Steering cell migration: lamellipodium dynamics and the regulation of directional persistence (original) (raw)

• Ridley, A. J. Life at the leading edge. Cell 145, 1012–1022 (2011).
  CAS PubMed Google Scholar
• Campellone, K. G. & Welch, M. D. A nucleator arms race: cellular control of actin assembly. Nature Rev. Mol. Cell Biol. 11, 237–251 (2010).
  CAS Google Scholar
• Insall, R. H. & Machesky, L. M. Actin dynamics at the leading edge: from simple machinery to complex networks. Dev. Cell 17, 310–322 (2009).
  CAS PubMed Google Scholar
• Loisel, T. P., Boujemaa, R., Pantaloni, D. & Carlier, M. F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613–616 (1999).
  CAS PubMed Google Scholar
• Rorth, P. Whence directionality: guidance mechanisms in solitary and collective cell migration. Dev. Cell 20, 9–18 (2011).
  CAS PubMed Google Scholar
• Stramer, B. et al. Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo. J. Cell Biol. 189, 681–689 (2010).
  CAS PubMed PubMed Central Google Scholar
• Moore, R. et al. Par3 controls neural crest migration by promoting microtubule catastrophe during contact inhibition of locomotion. Development 140, 4763–4775 (2013).
  CAS PubMed PubMed Central Google Scholar
• Teddy, J. M. & Kulesa, P. M. In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 131, 6141–6151 (2004).
  CAS PubMed Google Scholar
• Cooper, J. A. Cell biology in neuroscience: mechanisms of cell migration in the nervous system. J. Cell Biol. 202, 725–734 (2013).
  CAS PubMed PubMed Central Google Scholar
• Petrie, R. J., Doyle, A. D. & Yamada, K. M. Random versus directionally persistent cell migration. Nature Rev. Mol. Cell Biol. 10, 538–549 (2009).
  CAS Google Scholar
• Suraneni, P. et al. The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J. Cell Biol. 197, 239–251 (2012).
  CAS PubMed PubMed Central Google Scholar
• Krause, M. et al. Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571–583 (2004).
  CAS PubMed Google Scholar
• Wu, C. et al. Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 148, 973–987 (2012). Together with reference 11, this paper shows that the ARP2/3 complex is required for lamellipodium formation. These papers show that ARP2/3- deficient cells are defective in persistent cell migration (reference 11) and display highly reduced random cell migration and haptotaxis (reference 13).
  CAS PubMed PubMed Central Google Scholar
• Law, A. L. et al. Lamellipodin and the Scar/WAVE complex cooperate to promote cell migration in vivo. J. Cell Biol. 203, 673–689 (2013). This paper shows that lamellipodin directly interacts with the WAVE complex downstream of activated RAC, thereby controlling lamellipodium formation and the speed and persistence of cell migration in vitro , and both mesenchymal and epithelial collective cell migration in vivo.
  CAS PubMed PubMed Central Google Scholar
• Nurnberg, A., Kitzing, T. & Grosse, R. Nucleating actin for invasion. Nature Rev. Cancer 11, 177–187 (2011).
  Google Scholar
• Hoshino, D., Branch, K. M. & Weaver, A. M. Signaling inputs to invadopodia and podosomes. J. Cell Sci. 126, 2979–2989 (2013).
  CAS PubMed PubMed Central Google Scholar
• Paluch, E. K. & Raz, E. The role and regulation of blebs in cell migration. Curr. Opin. Cell Biol. 25, 582–590 (2013).
  CAS PubMed PubMed Central Google Scholar
• Poincloux, R. et al. Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc. Natl Acad. Sci. USA 108, 1943–1948 (2011).
  CAS PubMed Google Scholar
• Panopoulos, A., Howell, M., Fotedar, R. & Margolis, R. L. Glioblastoma motility occurs in the absence of actin polymer. Mol. Biol. Cell 22, 2212–2220 (2011).
  CAS PubMed PubMed Central Google Scholar
• Cooper, J. A. & Sept, D. New insights into mechanism and regulation of actin capping protein. Int. Rev. Cell Mol. Biol. 267, 183–206 (2008).
  CAS PubMed PubMed Central Google Scholar
• Romero, S. et al. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119, 419–429 (2004).
  CAS PubMed Google Scholar
• Bear, J. E. et al. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509–521 (2002).
  CAS PubMed Google Scholar
• Barzik, M. et al. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280, 28653–28662 (2005).
  CAS PubMed PubMed Central Google Scholar
• Pasic, L., Kotova, T. & Schafer, D. A. Ena/VASP proteins capture actin filament barbed ends. J. Biol. Chem. 283, 9814–9819 (2008).
  CAS PubMed PubMed Central Google Scholar
• Breitsprecher, D. et al. Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J. 30, 456–467 (2011).
  CAS PubMed PubMed Central Google Scholar
• Breitsprecher, D. et al. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943–2954 (2008).
  CAS PubMed PubMed Central Google Scholar
• Hansen, S. D. & Mullins, R. D. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J. Cell Biol. 191, 571–584 (2010).
  CAS PubMed PubMed Central Google Scholar
• Block, J. et al. FMNL2 drives actin-based protrusion and migration downstream of Cdc42. Curr. Biol. 22, 1005–1012 (2012). This study provides good evidence that FMNL2 is the first formin to robustly localize to the edge of lamellipodia as an N -myristoylated protein downstream of CDC42. It also shows that FMNL2 predominantly elongates actin filaments, thereby increasing cell migration speed.
  CAS PubMed PubMed Central Google Scholar
• Rottner, K., Behrendt, B., Small, J. V. & Wehland, J. VASP dynamics during lamellipodia protrusion. Nature Cell Biol. 1, 321–322 (1999).
