Abstract
The presynaptic membranes of the cone cell endings of the pigeon retina were investigated using the freeze-fracture technique.En face views of the cytoplasmic leaflet (P-face) of the split presynaptic membrane revealed several specialized membrane organizations, 1. membrane particle aggregates composed of 10–20 particles which were larger than the usual ones seen in the cell membrane, 2. fenestration-like circular structures of 30–50 nm in diameter which were not surrounded by membrane particles. 3. similiar circular structures as described above but which were accompanied by a few membrane particles on the circular margin and were considered to be an intermediate form of the first and second membrane structures. These three structures appeared simultaneously in one fracture plane of the presynaptic membrane; were situated at the same intervals from one another and were approximately equal in size to synaptic vesicles (30–50 nm). These findings strongly suggested that these three structures were serial events in presynaptic membrane organization.
When fortuitous cross fractures exposed both the P-face of the presynaptic membrane and the adjacent cytoplasm of the cone ending, fusion of the synaptic vesicles to the presynaptic membrane was observed, and was considered to be the opening of the synaptic vesicle to the synaptic cleft. These openings were also situated at the same distance as the structures described above.
These findings demonstrate the process of exocytosis of the synaptic vesicles by which the chemical transmitter is probably released to the synaptic cleft.
Zusammenfassung
Mit Hilfe der Gefrierätzungsmethode wurde die präsynaptische Membran von Zapfen-Endkolben der Taubenretina untersucht.
Spaltbilder der dem Zapfen-Zytoplasma aufliegenden präsynaptischen Membran lassen mehrere spezialisierte Membranstrukturen erkennen:
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1.
Ansammlungen von ca. 10–20 Partikeln, die größer sind als die Partikel die man üblicherweise im Bereich von Membranen antrifft
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2.
Fenestrationsartige kreisförmige Strukturen mit einem Durchmesser von ca. 30–50 nm. Im Bereich dieser Strukturen finden sich keine Partikel.
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3.
Kreisförmige Strukturen wie unter 2) beschrieben, an deren Rand sich jedoch wenige Partikel finden.
Die dritte Struktur wird als Zwischenform zwischen der ersten Struktur und der zweiten Struktur aufgefaßt. Alle drei Strukturen erscheinen simultan auf einem Gefrierbruch der präsynaptischen Zapfenmembran, sind in regelmäßigen Abständen zueinander angeordnet und von annähernd gleicher Größe wie die synaptischen Vesikel (30–50 nm). Diese Befunde lassen vermuten, daß es sich bei den genannten Strukturen um ineinander übergehende Organisationsformen der präsynaptischen Zapfen-Membran handelt.
In Gefrierbrüchen die sowohl das oben beschriebene Spaltbild der präsynaptischen Zapfen-Membran als auch das daran angrenzende Zytoplasma der Zapfen darstellen, konnte die Fusion der synaptischen Vesikel mit der präsynaptischen Membran beobachtet werden. Sie werden als Öffnung der synaptischen Vesikel in den synaptischen Spalt angesehen. Diese Öffnungen waren in gleichen Abständen wie die oben beschriebenen Strukturen der Zapfen-Membran angeordnet.
Die Ergebnisse der vorliegenden Untersuchungen zeigen den Prozeß der Exozytose von synaptischen Vesikeln, in deren Verlauf wahrscheinlich der chemische Transmitter in den synaptischen Spalt freigesetzt wird.
