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Neuromolecular Medicine 2002The classical experiments on synaptic vesicle recycling in the 1970s by Heuser and Reese, Ceccarelli, and their colleagues raised opposing theories regarding the speed,... (Review)
Review
The classical experiments on synaptic vesicle recycling in the 1970s by Heuser and Reese, Ceccarelli, and their colleagues raised opposing theories regarding the speed, mechanisms, and locations of membrane retrieval at the synapse. The Heuser and Reese experiments supported a model in which synaptic vesicle recycling is mediated by the formation of coated vesicles, is relatively slow, and occurs distally from active zones, the sites of neurotransmitter release. Because heavy levels of stimulation were needed to visualize the coated vesicles, Ceccarelli's experiments argued that synaptic vesicle recycling does not require the formation of coated vesicles, is relatively fast, and occurs directly at the active zone in a "kiss-and-run" reversal of exocytosis under more physiological conditions. For the next thirty years, these models have provided the foundation for studies of the rates, locations, and molecular elements involved in synaptic vesicle endocytosis. Here, we describe the evidence supporting each model and argue that the coated vesicle pathway is the most predominant physiological mechanism for recycling synaptic vesicles.
Topics: Animals; Clathrin; Coated Vesicles; Exocytosis; Humans; Models, Neurological; Nervous System; Presynaptic Terminals; Synaptic Membranes; Synaptic Transmission; Synaptic Vesicles
PubMed: 12428806
DOI: 10.1385/NMM:2:2:101 -
Trends in Neurosciences Mar 2013Rapid information processing in our nervous system relies on high-frequency fusion of transmitter-filled vesicles at chemical synapses. Some sensory synapses possess... (Review)
Review
Rapid information processing in our nervous system relies on high-frequency fusion of transmitter-filled vesicles at chemical synapses. Some sensory synapses possess prominent electron-dense ribbon structures that provide a scaffold for tethering synaptic vesicles at the active zone (AZ), enabling sustained vesicular release. Here, we review functional data indicating that some central and neuromuscular synapses can also sustain vesicle-fusion rates that are comparable to those of ribbon-type sensory synapses. Comparison of the ultrastructure across these different types of synapses, together with recent work showing that cytomatrix proteins can tether vesicles and speed vesicle reloading, suggests that filamentous structures may play a key role in vesicle supply. We discuss potential mechanisms by which vesicle tethering could contribute to sustained high rates of vesicle fusion across ribbon-type, central, and neuromuscular synapses.
Topics: Action Potentials; Animals; Caenorhabditis elegans Proteins; Cell Communication; Cell Membrane; Cytoskeletal Proteins; Drosophila Proteins; Humans; Kinetics; Membrane Fusion; Microscopy, Electron; Nerve Tissue Proteins; Neuromuscular Junction; Neurons; Neurotransmitter Agents; SNARE Proteins; Species Specificity; Synaptic Transmission; Synaptic Vesicles
PubMed: 23164531
DOI: 10.1016/j.tins.2012.10.001 -
Microbes and Environments 2020The nitrogen-fixing actinobacterium Frankia develops unique multicellular structures called vesicles, which are the site of nitrogen fixation. These vesicles are...
The nitrogen-fixing actinobacterium Frankia develops unique multicellular structures called vesicles, which are the site of nitrogen fixation. These vesicles are surrounded by a thick hopanoid lipid envelope that protects nitrogenase against oxygen inactivation. The phenotypes of five mutants that form smaller numbers of vesicles were investigated. The vesicles of these mutants were smaller than those of the wild type and had a phase dark appearance. They induced the expression of a glutamine synthetase gene in hyphae cells in response to ammonium starvation. These results suggest that genes impaired in the mutants do not function in global nitrogen regulation, but specifically function in vesicle differentiation.
Topics: Ammonium Compounds; Bacterial Proteins; Cytoplasmic Vesicles; Frankia; Glutamate-Ammonia Ligase; Mutation; Nitrogen Fixation
PubMed: 32269204
DOI: 10.1264/jsme2.ME19150 -
Cell Stem Cell Oct 2021During embryogenesis, optic vesicles develop from the diencephalon via a multistep process of organogenesis. Using induced pluripotent stem cell (iPSC)-derived human...
During embryogenesis, optic vesicles develop from the diencephalon via a multistep process of organogenesis. Using induced pluripotent stem cell (iPSC)-derived human brain organoids, we attempted to simplify the complexities and demonstrate formation of forebrain-associated bilateral optic vesicles, cellular diversity, and functionality. Around day 30, brain organoids attempt to assemble optic vesicles, which develop progressively as visible structures within 60 days. These optic vesicle-containing brain organoids (OVB-organoids) constitute a developing optic vesicle's cellular components, including primitive corneal epithelial and lens-like cells, retinal pigment epithelia, retinal progenitor cells, axon-like projections, and electrically active neuronal networks. OVB-organoids also display synapsin-1, CTIP-positive myelinated cortical neurons, and microglia. Interestingly, various light intensities could trigger photosensitive activity of OVB-organoids, and light sensitivities could be reset after transient photobleaching. Thus, brain organoids have the intrinsic ability to self-organize forebrain-associated primitive sensory structures in a topographically restricted manner and can allow interorgan interaction studies within a single organoid.