  CAS PubMed Google Scholar
• Lai, F. P. et al. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J. 27, 982–992 (2008). A seminal paper showing the molecular behaviour of the major players involved in lamellipodium formation.
  CAS PubMed PubMed Central Google Scholar
• Yang, Q., Zhang, X. F., Pollard, T. D. & Forscher, P. Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow. J. Cell Biol. 197, 939–956 (2012).
  CAS PubMed PubMed Central Google Scholar
• Giannone, G., Mege, R. M. & Thoumine, O. Multi-level molecular clutches in motile cell processes. Trends Cell Biol. 19, 475–486 (2009).
  CAS PubMed Google Scholar
• Rottner, K., Hanisch, J. & Campellone, K. G. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol. 20, 650–661 (2010).
  CAS PubMed Google Scholar
• Veltman, D. M., King, J. S., Machesky, L. M. & Insall, R. H. SCAR knockouts in Dictyostelium: WASP assumes SCAR's position and upstream regulators in pseudopods. J. Cell Biol. 198, 501–508 (2012).
  CAS PubMed PubMed Central Google Scholar
• Tang, H. et al. Loss of Scar/WAVE complex promotes N-WASP- and FAK-dependent invasion. Curr. Biol. 23, 107–117 (2013).
  CAS PubMed Google Scholar
• Derivery, E. & Gautreau, A. Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. Bioessays 32, 119–131 (2010).
  CAS PubMed Google Scholar
• Eden, S., Rohatgi, R., Podtelejnikov, A. V., Mann, M. & Kirschner, M. W. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418, 790–793 (2002).
  CAS PubMed Google Scholar
• Gautreau, A. et al. Purification and architecture of the ubiquitous Wave complex. Proc. Natl Acad. Sci. USA 101, 4379–4383 (2004).
  CAS PubMed Google Scholar
• Innocenti, M. et al. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nature Cell Biol. 6, 319–327 (2004).
  CAS PubMed Google Scholar
• Hirao, N. et al. NESH (Abi-3) is present in the Abi/WAVE complex but does not promote c-Abl-mediated phosphorylation. FEBS Lett. 580, 6464–6470 (2006).
  CAS PubMed Google Scholar
• Stovold, C. F., Millard, T. H. & Machesky, L. M. Inclusion of Scar/WAVE3 in a similar complex to Scar/WAVE1 and 2. BMC Cell Biol. 6, 11 (2005).
  PubMed PubMed Central Google Scholar
• Derivery, E., Lombard, B., Loew, D. & Gautreau, A. The Wave complex is intrinsically inactive. Cell. Motil. Cytoskeleton 66, 777–790 (2009).
  CAS PubMed Google Scholar
• Ismail, A. M., Padrick, S. B., Chen, B., Umetani, J. & Rosen, M. K. The WAVE regulatory complex is inhibited. Nature Struct. Mol. Biol. 16, 561–563 (2009).
  CAS Google Scholar
• Chen, Z. et al. Structure and control of the actin regulatory WAVE complex. Nature 468, 533–538 (2010). This paper presents the crystal structure of the WAVE complex, revealing that the ARP2/3-activating WCA domain of WAVE is sequestered within the complex, explaining how the WAVE complex is autoinhibited. Site-directed mutagenesis showed that the WAVE complex may be activated by RAC and Tyr phosphorylation.
  CAS PubMed PubMed Central Google Scholar
• Steffen, A. et al. Rac function is crucial for cell migration but is not required for spreading and focal adhesion formation. J. Cell Sci. 126, 4572–4588 (2013).
  CAS PubMed PubMed Central Google Scholar
• Kobayashi, K. et al. p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J. Biol. Chem. 273, 291–295 (1998).
  CAS PubMed Google Scholar
• Lebensohn, A. M. & Kirschner, M. W. Activation of the WAVE complex by coincident signals controls actin assembly. Mol. Cell 36, 512–524 (2009). This paper describes in vitro reconstitution of activation of the WAVE complex using purified components. To obtain full activation, prenylated RAC, PtdIns(3,4,5)P 3 -containing liposomes and the phosphorylated WAVE complex were required.
  CAS PubMed PubMed Central Google Scholar
• Oikawa, T. et al. PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nature Cell Biol. 6, 420–426 (2004).
  CAS PubMed Google Scholar
• Padrick, S. B. et al. Hierarchical regulation of WASP/WAVE proteins. Mol. Cell 32, 426–438 (2008).
  CAS PubMed PubMed Central Google Scholar
• Padrick, S. B., Doolittle, L. K., Brautigam, C. A., King, D. S. & Rosen, M. K. Arp2/3 complex is bound and activated by two WASP proteins. Proc. Natl Acad. Sci. USA 108, E472–E479 (2011).
  CAS PubMed Google Scholar
• Ti, S. C., Jurgenson, C. T., Nolen, B. J. & Pollard, T. D. Structural and biochemical characterization of two binding sites for nucleation-promoting factor WASp-VCA on Arp2/3 complex. Proc. Natl Acad. Sci. USA 108, E463–E471 (2011).
  CAS PubMed Google Scholar
• Echarri, A., Lai, M. J., Robinson, M. R. & Pendergast, A. M. Abl interactor 1 (Abi-1) wave-binding and SNARE domains regulate its nucleocytoplasmic shuttling, lamellipodium localization, and wave-1 levels. Mol. Cell. Biol. 24, 4979–4993 (2004).
  CAS PubMed PubMed Central Google Scholar
• Fan, P. D., Cong, F. & Goff, S. P. Homo- and hetero-oligomerization of the c-Abl kinase and Abelson-interactor-1. Cancer Res. 63, 873–877 (2003).
  CAS PubMed Google Scholar
• Miki, H., Yamaguchi, H., Suetsugu, S. & Takenawa, T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732–735 (2000).
