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Molecules and Cells

, Volume 29, Issue 4, pp 311–325 | Cite as

Regulation of actin cytoskeleton dynamics in cells

  • Sung Haeng LeeEmail author
  • Roberto Dominguez
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Abstract

The dynamic remolding of the actin cytoskeleton is a critical part of most cellular activities, and malfunction of cytoskeletal proteins results in various human diseases. The transition between two forms of actin, monomeric or G-actin and filamentous or F-actin, is tightly regulated in time and space by a large number of signaling, scaffolding and actin-binding proteins (ABPs). New ABPs are constantly being discovered in the post-genomic era. Most of these proteins are modular, integrating actin binding, protein-protein interaction, membrane-binding, and signaling domains. In response to extracellular signals, often mediated by Rho family GTPases, ABPs control different steps of actin cytoskeleton assembly, including filament nucleation, elongation, severing, capping, and depolymerization. This review summarizes structure-function relationships among ABPs in the regulation of actin cytoskeleton assembly.

Keywords

actin-binding protein actin cytoskeleton BAR protein F-actin filament cross-linking filament nucleation and elongation G-actin Rho-GTPase WH2 

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References

  1. Ahmed, M.A., Bamm, V.V., Shi, L., Steiner-Mosonyi, M., Dawson, J.F., Brown, L., Harauz, G., and Ladizhansky, V. (2009). Induced secondary structure and polymorphism in an intrinsically disordered structural linker of the CNS: solid-state NMR and FTIR spectroscopy of myelin basic protein bound to actin. Biophys. J. 96, 180–191.PubMedCrossRefGoogle Scholar
  2. Ahuja, R., Pinyol, R., Reichenbach, N., Custer, L., Klingensmith, J., Kessels, M.M., and Qualmann, B. (2007). Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 131, 337–350.PubMedCrossRefGoogle Scholar
  3. Amann, K.J., Guo, A.W., and Ervasti, J.M. (1999). Utrophin lacks the rod domain actin binding activity of dystrophin. J. Biol. Chem. 274, 35375–35380.PubMedCrossRefGoogle Scholar
  4. Arber, S., Barbayannis, F.A., Hanser, H., Schneider, C., Stanyon, C.A., Bernard, O., and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805–809.PubMedCrossRefGoogle Scholar
  5. Bachmann, C., Fischer, L., Walter, U., and Reinhard, M. (1999). The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274, 23549–23557.PubMedCrossRefGoogle Scholar
  6. Bailly, M., and Condeelis, J. (2002). Cell motility: insights from the backstage. Nat. Cell. Biol. 4, E292–294.PubMedCrossRefGoogle Scholar
  7. Bamburg, J.R. (1999). Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185–230.PubMedCrossRefGoogle Scholar
  8. Belmont, L.D., Orlova, A., Drubin, D.G., and Egelman, E.H. (1999). A change in actin conformation associated with filament instability after Pi release. Proc. Natl. Acad. Sci. USA 96, 29–34.PubMedCrossRefGoogle Scholar
  9. Bennett, V., and Baines, A.J. (2001). Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353–1392.PubMedGoogle Scholar
  10. Blanchard, A., Ohanian, V., and Critchley, D. (1989). The structure and function of alpha-actinin. J. Muscle Res. Cell Motil. 10, 280–289.PubMedCrossRefGoogle Scholar
  11. Borrego-Diaz, E., Kerff, F., Lee, S.H., Ferron, F., Li, Y., and Dominguez, R. (2006). Crystal structure of the actin-binding domain of alpha-actinin 1: evaluating two competing actinbinding models. J. Struct. Biol. 155, 230–238.PubMedCrossRefGoogle Scholar
  12. Bowman, G.D., Nodelman, I.M., Hong, Y., Chua, N.H., Lindberg, U., and Schutt, C.E. (2000). A comparative structural analysis of the ADF/cofilin family. Proteins 41, 374–384.PubMedCrossRefGoogle Scholar
  13. Breitsprecher, D., Kiesewetter, A.K., Linkner, J., Urbanke, C., Resch, G.P., Small, J.V., and Faix, J. (2008). Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943–2954.PubMedCrossRefGoogle Scholar
  14. Brindle, N.P., Holt, M.R., Davies, J.E., Price, C.J., and Critchley, D.R. (1996). The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin. Biochem. J. 318, 753–757.PubMedGoogle Scholar
  15. Broderick, M.J., and Winder, S.J. (2005). Spectrin, alpha-actinin, and dystrophin. Adv. Protein Chem. 70, 203–246.PubMedCrossRefGoogle Scholar
  16. Burbelo, P.D., Drechsel, D., and Hall, A. (1995). A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J. Biol. Chem. 270, 29071–29074.PubMedCrossRefGoogle Scholar
