Cofilin cooperates with fascin to disassemble filopodial actin filaments

Journal of Cell Science

Volumn 124, Issue 19, 2011, Pages 3305-3318

  Breitsprecher, Dennis ^a,d   Koestler, Stefan A ^b   Chizhov, Igor ^a   Nemethova, Maria ^c   Mueller, Jan ^c   Goode, Bruce L ^d   Small, J Victor ^c   Rottner, Klemens ^b,e   Faix, Jan ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d BRANDEIS UNIVERSITY   (United States)

^e HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Actin; Cofilin; Electron tomography; Fascin; Filopodia; TIRF microscopy

Indexed keywords

COFILIN; FASCIN;

ACTIN FILAMENT; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; ELECTRON TOMOGRAPHY; EMBRYO; FILOPODIUM; FLUORESCENCE MICROSCOPY; FLUOROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CARRIER PROTEINS; CELL LINE; GREEN FLUORESCENT PROTEINS; HUMANS; KINETICS; MICE; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; PHALLOIDINE; PROTEIN MULTIMERIZATION; PSEUDOPODIA; RECOMBINANT FUSION PROTEINS; TIME-LAPSE IMAGING;

EID: 80054023872     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.086934     Document Type: Article

References (73)

1. Adams, J. C. and Schwartz, M. A. (2000). Stimulation of fascin spikes by thrombospondin-1 is mediated by the GTPases Rac and Cdc42. J. Cell Biol. 150, 807-822.
2. Auinger, S. and Small, J. V. (2008). Correlated light and electron microscopy of the cytoskeleton. Methods in Cell Biol. 88, 257-272.
3. Andrianantoandro, E. and Pollard, T. D. (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 24, 13-23.
4. Aratyn, Y. S., Schaus, T. E., Taylor, E. W. and Borisy, G. G. (2007). Intrinsic dynamic behavior of fascin in filopodia. Mol. Biol. Cell 18, 3928-3940.
5. Bernstein. B.W. and Bamburg, J. R. (2010). ADF/cofilin: a functional node in cell biology.Trends Cell Biol. 4, 187-195.
6. Blanchoin, L. and Pollard, T. D. (1999). Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J. Biol. Chem. 274, 15538-15546.
7. Bobkov, A. A., Muhlrad, A., Shvetsov, A., Benchaar, S., Scoville, D., Almo, S. C. and Reisler, E. (2004). Cofilin (ADF) affects lateral contacts in F-actin. J. Mol. Biol. 337, 93-104.
8. 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.
9. Breitsprecher, D., Kiesewetter, A. K., Linkner, J., Vinzenz, M., Stradal, T. E. B., Small, J. V., Curth, U., Dickinson, R. B. and Faix, J. (2011). Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J. 30, 456-467.
10. Bugyi, B. and Carlier, M. F. (2010). Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449-470.
11. Cao, W., Goodarzi, J. P. and De La Cruz, E. M. (2006). Energetics and kinetics of cooperative cofilin-actin filament interactions. J. Mol. Biol. 361, 257-267
12. Carlier, M. F., Laurent, V., Santolini, J., Melki, R., Didry, D., Xia, G. X., Hong, Y., Chua, N. H. and Pantaloni, D. (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136, 1307-1322.
13. Carlier, M. F., Pantaloni, D., Evans, J. A., Lambooy, P. K., Korn, E. D. and Webb, M. R. (1988). The hydrolysis of ATP that accompanies actin polymerization is essentially irreversible. FEBS Lett. 235, 211-214.
14. Chesarone, M. A. and Goode, B. L. (2009). Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37.
15. Claessens, M. M., Semmrich, C., Ramos, L. and Bausch, A. R. (2008). Helical twist controls the thickness of F-actin bundles. Proc. Natl. Acad. Sci. USA105, 8819-8822.
16. Costantino, S., Kent, C. B., Godin, A. G., Kennedy, T. E., Wiseman, P. W. and Fournier, A. E. (2008). Semi-automated quantification of filopodial dynamics. J. Neurosci. Methods 171, 165-173.
17. Dent, E. W., Kwiatkowski, A. V., Mebane, L. M., Philippar, U., Barzik, M., Rubinson, D. A., Gupton, S., Van Veen, J. E., Furman, C., Zhang, J., Alberts, A. S., Mori, S. and Gertler, F. B. (2007). Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9, 1347-1359.
18. De La Cruz, E. M. (2005). Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. J. Mol. Biol. 346, 557-564.
19. De La Cruz, E. M. and Sept, D. (2010). The kinetics of cooperative cofilin binding reveals two states of the cofilin-actin filament. Biophys. J. 98, 1893-1901.
20. DeRosier, D. J. and Edds, K. T. (1980). Evidence for fascin cross-links between the actin filaments in coelomocyte filopodia. Exp. Cell Res. 126, 490-494.
21. Dickinson, R. B. and Purich, D. L. (2002). Clamped-filament elongation model for actin-based motors. Biophys. J. 82, 605-617.
