Cytoplasmic architecture of the axon terminal: Filamentous strands specifically associated with synaptic vesicles

doi:10.1016/0306-4522(91)90143-C

Neuroscience

Volume 40, Issue 2, 1991, Pages 587-598

https://doi.org/10.1016/0306-4522(91)90143-C Get rights and content

Abstract

Cytoplasmic architecture of axon terminals in rat central nervous tissue was examined by quick-freeze deep-etch method to determine how synaptic vesicles and their associated cytoplasmic environment are organized in the terminal and to know how these structures participate in the mechanism for neurotransmitter release. The axoplasm is divisible into two domains: one occupied by mitochondria in the middle of the terminal, called the mitochondrial domain, the other situated in the periphery and exclusively filled with spherical synaptic vesicles, 50–60 nm in diameter, the synaptic vesicle domain. The most characteristic feature of the mitochondrial domain was the appearance of many microtubules connected with mitochondria by filamentous strands. Large vesicles, 80–100 nm in diameter, were preferentially associated with the mitochondrial domain, and linked with microtubules wherever they appeared. The cytoplasmic matrix of the synaptic vesicle domain showed a more fibrillar texture than that of the mitochondrial domain because of the distribution of filamentous strands associated with synaptic vesicles. These strands were significantly thicker and longer (mean 11.7nm thick and 42.7 nm long) than those linking membrane-bound organelles to microtubules (mean 8.3 nm thick and 23.0 nm long), and connected vesicles to one another or to the plasma membrane, making a complicated network around the vesicles. Further, both strands were significantly different in dimension from actin filaments (mean 9.9 nm thick and 73.5 nm long) showing 5-nm axial periodicity. These strands, especially synaptic vesicle-associated ones including their network, were readily broken down in the most part by detergent treatment or chemical fixation, indicating that they are very delicate in nature. Granular materials, which are spherical and vary in size (6–20 nm in diameter), are also more conspicuous in the synaptic vesicle domain than in the mitochondrial domain.

More fibrillar and granular cytoplasmic structure of the synaptic vesicle domain may be crucial for synaptic vesicles to perform an essential role in releasing the transmitter.

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Cytoplasmic architecture of the axon terminal: Filamentous strands specifically associated with synaptic vesicles

Abstract

Trends Neurosci.

Biochem. Pharmac.

Neuroscience

Cell

Neuron

Neuroscience

Neuroscience

Neuroscience

Synapsin I bundles F-actin in a phosphorylation-dependent manner

Nature

Ultrastructural observations on the cytoarchitecture of axons processed by rapid-freezing and freeze-substitution

J. Neurocytol.

The structure of cytoplasm in directly frozen cultured cells. II Cytoplasmic domains associated with organelle movements

J. Cell Biol.

Synapsin I (protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agaroseembedded synaptosomes

J. Cell Biol.

Evidence for the concentration of F-actin and myosin in synapses and in the plasmalemmal zone of axons

Eur. J. Cell Biol.

Two classes of actin microfilaments are associated with the inner cytoskeleton of axons

J. Cell Biol.

Synaptic vesicle relationships with the presynaptic membrane as shown by a new method of fast chemical fixation

Neuroscience

Deep-etch structure of astrocytes at the superficial glia limitans, with special emphasis on the internal and external organization of their plasma membranes

J. Neurocytol.

Substructure of cisternal organelles of neuronal perikarya in immature rat brains revealed by quick-freeze and deep-etch techniques

Cell Tiss. Res.

Postnatal development of the inferior olivary complex in the rat: IV. Synaptogenesis of GABAergic afferent, analyzed by glutamic acid decar☐ylase immunocytochemistry

J. comp. Neurol.

Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotary-replicated Torpedo postsynaptic membrane

J. Cell Biol.

Filament organization revealed in platinum replicas of freeze-dried cytoskeletons

J. Cell Biol.