  CAS PubMed Google Scholar
• Disanza, A. et al. CDC42 switches IRSp53 from inhibition of actin growth to elongation by clustering of VASP. EMBO J. 32, 2735–2750 (2013).
  CAS PubMed PubMed Central Google Scholar
• Koronakis, V. et al. WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc. Natl Acad. Sci. USA 108, 14449–14454 (2011). This paper describes the cooperativity of active ARF proteins and active RAC for efficient WAVE complex activation in cell extracts. ARF proteins are activated downstream of PtdIns(3,4,5)P 3 in cell extracts. The requirement for ARF proteins specifically refers to ARF1, ARF5 or ARL1.
  CAS PubMed Google Scholar
• Schweitzer, J. K., Sedgwick, A. E. & D'Souza-Schorey, C. ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 22, 39–47 (2011).
  CAS PubMed Google Scholar
• Gillingham, A. K. & Munro, S. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23, 579–611 (2007).
  CAS PubMed Google Scholar
• Humphreys, D., Liu, T., Davidson, A. C., Hume, P. J. & Koronakis, V. The Drosophila Arf1 homologue Arf79F is essential for lamellipodium formation. J. Cell Sci. 125, 5630–5635 (2012).
  CAS PubMed PubMed Central Google Scholar
• Boulay, P. L., Cotton, M., Melancon, P. & Claing, A. ADP-ribosylation factor 1 controls the activation of the phosphatidylinositol 3-kinase pathway to regulate epidermal growth factor-dependent growth and migration of breast cancer cells. J. Biol. Chem. 283, 36425–36434 (2008).
  CAS PubMed PubMed Central Google Scholar
• Zhang, J. et al. Filamin A regulates neuronal migration through brefeldin A-inhibited guanine exchange factor 2-dependent Arf1 activation. J. Neurosci. 33, 15735–15746 (2013).
  CAS PubMed PubMed Central Google Scholar
• Humphreys, D., Davidson, A. C., Hume, P. J., Makin, L. E. & Koronakis, V. Arf6 coordinates actin assembly through the WAVE complex, a mechanism usurped by Salmonella to invade host cells. Proc. Natl Acad. Sci. USA 110, 16880–16885 (2013).
  CAS PubMed Google Scholar
• Lu, H. et al. Exo70 isoform switching upon epithelial-mesenchymal transition mediates cancer cell invasion. Dev. Cell 27, 560–573 (2013).
  CAS PubMed PubMed Central Google Scholar
• Liu, J. et al. Exo70 stimulates the Arp2/3 complex for lamellipodia formation and directional cell migration. Curr. Biol. 22, 1510–1515 (2012).
  CAS PubMed PubMed Central Google Scholar
• Zuo, X. et al. Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nature Cell Biol. 8, 1383–1388 (2006). This paper, together with reference 64, shows that EXO70, a component of the exocyst complex that is normally implicated in regulating exocytosis, binds to the ARP2/3 complex; this leads to increased interaction between WAVE2 and the ARP2/3 complex, thereby promoting actin filament branching, lamellipodium formation and the directional persistence of cell migration.
  CAS PubMed Google Scholar
• Baust, T., Czupalla, C., Krause, E., Bourel-Bonnet, L. & Hoflack, B. Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc. Natl Acad. Sci. USA 103, 3159–3164 (2006).
  CAS PubMed Google Scholar
• Anitei, M. et al. Protein complexes containing CYFIP/Sra/PIR121 coordinate Arf1 and Rac1 signalling during clathrin-AP-1-coated carrier biogenesis at the TGN. Nature Cell Biol. 12, 330–340 (2010).
  CAS PubMed Google Scholar
• Gautier, J. J. et al. Clathrin is required for Scar/Wave-mediated lamellipodium formation. J. Cell Sci. 124, 3414–3427 (2011).
  CAS PubMed Google Scholar
• Huang, C. H., Lin, T. Y., Pan, R. L. & Juang, J. L. The involvement of Abl and PTP61F in the regulation of Abi protein localization and stability and lamella formation in Drosophila S2 cells. J. Biol. Chem. 282, 32442–32452 (2007).
  CAS PubMed Google Scholar
• Leng, Y. et al. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl Acad. Sci. USA 102, 1098–1103 (2005).
  CAS PubMed Google Scholar
• Stuart, J. R., Gonzalez, F. H., Kawai, H. & Yuan, Z. M. c-Abl interacts with the WAVE2 signaling complex to induce membrane ruffling and cell spreading. J. Biol. Chem. 281, 31290–31297 (2006).
  CAS PubMed Google Scholar
• Sossey-Alaoui, K., Li, X. & Cowell, J. K. c-Abl-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration. J. Biol. Chem. 282, 26257–26265 (2007).
  CAS PubMed Google Scholar
• Fujita, A. et al. Imatinib mesylate (STI571)-induced cell edge translocation of kinase-active and kinase-defective Abelson kinase: requirements of myristoylation and src homology 3 domain. Mol. Pharmacol. 75, 75–84 (2009).
  CAS PubMed Google Scholar
• Westphal, R. S., Soderling, S. H., Alto, N. M., Langeberg, L. K. & Scott, J. D. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold. EMBO J. 19, 4589–4600 (2000).
  CAS PubMed PubMed Central Google Scholar
• Ardern, H. et al. Src-dependent phosphorylation of Scar1 promotes its association with the Arp2/3 complex. Cell. Motil. Cytoskeleton 63, 6–13 (2006).
  CAS PubMed Google Scholar
• Kim, Y. et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442, 814–817 (2006).
  CAS PubMed Google Scholar
• Miyamoto, Y., Yamauchi, J. & Tanoue, A. Cdk5 phosphorylation of WAVE2 regulates oligodendrocyte precursor cell migration through nonreceptor tyrosine kinase Fyn. J. Neurosci. 28, 8326–8337 (2008).
