Advertisement

Ultrastructure of Mammalian Cardiac Muscle

  • Michael S. Forbes
  • Nicholas Sperelakis
Part of the Developments in Cardiovascular Medicine book series (DICM, volume 90)

Abstract

The great majority of muscle cells of the mammalian heart are superbly organized entities. It is impressive to consider that observations on these myocytes are in most cases being made on cells that are roughly the same age as the entire animal; only a scant bit of evidence is yet available to suggest that any substantial capability for regeneration is intrinsic to the myocardia of higher vertebrates (see the section, Nuclei). Still these venerable cells can respond admirably under trying circumstances, such as those necessitating osmotic shrinkage or hypertrophy, in which cases they adjust their sarcolemmal and myoplasmic components to maintain an extraordinarily constant surface-volume ratio {l, 2}. In this chapter, we provide a sketch of the fine structure of cardiac muscle cells in mammalian heart. The many electron microscopic studies of such cells have served to point out the difficulty of making generalizations when considering the numerous aspects of myocardial substructure. We will, nevertheless, describe the salient features of myocardial cells, while pointing out along the way some of the variations on these basic themes that have been discovered to date.

Keywords

Sarcoplasmic Reticulum Cardiac Muscle Myocardial Cell Cardiac Muscle Cell Purkinje Fiber 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sperelakis N, Rubio R: Ultrastructural changes produced by hypertonicity in cat cardiac muscle. J Mol Cell Cardiol 3: 139–156, 1971.PubMedGoogle Scholar
  2. 2.
    Page E, McCallister LP: Quantitative electron microscopic description of heart muscle cells: Application to normal, hypertrophied and thyroxin-stimulated hearts. Am J Cardiol 31: 172–181, 1973.PubMedGoogle Scholar
  3. 3.
    Simpson FO, Rayns DG, Ledingham JM: The ultra-structure of ventricular and atrial myocardium. In: Challice CE, Virägh S (eds), Ultrastructure of the Mammalian Heart. New York: Academic Press, 1973, pp 1–41.Google Scholar
  4. 4.
    McNutt NS, Fawcett DW: Myocardial ultrastructure. In: Langer GA, Brady AJ (eds) The Mammalian Myocardium. New York: John Wiley and Sons, 1974, pp 1–49.Google Scholar
  5. 5.
    Sommer JR, Johnson EA: Ultrastructure of cardiac muscle. In: Berne RM, Sperelakis N, Geiger SR (eds) Handbook of Physiology. Sect 2: The cardiovascular system. Vol 1: The Heart. Bethesda MD: American Physiological Society, 1979, pp 113–186.Google Scholar
  6. 6.
    Sperelakis N, Forbes MS, Rubio R: The tubular systems of myocardial cells: Ultrastructure and possible function. In: Dhalla NS (ed) Recent Advances in Studies on Cardiac Structure and Metabolism. Vol 4: Myocardial Biology. Baltimore: University Park Press, 1974, pp 163–194.Google Scholar
  7. 7.
    Sommer JR, Waugh RA: The ultrastructure of the mammalian cardiac muscle cell—with special emphasis on the tubular membrane systems. Am J Pathol 82: 191–232, 1976.Google Scholar
  8. 8.
    Forbes MS, Sperelakis N: The membrane systems and cytoskeletal elements of mammalian myocardial cells. In: Dowben RM, Shay JW (eds) Cell and Muscle Motility, Vol 3. New York: Plenum, 1983, pp 89–155.Google Scholar
  9. 9.
    Jordan HE, Banks JB: A study of the intercalated discs of the heart of the beef. Am J Anat 22: 285–339, 1917.Google Scholar
  10. 10.
    Sjöstrand FS, Andersson-Cedergren E, Dewey MM: The ultrastructure of the intercalated disc of frog, mouse and guinea pig cardiac muscle. J Ultrastruct Res 1: 271–287, 1958.PubMedGoogle Scholar
  11. 11.
