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Specific Granules in Atrial Muscle Cells

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Specific Granules in Atrial Muscle Cells SPECIFIC GRANULES IN ATRIAL MUSCLE CELLS J. D. JAMIESON, M.D., and G. E. PALADE, M.D. From The Rockefeller Institute ABSTRACT Large populations (up to 600/cell) of spherical, electron-opaque granules ~ 0.3 to 0.4/~ in diameter are characteristically found in muscle fibers of mammalian atria. They are absent in muscle fibers of the ventricles. The granules arc concentrated in the sarcoplasmic core and occur in lesser numbers in the sarcoplasmic layers between myofibrils and under the plasma membrane. Their intimate association with a central voluminous Golgi complex and the frequent occurrence of material reminiscent of the granular content within the cisternae of the Golgi complex suggest that the latter is involved in the formation of the atrial granules. Atrial granules are larger and more numerous in smaller species (rat, mouse), and generally smaller and less numerous in larger mammals (dog, cat, human); they are absent from the atrial fibers of very young fetuses (rat) but are present in those of newborn animals. A small population of bodies containing glycogen particles and remnants of the endoplasmic reticulum and mitochondria occurs in the sarcoplasmic cores of atrial as well as ventricular muscle fibers in the rat; they contain acid phosphatase and thus appear to be residual bodies of autolytic loci. Their frequency increases with the age of the animal. Typical lipofuscin pigment granules, which are known to contain acid phosphatase and are found in the sarcoplasmic cores in old animals (cat, dog and human), are presumed to arise by progressive aggregation and fusion of small residual bodies. INTRODUCTION The fine structure of mammalian ventricular atrial muscle cells from a wide variety of mam- myocardium has been described in several reports malian species, placing particular emphasis on (1-3) which have placed special emphasis on the their granules. The inquiry was conducted in organization of myofibrils and disposition of order to select a favorable material for the future sarcoplasmic reticulum in its muscle cells. Mam- chemical and functional characterization of these malian atrial myocardium has been less extensively granules. studied: only a few reports (4-10) on the fine structure of its muscle cells have appeared. The MATERIALS AND METHODS presence of a population of dense granules within atrial muscle cells was mentioned by some of Preparation for Electron Microscopy these authors and studied in more detail by Hearts of a variety of laboratory animals (rat, Bompiani et al. (8) in the rat heart. In 1961, Palade mouse, hamster, guinea pig, bat, cat, rabbit, dog,) (11) reported that the number of atrial granules and of the pig, ox, and human were used in this appeared to decrease in the rat upon reserpine study. Large animals were anesthetized with ether treatment and suggested that they may be intra- or intravenous Na pentobarbital; smaller animals cellular storage sites for catecholamines. Since were sacrificed by a blow to the head. The chests then, we have undertaken an extensive survey of were quickly opened and portions of the atria and 151 ventricles removed for fixation. In many cases, carried out according to the method of Wood and especially with smaller animals, the heart was per- Barrnett (17), fused and distended with fixative which was allowed to react in situ for several minutes to minimize con- Autoradiography traction and distortion of the muscle. Human left Osmium tetroxide-fixed tissues were embedded in atrial appendage was obtained during open heart methacrylate or Epon 812 and sections prepared for surgery performed on patients with mitral stenosis. light and electron microscopic autoradiography ac- In another instance, human material was obtained cording to the method of Caro (18). 3 hours postmortem. The specimens were fixed at N0 ° for 1 to 3 hours OBSERVATIONS in 1 per cent OsO4 buffered to pH 7.6 with 0.1 M K phosphate; in some instances, the tissue was pre- General Description of Atrial Muscle Cells fixed at 0 ° for 1 to 3 hours in 6.25 per cent glu- taraldehyde in the same buffer (12), washed over- The general organization of these cells is similar night in the buffer with sucrose added to restore to that described by others in both atrial and ven- osmolarity, and finally fixed for 1 to 3 hours at 0 ° tricular muscle fibers (1, 2, 8). Of particular in 1 per cent OsO4 buffered to pH 7.6 with 0.1 interest for us were the structurcs comprising the M K phosphate. Following dehydration in the cold central sarcoplasmic column or core (Figs. 1 and in a graded series of ethanol solutions, the tissue 2). Centrally placed within this core is a single was embedded in Epon 812 according to the method of Luft (13), or in methacrylate cross-linked with 5 elongate nucleus with numerous large mitochon- per cent divinylbenzene (14). Sections were