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

Developmental Cell
Eva P KarasmanisElias T Spiliotis

Abstract

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.

Citations

Aug 26, 2018·Cytoskeleton·Konstantinos NakosElias T Spiliotis
Feb 17, 2019·The Journal of Biological Chemistry·Dominique V LessardChristopher L Berger
Sep 30, 2020·Molecular Biology of the Cell·Elias T Spiliotis, Michael A McMurray
Aug 9, 2019·Annual Review of Cell and Developmental Biology·Mithila Burute, Lukas C Kapitein
Oct 9, 2020·Journal of Neurogenetics·Amruta Vasudevan, Sandhya P Koushika
Jul 15, 2020·Physical Biology·Saurabh S MogreElena F Koslover
Jan 9, 2021·The Journal of Cell Biology·Ilona A KesisovaElias T Spiliotis
Nov 14, 2020·Cytoskeleton·Barry T DeRoseShae B Padrick
Dec 31, 2020·Molecular Biology of the Cell·Shalini MenonStephanie L Gupton
Nov 15, 2020·Current Opinion in Cell Biology·Benjamin L Woods, Amy S Gladfelter
Apr 16, 2020·Molecular and Cellular Neurosciences·Megan R RadlerElias T Spiliotis
Feb 29, 2020·Developmental Cell·Brigette Y MonroyKassandra M Ori-McKenney
May 26, 2021·Current Biology : CB·Jayne Aiken, Erika L F Holzbaur
May 26, 2021·Current Biology : CB·Elias T Spiliotis, Konstantinos Nakos
Jul 14, 2021·Trends in Cell Biology·Elias T Spiliotis, Ilona A Kesisova
Nov 20, 2021·The FEBS Journal·Ruolin Fan, Kwok-On Lai
Dec 7, 2021·Frontiers in Cell and Developmental Biology·Italo A CaviniRichard C Garratt
Dec 16, 2021·Journal of Cell Science·Anita BailletPatrick W Oakes

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