    Rhodin JAG, del Missier P, Reid LC: The structure of the specialized impulse-conduction system of the steer heart. Circulation 24: 349–367, 1961.Google Scholar
  12. 12.
    Hayashi K: An electron microscope study on the conduction system of the cow heart. Jpn Circ J 26: 765–842, 1962.PubMedGoogle Scholar
  13. 13.
    Jacobson SL: Culture of spontaneously contracting myocardial cells from adult rats. Cell Struct Function 2: 1–9, 1977.Google Scholar
  14. 14.
    Vahouny GV, Wei RW, Tamboli A, Albert EN: Adult canine myocytes: Isolation, morphology and biochemical characterizations. J Mol Cell Cardiol 11: 339–357, 1979.PubMedGoogle Scholar
  15. 15.
    Robinson TF, Hayward BS, Krueger JW, Sonnenblick EH, Wittenberg BA: Isolated heart myocytes: Ultrastructural case study technique. J Microscopy (Oxford) 124: 135–142, 1981.Google Scholar
  16. 16.
    Phillips SJ, Dacey DM: Mammalian ventricular heart cell shape, surface and fiber organization as seen with the scanning electron microscope (SEM). J Cell Biol 70: 85a, 1976.Google Scholar
  17. 17.
    Phillips SJ, Dacey DM, Bove A, Conger AD: Quantitative data on the shape of the mammalian ventricular heart cell. Fed Proc 36: 601, 1977.Google Scholar
  18. 18.
    Marino TA, Cook PN, Cook LT, Dwyer SJ III: The use of computer imaging techniques to visualize cardiac muscle cells in three dimensions. Anat Ree 198: 537–546, 1980.PubMedGoogle Scholar
  19. 19.
    Janicki JS, Weber KT, Gochman RF, Shroff S, Geheb FJ: Three-dimensional myocardial and ventricular shape: A surface representation. Am J Physiol 241: Hl–Hll, 1981Google Scholar
  20. 20.
    Nag AC, Fischman DA, Aumont MC, Zak R: Studies of isolated adult rat heart cells: The surface morphology and the influence of extracellular calcium ion concentration on cellular viability. Tissue Cell 9: 419–436, 1977.PubMedGoogle Scholar
  21. 21.
    Bishop SP, Drummond JL: Surface morphology and cell size measurement of isolated rat cardiac myocytes. J Mol Cell Cardiol 11: 423–433, 1979.PubMedGoogle Scholar
  22. 22.
    Goldstein MA, Schroeter JP, Sass RL: Optical diffraction of the Z lattice in canine cardiac muscle. J Cell Biol 75: 818–836, 1977.PubMedGoogle Scholar
  23. 23.
    Goldstein MA, Schroeter JP, Sass RL: The Z lattice in canine cardiac muscle. J Cell Biol 83: 187–204, 1979.PubMedGoogle Scholar
  24. 24.
    Landon DN: The influence of fixation upon the fine structure of the Z-disk of rat striated muscle. J Cell Sei 6: 257–276, 1970.Google Scholar
  25. 25.
    Anversa P, Olivetti G, Bracchi P-G, Loud AV: Postnatal development of the M-band in rat cardiac myofibrils. Circ Res 48: 561–568, 1981.PubMedGoogle Scholar
  26. 26.
    Forbes MS, Sperelakis N: The presence of transverse and axial tubules in the ventricular myocardium of embryonic and neonatal guinea pigs. Cell Tissue Res 166: 83–90, 1976.PubMedGoogle Scholar
  27. 27.
    Hirakow R, Gotoh T: Quantitative studies on the ultrastructural differentiation and growth of mammalian cardiac muscle cells. II. The atria and ventricles of the guinea pig. Acta Anat 108: 230–237, 1980.PubMedGoogle Scholar
  28. 28.