  17. Campbell, K.P., and Kahl, S.D. (1989). Association of dystrophin and an integral membrane glycoprotein. Nature 338, 259–262.PubMedCrossRefGoogle Scholar
  18. Caron, E., and Hall, A. (1998). Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282, 1717–1721.PubMedCrossRefGoogle Scholar
  19. Castrillon, D.H., and Wasserman, S.A. (1994). Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120, 3367–3377.PubMedGoogle Scholar
  20. Chereau, D., and Dominguez, R. (2006). Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J. Struct. Biol. 155, 195–201.PubMedCrossRefGoogle Scholar
  21. Chereau, D., Kerff, F., Graceffa, P., Grabarek, Z., Langsetmo, K., and Dominguez, R. (2005). Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly. Proc. Natl. Acad. Sci. USA 102, 16644–16649.PubMedCrossRefGoogle Scholar
  22. Chereau, D., Boczkowska, M., Skwarek-Maruszewska, A., Fujiwara, I., Hayes, D.B., Rebowski, G., Lappalainen, P., Pollard, T.D., and Dominguez, R. (2008). Leiomodin is an actin filament nucleator in muscle cells. Science 320, 239–243.PubMedCrossRefGoogle Scholar
  23. Condeelis, J., Singer, R.H., and Segall, J.E. (2005). The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21, 695–718.PubMedCrossRefGoogle Scholar
  24. Dawson, J.C., Legg, J.A., and Machesky, L.M. (2006). Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493–498.PubMedCrossRefGoogle Scholar
  25. Doctor, R.B., and Fouassier, L. (2002). Emerging roles of the actin cytoskeleton in cholangiocyte function and disease. Semin. Liver Dis. 22, 263–276.PubMedCrossRefGoogle Scholar
  26. Domanski, M., Hertzog, M., Coutant, J., Gutsche-Perelroizen, I., Bontems, F., Carlier, M.F., Guittet, E., and van Heijenoort, C. (2004). Coupling of folding and binding of thymosin beta4 upon interaction with monomeric actin monitored by nuclear magnetic resonance. J. Biol. Chem. 279, 23637–23645.PubMedCrossRefGoogle Scholar
  27. Dominguez, R. (2004). Actin-binding proteins—a unifying hypothesis. Trends Biochem. Sci. 29, 572–578.PubMedCrossRefGoogle Scholar
  28. Dominguez, R. (2007). The beta-thymosin/WH2 fold: multifunctionality and structure. Ann. N Y Acad. Sci. 1112, 86–94.PubMedCrossRefGoogle Scholar
  29. Dominguez, R. (2009). Actin filament nucleation and elongation factors—structure-function relationships. Crit. Rev. Biochem. Mol. Biol. 44, 351–366.PubMedCrossRefGoogle Scholar
  30. Edwards, D.C., Sanders, L.C., Bokoch, G.M., and Gill, G.N. (1999). Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1, 253–259.PubMedCrossRefGoogle Scholar
  31. Egelman, E.H. (1994). Actin filament structure. The ghost of ribbons past. Curr. Biol. 4, 79–81.PubMedCrossRefGoogle Scholar
  32. Eisenmann, K.M., Harris, E.S., Kitchen, S.M., Holman, H.A., Higgs, H.N., and Alberts, A.S. (2007). Dia-interacting protein modulates formin-mediated actin assembly at the cell cortex. Curr. Biol. 17, 579–591.PubMedCrossRefGoogle Scholar
  33. Engqvist-Goldstein, A.E., and Drubin, D.G. (2003). Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19, 287–332.PubMedCrossRefGoogle Scholar
  34. Etienne-Manneville, S., and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629–635.PubMedCrossRefGoogle Scholar
  35. Fedorov, A.A., Lappalainen, P., Fedorov, E.V., Drubin, D.G., and Almo, S.C. (1997). Structure determination of yeast cofilin. Nat. Struct. Biol. 4, 366–369.PubMedCrossRefGoogle Scholar
  36. Ferguson, K.M., Lemmon, M.A., Sigler, P.B., and Schlessinger, J. (1995). Scratching the surface with the PH domain. Nat. Struct. Biol. 2, 715–718.PubMedCrossRefGoogle Scholar
  37. Ferron, F., Rebowski, G., Lee, S.H., and Dominguez, R. (2007). Structural basis for the recruitment of profilin-actin complexes during filament elongation by Ena/VASP. EMBO J. 26, 4597–4606.PubMedCrossRefGoogle Scholar
  38. Foster, R., Hu, K.Q., Lu, Y., Nolan, K.M., Thissen, J., and Settleman, J. (1996). Identification of a novel human Rho protein with unusual properties: GTPase deficiency and in vivo farnesylation. Mol. Cell. Biol. 16, 2689–2699.PubMedGoogle Scholar
  39. Franzot, G., Sjoblom, B., Gautel, M., and Djinovic Carugo, K. (2005). The crystal structure of the actin binding domain from alpha-actinin in its closed conformation: structural insight into phospholipid regulation of alpha-actinin. J. Mol. Biol. 348, 151–165.PubMedCrossRefGoogle Scholar
