Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The many faces of actin: matching assembly factors with cellular structures

Nature Cell Biology volume 9, pages 1110–1121 (2007)Cite this article

Abstract

Actin filaments are major components of at least 15 distinct structures in metazoan cells. These filaments assemble from a common pool of actin monomers, but do so at different times and places, and in response to different stimuli. All of these structures require actin-filament assembly factors. To date, many assembly factors have been identified, including Arp2/3 complex, multiple formin isoforms and spire. Now, a major task is to figure out which factors assemble which actin-based structures. Here, we focus on structures at the plasma membrane, including both sheet-like protrusive structures (such as lamellipodia and ruffles) and finger-like protrusions (such as filopodia and microvilli). Insights gained from studies of adherens junctions and the immunological synapse are also considered.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Actin-based structures in metazoan cells.
Figure 2: Filament polymerization by actin assembly factors.
Figure 3: Schematic representations of models of assembly for lamellipodia, lamella, peripheral ruffles and filopodia.
Figure 4: Schematic representations of models for assembly of filopodia and microvilli.
Figure 5: Actin assembly factors and immune synapse.

Similar content being viewed by others

References

  1. Pollard, T. D., Blanchoin, L. & Mullins, R. D. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545–576 (2000).

    CAS  PubMed  Google Scholar 

  2. Moseley, J. B. & Goode, B. L. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70, 605–645 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Pollard, T. D. & Cooper, J. A. Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu. Rev. Biochem. 55, 987–1035 (1986).

    CAS  PubMed  Google Scholar 

  4. Wang, Y. L. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J. Cell Biol. 101, 597–602 (1985).

    CAS  PubMed  Google Scholar 

  5. Mallavarapu, A. & Mitchison, T. Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146, 1097–1106 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Theriot, J. A. & Mitchison, T. J. Actin microfilament dynamics in locomoting cells. Nature 352, 126–131 (1991).

    CAS  PubMed  Google Scholar 

  7. Rzadzinska, A. K. et al. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J. Cell Biol. 164, 887–897 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Goley, E. D. & Welch, M. D. The ARP2/3 complex: an actin nucleator comes of age. Nature Rev. Mol. Cell Biol. 7, 713–726 (2006).

    CAS  Google Scholar 

  9. Higgs, H. N. & Pollard, T. D. Regulation of actin filament formation through Arp2/3 complex: Activation by a Diverse Array of Proteins. Annu. Rev. Biochem. 70, 649–676 (2001).

    CAS  PubMed  Google Scholar 

  10. Machesky, L. M. et al. Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins. Biochem. J. 328, 105–112 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Jay, P. et al. ARP3β, the gene encoding a new human actin-related protein, is alternatively spliced and predominantly expressed in brain neuronal cells. Eur. J. Biochem. 267, 2921–2928 (2000).

    CAS  PubMed  Google Scholar 

  12. Millard, T. H. et al. Identification and characterisation of a novel human isoform of Arp2/3 complex subunit p16-ARC/ARPC5. Cell Motil. Cytoskeleton 54, 81–90 (2003).

    CAS  PubMed  Google Scholar 

  13. Hudson, A. M. & Cooley, L. A subset of dynamic actin rearrangements in Drosophila requires the Arp2/3 complex. J. Cell Biol. 156, 677–687 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Higgs, H. N. Formin proteins: a domain-based approach. Trends Biochem. Sci. 30, 342–353 (2005).

    CAS  PubMed  Google Scholar 

  15. Kovar, D. R. Molecular details of formin-mediated actin assembly. Curr. Opin. Cell Biol. 18, 11–17 (2006).

    CAS  PubMed  Google Scholar 

  16. Harris, E. S., Li, F. & Higgs, H. N. The mouse formin, FRLa, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. J. Biol. Chem. 279, 20076–20087 (2004).

    CAS  PubMed  Google Scholar 

  17. Harris, E. S., Rouiller, I., Hanein, D. & Higgs, H. N. Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J. Biol. Chem. 281, 14383–14392 (2006).