    Forbes MS, Sperelakis N: Structures located at the level of the Z bands in mouse ventricular myocardial cells. Tissue Cell 12: 467–489, 1980.PubMedGoogle Scholar
  29. 29.
    Ferrans VJ, Roberts WC: Intermyofibrillar and nuclear-myofibrillar connections in human and canine myocardium: An ultrastructural study. J Mol Cell Cardiol 5: 247–257, 1973.PubMedGoogle Scholar
  30. 30.
    Goldstein MA, Entman ML: Microtubules in mammalian heart muscle. J Cell Biol 80: 183–195, 1979.PubMedGoogle Scholar
  31. 31.
    Cartwright J Jr, Goldstein MA: Microtubules in the heart muscle of the postnatal and adult rat. J Mol Cell Cardiol 17: 1–7, 1985.PubMedGoogle Scholar
  32. 32.
    Park RS, Légier G, Cartwright J Jr, Goldstein MA: Perinuclear microtubules in postnatal rat heart. J Morphol 179: 13–19, 1984.PubMedGoogle Scholar
  33. 33.
    Behrendt H: Effect of anabolic steroids on rat heart muscle cells. I. Intermediate filaments. Cell Tissue Res 180: 303–315, 1977.PubMedGoogle Scholar
  34. 34.
    Fuseler JW, Shay JW, Feit H: The role of intermediate (10-nm) filaments in the development and integration of the myofibrillar contractile apparatus in the embryonic mammalian heart. In: Dowben RM, Shay J W (eds) Cell and Muscle Motility, Vol 1. New York: Plenum, 1981, pp 205–259Google Scholar
  35. 35.
    Carlsson E, Kjörell U, Thornell L-E, Lambertsson A, Strehler E: Differentiation of the myofibrils and the intermediate filament system during postnatal development of the rat heart. Eur J Cell Biol 217: 62–78, 1982.Google Scholar
  36. 36.
    Palmer JW, Tandler B, Hoppel CL: Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252: 8731–8739, 1977.PubMedGoogle Scholar
  37. 37.
    Wolkowicz PE, McMillan-Wood J: Respiration-dependent calcium ion uptake by two preparations of cardiac mitochondria. Biochem J 186: 257–266, 1980.PubMedGoogle Scholar
  38. 38.
    Matlib MA, Rebman D, Ashraf M, Rouslin W, Schwartz A: Differential activities of putative subsarcolemmal and interfibrillar mitochondria from cardiac muscle. J Mol Cell Cardiol 13: 163–170, 1981.PubMedGoogle Scholar
  39. 39.
    Forbes MS, Sperelakis N: Association between gap junctions and mitochondria in mammalian myocardial cells. Tissue Cell 14: 25–37, 1982.PubMedGoogle Scholar
  40. 40.
    Peracchia C: Calcium effects on gap junction structure and cell coupling. Nature (Lond) 271: 669–671, 1978.Google Scholar
  41. 41.
    Baldwin KM: Cardiac gap junction configuration after an uncoupling treatment as a function of time. J Cell Biol. 82: 66–75, 1979PubMedGoogle Scholar
  42. 42.
    Fawcett DW, McNutt NS: The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol 42: 1–45, 1969.PubMedGoogle Scholar
  43. 43.
    Kraus B, Cain H: Giant mitochondria in the human myocardium—morphogenesis and fate. Virchows Arch (B) 33: 77–89, 1980.Google Scholar
  44. 44.
    Brodsky WK, Arefyeva AM, Uryvaeva IV: Mitotic polyploidization of the mouse heart myocytes during the first postnatal week. Cell Tissue Res 210: 133–144, 1980.PubMedGoogle Scholar
  45. 45.
    Schmid G, Pfitzer P: Mitoses and binucleated cells in perinatal human hearts. Virchows Arch (B) 48: 59–67, 1985.Google Scholar
  46. 46.
    Gräbner W, Pfitzer P: Number of nuclei in isolated myocardial cells of pigs. Virchows Arch (B) 15: 279–294, 1974.Google Scholar
  47. 47.
