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Force-induced dynamical properties of multiple cytoskeletal filaments are distinct from that of single filaments.

Das D, Das D, Padinhateeri R - PLoS ONE (2014)

Bottom Line: Comparing stochastic simulation results with recent experimental data, we show that multi-filament collective catastrophes are slower than catastrophes of single filaments.We build a unified picture by establishing interconnections among all these collective phenomena.Additionally, we show that the collapse times during catastrophes can be sharp indicators of collective stall forces exceeding the additive contributions of single filaments.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Indian Institute of Technology Bombay, Mumbai 400076, India.

ABSTRACT
How cytoskeletal filaments collectively undergo growth and shrinkage is an intriguing question. Collective properties of multiple bio-filaments (actin or microtubules) undergoing hydrolysis have not been studied extensively earlier within simple theoretical frameworks. In this paper, we study the collective dynamical properties of multiple filaments under force, and demonstrate the distinct properties of a multi-filament system in comparison to a single filament. Comparing stochastic simulation results with recent experimental data, we show that multi-filament collective catastrophes are slower than catastrophes of single filaments. Our study also shows further distinctions as follows: (i) force-dependence of the cap-size distribution of multiple filaments are quantitatively different from that of single filaments, (ii) the diffusion constant associated with the system length fluctuations is distinct for multiple filaments, and (iii) switching dynamics of multiple filaments between capped and uncapped states and the fluctuations therein are also distinct. We build a unified picture by establishing interconnections among all these collective phenomena. Additionally, we show that the collapse times during catastrophes can be sharp indicators of collective stall forces exceeding the additive contributions of single filaments.

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Average cap size  as a function of  for (a) actin filaments and (b) microtubules, and for filament numbers  (red),  (green) and  (blue).The concentrations are  for actin, and  for microtubule. Y-axes are in log scale. Note that the single filament stall forces are 0.68 pN for actin and 0.97 pN for microtubule.
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pone-0114014-g006: Average cap size as a function of for (a) actin filaments and (b) microtubules, and for filament numbers (red), (green) and (blue).The concentrations are for actin, and for microtubule. Y-axes are in log scale. Note that the single filament stall forces are 0.68 pN for actin and 0.97 pN for microtubule.

Mentions: In Fig. 6, we plot against the scaled force , for actin filaments (Fig. 6a) and microtubules (Fig. 6b). Note that this figure is the counterpart of Fig. 5, that was studied for short filaments with possible boundary effects (see previous section). In Fig. 6, when , we see that mean cap-length , for single filament, rapidly decays to zero (see red curves in Fig. 6). There is a distinction between actin versus microtubule though – the force range over which cap is present is larger for microtubule than actin. However for , does not vanish at all — rather, it first reduces and then saturates (or stabilizes) to a finite value of subunits, at forces (see green curves for , and blue curves for in Fig. 6). These results reaffirm our observation in the last section that the multifilament system does show a distinct cap structure – while average cap length of a single filament is vanishingly small, the multifilament system always has a non-vanishing larger cap. Does this also reflect in the full cap size distribution?


Force-induced dynamical properties of multiple cytoskeletal filaments are distinct from that of single filaments.

Das D, Das D, Padinhateeri R - PLoS ONE (2014)

Average cap size  as a function of  for (a) actin filaments and (b) microtubules, and for filament numbers  (red),  (green) and  (blue).The concentrations are  for actin, and  for microtubule. Y-axes are in log scale. Note that the single filament stall forces are 0.68 pN for actin and 0.97 pN for microtubule.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4273989&req=5

pone-0114014-g006: Average cap size as a function of for (a) actin filaments and (b) microtubules, and for filament numbers (red), (green) and (blue).The concentrations are for actin, and for microtubule. Y-axes are in log scale. Note that the single filament stall forces are 0.68 pN for actin and 0.97 pN for microtubule.
Mentions: In Fig. 6, we plot against the scaled force , for actin filaments (Fig. 6a) and microtubules (Fig. 6b). Note that this figure is the counterpart of Fig. 5, that was studied for short filaments with possible boundary effects (see previous section). In Fig. 6, when , we see that mean cap-length , for single filament, rapidly decays to zero (see red curves in Fig. 6). There is a distinction between actin versus microtubule though – the force range over which cap is present is larger for microtubule than actin. However for , does not vanish at all — rather, it first reduces and then saturates (or stabilizes) to a finite value of subunits, at forces (see green curves for , and blue curves for in Fig. 6). These results reaffirm our observation in the last section that the multifilament system does show a distinct cap structure – while average cap length of a single filament is vanishingly small, the multifilament system always has a non-vanishing larger cap. Does this also reflect in the full cap size distribution?

Bottom Line: Comparing stochastic simulation results with recent experimental data, we show that multi-filament collective catastrophes are slower than catastrophes of single filaments.We build a unified picture by establishing interconnections among all these collective phenomena.Additionally, we show that the collapse times during catastrophes can be sharp indicators of collective stall forces exceeding the additive contributions of single filaments.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Indian Institute of Technology Bombay, Mumbai 400076, India.

ABSTRACT
How cytoskeletal filaments collectively undergo growth and shrinkage is an intriguing question. Collective properties of multiple bio-filaments (actin or microtubules) undergoing hydrolysis have not been studied extensively earlier within simple theoretical frameworks. In this paper, we study the collective dynamical properties of multiple filaments under force, and demonstrate the distinct properties of a multi-filament system in comparison to a single filament. Comparing stochastic simulation results with recent experimental data, we show that multi-filament collective catastrophes are slower than catastrophes of single filaments. Our study also shows further distinctions as follows: (i) force-dependence of the cap-size distribution of multiple filaments are quantitatively different from that of single filaments, (ii) the diffusion constant associated with the system length fluctuations is distinct for multiple filaments, and (iii) switching dynamics of multiple filaments between capped and uncapped states and the fluctuations therein are also distinct. We build a unified picture by establishing interconnections among all these collective phenomena. Additionally, we show that the collapse times during catastrophes can be sharp indicators of collective stall forces exceeding the additive contributions of single filaments.

Show MeSH
Related in: MedlinePlus