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Clathrin regenerates synaptic vesicles from endosomes
Open accessAbstract
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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“Indeed, ultrafast endocytosis initiates as fast as 20–50 ms after exocytosis and completes within 100 ms5–7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“In this pathway, endocytic invaginations always form at the edge of the active zone5–7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“Based on the reliance of ultrafast endocytosis on F-actin7 and the high sensitivity of actin polymerization to temperature change74–76, we attribute this result to a slowed actin turnover at the room temperature7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“When ultrafast endocytosis is blocked, a slow clathrin-mediated endocytic pathway can kick in7 - this is consistent with observations from live-cell imaging of endocytosis68–70.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“In our previous study, we demonstrated that ultrafast endocytosis fails when neurons are incubated at room temperature for 5 min prior to experiments – this failure is compensated by clathrin-mediated endocytosis7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“When ultrafast endocytosis is blocked, clathrin-mediated endocytosis takes its place7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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Multicolor Caged dSTORM Resolves the Ultrastructure of Synaptic Vesicles in the Brain
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“The observed time constant of 470 ms is consistent with the recent EM results from glutamatergic hippocampal synapses (Delvendahl et al., 2016; Watanabe et al., 2013, 2014).”
BackgroundMethodResultInfluentialSelf-citationRate-limiting recovery processes in neurotransmission under sustained stimulation
Ernst, A., Unger, N., Schütte, C., Walter, A. M., & Winkelmann, S. (2023) · Mathematical Biosciences · doi:10.1016/j.mbs.2023.109023 · Cited by 7
Quantitative Synaptic Biology: A Perspective on Techniques, Numbers and Expectations
Reshetniak, S., Fernández‐Busnadiego, R., Müller, M., Rizzoli, S. O., & Tetzlaff, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197298 · Cited by 6
“A further complication is that the clathrin involvement may take place not only at the plasma membrane, but also at a later step, on endosome-like organelles that initially formed without the involvement of clathrin at the plasma membrane [25,26].”
BackgroundSmall, C., Harper, C., Jiang, A., Kontaxi, C., Yak, N., Malapaka, A., Davenport, E. C., Wallis, T. P., Gormal, R. S., Joensuu, M., et al. (2022) · doi:10.1101/2022.12.12.520075 · Cited by 4
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“…pretreated neurons with four inhibitors targeting distinct pathways ( 1 ) and assessed their effects, including: (i) shRNA against clathrin heavy chain (CHC) to disrupt CME ( 42 ) with CHC KD confirmed by more than a 60 % reduction of CHC IF intensity in CHC KD neurons compared to WT neurons (fig.”
One Cycle Fuels Another: The Energetics of Neurotransmitter Release
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“…at the nerve terminal, but these have been proposed to serve as an intermediate in the pathway for clathrin-dependent synaptic vesicle regeneration after bulk endocytosis or the more recently described ultrafast endocytosis (Barysch et al., 2009; Kononenko et al., 2014; Watanabe et al., 2014).”
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“They are then either broken-up into SVs (Watanabe et al., 2014) or designated for lysosomal degradation, possibly after some time spend as a recycling endosome at the presynapse (Rizzoli, 2014).”
BackgroundDelayed recruitment of activity‐dependent bulk endocytosis in Fmr1 knockout neurons
Kim, N., Bonnycastle, K., Kind, P. C., & Cousin, M. A. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16178 · Cited by 4
“There is an emerging view that CME is an integrated component of a unified endosomal retrieval system which allows the presynapse to scale endocytosis to the extent of SV fusion, thus maintaining membrane tension (Blumrich et al., 2023 ; Kononenko et al., 2014 ; Watanabe et al., 2014 ).”