    Schneider R, Pfitzer P: Die zahl der kerne in isolierten zeilen des menschlichen myokards. Virchows Arch (B) 12: 238–258, 1973.Google Scholar
  48. 48.
    Bugaisky L, Zak R: Cellular growth of cardiac muscle after birth. Tex Rep Biol Med 39: 123–138, 1979.PubMedGoogle Scholar
  49. 49.
    Rumyantsev PP: Ultrastructural reorganization, DNA synthesis and mitotic division of myocytes in atria of rats with left ventricle infarction: An electron microscopic and autoradiographic study. Virchows Arch (B) 15: 357–378, 1974.Google Scholar
  50. 50.
    Rumyantsev PP, Snigirevskaya ES: The ultrastructure of differentiating cells of the heart muscle in the state of mitotic division. Acta Morphol Acad Sei Hung 16: 271–283, 1968.Google Scholar
  51. 51.
    Bloom S, Cancilla PA: Conformational changes in myocardial nuclei of rats. Circ Res 24: 189–196, 1969.PubMedGoogle Scholar
  52. 52.
    Langer GA: Ionic movements and the control of contraction. In: Langer GA, Brady AJ (eds) The Mammalian Myocardium. New York: John Wiley and Sons, 1974, pp 193–217.Google Scholar
  53. 53.
    Isenberg G, Klöckner U: Glycocalyx is not required for slow inward calcium current in isolated rat heart myocytes. Nature 284: 358–360, 1980.PubMedGoogle Scholar
  54. 54.
    Gabella G: Inpocketings of the cell membrane (caveolae) in the rat myocardium. J Ultrastruct Res 65: 135–147, 1978.PubMedGoogle Scholar
  55. 55.
    Levin KR, Page E: Quantitative studies on plasma-lemmal folds and caveolae of rabbit ventricular myocardial cells. Circ Res 467: 244–255, 1980.Google Scholar
  56. 56.
    Forssmann WG, Girardier L: A study of the T system in rat heart. J Cell Biol 44: 1–19, 1970.PubMedGoogle Scholar
  57. 57.
    Masson-Pévet M, Gros D, Besseisen E: The caveolae in rabbit sinus node and atrium. Cell Tissue Res 208: 183–196, 1980.PubMedGoogle Scholar
  58. 58.
    Forbes MS, Sperelakis N: A labyrinthine structure formed from a transverse tubule of mouse ventricular myocardium. J Cell Biol 56: 865–869, 1973.PubMedGoogle Scholar
  59. 59.
    Ishikawa H, Yamada E: Differentiation of the sarcoplasmic reticulum and T-system in developing mouse cardiac muscle. In: Lieberman M, Sano T (eds) Developmental and Physiological Correlates of Cardiac Muscle. New York: Raven, 1976, pp 21–35.Google Scholar
  60. 60.
    Forbes MS, Hawkey LA, Sperelakis N: The transverse-axial tubular system (TATS) of mouse myocardium: Its morphology in the developing and adult animal. Am J Anat 170: 143–162, 1984.PubMedGoogle Scholar
  61. 61.
    Sperelakis N, Rubio R: An orderly lattice of axial tubules which interconnect adjacent transverse tubules in guinea-pig ventricular myocardium. J Mol Cell Cardiol 2: 211–220, 1971.PubMedGoogle Scholar
  62. 62.
    Forbes MS, Sperelakis N: Myocardial couplings: Their structural variations in the mouse. J Ultrastruct Res 58: 50–65, 1977.PubMedGoogle Scholar
  63. 63.
    Forbes MS, Sperelakis N: Bridging junctional processes in couplings of striated, cardiac, and smooth muscle cells. Muscle Nerve 5: 674–681, 1982.Google Scholar
  64. 64.
    Ayettey AS, Navaratnam V: The fine structure of myocardial cells in the grey seal. J Anat 131: 748, 1980.Google Scholar
  65. 65.