  CAS PubMed PubMed Central Google Scholar
• Soderling, S. H. et al. A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J. Neurosci. 27, 355–365 (2007).
  CAS PubMed PubMed Central Google Scholar
• Miki, H., Fukuda, M., Nishida, E. & Takenawa, T. Phosphorylation of WAVE downstream of mitogen-activated protein kinase signaling. J. Biol. Chem. 274, 27605–27609 (1999).
  CAS PubMed Google Scholar
• Nakanishi, O., Suetsugu, S., Yamazaki, D. & Takenawa, T. Effect of WAVE2 phosphorylation on activation of the Arp2/3 complex. J. Biochem. 141, 319–325 (2007).
  CAS PubMed Google Scholar
• Danson, C. M., Pocha, S. M., Bloomberg, G. B. & Cory, G. O. Phosphorylation of WAVE2 by MAP kinases regulates persistent cell migration and polarity. J. Cell Sci. 120, 4144–4154 (2007).
  CAS PubMed PubMed Central Google Scholar
• Mendoza, M. C. et al. ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex. Mol. Cell 41, 661–671 (2011).
  CAS PubMed PubMed Central Google Scholar
• Panchal, S. C., Kaiser, D. A., Torres, E., Pollard, T. D. & Rosen, M. K. A conserved amphipathic helix in WASP/Scar proteins is essential for activation of Arp2/3 complex. Nature Struct. Biol. 10, 591–598 (2003).
  CAS PubMed Google Scholar
• Pocha, S. M. & Cory, G. O. WAVE2 is regulated by multiple phosphorylation events within its VCA domain. Cell. Motil. Cytoskeleton 66, 36–47 (2009).
  CAS PubMed PubMed Central Google Scholar
• Ura, S. et al. Pseudopod growth and evolution during cell movement is controlled through SCAR/WAVE dephosphorylation. Curr. Biol. 22, 553–561 (2012).
  CAS PubMed PubMed Central Google Scholar
• Chen, B. et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156, 195–207 (2014).
  CAS PubMed PubMed Central Google Scholar
• Vehlow, A. et al. Endophilin, Lamellipodin, and Mena cooperate to regulate F-actin-dependent EGF-receptor endocytosis. EMBO J. 32, 2722–2734 (2013).
  CAS PubMed PubMed Central Google Scholar
• Rossman, K. L., Der, C. J. & Sondek, J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nature Rev. Mol. Cell Biol. 6, 167–180 (2005).
  CAS Google Scholar
• Rodriguez-Viciana, P., Sabatier, C. & McCormick, F. Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 24, 4943–4954 (2004).
  CAS PubMed PubMed Central Google Scholar
• 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 Google Scholar
• Achard, V. et al. A “primer”-based mechanism underlies branched actin filament network formation and motility. Curr. Biol. 20, 423–428 (2010). This paper reports the direct visualization of the absolute requirement of a primer filament in order to generate an ARP2/3-dependent branched actin network.
  CAS PubMed Google Scholar
• Ichetovkin, I., Grant, W. & Condeelis, J. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12, 79–84 (2002).
  CAS PubMed Google Scholar
• Chen, Q. & Pollard, T. D. Actin filament severing by cofilin dismantles actin patches and produces mother filaments for new patches. Curr. Biol. 23, 1154–1162 (2013).
  CAS PubMed PubMed Central Google Scholar
• Zuchero, J. B., Coutts, A. S., Quinlan, M. E., Thangue, N. B. & Mullins, R. D. p53-cofactor JMY is a multifunctional actin nucleation factor. Nature Cell Biol. 11, 451–459 (2009).
  CAS PubMed Google Scholar
• Firat-Karalar, E. N., Hsiue, P. P. & Welch, M. D. The actin nucleation factor JMY is a negative regulator of neuritogenesis. Mol. Biol. Cell 22, 4563–4574 (2011).
  CAS PubMed PubMed Central Google Scholar
• Coutts, A. S., Weston, L. & La Thangue, N. B. A transcription co-factor integrates cell adhesion and motility with the p53 response. Proc. Natl Acad. Sci. USA 106, 19872–19877 (2009).
  CAS PubMed Google Scholar
• Schluter, K. et al. JMY is involved in anterograde vesicle trafficking from the _trans_-Golgi network. Eur. J. Cell Biol. 93, 194–204 (2014).
  PubMed Google Scholar
• Campellone, K. G., Webb, N. J., Znameroski, E. A. & Welch, M. D. WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134, 148–161 (2008).
  CAS PubMed PubMed Central Google Scholar
• Wagner, A. R., Luan, Q., Liu, S. L. & Nolen, B. J. Dip1 defines a class of Arp2/3 complex activators that function without preformed actin filaments. Curr. Biol. 23, 1990–1998 (2013). This paper reports, for the first time, that some ARP2/3 activators, such as the orthologous proteins DIP1 and SPIN90, induce nucleation of linear actin filaments. Such activators may prime the ARP2/3 complex for the subsequent generation of branched actin networks.
  CAS PubMed PubMed Central Google Scholar
• Kim, D. J. et al. Interaction of SPIN90 with the Arp2/3 complex mediates lamellipodia and actin comet tail formation. J. Biol. Chem. 281, 617–625 (2006).
  CAS PubMed Google Scholar
• Fukuoka, M. et al. A novel neural Wiskott-Aldrich syndrome protein (N-WASP) binding protein, WISH, induces Arp2/3 complex activation independent of Cdc42. J. Cell Biol. 152, 471–482 (2001).
