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. doi: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 = {Fri Jun 01 00:00:00 EDT 2018},
month = {Fri Jun 01 00:00:00 EDT 2018}
}
https://doi.org/10.1016/j.bpj.2018.05.010
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Figures / Tables:
Table 1: Variance ($σ$2) of Gaussian peaks fitted from translational and rotational displacement probability distribution functions
Works referencing / citing this record:
Myosin Va transport of liposomes in three-dimensional actin networks is modulated by actin filament density, position, and polarity
journal, April 2019
- Lombardo, Andrew T.; Nelson, Shane R.; Kennedy, Guy G.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
The ability of the kinesin-2 heterodimer KIF3AC to navigate microtubule networks is provided by the KIF3A motor domain
journal, November 2019
- Deeb, Stephanie K.; Guzik-Lendrum, Stephanie; Jeffrey, Jasper D.
- Journal of Biological Chemistry, Vol. 294, Issue 52
3D rotational motion of an endocytic vesicle on a complex microtubule network in a living cell
journal, January 2019
- Lee, Seohyun; Higuchi, Hideo
- Biomedical Optics Express, Vol. 10, Issue 12
Figures / Tables found in this record: