Can filament treadmilling alone account for the F-actin turnover in lamellipodia?

Cytoskeleton

Volumn 70, Issue 4, 2013, Pages 179-190

  Miyoshi, Takushi ^a,c   Watanabe, Naoki ^b  

^a KYOTO UNIVERSITY FACULTY OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c JAPANESE RED CROSS WAKAYAMA MEDICAL CENTER   (Japan)

Author keywords

Actin filament turnover; Cofilin; Filament severing; Lamellipodia; Single molecule speckle (SiMS) microscopy

Indexed keywords

F ACTIN;

ACCELERATION; ACTIN FILAMENT; ARTICLE; CELL FUNCTION; DEPOLYMERIZATION; FILAMENT TREADMILLING; IN VIVO STUDY; LAMELLIPODIUM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN METABOLISM;

ACTINS; ANIMALS; CELL MOVEMENT; HUMANS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; PSEUDOPODIA; XENOPUS LAEVIS;

EID: 84876314947     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21098     Document Type: Article

References (67)

1. Abraham VC, Krishnamurthi V, Taylor DL, Lanni F. 1999. The actin-based nanomachine at the leading edge of migrating cells. Biophys J 77:1721-1732.
2. Andrianantoandro E, Pollard TD. 2006. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13-23.
3. Bamburg JR, Bernstein BW. 2010. Roles of ADF/cofilin in actin polymerization and beyond. F1000 Biol Rep 2:62.
4. Bindschadler M, Osborn EA, Dewey CF Jr, McGrath JL. 2004. A mechanistic model of the actin cycle. Biophys J 86(5):2720-2739.
5. Borisy GG, Svitkina TM. 2000. Actin machinery: Pushing the envelope. Curr Opin Cell Biol 12(1):104-112.
6. Breitsprecher D, Kiesewetter AK, Linkner J, Urbanke C, Resch GP, Small JV, Faix J. 2008. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J 27:2943-2954.
7. Brieher WM, Kueh HY, Ballif BA, Mitchison TJ. 2006. Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J Cell Biol 175:315-324.
8. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, 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.
9. Carlsson AE. 2006. Stimulation of actin polymerization by filament severing. Biophys J 90:413-422.
10. Chan AY, Bailly M, Zebda N, Segall JE, Condeelis JS. 2000. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol 148:531-542.
11. Chan C, Beltzner CC, Pollard TD. 2009. Cofilin dissociates Arp2/3 complex and branches from actin filaments. Curr Biol 19:537-545.
12. DiNubile MJ, Cassimeris L, Joyce M, Zigmond SH. 1995. Actin filament barbed-end capping activity in neutrophil lysates: The role of capping protein-beta 2. Mol Biol Cell 6:1659-1671.
13. Disanza A, Carlier MF, Stradal TE, Didry D, Frittoli E, Confalonieri S, Croce A, Wehland J, Di Fiore PP, Scita G. 2004. Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat Cell Biol 6:1180-1188.
14. Ditlev JA, Vacanti NM, Novak IL, Loew LM. 2009. An open model of actin dendritic nucleation. Biophys J 96:3529-3542.
15. Estornes Y, Gay F, Gevrey JC, Navoizat S, Nejjari M, Scoazec JY, Chayvialle JA, Saurin JC, Abello J. 2007. Differential involvement of destrin and cofilin-1 in the control of invasive properties of Isreco1 human colon cancer cells. Int J Cancer 121:2162-2171.
16. Forscher P, Smith SJ. 1988. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107:1505-1516.
17. Fujiwara I, Vavylonis D, Pollard TD. 2007. Polymerization kinetics of ADP- and ADP-Pi-actin determined by fluorescence microscopy. Proc Natl Acad Sci USA 104:8827-8832.
18. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304:743-736.
19. Hansen SD, Mullins RD. 2010. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J Cell Biol 191:571-584.
20. Higashida C, Miyoshi T, Fujita A, Oceguera-Yanez F, Monypenny J, Andou Y, Narumiya S, Watanabe N. 2004. Actin polymerization-driven molecular movement of mDia1 in living cells. Science 303:2007-2010.
