Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

Science 315 (5808): 111-115

Copyright © 2007 by the American Association for the Advancement of Science

Differential Transmission of Actin Motion Within Focal Adhesions

Ke Hu,* Lin Ji,* Kathryn T. Applegate, Gaudenz Danuser,{dagger} Clare M. Waterman-Storer{dagger}

Abstract: Cell migration requires the transmission of motion generated in the actin cytoskeleton to the extracellular environment through a complex assembly of proteins in focal adhesions. We developed correlational fluorescent speckle microscopy to measure the coupling of focal-adhesion proteins to actin filaments. Different classes of focal-adhesion structural and regulatory molecules exhibited varying degrees of correlated motions with actin filaments, indicating hierarchical transmission of actin motion through focal adhesions. Interactions between vinculin, talin, and actin filaments appear to constitute a slippage interface between the cytoskeleton and integrins, generating a molecular clutch that is regulated during the morphodynamic transitions of cell migration.

Department of Cell Biology, The Scripps Research Institute, La Jolla, CA 92037, USA.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: waterman{at}scripps.edu (C.M.W.-S.); gdanuser{at}scripps.edu (G.D.)

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Integrin-dependent force transmission to the extracellular matrix by {alpha}-actinin triggers adhesion maturation.
P. Roca-Cusachs, A. del Rio, E. Puklin-Faucher, N. C. Gauthier, N. Biais, and M. P. Sheetz (2013)
PNAS 110, E1361-E1370
   Abstract »    Full Text »    PDF »
Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions.
W. R. Legant, C. K. Choi, J. S. Miller, L. Shao, L. Gao, E. Betzig, and C. S. Chen (2013)
PNAS 110, 881-886
   Abstract »    Full Text »    PDF »
SMB myosin heavy chain knockout enhances tonic contraction and reduces the rate of force generation in ileum and stomach antrum.
Q. Huang, G. J. Babu, M. Periasamy, and T. J. Eddinger (2013)
Am J Physiol Cell Physiol 304, C194-C206
   Abstract »    Full Text »    PDF »
At the leading edge of three-dimensional cell migration.
R. J. Petrie and K. M. Yamada (2012)
J. Cell Sci. 125, 5917-5926
   Abstract »    Full Text »    PDF »
Calcineurin-dependent cofilin activation and increased retrograde actin flow drive 5-HT-dependent neurite outgrowth in Aplysia bag cell neurons.
X.-F. Zhang, C. Hyland, D. Van Goor, and P. Forscher (2012)
Mol. Biol. Cell 23, 4833-4848
   Abstract »    Full Text »    PDF »
Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation.
F. Twiss, Q. Le Duc, S. Van Der Horst, H. Tabdili, G. Van Der Krogt, N. Wang, H. Rehmann, S. Huveneers, D. E. Leckband, and J. De Rooij (2012)
Biology Open 1, 1128-1140
   Abstract »    Full Text »    PDF »
Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell.
R. Yamin and K. G. Morgan (2012)
J. Physiol. 590, 4145-4154
   Abstract »    Full Text »    PDF »
Finding the weakest link - exploring integrin-mediated mechanical molecular pathways.
P. Roca-Cusachs, T. Iskratsch, and M. P. Sheetz (2012)
J. Cell Sci. 125, 3025-3038
   Abstract »    Full Text »    PDF »
United we stand - integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction.
U. S. Schwarz and M. L. Gardel (2012)
J. Cell Sci. 125, 3051-3060
   Abstract »    Full Text »    PDF »
Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow.
