Filopodia initiation: Focus on the Arp2/3 complex and formins

Cell Adhesion and Migration

Volumn 5, Issue 5, 2011, Pages

  Yang, Changsong ^a   Svitkina, Tatyana ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Actin; Arp2 3 complex; Ena VASP; Filopodia; Formins

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; CELL PROTEIN; FORMIN HOMOLOGY 1; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL ELONGATION; CELL FUNCTION; CELL ORGANELLE; FILOPODIUM; HUMAN; NONHUMAN; PROTEIN FUNCTION; REVIEW; SEQUENCE HOMOLOGY;

EID: 80053458405     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: None     Document Type: Review

References (87)

1. Ellermann V. On the detection of rhizopods in two cases of acute anterior poliomyelitis. In: Bruce A, Bramwell E, Campbell M, Eds. Review of neurology and psychiatry. Edinburgh: Otto Schulze Co. 1906; 353.
2. Harrison RG. Observations on the living developing nerve fiber. Anat Rec 1907; 1:116-8.
3. Gallo G, Letourneau PC. Regulation of growth cone actin filaments by guidance cues. J Neurobiol 2004; 58:92-102. (Pubitemid 37543341)
4. Drees F, Gertler FB. Ena/VASP: proteins at the tip of the nervous system. Curr Opin Neurobiol 2008; 18:53-9.
5. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 2009; 29:639-49.
6. Machesky LM, Li A. Fascin: Invasive filopodia promoting metastasis. Commun Integr Biol 2010; 3:263-70.
7. Vasioukhin V, Bauer C, Yin M, Fuchs E. Directed actin polymerization is the driving force for epithelial cellcell adhesion. Cell 2000; 100:209-19. (Pubitemid 30064909)
8. Wood W, Martin P. Structures in focus-filopodia. Int J Biochem Cell Biol 2002; 34:726-30.
9. Bourne JN, Harris KM. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 2008; 31:47-67.
10. Hotulainen P, Hoogenraad CC. Actin in dendritic spines: connecting dynamics to function. J Cell Biol 2010; 189:619-29.
11. Heiman MG, Shaham S. Twigs into branches: how a filopodium becomes a dendrite. Curr Opin Neurobiol 2010; 20:86-91.
12. Al-Alwan MM, Rowden G, Lee TD, West KA. Fascin is involved in the antigen presentation activity of mature dendritic cells. J Immunol 2001; 166:338-45. (Pubitemid 32038450)
13. Faix J, Rottner K. The making of filopodia. Curr Opin Cell Biol 2006; 18:18-25. (Pubitemid 43107603)
14. Gupton SL, Gertler FB. Filopodia: the fingers that do the walking. Sci STKE 2007; 2007:5.
15. Mattila PK, Lappalainen P. Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol2008; 9:446-54. (Pubitemid 351733400)
16. Faix J, Breitsprecher D, Stradal TE, Rottner K. Filopodia: Complex models for simple rods. Int J Biochem Cell Biol 2009; 41:1656-64.
17. Mellor H. The role of formins in filopodia formation. Biochim Biophys Acta 2010; 1803:191-200.
18. Mogilner A, Rubinstein B. The physics of filopodial protrusion. Biophys J 2005; 89:782-95. (Pubitemid 41098966)
19. Mogilner A. Mathematics of cell motility: have we got its number? J Math Biol 2009; 58:105-34.
20. Carlsson AE, Sept D. Mathematical modeling of cell migration. Methods Cell Biol 2008; 84:911-37.
21. Chhabra ES, Higgs HN. The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 2007; 9:1110-21. (Pubitemid 47500485)
22. Nicholson-Dykstra SM, Higgs HN. Arp2 depletion inhibits sheet-like protrusions but not linear protrusions of fibroblasts and lymphocytes. Cell Motil Cytoskeleton 2008; 65:904-22.
23. Ahmed S, Goh WI, Bu W. I-BAR domains, IRSp53 and filopodium formation. Semin Cell Dev Biol 2010; 21:350-6.
24. Goh WI, Sudhaharan T, Lim KB, Sem KP, Lau CL, Ahmed S. Rif-mDia1 interaction is Involved in filopodium formation independent of Cdc42 and Rac effectors. J Biol Chem 2011; 286:13681-94.
25. Korobova F, Svitkina T. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 2010; 21:165-76.
26. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, et al. Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 2003; 160:409-21. (Pubitemid 36182731)
27. Korobova F, Svitkina T. Arp2/3 complex is important for filopodia formation, growth cone motility and neuritogenesis in neuronal cells. Mol Biol Cell 2008; 19:1561-74. (Pubitemid 351805109)
28. Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, Bretscher A, et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 2002; 297:612-5. (Pubitemid 34815347)
29. Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier MF. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 2004; 119:419-29. (Pubitemid 39423843)
