Force generated by actomyosin contraction builds bridges between adhesive contacts

Olivier M. Rossier, Nils Gauthier, Nicolas Biais, Wynn Vonnegut, Marc Antoine Fardin, Philip Avigan, Evan R. Heller, Anurag Mathur, Saba Ghassemi, Michael S. Koeckert, James C. Hone, Michael Sheetz

Research output: Contribution to journalArticle

76 Citations (Scopus)

Abstract

Extracellular matrices in vivo are heterogeneous structures containing gaps that cells bridge with an actomyosin network. To understand the basis of bridging, we plated cells on surfaces patterned with fibronectin (FN)-coated stripes separated by non-adhesive regions. Bridges developed large tensions where concave cell edges were anchored to FN by adhesion sites. Actomyosin complexes assembled near those sites (both actin and myosin filaments) and moved towards the centre of the non-adhesive regions in a treadmilling network. Inhibition of myosin-II (MII) or Rho-kinase collapsed bridges, whereas extension continued over adhesive areas. Inhibition of actin polymerization (latrunculin-A, jasplakinolide) also collapsed the actomyosin network. We suggest that MII has distinct functions at different bridge regions: (1) at the concave edges of bridges, MIIA force stimulates actin filament assembly at adhesions and (2) in the body of bridges, myosin cross-links actin filaments and stimulates actomyosin network healing when breaks occur. Both activities ensure turnover of actin networks needed to maintain stable bridges from one adhesive region to another.

Original languageEnglish (US)
Pages (from-to)1055-1068
Number of pages14
JournalEMBO Journal
Volume29
Issue number6
DOIs
StatePublished - Mar 1 2010
Externally publishedYes

Fingerprint

Actomyosin
Adhesives
Actin Cytoskeleton
Myosin Type II
Actins
jasplakinolide
Myosins
Fibronectins
rho-Associated Kinases
Polymerization
Adhesion
Extracellular Matrix

Keywords

  • Actomyosin dynamics
  • Adhesion
  • Contractile treadmilling
  • Latrunculin
  • Patterned surfaces

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

Rossier, O. M., Gauthier, N., Biais, N., Vonnegut, W., Fardin, M. A., Avigan, P., ... Sheetz, M. (2010). Force generated by actomyosin contraction builds bridges between adhesive contacts. EMBO Journal, 29(6), 1055-1068. https://doi.org/10.1038/emboj.2010.2

Force generated by actomyosin contraction builds bridges between adhesive contacts. / Rossier, Olivier M.; Gauthier, Nils; Biais, Nicolas; Vonnegut, Wynn; Fardin, Marc Antoine; Avigan, Philip; Heller, Evan R.; Mathur, Anurag; Ghassemi, Saba; Koeckert, Michael S.; Hone, James C.; Sheetz, Michael.

In: EMBO Journal, Vol. 29, No. 6, 01.03.2010, p. 1055-1068.

Research output: Contribution to journalArticle

Rossier, OM, Gauthier, N, Biais, N, Vonnegut, W, Fardin, MA, Avigan, P, Heller, ER, Mathur, A, Ghassemi, S, Koeckert, MS, Hone, JC & Sheetz, M 2010, 'Force generated by actomyosin contraction builds bridges between adhesive contacts', EMBO Journal, vol. 29, no. 6, pp. 1055-1068. https://doi.org/10.1038/emboj.2010.2
Rossier OM, Gauthier N, Biais N, Vonnegut W, Fardin MA, Avigan P et al. Force generated by actomyosin contraction builds bridges between adhesive contacts. EMBO Journal. 2010 Mar 1;29(6):1055-1068. https://doi.org/10.1038/emboj.2010.2
Rossier, Olivier M. ; Gauthier, Nils ; Biais, Nicolas ; Vonnegut, Wynn ; Fardin, Marc Antoine ; Avigan, Philip ; Heller, Evan R. ; Mathur, Anurag ; Ghassemi, Saba ; Koeckert, Michael S. ; Hone, James C. ; Sheetz, Michael. / Force generated by actomyosin contraction builds bridges between adhesive contacts. In: EMBO Journal. 2010 ; Vol. 29, No. 6. pp. 1055-1068.
@article{7e6c306550f34ee99510595ad022ba36,
title = "Force generated by actomyosin contraction builds bridges between adhesive contacts",
abstract = "Extracellular matrices in vivo are heterogeneous structures containing gaps that cells bridge with an actomyosin network. To understand the basis of bridging, we plated cells on surfaces patterned with fibronectin (FN)-coated stripes separated by non-adhesive regions. Bridges developed large tensions where concave cell edges were anchored to FN by adhesion sites. Actomyosin complexes assembled near those sites (both actin and myosin filaments) and moved towards the centre of the non-adhesive regions in a treadmilling network. Inhibition of myosin-II (MII) or Rho-kinase collapsed bridges, whereas extension continued over adhesive areas. Inhibition of actin polymerization (latrunculin-A, jasplakinolide) also collapsed the actomyosin network. We suggest that MII has distinct functions at different bridge regions: (1) at the concave edges of bridges, MIIA force stimulates actin filament assembly at adhesions and (2) in the body of bridges, myosin cross-links actin filaments and stimulates actomyosin network healing when breaks occur. Both activities ensure turnover of actin networks needed to maintain stable bridges from one adhesive region to another.",
keywords = "Actomyosin dynamics, Adhesion, Contractile treadmilling, Latrunculin, Patterned surfaces",
author = "Rossier, {Olivier M.} and Nils Gauthier and Nicolas Biais and Wynn Vonnegut and Fardin, {Marc Antoine} and Philip Avigan and Heller, {Evan R.} and Anurag Mathur and Saba Ghassemi and Koeckert, {Michael S.} and Hone, {James C.} and Michael Sheetz",
year = "2010",
month = "3",
day = "1",
doi = "10.1038/emboj.2010.2",
language = "English (US)",
volume = "29",
pages = "1055--1068",
journal = "EMBO Journal",
issn = "0261-4189",
publisher = "Nature Publishing Group",
number = "6",