Q. Yang, X.-F. Zhang, T. D. Pollard, and P. Forscher (2012)
J. Cell Biol. 197, 939-956
   Abstract »    Full Text »    PDF »
Contributions of talin-1 to glioma cell-matrix tensional homeostasis.
S. Sen, W. P. Ng, and S. Kumar (2012)
J R Soc Interface 9, 1311-1317
   Abstract »    Full Text »    PDF »
Micro-environmental control of cell migration - myosin IIA is required for efficient migration in fibrillar environments through control of cell adhesion dynamics.
A. D. Doyle, M. L. Kutys, M. A. Conti, K. Matsumoto, R. S. Adelstein, and K. M. Yamada (2012)
J. Cell Sci. 125, 2244-2256
   Abstract »    Full Text »    PDF »
Actin stress fibers - assembly, dynamics and biological roles.
S. Tojkander, G. Gateva, and P. Lappalainen (2012)
J. Cell Sci. 125, 1855-1864
   Abstract »    Full Text »    PDF »
Phosphoinositide lipid phosphatase SHIP1 and PTEN coordinate to regulate cell migration and adhesion.
S. Mondal, K. K. Subramanian, J. Sakai, B. Bajrami, and H. R. Luo (2012)
Mol. Biol. Cell 23, 1219-1230
   Abstract »    Full Text »    PDF »
Quantitative mapping of averaged focal adhesion dynamics in migrating cells by shape normalization.
C. Mohl, N. Kirchgessner, C. Schafer, B. Hoffmann, and R. Merkel (2012)
J. Cell Sci. 125, 155-165
   Abstract »    Full Text »    PDF »
Adhesion dynamics at a glance.
M. Vicente-Manzanares and A. R. Horwitz (2011)
J. Cell Sci. 124, 3923-3927
   Full Text »    PDF »
How we discovered fluorescent speckle microscopy.
E. D. Salmon and C. M. Waterman (2011)
Mol. Biol. Cell 22, 3940-3942
   Abstract »    Full Text »    PDF »
Intersection of FOXO- and RUNX1-mediated gene expression programs in single breast epithelial cells during morphogenesis and tumor progression.
L. Wang, J. S. Brugge, and K. A. Janes (2011)
PNAS 108, E803-E812
   Abstract »    Full Text »    PDF »
Integrins in Cell Migration.
A. Huttenlocher and A. R. Horwitz (2011)
Cold Spring Harb Perspect Biol 3, a005074
   Abstract »    Full Text »    PDF »
Cadherins at cell-autonomous membrane contacts control macropinocytosis.
P. J. B. Sabatini, M. Zhang, R. V. Silverman-Gavrila, and M. P. Bendeck (2011)
J. Cell Sci. 124, 2013-2020
   Abstract »    Full Text »    PDF »
Actomyosin-generated tension controls the molecular kinetics of focal adhesions.
H. Wolfenson, A. Bershadsky, Y. I. Henis, and B. Geiger (2011)
J. Cell Sci. 124, 1425-1432
   Abstract »    Full Text »    PDF »
Dynamic and structural signatures of lamellar actomyosin force generation.
Y. Aratyn-Schaus, P. W. Oakes, and M. L. Gardel (2011)
Mol. Biol. Cell 22, 1330-1339
   Abstract »    Full Text »    PDF »
Integrins and Extracellular Matrix in Mechanotransduction.
M. A. Schwartz (2010)
Cold Spring Harb Perspect Biol 2, a005066
   Abstract »    Full Text »    PDF »
Advances in imaging cell-matrix adhesions.
D. C. Worth and M. Parsons (2010)
J. Cell Sci. 123, 3629-3638
   Abstract »    Full Text »    PDF »
Towards a quantitative understanding of mitotic spindle assembly and mechanics.
A. Mogilner and E. Craig (2010)
J. Cell Sci. 123, 3435-3445
   Abstract »    Full Text »    PDF »
Understanding the Structure and Function of the Immunological Synapse.
M. L. Dustin, A. K. Chakraborty, and A. S. Shaw (2010)
Cold Spring Harb Perspect Biol 2, a002311
   Abstract »    Full Text »    PDF »
Leading Tip Drives Soma Translocation via Forward F-Actin Flow during Neuronal Migration.
