Ultrastructure of Mammalian Cardiac Muscle

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 which 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 on 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 [1, 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 which have been discovered to date.

[1]  V. Mutt,et al.  The auricular myocardiocytes of the heart constitute an endocrine organ characterization of a porcine cardiac peptide hormone, cardiodilatin-126 , 2004, Cell and Tissue Research.

[2]  A. C. Shen,et al.  Localization of Ca2+ + Mg2+-ATPase of the sarcoplasmic reticulum in adult rat papillary muscle , 1982, The Journal of cell biology.

[3]  J. Shay,et al.  The Role of Intermediate (10-nm) Filaments in the Development and Integration of the Myofibrillar Contractile Apparatus in the Embryonic Mammalian Heart , 1981 .

[4]  R. Weinstein,et al.  The ultrastructure of the nexus. A correlated thin-section and freeze-cleave study. , 1970 .

[5]  Jane Sands Robb,et al.  Comparative Basic Cardiology , 1965 .

[6]  J. P. Schroeter,et al.  Optical diffraction of the Z lattice in canine cardiac muscle , 1977, The Journal of cell biology.

[7]  T. Gotoh,et al.  Quantitative studies on the ultrastructural differentiation and growth of mammalian cardiac muscle cells. I. The atria and ventricles of the rat. , 1980, Acta anatomica.

[8]  S. Goldfischer 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. , 1982, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[9]  R. Waugh,et al.  Comparative stereology of the mouse and finch left ventricle. , 1978, Tissue & cell.

[10]  M. Goldstein,et al.  Microtubules in the heart muscle of the postnatal and adult rat. , 1985, Journal of molecular and cellular cardiology.

[11]  R. Waugh,et al.  The ultrastructure of the mammalian cardiac muscle cell--with special emphasis on the tubular membrane systems. A review. , 1976, The American journal of pathology.

[12]  E. Raviola,et al.  Structure of rapidly frozen gap junctions , 1980, The Journal of cell biology.

[13]  R. Tomanek,et al.  Myocardial ultrastructure of young and senescent rats. , 1973, Journal of ultrastructure research.

[14]  W. V. Winkle The fenestrated collar of mammalian cardiac sarcoplasmic reticulum: A freeze‐fracture study , 1977 .

[15]  D. Fawcett THE SPORADIC OCCURRENCE IN CARDIAC MUSCLE OF ANOMALOUS Z BANDS EXHIBITING A PERIODIC STRUCTURE SUGGESTIVE OF TROPOMYOSIN , 1968, The Journal of cell biology.

[16]  M. Cantin,et al.  Ultrastructural cytochemistry of atrial muscle cells , 1980, Cell and Tissue Research.

[17]  P. Ganguly,et al.  Differential effect of thrombin on the growth of human fibroblasts , 1980, The Journal of cell biology.

[18]  D. Fawcett,et al.  THE ULTRASTRUCTURE OF THE CAT MYOCARDIUM , 1969, Journal of Cell Biology.

[19]  W. Claycomb,et al.  Ultrastructure of the Transverse Tubular System in Cultured Cardiac Muscle Cells , 1985 .

[20]  T. N. James,et al.  Specialized tissues and preferential conduction in the atria of the heart. , 1971, The American journal of cardiology.

[21]  R. Eisenberg,et al.  The T-SR junction in contracting single skeletal muscle fibers , 1982, The Journal of general physiology.

[22]  A. Benchimol,et al.  RECENT ADVANCES IN STUDIES ON CARDIAC STRUCTURE AND METABOLISM , 1973 .

[23]  M. Legato,et al.  Ultrastructural characteristics of the rat ventricular cell grown in tissue culture, with special reference to sarcomerogenesis. , 1972, Journal of molecular and cellular cardiology.

[24]  N. Sperelakis,et al.  Ultrastructural changes produced by hypertonicity in cat cardiac muscle. , 1971, Journal of molecular and cellular cardiology.

[25]  F. Plum Handbook of Physiology. , 1960 .

[26]  C. Hoppel,et al.  Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. , 1977, The Journal of biological chemistry.

[27]  M. A. Matlib,et al.  Differential activities of putative subsarcolemmal and interfibrillar mitochondria from cardiac muscle. , 1981, Journal of molecular and cellular cardiology.

[28]  A. Gilai,et al.  Structural changes in single muscle fibers after stimulation at a low frequency , 1979, The Journal of general physiology.

[29]  P. Cancilla,et al.  Conformational Changes in Myocardial Nuclei of Rats , 1969, Circulation research.

