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The Neuronal Endomembrane System III 0270.6474/85/0512-3135$02.00/O The Journal of Neuroscience Copyright 0 Society for Neuroscience Vol. 5, No. 12. pp. 3135-3144 Pnnted in U.S.A. December 1985 The Neuronal Endomembrane System III. The Origins of Axoplasmic Reticulum Discrete Axonal Cisternae the Axon Hillock’ JAMES D. LINDSEY2 AND MARK H. ELLISMAN Department of Neurosciences, University of California, San Diego, School of Medicine, La Jolla, California 92093 Abstract The axoplasmic reticulum (AR) and the discrete element vesicles were usually found in close association with the (e.g., vesicles, vesiculotubular bodies, multivesicular bodies, trans face of the Golgi apparatus. These results indirectly etc.) constitute the endomembrane system of the axon. It is support the hypothesis that vectors of fast axonal transport, reported here that the AR of bullfrog sciatic nerve readily fills namely the discrete elements, form directly at the trans face with osmium deposits during osmium impregnation. In con- of the Golgi apparatus. From here they move toward and trast, the discrete elements and mitochondria are highly subsequently down the axon without any membrane fission- resistant to impregnation. Hence this preparation is well fusion events with either RER or AR. AR, although it forms suited to address the nature of possible interactions between continuities with RER, retains a distinctly different chemical AR and rough endoplasmic reticulum (RER) in the axon composition from RER as evidenced by its much higher hillock. It is also ideal to study the origin of the axonal discrete affinity for osmium. Thus, it should be considered as an elements within the cell body as well as their interaction with endomembrane component separate from, although inti- other somal endomembrane system components. Tissues mately related to the RER. used in the present study were spinal ganglia, sciatic nerve, and spinal roots from Rana catesbeiana. Thick sections (1 to 2 km) of this material were studied by high voltage electron The axoplasmic reticulum (AR) is an extensive system of branched microscopy. In some cases, osmium impregnation was fol- membranous tubules that extend in a continuous manner through lowed by en bloc staining with lead aspartate. This made axoplasm (Droz et al., 1975; Tsukita and Ishikawa, 1976). This visible membranous structures that had not filled with os- reticulum can be subdivided into two categories: a central or core mium deposits during impregnation. Serial 170-nm-thick sec- reticulum that pervades the main portions of axoplasmic space, and tions of this latter material were prepared and serial stereo a subaxolemmal reticulum that forms networks of tubules adjacent pair electron micrographs of axon hillocks were collected. to the inner surface of the axonal plasma membrane (Droz et al., These were used to reconstruct three-dimensionally the AR 1975; Berthold, 1982). Connections between the core and subaxo- and to study its relationship with RER and with discrete lemma1 reticulum have been observed frequently. The observations elements. The impregnated AR within the axon hillock was in this study pertain mainly to elements associated with the core found to terminate as many proximally pointing finger-like reticulum. In addition to at least two types of AR, several forms of projections. A large portion of these projections were found discrete membrane-bound organelles are also found within axo- to form connections with RER. Some, however, terminated plasm. These include multivesicular bodies, multilamellar bodies, as true blind endings. Single unimpregnated discrete cister- and a variety of vesicles and vesiculotubular bodies (reviewed in nae were found throughout the cytoplasm of the cell body, Grafstein and Forman, 1980; Ellisman and Lindsey, 1983). The axon hillock, and axon. Large clusters of unimpregnated discrete nature of multivesicular bodies and multilamellar bodies has been unchallenged for over a decade (Grafstein and Forman, Received May 14, 1984; Revised May 16, 1985; 1980). The discrete nature of these and many other axoplasmic Accepted May 23, 1985 organelles has been noted in reports using analysis of serial sections (LaVail et al., 1980) and stereoscopic viewing of thick sections ’ This work was supported by grants from the National Institutes of Health (Ellisman and Porter, 1980; Ellisman and Lindsey, 1983). Together, (NS14718) the Muscular Dystrophy Association, the National Multiple Scle- the various discrete cisternae and the two forms of the AR constitute rosis Society, and the Eprlepsy Foundation of America to M. H. E. J. D. L. the endomembrane system of the axon. Within the cell body, the was supported by a Nattonal Science Foundation predoctoral fellowship. We endomembrane system compartments include: