàmori J (1980) Possible role of myofibroblasts in the pathogenesis of Dupuytren's contracture. Acta Morphol Acad Sci Hung 28:71–82

  48. Satoh I, Nitatori T (1980) On the fine structure of lymph hearts in Amphibia and reptiles. In: Bourne GH (ed) Hearts and heart-like organs, Vol 1, Academic Press, New York London, pp 149–171

  49. Schiebler TH, Wolff HH (1966) Elektronenmikroskopische Untersuchungen am Herzmuskel der Ratte während der Entwicklung. Z Zellforsch 69:22–40

  50. Schipp R, Beyerle-v. Wehren A (1970) Zur funktionellen Bedeutung der osmiophilen Granula in Herzorganen niederer Vertebraten. Eine vergleichend elektronenmikroskopische und pharmakologische Untersuchung am isolierten Herzen des Frosches und anderer poikilothermer Vertebraten. Z Zellforsch 108:243–267

  51. Schipp R, Flindt R (1968) Zur Feinstruktur und Innervation der Lymphherzmuskulatur der Amphibien. Z Anat Entwicklungsgesch 127:232–253

  52. Schulz LC (1958) Elektronenmikroskopische Untersuchungen der Herzmuskulatur des Schweines unter besonderer Berücksichtigung der sogenannten Kernreihen-Bildung. Dtsch tierärztl Wochenschr 65:117–122

  53. Stockdale F, Holtzer H (1961) DNA synthesis and myogenesis. Exp Cell Res 24:508–520

  54. Sutulov LS (1949) Structure of lymph-heart cross-striated muscle fibers (in Russian). Dokl Akad Nauk SSSR 68, 5:927–929

  55. Waldeyer W (1864) Anatomische und physiologische Untersuchungen über die Lymphherzen der Frösche. Z ration Med 21:105–124

  56. Weliky VN (1889) Supplement to the research of lymph hearts and vessels in some amphibians (in Russian, German summary). Zap Imper Akad Nauk 59, 6:1–45

  57. Wroblewski R, Anniko M, Edström L (1981) A new type of striated muscle in mammalian body: morphological, histochemical, and X-ray microanalytical observations of stapedius muscle in guinea pig. J Ultrastruct Res 76:46–56

  58. Yunge L, Ballak M, Beuzeron J, Lacasse J, Cantin M (1980) Ultrastructural cytochemistry of atrial and ventricular cardiocytes of the bullfrog (Rana catesbeiana). Relationship of specific granules with renin-like activity of the myocardium. Can J Pharmacol 58:1463–1476

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Correspondence to P. P. Rumyantsev.

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Markozashvili, M.I., Rumyantsev, P.P. Ultrastructure of muscle fibers and cells synthesizing DNA in lymph hearts of developing frogs and chick embryos. Cell Tissue Res. 238, 369–379 (1984). https://doi.org/10.1007/BF00217310

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Key words

  • Lymph heart
  • Myogenesis
  • Cell proliferation
  • DNA synthesis
  • Electron-microscopic autoradiography
  • Rana temporaria, developmental stages
  • Chick embryo