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References
Birks RI (1974) The relationship of transmitter release and storage to fine structure in a sympathetic ganglion. J Neurocytol 3:133–140
Birks RI, Huxley HE, Katz B (1960) The fine structure of the neuromuscular junction of the frog. J Physiol (Lond) 150:134–144
Branton D (1966) Fracture faces of frozen membranes. Proc Natl Acad Sci USA 55:1048–1056
Branton D (1971) Freeze-etching studies of membrane structure. Phil. Trans. B 261:133–138
Ceccarelli B, Hurlbut WP, Mauro A (1972) Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol 54:30–38
Ceccarelli B, Hurlbut WP, Mauro A (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57:499–524
Clark AW, Hurlbut WP, Mauro A (1972) Changes in the fine structure of the neuromuscular junction of the frog caused by black widow spider venom. J Cell Biol 52:1–14
Cohen AI (1963) The fine structure of the visual receptors of the pigeon. Exp Eye Res 2:88–97
Del Castillo J, Katz B (1954) Quantal components of the endplate potential. J Physiol (Lond) 124:560–573
De Robertis E, Bennett SH (1954) Submicroscopic vesicular component in the synapse. Fed Proc 13:35 (Abstr)
Dreifuss JJ, Akert K, Sandri C (1976) Specific arrangements of membrane particles at sites of exo-endocytosis in the freeze-etched neurohypophysis. Cell Tiss Res 165:317–325
Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol (Lond) 117:109–128
Heuser JE, Miledi R (1971) Effect of lanthanum ions on function and structure of frog neuromuscular junctions. Proc R Soc Lond B Biol Sci 179:247–260
Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315–344
Heuser JE, Reese TS, Landis DMD (1974) Functional changes in frog neuromuscular junctions studied with freeze-fracture. J. Neurocytol 3:109–131
Hubbard JI, Kwanbunbumpen S (1968) Evidence for the vesicle hypothesis. J Physiol (Lond) 194:407–420
Korneliussen H (1972) Ultrastructure of normal and stimulated motor endplates. Z Zellforsch Mikrosk Anat 130:28–57
Model PG, Highstein SM, Bennett MVL (1975) Depletion of vesicles and fatigue of transmission at a vertebrate central synapse. Brain Res 98:209–228
Nishiura M (1972) Designing of new model of freeze-etching apparatus. Kagaku (Tokyo) 42:431–438
Ohkuma M, Nishiura M (1973) Freeze-fracture and freeze-etch replica of the eye. I. Replica of the chorio-capillary, Bruch's membrane and retinal pigment epithelium. Folia ophthal Jap 24:197–209
Palay SL (1956) Synapses in the central nervous system. J Biophys Biochem Cytol 2:193–202
Perri V, Sacchi O, Raviola E, Raviola G (1972) Evaluation of the number and distribution of synaptic vesicles at cholinergic nerve-endings after sustained stimulation. Brain Res 39:526–529
Pfenninger K, Akert K, Moor H, Sadri C (1971) Freeze-fracturing of presynaptic membranes in the central nervous system. Philos Trans R Soc Lond B Biol Sci 261:387–388
Pysh JJ, Wiley RG (1974) Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. J Cell Biol 60:365–374
Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 65:192–222
Robertson JD (1956) The ultrastructure of a reptilian myoneural junction. J Biophys Biochem Cytol 2:381–394
Schacher SM, Holtzman E, Hood DC (1974) Uptake of horseradish peroxidase by frog photoreceptor synapses in the dark and the light. Nature (Lond) 249:261–263
Schacher S, Holtzman E, Hood DC (1976) Synaptic activity of frog retinal photoreceptors: a peroxidase uptake study. J Cell Biol 70:178–192
Schaeffer SF, Raviola E (1978) Membrane recycling in the cone cell endings of the turtle retina. J Cell Biol 79:802–825
Satir B, Schooley C, Satir P (1973) Membrane fusion in a model system. Mucocyst secretion in Tetra hymena. J Cell Biol 56:153–176
Theodosis DT, Dreifuss JJ, Orci L (1978) A freeze-fracture study of membrane events during neurohypophysial secretion. J Cell Biol 78:542–553
Zimmermann H, Whittaker VP (1974) Effect of electrical stimulation on the yield and composition of synaptic vesicles from cholinergic synapses of the electric organ of Torpedo: a combined biochemical, electrophysiological and morphological study. J Neurochem 22:435–450
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Matsumura, M., Okinami, S. & Ohkuma, M. Specialized intramembrane organizations of the cone presynaptic membrane in the pigeon retina. Albrecht von Graefes Arch. Klin. Ophthalmol. 214, 89–100 (1980). https://doi.org/10.1007/BF00572787
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DOI: https://doi.org/10.1007/BF00572787