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Intracisternal Granules of the Endoplasmic Reticulu?¢I in the Crayfish Oocyte

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Intracisternal Granules of the Endoplasmic Reticulu?¢I in the Crayfish Oocyte INTRACISTERNAL GRANULES OF THE ENDOPLASMIC RETICULU?¢I IN THE CRAYFISH OOCYTE H. W. BEAMS and RICHARD KESSEL. From the I)epartinent of Zoology, State University of Iowa, Iowa City The early literature on the origin of yolk contains note that similar intracisternal granules are not numerous studies which assert that a close morpho- found in the pancreas of the mouse (5) or rat (7). logical relationship exists between the developing Large, dense granules of unknown significance yolk masses and certain cellular organelles. The have also been reported within the cisternae of nucleus, mitochondria, Golgi material, and er- the endoplasmic reticulum of the spider oocyte (1). gastoplasm have all, at one time or other, been In the course of a preliminary study on the fine implicated in the synthesis of yolk and of other structure of the crayfish egg it was noted that the types of secretion as well (@ Bowen, 2; Wilson, endoplasmic reticulum possessed sharply defined 12). The description of the fine structure of the intracisterna] granules. The fact that this condition ergastoplasm (endoplasmic reticulum), coupled is infrequently found in other cells seemed to with the firm evidence for the synthesis of protein warrant a description of it here. involving ribosomes, has led investigators to look for evidence of a close morphological relationship MATERIALS AND METHODS between the genesis of the protein-rich secretion Crayfish (Cambarus virilis) were collected locally granules and the elements of the endoplasmic during the spring and summer and pieces of the reticulum. Studies have been reported where large ovary fixed for 1 hour in cold Palade's solution secretion masses appear within the cisternae of buffered at pH 7.5 (6). The specimens were then the endoplasmic reticulum (cf. Porter, 8, for dehydrated rapidly, embedded in methacrylate, and literature). However, the best documented studies sectioned with a Porter-Blum microtome. The which seem to involve the endoplasmic reticulum sections were stained with lead hydroxide (4) and in the synthesis of protein secretion are those of examined with an RCA EMU 3D electron micro- Palade (7) and Siekevitz and Palade (9-11). scope. They present evidence which suggests that in the DESCRIPTION guinea pig pancreas the ribosomes synthesize the enzymes which traverse the cisternal membranes The season in which the ovaries were fixed is one and gave rise to the relatively large intracisternal in which rapid growth of the egg occurs, that is, granules; the latter probably have chemical a rapid synthesis and deposition of materials such properties similar to those of the definitive as lipids, glycogen, and yolk; the last is often of a zymogen granules. How the intracisternal granules heterogeneous nature, but generally is composed are delivered to other regions of the cytoplasm is of a high concentration of protein (3). An analysis not clear; they may exit in some way through the of the biochemistry of the crayfish egg has not to cisternae of the Golgi complex. It is interesting to our knowledge been made and the identity of the FIGURE 1 Survey electron micrograph showing form and distribution of the cisternal stacks of endoplasmic reticulum (ER) and lipid droplets (L). The groups of parallel cisternae arc limited by membranes bearing ribosomes and contain numerous intracisternal granules (IG). Intracisternal granules are also found in certain dilated regions of the loosely arranged and branching cisternae (DC). Note dense yolk body (Y) and unidentified vesicle (V). X 14,000. FIaURE 0 Dense yolk body (Y) which appears to be surrounded by membranes of the endoplasmic reticulum (arrows). X 14,000. 158 B n I E F N O T E S S n I E F N O T E S 159 various fine structural components is based upon about 40 to 60 m# in diameter. In some prepara- their morphology alone. tions parallel lines (lamellae ?) of a greater density A low power electron micrograph of a growing than the remaining part of the granule are ob- o6cyte is illustrated in Fig. 1. The two most striking served (Fig. 6). components of the cytoplasm, namely, the endo- The parallel cisternae appear somewhat dis- plasmic reticulum (ER) and lipid droplets (L), tended possibly due to the accumulation of are easily recognizable by their characteristic granules within them. The more highly magnified appearance. These are embedded in a continuous electron micrographs (Figs. 5, 6) show clearly the hyaline and homogeneous appearing cytoplasmic ribosomes arranged on the outer surface of the ground substance. The endoplasmic reticulum membranes bounding the cisternae and the extends throughout the ground cytoplasm and is rosettes of ribosomes located in the space between composed, in places, of stacks of parallel cisternae the membranes of the stacked