Roles of membrane mechanics-mediated feedback in membrane traffic
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Phase Field Modeling of Inhomogeneous Biomembranes in Flow
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SV2A-Syt1 interaction controls surface nanoclustering and access to recycling synaptic vesiclesPreprint
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InfluentialSelf-citationOsipenko, D. S., Galimzyanov, T. R., & Akimov, S. A. (2016) · Biochemistry (Moscow) Supplement Series A Membrane and Cell Biology · doi:10.1134/s1990747816030077 · Cited by 3
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“These structures were revealed to be larger than synaptic vesicles and resemble recycling endosomes described elsewhere (Kamin et al, 2014; Revelo et al, 2014; Watanabe et al, 2014; Jung et al, 2015).”
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“In the pre-synaptic compartment, clathrin surrounded synaptic vesicles ( Figure 3I ) and budding vesicles on internal membrane compartments ( Figure 3J ), which is in agreement with previous time-resolved EM experiments ( Watanabe et al., 2014 ).”
Optical recordings of synaptic vesicle fusion reveal diffusional dispersionPreprint
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The molecular infrastructure of glutamatergic synapses in the mammalian forebrain
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“Before docking and priming, synaptic vesicles are formed, primarily through clathrin-mediated endocytosis (Heuser and Reese 1973; Maycox et al. 1992; Watanabe et al. 2014).”
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Metabotropic glutamate receptor internalization and synaptic AMPA receptor endocytosis by dopamine
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Cool views of membrane remodeling
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“…et al., 2013b), endosomes are defined as structures larger than 100 nm and located more than 50 nm away from the dense projection, as described by (Watanabe et al., 2014); however, by an alternative definition of endosome, structures with sizes larger than SVs and DCVs, with an electron dense…”
Synaptic Vesicle Recycling at the Developing Presynapse
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“As stated in the introduction, various modes of endocytosis are proposed to coexist at the presynapse, namely CME, ADBE and UFE.”
InfluentialNeuronal functions of clathrin-associated endocytic sorting adaptors – from molecules to disease
Kononenko, N. L., & Haucke, V. (2020) · e-Neuroforum · doi:10.1515/nf-2020-0023 · Cited by 2
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Release sites are positioned to activate NMDA receptorsPreprint
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Dynamin forms liquid-like condensates at synapses to support ultrafast endocytosisPreprint
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The molecular infrastructure of glutamatergic synapses in the mammalian forebrainPreprint
Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2024) · eLife · doi:10.7554/elife.100335.1 · Cited by 2
Slow scission of single synaptic vesicles by Dynamin at physiological temperaturePreprint
Krishnan, S., Lehrich, J., Tsytsyura, Y., Glyvuk, N., Duan, J., & Klingauf, J. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.18.643914 · Cited by 2
“This was reflected in the stoichiometry of Dynamin molecules which at most form a little more than a turn at the vesicle neck (Extended data Fig.6) while Dynamin can assemble to up to 3 turns in non-neuronal fission sites 12 .”
Handshaking for ultrafast endocytosis: Dynamin1xA and Endophilin A1 sealed the deal
López-Begines, S., & Fernández‐Chacón, R. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00179-1 · Cited by 1
“Strikingly, those events turned out to be independent of clathrin, the typical molecular scaffold mediating vesicular uptake of cargo at the plasma membrane (Watanabe et al, 2013, 2014).”
BackgroundMethodTan, H., McAdam, R. L., Morton, A., Cousin, M. A., & Smillie, K. J. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70134 · Cited by 1
Parameter Optimization for a Neurotransmission Recovery Model
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“Our approximation of the vesicle recovery rate is based on Watanabe et al. (Watanabe et al. 2014) who found and tracked a sequence of events in vesicle recovery.”
Diacylglycerol kinases: Molecular mechanism of cellular and physiological functions
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Merighi, A., Sbriz, M., & Lossi, L. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1839947 · Cited by 1
“Importantly, SCVs are rapidly retrieved via clathrin-mediated endocytosis or ultrafast endocytic pathways, refilled, and recycled to terminate fast signaling (Watanabe et al., 2014).”
