Ultrafast endocytosis can retrieve a single, large endocytic vesicle as fast as 50–100 ms after synaptic vesicle fusion. However, the fate of the large endocytic vesicles is not known. Here we demonstrate that these vesicles transition to a synaptic endosome about one second after stimulation. The endosome is resolved into coated vesicles after 3 s, which in turn become small-diameter synaptic vesicles 5–6 s after stimulation. We disrupted clathrin function using RNA interference (RNAi) and found that clathrin is not required for ultrafast endocytosis but is required to generate synaptic vesicles from the endosome. Ultrafast endocytosis fails when actin polymerization is disrupted, or when neurons are stimulated at room temperature instead of physiological temperature. In the absence of ultrafast endocytosis, synaptic vesicles are retrieved directly from the plasma membrane by clathrin-mediated endocytosis. These results may explain discrepancies among published experiments concerning the role of clathrin in synaptic vesicle endocytosis.
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We would like to thank D. Lorenz and A. Muenster-Wandowski for providing access to electron microscopy, J. Iwasa for the original model figure, S. Jorgensen for image processing, and C. Garner for discussions. We thank EMBO for providing the travel funds (S.W.). The research was funded by the US National Institutes of Health (NS034307 EMJ), European Research Council grant (249939 SYNVGLUT CR), and German Research Council grants (Neurocure EXC 257 EMJ+CR, SFB 665 + SFB 958 CR). E.M.J. is an Investigator of the Howard Hughes Medical Institute and is an Alexander von Humboldt Scholar.
The authors declare no competing financial interests.
Extended data figures and tables
Ultrafast endocytosis removes membrane added by vesicle fusion at the lateral edge of the active zone. Large endocytic vesicles then fuse to endosomes. Endosomes are resolved into synaptic vesicles via a clathrin-dependent process. Newly formed synaptic vesicles can be recruited back to the active zone.
Hippocampal synapses were stimulated once and frozen at the indicated times. The experiments were performed at 37 °C in the presence of 4 mM external Ca2+. a, Electron micrographs showing invaginations and large endocytic vesicles (arrowheads) recovered via ultrafast endocytosis. b, Micrographs showing single coated buds (left, middle) or multiple buds (right) forming on an endosome. Arrows indicate coated buds on an endosome. c, Virtual section from an electron tomogram (left) and reconstruction (middle) showing a synaptic endosome with buds following a single stimulus. Arrows indicate coated buds on an endosome. The average intensity of coated buds from the top 20 nm (right, top) and the bottom 40 nm (right, bottom) is shown. Clathrin-cages can be preserved in our fixation and are visible in the tomogram. We found a total of 32 endosomes in these reconstructions (14 endosomes in the unstimulated control and 28 endosomes 3 s after stimulation). Of the total 32 endosomes, none were connected to the plasma membrane or showed evidence of a truncated tubule extending from the endosomal membrane. Of the 14 unstimulated endosomes, 8 were contained within single tomograms, and are therefore unambiguously closed on both ends. Of the 28 endosomes in stimulated synapses, 16 endosomes were contained within single tomograms so that it was clear that no attachment to the plasma membrane was possible. d, Examples of a coated pit on the plasma membrane (top) and a coated bud on an endosome (bottom). Note that the morphology of the coats is similar. e, Increase in the number of each endocytic structure per synaptic profile after a single stimulus at 37 °C. The prevalence of large endocytic vesicles and endosomes is followed by an increase in the number of clathrin-coated vesicles. Coated pits were not observed on the plasma membrane (PM). f, Frequency of profiles or tomograms that contain endosomal structures at 37 °C. Approximately 60% of unstimulated synapses contained one endosome. One second after stimulation, 60% of the synapses contained at least one endosome, and half of those synapses contained two endosomes. Three seconds after stimulation, ∼30% of the synapses contained budded endosomes and clathrin-coated vesicles, suggesting that those synapses were active. The standard error of the mean is shown in each graph. At least 146 synaptic profiles were analysed from each time point. For n values, detailed numbers and statistical analysis, see Supplementary Table 1.