    Ayettey AS, Navaratnam V: The ultrastructure of myocardial cells in the golden hamster Cricetus auratus. J Anat 132: 519–524, 1981.PubMedGoogle Scholar
  66. 66.
    Forbes MS, Plantholt BA, Sperelakis N: Cytochemical staining procedures selective for sarcotubular systems of muscle: Applications and modifications. J Ultrastruct Res 60: 306–327, 1977.PubMedGoogle Scholar
  67. 67.
    Legato MJ: Cellular mechanisms of normal growth in the mammalian heart. II. A quantitative and qualitative comparison between the right and left ventricular myocytes in the dog from birth to five months of age. Circ Res 44: 263–279, 1979.PubMedGoogle Scholar
  68. 68.
    Legato MJ: Ultrastructural characteristics of the rat ventricular cell grown in tissue culture, with special reference to sarcomerogenesis. J Mol Cell Cardiol 4: 299–317, 1972.PubMedGoogle Scholar
  69. 69.
    Moses RL, Claycomb WC: Disorganization and re-establishment of cardiac muscle cell ultrastructure in cultured adult rat ventricular muscle cells. J Ultrastruct Res 81: 358–374, 1982.PubMedGoogle Scholar
  70. 70.
    Moses RL, Claycomb WC: Ultrastructure of the transverse tubular system in cultured cardiac muscle cells. Dev Cardiol Med 49: 422–440, 1985.Google Scholar
  71. 71.
    Van Winkle WB: The fenestrated collar of mammalian cardiac sarcoplasmic reticulum: A freeze-fracture study. Am J Anat 149: 277–282, 1977.PubMedGoogle Scholar
  72. 72.
    Forbes MS, Hawkey LA, Jirge SK, Sperelakis N: The sarcoplasmic reticulum of mouse heart: Its divisions, configurations, and distribution. J Ultrastruct Res 93: 1–16, 1985.PubMedGoogle Scholar
  73. 73.
    Dolber PC, Sommer JR: Freeze-fracture appearance of rabbit cardiac sarcoplasmic reticulum: A freeze-fracture study. In: Bailey G (ed) Thirty-eighth Annual EMSA Meeting, Baton Rouge: Claitor’s, 1980, pp 630–631.Google Scholar
  74. 74.
    Scales DJ: Aspects of the cardiac sarcotubular system revealed by freeze-fracture electron microscopy. J Mol Cell Cardiol 13: 373–380, 1981.PubMedGoogle Scholar
  75. 75.
    Slade AM, Severs NJ: Rough endoplasmic reticulum in the adult mammalian cardiac muscle cell. J Sub-microscCytol 17: 531–536, 1985.PubMedGoogle Scholar
  76. 76.
    Somlyo AV: Bridging structures spanning the junctional gap at the triad of skeletal muscle. J Cell Biol 80: 743–750, 1979.PubMedGoogle Scholar
  77. 77.
    Eisenberg BR, Gilai A: Structural changes in single muscle fibers after stimulation at a low frequency. J Gen Physiol 74: 1–16, 1979.PubMedGoogle Scholar
  78. 78.
    Eisenberg BR, Eisenberg RS: The T-SR junction in contracting single skeletal muscle fibers. J Gen Physiol 79: 1–19, 1982.PubMedGoogle Scholar
  79. 79.
    Brunschwig JP, Brandt N, Caswell AH, Lukeman DS: Ultrastructural observations of isolated intact and fragmented junctions of skeletal muscle by use of tannic acid mordanting. J Cell Biol 93: 533–542, 1982.PubMedGoogle Scholar
  80. 80.
    Kelly DE, Kuda AM: Subunits of the triadic junc¬tion in fast skeletal muscle as revealed by freeze-fracture. J Ultrastruct Res 68: 220–233, 1979PubMedGoogle Scholar
  81. 81.