    CAS  PubMed  Google Scholar 

  18. Moseley, J. B. & Goode, B. L. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280, 28023–28033 (2005).

    CAS  PubMed  Google Scholar 

  19. Michelot, A. et al. The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell 17, 2296–2313 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Chhabra, E. S. & Higgs, H. N. INF2 is a WH2 motif-containing formin that severs actin filaments and accelerates both polymerization and depolymerization. J. Biol. Chem. 281, 26754–26767 (2006).

    CAS  PubMed  Google Scholar 

  21. Higgs, H. N. & Peterson, K. J. Phylogenetic analysis of the formin homology 2 (FH2) domain. Mol. Biol. Cell 16, 1–13 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Eng, C. H., Huckaba, T. M. & Gundersen, G. G. The formin mDia regulates GSK3β through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol. Biol. Cell 17, 5004–5016 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Gomez, T. S. et al. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26, 177–190 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Wallar, B. J. & Alberts, A. S. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13, 435–446 (2003)

    CAS  PubMed  Google Scholar 

  25. Kerkhoff, E. Cellular functions of the Spir actin-nucleation factors. Trends Cell Biol. 16, 477–483 (2006).

    CAS  PubMed  Google Scholar 

  26. Quinlan, M. E., Heuser, J. E., Kerkhoff, E. & Mullins, R. D. Drosophila Spire is an actin nucleation factor. Nature 433, 382–388 (2005).

    CAS  PubMed  Google Scholar 

  27. Rosales-Nieves, A. E. et al. Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nature Cell Biol. 8, 367–376 (2006).

    CAS  PubMed  Google Scholar 

  28. Abercrombie, M., Heaysman, J. E. & Pegrum, S. M. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59, 393–398 (1970).

    CAS  PubMed  Google Scholar 

  29. Abercrombie, M., Heaysman, J. E. & Pegrum, S. M. The locomotion of fibroblasts in culture. II. “Ruffling”. Exp. Cell Res. 60, 437–444 (1970).

    CAS  PubMed  Google Scholar 

  30. Abercrombie, M., Heaysman, J. E. & Pegrum, S. M. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp. Cell Res. 62, 389–398 (1970).

    CAS  PubMed  Google Scholar 

  31. Abercrombie, M., Heaysman, J. E. & Pegrum, S. M. The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp. Cell Res. 67, 359–367 (1971).

    CAS  PubMed  Google Scholar 

  32. Izzard, C. S. & Lochner, L. R. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell Sci. 21, 129–159 (1976).

    CAS  PubMed  Google Scholar 

  33. Bailly, M. et al. Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp. Cell Res. 241, 285–299 (1998).

    CAS  PubMed  Google Scholar 

  34. Gupton, S. L. & Waterman-Storer, C. M. Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361–1374 (2006).

    CAS  PubMed  Google Scholar 

  35. Svitkina, T., Verkhovsky, A. B., McQuade, K. M. & Borisy, G. G. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139, 397–415 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Svitkina, T. M. & Borisy, G. G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009–1026 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Ponti, A. et al. Two distinct actin networks drive the protrusion of migrating cells. Science 305, 1782–1786 (2004).

    CAS  PubMed  Google Scholar 

  38. Mullins, R. D., Heuser, J. A. & Pollard, T. D. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl Acad. Sci. USA 95, 6181–6186 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Waterman-Storer, C. M., Desai, A., Bulinski, J. C. & Salmon, E. D. Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227–1230 (1998).

    CAS  PubMed  Google Scholar 

  40. Iwasa, J. H. & Mullins, R. D. Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr. Biol. 17, 395–406 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Small, J. V., Herzog, M. & Anderson, K. Actin filament organization in the fish keratocyte lamellipodium. J. Cell Biol. 129, 1275–1286 (1995).

    CAS  PubMed  Google Scholar 

  42. Svitkina, T. M., Shevelev, A. A., Bershadsky, A. D. & Gelfand, V. I. Cytoskeleton of mouse embryo fibroblasts. Electron microscopy of platinum replicas. Eur. J. Cell Biol. 34, 64–74 (1984).