  40. Frost, A., De Camilli, P., and Unger, V.M. (2007). F-BAR proteins join the BAR family fold. Structure 15, 751–753.PubMedCrossRefGoogle Scholar
  41. Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E.H., De Camilli, P., and Unger, V.M. (2008). Structural basis of membrane invagination by F-BAR domains. Cell 132, 807–817.PubMedCrossRefGoogle Scholar
  42. Galkin, V.E., Orlova, A., VanLoock, M.S., Rybakova, I.N., Ervasti, J.M., and Egelman, E.H. (2002). The utrophin actin-binding domain binds F-actin in two different modes: implications for the spectrin superfamily of proteins. J. Cell Biol. 157, 243–251.PubMedCrossRefGoogle Scholar
  43. Galkin, V.E., Orlova, A., VanLoock, M.S., and Egelman, E.H. (2003). Do the utrophin tandem calponin homology domains bind Factin in a compact or extended conformation? J. Mol. Biol. 331, 967–972.PubMedCrossRefGoogle Scholar
  44. Gallop, J.L., Jao, C.C., Kent, H.M., Butler, P.J., Evans, P.R., Langen, R., and McMahon, H.T. (2006). Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25, 2898–2910.PubMedCrossRefGoogle Scholar
  45. Garcia-Alvarez, B., Bobkov, A., Sonnenberg, A., and de Pereda, J.M. (2003). Structural and functional analysis of the actin binding domain of plectin suggests alternative mechanisms for binding to F-actin and integrin beta4. Structure 11, 615–625.PubMedCrossRefGoogle Scholar
  46. Gimona, M., Djinovic-Carugo, K., Kranewitter, W.J., and Winder, S.J. (2002). Functional plasticity of CH domains. FEBS Lett. 513, 98–106.PubMedCrossRefGoogle Scholar
  47. Gimona, M., and Winder, S.J. (1998). Single calponin homology domains are not actin-binding domains. Curr. Biol. 8, R674–675.PubMedCrossRefGoogle Scholar
  48. Goldsmith, S.C., Pokala, N., Shen, W., Fedorov, A.A., Matsudaira, P., and Almo, S.C. (1997). The structure of an actin-crosslinking domain from human fimbrin. Nat. Struct. Biol. 4, 708–712.PubMedCrossRefGoogle Scholar
  49. Goode, B.L., and Eck, M.J. (2007). Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76, 593–627.PubMedCrossRefGoogle Scholar
  50. Govind, S., Kozma, R., Monfries, C., Lim, L., and Ahmed, S. (2001). Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J. Cell Biol. 152, 579–594.PubMedCrossRefGoogle Scholar
  51. Graceffa, P., and Dominguez, R. (2003). Crystal structure of monomeric actin in the ATP state. Structural basis of nucleotide-dependent actin dynamics. J. Biol. Chem. 278, 34172–34180.PubMedCrossRefGoogle Scholar
  52. Grintsevich, E.E., Benchaar, S.A., Warshaviak, D., Boontheung, P., Halgand, F., Whitelegge, J.P., Faull, K.F., Loo, R.R., Sept, D., Loo, J.A., et al. (2008). Mapping the cofilin binding site on yeast G-actin by chemical cross-linking. J. Mol. Biol. 377, 395–409.PubMedCrossRefGoogle Scholar
  53. Guan, J.Q., Vorobiev, S., Almo, S.C., and Chance, M.R. (2002). Mapping the G-actin binding surface of cofilin using synchrotron protein footprinting. Biochemistry 41, 5765–5775.PubMedCrossRefGoogle Scholar
  54. Habermann, B. (2004). The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250–255.PubMedCrossRefGoogle Scholar
  55. Hall, A. (1994). Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10, 31–54.PubMedCrossRefGoogle Scholar
  56. Hanein, D., Volkmann, N., Goldsmith, S., Michon, A.M., Lehman, W., Craig, R., DeRosier, D., Almo, S., and Matsudaira, P. (1998). An atomic model of fimbrin binding to F-actin and its implications for filament crosslinking and regulation. Nat. Struct. Biol. 5, 787–792.PubMedCrossRefGoogle Scholar
  57. Helfer, E., Nevalainen, E.M., Naumanen, P., Romero, S., Didry, D., Pantaloni, D., Lappalainen, P., and Carlier, M.F. (2006). Mammalian twinfilin sequesters ADP-G-actin and caps filament barbed ends: implications in motility. EMBO J. 25, 1184–1195.PubMedCrossRefGoogle Scholar
  58. Henne, W.M., Kent, H.M., Ford, M.G., Hegde, B.G., Daumke, O., Butler, P.J., Mittal, R., Langen, R., Evans, P.R., and McMahon, H.T. (2007). Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839–852.PubMedCrossRefGoogle Scholar
  59. Hertzog, M., van Heijenoort, C., Didry, D., Gaudier, M., Coutant, J., Gigant, B., Didelot, G., Preat, T., Knossow, M., Guittet, E., et al. (2004). The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117, 611–623.PubMedCrossRefGoogle Scholar
  60. Ho, H.Y., Rohatgi, R., Lebensohn, A.M., Le, M., Li, J., Gygi, S.P., and Kirschner, M.W. (2004). Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118, 203–216.PubMedCrossRefGoogle Scholar
