Independent anterograde transport and retrograde cotransport of domain components of myelinated axons
Neurons are highly polarized cells organized into functionally and molecularly distinct domains. A key question is whether the multiprotein complexes that comprise these domains are preassembled, transported, and inserted as a complex or whether their components are transported independently and ass...
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Veröffentlicht in: | The Journal of cell biology 2020-06, Vol.219 (6), p.1 |
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description | Neurons are highly polarized cells organized into functionally and molecularly distinct domains. A key question is whether the multiprotein complexes that comprise these domains are preassembled, transported, and inserted as a complex or whether their components are transported independently and assemble locally. Here, we have dynamically imaged, in pairwise combinations, the vesicular transport of fluorescently tagged components of the nodes of Ranvier and other myelinated axonal domains in sensory neurons cultured alone or together with Schwann cells at the onset of myelination. In general, most proteins are transported independently in the anterograde direction. In contrast, there is substantial cotransport of proteins from distinct domains in the retrograde direction likely due to coendocytosis along the axon. Early myelination did not substantially change these patterns of transport, although it increased the overall numbers of axonal transport vesicles. Our results indicate domain components are transported in separate vesicles for local assembly, not as preformed complexes, and implicate endocytosis along axons as a mechanism of clearance. |
doi_str_mv | 10.1083/jcb.201906071 |
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A key question is whether the multiprotein complexes that comprise these domains are preassembled, transported, and inserted as a complex or whether their components are transported independently and assemble locally. Here, we have dynamically imaged, in pairwise combinations, the vesicular transport of fluorescently tagged components of the nodes of Ranvier and other myelinated axonal domains in sensory neurons cultured alone or together with Schwann cells at the onset of myelination. In general, most proteins are transported independently in the anterograde direction. In contrast, there is substantial cotransport of proteins from distinct domains in the retrograde direction likely due to coendocytosis along the axon. Early myelination did not substantially change these patterns of transport, although it increased the overall numbers of axonal transport vesicles. 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A key question is whether the multiprotein complexes that comprise these domains are preassembled, transported, and inserted as a complex or whether their components are transported independently and assemble locally. Here, we have dynamically imaged, in pairwise combinations, the vesicular transport of fluorescently tagged components of the nodes of Ranvier and other myelinated axonal domains in sensory neurons cultured alone or together with Schwann cells at the onset of myelination. In general, most proteins are transported independently in the anterograde direction. In contrast, there is substantial cotransport of proteins from distinct domains in the retrograde direction likely due to coendocytosis along the axon. Early myelination did not substantially change these patterns of transport, although it increased the overall numbers of axonal transport vesicles. Our results indicate domain components are transported in separate vesicles for local assembly, not as preformed complexes, and implicate endocytosis along axons as a mechanism of clearance.</description><subject>Animals</subject><subject>Ankyrins - genetics</subject><subject>Ankyrins - metabolism</subject><subject>Anterograde transport</subject><subject>Axonal transport</subject><subject>Axonal Transport - physiology</subject><subject>Axons</subject><subject>Axons - metabolism</subject><subject>Cell Adhesion Molecules - genetics</subject><subject>Cell Adhesion Molecules - metabolism</subject><subject>Cells, Cultured</subject><subject>Cytoplasm - metabolism</subject><subject>Endocytosis</subject><subject>Endocytosis - genetics</subject><subject>Endocytosis - physiology</subject><subject>Myelin Sheath - metabolism</subject><subject>Myelination</subject><subject>Nerve Growth Factors - genetics</subject><subject>Nerve Growth Factors - metabolism</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Neuroscience</subject><subject>Nodes of Ranvier</subject><subject>Protein Domains</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Schwann Cells</subject><subject>Sensory neurons</subject><subject>Trafficking</subject><subject>Transport</subject><subject>Transport Vesicles - metabolism</subject><subject>Vesicles</subject><subject>Vesicular Transport Proteins - genetics</subject><subject>Vesicular Transport Proteins - metabolism</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUFP3DAQha0KVLbbHntFkbj0Ephx7LV9QUIr2iIhcYGzZZIJzSqxg51F8O9xBCyFy1h67-nTjB9jPxGOEXR1sqlvjzmggRUo_MIWKAWUGgXssQUAx9JILg_Yt5Q2ACCUqL6yg4pzbVCqBaML39BIefipcH6iGO6ia6iYovNpDHFWmyLS9GbU4d0KbdGEwXU-q8MYfIakWRyeqO-8m6gp3GPw6Tvbb12f6Mfru2Q3v8-v13_Ly6s_F-uzy7IWGqeSyJA0rRRIElqNUFMjJME89Yq0lsCBuFaaHLZKY-sQTKMq7oRsa14t2ekLd9zeDtTUeZ_oejvGbnDxyQbX2Y-O7_7Zu_BgFV_JCiEDfr0CYrjfUprs0KWa-t55CttkeWUAhRH555fs6FN0E7bR5_MsFyBWUikzA8uXVB1DSpHa3TIIdi7Q5gLtrsCcP_z_gl36rbHqGcLAmQA</recordid><startdate>20200601</startdate><enddate>20200601</enddate><creator>Bekku, Yoko</creator><creator>Salzer, James L</creator><general>Rockefeller University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3206-1396</orcidid><orcidid>https://orcid.org/0000-0001-9126-7197</orcidid></search><sort><creationdate>20200601</creationdate><title>Independent anterograde transport and retrograde cotransport of domain components of myelinated axons</title><author>Bekku, Yoko ; 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A key question is whether the multiprotein complexes that comprise these domains are preassembled, transported, and inserted as a complex or whether their components are transported independently and assemble locally. Here, we have dynamically imaged, in pairwise combinations, the vesicular transport of fluorescently tagged components of the nodes of Ranvier and other myelinated axonal domains in sensory neurons cultured alone or together with Schwann cells at the onset of myelination. In general, most proteins are transported independently in the anterograde direction. In contrast, there is substantial cotransport of proteins from distinct domains in the retrograde direction likely due to coendocytosis along the axon. Early myelination did not substantially change these patterns of transport, although it increased the overall numbers of axonal transport vesicles. 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subjects | Animals Ankyrins - genetics Ankyrins - metabolism Anterograde transport Axonal transport Axonal Transport - physiology Axons Axons - metabolism Cell Adhesion Molecules - genetics Cell Adhesion Molecules - metabolism Cells, Cultured Cytoplasm - metabolism Endocytosis Endocytosis - genetics Endocytosis - physiology Myelin Sheath - metabolism Myelination Nerve Growth Factors - genetics Nerve Growth Factors - metabolism Neurons Neurons - metabolism Neuroscience Nodes of Ranvier Protein Domains Protein transport Proteins Rats Rats, Sprague-Dawley Schwann Cells Sensory neurons Trafficking Transport Transport Vesicles - metabolism Vesicles Vesicular Transport Proteins - genetics Vesicular Transport Proteins - metabolism |
title | Independent anterograde transport and retrograde cotransport of domain components of myelinated axons |
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