    CAS  PubMed  Google Scholar 

  43. Giannone, G. et al. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561–575 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Svitkina, T. M. et al. Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160, 409–421 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Welch, M. D. et al. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 138, 375–384 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Bailly, M. et al. Relationship between Arp2/3 complex and the barbed ends of actin filaments at the leading edge of carcinoma cells after epidermal growth factor stimulation. J. Cell Biol. 145, 331–345 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Falet, H. et al. Importance of free actin filament barbed ends for Arp2/3 complex function in platelets and fibroblasts. Proc. Natl Acad. Sci. USA 99, 16782–16787 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Strasser, G. A. et al. Arp2/3 is a negative regulator of growth cone translocation. Neuron 43, 81–94 (2004).

    CAS  PubMed  Google Scholar 

  49. Miyoshi, T. et al. Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: evidence of frequent filament severing. J. Cell Biol. 175, 947–955 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Gupton, S. L. et al. Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin. J. Cell Biol. 168, 619–631 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Bailly, M. et al. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr. Biol. 11, 620–625 (2001).

    CAS  PubMed  Google Scholar 

  52. Steffen, A. et al. Filopodia formation in the absence of functional WAVE- and Arp2/3-complexes. Mol. Biol. Cell. 17, 2581–2591 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Rogers, S. L., Wiedemann, U., Stuurman, N. & Vale, R. D. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162, 1079–1088 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Di Nardo, A. et al. Arp2/3 complex-deficient mouse fibroblasts are viable and have normal leading-edge actin structure and function. Proc. Natl Acad. Sci. USA 102, 16263–16268 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Mogilner, A. & Edelstein-Keshet, L. Regulation of actin dynamics in rapidly moving cells: a quantitative analysis. Biophys. J. 83, 1237–1258 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Suetsugu, S., Yamazaki, D., Kurisu, S. & Takenawa, T. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 5, 595–609 (2003).

    CAS  PubMed  Google Scholar 

  57. Buccione, R., Orth, J. D. & McNiven, M. A. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nature Rev. Mol. Cell Biol. 5, 647–657 (2004).

    CAS  Google Scholar 

  58. Legg, J. A. et al. N-WASP involvement in dorsal ruffle formation in mouse embryonic fibroblasts. Mol. Biol Cell. 18, 678–687 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Svitkina, T. Electron microscopic analysis of the leading edge in migrating cells. Methods Cell Biol. 79, 295–319 (2007).

    CAS  PubMed  Google Scholar 

  60. Goulimari, P. et al. Gα12/13 is essential for directed cell migration and localized Rho-Dia1 function. J. Biol. Chem. 280, 42242–42251 (2005).

    CAS  PubMed  Google Scholar 

  61. Kurokawa, K. & Matsuda, M. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol. Biol. Cell 16, 4294–4303 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Pertz, O., Hodgson, L., Klemke, R. L. & Hahn, K. M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069–1072 (2006).

    CAS  PubMed  Google Scholar 

  63. Watanabe, N. et al. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044–3056 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Aderem, A. & Underhill, D. M. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593–623 (1999).

    CAS  PubMed  Google Scholar 

  65. Niedergang, F. & Chavrier, P. Signaling and membrane dynamics during phagocytosis: many roads lead to the phagos(R)ome. Curr. Opin. Cell Biol. 16, 422–428 (2004).

    CAS  PubMed  Google Scholar 

  66. May, R. C., Caron, E., Hall, A. & Machesky, L. M. Involvement of the Arp2/3 complex in phagocytosis mediated by FcγR or CR3. Nature Cell Biol. 2, 246–248 (2000).

    CAS  PubMed  Google Scholar 

  67. Lorenzi, R. et al. Wiskott-Aldrich syndrome protein is necessary for efficient IgG-mediated phagocytosis. Blood 95, 2943–2946 (2000).

    CAS  PubMed  Google Scholar 

  68. Colucci-Guyon, E. et al. A role for mammalian diaphanous-related formins in complement receptor (CR3)-mediated phagocytosis in macrophages. Curr. Biol. 15, 2007–2012 (2005).