  61. Holmes, K.C., Popp, D., Gebhard, W., and Kabsch, W. (1990). Atomic model of the actin filament. Nature 347, 44–49.PubMedCrossRefGoogle Scholar
  62. Huang, K.Y., Lai, M.W., Lee, W.I., and Huang, Y.C. (2008). Fatal cytomegalovirus gastrointestinal disease in an infant with Wiskott-Aldrich syndrome. J. Formos. Med. Assoc. 107, 64–67.PubMedCrossRefGoogle Scholar
  63. Hussey, P.J., Ketelaar, T., and Deeks, M.J. (2006). Control of the actin cytoskeleton in plant cell growth. Annu. Rev. Plant Biol. 57, 109–125.PubMedCrossRefGoogle Scholar
  64. Itoh, T., and De Camilli, P. (2006). BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897–912.PubMedGoogle Scholar
  65. Itoh, G., and Yumura, S. (2007). A novel mitosis-specific dynamic actin structure in Dictyostelium cells. J. Cell Sci. 120, 4302–4309.PubMedCrossRefGoogle Scholar
  66. Janmey, P.A., Stossel, T.P., and Lind, S.E. (1986). Sequential binding of actin monomers to plasma gelsolin and its inhibition by vitamin D-binding protein. Biochem. Biophys. Res. Commun. 136, 72–79.PubMedCrossRefGoogle Scholar
  67. Kaksonen, M., Toret, C.P., and Drubin, D.G. (2006). Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7, 404–414.PubMedCrossRefGoogle Scholar
  68. Kamioka, Y., Fukuhara, S., Sawa, H., Nagashima, K., Masuda, M., Matsuda, M., and Mochizuki, N. (2004). A novel dynamin-associating molecule, formin-binding protein 17, induces tubular membrane invaginations and participates in endocytosis. J. Biol. Chem. 279, 40091–40099.PubMedCrossRefGoogle Scholar
  69. Keep, N.H., Winder, S.J., Moores, C.A., Walke, S., Norwood, F.L., and Kendrick-Jones, J. (1999). Crystal structure of the actin-binding region of utrophin reveals a head-to-tail dimer. Structure 7, 1539–1546.PubMedCrossRefGoogle Scholar
  70. Kennedy, S.P., Warren, S.L., Forget, B.G., and Morrow, J.S. (1991). Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid beta-spectrin. J. Cell Biol. 115, 267–277.PubMedCrossRefGoogle Scholar
  71. Kessels, M.M., and Qualmann, B. (2004). The syndapin protein family: linking membrane trafficking with the cytoskeleton. J. Cell Sci. 117, 3077–3086.PubMedCrossRefGoogle Scholar
  72. Klein, M.G., Shi, W., Ramagopal, U., Tseng, Y., Wirtz, D., Kovar, D.R., Staiger, C.J., and Almo, S.C. (2004). Structure of the actin crosslinking core of fimbrin. Structure 12, 999–1013.PubMedCrossRefGoogle Scholar
  73. Knight, B., Laukaitis, C., Akhtar, N., Hotchin, N.A., Edlund, M., and Horwitz, A.R. (2000). Visualizing muscle cell migration in situ. Curr. Biol. 10, 576–585.PubMedCrossRefGoogle Scholar
  74. Kovar, D.R., Harris, E.S., Mahaffy, R., Higgs, H.N., and Pollard, T.D. (2006). Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124, 423–435.PubMedCrossRefGoogle Scholar
  75. Kozma, R., Ahmed, S., Best, A., and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15, 1942–1952.PubMedGoogle Scholar
  76. Krause, M., Dent, E.W., Bear, J.E., Loureiro, J.J., and Gertler, F.B. (2003). Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541–564.PubMedCrossRefGoogle Scholar
  77. Krause, M., Leslie, J.D., Stewart, M., Lafuente, E.M., Valderrama, F., Jagannathan, R., Strasser, G.A., Rubinson, D.A., Liu, H., Way, M., et al. (2004). Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571–583.PubMedCrossRefGoogle Scholar
  78. Krugmann, S., Jordens, I., Gevaert, K., Driessens, M., Vandekerckhove, J., and Hall, A. (2001). Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645–1655.PubMedCrossRefGoogle Scholar
  79. Kuhnel, K., Jarchau, T., Wolf, E., Schlichting, I., Walter, U., Wittinghofer, A., and Strelkov, S.V. (2004). The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat. Proc. Natl. Acad. Sci. USA 101, 17027–17032.PubMedCrossRefGoogle Scholar
  80. Lappalainen, P., Fedorov, E.V., Fedorov, A.A., Almo, S.C., and Drubin, D.G. (1997). Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J. 16, 5520–5530.PubMedCrossRefGoogle Scholar
  81. Lappalainen, P., Kessels, M.M., Cope, M.J., and Drubin, D.G. (1998). The ADF homology (ADF-H) domain: a highly exploited actin-binding module. Mol. Biol. Cell 9, 1951–1959.PubMedGoogle Scholar
  82. Lee, S.H., Kerff, F., Chereau, D., Ferron, F., Klug, A., and Dominguez, R. (2007). Structural basis for the actin-binding function of missingin-metastasis. Structure 15, 145–155.PubMedCrossRefGoogle Scholar
  83. Lee, S.H., Weins, A., Hayes, D.B., Pollak, M.R., and Dominguez, R. (2008). Crystal structure of the actin-binding domain of alphaactinin-4 Lys255Glu mutant implicated in focal segmental glomerulosclerosis. J. Mol. Biol. 376, 317–324.PubMedCrossRefGoogle Scholar