22. Dickinson, R. B., Caro, L. and Purich, D. L. (2004). Force generation by cytoskeletal filament end-tracking proteins. Biophys. J. 87, 2838-2854.
23. Du, J. and Frieden, C. (1998). Kinetic studies on the effect of yeast cofilin on yeast actin polymerization. Biochemistry 37, 13276-13284.
24. Faix, J., Breitsprecher, D., Stradal, T. E. and Rottner, K. (2009). Filopodia: Complex models for simple rods. Int. J. Biochem. Cell Biol. 41, 1656-1664.
25. Galkin, V. E., Orlova, A., Lukoyanova, N., Wriggers, W. and Egelman, E. H. (2001). Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J. Cell Biol. 153, 75-86.
26. Galkin, V. E., Orlova, A., VanLoock, M. S., Shvetsov, A., Reisler, E. and Egelman, E. H. (2003). ADF/cofilin use an intrinsic mode of F-actin instability to disrupt actin filaments. J. Cell Biol. 163, 1057-1066.
27. Gandhi, M., Achard, V., Blanchoin, L. and Goode, B. L. (2009). Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol. Cell 34, 364-374.
28. Gehler, S., Shaw, A. E., Sarmiere, P. D., Bamburg, J. R. and Letourneau, P. C. (2004). Brain-derived neurotrophic factor regulation of retinal growth cone filopodial dynamics is mediated through actin depolymerizing factor/cofilin. J. Neurosci. 24, 10741-10749.
29. Geraldo, S. and Gordon-Weeks, P. R. (2009). Cytoskeletal dynamics in growth-cone steering. J. Cell. Sci. 122, 3595-3604.
30. Hotulainen, P. and Hoogenraad, C. C. (2010). Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189, 619-629.
31. Hotulainen, P., Paunola, E., Vartiainen, M. K. and Lappalainen, P. (2005). Actindepolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol. Biol. Cell 16, 649-664.
32. Insall, R. H. and Machesky, L. M. (2009). Actin dynamics at the leading edge: from simple machinery to complex networks. Dev. Cell. 17, 310-322.
33. Ishikawa, R., Sakamoto, T., Ando, T., Higashi-Fujime, S. and Kohama, K. (2003). Polarized actin bundles formed by human fascin-1: their sliding and disassembly on myosin II and myosin V in vitro. J. Neurochem. 87, 676-685.
34. Iwasa, J. H. and Mullins, R. D. (2007). Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr. Biol. 17, 395-406.
35. Kiuchi, T., Ohashi, K., Kurita, S. and Mizuno, K. (2007). Cofilin promotes stimulusinduced lamellipodium formation by generating an abundant supply of actin monomers. J. Cell Biol. 177, 465-476.
36. Koestler, S. A., Auinger, S., Vinzenz, M., Rottner, K. and Small, J. V. (2008). Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front. Nat. Cell Biol. 10, 306-313.
37. Kuhn, J. R. and Pollard, T. D. (2005). Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys. J. 88, 1387-1402.
38. Kremer, J. R., Mastronarde, D. N. and McIntosh, J. R. (1996). Computer visualization of threedimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
39. Kwiatkowski, A. V., Rubinson, D. A., Dent, E. W., Edward van Veen, J., Leslie, J. D., Zhang, J., Mebane, L. M., Philippar, U., Pinheiro, E. M., Burds, A. A., Bronson, R. T., Mori, S., Fässler, R, and Gertler, F. B. (2007). Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 56, 441-455.
40. Lai, F. P., Szczodrak, M., Block, J., Faix, J., Breitsprecher, D., Mannherz, H. G., Stradal, T. E., Dunn, G. A., Small, J. V. and Rottner, K. (2008). Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J. 27, 982-992.
41. Li, A., Dawson, J. C., Forero-Vargas, M., Spence, H. J., Yu, X., Konig, I., Anderson, K. and Machesky, L. M. (2010). The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr. Biol. 20, 339-345.
42. Lieleg, O., Claessens, M. M., Heussinger, C., Frey, E. and Bausch, A. R. (2007). Mechanics of bundled semiflexible polymer networks. Phys. Rev. Lett. 99, 088102.
43. Loisel, T. P., Boujemaa, R., Pantaloni, D. and Carlier, M. F. (1999). Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616.
44. Maciver, S. K., Wachsstock, D. H., Schwarz, W. H. and Pollard, T. D. (1991). The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with a-actinin. J. Cell Biol. 115, 1621-1628.
45. Mannherz, H. G., Gonsior, S. M., Gremm, D., Wu, X., Pope, B. J. and Weeds, A. G. (2005). Activated cofilin colocalises with Arp2/3 complex in apoptotic blebs during programmed cell death. Eur. J. Cell Biol. 84, 503-515.
46. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
47. McCullough, B. R., Blanchoin, L., Martiel, J. L. and De la Cruz, E. M. (2008). Cofilin increases the bending flexibility of actin filaments: implications for severing and cell mechanics. J. Mol. Biol. 381, 550-558.