[30]  N. Sperelakis,et al.  The sarcoplasmic reticulum of mouse heart: its divisions, configurations, and distribution. , 1985, Journal of ultrastructure research.

[31]  D. E. Kelly,et al.  Traversing filaments in desmosomal and hemidesmosomal attachments: Freeze‐fracture approaches toward their characterization , 1981, The Anatomical record.

[32]  M. Lieberman,et al.  Developmental and physiological correlates of cardiac muscle , 1977 .

[33]  S. L. Jacobson Culture of Spontaneously Contracting Myocardial Cells from Adult Rats , 1977 .

[34]  H. E. Jordan,et al.  A study of the intercalated discs of the heart of the beef , 1917 .

[35]  A. Martínez-Palomo,et al.  TRANSITIONAL CARDIAC CELLS OF THE CONDUCTIVE SYSTEM OF THE DOG HEART , 1970, The Journal of cell biology.

[36]  L. Thornell An ultrahistochemical study on glycogen in cow Purkinje fibres. , 1974, Journal of molecular and cellular cardiology.

[37]  M. Goldstein,et al.  Perinuclear microtubules in postnatal rat heart , 1984, Journal of morphology.

[38]  N. Sperelakis,et al.  The tubular systems of myocardial cells: ultrastructure and possible function. , 1974, Recent advances in studies on cardiac structure and metabolism.

[39]  N. Sperelakis,et al.  A LABYRINTHINE STRUCTURE FORMED FROM A TRANSVERSE TUBULE OF MOUSE VENTRICULAR MYOCARDIUM , 1973, The Journal of cell biology.

[40]  W. Roberts,et al.  Intermyofibrillar and nuclear-myofibrillar connections in human and canine myocardium. An ultrastructural study. , 1973, Journal of molecular and cellular cardiology.

[41]  K. Rybicka Sarcoplasmic reticulum in the conducting fibers of the dog heart , 1977, The Anatomical record.

[42]  E. Albert,et al.  Adult canine myocytes: isolation, morphology and biochemical characteristics. , 1979, Journal of molecular and cellular cardiology.

[43]  N. Sperelakis,et al.  The membrane systems and cytoskeletal elements of mammalian myocardial cells. , 1983, Cell and muscle motility.

[44]  R. Zak,et al.  Cellular growth of cardiac muscle after birth. , 1979, Texas reports on biology and medicine.

[45]  D. Friend,et al.  Morphology and Metabolism of Intact Muscle Cells Isolated from Adult Rat Heart , 1970, Circulation research.

[46]  D. Scales Aspects of the mammalian cardiac sarcotubular system revealed by freeze fracture electron microscopy. , 1981, Journal of molecular and cellular cardiology.

[47]  D. N. Landon The influence of fixation upon the fine structure of the Z-disk of rat striated muscle. , 1970, Journal of cell science.

[48]  N. Sperelakis,et al.  An orderly lattice of axial tubules which interconnect adjacent transverse tubules in guinea-pig ventricular myocardium. , 1971, Journal of molecular and cellular cardiology.

[49]  R. Waugh,et al.  LAMELLAR JUNCTIONAL SARCOPLASMIC RETICULUM , 1974, Journal of Cell Biology.

[50]  M. Legato,et al.  Sarcomerogenesis in human myocardium. , 1970, Journal of molecular and cellular cardiology.

[51]  G. Isenberg,et al.  Glycocalyx is not required for slow inward calcium current in isolated rat heart myocytes , 1980, Nature.

[52]  J S Janicki,et al.  Three-dimensional myocardial and ventricular shape: a surface representation. , 1981, The American journal of physiology.

[53]  H. J. Weinstein An electron microscope study of cardiac muscle. , 1954, Experimental cell research.

[54]  R. Schneider,et al.  Die Zahl der Kerne in isolierten Zellen des menschlichen Myokards , 1972, Virchows Archiv B Cell Pathology.

[55]  M. Cantin,et al.  Localization of immunoreactive synthetic atrial natriuretic factor (ANF) in the heart of various animal species. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[56]  D. Fawcett,et al.  THE ULTRASTRUCTURE OF THE CAT MYOCARDIUM , 1969, The Journal of cell biology.

[57]  N. Sperelakis,et al.  The transverse-axial tubular system (TATS) of mouse myocardium: its morphology in the developing and adult animal. , 1984, The American journal of anatomy.

[58]  B. Kraus,et al.  Giant mitochondria in the human myocardium — Morphogenesis and fate , 1980, Virchows Archiv. B, Cell pathology including molecular pathology.