Topics: Cell Differentiation; Embryonic Development; Humans; Induced Pluripotent Stem Cells; Organogenesis; Organoids; Prosencephalon
PubMed: 34407456
DOI: 10.1016/j.stem.2021.07.010 -
Cell Biology International Reports Dec 1989The uptake of extracellular tracers into synaptic nerve terminals has been a phenomenon of persistent interest. Uptake is into synaptic vesicles, hence vesicles spend... (Review)
Review
The uptake of extracellular tracers into synaptic nerve terminals has been a phenomenon of persistent interest. Uptake is into synaptic vesicles, hence vesicles spend part of their life in continuity with the plasma membrane, as expected if exocytosis underlies the quantal discharge of neurotransmitters. However, exactly how or when synaptic vesicles acquire extracellular tracers has not been unambiguously determined. Two schools of thought have developed, one holding that vesicles acquire tracers directly via a reversible exo/endocytotic sequence in which they consistently maintain their biochemical identity during their transient continuity with the plasma membrane, the other holding that synaptic vesicles acquire tracers indirectly, via the formation of clathrin-coated vesicles which are spatially and temporally separate from exocytosis and reverse a temporary loss of the vesicles' individual identity upon merger with the plasma membrane. Efforts to distinguish between these two alternatives have generated an interesting diversity of electron microscopic experiments, many of which are reviewed here. However, definitive determination of which view is correct may ultimately require direct visualization of synaptic vesicle turnover in living nerve terminals. To this end, we here review the results of visualizing endocytosis in tissue cultured cells, where light microscopy can provide sufficient resolution to reveal membrane dynamics in living cells. This has allowed visual discrimination of two different types of endocytosis, one clathrin-mediated (coated vesicle formation) and the other actin-mediated (macropinocytosis). Current work is also reviewed which aims at determining experimental methods for inhibiting each type of endocytosis selectively. Hypertonicity and severe cytoplasmic acidification turn out to inhibit coated vesicle formation, while cytochalasin D and mild cytoplasmic acidification selectively inhibit macropinocytosis. Applied to nerves, these various treatments affect synaptic vesicle turnover in a manner that supports the notion that synaptic vesicle membrane recycles via the "indirect" route of coated vesicle formation.
Topics: Animals; Coated Pits, Cell-Membrane; Endosomes; Synaptic Vesicles
PubMed: 2576862
DOI: 10.1016/0309-1651(89)90020-9 -
Neurochemical Research Jul 1997Secretory vesicles are localized in specific compartments within neurosecretory cells. Morphometric, cytochemical and electrophysiological techniques have allowed the... (Review)
Review
Secretory vesicles are localized in specific compartments within neurosecretory cells. Morphometric, cytochemical and electrophysiological techniques have allowed the definition of secretory vesicle compartments. These are different pools in which vesicles are in various states of releasability. The transit of vesicles between compartments is not random, but an event controlled and regulated by Ca2+ and the cortical F-actin network. Cortical F-actin disassembly, a Ca(2+)-dependent event, controls the transit of secretory vesicles from the reserve compartment to the release-ready vesicle pool. Furthermore, the recent development of new technical approaches (patch-clamp membrane capacitance, electrochemical detection of amines with carbon-fibre microelectrodes) has now permitted us to understand the kinetics of single vesicle exocytosis.
Topics: Animals; Cell Membrane; Cytoplasmic Granules; Electrochemistry; Exocytosis; Kinetics; Neurosecretory Systems; Patch-Clamp Techniques
PubMed: 9232636
DOI: 10.1023/a:1022087910902 -
Frontiers in Physiology 2021The preparation of plasma membrane vesicles from a large variety of cells has contributed a wealth of information on the identity and vectorial properties of membrane...
The preparation of plasma membrane vesicles from a large variety of cells has contributed a wealth of information on the identity and vectorial properties of membrane transporters and enzymes. Vesicles from red blood cell (RBC) membranes are generated in media of extremely low tonicity. For functional studies, it is required to suspend the vesicles in higher tonicity media in order to bring the concentrations of the substrates of transporters and enzymes under investigation within the physiological ranges. We investigated the effects of hypertonic transitions on the vesicle morphology using transmission electron microscopy. The results show that hypertonic transitions cause an irreversible osmotic collapse of sealed membrane vesicles. Awareness of the collapsed condition of vesicles during functional studies is critical for the proper interpretation of experimental results.
