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.

Science 17 September 2004:
Vol. 305. no. 5691, pp. 1782 - 1786
DOI: 10.1126/science.1100533
Prev | Table of Contents | Next

Reports

Two Distinct Actin Networks Drive the Protrusion of Migrating Cells

A. Ponti, M. Machacek, S. L. Gupton, C. M. Waterman-Storer,*{dagger} G. Danuser*{dagger}

Cell migration initiates by extension of the actin cytoskeleton at the leading edge. Computational analysis of fluorescent speckle microscopy movies of migrating epithelial cells revealed this process is mediated by two spatially colocalized but kinematically, kinetically, molecularly, and functionally distinct actin networks. A lamellipodium network assembled at the leading edge but completely disassembled within 1 to 3 micrometers. It was weakly coupled to the rest of the cytoskeleton and promoted the random protrusion and retraction of the leading edge. Productive cell advance was a function of the second colocalized network, the lamella, where actomyosin contraction was integrated with substrate adhesion.

Department of Cell Biology, The Scripps Research Institute (TSRI), 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.) and gdanuser{at}scripps.edu (G.D.)

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts.
W. D. Bradley and A. J. Koleske (2009)
J. Cell Sci. 122, 3441-3454
   Abstract »    Full Text »    PDF »
Clustering of {alpha}5{beta}1 integrins determines adhesion strength whereas {alpha}v{beta}3 and talin enable mechanotransduction.
P. Roca-Cusachs, N. C. Gauthier, A. del Rio, and M. P. Sheetz (2009)
PNAS 106, 16245-16250
   Abstract »    Full Text »    PDF »
Multi-scale models of cell and tissue dynamics.
M. A. Stolarska, Y. Kim, and H. G. Othmer (2009)
Phil Trans R Soc A 367, 3525-3553
   Abstract »    Full Text »    PDF »
Shifting views on the leading role of the lamellipodium in cell migration: speckle tracking revisited.
P. Vallotton and J. V. Small (2009)
J. Cell Sci. 122, 1955-1958
   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 »
Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion.
S. Lapetina, C. C. Mader, K. Machida, B. J. Mayer, and A. J. Koleske (2009)
J. Cell Biol. 185, 503-519
   Abstract »    Full Text »    PDF »
Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array.
C. J. Staiger, M. B. Sheahan, P. Khurana, X. Wang, D. W. McCurdy, and L. Blanchoin (2009)
J. Cell Biol. 184, 269-280
   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 »
Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells.
K. Zaoui, S. Honore, D. Isnardon, D. Braguer, and A. Badache (2008)
J. Cell Biol. 183, 401-408
   Abstract »    Full Text »    PDF »
Dynamic stabilization of actin filaments.
H. Y. Kueh, W. M. Brieher, and T. J. Mitchison (2008)
PNAS 105, 16531-16536
   Abstract »    Full Text »    PDF »
Dynein drives nuclear rotation during forward progression of motile fibroblasts.
J. R. Levy and E. L. F. Holzbaur (2008)
J. Cell Sci. 121, 3187-3195
   Abstract »    Full Text »    PDF »
Actin disassembly by cofilin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers.
H. Y. Kueh, G. T. Charras, T. J. Mitchison, and W. M. Brieher (2008)
J. Cell Biol. 182, 341-353
   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 »
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 »
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 »
Phosphorylation of WAVE2 by MAP kinases regulates persistent cell migration and polarity.
C. M. Danson, S. M. Pocha, G. B. Bloomberg, and G. O. Cory (2007)
J. Cell Sci. 120, 4144-4154
   Abstract »    Full Text »    PDF »
Cutting Edge: Atypical PKCs Regulate T Lymphocyte Polarity and Scanning Behavior.
E. Real, S. Faure, E. Donnadieu, and J. Delon (2007)
J. Immunol. 179, 5649-5652
   Abstract »    Full Text »    PDF »
Cdc42 is required for EGF-stimulated protrusion and motility in MTLn3 carcinoma cells.
M. El-Sibai, P. Nalbant, H. Pang, R. J. Flinn, C. Sarmiento, F. Macaluso, M. Cammer, J. S. Condeelis, K. M. Hahn, and J. M. Backer (2007)
J. Cell Sci. 120, 3465-3474
   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 »
Comparative Maps of Motion and Assembly of Filamentous Actin and Myosin II in Migrating Cells.
S. Schaub, S. Bohnet, V. M. Laurent, J.-J. Meister, and A. B. Verkhovsky (2007)
Mol. Biol. Cell 18, 3723-3732
   Abstract »    Full Text »    PDF »
The Abl-related Gene Tyrosine Kinase Acts through p190RhoGAP to Inhibit Actomyosin Contractility and Regulate Focal Adhesion Dynamics upon Adhesion to Fibronectin.
J. G. Peacock, A. L. Miller, W. D. Bradley, O. C. Rodriguez, D. J. Webb, and A. J. Koleske (2007)
Mol. Biol. Cell 18, 3860-3872
   Abstract »    Full Text »    PDF »
Multicolor Super-Resolution Imaging with Photo-Switchable Fluorescent Probes.
M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang (2007)
Science 317, 1749-1753
   Abstract »    Full Text »    PDF »
Control of Actin Assembly Dynamics in Cell Motility.
M.-F. Carlier and D. Pantaloni (2007)
J. Biol. Chem. 282, 23005-23009
   Full Text »    PDF »
Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions.
S. Rhee, H. Jiang, C.-H. Ho, and F. Grinnell (2007)
PNAS 104, 5425-5430
   Abstract »    Full Text »    PDF »
Prostate-Derived ETS Factor Is a Mediator of Metastatic Potential through the Inhibition of Migration and Invasion in Breast Cancer.
D. P. Turner, O. Moussa, M. Sauane, P. B. Fisher, and D. K. Watson (2007)
Cancer Res. 67, 1618-1625
   Abstract »    Full Text »    PDF »
Differential Transmission of Actin Motion Within Focal Adhesions.
K. Hu, L. Ji, K. T. Applegate, G. Danuser, and C. M. Waterman-Storer (2007)
Science 315, 111-115
   Abstract »    Full Text »    PDF »
S-adenosylhomocysteine hydrolase is localized at the front of chemotaxing cells, suggesting a role for transmethylation during migration.
S. Shu, D. C. Mahadeo, X. Liu, W. Liu, C. A. Parent, and E. D. Korn (2006)
PNAS 103, 19788-19793
   Abstract »    Full Text »    PDF »
Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast.
T. M. Huckaba, T. Lipkin, and L. A. Pon (2006)
J. Cell Biol. 175, 957-969
   Abstract »    Full Text »    PDF »
Probing the integrin-actin linkage using high-resolution protein velocity mapping.
C. M. Brown, B. Hebert, D. L. Kolin, J. Zareno, L. Whitmore, A. R. Horwitz, and P. W. Wiseman (2006)
J. Cell Sci. 119, 5204-5214
   Abstract »    Full Text »    PDF »
Dissection of amoeboid movement into two mechanically distinct modes.
K. Yoshida and T. Soldati (2006)
J. Cell Sci. 119, 3833-3844
   Abstract »    Full Text »    PDF »
From imaging to understanding: Frontiers in Live Cell Imaging, Bethesda, MD, April 19-21, 2006.
Y.-l. Wang, K. M. Hahn, R. F. Murphy, and A. F. Horwitz (2006)
J. Cell Biol. 174, 481-484
   Abstract »    Full Text »    PDF »
Sleeping beauty transposon-based phenotypic analysis of mice: lack of arpc3 results in defective trophoblast outgrowth..
K. Yae, V. W. Keng, M. Koike, K. Yusa, M. Kouno, Y. Uno, G. Kondoh, T. Gotow, Y. Uchiyama, K. Horie, et al. (2006)
Mol. Cell. Biol. 26, 6185-6196
   Abstract »    Full Text »    PDF »
Rac1-null Mouse Embryonic Fibroblasts Are Motile and Respond to Platelet-derived Growth Factor.
L. Vidali, F. Chen, G. Cicchetti, Y. Ohta, and D. J. Kwiatkowski (2006)
Mol. Biol. Cell 17, 2377-2390
   Abstract »    Full Text »    PDF »
FGF-2-Induced Wound Healing in Corneal Endothelial Cells Requires Cdc42 Activation and Rho Inactivation through the Phosphatidylinositol 3-Kinase Pathway..
J. G. Lee and E. P. Kay (2006)
Invest. Ophthalmol. Vis. Sci. 47, 1376-1386
   Abstract »    Full Text »    PDF »
h2-calponin Is Regulated by Mechanical Tension and Modifies the Function of Actin Cytoskeleton.
M. M. Hossain, J. F. Crish, R. L. Eckert, J. J.-C. Lin, and J.-P. Jin (2005)
J. Biol. Chem. 280, 42442-42453
   Abstract »    Full Text »    PDF »
Blebbistatin, a Novel Inhibitor of Myosin II ATPase Activity, Increases Aqueous Humor Outflow Facility in Perfused Enucleated Porcine Eyes.
M. Zhang and P. V. Rao (2005)
Invest. Ophthalmol. Vis. Sci. 46, 4130-4138
   Abstract »    Full Text »    PDF »
Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis.
S. O. Dean, S. L. Rogers, N. Stuurman, R. D. Vale, and J. A. Spudich (2005)
PNAS 102, 13473-13478
   Abstract »    Full Text »    PDF »
Adhesion-dependent and Contractile Ring-independent Equatorial Furrowing during Cytokinesis in Mammalian Cells.
M. Kanada, A. Nagasaki, and T. Q.P. Uyeda (2005)
Mol. Biol. Cell 16, 3865-3872
   Abstract »    Full Text »    PDF »
Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells.
M. J. Lehmann, N. M. Sherer, C. B. Marks, M. Pypaert, and W. Mothes (2005)
J. Cell Biol. 170, 317-325
   Abstract »    Full Text »    PDF »
Actopaxin Interacts with TESK1 to Regulate Cell Spreading on Fibronectin.
D. P. LaLonde, M. C. Brown, B. P. Bouverat, and C. E. Turner (2005)
J. Biol. Chem. 280, 21680-21688
   Abstract »    Full Text »    PDF »
Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin.
S. L. Gupton, K. L. Anderson, T. P. Kole, R. S. Fischer, A. Ponti, S. E. Hitchcock-DeGregori, G. Danuser, V. M. Fowler, D. Wirtz, D. Hanein, et al. (2005)
J. Cell Biol. 168, 619-631
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)