    Forbes MS, Sperelakis N: Spheroidal bodies in the junctional sarcoplasmic reticulum of lizard myocardial cells. J Cell Biol 60: 602–615, 1974.PubMedGoogle Scholar
  82. 82.
    Jewett PH, Sommer JR, Johnson EA: Cardiac muscle: Its ultrastructure in the finch and hummingbird with special reference to the sarcoplasmic reticulum. J Cell Biol. 49: 50–65, 1971.PubMedGoogle Scholar
  83. 83.
    Waugh RA, Sommer JR: Lamellar junctional sarcoplasmic reticulum: A specialization of cardiac sarcoplasmic reticulum. J Cell Biol. 63: 337–343, 1974.PubMedGoogle Scholar
  84. 84.
    Jorgensen AO, Shen A C-Y, Daly P, MacLennan DH: Localization of Ca2+ + Mg2+-ATPase of the sarcoplasmic reticulum in adult rat papillary muscle. J Cell Biol 93: 883–892, 1982.PubMedGoogle Scholar
  85. 85.
    Jorgensen AO, Campbell KP: Evidence for the presence of calsequestrin in two structurally different regions of myocardial sarcoplasmic reticulum. J Cell Biol 98: 1597–1602, 1984.PubMedGoogle Scholar
  86. 86.
    Jorgensen AO, Shen A C-Y, Campbell KP: Ultra-structural localization of calsequestrin in adult rat atrial and ventricular muscle cells. J Cell Biol 101: 257–268, 1985.PubMedGoogle Scholar
  87. 87.
    Bossen EH, Sommer JR, Waugh RA: Comparative stereology of the mouse and finch left ventricle. Tissue Cell 10: 773–784, 1978.PubMedGoogle Scholar
  88. 88.
    Page E, Surdyk-Droske M: Distribution, surface density, and membrane area of diadic junctional contacts between plasma membrane and terminal cisterns in mammalian ventricle. Circ Res 45: 260–267, 1979.PubMedGoogle Scholar
  89. 89.
    Forbes MS, Sperelakis N: Intercalated discs of mammalian heart: A review of structure and function. Tissue Cell 17: 605–648, 1985.PubMedGoogle Scholar
  90. 90.
    McNutt NS: Ultrastructure of the myocardial sarco-lemma. Circ Res 37: 1–13, 1975.PubMedGoogle Scholar
  91. 91.
    Rayns DG, Simpson FO, Ledingham JM: Ultra-structure of desmosomes of mammalian intercalated disc: Appearances after lanthanum treatment. J Cell Biol 42: 322–326, 1969.PubMedGoogle Scholar
  92. 92.
    Kelly DE, Kuda AM: Traversing filaments in desmosomal and hemidesmosomal attachments: Freeze-fracture approaches toward their characterization. Anat Rec 199: 1014, 1981.Google Scholar
  93. 93.
    Kawamura K, James TN: Comparative ultrastructure of cellular junctions in working myocardium and the conduction system under normal and pathologic conditions. J Mol Cell Cardiol 3: 31–60, 1971.PubMedGoogle Scholar
  94. 94.
    Berry MN, Friend DS, Scheuer J: Morphology and metabolism of intact muscle cells isolated from adult rat heart. Circ Res 26: 679–687, 1970.PubMedGoogle Scholar
  95. 95.
    Kensler RW, Goodenough DA: Isolation of mouse myocardial gap junctions. J Cell Biol 86: 755–764, 1980.PubMedGoogle Scholar
  96. 96.
    Sperelakis N: Propagation mechanisms in heart. Ann Rev Physiol 41: 441–457, 1979.Google Scholar
  97. 97.
    Raviola E, Goodenough DA, Raviola G: Structure of rapidly frozen gap junctions. J Cell Biol 87: 273–279, 1980.PubMedGoogle Scholar
  98. 98.
    McNutt NS, Weinstein RS: The ultrastructure of the nexus: A correlated thin-section and freeze-cleave study. J Cell Biol 47: 666–688, 1970.PubMedGoogle Scholar
  99. 99.