cut on dria packed around each of its poles. Adjacent to a Porter-Blum microtome equipped with a diamond one, and occasionally to both, of the poles of the knife, collected on naked copper grids, and stained nucleus, the sarcoplasmic core contains a large with 0.5 per cent aqueous uranyl acetate for 30 population of spherical, clcctron-opaque granules minutes followed by alkaline lead or with alkaline intimately interspersed among the elements of a lead solution alone (15). The sections were strength- voluminous Golgi complcx. Similar granulcs are ened by a thin coat of carbon and examined in an found in much smallcr numbers in other loci in the RCA EMU 2B electron microscope or a Siemens cell as discussed later. In addition to these predom- Elmiskop I equipped with a 50 ~t objective aperture inant structures, the sarcoplasmic core contains ele- and operated with a double condenser at 80 kv. ments of rough endoplasmic reticulum, accumula- Cytochemical Procedures tions of glycogen particles, a few lipid droplets, and, scattered among all thcsc components, a The Gomori reaction for the detection of acid phosphatase (16) was performed on 50 tt frozen variable number of polymorphic bodies which sections of rat atrium and ventricle fixed in the cold could be described as dense bodies, residual for 2 hours with 4 per cent glutaraldehyde in 0.05 bodies, or lipofuscin pigment granules. M Na cacodylate (pH 7.1) and subsequently washed The sarcoplasmic core is enveloped by bundles for 2 hours at 0 ° in buffer to which 8 per cent sucrose typical myofibrils which occupy the remainder of was added. The sections were incubated at 0 ° for 1 the cell volume. These bundles arc separated by hour in 3 per cent Na-C~-glycerophosphate in 0.1 M sarcoplasmic layers containing mitochondria, ele- Na acetate at pH 5.0; the reaction mixture contained ments of the sarcoplasmic rcticulum, atrial gran- 0.12 per cent PbNO3 to precipitate liberated in- ules, and glycogen particles. The volume of the organic phosphate as electron-opaque lead phos- cell occupied by the myofibrillar envelope varies phate. Following a brief wash in acetate buffer, the sections were fixed at 0 ° in 1 per cent OsO4 in 0,1 according to the region of the atrium examined, M Na cacodylate (pH 7.1) for 11~ hours. Routine tending to be small in cells of the nodal and con- dehydration and embedment in Epon 812 followed. ductile tissue and relatively large in the rest. The chromaiCfin reaction for the detection of Atrial muscle fibers are bounded by a usual norepinephrine and cpinephrine in thin section was plasma membrane covered externally by a base- FIGURE 1 Longitudinally sectioned muscle cell illustrating general features of atrial muscle cell. Anterior wall of the right atrium (rat). The sarcoplasmie core contains a popu- lation of spherical granules (ag) , profiles of the Golgi complex (G), numerous mitochondria, an occasional residual body (rb), and a few lipid droplets (1). Sarcoplasmie layers between myofibrils contain an occasional granule. × 13,000. 152 THE JOURNAL OF CELL BIOLOGY " VOLUME 23, 1964 J. D. JAMIESON AND G. E. PALADE Atrial Granules 153 ment membrane; the intercellular junctions consist the material contained in the granule varies with of typical intercalated discs. the type of fixative, the embedding medium, and The structures in the sarcoplasmic core, specif- the staining procedures employed on the section. ically the atrial granules and their relationship to After OsO4 fixation, Epon embedment, and alka- neighboring elements, will be discussed in detail line lead staining, the content is electron-opaque below. As indicated, many mammalian species and finely granular. Embedment in methacrylate were examined but, as the heart of the rat was following OsO4 fixation tends to enhance this most extensively studied, the description and granularity, as does staining the tissue block with illustration will be based primarily on this material. potassium permanganate prior to embedding (Fig. 9). If glutaraldehyde fixation precedes Detailed Description of Atrial Granules osmium tetroxide fixation, the content of the granules is much less opaque and generally more 1. GENERAL INTRACELLULAR DISTRIBUTION homogeneous (@ Fig. 5). Finally, the content OF GRANULES becomes extremely opaque in sections stained with As already mentioned, most of the "specific" uranyl acetate. granules of the atrial muscle cells occur within the 3. RELATIONS OF SPECIFIC GRANULES TO sarcoplasmic core where they arc packed in large COMPONENTS IN THE CENTRAL COR~ masses (up to 600 per cell) (Figs. 2 and 3) adjacent to one pole of the nucleus. Occasionally a few a. GOLGI COMPLEX: The large masses of granules are found on the sides and adjacent to specific granules are intimately associated with a the other pole of the nucleus. Because of the spindle voluminous Golgi complex whose elements appear shape of the sarcoplasmic core, the granular mass scattered throughout the sarcoplasmic core.
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