  84. Lehman, W., Craig, R., Kendrick-Jones, J., and Sutherland-Smith, A.J. (2004). An open or closed case for the conformation of calponin homology domains on F-actin? J. Muscle Res. Cell Motil. 25, 351–358.PubMedCrossRefGoogle Scholar
  85. Li, F., and Higgs, H.N. (2003). The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 13, 1335–1340.PubMedCrossRefGoogle Scholar
  86. Liu, Y., and Eisenberg, D. (2002). 3D domain swapping: as domains continue to swap. Protein Sci. 11, 1285–1299.PubMedCrossRefGoogle Scholar
  87. Liverman, A.D., Cheng, H.C., Trosky, J.E., Leung, D.W., Yarbrough, M.L., Burdette, D.L., Rosen, M.K., and Orth, K. (2007). Arp2/3-independent assembly of actin by Vibrio type III effector VopL. Proc. Natl. Acad. Sci. USA 104, 17117–17122.PubMedCrossRefGoogle Scholar
  88. Lu, Y., and Settleman, J. (1999). The role of rho family GTPases in development: lessons from Drosophila melanogaster. Mol. Cell Biol. Res. Commun. 1, 87–94.PubMedCrossRefGoogle Scholar
  89. Lundberg, S., Bjork, J., Lofvenberg, L., and Backman, L. (1995). Cloning, expression and characterization of two putative calcium-binding sites in human non-erythroid alpha-spectrin. Eur. J. Biochem. 230, 658–665.PubMedCrossRefGoogle Scholar
  90. Luo, L., Jan, L.Y., and Jan, Y.N. (1997). Rho family GTP-binding proteins in growth cone signalling. Curr. Opin. Neurobiol. 7, 81–86.PubMedCrossRefGoogle Scholar
  91. Mabuchi, I., Hamaguchi, Y., Fujimoto, H., Morii, N., Mishima, M., and Narumiya, S. (1993). A rho-like protein is involved in the organisation of the contractile ring in dividing sand dollar eggs. Zygote 1, 325–331.PubMedCrossRefGoogle Scholar
  92. Machesky, L.M., and Gould, K.L. (1999). The Arp2/3 complex: a multifunctional actin organizer. Curr. Opin. Cell Biol. 11, 117–121.PubMedCrossRefGoogle Scholar
  93. Machesky, L.M., and Insall, R.H. (1998). Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347–1356.PubMedCrossRefGoogle Scholar
  94. Machesky, L.M., Atkinson, S.J., Ampe, C., Vandekerckhove, J., and Pollard, T.D. (1994). Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J. Cell Biol. 127, 107–115.PubMedCrossRefGoogle Scholar
  95. Machesky, L.M., Mullins, R.D., Higgs, H.N., Kaiser, D.A., Blanchoin, L., May, R.C., Hall, M.E., and Pollard, T.D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96, 3739–3744.PubMedCrossRefGoogle Scholar
  96. Machner, M.P., Urbanke, C., Barzik, M., Otten, S., Sechi, A.S., Wehland, J., and Heinz, D.W. (2001). ActA from Listeria monocytogenes can interact with up to four Ena/VASP homology 1 domains simultaneously. J. Biol. Chem. 276, 40096–40103.PubMedCrossRefGoogle Scholar
  97. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., and Narumiya, S. (1999). Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285, 895–898.PubMedCrossRefGoogle Scholar
  98. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., and Mochizuki, N. (2006). Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25, 2889–2897.PubMedCrossRefGoogle Scholar
  99. Mattila, P.K., and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446–454.PubMedCrossRefGoogle Scholar
  100. Mattila, P.K., Pykalainen, A., Saarikangas, J., Paavilainen, V.O., Vihinen, H., Jokitalo, E., and Lappalainen, P. (2007). Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176, 953–964.PubMedCrossRefGoogle Scholar
  101. McGough, A., Way, M., and DeRosier, D. (1994). Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis. J. Cell Biol. 126, 433–443.PubMedCrossRefGoogle Scholar
  102. McGough, A.M., Staiger, C.J., Min, J.K., and Simonetti, K.D. (2003). The gelsolin family of actin regulatory proteins: modular structures, versatile functions. FEBS Lett. 552, 75–81.PubMedCrossRefGoogle Scholar
  103. McLaughlin, P.J., Gooch, J.T., Mannherz, H.G., and Weeds, A.G. (1993). Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature 364, 685–692.PubMedCrossRefGoogle Scholar
  104. McMahon, H.T., and Gallop, J.L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590–596.PubMedCrossRefGoogle Scholar
  105. Miki, H., Yamaguchi, H., Suetsugu, S., and Takenawa, T. (2000). IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732–735.PubMedCrossRefGoogle Scholar
  106. Millard, T.H., Bompard, G., Heung, M.Y., Dafforn, T.R., Scott, D.J., Machesky, L.M., and Futterer, K. (2005). Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J. 24, 240–250.PubMedCrossRefGoogle Scholar
