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Title: Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Abstract

Here, intracellular cargos are transported by molecular motors along actin and microtubules, but how their dynamics depends on the complex structure of the cytoskeletal network remains unclear. In this study, we investigated this longstanding question by measuring simultaneously the rotational and translational dynamics of cargos at microtubule intersections in living cells. We engineered two-faced particles that are fluorescent on one hemisphere and opaque on the other and used their optical anisotropy to report the rotation of cargos. We show that cargos undergo brief episodes of unidirectional and rapid rotation while pausing at microtubule intersections. Probability and amplitude of the cargo rotation depend on the geometry of the intersecting filaments. The cargo rotation is not random motion due to detachment from microtubules, as revealed by statistical analyses of the translational and rotational dynamics. Instead, it is an active rotation driven by motor proteins. Although cargos are known to pause at microtubule intersections, this study reveals a different dimension of dynamics at this seemingly static state and, more importantly, provides direct evidence showing the correlation between cargo rotation and the geometry of underlying microtubule intersections.

Authors:
; ; ; ;
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1527036
Alternate Identifier(s):
OSTI ID: 1466757; OSTI ID: 1495259
Report Number(s):
SAND-2018-8863J
Journal ID: ISSN 0006-3495; S0006349518305861; PII: S0006349518305861
Grant/Contract Number:  
NA0003525; AC04-94AL85000
Resource Type:
Published Article
Journal Name:
Biophysical Journal
Additional Journal Information:
Journal Name: Biophysical Journal Journal Volume: 114 Journal Issue: 12; Journal ID: ISSN 0006-3495
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Gao, Yuan, Anthony, Stephen M., Yu, Yanqi, Yi, Yi, and Yu, Yan. Cargos Rotate at Microtubule Intersections during Intracellular Trafficking. United States: N. p., 2018. Web. https://doi.org/10.1016/j.bpj.2018.05.010.
Gao, Yuan, Anthony, Stephen M., Yu, Yanqi, Yi, Yi, & Yu, Yan. Cargos Rotate at Microtubule Intersections during Intracellular Trafficking. United States. https://doi.org/10.1016/j.bpj.2018.05.010
Gao, Yuan, Anthony, Stephen M., Yu, Yanqi, Yi, Yi, and Yu, Yan. Fri . "Cargos Rotate at Microtubule Intersections during Intracellular Trafficking". United States. https://doi.org/10.1016/j.bpj.2018.05.010.
@article{osti_1527036,
title = {Cargos Rotate at Microtubule Intersections during Intracellular Trafficking},
author = {Gao, Yuan and Anthony, Stephen M. and Yu, Yanqi and Yi, Yi and Yu, Yan},
abstractNote = {Here, intracellular cargos are transported by molecular motors along actin and microtubules, but how their dynamics depends on the complex structure of the cytoskeletal network remains unclear. In this study, we investigated this longstanding question by measuring simultaneously the rotational and translational dynamics of cargos at microtubule intersections in living cells. We engineered two-faced particles that are fluorescent on one hemisphere and opaque on the other and used their optical anisotropy to report the rotation of cargos. We show that cargos undergo brief episodes of unidirectional and rapid rotation while pausing at microtubule intersections. Probability and amplitude of the cargo rotation depend on the geometry of the intersecting filaments. The cargo rotation is not random motion due to detachment from microtubules, as revealed by statistical analyses of the translational and rotational dynamics. Instead, it is an active rotation driven by motor proteins. Although cargos are known to pause at microtubule intersections, this study reveals a different dimension of dynamics at this seemingly static state and, more importantly, provides direct evidence showing the correlation between cargo rotation and the geometry of underlying microtubule intersections.},
doi = {10.1016/j.bpj.2018.05.010},
journal = {Biophysical Journal},
number = 12,
volume = 114,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.bpj.2018.05.010

Citation Metrics:
Cited by: 1 work
Citation information provided by
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Figures / Tables:

Table 1 Table 1: Variance ($σ$2) of Gaussian peaks fitted from translational and rotational displacement probability distribution functions

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Works referencing / citing this record:

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3D rotational motion of an endocytic vesicle on a complex microtubule network in a living cell
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