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Mechanistic Determinants of Slow Axonal Transport and Presynaptic Targeting of Clathrin Packets

Archan Ganguly, Florian Wernert, View ORCID ProfileSébastien Phan, View ORCID ProfileDaniela Boassa, Utpal Das, Rohan Sharma, Ghislaine Caillol, Xuemei Han, View ORCID ProfileJohn R. Yates III, View ORCID ProfileMark H. Ellisman, View ORCID ProfileChristophe Leterrier, View ORCID ProfileSubhojit Roy
doi: https://doi.org/10.1101/2020.02.20.958140
Archan Ganguly
1Department of Pathology, University of California, San Diego, La Jolla, CA
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
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Florian Wernert
3Aix Marseille Université, CNRS, INP UMR7051, NeuroCyto, Marseille, France
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Sébastien Phan
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
4National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA
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Daniela Boassa
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
4National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA
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Utpal Das
1Department of Pathology, University of California, San Diego, La Jolla, CA
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
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Rohan Sharma
1Department of Pathology, University of California, San Diego, La Jolla, CA
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
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Ghislaine Caillol
3Aix Marseille Université, CNRS, INP UMR7051, NeuroCyto, Marseille, France
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Xuemei Han
5Department of Cell Biology, The Scripps Research Institute, La Jolla, CA
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John R. Yates III
5Department of Cell Biology, The Scripps Research Institute, La Jolla, CA
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  • ORCID record for John R. Yates III
Mark H. Ellisman
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
4National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, CA
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Christophe Leterrier
3Aix Marseille Université, CNRS, INP UMR7051, NeuroCyto, Marseille, France
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Subhojit Roy
1Department of Pathology, University of California, San Diego, La Jolla, CA
2Department of Neurosciences, University of California, San Diego, La Jolla, CA
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  • For correspondence: sroy@ucsd.edu
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SUMMARY

Clathrin has established roles in endocytosis, with clathrin-cages enclosing membrane infoldings, followed by rapid disassembly and reuse of monomers. However, in neurons, clathrin synthesized in cell-bodies is conveyed into axons and synapses via slow axonal transport; as shown by classic pulse-chase radiolabeling. What is the cargo-structure, and mechanisms underlying transport and presynaptic-targeting of clathrin? What is the precise organization at synapses? Combining live-imaging, mass-spectrometry (MS), Apex-labeled EM-tomography and super-resolution, we found that unlike dendrites where clathrin transiently assembles/disassembles as expected, axons contain stable ‘transport-packets’ that move intermittently with an anterograde bias; with actin/myosin-VI as putative tethers. Transport-packets are unrelated to endocytosis, and the overall kinetics generate a slow biased flow of axonal clathrin. Synapses have integer-numbers of clathrin-packets circumferentially abutting the synaptic-vesicle cluster, advocating a model where delivery of clathrin-packets by slow axonal transport generates a radial organization of clathrin at synapses. Our experiments reveal novel trafficking mechanisms, and an unexpected nanoscale organization of synaptic clathrin.

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  • Revised title and abstract, other minor changes n text.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 05, 2020.
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Mechanistic Determinants of Slow Axonal Transport and Presynaptic Targeting of Clathrin Packets
Archan Ganguly, Florian Wernert, Sébastien Phan, Daniela Boassa, Utpal Das, Rohan Sharma, Ghislaine Caillol, Xuemei Han, John R. Yates III, Mark H. Ellisman, Christophe Leterrier, Subhojit Roy
bioRxiv 2020.02.20.958140; doi: https://doi.org/10.1101/2020.02.20.958140
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Mechanistic Determinants of Slow Axonal Transport and Presynaptic Targeting of Clathrin Packets
Archan Ganguly, Florian Wernert, Sébastien Phan, Daniela Boassa, Utpal Das, Rohan Sharma, Ghislaine Caillol, Xuemei Han, John R. Yates III, Mark H. Ellisman, Christophe Leterrier, Subhojit Roy
bioRxiv 2020.02.20.958140; doi: https://doi.org/10.1101/2020.02.20.958140

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