M. He, Z.-h. Zhang, C.-b. Guan, D. Xia, and X.-b. Yuan (2010)
J. Neurosci. 30, 10885-10898
   Abstract »    Full Text »    PDF »
Vinculin Is a Dually Regulated Actin Filament Barbed End-capping and Side-binding Protein.
C. Le Clainche, S. P. Dwivedi, D. Didry, and M.-F. Carlier (2010)
J. Biol. Chem. 285, 23420-23432
   Abstract »    Full Text »    PDF »
The switchable integrin adhesome.
R. Zaidel-Bar and B. Geiger (2010)
J. Cell Sci. 123, 1385-1388
   Full Text »    PDF »
Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation.
A. M. Pasapera, I. C. Schneider, E. Rericha, D. D. Schlaepfer, and C. M. Waterman (2010)
J. Cell Biol. 188, 877-890
   Abstract »    Full Text »    PDF »
Force transmission in migrating cells.
M. F. Fournier, R. Sauser, D. Ambrosi, J.-J. Meister, and A. B. Verkhovsky (2010)
J. Cell Biol. 188, 287-297
   Abstract »    Full Text »    PDF »
Guanine Nucleotide Exchange Factor-H1 Regulates Cell Migration via Localized Activation of RhoA at the Leading Edge.
P. Nalbant, Y.-C. Chang, J. Birkenfeld, Z.-F. Chang, and G. M. Bokoch (2009)
Mol. Biol. Cell 20, 4070-4082
   Abstract »    Full Text »    PDF »
Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions.
C. Albiges-Rizo, O. Destaing, B. Fourcade, E. Planus, and M. R. Block (2009)
J. Cell Sci. 122, 3037-3049
   Abstract »    Full Text »    PDF »
Coronin 2A regulates a subset of focal-adhesion-turnover events through the cofilin pathway.
T. W. Marshall, H. L. Aloor, and J. E. Bear (2009)
J. Cell Sci. 122, 3061-3069
   Abstract »    Full Text »    PDF »
Role of Partitioning-defective 1/Microtubule Affinity-regulating Kinases in the Morphogenetic Activity of Helicobacter pylori CagA.
H. Lu, N. Murata-Kamiya, Y. Saito, and M. Hatakeyama (2009)
J. Biol. Chem. 284, 23024-23036
   Abstract »    Full Text »    PDF »
Cluster size regulates protein sorting in the immunological synapse.
N. C. Hartman, J. A. Nye, and J. T. Groves (2009)
PNAS 106, 12729-12734
   Abstract »    Full Text »    PDF »
Epidermal Growth Factor-induced Contraction Regulates Paxillin Phosphorylation to Temporally Separate Traction Generation from De-adhesion.
I. C. Schneider, C. K. Hays, and C. M. Waterman (2009)
Mol. Biol. Cell 20, 3155-3167
   Abstract »    Full Text »    PDF »
Testing the lamella hypothesis: the next steps on the agenda.
G. Danuser (2009)
J. Cell Sci. 122, 1959-1962
   Full Text »    PDF »
Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization.
J. Colombelli, A. Besser, H. Kress, E. G. Reynaud, P. Girard, E. Caussinus, U. Haselmann, J. V. Small, U. S. Schwarz, and E. H. K. Stelzer (2009)
J. Cell Sci. 122, 1665-1679
   Abstract »    Full Text »    PDF »
Genetic and cell biological analysis of integrin outside-in signaling.
K. R. Legate, S. A. Wickstrom, and R. Fassler (2009)
Genes & Dev. 23, 397-418
   Abstract »    Full Text »    PDF »
Integrin signalling at a glance.
D. S. Harburger and D. A. Calderwood (2009)
J. Cell Sci. 122, 159-163
   Full Text »    PDF »
The mechanical integrin cycle.
E. Puklin-Faucher and M. P. Sheetz (2009)
J. Cell Sci. 122, 179-186
   Abstract »    Full Text »    PDF »
Integrins in cell migration - the actin connection.
M. Vicente-Manzanares, C. K. Choi, and A. R. Horwitz (2009)
J. Cell Sci. 122, 199-206
   Abstract »    Full Text »    PDF »
Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed.
M. L. Gardel, B. Sabass, L. Ji, G. Danuser, U. S. Schwarz, and C. M. Waterman (2008)