  CAS PubMed PubMed Central Google Scholar
• Fukumi-Tominaga, T. et al. DIP/WISH-deficient mice reveal Dia- and N-WASP-interacting protein as a regulator of cytoskeletal dynamics in embryonic fibroblasts. Genes Cells 14, 1197–1207 (2009).
  CAS PubMed Google Scholar
• Oh, H. et al. SPIN90 knockdown attenuates the formation and movement of endosomal vesicles in the early stages of epidermal growth factor receptor endocytosis. PLoS ONE 8, e82610 (2013).
  PubMed PubMed Central Google Scholar
• Kim, S. H. et al. Interaction of SPIN90 with syndapin is implicated in clathrin-mediated endocytic pathway in fibroblasts. Genes Cells 11, 1197–1211 (2006).
  CAS PubMed Google Scholar
• Basu, R. & Chang, F. Characterization of dip1p reveals a switch in Arp2/3-dependent actin assembly for fission yeast endocytosis. Curr. Biol. 21, 905–916 (2011).
  CAS PubMed PubMed Central Google Scholar
• Vinzenz, M. et al. Actin branching in the initiation and maintenance of lamellipodia. J. Cell Sci. 125, 2775–2785 (2012).
  CAS PubMed Google Scholar
• Wu, C. et al. Loss of Arp2/3 induces an NF-κB-dependent, nonautonomous effect on chemotactic signaling. J. Cell Biol. 203, 907–916 (2013).
  CAS PubMed PubMed Central Google Scholar
• Reinhard, M. et al. The 46/50 kDa phosphoprotein VASP purified from human platelets is a novel protein associated with actin filaments and focal contacts. EMBO J. 11, 2063–2070 (1992).
  CAS PubMed PubMed Central Google Scholar
• Gertler, F. B., Niebuhr, K., Reinhard, M., Wehland, J. & Soriano, P. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87, 227–239 (1996).
  CAS PubMed Google Scholar
• Chereau, D. & Dominguez, R. Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J. Struct. Biol. 155, 195–201 (2006).
  CAS PubMed Google Scholar
• Michael, M., Vehlow, A., Navarro, C. & Krause, M. c-Abl, Lamellipodin, and Ena/VASP proteins cooperate in dorsal ruffling of fibroblasts and axonal morphogenesis. Curr. Biol. 20, 783–791 (2010).
  CAS PubMed PubMed Central Google Scholar
• Skoble, J., Auerbuch, V., Goley, E. D., Welch, M. D. & Portnoy, D. A. Pivotal role of VASP in Arp2/3 complex-mediated actin nucleation, actin branch-formation, and Listeria monocytogenes motility. J. Cell Biol. 155, 89–100 (2001).
  CAS PubMed PubMed Central Google Scholar
• Philippar, U. et al. A Mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. Dev. Cell 15, 813–828 (2008).
  CAS PubMed PubMed Central Google Scholar
• Pellegrin, S. & Mellor, H. The Rho family GTPase Rif induces filopodia through mDia2. Curr. Biol. 15, 129–133 (2005).
  CAS PubMed Google Scholar
• Schirenbeck, A., Bretschneider, T., Arasada, R., Schleicher, M. & Faix, J. 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
• Lebrand, C. et al. Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37–49 (2004).
  CAS PubMed Google Scholar
• Yang, C. et al. Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol. 5, e317 (2007).
  PubMed PubMed Central Google Scholar
• Block, J. et al. Filopodia formation induced by active mDia2/Drf3. J. Microsc. 231, 506–517 (2008).
  CAS PubMed Google Scholar
• Gupton, S. L., Eisenmann, K., Alberts, A. S. & Waterman-Storer, C. M. mDia2 regulates actin and focal adhesion dynamics and organization in the lamella for efficient epithelial cell migration. J. Cell Sci. 120, 3475–3487 (2007).
  CAS PubMed Google Scholar
• Mejillano, M. R. et al. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363–373 (2004).
  CAS PubMed Google Scholar
• Uruno, T., Remmert, K. & Hammer, J. A. CARMIL is a potent capping protein antagonist: identification of a conserved CARMIL domain that inhibits the activity of capping protein and uncaps capped actin filaments. J. Biol. Chem. 281, 10635–10650 (2006).
  CAS PubMed Google Scholar
• Yang, C. et al. Mammalian CARMIL inhibits actin filament capping by capping protein. Dev. Cell 9, 209–221 (2005).
  CAS PubMed PubMed Central Google Scholar
• Jung, G., Remmert, K., Wu, X., Volosky, J. M. & Hammer, J. A. The Dictyostelium CARMIL protein links capping protein and the Arp2/3 complex to type I myosins through their SH3 domains. J. Cell Biol. 153, 1479–1497 (2001).
  CAS PubMed PubMed Central Google Scholar
• Zwolak, A. et al. CARMIL leading edge localization depends on a non-canonical PH domain and dimerization. Nature Commun. 4, 2523 (2013).
  Google Scholar
• Liang, Y., Niederstrasser, H., Edwards, M., Jackson, C. E. & Cooper, J. A. Distinct roles for CARMIL isoforms in cell migration. Mol. Biol. Cell 20, 5290–5305 (2009).
  CAS PubMed PubMed Central Google Scholar
• Bugyi, B., Didry, D. & Carlier, M. F. How tropomyosin regulates lamellipodial actin-based motility: a combined biochemical and reconstituted motility approach. EMBO J. 29, 14–26 (2010).
  CAS PubMed Google Scholar
• Reymann, A. C. et al. Actin network architecture can determine myosin motor activity. Science 336, 1310–1314 (2012).
  CAS PubMed PubMed Central Google Scholar
• Wilson, C. A. et al. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465, 373–377 (2010).
  CAS PubMed PubMed Central Google Scholar
• Blanchoin, L., Pollard, T. D. & Mullins, R. D. Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr. Biol. 10, 1273–1282 (2000).