    CAS  PubMed  Google Scholar 

  69. Linder, S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107–117 (2007).

    CAS  PubMed  Google Scholar 

  70. Yamaguchi, H., Pixley, F. & Condeelis, J. Invadopodia and podosomes in tumor invasion. Eur. J. Cell Biol. 85, 213–218 (2006).

    CAS  PubMed  Google Scholar 

  71. Goicoechea, S. et al. Palladin binds to Eps8 and enhances the formation of dorsal ruffles and podosomes in vascular smooth muscle cells. J. Cell Sci. 119, 3316–3324 (2006).

    CAS  PubMed  Google Scholar 

  72. Moreau, V. et al. Cdc42-driven podosome formation in endothelial cells. Eur. J. Cell Biol. 85, 319–325 (2006).

    CAS  PubMed  Google Scholar 

  73. Hufner, K. et al. The VC region of Wiskott-Aldrich syndrome protein induces Arp2/3 complex-dependent actin nucleation. J. Biol. Chem. 276, 35761–35767 (2001).

    CAS  PubMed  Google Scholar 

  74. Linder, S. et al. The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J. Immunol. 165, 221–225 (2000).

    CAS  PubMed  Google Scholar 

  75. Burns, S. et al. Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142–1149 (2001).

    CAS  PubMed  Google Scholar 

  76. Linder, S., Nelson, D., Weiss, M. & Aepfelbacher, M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl Acad. Sci. USA 96, 9648–9653 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Mizutani, K. et al. Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res. 62, 669–674 (2002).

    CAS  PubMed  Google Scholar 

  78. Yamaguchi, H. et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441–452 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Pellegrin, S. & Mellor, H. The Rho family GTPase Rif induces filopodia through mDia2. Curr. Biol. 15, 129–133 (2005).

    CAS  PubMed  Google Scholar 

  80. DeRosier, D. J. & Tilney, L. G. F-actin bundles are derivatives of microvilli: What does this tell us about how bundles might form? J. Cell Biol. 148, 1–6 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Faix, J. & Rottner, K. The making of filopodia. Curr. Opin. Cell Biol. 18, 18–25 (2006).

    CAS  PubMed  Google Scholar 

  82. Zheng, J. Q., Wan, J. J. & Poo, M. M. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140–1149 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Galbraith, C. G., Yamada, K. M. & Galbraith, J. A. Polymerizing actin fibers position integrins primed to probe for adhesion sites. Science 315, 992–995 (2007).

    CAS  PubMed  Google Scholar 

  84. Lehmann, M. J. et al. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170, 317–325 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Sherer, N. M. et al. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biol. 9, 310–315 (2007).

    CAS  PubMed  Google Scholar 

  86. Lidke, D. S. et al. Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J. Cell Biol. 170, 619–626 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Jontes, J. D. & Smith, S. J. Filopodia, spines, and the generation of synaptic diversity. Neuron 27, 11–14 (2000).

    CAS  PubMed  Google Scholar 

  88. Lindberg, U., Hoglund, A. S. & Karlsson, R. On the ultrastructural organization of the microfilament system and the possible role of profilactin. Biochimie 63, 307–323 (1981).

    CAS  PubMed  Google Scholar 

  89. Small, J. V., Rinnerthaler, G. & Hinssen, H. Organization of actin meshworks in cultured cells: the leading edge. Cold Spring Harb. Symp. Quant. Biol. 46, 599–611 (1982).

    PubMed  Google Scholar 

  90. Lewis, A. K. & Bridgman, P. C. Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119, 1219–1243 (1992).

    CAS  PubMed  Google Scholar 

  91. Vignjevic, D. et al. Role of fascin in filopodial protrusion. J. Cell Biol. 174, 863–875 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Miki, H., Sasaki, T., Takai, Y. & Takenawa, T. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93–96 (1998).

    CAS  PubMed  Google Scholar 

  93. Snapper, S. B. et al. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nature Cell Biol. 3, 897–904 (2001).

    CAS  PubMed  Google Scholar 

  94. Peng, J. et al. Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr. Biol. 13, 534–545 (2003).

    CAS  PubMed  Google Scholar 

  95. Wallar, B. J. et al. The basic region of the diaphanous-autoregulatory domain (DAD) is required for autoregulatory interactions with the diaphanous-related formin inhibitory domain. J. Biol. Chem. 281, 4300–4307 (2006).