J. Cell Biol. 183, 999-1005
   Abstract »    Full Text »    PDF »
BIOPHYSICS: Clutch Dynamics.
Y. Aratyn-Schaus and M. L. Gardel (2008)
Science 322, 1646-1647
   Abstract »    Full Text »    PDF »
Traction Dynamics of Filopodia on Compliant Substrates.
C. E. Chan and D. J. Odde (2008)
Science 322, 1687-1691
   Abstract »    Full Text »    PDF »
Structural model and functional significance of pH-dependent talin-actin binding for focal adhesion remodeling.
J. Srivastava, G. Barreiro, S. Groscurth, A. R. Gingras, B. T. Goult, D. R. Critchley, M. J. S. Kelly, M. P. Jacobson, and D. L. Barber (2008)
PNAS 105, 14436-14441
   Abstract »    Full Text »    PDF »
Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner.
H. Hirata, H. Tatsumi, and M. Sokabe (2008)
J. Cell Sci. 121, 2795-2804
   Abstract »    Full Text »    PDF »
Paxillin comes of age.
N. O. Deakin and C. E. Turner (2008)
J. Cell Sci. 121, 2435-2444
   Abstract »    Full Text »    PDF »
Regulation of Actin Assembly Associated With Protrusion and Adhesion in Cell Migration.
C. Le Clainche and M.-F. Carlier (2008)
Physiol Rev 88, 489-513
   Abstract »    Full Text »    PDF »
Tyrosine phosphatase PTP{alpha} regulates focal adhesion remodeling through Rac1 activation.
M. T. Herrera Abreu, P. Castellanos Penton, V. Kwok, E. Vachon, D. Shalloway, L. Vidali, W. Lee, C. A. McCulloch, and G. P. Downey (2008)
Am J Physiol Cell Physiol 294, C931-C944
   Abstract »    Full Text »    PDF »
Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells.
Y. Kaizuka, A. D. Douglass, R. Varma, M. L. Dustin, and R. D. Vale (2007)
PNAS 104, 20296-20301
   Abstract »    Full Text »    PDF »
Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes.
H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig (2007)
PNAS 104, 20308-20313
   Abstract »    Full Text »    PDF »
Vinculin controls focal adhesion formation by direct interactions with talin and actin.
J. D. Humphries, P. Wang, C. Streuli, B. Geiger, M. J. Humphries, and C. Ballestrem (2007)
J. Cell Biol. 179, 1043-1057
   Abstract »    Full Text »    PDF »
Cardiac-Myocyte-Specific Excision of the Vinculin Gene Disrupts Cellular Junctions, Causing Sudden Death or Dilated Cardiomyopathy.
A. E. Zemljic-Harpf, J. C. Miller, S. A. Henderson, A. T. Wright, A. M. Manso, L. Elsherif, N. D. Dalton, A. K. Thor, G. A. Perkins, A. D. McCulloch, et al. (2007)
Mol. Cell. Biol. 27, 7522-7537
   Abstract »    Full Text »    PDF »
Mapping the dynamics of shear stress-induced structural changes in endothelial cells.
R. E. Mott and B. P. Helmke (2007)
Am J Physiol Cell Physiol 293, C1616-C1626
   Abstract »    Full Text »    PDF »
Retrograde Fluxes of Focal Adhesion Proteins in Response to Cell Migration and Mechanical Signals.
W.-h. Guo and Y.-l. Wang (2007)
Mol. Biol. Cell 18, 4519-4527
   Abstract »    Full Text »    PDF »
mDia2 regulates actin and focal adhesion dynamics and organization in the lamella for efficient epithelial cell migration.
S. L. Gupton, K. Eisenmann, A. S. Alberts, and C. M. Waterman-Storer (2007)
J. Cell Sci. 120, 3475-3487
   Abstract »    Full Text »    PDF »
Forces and Bond Dynamics in Cell Adhesion.
E. A. Evans and D. A. Calderwood (2007)
Science 316, 1148-1153
   Abstract »    Full Text »    PDF »
Flux at Focal Adhesions: Slippage Clutch, Mechanical Gauge, or Signal Depot.
Y.-l. Wang (2007)
Sci. STKE 2007, pe10
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882