Lamellipodial Actin Mechanically Links Myosin Activity with Adhesion-Site Formation

Grégory Giannone, Benjamin J. Dubin-Thaler, Olivier Rossier, Yunfei Cai, Oleg Chaga, Guoying Jiang, William Beaver, Hans Günther Döbereiner, Yoav Freund, Gary Borisy, Michael Sheetz

Research output: Contribution to journalArticle

343 Scopus citations

Abstract

Cell motility proceeds by cycles of edge protrusion, adhesion, and retraction. Whether these functions are coordinated by biochemical or biomechanical processes is unknown. We find that myosin II pulls the rear of the lamellipodial actin network, causing upward bending, edge retraction, and initiation of new adhesion sites. The network then separates from the edge and condenses over the myosin. Protrusion resumes as lamellipodial actin regenerates from the front and extends rearward until it reaches newly assembled myosin, initiating the next cycle. Upward bending, observed by evanescence and electron microscopy, results in ruffle formation when adhesion strength is low. Correlative fluorescence and electron microscopy shows that the regenerating lamellipodium forms a cohesive, separable layer of actin above the lamellum. Thus, actin polymerization periodically builds a mechanical link, the lamellipodium, connecting myosin motors with the initiation of adhesion sites, suggesting that the major functions driving motility are coordinated by a biomechanical process.

Original languageEnglish (US)
Pages (from-to)561-575
Number of pages15
JournalCell
Volume128
Issue number3
DOIs
StatePublished - Feb 9 2007
Externally publishedYes

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

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    Giannone, G., Dubin-Thaler, B. J., Rossier, O., Cai, Y., Chaga, O., Jiang, G., Beaver, W., Döbereiner, H. G., Freund, Y., Borisy, G., & Sheetz, M. (2007). Lamellipodial Actin Mechanically Links Myosin Activity with Adhesion-Site Formation. Cell, 128(3), 561-575. https://doi.org/10.1016/j.cell.2006.12.039