a–e, Histograms (left) and cumulative plots (right), showing the size of large endocytic vesicles (red) and endosomes (orange) after one stimulus from control cells without ferritin (a), scrambled shRNA infected cells (b), and clathrin knockdown cells (c) both with ferritin. Ten stimuli were applied to scrambled shRNA (d) or clathrin knockdown cells (e). The large endocytic vesicles are defined as those that are within 50 nm of active zone and larger than a synaptic vesicle by visual inspection. Endosomes are defined as large vesicles greater than 50 nm from the active zone (often in the centre of the bouton) and are larger than ∼100 nm. Any vesicular compartment that has coated buds in the centre of the bouton is also categorized as an endosome. The numbers of endocytic structures in (a) represent all the structures scored from 100 ms and 300 ms time points. The number of large vesicles and endosomes in b–e represent all the ferritin-positive structures from later time points (3, 10, and 20 s). In the control shRNA (b), the number of large endocytic vesicles and endosomes has declined by these late time points, whereas the ferritin is trapped in large endocytic vesicles and synaptic endosomes in the clathrin knockdown experiments. Because ferritin passes from large endocytic vesicles to even larger budded endosomes, it is probable that the endocytic vesicles fuse with either each other or an existing compartment.
a, Left, western blot showing clathrin levels after one-week expression of a scrambled shRNA control or clathrin heavy chain shRNA in cultured hippocampal neurons. Right, an 80% reduction was observed (n = 3, P < 0.001, paired t-test). b, Normalized ratio of clathrin heavy chain and synaptophysin fluorescence in control and clathrin knockdown (chc KD) cultures. The clathrin/synaptophysin ratio is reduced to 64% in the knockdown cells. c, The mean fluorescence intensity (normalized to 30 min) representing the amount of transferrin uptake in control and knockdown cells. Transferrin uptake was reduced by 66% in the knockdown cells. d, e, Fluorescence images of immunocytochemical staining of hippocampal autaptic cultures using anti-synaptophysin (left), anti-clathrin heavy chain (middle), and merge in control (d) and clathrin knockdown cultures (e). f, Example micrographs of hippocampal mass cultures showing transferrin uptake. The standard error of the mean is shown. ***P < 0.001. For detailed numbers and statistical analysis, see Supplementary Table 1.
a, b, Sample traces from cell-attached voltage clamp during light stimulation in control (a) and clathrin knockdown (b). Number of action potentials triggered during the 10 ms light pulse is shown to the right. c, Readily-releasable pool (RRP) in control and clathrin knockdown cells, defined by brief application of 500 mM sucrose to autaptic neurons (control: 622 ± 56 pC, knockdown: 443 ± 52 pC, P < 0.01). d, Vesicular release probability (Pvr) in these cells (control 5.4 ± 0.4%, n = 54; knockdown 3.5 ± 0.4%, n = 48; P < 0.001). e, f, Average miniature EPSC (mEPSC) frequency (e) and amplitude (f). No change was observed in knockdown cells. g, Average number of synaptic vesicles per synaptic profile (n = 142 synapses for control and 137 for knockdown). h, Average number of docked vesicles in active zones per synaptic profile (control: no stimulation, 1.5 ± 0.1, n = 142 synapses; 100 ms, 0.8 ± 0.1, n = 142 synapses; knockdown: no stimulation, 1.2 ± 0.1, n = 137 synapses; 100 ms after stimulation, 1.0 ± 0.1, n = 149 synapses). The fraction of docked vesicles that fuse is greatly reduced by clathrin knockdown. P values are calculated against the unstimulated control shRNA cells. The standard error of the mean is shown in each graph. ***P < 0.001, **P < 0.01, and *P < 0.05, respectively. n.s., not significant.
