Myosin II contributes to cell-scale actin network treadmilling through network disassembly

Cyrus A. Wilson, Mark A. Tsuchida, Greg M. Allen, Erin L. Barnhart, Kathryn T. Applegate, Patricia T. Yam, Lin Ji, Kinneret Keren, Gaudenz Danuser, Julie A. Theriot

Research output: Contribution to journalArticle

234 Citations (Scopus)

Abstract

Crawling locomotion of eukaryotic cells is achieved by a process dependent on the actin cytoskeleton: protrusion of the leading edge requires assembly of a network of actin filaments, which must be disassembled at the cell rear for sustained motility. Although ADF/cofilin proteins have been shown to contribute to actin disassembly, it is not clear how activity of these locally acting proteins could be coordinated over the distance scale of the whole cell. Here we show that non-muscle myosin II has a direct role in actin network disassembly in crawling cells. In fish keratocytes undergoing motility, myosin II is concentrated in regions at the rear with high rates of network disassembly. Activation of myosin II by ATP in detergent-extracted cytoskeletons results in rear-localized disassembly of the actin network. Inhibition of myosin II activity and stabilization of actin filaments synergistically impede cell motility, suggesting the existence of two disassembly pathways, one of which requires myosin II activity. Our results establish the importance of myosin II as an enzyme for actin network disassembly; we propose that gradual formation and reorganization of an actomyosin network provides an intrinsic destruction timer, enabling long-range coordination of actin network treadmilling in motile cells.

Original languageEnglish (US)
Pages (from-to)373-377
Number of pages5
JournalNature
Volume465
Issue number7296
DOIs
StatePublished - May 20 2010

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Myosin Type II
Actins
Actin Cytoskeleton
Actin Depolymerizing Factors
Actomyosin
Eukaryotic Cells
Locomotion
Cytoskeleton
Detergents
Cell Movement
Fishes
Adenosine Triphosphate
Enzymes

ASJC Scopus subject areas

  • General

Cite this

Wilson, C. A., Tsuchida, M. A., Allen, G. M., Barnhart, E. L., Applegate, K. T., Yam, P. T., ... Theriot, J. A. (2010). Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature, 465(7296), 373-377. https://doi.org/10.1038/nature08994

Myosin II contributes to cell-scale actin network treadmilling through network disassembly. / Wilson, Cyrus A.; Tsuchida, Mark A.; Allen, Greg M.; Barnhart, Erin L.; Applegate, Kathryn T.; Yam, Patricia T.; Ji, Lin; Keren, Kinneret; Danuser, Gaudenz; Theriot, Julie A.

In: Nature, Vol. 465, No. 7296, 20.05.2010, p. 373-377.

Research output: Contribution to journalArticle

Wilson, CA, Tsuchida, MA, Allen, GM, Barnhart, EL, Applegate, KT, Yam, PT, Ji, L, Keren, K, Danuser, G & Theriot, JA 2010, 'Myosin II contributes to cell-scale actin network treadmilling through network disassembly', Nature, vol. 465, no. 7296, pp. 373-377. https://doi.org/10.1038/nature08994
Wilson CA, Tsuchida MA, Allen GM, Barnhart EL, Applegate KT, Yam PT et al. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature. 2010 May 20;465(7296):373-377. https://doi.org/10.1038/nature08994
Wilson, Cyrus A. ; Tsuchida, Mark A. ; Allen, Greg M. ; Barnhart, Erin L. ; Applegate, Kathryn T. ; Yam, Patricia T. ; Ji, Lin ; Keren, Kinneret ; Danuser, Gaudenz ; Theriot, Julie A. / Myosin II contributes to cell-scale actin network treadmilling through network disassembly. In: Nature. 2010 ; Vol. 465, No. 7296. pp. 373-377.
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