Multiple kinesins induce tension for smooth cargo transport

Tjioe, Marco; Vaidya, Rohit; Troitskaia, Alice; Bookwalter, Carol S.; Trybus, Kathleen M.; Chemla, Yann R.; Selvin, Paul R.

doi:10.7554/elife.50974

Cited by 17 publications

(26 citation statements)

References 51 publications

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“…We remark that an asymmetric tug-of-war may even occur in motor interactions of a single type, as recently observed in force-gliding assay experiments of kinesins moving microtubule cargoes in Tjioe et al. ( 2019 ). The analysis proposed here could be applied to models accounting for switching between different behaviors (states) of kinesin motors, such as “driving” kinesins pulling on a microtubule and “resisting” kinesins holding it back (Tjioe et al.…”

Section: Application To Cooperative and Tug-of-war Models Of Cargo Trsupporting

confidence: 77%

“…The run lengths in panels b and d are plotted on a log-log scale to allow for visualization of differences between the models considered. The definitions of effective velocity and run length used are provided in the text of a single type, as recently observed in force-gliding assay experiments of kinesins moving microtubule cargoes in Tjioe et al (2019). The analysis proposed here could be applied to models accounting for switching between different behaviors (states) of kinesin motors, such as "driving" kinesins pulling on a microtubule and "resisting" kinesins holding it back (Tjioe et al 2019).…”

Section: Tug-of-war Models Of Cargo Transportmentioning

confidence: 99%

“…Our primary motivating examples are related to intracellular transport. Some prominent recent investigations include the study of mRNA localization in oocyte development (Zimyanin et al 2008;Trong et al 2015;Ciocanel et al 2017), cell polarization in the budding yeast (Bressloff and Xu 2015), neurofilament transport along axons (Jung and Brown 2009;Li et al 2014), interactions of teams of molecular motor proteins (Klumpp and Lipowsky 2005;Müller et al 2008;Kunwar and Mogilner 2010;Müller et al 2010;Tjioe et al 2019), and sliding of parallel microtubules by teams of cooperative identical motors (Allard et al 2019). Microtubule-based transport of cargo is typically mediated by kinesin motors moving material to the cell periphery and by dynein motors carrying it to the nucleus.…”

Section: Introductionmentioning

confidence: 99%

“… 2010 ; Tjioe et al. 2019 ), and sliding of parallel microtubules by teams of cooperative identical motors (Allard et al. 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Renewal Reward Perspective on Linear Switching Diffusion Systems in Models of Intracellular Transport

et al. 2020

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In many biological systems, the movement of individual agents is characterized having multiple qualitatively distinct behaviors that arise from a variety of biophysical states. For example, in cells the movement of vesicles, organelles, and other intracellular cargo is affected by their binding to and unbinding from cytoskeletal filaments such as microtubules through molecular motor proteins. A typical goal of theoretical or numerical analysis of models of such systems is to investigate effective transport properties and their dependence on model parameters. While the effective velocity of particles undergoing switching diffusion dynamics is often easily characterized in terms of the long-time fraction of time that particles spend in each state, the calculation of the effective diffusivity is more complicated because it cannot be expressed simply in terms of a statistical average of the particle transport state at one moment of time. However, it is common that these systems are regenerative, in the sense that they can be decomposed into independent cycles marked by returns to a base state. Using decompositions of this kind, we calculate effective transport properties by computing the moments of the dynamics within each cycle and then applying renewal reward theory. This method provides a useful alternative large-time analysis to direct homogenization for linear advection–reaction–diffusion partial differential equation models. Moreover, it applies to a general class of semi-Markov processes and certain stochastic differential equations that arise in models of intracellular transport. Applications of the proposed renewal reward framework are illustrated for several case studies such as mRNA transport in developing oocytes and processive cargo movement by teams of molecular motor proteins.

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Section: Application To Cooperative and Tug-of-war Models Of Cargo Trsupporting

confidence: 77%

Section: Tug-of-war Models Of Cargo Transportmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“… 2010 ; Tjioe et al. 2019 ), and sliding of parallel microtubules by teams of cooperative identical motors (Allard et al. 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Renewal Reward Perspective on Linear Switching Diffusion Systems in Models of Intracellular Transport

et al. 2020

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“…We confirmed that tau was also inhibitory to both motors without added salt ( Figure S3B-E, Movie S2), and both K560 and DDR quickly detached when they encountered a tau condensate on the MT (Siahaan et al, 2019)( Figure S3F). We also tested whether multiple motor assemblies walk more successfully on taucoated MTs, as this was shown to be an effective strategy to bypass static obstacles on MTs (Ferro et al, 2019;Tjioe et al, 2019). MT decoration by tau fully inhibited the motility of beads driven by multiple K560 or DDR motors as strongly as it inhibited individual motors ( Figure S4).…”

Section: The Regulatory Role Of a Map Cannot Be Predicted Based On Mtmentioning

confidence: 99%

The mechanism of motor inhibition by microtubule-associated proteins

Ferro

Eshun-Wilson

Golcuk

et al. 2020

Preprint

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Microtubule (MT)-associated proteins (MAPs) regulate intracellular transport by selectively recruiting or excluding kinesin and dynein motors from MTs. We used single-molecule and cryo-electron imaging to determine the mechanism of MAP-motor interactions in vitro. Unexpectedly, we found that the regulatory role of a MAP cannot be predicted based on whether it overlaps with the motor binding site or forms liquid condensates on the MT. Although the MT binding domain (MTBD) of MAP7 overlaps with the kinesin-1 binding site, tethering of kinesin-1 by the MAP7 projection domain supersedes this inhibition and results in biphasic regulation of kinesin-1 motility. Conversely, the MTBD of tau inhibits dynein motility without overlapping with the dynein binding site or by forming tau islands on the MT. Our results indicate that MAPs sort intracellular cargos moving in both directions, as neither dynein nor kinesin can walk on a MAP-coated MT without favorably interacting with that MAP.

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