  CAS PubMed Google Scholar
• Gandhi, M. et al. GMF is a cofilin homolog that binds Arp2/3 complex to stimulate filament debranching and inhibit actin nucleation. Curr. Biol. 20, 861–867 (2010). The first paper to show that GMF is a specialized paralogue of cofilin that debranches ARP2/3 branched junctions from actin networks.
  CAS PubMed PubMed Central Google Scholar
• Ydenberg, C. A. et al. GMF severs actin-Arp2/3 complex branch junctions by a cofilin-like mechanism. Curr. Biol. 23, 1037–1045 (2013).
  CAS PubMed PubMed Central Google Scholar
• Luan, Q. & Nolen, B. J. Structural basis for regulation of Arp2/3 complex by GMF. Nature Struct. Mol. Biol. 20, 1062–1068 (2013).
  CAS Google Scholar
• Boczkowska, M., Rebowski, G. & Dominguez, R. Glia maturation factor (GMF) interacts with Arp2/3 complex in a nucleotide state-dependent manner. J. Biol. Chem. 288, 25683–25688 (2013).
  CAS PubMed PubMed Central Google Scholar
• Lippert, D. N. & Wilkins, J. A. Glia maturation factor gamma regulates the migration and adherence of human T lymphocytes. BMC Immunol. 13, 21 (2012).
  CAS PubMed PubMed Central Google Scholar
• Zuo, P. et al. The expression of glia maturation factors and the effect of glia maturation factor-gamma on angiogenic sprouting in zebrafish. Exp. Cell Res. 319, 707–717 (2013).
  CAS PubMed Google Scholar
• Li, Y. L. et al. Identification of glia maturation factor β as an independent prognostic predictor for serous ovarian cancer. Eur. J. Cancer 46, 2104–2118 (2010).
  CAS PubMed Google Scholar
• Zuo, P. et al. High GMFG expression correlates with poor prognosis and promotes cell migration and invasion in epithelial ovarian cancer. Gynecol. Oncol. 132, 745–751 (2014).
  CAS PubMed Google Scholar
• Kaksonen, M., Peng, H. B. & Rauvala, H. Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J. Cell Sci. 113, 4421–4426 (2000).
  CAS PubMed Google Scholar
• Cai, L., Makhov, A. M., Schafer, D. A. & Bear, J. E. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134, 828–842 (2008).
  CAS PubMed PubMed Central Google Scholar
• Helgeson, L. A. & Nolen, B. J. Mechanism of synergistic activation of Arp2/3 complex by cortactin and N-WASP. eLife 2, e00884 (2013).
  PubMed PubMed Central Google Scholar
• Bryce, N. S. et al. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr. Biol. 15, 1276–1285 (2005).
  CAS PubMed Google Scholar
• Lai, F. P. et al. Cortactin promotes migration and platelet-derived growth factor-induced actin reorganization by signaling to Rho-GTPases. Mol. Biol. Cell 20, 3209–3223 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sung, B. H., Zhu, X., Kaverina, I. & Weaver, A. M. Cortactin controls cell motility and lamellipodial dynamics by regulating ECM secretion. Curr. Biol. 21, 1460–1469 (2011).
  CAS PubMed PubMed Central Google Scholar
• Clark, E. S., Whigham, A. S., Yarbrough, W. G. & Weaver, A. M. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67, 4227–4235 (2007).
  CAS PubMed Google Scholar
• Puthenveedu, M. A. et al. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761–773 (2010).
  CAS PubMed PubMed Central Google Scholar
• Chan, K. T., Creed, S. J. & Bear, J. E. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol. 21, 481–488 (2011).
  CAS PubMed PubMed Central Google Scholar
• de Hostos, E. L. et al. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J. Cell Biol. 120, 163–173 (1993).
  CAS PubMed Google Scholar
• Brieher, W. M., Kueh, H. Y., Ballif, B. A. & Mitchison, T. J. Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J. Cell Biol. 175, 315–324 (2006).
  CAS PubMed PubMed Central Google Scholar
• Galkin, V. E. et al. Coronin-1A stabilizes F-actin by bridging adjacent actin protomers and stapling opposite strands of the actin filament. J. Mol. Biol. 376, 607–613 (2008).
  CAS PubMed Google Scholar
• Gandhi, M., Achard, V., Blanchoin, L. & Goode, B. L. Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol. Cell 34, 364–374 (2009).
  CAS PubMed PubMed Central Google Scholar
• Humphries, C. L. et al. Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. J. Cell Biol. 159, 993–1004 (2002).
  CAS PubMed PubMed Central Google Scholar
• Liu, S. L., Needham, K. M., May, J. R. & Nolen, B. J. Mechanism of a concentration-dependent switch between activation and inhibition of Arp2/3 complex by coronin. J. Biol. Chem. 286, 17039–17046 (2011).
  CAS PubMed PubMed Central Google Scholar
• Cai, L., Marshall, T. W., Uetrecht, A. C., Schafer, D. A. & Bear, J. E. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128, 915–929 (2007).
  CAS PubMed PubMed Central Google Scholar
• Cai, L., Holoweckyj, N., Schaller, M. D. & Bear, J. E. Phosphorylation of coronin 1B by protein kinase C regulates interaction with Arp2/3 and cell motility. J. Biol. Chem. 280, 31913–31923 (2005).
  CAS PubMed Google Scholar
• Williams, H. C. et al. Role of coronin 1B in PDGF-induced migration of vascular smooth muscle cells. Circ. Res. 111, 56–65 (2012).
  CAS PubMed Google Scholar
• Rocca, D. L., Martin, S., Jenkins, E. L. & Hanley, J. G. Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nature Cell Biol. 10, 259–271 (2008).
