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Title: Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Journal Article · · Biophysical Journal
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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.

Research Organization:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Organization:
USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
NA0003525; AC04-94AL85000
OSTI ID:
1527036
Alternate ID(s):
OSTI ID: 1466757; OSTI ID: 1495259
Report Number(s):
SAND-2018-8863J; S0006349518305861; PII: S0006349518305861
Journal Information:
Biophysical Journal, Journal Name: Biophysical Journal Vol. 114 Journal Issue: 12; ISSN 0006-3495
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

Cited By (3)

Myosin Va transport of liposomes in three-dimensional actin networks is modulated by actin filament density, position, and polarity journal April 2019
The ability of the kinesin-2 heterodimer KIF3AC to navigate microtubule networks is provided by the KIF3A motor domain journal November 2019
3D rotational motion of an endocytic vesicle on a complex microtubule network in a living cell journal January 2019

Figures / Tables (5)

Table 1(p. 10)table Table 1
Figure 1(p. 16)figure Figure 1
Figure 2(p. 17)figure Figure 2
s) for cargos in dynein-inhibited cells. A total of 800 steps from 14 cargos were analyzed. ($$D$$)$$P$$($Δx$, $Δt$ = 1s) for cargos in microtubule-disrupted cells. A total of 7000 steps from 11 cargos were analyzed. In all plots, solid black lines indicate bimodal Gaussian fitting and dashed lines indicate single Gaussian peak fitting. Single Gaussian peaks with similar variance are shown in the same color." data-ostiid="1527036">
Figure 3(p. 17)figure Figure 3
s) for cargos in dynein-inhibited cells. A total of 800 steps from 14 cargos were analyzed. ($$D$$)$$P$$($Δx$, $Δt$ = 1s) for cargos in microtubule-disrupted cells. A total of 7000 steps from 11 cargos were analyzed. In all plots, solid black lines indicate bimodal Gaussian fitting and dashed lines indicate single Gaussian peak fitting. Single Gaussian peaks with similar variance are shown in the same color." data-ostiid="1527036">
Figure 4(p. 18)figure Figure 4

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