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“The generation of SVs from the endosome involves clathrin-like cages surrounding vesicles that facilitate endocytosis and trafficking (Watanabe et al., 2014).”
BackgroundFlash-and-Freeze: A Novel Technique to Capture Membrane Dynamics with Electron Microscopy
Li, S., Raychaudhuri, S., & Watanabe, S. (2017) · Journal of Visualized Experiments · doi:10.3791/55664-v · Cited by 1
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Electrophysiological Analysis of the Synaptic Vesicle Priming Process
Nestvogel, D. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6444 · Cited by 1
AP2 regulates Thickveins trafficking through Rab11 to attenuate NMJ growth signaling in DrosophilaPreprint
Dwivedi, M. K., Choudhury, S. D., Patnaik, A., Mishra, S., Raghu, P., & Kumar, V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.28.428584 · Cited by 1
“5 membrane endocytosis cannot be ruled out [31].”
BackgroundInvestigating post-translational modifications and novel interaction partners of otoferlin
Cepeda, A. P. (2019) · doi:10.53846/goediss-7705 · Cited by 1
Jarazo, J., da Silva, E. S., Glaab, E., Perez-Bercoff, D., & Schwamborn, J. C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.20.533485 · Cited by 1
Rho GTPase signaling and mDia facilitate endocytosis via presynaptic actinPreprint
Oevel, K., Hohensee, S., Kumar, A., Rosas-Brugada, I., Bartolini, F., Soykan, T., & Haucke, V. (2024) · eLife · doi:10.7554/elife.92755.2 · Cited by 1
Ultrafast endocytosis in mouse cortical inhibitory synapsesPreprint
Eddings, C. R., & Watanabe, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.06.658279 · Cited by 1
“As in previous studies, cationized ferritin particles acted as fluid-phase markers of endocytosis 20,37 .”
Self-citationThe molecular infrastructure of glutamatergic synapses in the mammalian forebrainPreprint
Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2025) · eLife · doi:10.7554/elife.100335.2 · Cited by 1
Structure-function analysis of the Vesicular glutamate transporter 1 (VGLUT1) C-terminus
Jordan, J.-C. (2015) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-8460
Lewis, S. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3865
Towards unified vesicle endocytosis
Lučić, V. (2014) · Nature · doi:10.1038/nature13925
Endocytosis and Synaptic Function
Soukup, S., Verstreken, P., & Vilain, S. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803783-6.00007-9
Molecular physiology of signal transmission along the auditory pathway
Butola, T. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6529
Ni, Y.-X., Xue, W., Zhou, N., Yung, W., Lin, R., Kao, R. Y. T., Duan, Z., Tang, X.-M., Liu, M., Zhang, W., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/284166
“In contrast, when examining synaptic vesicles, the endocytosis of which involves CCVs of small size (40-45 nm in diameter) (Zhang et al., 1998, Watanabe et al., 2014), no changes of synaptic vesicle formation or related function were observed by kif5b knockout in mouse cortex (Figure S6).”
BackgroundWen, X. (2018) · DigitalCommons@UNMC
ATP Depletion Impairs Activity-dependent Ultrafast Endocytosis at Hippocampal Synapses
Gan, Q., & Watanabe, S. (2018) · Microscopy and Microanalysis · doi:10.1017/s1431927618007043
Self-citationChen, R. (2017) · TSpace (University of Toronto)
The endolysosomal system in neuronal physiology and pathology
Sanchez, S. V. (2019)
Bilkey, J., Nahirney, P. C., & Delaney, K. R. (2019) · Synapse · doi:10.1002/syn.22136
“In a follow‐up study, Watanabe et al. (2014) tracked the fate of the large vesicles with subsequent fixation time points.”
BackgroundInfluentialRedlingshöfer, L., McLeod, F., Camus, M., Chen, Y., Burden, J., Vila, E. P., Briant, K., Dannhauser, P. N., Salinas, P., & Brodsky, F. (2019) · bioRxiv · doi:10.1101/815183 · Cited by 2
Morphological Studies of Synaptic Vesicle Recycling at the Inner Hair Cell Ribbon Synapse
Kroll, J. (2020) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7800
Liu, Z., Zhu, Y., Hu, Y., & Sun, J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.03.433702
Molecular mechanisms of synaptic vesicle recycling with a focus on Endophilin A and Rabconnectin-3a
Gowrisankaran, S. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7717
Faculty Opinions recommendation of Synaptic vesicles transiently dock to refill release sites.
Klyachko, V. A. (2021) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738749520.793583444
Olsthoorn, H. M. (2021) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-8919
Long-Term Temporal Dynamics of Synaptic Vesicles
Truckenbrodt, S. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6481
Expansionsmikroskopie des Rattenhirns zur subzellulären Lokalisation synaptischer Proteine
Kemna, N. A. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9052
Kohansal-Nodehi, M. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6118
Mayor, S., & Hemalatha, A. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733515523.793555324
Faculty Opinions recommendation of Synaptic vesicles transiently dock to refill release sites.
Chapman, E. R., & Vevea, J. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738749520.793581127
Faculty Opinions recommendation of Synaptic vesicles transiently dock to refill release sites.
Brodin, L. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738749520.793578967
Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosisPreprint
Jing, H., Ogunmowo, T. H., Raychaudhuri, S., Kusick, G. F., Imoto, Y., Li, S., Itoh, K., Chapman, E. R., Ha, T., Watanabe, S., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.12.495801
Self-citationKinetic analysis of neuronal SNARE protein interactions
Pribicevic, S. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9392
Revealing ultrastructural changes that determine the development of a CNS synapse
Hintze, A. (2023) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9828
Reversal of cell, circuit and seizure phenotypes in a mouse model of DNM1 epileptic encephalopathyPreprint
Bonnycastle, K., Dobson, K. L., Blumrich, E.-M., Gajbhiye, A., Davenport, E. C., Pronot, M., Steinruecke, M., Trost, M., Gonzalez‐Sulser, A., & Cousin, M. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.14.536870
Excitation-Secretion Coupling of Dense-Core Vesicle Release
Cirkovic, V. (2023) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-10009
Mahapatra, S., & Takahashi, T. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.01.551580
“This was somewhat unexpected since in hippocampal culture Latrunculin-A blocks ultra-fast endocytosis (UFE, Watanabe et al. 2013), which occurs preferentially at physiological temperature (Watanabe et al., 2014).”
Background
Metadata
- Authors
- Watanabe, S., Trimbuch, T., Camacho-Pérez, M., Rost, B. R., Brokowski, B., Söhl-Kielczynski, B., Felies, A., Davis, M. W., Rosenmund, C., & Jorgensen, E. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Charité – Universitätsmedizin Berlin (DE)
- German Center for Neurodegenerative Diseases (DE)
- Corresponding author
- Rosenmund, Christian
- Venue
- Nature
- Published
- 2014-10-08
- Volume
- 515
- Issue
- 7526
- Pages
- 228-233
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4291189
- OpenAlex
- W2029980283
- Cited by
- 333
- References
- 49
- Citations by year
- 2026: 17 · 2025: 30 · 2024: 29 · 2023: 26 · 2022: 33 · 2021: 26 · 2020: 32 · 2019: 29 · 2018: 20 · 2017: 33 · 2016: 22 · 2015: 29 · 2014: 7
- FWCI
- 15.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DZNE Pub (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Neurological Disorders and Stroke (R37NS034307, NS034307, R01NS034307)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- clathrin, synaptic vesicle recycling, coated vesicles, clathrin-mediated endocytosis, actin polymerization, temperature dependence, optogenetic stimulation, high-pressure freezing, axon terminals, synaptic vesicle fusion
- MeSH terms
- Animals, Cell Membrane, Clathrin, Endocytosis, Humans, Endosomes, Synaptic Vesicles, Temperature, Mice
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