}

TY - JOUR

T1 - Force generated by actomyosin contraction builds bridges between adhesive contacts

AU - Rossier, Olivier M.

AU - Gauthier, Nils

AU - Biais, Nicolas

AU - Vonnegut, Wynn

AU - Fardin, Marc Antoine

AU - Avigan, Philip

AU - Heller, Evan R.

AU - Mathur, Anurag

AU - Ghassemi, Saba

AU - Koeckert, Michael S.

AU - Hone, James C.

AU - Sheetz, Michael

PY - 2010/3/1

Y1 - 2010/3/1

N2 - Extracellular matrices in vivo are heterogeneous structures containing gaps that cells bridge with an actomyosin network. To understand the basis of bridging, we plated cells on surfaces patterned with fibronectin (FN)-coated stripes separated by non-adhesive regions. Bridges developed large tensions where concave cell edges were anchored to FN by adhesion sites. Actomyosin complexes assembled near those sites (both actin and myosin filaments) and moved towards the centre of the non-adhesive regions in a treadmilling network. Inhibition of myosin-II (MII) or Rho-kinase collapsed bridges, whereas extension continued over adhesive areas. Inhibition of actin polymerization (latrunculin-A, jasplakinolide) also collapsed the actomyosin network. We suggest that MII has distinct functions at different bridge regions: (1) at the concave edges of bridges, MIIA force stimulates actin filament assembly at adhesions and (2) in the body of bridges, myosin cross-links actin filaments and stimulates actomyosin network healing when breaks occur. Both activities ensure turnover of actin networks needed to maintain stable bridges from one adhesive region to another.

AB - Extracellular matrices in vivo are heterogeneous structures containing gaps that cells bridge with an actomyosin network. To understand the basis of bridging, we plated cells on surfaces patterned with fibronectin (FN)-coated stripes separated by non-adhesive regions. Bridges developed large tensions where concave cell edges were anchored to FN by adhesion sites. Actomyosin complexes assembled near those sites (both actin and myosin filaments) and moved towards the centre of the non-adhesive regions in a treadmilling network. Inhibition of myosin-II (MII) or Rho-kinase collapsed bridges, whereas extension continued over adhesive areas. Inhibition of actin polymerization (latrunculin-A, jasplakinolide) also collapsed the actomyosin network. We suggest that MII has distinct functions at different bridge regions: (1) at the concave edges of bridges, MIIA force stimulates actin filament assembly at adhesions and (2) in the body of bridges, myosin cross-links actin filaments and stimulates actomyosin network healing when breaks occur. Both activities ensure turnover of actin networks needed to maintain stable bridges from one adhesive region to another.

KW - Actomyosin dynamics

KW - Adhesion

KW - Contractile treadmilling

KW - Latrunculin

KW - Patterned surfaces

UR - http://www.scopus.com/inward/record.url?scp=77949568954&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77949568954&partnerID=8YFLogxK

U2 - 10.1038/emboj.2010.2

DO - 10.1038/emboj.2010.2

M3 - Article

C2 - 20150894

AN - SCOPUS:77949568954

VL - 29

SP - 1055

EP - 1068

JO - EMBO Journal

JF - EMBO Journal

SN - 0261-4189

IS - 6

ER -