Neurotransmitter release: fusion or ‘kiss-and-run’?

Fesce, Riccardo; Grohovaz, Fabio; Valtorta, Flavia; Meldolesi, Jacopo

doi:10.1016/0962-8924(94)90025-6

Cited by 309 publications

(225 citation statements)

References 26 publications

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“…The fast endocytotic mechanism we report here possesses several hallmarks of the`kiss and run' pathway proposed by Bruno Ceccarelli and colleagues (Ceccarelli et al 1973;Ceccarelli & Hurlbut 1980; for review, see Fesce et al 1994). This is a more complete and explanatory presentation of work reported in a recent paper (Klingauf et al 1998).…”

Section: Introductionmentioning

confidence: 95%

“…Vesicles may also reform directly by uncoating of clathrin-coated vesicles without equilibration with endosomes (Takei et al 1996). In a more rapid endocytotic pathway, generally known as`kiss and run' (Ceccarelli et al 1973;Ceccarelli & Hurlbut 1980;Fesce et al 1994), vesicles are rapidly retrieved after short-lived fusion pore openings (Ceccarelli & Hurlbut 1980;Fesce et al 1994;Henkel & Betz 1995;Koenig & Ikeda 1996;Murthy & Stevens 1998). In the`kiss and run' pathway, synaptic vesicles would retain their complex molecular composition and therefore be swiftly handled throughout the cycle during wide range of stimuli.…”

Section: Introductionmentioning

confidence: 99%

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Properties of fast endocytosis at hippocampal synapses

Kavalali¹,

Klingauf

Tsien

1999

Phil. Trans. R. Soc. Lond. B

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Regulation of synaptic transmission is a widespread means for dynamic alterations in nervous system function. In several cases, this regulation targets vesicular recycling in presynaptic terminals and may result in substantial changes in e¤ciency of synaptic transmission. Traditionally, experimental accessibility of the synaptic vesicle cycle in central neuronal synapses has been largely limited to the exocytotic side, which can be monitored with electrophysiological responses to neurotransmitter release. Recently, physiological measurements on the endocytotic portion of the cycle have been made possible by the introduction of styryl dyes such as FM1-43 as £uorescent markers for recycling synaptic vesicles. Here we demonstrate the existence of fast endocytosis in hippocampal nerve terminals and derive its kinetics from £uorescence measurements using dyes with varying rates of membrane departitioning. The rapid mode of vesicular retrieval was greatly speeded by exposure to staurosporine or elevated extracellular calcium. The e¡ective time-constant for retrieval can be 52 seconds under appropriate conditions. Thus, hippocampal synapses capitalize on e¤cient mechanisms for endocytosis and their vesicular retrieval is subject to modulatory control.

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Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Properties of fast endocytosis at hippocampal synapses

Kavalali¹,

Klingauf

Tsien

1999

Phil. Trans. R. Soc. Lond. B

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“…Such a slow pathway may represent a significant bottleneck for vesicle recycling under conditions of high activity, especially for the hippocampal synapses, which typically contain just 100-200 vesicles. Thus, an alternative mechanism has been proposed, known as the kiss-and-run pathway (Fesce et al 1994), in which vesicles transiently fuse with the plasma membrane through a relatively small pore, and endocytosis occurs simply by closure of the pore and retraction of the vesicle. A kiss-and-run mechanism might be able to recycle vesicles much more quickly than could the classical pathway.…”

Section: Using Fm Dyes To Image the Fine Dynamics Of Exocytosismentioning

confidence: 99%

Imaging Synaptic Vesicle Recycling by Staining and Destaining Vesicles with FM Dyes