30. Kovar DR, Pollard TD. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci USA 2004; 101:14725-30. (Pubitemid 39410742)
31. Breitsprecher D, Kiesewetter AK, Linkner J, Urbanke C, Resch GP, Small JV, et al. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J 2008; 27:2943-54.
32. Hansen SD, Mullins RD. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J Cell Biol 2010; 191:571-84.
33. Mullins RD, Heuser JA, Pollard TD. 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 1998; 95:6181-6. (Pubitemid 28248985)
34. Svitkina TM, Verkhovsky AB, McQuade KM, Borisy GG. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J Cell Biol 1997; 139:397-415. (Pubitemid 27459313)
35. Svitkina TM, Borisy GG. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 1999; 145:1009-26. (Pubitemid 29270059)
36. Goley ED, Welch MD. The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 2006; 7:713-26. (Pubitemid 44450456)
37. Pollard TD. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 2007; 36:451-77. (Pubitemid 47007562)
38. Le Clainche C, Carlier MF. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 2008; 88:489-513. (Pubitemid 351520086)
39. Machesky LM, Insall RH. Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 1998; 8:1347-56. (Pubitemid 29020143)
40. Innocenti M, Gerboth S, Rottner K, Lai FP, Hertzog M, Stradal TE, et al. Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 2005; 7:969-76. (Pubitemid 41486270)
41. Derivery E, Gautreau A. Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. Bioessays 2010; 32:119-31.
42. Campellone KG, Welch MD. A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 2010; 11:237-51.
43. Higgs HN, Peterson KJ. Phylogenetic analysis of the formin homology 2 domain. Mol Biol Cell 2005; 16:1-13. (Pubitemid 40024285)
44. Higgs HN. Formin proteins: a domain-based approach. Trends Biochem Sci 2005; 30:342-53. (Pubitemid 40799053)
45. Goode BL, Eck MJ. Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 2007; 76:593-627.
46. Paul AS, Pollard TD. Review of the mechanism of processive actin filament elongation by formins. Cell Motil Cytoskeleton 2009; 66:606-17.
47. Yang C, Czech L, Gerboth S, Kojima S, Scita G, Svitkina T. Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 2007; 5:317.
48. Gates J, Mahaffey JP, Rogers SL, Emerson M, Rogers EM, Sottile SL, et al. Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 2007; 134:2027-39. (Pubitemid 46979790)
49. Falet H, Hoffmeister KM, Neujahr R, Hartwig JH. Normal Arp2/3 complex activation in platelets lacking WASp. Blood 2002; 100:2113-22. (Pubitemid 35001246)
50. Vignjevic D, Yarar D, Welch MD, Peloquin J, Svitkina T, Borisy GG. Formation of filopodia-like bundles in vitro from a dendritic network. J Cell Biol 2003; 160:951-62. (Pubitemid 36350849)
51. Haviv L, Brill-Karniely Y, Mahaffy R, Backouche F, Ben-Shaul A, Pollard TD, et al. Reconstitution of the transition from lamellipodium to filopodium in a membrane-free system. Proc Natl Acad Sci USA 2006; 103:4906-11.
52. Brill-Karniely Y, Ideses Y, Bernheim-Groswasser A, Ben-Shaul A. From branched networks of actin filaments to bundles. Chemphyschem 2009; 10:2818-27.
53. Lee K, Gallop JL, Rambani K, Kirschner MW. Selfassembly of filopodia-like structures on supported lipid bilayers. Science 2010; 329:1341-5.
54. Norris AD, Dyer JO, Lundquist EA. The Arp2/3 complex, UNC-115/abLIM and UNC-34/Enabled regulate axon guidance and growth cone filopodia formation in Caenorhabditis elegans. Neural Dev 2009; 4:38.
55. Goncalves-Pimentel C, Gombos R, Mihaly J, Sanchez- Soriano N, Prokop A. Dissecting regulatory networks of filopodia formation in a Drosophila growth cone model. PLoS One 2011; 6:18340.
56. Qualmann B, Kelly RB. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol 2000; 148:1047-62.
57. Biyasheva A, Svitkina T, Kunda P, Baum B, Borisy G. Cascade pathway of filopodia formation downstream of SCAR. J Cell Sci 2004; 117:837-48. (Pubitemid 38396712)
58. Johnston SA, Bramble JP, Yeung CL, Mendes PM, Machesky LM. Arp2/3 complex activity on filopodia of spreading cells. BMC Cell Biol 2008; 9:65.
59. Cohen M, Georgiou M, Stevenson NL, Miodownik M, Baum B. Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. Dev Cell 2010; 19:78-89.
60. Miki H, Sasaki T, Takai Y, Takenawa T. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 1998; 391:93-6. (Pubitemid 28079222)
61. Cory GO, Garg R, Cramer R, Ridley AJ. Phosphorylation of tyrosine 291 enhances the ability of WASp to stimulate actin polymerization and filopodium formation. J Biol Chem 2002; 277:45115-21. (Pubitemid 36159113)
