Summary
The morphology, composition, and function of struts that interconnect the lateral surfaces of cardiomyocytes were examined in the hearts of rats and hamsters. Methods included brightfield and fluorescent light microscopy, secondary and backscatter scanning electron microscopy, and transmission electron microscopy in conjunction with silver stain, cationic dye, and antibody to type-I collagen. These studies reveal a twisted, beaded appearance and a complex substructure of collagen fibrils embedded in a ground substance that has a positive reaction with cationic dye. A hierarchy of patterns of branching and attachment was seen among intercellular struts ranging in diameter from 0.1 μm to several urn. The hypothesis that struts tether not only the surfaces but the contractile lattices of laterally adjacent myocytes is supported by the following: (a) the attachments of struts to the collagen weave of the sarcolemma, often lateral to the level of Z bands, (b) the presence of collagen type I in a composite material arrangement, (c) the relative dispositions and configurational changes of struts and myocyte surfaces in various physiological states and induced, non-physiological perturbations of cardiac muscle, (d) the corrugated sarcolemmas with infoldings near Z bands, and (e) the continuity of intracellular filaments from Z bands to the inner aspect of the sarcolemma in relaxed and contracted myocytes. Implications of struts acting as tethers and sites for storage of energy in the motions of myocytes during the cardiac cycle are discussed.
Similar content being viewed by others
References
Ahumada GG, Saffitz JE (1984) Fibronectin in rat heart: a link between cardiac myocytes and collagen. J Histochem Cytochem 32:383–388
Alexander R McN (1974) The mechanics of jumping by a dog (Canis familiaris). J Zool Lond 173:549–573
Bairati A (1938) Struttura e proprieta fisiche del sarcolemma della fibra muscolare striata. Z Zellforsch 27: 100–124
Bennett-Clark HC (1976) Energy storage in jumping animals, vol 1: Perspectives in experimental biology. Pergamon, Oxford
Borg TK, Caulfield JB (1981) The collagen matrix of the heart. Fed Proc 40:2037–2041
Borg TK, Johnson LD, Lill PH (1983) Specific attachment of collagen to cardiac myocytes: in vivo and in vitro. Dev Biol 97:417–423
Borg TK, Buggy J, Sullivan T, Laks J, Terracio L (1986a) Morphological and biochemical characteristics of the connective tissue network during normal development and hypertrophy. J Mol Cell Cardiol 18 [Suppl 1] 247 (abstract)
Borg TK, Terracio L, Rubin K, Gulberg D, Craig S (1986b) Colocalization of a collagen binding protein and vinculin in cardiac myocytes. Fed Proc 45:3837 [Abstract]
Brady AJ, Farnsworth SP (1986) Cardiac myocyte stiffness following extraction with detergent and high salt solutions. Am J Physiol 19:H932-H943
Brady AJ, Tan ST, Ricchiuti NV (1979) Contractile force measured in unskinned isolated adult rat heart fibres. Nature 282:728–729
Capasso JM, Remily RM, Smith RH, Sonnenblick EH (1983) Sex differences in myocardial contractility in the rat. Basic Res Cardiol 78:156–171
Caulfield JB (1983) Alterations in cardiac collagen with hypertrophy, vol 8: Perspectives in cardiovascular research. Raven, New York, pp 49–57
Caulfield JB, Borg TK (1979) The collagen network of the heart. Eab Invest 40:364–372
Chiesi M, Ho MM, Inesi G, Somlyo AV, Somlyo AP (1981) Primary role of sarcoplasmic reticulum in phasic contractile activation of cardiac myocytes with shunted myolemma. J Cell Biol 91:728–742
Cohen-Gould L, Robinson TF (1985) A novel method of immunogold staining for TEM and HVEM. In: Bailey GW (ed) 43rd Proc Elec Micr Soc Amer. San Francisco Press, San Francisco, pp 438–439
Ellisman MH, Porter KR (1980) Microtrabecular structure of the axoplasmic matrix: visualization of cross-linking structures and their distribution. J Cell Biol 87:464–479
Fabiato A, Fabiato F (1978) Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J Gen Physiol 72:667–699
Fawcett DW, McNutt NS (1974) Myocardial ultrastructure. In: Brady AJ, Eanger GW (eds) The mammalian myocardium. Wiley, New York London Sydney Toronto, pp 31–37
Ferrans VJ, Roberts WC (1973) Intermyofibrillar and nuclearmyo-fibrillar connections in human and canine myocardium: an ultrastructural study. J Mol Cell Cardiol 5:247–257