the rough endoplas- wish to thank Dolores Taitano for word processing, Thomas Deerinck and mic reticulum (RER), lysosomes, the Golgi apparatus and associated Derek Leong for technical assrstance, Dr. Stephen Young for valuable tubules, and small discrete elements such as vesicles and multive- assrstance during the computer reconstructions, Dr. Phillip Groves for the sicular bodies (Lindsey and Ellisman, 1985a, b). use of his computing facilities, and the University of Colorado for use of the Interest in the axonal endomembrane system originated from National High Voltage Electron Microscope Resource Facility (P41.RROO592). biochemical and autoradiographic evidence indicating that fast ax- ’ Current address: Retinal Degeneration Center, Wilmer Ophthalmological onal transport is mediated by membranous components of the Institute, Johns Hopkins University School of Medicine, 600 North Wolfe neuron (Barondes, 1967; Droz et al., 1973, 1975). Compelling Street, Baltimore, MD 21205. evidence from several groups that discrete elements move relatively 3 To whom correspondence should be addressed, rapidly in both the orthograde and retrograde directions has recently 3135 3136 Lindsey and Ellisman Vol. 5, No. 12, Dec. 1985 extended this concept. (Tsukita and Ishikawa, 1980; Smith, 1980; Analysis of serial sections. Serial series (170 nm thick) from tissue stained Brady et al., 1982; Ellisman and Lindsey, 1983). The AR, however, en bloc with Walton’s lead aspartate (Walton, 1977) were collected on appears to be relatively stationary (Ellisman and Lindsey, 1983). Formvar-coated slot grids, carbon stabilized, and examined at 100 KeV. Recent findings have also shown that most molecules destined for Serial axon hrllock images were collected at low magnification and at +5;” fast axonal transport pass through the Golgi apparatus (GA) (Ham- and -5” tilt (instrument magnification x 6600). These images were next enlarged to 20 x 25 cm prints. The prints were reproduced onto xerographtc merschlag et al., 1982). Collectively, these findings indicate that transparencies (Chartpak, AFX25) using a Minolta EP530R copier at exactly each of these systems may play distinct roles in the fast transport 100% original magnification. (Most photocopters were found not to reproduce of new neuronal products. at exactly 1 OO%.) Uncertainty remains, however, concerning the intimate anatomical To reconstruct the AR, stereoscopically, alignment marks were made at interrelationships of these systems. Treatment of neurons with a four separate points on the first xerographic film image from a given tilt series double impregnation using heavy-metal salt solutions fills the lumen using a felt-tipped marking pen. On a light box, the next corresponding tilt of all membrane compartments within the cell with an electron-dense film Image of the series was aligned with the first based on ultrastructural deposit (Thierry and Rambourg, 1974). High voltage electron micro- landmarks such as lysosomes and mitochondria. The altgnment marks on scopic examination of treated neurons produced images that show the first film image were then duplicated on the second film image with the felt pen. This was repeated in sequence for all of the film images of a given AR joining to tubular profiles in the cell soma that look much like set and its matching tilt set (i.e., the other half of the stereo serial series). impregnated RER (Droz et al., 1975). This finding was recently Next, a clear acetate transparency was laid over the first film image of one confirmed using stereoscopic analysis (Rambourg et al., 1983) and, side of the stereo-tilt series. Outlines of the axolemma and AR were then in the case of photoreceptors, by serial section reconstruction of drawn with a felt-tipped pen along with the alignment marks. The acetate conventionally fixed tissue (Mercurio and Holtzman, 1982). However, transparency was then aligned over the next film image of the tilt series and a histochemical study using silver proteinate (a technique that outlines of this axolemma and AR were drawn. This was repeated for the demonstrates the presence of sugars such as are found on glyco- remainder of the tilt series and also for the matching tilt series. The recon- proteins) found that, although AR in the axon and tubular profiles structed drawrngs from each of the two sets were aligned in a stereoscopic near the GA in the cell body stain positive, there was no staining of viewing device so as to project one of the drawings to one eye and the other RER (Quatacker, 1981). This latter finding at the very least argues drawing to the other eye. To study the relationship between AR and unimpregnated membrane against the presence of a simple continuity between RER and AR. systems of the axon, the xerographic film reproductions
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