    Rambourg A, Segretain D, Clermont Y: Tridimen¬sional architecture of the Golgi apparatus in the atrial muscle cell of the rat. Am J Anat 170: 163–179, 1984.PubMedGoogle Scholar
  100. 100.
    Cantin M, Benchimol S, Castonguay Y, Berlinguet J-C, Huet M: Ultrastructural cytochemistry of atrial muscle cells. V. Characterization of specific granules in the human left atrium. J Ultrastruct Res 52: 179–192, 1975.PubMedGoogle Scholar
  101. 101.
    Cantin M, Gutkowska J, Thibault G, Milne RW, Ledoux S, Min Li S, Chapeau C, Garcia R, Hamet P, Genest J: Immunocytochemical localization of atrial natriuretic factor in the heart and salivary glands. Histochemistry 80: 113–127, 1984.PubMedGoogle Scholar
  102. 102.
    Forssmann W. G., Birr C, Carlquist M, Christmann M, Finke R, Henschen A, Hock D, Kirschheim H, Kreye V, Lottspeich F, Metz J, Mutt V, Reinecke M: The auricular myocardiocytes of the heart constitute an endocrine organ. Characterization of a porcine cardiac peptide hormone, cardiodilatin-126. Cell Tissue Res 238: 425–430, 1984.PubMedGoogle Scholar
  103. 103.
    Chapeau C, Gutkowska J, Schiller PW, Milne RW, Thibaut G, Garcia R, Genest J, Cantin M: Localization of immunoreactive synthetic atrial natriuretic factor (ANF) in the heart of various animal species. J Histochem Cytochem 33: 541–550, 1985.PubMedGoogle Scholar
  104. 104.
    Goldfischer S: The internal reticular apparatus of Camillo Golgi: A complex, heterogeneous organelle, enriched in acid, neutral and alkaline phosphatases, and involved in glycosylation, secretion, membrane flow, lysosome formation, and intracellular digestion. J Histochem Cytochem 30: 717–733, 1982.PubMedGoogle Scholar
  105. 105.
    Claycomb WC: DNA fragmentation as a developmental program for cellular aging in cardiac muscle. Develop Cardiol Med 49: 399–409, 1985.Google Scholar
  106. 106.
    Tomanek J, Karlsson UL: Myocardial ultrastructure of young and senescent rats. J Ultrastruct Res 42: 201–220, 1973.PubMedGoogle Scholar
  107. 107.
    Herzog V, Fahimi HD: Identification of peroxisomes (microbodies) in mouse myocardium. J Mol Cell Cardiol 8: 271–281, 1976.PubMedGoogle Scholar
  108. 108.
    Hicks L, Fahimi HD: Peroxisomes (microbodies) in the myocardium of rodents and primates. A comparative ultrastructural cytochemical study. Cell Tissue Res 175: 467–481, 1977.PubMedGoogle Scholar
  109. 109.
    Virägh S, Challice CE: The impulse generation and conduction system of the heart. In: Challice CE, Viragh S (eds) Ultrastructure of the Mammalian Heart. New York: Academic Press, 1973, pp 43–90.Google Scholar
  110. 110.
    James TN, Sherf L: Specialized tissues and preferential conduction in the atria of the heart. Am J Cardiol 28: 414–427, 1971.PubMedGoogle Scholar
  111. 111.
    James TN, Sherf L, Urthaler F: Fine structure of the bundle-branches. Br Heart J 36: 1–18, 1974.PubMedGoogle Scholar
  112. 112.
    Truex RC: Structural basis of atrial and ventricular conduction. Cardiovasc Clin 6: 2–24, 1974.Google Scholar
  113. 113.
    Sherf L, James TN: Fine structure of cells and their histological organization within internodal pathways of the heart: Clinical and electrocardiographic implications. Am J Cardiol 44: 345–369, 1979.PubMedGoogle Scholar
  114. 114.