[59]  M. Cantin,et al.  Ultrastructural cytochemistry of atrial muscle cells. V. Characterization of specific granules in the human left atrium. , 1975, Journal of ultrastructure research.

[60]  C. Peracchia,et al.  Calcium effects on gap junction structure and cell coupling , 1978, Nature.

[61]  P. Pfitzer,et al.  Mitoses and binucleated cells in perinatal human hearts , 1985, Virchows Archiv. B, Cell pathology including molecular pathology.

[62]  W. Claycomb,et al.  Disorganization and reestablishment of cardiac muscle cell ultrastructure in cultured adult rat ventricular muscle cells. , 1982, Journal of ultrastructure research.

[63]  T. N. James,et al.  Comparative ultrastructure of cellular junctions in working myocardium and the conduction system under normal and pathologic conditions. , 1971, Journal of molecular and cellular cardiology.

[64]  L. Thornell,et al.  Filament systems in the Purkinje fibers of the heart. , 1981, The American journal of physiology.

[65]  D. Goodenough,et al.  Isolation of mouse myocardial gap junctions , 1980, The Journal of cell biology.

[66]  J. Sommer,et al.  Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. , 1968 .

[67]  N. Sperelakis,et al.  Cytochemical staining procedures selective for sarcotubular systems of muscle: modifications and applications. , 1977, Journal of ultrastructure research.

[68]  T. N. James,et al.  Fine structure of the bundle-branches. , 1974, British heart journal.

[69]  M. Entman,et al.  Microtubules in mammalian heart muscle , 1979, The Journal of cell biology.

[70]  J. Ledingham,et al.  ULTRASTRUCTURE OF DESMOSOMES IN MAMMALIAN INTERCALATED DISC; APPEARANCES AFTER LANTHANUM TREATMENT , 1969, The Journal of cell biology.

[71]  P. Pfitzer,et al.  Number of nuclei in isolated myocardial cells of pigs , 1974, Virchows Archiv. B, Cell pathology.

[72]  T. N. James,et al.  Fine structure of cells and their histologic organization within internodal pathways of the heart: clinical and electrocardiographic implications. , 1979, The American journal of cardiology.

[73]  N. Sperelakis Propagation mechanisms in heart. , 1979, Annual review of physiology.

[74]  V. Navaratnam,et al.  The ultrastructure of myocardial cells in the golden hamster Cricetus auratus. , 1981, Journal of anatomy.

[75]  E. Strehler,et al.  Differentiation of the myofibrils and the intermediate filament system during postnatal development of the rat heart. , 1982, European journal of cell biology.

[76]  E. Page,et al.  Quantitative electron microscopic description of heart muscle cells. Application to normal, hypertrophied and thyroxin-stimulated hearts. , 1973, The American journal of cardiology.

[77]  S. Virágh,et al.  THE IMPULSE GENERATION AND CONDUCTION SYSTEM OF THE HEART , 1973 .

[78]  N. Sperelakis,et al.  The presence of transverse and axial tubules in the ventricular myocardium of embryonic and neonatal guinea pigs , 1976, Cell and Tissue Research.

[79]  N. Sperelakis,et al.  Bridging junctional processes in couplings of skeletal, cardiac, and smooth muscle , 1982 .

[80]  J. P. Schroeter,et al.  The Z lattice in canine cardiac muscle , 1979, The Journal of cell biology.

[81]  N. Baba,et al.  Atrioventricular node and Purkinje fibers of the guinea pig heart. , 1971, The American journal of anatomy.

[82]  W. Claycomb DNA Fragmentation as a Developmental Program for Cellular Aging in Cardiac Muscle , 1985 .

[83]  N. Sperelakis,et al.  Myocardial couplings: their structural variations in the mouse. , 1977, Journal of ultrastructure research.

[84]  D. E. Kelly,et al.  Subunits of the triadic junction in fast skeletal muscle as revealed by freeze-fracture. , 1979, Journal of ultrastructure research.

[85]  E. Page,et al.  Quantitative Studies on Plasmalemmal Folds and Caveolae of Rabbit Ventricular Myocardial Cells , 1980, Circulation research.

[86]  S J Dwyer,et al.  The use of computer imaging techniques to visualize cardiac muscle cells in three dimensions , 1980, The Anatomical record.

[87]  N. Sperelakis,et al.  SPHEROIDAL BODIES IN THE JUNCTIONAL SARCOPLASMIC RETICULUM OF LIZARD MYOCARDIAL CELLS , 1974, The Journal of cell biology.