  107. Moores, C.A., Keep, N.H., and Kendrick-Jones, J. (2000). Structure of the utrophin actin-binding domain bound to F-actin reveals binding by an induced fit mechanism. J. Mol. Biol. 297, 465–480.PubMedCrossRefGoogle Scholar
  108. Mullins, R.D., Heuser, J.A., and Pollard, T.D. (1998). 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.PubMedCrossRefGoogle Scholar
  109. Myers, K.A., He, Y., Hasaka, T.P., and Baas, P.W. (2006). Microtubule transport in the axon: re-thinking a potential role for the actin cytoskeleton. Neuroscientist 12, 107–118.PubMedCrossRefGoogle Scholar
  110. Nakagawa, H., Miki, H., Nozumi, M., Takenawa, T., Miyamoto, S., Wehland, J., and Small, J.V. (2003). IRSp53 is colocalised with WAVE2 at the tips of protruding lamellipodia and filopodia independently of Mena. J. Cell Sci. 116, 2577–2583.PubMedCrossRefGoogle Scholar
  111. Nobes, C.D., and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235–1244.PubMedCrossRefGoogle Scholar
  112. Noegel, A., Witke, W., and Schleicher, M. (1987). Calcium-sensitive non-muscle alpha-actinin contains EF-hand structures and highly conserved regions. FEBS Lett. 221, 391–396.PubMedCrossRefGoogle Scholar
  113. Norwood, F.L., Sutherland-Smith, A.J., Keep, N.H., and Kendrick-Jones, J. (2000). The structure of the N-terminal actin-binding domain of human dystrophin and how mutations in this domain may cause Duchenne or Becker muscular dystrophy. Structure 8, 481–491.PubMedCrossRefGoogle Scholar
  114. Oda, T., Iwasa, M., Aihara, T., Maeda, Y., and Narita, A. (2009). The nature of the globular- to fibrous-actin transition. Nature 457, 441–445.PubMedCrossRefGoogle Scholar
  115. Ojala, P.J., Paavilainen, V.O., Vartiainen, M.K., Tuma, R., Weeds, A.G., and Lappalainen, P. (2002). The two ADF-H domains of twinfilin play functionally distinct roles in interactions with actin monomers. Mol. Biol. Cell 13, 3811–3821.PubMedCrossRefGoogle Scholar
  116. Otomo, T., Tomchick, D.R., Otomo, C., Panchal, S.C., Machius, M., and Rosen, M.K. (2005). Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 433, 488–494.PubMedCrossRefGoogle Scholar
  117. Otterbein, L.R., Graceffa, P., and Dominguez, R. (2001). The crystal structure of uncomplexed actin in the ADP state. Science 293, 708–711.PubMedCrossRefGoogle Scholar
  118. Otterbein, L.R., Cosio, C., Graceffa, P., and Dominguez, R. (2002). Crystal structures of the vitamin D-binding protein and its complex with actin: structural basis of the actin-scavenger system. Proc. Natl. Acad. Sci. USA 99, 8003–8008.PubMedCrossRefGoogle Scholar
  119. Otto, J.J. (1994). Actin-bundling proteins. Curr. Opin. Cell Biol. 6, 105–109.PubMedCrossRefGoogle Scholar
  120. Paavilainen, V.O., Merckel, M.C., Falck, S., Ojala, P.J., Pohl, E., Wilmanns, M., and Lappalainen, P. (2002). Structural conservation between the actin monomer-binding sites of twinfilin and actin-depolymerizing factor (ADF)/cofilin. J. Biol. Chem. 277, 43089–43095.PubMedCrossRefGoogle Scholar
  121. Paavilainen, V.O., Oksanen, E., Goldman, A., and Lappalainen, P. (2008). Structure of the actin-depolymerizing factor homology domain in complex with actin. J. Cell Biol. 182, 51–59.PubMedCrossRefGoogle Scholar
  122. Pascual, J., Pfuhl, M., Walther, D., Saraste, M., and Nilges, M. (1997). Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil. J. Mol. Biol. 273, 740–751.PubMedCrossRefGoogle Scholar
  123. Pasic, L., Kotova, T., and Schafer, D.A. (2008). Ena/VASP proteins capture actin filament barbed ends. J. Biol. Chem. 283, 9814–9819.PubMedCrossRefGoogle Scholar
  124. Paunola, E., Mattila, P.K., and Lappalainen, P. (2002). WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett. 513, 92–97.PubMedCrossRefGoogle Scholar
  125. Peng, J., Wallar, B.J., Flanders, A., Swiatek, P.J., and Alberts, A.S. (2003). 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.PubMedCrossRefGoogle Scholar
  126. Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J., Evans, P.R., and McMahon, H.T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499.PubMedCrossRefGoogle Scholar
  127. Pollard, T.D., and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465.PubMedCrossRefGoogle Scholar
  128. Pollard, T.D., Blanchoin, L., and Mullins, R.D. (2000). Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545–576.PubMedCrossRefGoogle Scholar
  129. Prehoda, K.E., Scott, J.A., Mullins, R.D., and Lim, W.A. (2000). Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801–806.PubMedCrossRefGoogle Scholar