    Colborn GL, Carsey E Jr: Electron microscopy of the sinoatrial node of the squirrel monkey Saimiri saurem. J Mol Cell Cardiol 4: 525–536, 1972.PubMedGoogle Scholar
  115. 115.
    Fawcett DW: The sporadic occurrence in cardiac muscle of anomalous Z bands exhibiting a periodic structure suggestive of tropomyosin. J Cell Biol 36: 266–270, 1968.PubMedGoogle Scholar
  116. 116.
    Legato MJ: Sarcomerogenesis in human myocardium. J Mol Cell Cardiol 1: 425–437, 1970.PubMedGoogle Scholar
  117. 117.
    Rybicka K: Sarcoplasmic reticulum in the conducting fibers of the dog heart. Anat Ree 189: 237–262, 1977.Google Scholar
  118. 118.
    Osculati F, Garibaldi E: Particolari strutturali delle fibre del Purkinje del cuore di ratto; osservazioni al microscopio elettronico effuttuate anche applicando la tecnica della perossidasei. Boll Soc Med Chir (Pavia) 88: 403–437, 1974.Google Scholar
  119. 119.
    Osculati F, Garibaldi E: Fine structural aspects of the Purkinje fibres of the dog’s heart. J Submicr Cytol 6: 39–53, 1974.Google Scholar
  120. 120.
    Osculati F, Amati S, Petrini E, Francheschini F, Cinti S: Ultrastructural investigation of the Purkinje fibres of rabbit’s and cat’s heart. J Submicr Cytol 10: 185–197, 1978.Google Scholar
  121. 121.
    Osculati F, Amati S, Petrini E, Marelli M, Gazzanelli G: A study on the organization of the tubular endoplasmic reticulum in the rat heart conduction fibres. J Submicr Cytol 10: 371–380, 1978.Google Scholar
  122. 122.
    Robb JS: Comparative Basic Cardiology. New York: Grune and Stratton, 1965.Google Scholar
  123. 123.
    Moravec M, Moravec J: Intrinsic innervation of the atrioventricular junction of the rat heart. Am J Anat 171: 307–319, 1984.PubMedGoogle Scholar
  124. 124.
    Sommer JR, Johnson EA: Cardiac muscle: A comparative study of Purkinje fibers and ventricular fibers. J Cell Biol 36: 497–526, 1968PubMedGoogle Scholar
  125. 125.
    Kim S, Baba N: Atrioventricular node and Purkinje fibers of the guinea pig heart. Am J Anat 132: 339–354, 1971.PubMedGoogle Scholar
  126. 126.
    Thorneil L-E: The fine structure of Purkinje fiber glycogen: A comparative study of negatively stained and cytochemically stained particles. J Ultrastruct Res 49: 157–166, 1974.Google Scholar
  127. 127.
    Thornell LE: An ultrahistochemical study on glycogen in cow Purkinje fibers. J Mol Cell Cardiol 6: 439–448, 1974.PubMedGoogle Scholar
  128. 128.
    Thornell LE: Ultrastructural variations of Z bands in cow Purkinje fibers. J Mol Cell Cardiol 5: 409–417, 1973.PubMedGoogle Scholar
  129. 129.
    Martinez-Palomo A, Alanis J, Benitez D: Transitional cardiac cells of the conductive system of the dog heart: Distinguishing morphological and electrophysiological features. J Cell Biol 47: 1–17, 1970.PubMedGoogle Scholar
  130. 130.
    Thornell L-E, Eriksson A: Filament systems in the Purkinje fibers of the heart. Am J Physiol 241: H291–H305, 1981.PubMedGoogle Scholar
  131. 131.
    Weinstein HJ: An electron microscope study of cardiac muscle. Exp Cell Res 7: 130–146, 1954.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1989

Authors and Affiliations

  • Michael S. Forbes
  • Nicholas Sperelakis

There are no affiliations available

Personalised recommendations