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Active contraction of microtubule networks.

Foster PJ, F├╝rthauer S, Shelley MJ, Needleman DJ - Elife (2015)

Bottom Line: It remains unclear how cytoskeletal filaments and motor proteins organize into cellular scale structures and how molecular properties of cytoskeletal components affect the large-scale behaviors of these systems.Here, we investigate the self-organization of stabilized microtubules in Xenopus oocyte extracts and find that they can form macroscopic networks that spontaneously contract.These results demonstrate that the motor-driven clustering of filament ends is a generic mechanism leading to contraction.

View Article: PubMed Central - PubMed

Affiliation: John A. Paulson School of Engineering and Applied Sciences, FAS Center for Systems Biology, Harvard University, Cambridge, United States.

ABSTRACT
Many cellular processes are driven by cytoskeletal assemblies. It remains unclear how cytoskeletal filaments and motor proteins organize into cellular scale structures and how molecular properties of cytoskeletal components affect the large-scale behaviors of these systems. Here, we investigate the self-organization of stabilized microtubules in Xenopus oocyte extracts and find that they can form macroscopic networks that spontaneously contract. We propose that these contractions are driven by the clustering of microtubule minus ends by dynein. Based on this idea, we construct an active fluid theory of network contractions, which predicts a dependence of the timescale of contraction on initial network geometry, a development of density inhomogeneities during contraction, a constant final network density, and a strong influence of dynein inhibition on the rate of contraction, all in quantitative agreement with experiments. These results demonstrate that the motor-driven clustering of filament ends is a generic mechanism leading to contraction.

No MeSH data available.


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Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.(A) Microtubule sliding by dynein drives microtubule minus ends together. (B) Minus end clustering leads to the formation of aster-like structures. Due to steric interactions between microtubules, there is an upper limit to the local microtubule density. (C) The microtubule network is composed of interacting asters. Motor activity driving aster cores together leads to bulk contraction of the network.DOI:http://dx.doi.org/10.7554/eLife.10837.012
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fig4: Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.(A) Microtubule sliding by dynein drives microtubule minus ends together. (B) Minus end clustering leads to the formation of aster-like structures. Due to steric interactions between microtubules, there is an upper limit to the local microtubule density. (C) The microtubule network is composed of interacting asters. Motor activity driving aster cores together leads to bulk contraction of the network.DOI:http://dx.doi.org/10.7554/eLife.10837.012

Mentions: We obtain an expression for the active stress, , by considering the microscopic behaviors of microtubules and motor proteins. As the contracting networks consist of microtubule asters (Figure 1D, E), and microtubule asters in meiotic extracts are thought to assemble by the dynein-induced clustering of microtubule minus ends (Verde et al., 1991), we hypothesize that the contraction process is also driven by dynein pulling microtubule minus ends towards each other (Figure 4A).10.7554/eLife.10837.012Figure 4.Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.


Active contraction of microtubule networks.

Foster PJ, F├╝rthauer S, Shelley MJ, Needleman DJ - Elife (2015)

Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.(A) Microtubule sliding by dynein drives microtubule minus ends together. (B) Minus end clustering leads to the formation of aster-like structures. Due to steric interactions between microtubules, there is an upper limit to the local microtubule density. (C) The microtubule network is composed of interacting asters. Motor activity driving aster cores together leads to bulk contraction of the network.DOI:http://dx.doi.org/10.7554/eLife.10837.012
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4764591&req=5

fig4: Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.(A) Microtubule sliding by dynein drives microtubule minus ends together. (B) Minus end clustering leads to the formation of aster-like structures. Due to steric interactions between microtubules, there is an upper limit to the local microtubule density. (C) The microtubule network is composed of interacting asters. Motor activity driving aster cores together leads to bulk contraction of the network.DOI:http://dx.doi.org/10.7554/eLife.10837.012
Mentions: We obtain an expression for the active stress, , by considering the microscopic behaviors of microtubules and motor proteins. As the contracting networks consist of microtubule asters (Figure 1D, E), and microtubule asters in meiotic extracts are thought to assemble by the dynein-induced clustering of microtubule minus ends (Verde et al., 1991), we hypothesize that the contraction process is also driven by dynein pulling microtubule minus ends towards each other (Figure 4A).10.7554/eLife.10837.012Figure 4.Cartoon of the microscopic model underlying the active fluid theory of network contractions by minus end clustering.

Bottom Line: It remains unclear how cytoskeletal filaments and motor proteins organize into cellular scale structures and how molecular properties of cytoskeletal components affect the large-scale behaviors of these systems.Here, we investigate the self-organization of stabilized microtubules in Xenopus oocyte extracts and find that they can form macroscopic networks that spontaneously contract.These results demonstrate that the motor-driven clustering of filament ends is a generic mechanism leading to contraction.

View Article: PubMed Central - PubMed

Affiliation: John A. Paulson School of Engineering and Applied Sciences, FAS Center for Systems Biology, Harvard University, Cambridge, United States.

ABSTRACT
Many cellular processes are driven by cytoskeletal assemblies. It remains unclear how cytoskeletal filaments and motor proteins organize into cellular scale structures and how molecular properties of cytoskeletal components affect the large-scale behaviors of these systems. Here, we investigate the self-organization of stabilized microtubules in Xenopus oocyte extracts and find that they can form macroscopic networks that spontaneously contract. We propose that these contractions are driven by the clustering of microtubule minus ends by dynein. Based on this idea, we construct an active fluid theory of network contractions, which predicts a dependence of the timescale of contraction on initial network geometry, a development of density inhomogeneities during contraction, a constant final network density, and a strong influence of dynein inhibition on the rate of contraction, all in quantitative agreement with experiments. These results demonstrate that the motor-driven clustering of filament ends is a generic mechanism leading to contraction.

No MeSH data available.


Related in: MedlinePlus