Hitching a Ride: Mechanics of Transport Initiation through Linker-Mediated Hitchhiking

Saurabh S. Mogre; Jenna R. Christensen; Cassandra S. Niman; Samara L. Reck-Peterson; Elena F. Koslover

doi:10.1016/j.bpj.2020.01.024

Hitching a Ride: Mechanics of Transport Initiation through Linker-Mediated Hitchhiking

Saurabh S. Mogre, Jenna R. Christensen, Cassandra S. Niman, Samara L. Reck-Peterson, Elena F. Koslover^*

^*Corresponding author for this work

Molecular Biosciences

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

In contrast to the canonical picture of transport by direct attachment to motor proteins, recent evidence shows that a number of intracellular “cargos” navigate the cytoplasm by hitchhiking on motor-driven “carrier” organelles. We describe a quantitative model of intracellular cargo transport via hitchhiking, examining the efficiency of hitchhiking initiation as a function of geometric and mechanical parameters. We focus specifically on the parameter regime relevant to the hitchhiking motion of peroxisome organelles in fungal hyphae. Our work predicts the dependence of transport initiation rates on the distribution of cytoskeletal tracks and carrier organelles, as well as the number, length, and flexibility of the linker proteins that mediate contact between the carrier and the hitchhiking cargo. Furthermore, we demonstrate that attaching organelles to microtubules can result in a substantial enhancement of the hitchhiking initiation rate in tubular geometries such as those found in fungal hyphae. This enhancement is expected to increase the overall transport rate of hitchhiking organelles and lead to greater efficiency in organelle dispersion. Our results leverage a quantitative physical model to highlight the importance of organelle encounter dynamics in noncanonical intracellular transport.

Original language	English (US)
Pages (from-to)	1357-1369
Number of pages	13
Journal	Biophysical Journal
Volume	118
Issue number	6
DOIs	https://doi.org/10.1016/j.bpj.2020.01.024
State	Published - Mar 24 2020

Funding

We thank Hiroyuki Hakozaki for assistance with lattice light sheet imaging and processing, as well as the Nikon Imaging Center at UC San Diego for help with imaging and data analysis. S.S.M. acknowledges funding via a predoctoral fellowship from the Visible Molecular Cell Consortium/Center for Trans-scale Structural Biology and Biophysics ; E.F.K. was supported by a fellowship from the Alfred P. Sloan Foundation and funding from the National Science Foundation CAREER Award Program ( 1848057 ). J.R.C. is funded by a postdoctoral fellowship from the National Institutes of Health ( F32GM126692 ), and S.L.R.-P. is funded by the Howard Hughes Medical Institute and the National Institutes of Health ( R01GM121772 ). We thank Hiroyuki Hakozaki for assistance with lattice light sheet imaging and processing, as well as the Nikon Imaging Center at UC San Diego for help with imaging and data analysis. S.S.M. acknowledges funding via a predoctoral fellowship from the Visible Molecular Cell Consortium/Center for Trans-scale Structural Biology and Biophysics; E.F.K. was supported by a fellowship from the Alfred P. Sloan Foundation and funding from the National Science Foundation CAREER Award Program (1848057). J.R.C. is funded by a postdoctoral fellowship from the National Institutes of Health (F32GM126692), and S.L.R.-P. is funded by the Howard Hughes Medical Institute and the National Institutes of Health (R01GM121772).

ASJC Scopus subject areas

Biophysics

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abstract = "In contrast to the canonical picture of transport by direct attachment to motor proteins, recent evidence shows that a number of intracellular “cargos” navigate the cytoplasm by hitchhiking on motor-driven “carrier” organelles. We describe a quantitative model of intracellular cargo transport via hitchhiking, examining the efficiency of hitchhiking initiation as a function of geometric and mechanical parameters. We focus specifically on the parameter regime relevant to the hitchhiking motion of peroxisome organelles in fungal hyphae. Our work predicts the dependence of transport initiation rates on the distribution of cytoskeletal tracks and carrier organelles, as well as the number, length, and flexibility of the linker proteins that mediate contact between the carrier and the hitchhiking cargo. Furthermore, we demonstrate that attaching organelles to microtubules can result in a substantial enhancement of the hitchhiking initiation rate in tubular geometries such as those found in fungal hyphae. This enhancement is expected to increase the overall transport rate of hitchhiking organelles and lead to greater efficiency in organelle dispersion. Our results leverage a quantitative physical model to highlight the importance of organelle encounter dynamics in noncanonical intracellular transport.",

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Hitching a Ride: Mechanics of Transport Initiation through Linker-Mediated Hitchhiking

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