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PMID: 9265656 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization.

The Journal of cell biology ·Vol. 138 ·No. 4 ·1997-08-25 ·Pages 913-26

Machesky LM, Hall A

Abstract

Most animal cells use a combination of actin-myosin-based contraction and actin polymerization- based protrusion to control their shape and motility. The small GTPase Rho triggers the formation of contractile stress fibers and focal adhesion complexes (Ridley, A.J., and A. Hall. 1992. Cell. 70:389-399) while a close relative, Rac, induces lamellipodial protrusions and focal complexes in the lamellipodium (Nobes, C.D., and A. Hall. 1995. Cell. 81:53-62; Ridley, A.J., H.F. Paterson, C.L. Johnston, D. Diekmann, and A. Hall. 1992. Cell. 70:401-410); the Rho family of small GTPases may thus play an important role in regulating cell movement. Here we explore the roles of actin polymerization and extracellular matrix in Rho- and Rac-stimulated cytoskeletal changes. To examine the underlying mechanisms through which these GTPases control F-actin assembly, fluorescently labeled monomeric actin, Cy3-actin, was introduced into serum-starved Swiss 3T3 fibroblasts. Incorporation of Cy3- actin into lamellipodial protrusions is concomitant with F-actin assembly after activation of Rac, but Cy3-actin is not incorporated into stress fibers formed immediately after Rho activation. We conclude that Rac induces rapid actin polymerization in ruffles near the plasma membrane, whereas Rho induces stress fiber assembly primarily by the bundling of actin filaments. Activation of Rho or Rac also leads to the formation of integrin adhesion complexes. Integrin clustering is not required for the Rho-induced assembly of actin-myosin filament bundles, or for vinculin association with actin bundles, but is required for stress fiber formation. Integrin-dependent focal complex assembly is not required for the Rac-induced formation of lamellipodia or membrane ruffles. It appears, therefore, that the assembly of large integrin complexes is not required for most of the actin reorganization or cell morphology changes induced by Rac or Rho activation in Swiss 3T3 fibroblasts.

