Skeletal framework of mammalian heart muscle. Arrangement of inter- and pericellular connective tissue structures

Abstract

We have studied the connective tissue of mammalian heart muscle in order to obtain an integrated description of extracellular structures and their dispositions relative to cardiac myocytes. Light microscopy and several types of electron microscopy have been employed in these investigations. The epimysium, the sheath of connective tissue that surrounds the muscle, contains relatively large fibers of collagen and elastin. In papillary muscles of rat, the large collagen fibers of the epimysium form a weave pattern at slack length (sarcomere lengths 1.8 to 2.0 micron) but are well aligned in states of stretch along the long axis of the muscle (sarcomere length 2.3 to 2.5 micron). We propose that the epimysial collagen network protects the sarcomeres from being stretched beyond lengths favorable to maximal force production. The endomysium is defined as the connective tissue that surrounds and interconnects myocytes; it consists of intercellular struts (bundles of collagen fibrils, often attached near Z-band level), a weave of bundles of collagen fibrils that envelopes myocytes, and a collagen fibril-microthread-granule lattice that bridges cells and fills the extracellular matrix. In contracted muscles festoons of sarcolemma are attached to Z-bands, thus forming regions for transmission of force across the sarcolemma. Perimysial bundles of collagen connect epimysium to endomysium and surround groups of myocytes. Collagen fibers often have a twisted configuration, probably for enhanced tensile strength. Superimposed on the large extracellular structures is the polyanion-rich lattice comprised of unit collagen fibrils, microthreads, and granules. Amorphous ground substance forms a matrix in which the fibrils of collagen fibers are embedded; it appears continuous with the cell coat in regions of fiber attachment. Elastic fibers interconnect cells and helically wind around myocytes. Circumferential forces from elastin stretched about shortened, thickened myocytes in systole should promote elongation in tandem with intramyocyte forces of elongation.