cisternae (Fig. 5, that are limited by membranes having great RR). Ribosomes attached to the membranes and numbers of ribosomes attached to their outer in the rosettes measure about 15 m# in diameter. surface (Figs. 3 to 6). The groups of closely packed The loosely arranged network portion of the parallel cisternae are connected at their ends with endoplasmic reticulum which permeates through- other cisternae of similar shape and structure, but out the ground cytoplasm seems to have a struc- without preferred orientation; instead, they ture similar to that of the parallel cisternae; i.e., extend in all directions from the stacked cisternae, composed of flattened vesicles that are limited by branching and anastomosing freely so that the membranes. However, one important difference entire system of membrane-limited cisternae is noted, namely, that fewer ribosomes are present appears interconnected, a morphological condition on the outer surface of the membranes limiting suitable to serve as the basis for an active transport the randomly arranged cisternae than are present system (Fig. 1). on membranes of the parallel, stacked cisternae. From the description noted above it is clear that In many instances, the randomly arranged the fine structure of the endoplasmic reticulum in cisternae appear to be devoid of ribosomes. The the developing crayfish egg is, to some degree, loosely arranged network of endoplasmic reticulum similar to that in many other types of cells. How- also shows variation in the width of its branching ever, it differs from the condition in most other cisternae; the more dilated regions contain intra- cells in its distribution and in possessing clearly cisternal granules (Fig. 1, DC) while the remaining defined, well developed intracisternal granules portions often appear collapsed. (Figs. 1, 5, 6, IG). The granules, as well as the At this stage in the growth of the egg, no large entire content of the cisternae, appear more dense yolk spheres are present in the cytoplasm as is the than the surrounding cytoplasmic matrix. They case in the more mature o6cyte. However, dense are relatively numerous, discrete, and measure bodies are seen which are probably yolk (Figs. FIGURE 3 A yolk body (Y) showing continuity (arrow) with a granule-containing cisterna of the cndoplasmic reticulum. X 38,000. FIGURE 4 Yolk body (1I) in which scattered patches of discrete granules are apparent (arrow). The granules are similar to those within cisternae of endoplasmic reticulum. L, lipid droplet. X 32,000. FIGURES 5 AND 6 Sections through groups of cistcrnal stacks. The membranes bear ribosomes on their outer surface. Ribosomes are also found arranged as rosettes between the parallel cisternae (RR). Within the cistcrnae are intracisternal granule~ (1G). A portion of a vesicle (V) is sccn in Fig. 5. Fig. 5, X 32,000; Fig. 6, X 47,000. 160 B R I E F N O T E S B R I E F N 0 T E S 161 l to 4, Y). These bodies seem to be located within ribosomes. They then "flow" into and along the the cavities of the endoplasmic reticulum as unoriented cisternae to regions or pockets where judged by the fact that cisternal membranes they collect, expand the cisternae, and undergo appear to surround them (Figs. 2, 3, arrow). In transformation into a finely granular, relatively fact, in Fig. 3 a continuity is demonstrated between large yolk body which may or may not remain the yolk body and a granule-containing cisterna associated with the cisternae. of the endoplasmic reticulum. It is also possible to observe instances in which the forming yolk This research was aided in part by grants RG-4706, 5479, and 9230 from the National Institutes of body contains granules similar to the intracisternal Health, United States Public Health Service, and granules of the endoplasmic reticulum (Fig. 4, grant G-9879 from the National Science Foundation. arrow). These appear to be undergoing a dis- Received for publication, October 9, 1961. solution process which results in the eventual formation of a more homogeneous yolk body. BIBLIOGRAPHY Membrane-bounded vesicles (Figs. 1, 2, V) l. ANDRE, J., and ROUILLER, C., J. Biophysic. and were observed in the cytoplasm. Their identity is Bioehem. Cytol., 1957, 3, 977. unknown; they do not appear to be connected 2. BO~N, R. H., Quart. Rev. Biol., 1929, 4, 299 with the endoplasmic reticulum. and 484. It is interesting to note that both the mito- 3. BRACHET,J., The Biochemistry of Development, chondria and the Golgi material are relatively New York, Pergamon Press, 1960. sparse at this stage in the developing crayfish egg. 4. DALTON, A. J., and ZEIOEL, R. F., J. Biophysic. and Biochem. Cytol., 1960, 7,409. SUMMARY 5. FAR•UHAR, M. G., and WILLINGS, S. R., J. Biophysic. and Biochem. Cytol., 1957, 3, 319. This note records an additional observation of 6. PALADE, G. E., J. Exp. Med., 1952, 95, 281. well defined granules of uniform size within the 7. PALADE, G. E., J. aiophysic, and Bioehem. Cytol., cisternae of the endoplasmic reticulum.
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