Hoopmann¹,

Rizzoli²,

Betz³

2011

Cold Spring Harb Protoc

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The synaptic vesicle is the essential organelle of the synapse. Many approaches for studying synaptic vesicle recycling have been devised, one of which, the styryl (FM) dye, is well suited for this purpose. FM dyes reversibly stain, but do not permeate, membranes; hence they can specifically label membrane-bound organelles. Their quantum yield is drastically higher when bound to membranes than when in aqueous solution. This protocol describes the imaging of synaptic vesicle recycling by staining and destaining vesicles with FM dyes. Nerve terminals are stimulated (electrically or by depolarization with high K + ) in the presence of dye, their vesicles are then allowed to recycle, and finally dye is washed from the chamber. In neuromuscular junction (NMJ) preparations, movements of the muscle must be inhibited if imaging during stimulation is desired (e.g., by application of curare, a potent acetylcholine receptor inhibitor). The main characteristics of FM dyes are also reviewed here, as are recent FM dye monitoring techniques that have been used to investigate the kinetics of synaptic vesicle fusion. MATERIALSIt is essential that you consult the appropriate Material Safety Data Sheets and your institution's Environmental Health and Safety Office for proper handling of equipment and hazardous materials used in this protocol. Reagents FM dye(s)Dye concentrations are usually 2-10 µM for FM1-43 or FM4-64, and 25-40 µM for FM2-10. The dyes readily dissolve in water; stocks of 1-5 mM concentration should be prepared and can be stored at 4˚C. Neuronal tissue or cell sample of interest Equipment Imaging setupAn upright epifluorescence microscope equipped with a 40×-60× water-immersion objective is optimal. When working with cell cultures, the advantages of high-resolution oil-immersion objectives (e.g., 100×/1.4 numerical aperture [NA]) can be exploited by using an inverted setup. For FM1-43, maximal fluorescence is at 465-nm excitation/560-nm emission (Henkel et al. 1996); a conventional fluorescein filter set (435-nm excitation) can also be used. Because the major concern in FM imaging is phototoxicity (which appears usually before any clear signs of photobleaching and alters the ability of the preparations to recycle vesicles), keep the illumination to a minimum by including neutral-density filters. For example, when using a 40×/0.75-NA water-immersion objective with a 100-W mercury lamp, 5%-15% transmission is sufficient. On confocal setups, an argon 488-nm laser line is typically used for excitation, but special care has to be taken to avoid phototoxicity. Images are typically acquired by charge-coupled device (CCD) cameras or photomultiplier tubes, which allows for fast acquisition rates and software-based quantitative image analysis.Neuronal stimulator (see Step 3)

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“…Following 2 h of low-frequency stimulation at 2 Hz, the synaptic vesicle was released and retrieved at the same site instead of forming clathrin-coated vesicles [3] . This mode was later named "kiss-and-run" endocytosis [5] . Bulk endocytosis, which is a phenomenon in which a large piece of membrane is retrieved from the presynaptic plasma membrane, has also been frequently observed in several model cells, including the frog NMJ [4] , rat hippocampal neurons [6] and goldfish bipolar cells [7] .…”

Section: Introductionmentioning

confidence: 99%

Synaptic vesicle recycling at the calyx of Held

Xue

Mei

2011

Acta Pharmacol Sin

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Efficient endocytosis is crucial for maintaining synaptic transmission because of its role in retrieving constituent membrane and associated proteins. In the past three decades three modes of endocytosis have been proposed involving the central nervous system: clathrin-mediated endocytosis, kiss-and-run endocytosis and bulk endocytosis. These forms of endocytosis can be induced under different conditions, but their detailed molecular mechanisms and functions are largely unknown. Here, we review the existence and initiation of all three modes of endocytosis at a giant glutamatergic synapse, the calyx of Held. The possibility of direct electrophysiology recording in this synapse allows for accurate tracking of exocytosis and endocytosis via capacitance measurements. Future aims will be focused on identifying the molecules that undergo the different mechanisms of endocytosis and the conditions under which different forms of endocytosis predominate.

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Neurotransmitter release: fusion or ‘kiss-and-run’?

Cited by 309 publications

References 26 publications

Properties of fast endocytosis at hippocampal synapses

Properties of fast endocytosis at hippocampal synapses

Imaging Synaptic Vesicle Recycling by Staining and Destaining Vesicles with FM Dyes

Synaptic vesicle recycling at the calyx of Held

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