    CAS  PubMed  Google Scholar 

  96. Schirenbeck, A. et al. The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nature Cell Biol. 7, 619–625 (2005).

    CAS  PubMed  Google Scholar 

  97. Brieher, W. M., Coughlin, M. & Mitchison, T. J. Fascin-mediated propulsion of Listeria monocytogenes independent of frequent nucleation by the Arp2/3 complex. J. Cell Biol. 165, 233–242 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Vignjevic, D. et al. Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 160, 951–962 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Medalia, O. et al. Organization of actin networks in intact filopodia. Curr. Biol. 17, 79–84 (2007).

    CAS  PubMed  Google Scholar 

  100. Mooseker, M. S. & Tilney, L. G. Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J. Cell Biol. 67, 725–743 (1975).

    CAS  PubMed  Google Scholar 

  101. Gorelik, J. et al. Dynamic assembly of surface structures in living cells. Proc. Natl Acad. Sci. USA 100, 5819–5822 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Majstoravich, S. et al. Lymphocyte microvilli are dynamic, actin-dependent structures that do not require Wiskott-Aldrich syndrome protein (WASp) for their morphology. Blood 104, 1396–1403 (2004).

    CAS  PubMed  Google Scholar 

  103. von Andrian, U. H. et al. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell 82, 989–999 (1995).

    CAS  PubMed  Google Scholar 

  104. Singer, II et al. CCR5, CXCR4, and CD4 are clustered and closely apposed on microvilli of human macrophages and T cells. J. Virol. 75, 3779–3790 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Tyska, M. J. & Mooseker, M. S. MYO1A (brush border myosin I) dynamics in the brush border of LLC–PK1–CL4 cells. Biophys. J. 82, 1869–1883 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Hirokawa, N., Tilney, L. G., Fujiwara, K. & Heuser, J. E. Organization of actin, myosin, and intermediate filaments in the brush border of intestinal epithelial cells. J. Cell Biol. 94, 425–443 (1982).

    CAS  PubMed  Google Scholar 

  107. Heintzelman, M. B. & Mooseker, M. S. Assembly of the intestinal brush border cytoskeleton. Curr. Top. Dev. Biol. 26, 93–122 (1992).

    CAS  PubMed  Google Scholar 

  108. Bretscher, A. Microfilament structure and function in the cortical cytoskeleton. Annu. Rev. Cell Biol. 7, 337–374 (1991).

    CAS  PubMed  Google Scholar 

  109. Dustin, M. L. A dynamic view of the immunological synapse. Semin. Immunol. 17, 400–410 (2005).

    CAS  PubMed  Google Scholar 

  110. Billadeau, D. D. & Burkhardt, J. K. Regulation of cytoskeletal dynamics at the immune synapse: new stars join the actin troupe. Traffic 7, 1451–1460 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Eisenmann, K. M. et al. T cell responses in mammalian Diaphanous-related formin mDia1 knock-out mice. J. Biol. Chem. 282, 25152–25158 (2007).

    CAS  PubMed  Google Scholar 

  112. Nolz, J. C. et al. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16, 24–34 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Wen, Y. et al. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nature Cell Biol. 6, 820–830 (2004).

    CAS  PubMed  Google Scholar 

  114. Yamana, N. et al. The Rho–mDia1 pathway regulates cell polarity and focal adhesion turnover in migrating cells through mobilizing Apc and c-Src. Mol. Cell. Biol. 26, 6844–6858 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Ishizaki, T. et al. Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nature Cell Biol. 3, 8–14 (2001).

    CAS  PubMed  Google Scholar 

  116. Aberle, H. et al. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107, 3655–3663 (1994).

    CAS  PubMed  Google Scholar 

  117. Nathke, I. S. et al. Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125, 1341–1352 (1994).

    CAS  PubMed  Google Scholar 

  118. Gates, J. & Peifer, M. Can 1000 reviews be wrong? Actin, α-catenin, and adherens junctions. Cell 123, 769–772 (2005).