[88]  Rumyantsev Pp,et al.  The ultrastructure of differentiating cells of the heart muscle in the state of mitotic division. , 1968 .

[89]  M. Moravec,et al.  Intrinsic innervation of the atrioventricular junction of the rat heart. , 1984, The American journal of anatomy.

[90]  L. Girardier,et al.  A STUDY OF THE T SYSTEM IN RAT HEART , 1970, The Journal of cell biology.

[91]  K. Hayashi An electron microscope study on the conduction system of the cow heart. , 1962, Japanese circulation journal.

[92]  K. Campbell,et al.  Ultrastructural localization of calsequestrin in adult rat atrial and ventricular muscle cells , 1985, The Journal of cell biology.

[93]  S. Bishop,et al.  Surface morphology and cell size measurement of isolated rat cardiac myocytes. , 1979, Journal of molecular and cellular cardiology.

[94]  G. Colborn,et al.  Electron microscopy of the sinoatrial node of the squirrel monkey Saimiri sciureus. , 1972, Journal of molecular and cellular cardiology.

[95]  H. Behrendt Effect of anabolic steroids on rat heart muscle cells , 1977, Cell and Tissue Research.

[96]  G. Gabella Inpocketings of the cell membrane (caveolae) in the rat myocardium. , 1978, Journal of Ultrastructure Research.

[97]  G. Langer,et al.  The mammalian myocardium , 1974 .

[98]  K. Campbell,et al.  Evidence for the presence of calsequestrin in two structurally different regions of myocardial sarcoplasmic reticulum , 1984, The Journal of cell biology.

[99]  E. Page,et al.  Distribution, Surface Density, and Membrane Area of Diadic Junctional Contacts between Plasma Membrane and Terminal Cisterns in Mammalian Ventricle , 1979, Circulation research.

[100]  P. Jewett,et al.  CARDIAC MUSCLE Its Ultrastructure in the Finch and Hummingbird with Special Reference to the Sarcoplasmic Reticulum , 1971 .

[101]  L. Thornell The fine structure of Purkinje fiber glycogen. A comparative study of negatively stained and cytochemically stained particles. , 1974, Journal of ultrastructure research.

[102]  D. Fischman,et al.  Studies of isolated adult rat heart cells: the surface morphology and the influence of extracellular calcium ion concentration on cellular viability. , 1977, Tissue & cell.

[103]  N. Sperelakis,et al.  Intercalated discs of mammalian heart: a review of structure and function. , 1985, Tissue & cell.

[104]  L. Thornell Ultrastructural variations of Z bands in cow Purkinje fibres. , 1973, Journal of molecular and cellular cardiology.

[105]  N. Sperelakis,et al.  Association between mitochondria and gap junctions in mammalian myocardial cells. , 1982, Tissue & cell.

[106]  P. Wolkowicz,et al.  Respiration-dependent calcium ion uptake by two preparations of cardiac mitochondria. Effects of palmitoyl-coenzyme A and palmitoylcarnitine on calcium ion cycling and nicotinamide nucleotide reduction state. , 1980, The Biochemical journal.

[107]  S. Ebashi,et al.  Cell and Muscle Motility , 1983, Springer US.

[108]  E. Sonnenblick,et al.  Isolated heart myocytes: ultrastructural case study technique , 1981, Journal of microscopy.

[109]  H. Fahimi,et al.  Identification of peroxisomes (microbodies) in mouse myocardium. , 1976, Journal of molecular and cellular cardiology.

[110]  F. Sjöstrand,et al.  The ultrastructure of the intercalated discs of frog, mouse and guinea pig cardiac muscle. , 1958, Journal of ultrastructure research.

[111]  N. Sperelakis,et al.  Structures located at the levels of the Z bands in mouse ventricular myocardial cells. , 1980, Tissue & cell.

[112]  C. E. Kossmann,et al.  The Structure of the Specialized Impulse‐Conducting System of the Steer Heart , 1961, Circulation.

[113]  N. McNutt Ultrastructure of the myocardial sarcolemma. , 1975, Circulation research.

[114]  P. Anversa,et al.  Postnatal Development of the M‐Band in Rat Cardiac Myofibrils , 1981, Circulation research.

[115]  D. Segretain,et al.  Tridimensional architecture of the Golgi apparatus in the atrial muscle cell of the rat. , 1984, The American journal of anatomy.

[116]  M. Legato 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 , 1979, Circulation research.