Rotation of endosomes demonstrates coordination of molecular motors during axonal transport

Kaplan, Luke; Ierokomos, Athena; Chowdary, Praveen D.; Bryant, Zev; Cui, Bianxiao

doi:10.1126/sciadv.1602170

Cited by 47 publications

(61 citation statements)

References 42 publications

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“…Instead, it is an active rotation driven by motor proteins as they coordinate to navigate through microtubule intersections. Cargos exhibited increased rotation at pauses in our study, which is different from observations by Kaplan et al that cargo rotation in axons is constrained at pauses (24). This discrepancy is possibly due to the different geometry of microtubules in Vero cells and axons.…”

Section: Discussioncontrasting

confidence: 99%

“…Gu et al showed that cargos rotate in axons because of partial detachment from microtubules (22). Kaplan et al in a very recent study also used gold nanorod probes to demonstrate that cargo rotation in axons increases during transient reversals of transport (24). Our group recently demonstrated that rod-shaped phagosomes rotate both in-plane and longitudinally as they are transported in cells (25).…”

Section: Introductionmentioning

confidence: 94%

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Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Gao

Anthony

et al. 2018

Biophysical Journal

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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.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 94%

Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Gao

Anthony

et al. 2018

Biophysical Journal

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“…Recent measurements observed rotational motion in the trajectories of endosomal cargos carrying gold nanorods. 30 In addition, correlative live-cell and super-resolution microscopy showed that rotational movement could be used by cargos to avoid steric obstacles. 29 These studies proposed that rotational movement and off-axis stepping might result from having a mix of motors, such as kinesin-2 or dynein, on the cargo along with kinesin-1.…”

Section: Discussionmentioning

confidence: 99%

“…It has been proposed that rotation of a cargo around the MT requires the presence of both kinesin and dynein motors on the cargo or the distortion of the lipid cargo. 26,29,30 To test whether a single type of motor can rotate a rigid cargo around the MT, we tracked beads driven by multiple kinesins or dyneins on MT bridges. If the beads were positioned below the MT when they reached the end of the bridge, they were challenged to bypass the PDMS wall ( Fig.…”

Section: Multi-motor Cargos Rotate Around the Mt To Avoid Large Obstamentioning

confidence: 99%

Kinesin-1 and dynein use distinct mechanisms to bypass obstacles

Ferro

Can

Turner

et al. 2019

Preprint

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Kinesin-1 and cytoplasmic dynein are microtubule (MT) motors that transport intracellular cargos. It remains unclear how these motors move along MTs densely coated with obstacles of various sizes in the cytoplasm. Here, we tested the ability of single and multiple motors to bypass synthetic obstacles on MTs in vitro. Contrary to previous reports, we found that mammalian dynein is highly capable of bypassing obstacles. Unlike dynein, single kinesin motors stall in the presence of obstacles, consistent with their inability to take sideways steps to neighboring protofilaments. Kinesins overcome this limitation when working in teams, bypassing obstacles as effectively as multiple dyneins. Cargos driven by multiple kinesin or dyneins are also capable of rotating around the MT to bypass large obstacles. These results suggest that multiplicity of motors is required not only for transporting cargos over long distances and generating higher forces, but also for maneuvering of the cargos on obstacle-coated MT surfaces.

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“…When (47,48). In these GNR-containing early endosomes, the GNR is wrapped tightly by the membrane and show no significant movement relative to the vesicle, which meets the criterion for rotational tracking (16).…”

Section: Resultsmentioning

confidence: 84%

Resolving Cargo-motor-track Interactions in Living Cells with Bifocal Parallax Single Particle Tracking

Cheng

Chen

Dong

et al. 2020

Preprint

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AbstractResolving coordinated biomolecular interactions in living cellular environments is vital for understanding the mechanisms of molecular nanomachines. The conventional approach relies on localizing and tracking target biomolecules and/or subcellular organelles labeled with imaging probes. However, it is challenging to gain information on rotational dynamics, which can be more indicative of the work done by molecular motors and their dynamic binding status. Herein, a bifocal parallax single particle tracking method using half-plane point spread functions has been developed to resolve the full-range azimuth angle (0-360°), polar angle, and 3D displacement in real time under complex living cell conditions. Using this method, quantitative rotational and translational motion of the cargo in a 3D cell cytoskeleton was obtained. Not only well-known active intracellular transport and free diffusion were observed but new interactions, tight attachment and tethered rotation, were discovered for better interpretation of the dynamics of cargo-motor-track interactions at various types of microtubule intersections.Significance StatementTranslation and rotational motion of cargo during pauses at the microtubule intersections in living cells were revealed by high-accuracy three-dimensional single particle rotational tracking. The current study demonstrates the potential of studying coordinated interactions in living cellular environments by resolving characteristic rotational motions.

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Rotation of endosomes demonstrates coordination of molecular motors during axonal transport

Abstract: Multipolarization microscopy shows tight linkage of the rotational dynamics of axonal endosomes to molecular motor activity.

Cited by 47 publications

References 42 publications

Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Cargos Rotate at Microtubule Intersections during Intracellular Trafficking

Kinesin-1 and dynein use distinct mechanisms to bypass obstacles

Resolving Cargo-motor-track Interactions in Living Cells with Bifocal Parallax Single Particle Tracking

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