Collective force generated by multiple biofilaments can exceed the sum of forces due to individual ones

Das, Debapratim; Das, Dibyendu; Padinhateeri, Ranjith

doi:10.1088/1367-2630/16/6/063032

Cited by 25 publications

(52 citation statements)

References 38 publications

(179 reference statements)

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“…6). With this understanding of the connection between the non-equilibrium dynamics and non-additivity of stall forces, we study another model for filaments [31] in the next section, and show that the same ideas can be carried forward.…”

Section: B a Generalized Random Hydrolysis Model For Filamentsmentioning

confidence: 95%

“…[26,28,31,50,80,81]. Similar to the filaments, motors also work against load and have been modelled in several studies [32-34, 75, 76].…”

Section: Collective Stall Force For Multiple Cytoskeletal Filamenmentioning

confidence: 99%

“…Here, we focus on the simplified model of this process as discussed in Refs. [31,90], where we neglect complexities related to biofilaments such as structural details, mechanical flexibility, possible interplay between mechanical forces and hydrolysis events and the possible multi-stage nature of the hydrolysis process [17,85,88,93,94]. As shown in Fig.…”

Section: A a Random Hydrolysis Model For Cytoskeletal Filamentsmentioning

confidence: 99%

“…On the theoretical and computational front, there are a number of very detailed models for understanding the force-velocity dynamics of a single biofilament [50][51][52][53], as well as a few that try to model the dynamics of multiple biofilaments [26,[28][29][30][31][54][55][56]. Some of these theoretical studies have demonstrated that the stall force of multiple, non-interacting filaments without ATP/GTP dynamics, scales linearly with the number of filaments [26,[28][29][30]54].…”

Section: Introductionmentioning

confidence: 99%

“…Some of these theoretical studies have demonstrated that the stall force of multiple, non-interacting filaments without ATP/GTP dynamics, scales linearly with the number of filaments [26,[28][29][30]54]. In contrast, a few other recent papers quite clearly report that inclusion of ATP/GTP hydrolysis can lead to either enhanced or reduced cooperativity in the maximum force generated by multiple growing filaments; the stall forces need not always scale with the number of filaments [31,[56][57][58]. In other words, the stall forces of individual filaments are non-additive in general, that is, the collective stall force produced by N number of filaments (denoted by f (N ) s ) is not just a simple sum of individual stall forces of single filaments (i.e., f (N )…”

Section: Introductionmentioning

confidence: 99%

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Sufficient conditions for the additivity of stall forces generated by multiple filaments or motors

Bameta

Das

et al. 2017

Phys. Rev. E

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Molecular motors and cytoskeletal filaments work collectively most of the time under opposing forces. This opposing force may be due to cargo carried by motors or resistance coming from the cell membrane pressing against the cytoskeletal filaments. Some recent studies have shown that the collective maximum force (stall force) generated by multiple cytoskeletal filaments or molecular motors may not always be just a simple sum of the stall forces of the individual filaments or motors. To understand this excess or deficit in the collective force, we study a broad class of models of both cytoskeletal filaments and molecular motors. We argue that the stall force generated by a group of filaments or motors is additive, that is, the stall force of N number of filaments (motors) is N times the stall force of one filament (motor), when the system is in equilibrium at stall. Conversely, we show that this additive property typically does not hold true when the system is not at equilibrium at stall. We thus present a novel and unified understanding of the existing models exhibiting such nonaddivity, and generalise our arguments by developing new models that demonstrate this phenomena. We also propose a quantity similar to thermodynamic efficiency to easily predict this deviation from stall-force additivity for filament and motor collectives.

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Section: B a Generalized Random Hydrolysis Model For Filamentsmentioning

confidence: 95%

“…[26,28,31,50,80,81]. Similar to the filaments, motors also work against load and have been modelled in several studies [32-34, 75, 76].…”

Section: Collective Stall Force For Multiple Cytoskeletal Filamenmentioning

confidence: 99%

Section: A a Random Hydrolysis Model For Cytoskeletal Filamentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Sufficient conditions for the additivity of stall forces generated by multiple filaments or motors

Bameta

Das

et al. 2017

Phys. Rev. E

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Collective dynein transport of the nucleus by pulling on astral microtubules during Saccharomyces cerevisiae mitosis

Jain

Khetan

Yadav

et al. 2021

Yeast

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Positioning the nucleus at the bud neck during Saccharomyces cerevisiae mitosis involves pulling forces of cytoplasmic dynein localized in the daughter cell. Although genetic analysis has revealed a complex network positioning the nucleus, quantification of the forces acting on the nucleus and the number of dyneins driving the process has remained difficult. To better understand the collective forces involved in nuclear positioning, we compare a model of dyneins-driven microtubule (MT) pulling, MT pushing, and cytoplasmic drag to experiments. During S. cerevisiae mitosis, MTs interacting with the cortex nucleated by the daughter spindle pole body (SPB) (SPB-D) are longer than the mother SPB (SPB-M), increasing further during spindle elongation in anaphase. Interphasic SPB mobility is effectively diffusive, while the mitotic mobility is directed. By optimizing a computational model of the mobility of the nucleus due to diffusion and MTs pushing at the cell membrane to experiment, we estimate the viscosity governing the drag force on nuclei during positioning. A force balance model of mitotic SPB mobility compared to experimental mobility suggests that even one or two dynein dimers are sufficient to move the nucleus in the bud neck. Using stochastic computer simulations of a budding cell, we find that punctate dynein localization can generate sufficient force to reel in the nucleus to the bud neck. Compared to uniform motor localization, puncta involve fewer motors suggesting a functional role for motor clustering. Stochastic simulations also suggest that a higher number of force generators than predicted by force balance may be required to ensure the robustness of spindle positioning. Take Away• Saccharomyces cerevisiaea cytoplasmic viscosity is estimated by quantifying the in vivo mobility of the nucleus and comparing to simulations.• The in vivo length dynamics of microtubules (MTs) interacting with daughter bud cortex during nuclear positioning in mitosis are measured.• We developed a model of astral MT interactions with cortical dynein in the process of nuclear positioning during mitosis.• A force balance model predicts the minimal force required for nuclear positioning. Kunalika Jain and Neha Khetan contributed equally to the manuscript.

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Effects of length-dependent positive feedback on length distributions of microtubules undergoing hydrolysis

2022

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Collective force generated by multiple biofilaments can exceed the sum of forces due to individual ones

Cited by 25 publications

References 38 publications

Sufficient conditions for the additivity of stall forces generated by multiple filaments or motors

Sufficient conditions for the additivity of stall forces generated by multiple filaments or motors

Collective dynein transport of the nucleus by pulling on astral microtubules during Saccharomyces cerevisiae mitosis

Effects of length-dependent positive feedback on length distributions of microtubules undergoing hydrolysis

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