  130. Prokopenko, S.N., Saint, R., and Bellen, H.J. (2000). Untying the Gordian knot of cytokinesis. Role of small G proteins and their regulators. J. Cell Biol. 148, 843–848.PubMedCrossRefGoogle Scholar
  131. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A., and Boone, C. (2002). Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615.PubMedCrossRefGoogle Scholar
  132. Puppo, A., Chun, J.T., Gragnaniello, G., Garante, E., and Santella, L. (2008). Alteration of the cortical actin cytoskeleton deregulates Ca2+ signaling, monospermic fertilization, and sperm entry. PLoS ONE 3, e3588.PubMedCrossRefGoogle Scholar
  133. Pylypenko, O., Lundmark, R., Rasmuson, E., Carlsson, S.R., and Rak, A. (2007). The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J. 26, 4788–4800.PubMedCrossRefGoogle Scholar
  134. Quinlan, M.E., Heuser, J.E., Kerkhoff, E., and Mullins, R.D. (2005). Drosophila Spire is an actin nucleation factor. Nature 433, 382–388.PubMedCrossRefGoogle Scholar
  135. Rafelski, S.M., and Theriot, J.A. (2004). Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73, 209–239.PubMedCrossRefGoogle Scholar
  136. Raftopoulou, M., and Hall, A. (2004). Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23–32.PubMedCrossRefGoogle Scholar
  137. Rando, T.A. (2001). The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24, 1575–1594.PubMedCrossRefGoogle Scholar
  138. Renault, L., Bugyi, B., and Carlier, M.F. (2008). Spire and Cordonbleu: multifunctional regulators of actin dynamics. Trends Cell Biol. 18, 494–504.PubMedCrossRefGoogle Scholar
  139. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389–399.PubMedCrossRefGoogle Scholar
  140. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D., and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401–410.PubMedCrossRefGoogle Scholar
  141. Robinson, R.C., Turbedsky, K., Kaiser, D.A., Marchand, J.B., Higgs, H.N., Choe, S., and Pollard, T.D. (2001). Crystal structure of Arp2/3 complex. Science 294, 1679–1684.PubMedCrossRefGoogle Scholar
  142. Rybakova, I.N., Patel, J.R., Davies, K.E., Yurchenco, P.D., and Ervasti, J.M. (2002). Utrophin binds laterally along actin filaments and can couple costameric actin with sarcolemma when overexpressed in dystrophin-deficient muscle. Mol. Biol. Cell 13, 1512–1521.PubMedCrossRefGoogle Scholar
  143. Saarikangas, J., Zhao, H., Pykalainen, A., Laurinmaki, P., Mattila, P.K., Kinnunen, P.K., Butcher, S.J., and Lappalainen, P. (2009). Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr. Biol. 19, 95–107.PubMedCrossRefGoogle Scholar
  144. Salazar, M.A., Kwiatkowski, A.V., Pellegrini, L., Cestra, G., Butler, M.H., Rossman, K.L., Serna, D.M., Sondek, J., Gertler, F.B., and De Camilli, P. (2003). Tuba, a novel protein containing bin/amphiphysin/Rvs and Dbl homology domains, links dynamin to regulation of the actin cytoskeleton. J. Biol. Chem. 278, 49031–49043.PubMedCrossRefGoogle Scholar
  145. Schutt, C.E., Myslik, J.C., Rozycki, M.D., Goonesekere, N.C., and Lindberg, U. (1993). The structure of crystalline profilin-betaactin. Nature 365, 810–816.PubMedCrossRefGoogle Scholar
  146. Scita, G., Confalonieri, S., Lappalainen, P., and Suetsugu, S. (2008). IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol. 18, 52–60.PubMedCrossRefGoogle Scholar
  147. Scoville, D., Stamm, J.D., Toledo-Warshaviak, D., Altenbach, C., Phillips, M., Shvetsov, A., Rubenstein, P.A., Hubbell, W.L., and Reisler, E. (2006). Hydrophobic loop dynamics and actin filament stability. Biochemistry 45, 13576–13584.PubMedCrossRefGoogle Scholar
  148. Sellers, J.R. (2000). Myosins: a diverse superfamily. Biochim. Biophys. Acta 1496, 3–22.PubMedCrossRefGoogle Scholar
  149. Settleman, J. (1999). Rho GTPases in development. Prog. Mol. Subcell Biol. 22, 201–229.PubMedGoogle Scholar
  150. Sevcik, J., Urbanikova, L., Kost’an, J., Janda, L., and Wiche, G. (2004). Actin-binding domain of mouse plectin. Crystal structure and binding to vimentin. Eur. J. Biochem. 271, 1873–1884.PubMedCrossRefGoogle Scholar
  151. Shafer, A., and Voss, J. (2004). The use of spin-labeled ligands as biophysical probes to report real-time endocytosis of G proteincoupled receptors in living cells. Sci. STKE 2004, pl9.Google Scholar
  152. Shimada, A., Niwa, H., Tsujita, K., Suetsugu, S., Nitta, K., Hanawa-Suetsugu, K., Akasaka, R., Nishino, Y., Toyama, M., Chen, L., et al. (2007). Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761–772.PubMedCrossRefGoogle Scholar