21. Higashida C, Suetsugu S, Tsuji T, Monypenny J, Narumiya S, Watanabe N. 2008. G-actin regulates rapid induction of actin nucleation by mDia1 to restore cellular actin polymers. J Cell Sci 121:3403-3412.
22. Hotulainen P, Paunola E, Vartiainen MK, Lappalainen P. 2005. Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol Biol Cell 16:649-664.
23. Hug C, Jay PY, Reddy I, McNally JG, Bridgman PC, Elson EL, Cooper JA. 1995. Capping protein levels influence actin assembly and cell motility in dictyostelium. Cell 81:591-600.
24. Kiuchi T, Ohashi K, Kurita S, Mizuno K. 2007. Cofilin promotes stimulus-induced lamellipodium formation by generating an abundant supply of actin monomers. J Cell Biol 177:465-476.
25. Kiuchi T, Nagai T, Ohashi K, Mizuno K. 2011. Measurements of spatiotemporal changes in G-actin concentration reveal its effect on stimulus-induced actin assembly and lamellipodium extension. J Cell Biol 193:365-380.
26. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD. 2006. Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124:423-435.
27. Kueh HY, Charras GT, Mitchison TJ, Brieher WM. 2008. Actin disassembly by cofilin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers. J Cell Biol 182:341-353.
28. Lai FP, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, Stradal TE, Dunn GA, Small JV, Rottner K. 2008. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27:982-992.
29. Maciver SK. 1998. How ADF/cofilin depolymerizes actin filaments. Curr Opin Cell Biol 10:140-144.
30. Maly IV, Borisy GG. 2001. Self-organization of a propulsive actin network as an evolutionary process. Proc Natl Acad Sci USA 98:11324-11329.
31. Millius A, Watanabe N, Weiner OD. 2012. Diffusion, capture and recycling of SCAR/WAVE and Arp2/3 complexes observed in cells by single-molecule imaging. J Cell Sci 125:1165-1176.
32. Miyoshi T, Tsuji T, Higashida C, Hertzog M, Fujita A, Narumiya S, Scita G, Watanabe N. 2006. Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: Evidence of frequent filament severing. J Cell Biol 175:947-955.
33. Mogilner A, Edelstein-Keshet L. 2002. Regulation of actin dynamics in rapidly moving cells: A quantitative analysis. Biophys J 83(3):1237-1258.
34. Mogilner A, Oster G. 2003. Polymer motors: Pushing out the front and pulling up the back. Curr Biol 13:R721-R733.
35. Moriyama K, Yahara I. 1999. Two activities of cofilin, severing and accelerating directional depolymerization of actin filaments, are affected differentially by mutations around the actin-binding helix. EMBO J 18:6752-6761.
36. Nagata-Ohashi K, Ohta Y, Goto K, Chiba S, Mori R, Nishita M, Ohashi K, Kousaka K, Iwamatsu A, Niwa R, et al. 2004. A pathway of neuregulin-induced activation of cofilin-phosphatase Slingshot and cofilin in lamellipodia. J Cell Biol 165:465-471.
37. Narita A, Takeda S, Yamashita A, Maeda Y. 2006. Structural basis of actin filament capping at the barbed-end: A cryo-electron microscopy study. EMBO J 25:5626-5633.
38. Novak IL, Slepchenko BM, Mogilner A. 2008. Quantitative analysis of G-actin transport in motile cells. Biophys J 95(4):1627-1638.
39. Okada K, Blanchoin L, Abe H, Chen H, Pollard TD, Bamburg JR. 2002. Xenopus actin-interacting protein 1 (XAip1) enhances cofilin fragmentation of filaments by capping filament ends. J Biol Chem 277:43011-43016.
40. Okada K, Ravi H, Smith EM, Goode BL. 2006. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: A coordinated mechanism for severing and capping filaments. Mol Biol Cell 17:2855-2868.
41. Ono S. 2003. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: New blades for twisted filaments. Biochemistry 42:13363-13370.