    CAS  PubMed  Google Scholar 

  119. Yamada, S. et al. Deconstructing the cadherin-catenin-actin complex. Cell 123, 889–901 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Pilot, F., Philippe, J. M., Lemmers, C. & Lecuit, T. Spatial control of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 442, 580–584 (2006).

    CAS  PubMed  Google Scholar 

  121. Tamada, M., Perez, T. D., Nelson, W. J. & Sheetz, M. P. Two distinct modes of myosin assembly and dynamics during epithelial wound closure. J. Cell Biol. 176, 27–33 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Adams, C. L., Nelson, W. J. & Smith, S. J. Quantitative analysis of cadherin–catenin–actin reorganization during development of cell–cell adhesion. J. Cell Biol. 135, 1899–1911 (1996).

    CAS  PubMed  Google Scholar 

  123. Adams, C. L., Chen, Y. T., Smith, S. J. & Nelson, W. J. Mechanisms of epithelial cell–cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J. Cell Biol. 142, 1105–1119 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Vasioukhin, V., Bauer, C., Yin, M. & Fuchs, E. Directed actin polymerization is the driving force for epithelial cell–cell adhesion. Cell 100, 209–219 (2000).

    CAS  PubMed  Google Scholar 

  125. Yonemura, S., Itoh, M., Nagafuchi, A. & Tsukita, S. Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J. Cell Sci. 108, 127–142 (1995).

    CAS  PubMed  Google Scholar 

  126. Vaezi, A., Bauer, C., Vasioukhin, V. & Fuchs, E. Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Dev. Cell 3, 367–381 (2002).

    CAS  PubMed  Google Scholar 

  127. Ivanov, A. I. et al. Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol. Biol Cell. 16, 2636–2650 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Verma, S. et al. Arp2/3 activity is necessary for efficient formation of E-cadherin adhesive contacts. J. Biol. Chem. 279, 34062–34070 (2004).

    CAS  PubMed  Google Scholar 

  129. Yamada, S. & Nelson, W. J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell cell adhesion. J. Cell Biol. 178, 517–527 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Kobielak, A., Pasolli, H. A. & Fuchs, E. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nature Cell Biol. 6, 21–30 (2004).

    CAS  PubMed  Google Scholar 

  131. Drees, F. et al. α-catenin is a molecular switch that binds E-cadherin–β-catenin and regulates actin-filament assembly. Cell 123, 903–915 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Abercrombie, M. & Ambrose, E. J. Interference microscope studies of cell contacts in tissue culture. Exp Cell Res. 15, 332–345 (1958).

    CAS  PubMed  Google Scholar 

  133. Ingram, V. M. A side view of moving fibroblasts. Nature 222, 641–644 (1969).

    CAS  PubMed  Google Scholar 

  134. Abercrombie, M. The crawling movement of metazoan cells. Proc. R. Soc. Lond. 207, 129–147 (1980).

    Google Scholar 

Download references

Acknowledgements

We are indebted to many for useful discussions, including A. Alberts, D. Billadeau, J. Burkhardt, J. Condeelis, F. Flures, G. Gundersen, M. McNiven, D. Mullins, S. Nicholson-Dykstra, T. Svitkina and C. Waterman-Storer. We also thank our anonymous reviewers, whose comments improved this work immensely. This work was supported by National Institutes of Health grant GM069818 and by a Pew Biomedical Scholars Award.

Author information

Authors and Affiliations

  1. Ekta Seth Chhabra and Henry N. Higgs are in the Department of Biochemistry, Dartmouth Medical School, Hanover, NH 03755, USA. henry.n.higgs@dartmouth.edu,

    Ekta Seth Chhabra & Henry N. Higgs

Authors
  1. Ekta Seth Chhabra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henry N. Higgs
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chhabra, E., Higgs, H. The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9, 1110–1121 (2007). https://doi.org/10.1038/ncb1007-1110

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb1007-1110

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing