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Polarity of Neuronal Membrane Traffic Requires Sorting of Kinesin Motor Cargo during Entry into Dendrites by a Microtubule-Associated Septin
Journal article   Open access   Peer reviewed

Polarity of Neuronal Membrane Traffic Requires Sorting of Kinesin Motor Cargo during Entry into Dendrites by a Microtubule-Associated Septin

Eva P Karasmanis, Cat-Thi Phan, Dimitrios Angelis, Ilona A Kesisova, Casper C Hoogenraad, Richard J McKenney and Elias T Spiliotis
Developmental cell, v 46(2), pp 204-218
16 Jul 2018
PMID: 30016622
url
https://doi.org/10.1016/j.devcel.2018.06.013View
Published, Version of Record (VoR) Open

Abstract

dendritic sorting microtubule motors kinesins neuronal polarity dendrites neuronal trafficking microtubules membrane traffic septins microtubule-associated proteins
Neuronal function requires axon-dendrite membrane polarity, which depends on sorting of membrane traffic during entry into axons. Due to a microtubule network of mixed polarity, dendrites receive vesicles from the cell body without apparent capacity for directional sorting. We found that, during entry into dendrites, axonally destined cargos move with a retrograde bias toward the cell body, while dendritically destined cargos are biased in the anterograde direction. A microtubule-associated septin (SEPT9), which localizes specifically in dendrites, impedes axonal cargo of kinesin-1/KIF5 and boosts kinesin-3/KIF1 motor cargo further into dendrites. In neurons and in vitro single-molecule motility assays, SEPT9 suppresses kinesin-1/KIF5 and enhances kinesin-3/KIF1 in a manner that depends on a lysine-rich loop of the kinesin motor domain. This differential regulation impacts partitioning of neuronal membrane proteins into axons-dendrites. Thus, polarized membrane traffic requires sorting during entry into dendrites by a septin-mediated mechanism that bestows directional bias on microtubules of mixed orientation. [Display omitted] •Kinesin motor cargos enter dendrites with differential motility and directional bias•SEPT9 is a dendritic MAP that impedes movement of kinesin-1/KIF5 and axonal cargo•SEPT9 promotes anterograde movement of kinesin-3/KIF1A and its dendritic cargo•SEPT9 distinguishes between loops L12 of KIF5 and KIF1A for entry into dendrites Polarized neuronal membrane traffic relies primarily on sorting at axonal entry, while dendrites appear to lack directional sorting due to mixed microtubule orientation. Karasmanis et al. show that a dendritically enriched microtubule-associated septin, SEPT9, impedes axonal kinesin-1/KIF5 but promotes dendritic kinesin-3/KIF1A motor cargo, thereby bestowing directional bias during dendritic entry.

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Web of Science research areas
Cell Biology
Developmental Biology
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