MeSH Terms
3T3 Cells Actins/analysis,metabolism,physiology Animals Cell Adhesion/drug effects Cell Movement/drug effects Culture Media, Serum-Free Cytoskeleton/drug effects,metabolism,physiology Enzyme Activation Extracellular Matrix/physiology GTP Phosphohydrolases/metabolism,physiology GTP-Binding Proteins/physiology Mice Platelet-Derived Growth Factor/pharmacology Polymers/metabolism rac GTP-Binding Proteins rho GTP-Binding Proteins
Chemicals
Actins Culture Media, Serum-Free Platelet-Derived Growth Factor Polymers GTP Phosphohydrolases GTP-Binding Proteins rac GTP-Binding Proteins rho GTP-Binding Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Machesky L M
Department of Molecular Medicine, Medical Research Council Laboratory for Molecular Cell Biology, University College London, United Kingdom. dmcblam@ucl.ac.uk
Hall A
References (37)
37 references, click to expand
  1. ADP-ribosylation of the GTP-binding protein Rho by Clostridium limosum exoenzyme affects basal, but not N-formyl-peptide-stimulated, actin polymerization in human myeloid leukaemic (HL60) cells.
    Biochem J. 1994 May 1;299 ( Pt 3):775-9 PMID: 8192667
  2. Involvement of microtubules in the control of adhesion-dependent signal transduction.
    Curr Biol. 1996 Oct 1;6(10):1279-89 PMID: 8939572
  3. Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells.
    Mol Cell Biol. 1995 Feb;15(2):1110-22 PMID: 7823927
  4. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia.
    Cell. 1995 Apr 7;81(1):53-62 PMID: 7536630
  5. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin.
    J Biol Chem. 1971 Aug 10;246(15):4866-71 PMID: 4254541
  6. Kinetics of the cooperative association of actin to actin filaments.
    Biophys Chem. 1975 Jul;3(3):215-25 PMID: 1174645
  7. Chemotactic peptide modulation of actin assembly and locomotion in neutrophils.
    J Cell Biol. 1984 Apr;98(4):1265-71 PMID: 6232281
  8. Reorganization of actin filament bundles in living fibroblasts.
    J Cell Biol. 1984 Oct;99(4 Pt 1):1478-85 PMID: 6541223
  9. Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation.
    Biochemistry. 1984 Dec 18;23(26):6631-41 PMID: 6543322
  10. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling.
    J Cell Biol. 1985 Aug;101(2):597-602 PMID: 4040521
  11. An actin-nucleating activity in polymorphonuclear leukocytes is modulated by chemotactic peptides.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2707-14 PMID: 3793753
  12. Calcium ionophore, phorbol ester, and chemotactic peptide-induced cytoskeleton reorganization in human neutrophils.
    J Clin Invest. 1987 May;79(5):1359-64 PMID: 3106415
  13. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton.
    Annu Rev Cell Biol. 1988;4:487-525 PMID: 3058164
  14. The dynamic distribution of fluorescent analogues of actin and myosin in protrusions at the leading edge of migrating Swiss 3T3 fibroblasts.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2631-45 PMID: 3204122
  15. Analysis of rhodamine and fluorescein-labeled F-actin diffusion in vitro by fluorescence photobleaching recovery.
    Biophys J. 1988 Nov;54(5):801-15 PMID: 3242630
  16. Focal contacts: transmembrane links between the extracellular matrix and the cytoskeleton.
    Bioessays. 1989 Apr;10(4):104-8 PMID: 2658985
  17. Identification of actin nucleation activity and polymerization inhibitor in ameboid cells: their regulation by chemotactic stimulation.
    J Cell Biol. 1989 Nov;109(5):2207-13 PMID: 2553744
  18. Exogenous nucleation sites fail to induce detectable polymerization of actin in living cells.
    J Cell Biol. 1990 Feb;110(2):359-65 PMID: 2404991
  19. Actin-membrane interaction in focal adhesions.
    Cell Differ Dev. 1990 Dec 2;32(3):337-42 PMID: 2129156
  20. Control of actin polymerization in live and permeabilized fibroblasts.
    J Cell Biol. 1991 Aug;114(3):503-13 PMID: 1860882
  21. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  22. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling.
    Cell. 1992 Aug 7;70(3):401-10 PMID: 1643658
  23. On the crawling of animal cells.
    Science. 1993 May 21;260(5111):1086-94 PMID: 8493552
  24. Fast axonal transport is required for growth cone advance.
    Nature. 1993 Nov 4;366(6450):66-9 PMID: 7694151
  25. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets.
    Cell. 1995 Aug 25;82(4):643-53 PMID: 7664343
  26. ADP-ribosylation of Rho enhances actin polymerization-coupled shape oscillations in human neutrophils.
    FEBS Lett. 1995 Sep 25;372(2-3):161-4 PMID: 7556660
  27. Motility of vinculin-deficient F9 embryonic carcinoma cells analyzed by video, laser confocal, and reflection interference contrast microscopy.
    Exp Cell Res. 1995 Dec;221(2):311-9 PMID: 7493629
  28. Integrin transmembrane signaling and cytoskeletal control.
    Curr Opin Cell Biol. 1995 Oct;7(5):681-9 PMID: 8573343
  29. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases.
    J Cell Biol. 1995 Dec;131(6 Pt 2):1857-65 PMID: 8557752
  30. Sphingosine-1-phosphate rapidly induces Rho-dependent neurite retraction: action through a specific cell surface receptor.
    EMBO J. 1996 May 15;15(10):2388-92 PMID: 8665846
  31. Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate.
    Nature. 1996 Jun 6;381(6582):531-5 PMID: 8632828
  32. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase)
    Science. 1996 Jul 12;273(5272):245-8 PMID: 8662509
  33. The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton.
    Mol Cell Biol. 1996 Oct;16(10):5313-27 PMID: 8816443
  34. Signal transduction and actin filament organization.
    Curr Opin Cell Biol. 1996 Feb;8(1):66-73 PMID: 8791404
  35. Physical association of the small GTPase Rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells.
    Mol Biol Cell. 1996 Mar;7(3):435-42 PMID: 8868471
  36. Getting membrane flow and the cytoskeleton to cooperate in moving cells.
    Cell. 1996 Nov 15;87(4):601-6 PMID: 8929529
  37. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells.
    Cell. 1994 Nov 4;79(3):507-13 PMID: 7954816
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1997-08-25
Pages
913-26
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2138040
Subset
IM
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