42. Pavlov D, Muhlrad A, Cooper J, Wear M, Reisler E. 2007. Actin filament severing by cofilin. J Mol Biol 365:1350-1358.
43. Pollard TD, Blanchoin L, Mullins RD. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545-576.
44. Pudney M, Varma MG, Leake CJ. 1973. Establishment of a cell line (XTC-2) from the South African clawed toad, Xenopus laevis. Experientia 29:466-467.
45. Rogers SL, Wiedemann U, Stuurman N, Vale RD. 2003. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J Cell Biol 162:1079-1088.
46. Ross SM. 1996.Stochastic Process. New York:John Wiley & Sons Inc.
47. Ryan GL, Petroccia HM, Watanabe N, Vavylonis D. 2012a. Excitable actin dynamics in lamellipodial protrusion and retraction. Biophys J 102:1493-1502.
48. Ryan GL, Watanabe N, Vavylonis D. 2012b. A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. Cytoskeleton (Hoboken) 69:195-206.
49. Schafer DA, Jennings PB, Cooper JA. 1996. Dynamics of capping protein and actin assembly in vitro: Uncapping barbed ends by polyphosphoinositides. J Cell Biol 135:169-179.
50. Schaus TE, Borisy GG. 2008. Performance of a population of independent filaments in lamellipodial protrusion. Biophys J 95:1393-1411.
51. Small JV, Isenberg G, Celis JE. 1978. Polarity of actin at the leading edge of cultured cells. Nature 272:638-639.
52. Small JV, Herzog M, Anderson K. 1995. Actin filament organization in the fish keratocyte lamellipodium. J Cell Biol 129:1275-1286.
53. Smith MB, Karatekin E, Gohlke A, Mizuno H, Watanabe N, Vavylonis D. 2011. Interactive, computer-assisted tracking of speckle trajectories in fluorescence microscopy: Application to actin polymerization and membrane fusion. Biophys J 101:1794-1804.
54. Smith MB, Kiuchi T, Watanabe N, Vavylonis D. 2013. Distributed actin turnover in the lamellipodium and FRAP kinetics. Biophys J 104:247-257.
55. Southwick FS, Young CL. 1990. The actin released from profilin-actin complexes is insufficient to account for the increase in F-actin in chemoattractant-stimulated polymorphonuclear leukocytes. J Cell Biol 110:1965-1973.
56. Stuhrmann B, Huber F, Kas J. 2011. Robust organizational principles of protrusive biopolymer networks in migrating living cells. PLoS ONE 6:e14471.
57. Svitkina TM, Borisy GG. 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.
58. Tania N, Prosk E, Condeelis J, Edelstein-Keshet L. 2011. A temporal model of cofilin regulation and the early peak of actin barbed ends in invasive tumor cells. Biophys J 100:1883-1892.
59. Theriot JA, Mitchison TJ. 1991. Actin microfilament dynamics in locomoting cells. Nature 352:126-131.
60. Tsuji T, Miyoshi T, Higashida C, Narumiya S, Watanabe N. 2009. An order of magnitude faster AIP1-associated actin disruption than nucleation by the Arp2/3 complex in lamellipodia. PLoS ONE 4:e4921.
61. Urban E, Jacob S, Nemethova M, Resch GP, Small JV. 2010. Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat Cell Biol 12:429-435.
62. Vale RD. 2008. Microscopes for fluorimeters: The era of single molecule measurements. Cell 135:779-785.
63. Wang YL. 1985. Exchange of actin subunits at the leading edge of living fibroblasts: Possible role of treadmilling. J Cell Biol 101:597-602.
64. Watanabe N. 2010. Inside view of cell locomotion through single-molecule: Fast F-/G-actin cycle and G-actin regulation of polymer restoration. Proc Jpn Acad Ser B Phys Biol Sci 86:62-83.
65. Watanabe N. 2012. Fluorescence single-molecule imaging of actin turnover and regulatory mechanisms. Meth Enzymol 505:219-232.
66. Watanabe N, Mitchison TJ. 2002. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295:1083-1086.
67. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S. 1999. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1:136-43.