Extended Data Figure 6 Following a single stimulus, clathrin is required at endosomes to regenerate synaptic vesicles.
a, Virtual section from an electron tomogram (left) and a reconstruction (right) showing a budded synaptic endosome containing ferritin particles in the scrambled shRNA control cell. We found a total of 33 endosomes in these reconstructions. Of these 33 endosomes, none were connected to the plasma membrane or showed evidence of a tubule extending from the endosomal membrane. A total of 17 of these 33 total endosomes were fully contained within the 200 nm tomogram. Of these 33 endosomes, 16 were ferritin-positive, and 8 of these 16 endosomes were fully contained in the tomogram. b, Micrographs showing ferritin-positive synaptic vesicles docked to active zone 10–20 s after stimulation. c, Average number of ferritin particles in large endocytic vesicles, clathrin-coated vesicles, and synaptic vesicles per synaptic profile examined. At least 134 synapses were analysed per time point. Ferritin progresses to synaptic vesicles in the control, but is trapped in large endocytic vesicles or endosomes in the clathrin knockdown. The fraction of synaptic profiles with ferritin was 27% for the control and 31% in the knockdown, suggesting that 70% of the synapses were silent. The mean number of ferritin particles found in an individual endosome, clathrin-coated vesicle, and synaptic vesicle, are 9.3 ± 1.0, 2.0 ± 0.2, and 1.9 ± 0.2, respectively. The total number of ferritin particles (indicated above), declined by 40% in the control relative to the 1 s time point but not in the knockdown, either due to the fusion of the newly formed synaptic vesicles or by return of excess membrane to the surface of the synapse. The standard error of the mean is shown. d, Distribution of ferritin-positive clathrin-coated vesicles (yellow) and synaptic vesicles (blue) relative to the active zone at defined time points after stimulation in the control cells. Numbers are binned by 50 nm. The first bin ‘0 nm’ means vesicles are docked in active zone. Endosomes are found at 285 ± 38 nm from the active zone. Note that the data in this figure represent further analysis of the data shown in Fig. 3.
Extended Data Figure 7 Following high-frequency stimulation, clathrin is required at endosomes to regenerate synaptic vesicles.
a, Average number of action potentials in 10 ms bins relative to light pulses during high-frequency stimulation (10 stimuli at 20 Hz, 0.5 s). Sample traces are shown above. Each light pulse triggered at least one action potential in both control and clathrin shRNA-treated cultures. b, Average number of ferritin molecules in large endocytic vesicles, clathrin-coated vesicles, and synaptic vesicles per profile examined. Ferritin is transferred from large endocytic vesicles to synaptic vesicles in the control but is trapped in large endocytic vesicles or endosomes in the clathrin knockdown. The number of profiles with ferritin particles after stimulation was 34% in the control and 36% in the clathrin knockdown, suggesting that 65% of the synapses were silent. On average, the number of ferritin molecules found in an individual endosome, clathrin-coated vesicle, and synaptic vesicle, are 9.2 ± 1.0, 1.9 ± 0.3, and 2.0 ± 0.2. At least 142 synapses were analysed per time point. The total number of ferritin particles (indicated above each time point), declined by 36% in the control, and by 23% in the knockdown relative to the 1 s time point. c, Distribution of ferritin-positive clathrin-coated vesicles (yellow) and synaptic vesicles (blue) relative to the active zone at defined time points after stimulation in the control shRNA cells. Numbers are binned by 50 nm. The first bin ‘0 nm’ means vesicles are docked at the active zone. Endosomes are found at 286 ± 43 nm from the active zone. The standard error of the mean is shown in each graph. Note that this figure represents further analysis of the data from Fig. 4.
Extended Data Figure 8 Pitstop 2 blocks regeneration of synaptic vesicles from endosomes after high-frequency stimulation.
