Cytoskeletal coherence requires myosin-IIA contractility

Yunfei Cai, Olivier Rossier, Nils C. Gauthier, Nicolas Biais, Marc Antoine Fardin, Xian Zhang, Lawrence W. Miller, Benoit Ladoux, Virginia W. Cornish, Michael Sheetz

Research output: Contribution to journalArticle

132 Citations (Scopus)

Abstract

Maintaining a physical connection across cytoplasm is crucial for many biological processes such as matrix force generation, cell motility, cell shape and tissue development. However, in the absence of stress fibers, the coherent structure that transmits force across the cytoplasm is not understood. We find that nonmuscle myosin-II (NMII) contraction of cytoplasmic actin filaments establishes a coherent cytoskeletal network irrespective of the nature of adhesive contacts. When NMII activity is inhibited during cell spreading by Rho kinase inhibition, blebbistatin, caldesmon overexpression or NMIIA RNAi, the symmetric traction forces are lost and cell spreading persists, causing cytoplasm fragmentation by membrane tension that results in 'C' or dendritic shapes. Moreover, local inactivation of NMII by chromophore-assisted laser inactivation causes local loss of coherence. Actin filament polymerization is also required for cytoplasmic coherence, but microtubules and intermediate filaments are dispensable. Loss of cytoplasmic coherence is accompanied by loss of circumferential actin bundles. We suggest that NMIIA creates a coherent actin network through the formation of circumferential actin bundles that mechanically link elements of the peripheral actin cytoskeleton where much of the force is generated during spreading.

Original languageEnglish (US)
Pages (from-to)413-423
Number of pages11
JournalJournal of Cell Science
Volume123
Issue number3
DOIs
StatePublished - Feb 1 2010
Externally publishedYes

Fingerprint

Nonmuscle Myosin Type IIA
Myosin Type II
Actin Cytoskeleton
Actins
Cytoplasm
Cytoskeleton
Chromophore-Assisted Light Inactivation
Calmodulin-Binding Proteins
Biological Phenomena
rho-Associated Kinases
Stress Fibers
Intermediate Filaments
Cell Shape
Traction
RNA Interference
Microtubules
Polymerization
Adhesives
Cell Movement
Membranes

Keywords

  • Actin
  • Cell spreading
  • Coherence
  • Fibroblast
  • Myosin-II
  • Traction force

ASJC Scopus subject areas

  • Cell Biology

Cite this

Cai, Y., Rossier, O., Gauthier, N. C., Biais, N., Fardin, M. A., Zhang, X., ... Sheetz, M. (2010). Cytoskeletal coherence requires myosin-IIA contractility. Journal of Cell Science, 123(3), 413-423. https://doi.org/10.1242/jcs.058297

Cytoskeletal coherence requires myosin-IIA contractility. / Cai, Yunfei; Rossier, Olivier; Gauthier, Nils C.; Biais, Nicolas; Fardin, Marc Antoine; Zhang, Xian; Miller, Lawrence W.; Ladoux, Benoit; Cornish, Virginia W.; Sheetz, Michael.

In: Journal of Cell Science, Vol. 123, No. 3, 01.02.2010, p. 413-423.

Research output: Contribution to journalArticle

Cai, Y, Rossier, O, Gauthier, NC, Biais, N, Fardin, MA, Zhang, X, Miller, LW, Ladoux, B, Cornish, VW & Sheetz, M 2010, 'Cytoskeletal coherence requires myosin-IIA contractility', Journal of Cell Science, vol. 123, no. 3, pp. 413-423. https://doi.org/10.1242/jcs.058297
Cai Y, Rossier O, Gauthier NC, Biais N, Fardin MA, Zhang X et al. Cytoskeletal coherence requires myosin-IIA contractility. Journal of Cell Science. 2010 Feb 1;123(3):413-423. https://doi.org/10.1242/jcs.058297
Cai, Yunfei ; Rossier, Olivier ; Gauthier, Nils C. ; Biais, Nicolas ; Fardin, Marc Antoine ; Zhang, Xian ; Miller, Lawrence W. ; Ladoux, Benoit ; Cornish, Virginia W. ; Sheetz, Michael. / Cytoskeletal coherence requires myosin-IIA contractility. In: Journal of Cell Science. 2010 ; Vol. 123, No. 3. pp. 413-423.
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