62. Bu W, Chou AM, Lim KB, Sudhaharan T, Ahmed S. The Toca-1-N-WASP Complex Links Filopodial Formation to Endocytosis. J Biol Chem 2009; 284:11622-36.
63. Sheldon H, Andre M, Legg JA, Heal P, Herbert JM, Sainson R, et al. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation- promoting factors. FASEB J 2009; 23:513-22.
64. Lommel S, Benesch S, Rottner K, Franz T, Wehland J, Kuhn R. Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep 2001; 2:850-7. (Pubitemid 32982755)
65. Snapper SB, Takeshima F, Anton I, Liu CH, Thomas SM, Nguyen D, et al. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 2001; 3:897-904. (Pubitemid 32952254)
66. Co C, Wong DT, Gierke S, Chang V, Taunton J. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 2007; 128:901-13. (Pubitemid 46341410)
67. Takano K, Watanabe-Takano H, Suetsugu S, Kurita S, Tsujita K, Kimura S, et al. Nebulin and N-WASP cooperate to cause IGF-1-induced sarcomeric actin filament formation. Science 2010; 330:1536-40.
68. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG. Lamellipodial versus filopodial mode of the actin nanomachinery; pivotal role of the filament barbed end. Cell 2004; 118:363-73. (Pubitemid 39061116)
69. Lebrand C, Dent EW, Strasser GA, Lanier LM, Krause M, Svitkina TM, et al. Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 2004; 42:37-49. (Pubitemid 38456966)
70. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J, et al. Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 2007; 56:441-55. (Pubitemid 350030877)
71. Han YH, Chung CY, Wessels D, Stephens S, Titus MA, Soll DR, et al. Requirement of a vasodilator-stimulated phosphoprotein (VASP) family member for cell adhesion, the formation of filopodia and chemotaxis in Dictyostelium. J Biol Chem 2002; 17:17.
72. Homem CC, Peifer M. Exploring the roles of diaphanous and enabled activity in shaping the balance between filopodia and lamellipodia. Mol Biol Cell 2009; 20:5138-55.
73. Peng J, Wallar BJ, Flanders A, Swiatek PJ, Alberts AS. Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr Biol 2003; 13:534-45. (Pubitemid 36391930)
74. Pellegrin S, Mellor H. The Rho family GTPase Rif induces filopodia through mDia2. Curr Biol 2005; 15:129-33.
75. Harris ES, Gauvin TJ, Heimsath EG, Higgs HN. Assembly of filopodia by the formin FRL2 (FMNL3). Cytoskeleton (Hoboken) 2010; 67:755-72.
76. Harris ES, Rouiller I, Hanein D, Higgs HN. Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J Biol Chem 2006; 281:14383-92. (Pubitemid 43848368)
77. Lambrechts A, Kwiatkowski AV, Lanier LM, Bear JE, Vandekerckhove J, Ampe C, et al. cAMP-dependent protein kinase phosphorylation of EVL, a Mena/VASP relative, regulates its interaction with actin and SH3 domains. J Biol Chem 2000; 275:36143-51.
78. Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG. Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 2007; 18:2579-91. (Pubitemid 47025723)
79. Dent EW, Kwiatkowski AV, Mebane LM, Philippar U, Barzik M, Rubinson DA, et al. Filopodia are required for cortical neurite initiation. Nat Cell Biol 2007; 9:1347-59. (Pubitemid 350201748)
80. Schirenbeck A, Bretschneider T, Arasada R, Schleicher M, Faix J. The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat Cell Biol 2005; 7:619-25. (Pubitemid 40796985)
81. Matusek T, Gombos R, Szecsenyi A, Sanchez-Soriano N, Czibula A, Pataki C, et al. Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci 2008; 28:13310-9.
82. Block J, Stradal TE, Hanisch J, Geffers R, Kostler SA, Urban E, et al. Filopodia formation induced by active mDia2/Drf3. J Microsc 2008; 231:506-17.
83. Steffen A, Faix J, Resch GP, Linkner J, Wehland J, Small JV, et al. Filopodia formation in the absence of functional WAVE- and Arp2/3-complexes. Mol Biol Cell 2006; 17:2581-91. (Pubitemid 43825496)
84. Pronk S, Geissler PL, Fletcher DA. Limits of filopodium stability. Phys Rev Lett 2008; 100:258102.
85. Beli P, Mascheroni D, Xu D, Innocenti M. WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat Cell Biol 2008; 10:849-57. (Pubitemid 351927713)
86. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M, et al. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 2008; 180:1245-60. (Pubitemid 351468478)
87. Ideses Y, Brill-Karniely Y, Haviv L, Ben-Shaul A, Bernheim-Groswasser A. Arp2/3 branched actin network mediates filopodia-like bundles formation in vitro. PLoS ONE 2008; 3:3297.