Fish D, Orenstein J, Bloom S (1984) Passive stiffness of isolated cardiac and skeletal myocytes in the hamster. Circ Res 54:267–276
Frank J, Beydler S (1985) Intercellular connections in rabbit heart as revealed by quick-frozen, deep-etched, and rotary-replicated papillary muscle. J Ultrastruct Res 90:183–193
Johnson DA, Gautsch JW, Sportsman JR, Elder JH (1984) Improved technique utilizing non-fat dry milk for analysis of proteins and nucleic acids transferred to nitrocellulose. Gen Anal Techn 1:3–8
Junker J, Sommer J (1977) Anchorfibers and the topography of junctional sarcoplasmic reticulum. In: Bailey GW (ed) 35th Proc Elec Micr Soc Amer. Claitor, Baton Rouge, pp 582–583
Linsenmayer TF (1981) Collagen. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum, New York, p 15
McCullough D (1976) The great bridge. Avon, New York, p 418
McGraw-Hill dictionary of scientific and technical terms (1984). 3rd ed, New York, p 1571
Muir AR (1967) The effects of divalent cations on the ultrastructure of the perfused rat heart. J Anat 101:239–261
Pardo JV, Siliciano JD, Craig SW (1983) Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J Cell Biol 97:1081–1088
Robinson TF (1980) Lateral connections between heart muscle cells as revealed by conventional and high voltage transmission electron microscopy. Cell Tissue Res 211:353–359
Robinson TF, Winegrad S (1981) A variety of intercellular connections in heart muscle. J Mol Cell Cardiol 13:185–195
Robinson TF, Hayward BS, Krueger JW, Sonnenblick EH, Wittenberg BA (1981) Isolated heart myocytes: ultrastructural case study technique. J Microsc 124:135–142
Robinson TF, Cohen-Gould L, Factor SM (1983) Skeletal framework of mammalian heart muscle: arrangement of inter-and pericellular connective tissue structures. Lab Invest 49:482–498
Robinson TF, Cohen-Gold L, Remily RM, Capasso JM, Factor SM (1985) Extracellular structures in heart muscle, Vol 5: Advances in myocardiology. Plenum, New York, pp 243–255
Saeki Y, Sagawa K, Hiroyuki S (1978) Dynamic stiffness of cat heart muscle in Ba+2-induced contracture. Circ Res 42:324–333
Schwartz E, Goldfischer S, Coltoff-Schiller B, Blumenfeld OO (1985) Extracellular matrix microfibrils are composed of core proteins coated with fibronectin. J Histochem Cytochem 33:268–274
Severs NJ, Slade AM, Powell T, Twist VW, Jones GE (1985) Morphometric analysis of the isolated calcium-tolerant cardiac myocyte: organelle volumes, sarcomere length, plasma membrane surface folds, and intramembrane particle density and distribution. Cell Tissue Res 240:159–168
Shear CR, Bloch RJ (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol 101:240–256
Spotnitz HM, Spotnitz WD, Cottrell TS, Spiro D, Sonnenblick EH (1974) Cellular basis for volume-related wall thickness changes in the rat left ventricle. J Mol Cell Cardiol 6:317–331
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Viidik A (1979) Biomechanical behavior of soft connective tissues. In: Akkas N (ed) Progress in Biomechanics. Sijthoff and Noordhoff. Alphen aan den Rijn, 75–113
Wainwright SA, Biggs WD, Currey JD, Gosline JM (1982) Mechanical design in organisms. Princeton Univ, Princeton, pp 9–14, 86–91
Waldman LK, Fung YC, Covell JW (1985) Transmural myocardial deformation in the canine left ventricle. Circ Res 57:152–163
Whalen WJ (1967) Oxygen availability in muscle. In: Tanz RJ, Kavaler F, Roberts J (eds) Factors influencing myocardial contractility. Academic, New York, pp 395–400
Winegrad S, Robinson TF (1978) Force generation among cells in the relaxing heart. Europ J Cardiol 7 [Suppl]: 63–70
Wittenberg BA, Robinson TF (1981) Oxygen requirements, morphology, cell coat and membrane permeability of calcium-tolerant myocytes from hearts of adult rats. Cell Tissue Res 216:231–251
Wittenberg BA, White RL, Ginzberg RD, Spray DC (1986) Effect of calcium on the dissociation of the mature rat heart into individual and paired myocytes: electrical properties of cell pairs. Circ Res 59:143–150
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Robinson, T.F., Factor, S.M., Capasso, J.M. et al. Morphology, composition, and function of struts between cardiac myocytes of rat and hamster. Cell Tissue Res. 249, 247–255 (1987). https://doi.org/10.1007/BF00215507
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00215507