48. McGough, A. and Chiu, W. (1999). ADF/cofilin weakens lateral contacts in the actin filament. J. Mol. Biol. 291, 513-519.
49. McGough, A., Pope, B., Chiu, W. and Weeds, A. (1997). Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138, 771-781.
50. Medalia, O., Beck, M., Ecke, M., Weber, I., Neujahr, R., Baumeister, W. and Gerisch, G. (2007). Organization of actin networks in intact filopodia. Curr. Biol. 17, 79-84.
51. Michelot, A., Berro, J., Guerin, C., Boujemaa-Paterski, R., Staiger, C. J., Martiel, J. L. and Blanchoin, L. (2007). Actin-filament stochastic dynamics mediated by ADF/cofilin. Curr. Biol. 17, 825-833.
52. Moseley, J. B., Okada, K., Balcer, H. I., Kovar, D. R., Pollard, T. D. and Goode, B. L. (2006). Twinfilin is an actin-filament-severing protein and promotes rapid turnover of actin structures in vivo. J. Cell. Sci. 119, 1547-1557.
53. Mouneimne, G., Soon, L., DesMarais, V., Sidani, M., Song, X., Yip, S. C., Ghosh, M., Eddy, R., Backer, J. M. and Condeelis J. (2004). Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J. Cell Biol. 166, 697-708.
54. Nemethova, M., Auinger, S. and Small, J. V. (2008). Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 180, 1234-1244.
55. Oser, M. and Condeelis, J. (2009). The cofilin activity cycle in lamellipodia and invadopodia. J. Cell. Biochem. 108, 1252-1262.
56. Oser, M., Yamaguchi, H., Mader, C. C., Bravo-Cordero, J. J., Arias, M., Chen, X., Desmarais, V., van Rheenen, J., Koleske, A. J. and Condeelis, J. (2009). Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 186, 571-587.
57. Otto, J. J., Kane, R. E. and Bryan, J. (1979). Formation of filopodia in coelomocytes: localization of fascin, a 58,000 dalton actin cross-linking protein. Cell 17, 285-293.
58. 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.
59. Pavlov, D., Muhlrad, A., Cooper, J., Wear, M. and Reisler, E. (2007). Actin filament severing by cofilin. J. Mol. Biol. 365, 1350-1358.
60. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
61. Prochniewicz, E., Janson, N., Thomas, D. D. and De la Cruz, E. M. (2005). Cofilin increases the torsional flexibility and dynamics of actin filaments. J. Mol. Biol. 353, 990-1000.
62. Ressad, F., Didry, D., Xia, G. X., Hong, Y., Chua, N. H., Pantaloni, D. and Carlier, M. F. (1998). Kinetic analysis of the interaction of actin-depolymerizing factor (ADF)/cofilin with G- and F-actins. Comparison of plant and human ADFs and effect of phosphorylation. J. Biol. Chem. 273, 20894-20902.
63. Romero, S., Le Clainche, C., Didry, D., Egile, C., Pantaloni, D. and Carlier, M. F. (2004). Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119, 419-429.
64. Romero, S., Didry, D., Larquet, E., Boisset, N., Pantaloni, D. and Carlier, M. F. (2007). How ATP hydrolysis controls filament assembly from profilin-actin: implication for formin processivity. J. Biol. Chem. 282, 8435-8445.
65. Schirenbeck, A., Arasada, R., Bretschneider, T., Stradal, T. E., Schleicher, M. and Faix, J. (2006). The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc. Natl. Acad. Sci. USA 103, 7694-7699.
66. Schmoller, K. M., Semmrich, C. and Bausch, A. R. (2011). Slow down of actin depolymerization by cross-linking molecules. J. Struct. Biol. 173, 350-357.
67. Sheetz, M. P., Wayne, D. B. and Pearlman, A. L. (1992). Extension of filopodia by motor-dependent actin assembly. Cell Motil. Cytoskeleton 22, 160-169.
68. Spudich, J. A. and Watt, S. (1971). The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871.
69. Suarez, C., Roland, J., Boujemaa-Paterski, R., Kang, H., McCullough, B. R., Reymann, A. C., Guérin, C., Martiel, J. L., De La Cruz, E. M. and Blanchoin, L. (2011). Cofilin tunes the nucleotide state of actin filaments and severs at bare and decorated segment boundaries. Curr. Biol. 21, 862-868.
70. Svitkina, T. M. and Borisy, G. G. (1999). Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009-1026.
71. Urban, E., Jacob,S., Nemethova, M., Resch, G. P. and Small, J. V. (2010). Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat. Cell Biol. 12, 429-435.
72. Vignjevic, D., Kojima, S., Aratyn, Y., Danciu, O., Svitkina, T. and Borisy, G. G. (2006). Role of fascin in filopodial protrusion. J. Cell Biol. 174, 863-875.
73. Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., Segall, J., Eddy, R., Miki, H., Takenawa, T. and Condeelis J. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452.