  CAS PubMed Google Scholar
• Maritzen, T. et al. Gadkin negatively regulates cell spreading and motility via sequestration of the actin-nucleating ARP2/3 complex. Proc. Natl Acad. Sci. USA 109, 10382–10387 (2012).
  CAS PubMed Google Scholar
• Dang, I. et al. Inhibitory signalling to the Arp2/3 complex steers cell migration. Nature 503, 281–284 (2013). This paper reports the identification of the ARP2/3 inhibitory protein Arpin and its inhibitory role in cell migration. Arpin inhibits the two major parameters of cell migration: cell speed and directional persistence.
  CAS PubMed Google Scholar
• Nakamura, Y. et al. PICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity. EMBO J. 30, 719–730 (2011).
  CAS PubMed PubMed Central Google Scholar
• Rocca, D. L. et al. The small GTPase Arf1 modulates Arp2/3-mediated actin polymerization via PICK1 to regulate synaptic plasticity. Neuron 79, 293–307 (2013).
  CAS PubMed PubMed Central Google Scholar
• Harms, B. D., Bassi, G. M., Horwitz, A. R. & Lauffenburger, D. A. Directional persistence of EGF-induced cell migration is associated with stabilization of lamellipodial protrusions. Biophys. J. 88, 1479–1488 (2005).
  CAS PubMed PubMed Central Google Scholar
• Arrieumerlou, C. & Meyer, T. A local coupling model and compass parameter for eukaryotic chemotaxis. Dev. Cell 8, 215–227 (2005). This study challenges the model that lamellipodium formation during chemotaxis is controlled by the global integration of competing signals. It instead shows that cells self-polarize and that the local activation of receptors generates small protrusions of existing lamellipodia towards the guidance cue (see also reference 163).
  CAS PubMed Google Scholar
• Andrew, N. & Insall, R. H. Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nature Cell Biol. 9, 193–200 (2007). This study challenges existing models that lamellipodia are generated de novo in the direction of a guidance cue. This paper instead shows that lamellipodia are randomly generated and the ones that extend towards the chemoattractant are maintained.
  CAS PubMed Google Scholar
• Welch, M. D., Rosenblatt, J., Skoble, J., Portnoy, D. A. & Mitchison, T. J. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281, 105–108 (1998).
  CAS PubMed Google Scholar
• Smith, G. A., Theriot, J. A. & Portnoy, D. A. The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135, 647–660 (1996).
  CAS PubMed Google Scholar
• Krause, M. et al. Fyn-binding protein (Fyb)/SLP-76- associated protein (SLAP), Ena/vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J. Cell Biol. 149, 181–194 (2000).
  CAS PubMed PubMed Central Google Scholar
• Brandman, O. & Meyer, T. Feedback loops shape cellular signals in space and time. Science 322, 390–395 (2008).
  CAS PubMed PubMed Central Google Scholar
• Danuser, G., Allard, J. & Mogilner, A. Mathematical modeling of eukaryotic cell migration: insights beyond experiments. Annu. Rev. Cell Dev. Biol. 29, 501–528 (2013).
  CAS PubMed PubMed Central Google Scholar
• Wu, C. F. & Lew, D. J. Beyond symmetry-breaking: competition and negative feedback in GTPase regulation. Trends Cell Biol. 23, 476–483 (2013).
  CAS PubMed PubMed Central Google Scholar
• Novak, B. & Tyson, J. J. Design principles of biochemical oscillators. Nature Rev. Mol. Cell Biol. 9, 981–991 (2008).
  CAS Google Scholar
• Weiner, O. D. et al. Spatial control of actin polymerization during neutrophil chemotaxis. Nature Cell Biol. 1, 75–81 (1999).
  CAS PubMed Google Scholar
• Osmani, N., Peglion, F., Chavrier, P. & Etienne-Manneville, S. Cdc42 localization and cell polarity depend on membrane traffic. J. Cell Biol. 191, 1261–1269 (2010).
  CAS PubMed PubMed Central Google Scholar
• Bretscher, M. S. Asymmetry of single cells and where that leads. Annu. Rev. Biochem. 83, 275–289 (2014).
  CAS PubMed Google Scholar
• Desai, S. P., Bhatia, S. N., Toner, M. & Irimia, D. Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys. J. 104, 2077–2088 (2013).
  CAS PubMed PubMed Central Google Scholar
• Iden, S. & Collard, J. G. Crosstalk between small GTPases and polarity proteins in cell polarization. Nature Rev. Mol. Cell Biol. 9, 846–859 (2008).
  CAS Google Scholar
• Etienne-Manneville, S. Microtubules in cell migration. Annu. Rev. Cell Dev. Biol. 29, 471–499 (2013).
  CAS PubMed Google Scholar
• Bos, J. L., Rehmann, H. & Wittinghofer, A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865–877 (2007).
  CAS PubMed Google Scholar
• Castro-Castro, A. et al. Coronin 1A promotes a cytoskeletal-based feedback loop that facilitates Rac1 translocation and activation. EMBO J. 30, 3913–3927 (2011).
  CAS PubMed PubMed Central Google Scholar
• Fujiwara, I., Remmert, K. & Hammer, J. A. Direct observation of the uncapping of capping protein-capped actin filaments by CARMIL homology domain 3. J. Biol. Chem. 285, 2707–2720 (2010).
  CAS PubMed Google Scholar
• Garcia Arguinzonis, M. I., Galler, A. B., Walter, U., Reinhard, M. & Simm, A. Increased spreading, Rac/p21-activated kinase (PAK) activity, and compromised cell motility in cells deficient in vasodilator-stimulated phosphoprotein (VASP). J. Biol. Chem. 277, 45604–45610 (2002).
  CAS PubMed Google Scholar
• Lawson, C. D. & Burridge, K. The on-off relationship of Rho and Rac during integrin-mediated adhesion and cell migration. Small GTPases 5, e27958 (2014).