PubMed: 34512397
DOI: 10.3389/fphys.2021.727726 -
Annual Review of Physiology 1999Patch-clamp capacitance measurements can monitor in real time the kinetics of exocytosis and endocytosis in living cells. We review the application of this technique to... (Review)
Review
Patch-clamp capacitance measurements can monitor in real time the kinetics of exocytosis and endocytosis in living cells. We review the application of this technique to the giant presynaptic terminals of goldfish bipolar cells. These terminals secrete glutamate via the fusion of small, clear-core vesicles at specialized, active zones of release called synaptic ribbons. We compare the functional characteristics of transmitter release at ribbon-type and conventional synapses, both of which have a unique capacity for fast and focal vesicle fusion. Subsequent rapid retrieval and recycling of fused synaptic vesicle membrane allow presynaptic terminals to function independently of the cell soma and, thus, as autonomous computational units. Together with the mobilization of reserve vesicle pools, local cycling of synaptic vesicles may delay the onset of vesicle pool depletion and sustain neuronal output during high stimulation frequencies.
Topics: Animals; Calcium; Electric Conductivity; Electrophysiology; Endocytosis; Exocytosis; Glutamic Acid; Nerve Endings; Synapses; Synaptic Vesicles
PubMed: 10099708
DOI: 10.1146/annurev.physiol.61.1.725 -
Molecular Membrane Biology Nov 2010Coat proteins orchestrate membrane budding and molecular sorting during the formation of transport intermediates. Coat protein complex I (COPI) vesicles shuttle between... (Review)
Review
Coat proteins orchestrate membrane budding and molecular sorting during the formation of transport intermediates. Coat protein complex I (COPI) vesicles shuttle between the Golgi apparatus and the endoplasmic reticulum and between Golgi stacks. The formation of a COPI vesicle proceeds in four steps: coat self-assembly, membrane deformation into a bud, fission of the coated vesicle and final disassembly of the coat to ensure recycling of coat components. Although some issues are still actively debated, the molecular mechanisms of COPI vesicle formation are now fairly well understood. In this review, we argue that physical parameters are critical regulators of COPI vesicle formation. We focus on recent real-time in vitro assays highlighting the role of membrane tension, membrane composition, membrane curvature and lipid packing in membrane remodelling and fission by the COPI coat.
Topics: COP-Coated Vesicles; Coat Protein Complex I; Physical Phenomena; Protein Transport
PubMed: 21067455
DOI: 10.3109/09687688.2010.510485 -
Yakugaku Zasshi : Journal of the... 2011The world constructed by self-organization of some amphiphils was discussed on the basis of micelle formation, vesicle formation, and oriented-nano-wire formation.... (Review)
Review
The world constructed by self-organization of some amphiphils was discussed on the basis of micelle formation, vesicle formation, and oriented-nano-wire formation. First, the micelle formation of a both water- and oil- soluble surfactant, Aerosol OT, was discussed. Solution states of micelles and monomer were discussed on the basis of thermodinamic and NMR spectroscopic analyses of micelle formation. Next, micelle-vesicle transition was discussed. It was proposed that the phospholipid LUV formation by removing detergents and destruction by adding detergents occurred via 4 stages. The 4 stage model instead of the 3 stage model could not only elucidate the complicated phenomena observed during micelle-vesicle transition, but predicted the size and properties of the vesicles formed by detergent removal from mixed micelles. Next, the vesicle formation of a fatty acid with a single hydrophobic chain different from phospholipid, which has two hydorophobic chains, was discussed. The vesicle formation was strongly affected by the presence of preformed vesicles and the size was biased on the preformed vesicles. It was shown there exist two pass ways in the process of micelle-vesicle transition by pH jump. One is fission of the preformed vesicles after transfer of monomers from newly added oleate micelles and the other is transition from the mixed micelles after partial solubilization by the oreate micelles. Then, the vesicle formation of HCO-10, which has 3 hydrophobic chains, the mixed vesicle formation of phosphatidylethanolamine and lysophosphtidylcholine, which can not form vesicles, and the phospholipid vesicle formation and destruction by removing and adding PEG-lipid, were discussed. Lastly, oriented nano wire formation of mulamyldipeptid-conjugated lipids with ca 5 nm of diameter was discussed.
Topics: Dioctyl Sulfosuccinic Acid; Fatty Acids; Hydrogen-Ion Concentration; Hydrophobic and Hydrophilic Interactions; Micelles; Nanowires; Particle Size; Phospholipids; Solutions; Surface-Active Agents; Thermodynamics; Unilamellar Liposomes
PubMed: 22129875
DOI: 10.1248/yakushi.131.1765