Pitstop 2 is an inhibitor of clathrin terminal domain and blocks clathrin-mediated endocyotosis49. a, c, Electron micrographs showing ferritin containing vesicles in DMSO-treated (a) and Pitstop-2-treated cells (c) at different time points after stimulation. Ferritin is found in large vesicles after stimulation (middle) and in synaptic vesicles (right) in control, but it is trapped in endosomes in the Pitstop-2-treated cells. b, d, Average increase in ferritin-positive structures per synaptic profile in DMSO-treated (b) or Pitstop-2-treated cells (d). Ferritin progressed to synaptic vesicle-like structures in the control but remained in endosomes or large endocytic vesicles in Pitstop-2-treated cells. Clathrin-coated pits on the plasma membrane were not present at any time point and were not plotted. At least 140 synapses were analysed per time point. e, Virtual section from an electron tomogram (left) and a reconstruction (right) showing a synaptic endosome with buds following 10 stimuli at 20 Hz. Of 32 tomograms reconstructed from the 3 s time point, 25 of them showed at least one endosome in the terminal, and 7 showed budded endosomes. None of these endosomes were connected to the plasma membrane. The standard error of the mean is shown in each graph. For detailed numbers and statistical analysis, see Supplementary Table 1.
Extended Data Figure 9 Synaptic vesicles are regenerated directly from the plasma membrane in the absence of ultrafast endocytosis.
a, b, Average diameter of clathrin-coated pits, clathrin-coated vesicles, and synaptic vesicles in the latrunculin-A treated cells (a) or cells incubated at 22 °C for 5 min (b). The diameter of these structures is similar suggesting a precursor–product relationship. Diameter of coated pits was determined by the full-width at the half maximum depth of the pit. For detailed numbers and statistical analysis, see Supplementary Table 1.
This file contains Supplementary Text, describing detailed results from electrophysiology and Pitstop 2 experiments and Supplementary Table 1, which describes the statistical methods used and detailed values obtained in each experiment. (PDF 595 kb)
Supplementary Video 1. A movie showing a single tomogram of a synapse treated with scrambled shRNA 3 s after stimulation.
White arrow indicates a ferritin-positive spherical synaptic endosomes. Note that this synaptic endosome is not connected to the plasma membrane by a membrane tubule. Due to the resolution of the movie, ferritin particles may be hard to observe. (MOV 20243 kb)
The white arrow indicates a ferritin-positive spherical synaptic endosomes. Note that this synaptic endosome is not connected to the plasma membrane but is in a close contact with endoplasmic reticulum. (MOV 15521 kb)
Serial tomograms of two complete synapses 3 s after stimulation that had been treated as a control with scrambled shRNA.
The white arrows indicate three ferritin-positive synaptic endosomes. These endosomes are largely spherical, but endosome #2 is oblong and #3 is capped by a coat. Note that none of these endosomes are connected to the plasma membrane by a tubule. Occasionally, endosomes are associated with the plasma membrane via filamentous structures (for example endosome #2). (MOV 22600 kb)
The white arrows indicate three ferritin-positive spherical synaptic endosomes. Black arrows indicate three ferritin-positive synaptic endosomes with coated buds. Note that none of these endosomes are connected to the plasma membrane by an involution of the plasma membrane. Occasionally, endosomes are associated with the plasma membrane via filamentous structures (for example endosome #4 and 5). (MOV 27245 kb)
The white arrows indicate three ferritin-positive spherical synaptic endosomes. Black arrows indicate three ferritin-positive synaptic endosomes with coated buds. Note that none of these endosomes are connected to the plasma membrane by an involution of the plasma membrane. Occasionally, endosomes are associated with the plasma membrane via filamentous structures (for example endosome #4 and 5). (MOV 7568 kb)
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Watanabe, S., Trimbuch, T., Camacho-Pérez, M. et al. Clathrin regenerates synaptic vesicles from endosomes. Nature 515, 228–233 (2014). https://doi.org/10.1038/nature13846
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