  PubMed PubMed Central Google Scholar
• Jones, M. C., Machida, K., Mayer, B. J. & Turner, C. E. Paxillin kinase linker (PKL) regulates Vav2 signaling during cell spreading and migration. Mol. Biol. Cell 24, 1882–1894 (2013).
  CAS PubMed PubMed Central Google Scholar
• Weiner, O. D. et al. A PtdInsP3- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nature Cell Biol. 4, 509–513 (2002).
  CAS PubMed Google Scholar
• Millius, A., Dandekar, S. N., Houk, A. R. & Weiner, O. D. Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. Curr. Biol. 19, 253–259 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kuiper, J. W., Sun, C., Magalhaes, M. A. & Glogauer, M. Rac regulates PtdInsP3 signaling and the chemotactic compass through a redox-mediated feedback loop. Blood 118, 6164–6171 (2011).
  CAS PubMed Google Scholar
• Cheng, G., Diebold, B. A., Hughes, Y. & Lambeth, J. D. Nox1-dependent reactive oxygen generation is regulated by Rac1. J. Biol. Chem. 281, 17718–17726 (2006).
  CAS PubMed Google Scholar
• Taulet, N., Delorme-Walker, V. D. & DerMardirossian, C. Reactive oxygen species regulate protrusion efficiency by controlling actin dynamics. PLoS ONE 7, e41342 (2012).
  CAS PubMed PubMed Central Google Scholar
• Morimatsu, T., Kawagoshi, A., Yoshida, K. & Tamura, M. Actin enhances the activation of human neutrophil NADPH oxidase in a cell-free system. Biochem. Biophys. Res. Commun. 230, 206–210 (1997).
  CAS PubMed Google Scholar
• Usatyuk, P. V. et al. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J. Biol. Chem. 282, 23284–23295 (2007).
  CAS PubMed Google Scholar
• Pankov, R. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793–802 (2005).
  CAS PubMed PubMed Central Google Scholar
• Millius, A., Watanabe, N. & Weiner, O. D. Diffusion, capture and recycling of SCAR/WAVE and Arp2/3 complexes observed in cells by single-molecule imaging. J. Cell Sci. 125, 1165–1176 (2012).
  CAS PubMed PubMed Central Google Scholar
• Heider, M. R. & Munson, M. Exorcising the exocyst complex. Traffic 13, 898–907 (2012).
  CAS PubMed PubMed Central Google Scholar
• Parrini, M. C. et al. SH3BP1, an exocyst-associated RhoGAP, inactivates Rac1 at the front to drive cell motility. Mol. Cell 42, 650–661 (2011).
  CAS PubMed PubMed Central Google Scholar
• Endris, V. et al. SrGAP3 interacts with lamellipodin at the cell membrane and regulates Rac-dependent cellular protrusions. J. Cell Sci. 124, 3941–3955 (2011).
  CAS PubMed Google Scholar
• Soderling, S. H. et al. The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nature Cell Biol. 4, 970–975 (2002).
  CAS PubMed Google Scholar
• Suetsugu, S. & Gautreau, A. Synergistic BAR-NPF interactions in actin-driven membrane remodeling. Trends Cell Biol. 22, 141–150 (2012).
  CAS PubMed Google Scholar
• Yamazaki, D., Itoh, T., Miki, H. & Takenawa, T. srGAP1 regulates lamellipodial dynamics and cell migratory behavior by modulating Rac1 activity. Mol. Biol. Cell 24, 3393–3405 (2013).
  CAS PubMed PubMed Central Google Scholar
• Allard, J. & Mogilner, A. Traveling waves in actin dynamics and cell motility. Curr. Opin. Cell Biol. 25, 107–115 (2013).
  CAS PubMed Google Scholar
• Ryan, G. L., Watanabe, N. & Vavylonis, D. A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. Cytoskeleton 69, 195–206 (2012).
  CAS PubMed Google Scholar
• Xiong, Y., Huang, C. H., Iglesias, P. A. & Devreotes, P. N. Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc. Natl Acad. Sci. USA 107, 17079–17086 (2010). This paper reports the so-called LEGI-BEN model of cell migration, which is a major model accounting for chemotactic behaviour. It explains in particular how cells are intrinsically able to maintain a polarized state associated with directional persistence through the propagation of waves, which involves positive feedback and an inhibitor, and how this ability is biased in chemotaxis to obtain accurate directionality.
  CAS PubMed Google Scholar
• Bugyi, B. & Carlier, M. F. Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449–470 (2010).
  CAS PubMed Google Scholar
• Pollard, T. D. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36, 451–477 (2007).
  CAS PubMed Google Scholar
• Carlier, M. F., Husson, C., Renault, L. & Didry, D. Control of actin assembly by the WH2 domains and their multifunctional tandem repeats in Spire and Cordon-Bleu. Int. Rev. Cell Mol. Biol. 290, 55–85 (2011).
  CAS PubMed Google Scholar
• Qualmann, B. & Kessels, M. M. New players in actin polymerization—WH2-domain-containing actin nucleators. Trends Cell Biol. 19, 276–285 (2009).
  CAS PubMed Google Scholar
• Chesarone, M. A. & Goode, B. L. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28–37 (2009).
  CAS PubMed PubMed Central Google Scholar
• Morishige, M. et al. GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nature Cell Biol. 10, 85–92 (2008).
  CAS PubMed Google Scholar
• Haines, E., Saucier, C. & Claing, A. The adaptor proteins p66Shc and Grb2 regulate the activation of the GTPases ARF1 and ARF6 in invasive breast cancer cells. J. Biol. Chem. 289, 5687–5703 (2014).
  CAS PubMed PubMed Central Google Scholar