  153. Suetsugu, S., Murayama, K., Sakamoto, A., Hanawa-Suetsugu, K., Seto, A., Oikawa, T., Mishima, C., Shirouzu, M., Takenawa, T., and Yokoyama, S. (2006). The RAC binding domain/IRSp53-MIM homology domain of IRSp53 induces RAC-dependent membrane deformation. J. Biol. Chem. 281, 35347–35358.PubMedCrossRefGoogle Scholar
  154. Sutherland-Smith, A.J., Moores, C.A., Norwood, F.L., Hatch, V., Craig, R., Kendrick-Jones, J., and Lehman, W. (2003). An atomic model for actin binding by the CH domains and spectrin-repeat modules of utrophin and dystrophin. J. Mol. Biol. 329, 15–33.PubMedCrossRefGoogle Scholar
  155. Takenawa, T., and Suetsugu, S. (2007). The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37–48.PubMedCrossRefGoogle Scholar
  156. Tam, V.C., Serruto, D., Dziejman, M., Brieher, W., and Mekalanos, J.J. (2007). A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1, 95–107.PubMedCrossRefGoogle Scholar
  157. Tarricone, C., Xiao, B., Justin, N., Walker, P.A., Rittinger, K., Gamblin, S.J., and Smerdon, S.J. (2001). The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 411, 215–219.PubMedCrossRefGoogle Scholar
  158. Vartiainen, M.K., Guettler, S., Larijani, B., and Treisman, R. (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749–1752.PubMedCrossRefGoogle Scholar
  159. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Saito, Y., Nakao, K., Jockusch, B.M., and Narumiya, S. (1997). 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.PubMedCrossRefGoogle Scholar
  160. Weissenhorn, W. (2005). Crystal structure of the endophilin-A1 BAR domain. J. Mol. Biol. 351, 653–661.PubMedCrossRefGoogle Scholar
  161. Winder, S.J., Gibson, T.J., and Kendrick-Jones, J. (1995). Dystrophin and utrophin: the missing links! FEBS Lett. 369, 27–33.PubMedCrossRefGoogle Scholar
  162. Xu, Y., Moseley, J.B., Sagot, I., Poy, F., Pellman, D., Goode, B.L., and Eck, M.J. (2004). Crystal structures of a Formin Homology-2 domain reveal a tethered dimer architecture. Cell 116, 711–723.PubMedCrossRefGoogle Scholar
  163. Yamaguchi, H., and Condeelis, J. (2007). Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773, 642–652.PubMedCrossRefGoogle Scholar
  164. Yamagishi, A., Masuda, M., Ohki, T., Onishi, H., and Mochizuki, N. (2004). A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J. Biol. Chem. 279, 14929–14936.PubMedCrossRefGoogle Scholar
  165. Yang, N., Higuchi, O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E., and Mizuno, K. (1998). Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393, 809–812.PubMedCrossRefGoogle Scholar
  166. Yarmola, E.G., Parikh, S., and Bubb, M.R. (2001). Formation and implications of a ternary complex of profilin, thymosin beta 4, and actin. J. Biol. Chem. 276, 45555–45563.PubMedCrossRefGoogle Scholar
  167. Yarmola, E.G., Klimenko, E.S., Fujita, G., and Bubb, M.R. (2007). Thymosin beta4: actin regulation and more. Ann. N Y Acad. Sci. 1112, 76–85.PubMedCrossRefGoogle Scholar
  168. Ylanne, J., Scheffzek, K., Young, P., and Saraste, M. (2001a). Crystal structure of the alpha-actinin rod reveals an extensive torsional twist. Structure 9, 597–604.PubMedCrossRefGoogle Scholar
  169. Ylanne, J., Scheffzek, K., Young, P., and Saraste, M. (2001b). Crystal structure of the alpha-actinin rod: four spectrin repeats forming a thight dimer. Cell Mol. Biol. Lett. 6, 234.PubMedGoogle Scholar
  170. Zhu, G., Chen, J., Liu, J., Brunzelle, J.S., Huang, B., Wakeham, N., Terzyan, S., Li, X., Rao, Z., Li, G., et al. (2007). Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J. 26, 3484–3493.PubMedCrossRefGoogle Scholar
  171. Zigmond, S.H. (2004a). Beginning and ending an actin filament: control at the barbed end. Curr. Top Dev. Biol. 63, 145–188.PubMedCrossRefGoogle Scholar
  172. Zigmond, S.H. (2004b). Formin-induced nucleation of actin filaments. Curr. Opin. Cell Biol. 16, 99–105.PubMedCrossRefGoogle Scholar

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© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2010

Authors and Affiliations

  1. 1.Department of Cellular and Molecular MedicineChosun University School of MedicineGwangjuKorea
  2. 2.Research Center for Resistant CellsChosun University School of MedicineGwangjuKorea
  3. 3.Department of PhysiologyUniversity of Pennsylvania School of MedicinePhiladelphiaUSA

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