Distributed actin turnover in the lamellipodium and FRAP kinetics

Biophysical Journal

Volumn 104, Issue 1, 2013, Pages 247-257

  Smith, Matthew B ^a   Kiuchi, Tai ^b   Watanabe, Naoki ^b   Vavylonis, Dimitrios ^a  

^a LEHIGH UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; DIFFUSION; FIBROBLAST; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; KINETICS; METABOLISM; MICROSCOPY; PSEUDOPODIUM;

ACTINS; ANIMALS; COMPUTER SIMULATION; DIFFUSION; FIBROBLASTS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; KINETICS; MICROSCOPY; MODELS, BIOLOGICAL; PSEUDOPODIA;

EID: 84872141055     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.11.3819     Document Type: Article

References (58)

1. T.D. Pollard, and J.A. Cooper Actin, a central player in cell shape and movement Science 326 2009 1208 1212
2. N. Watanabe Inside view of cell locomotion through single-molecule: fast F-/G-actin cycle and G-actin regulation of polymer restoration Proc. Jpn. Acad. B 86 2010 62 83
3. T.M. Svitkina, and A.B. Verkhovsky G.G. Borisy Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation J. Cell Biol. 139 1997 397 415 (Pubitemid 27459313)
4. A.J. Ridley, and M.A. Schwartz A.R. Horwitz Cell migration: integrating signals from front to back Science 302 2003 1704 1709 (Pubitemid 37505725)
5. J.A. Theriot, and T.J. Mitchison Actin microfilament dynamics in locomoting cells Nature 352 1991 126 131 (Pubitemid 21896707)
6. M. Bailly, and F. Macaluso J.S. Condeelis Relationship between Arp2/3 complex and the barbed ends of actin filaments at the leading edge of carcinoma cells after epidermal growth factor stimulation J. Cell Biol. 145 1999 331 345 (Pubitemid 29198305)
7. A.Y. Chan, and S. Raft J.S. Condeelis EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells J. Cell Sci. 111 1998 199 211 (Pubitemid 28064145)
8. D. van Goor, and C. Hyland P. Forscher The role of actin turnover in retrograde actin network flow in neuronal growth cones PLoS ONE 7 2012 e30959
9. N. Watanabe, and T.J. Mitchison Single-molecule speckle analysis of actin filament turnover in lamellipodia Science 295 2002 1083 1086 (Pubitemid 34132240)
10. A. Ponti, and A. Matov G. Danuser Periodic patterns of actin turnover in lamellipodia and lamellae of migrating epithelial cells analyzed by quantitative fluorescent speckle microscopy Biophys. J. 89 2005 3456 3469 (Pubitemid 41636100)
11. T. Miyoshi, and T. Tsuji N. Watanabe Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: evidence of frequent filament severing J. Cell Biol. 175 2006 947 955 (Pubitemid 44969200)
12. F.P. Lai, and M. Szczodrak K. Rottner Arp2/3 complex interactions and actin network turnover in lamellipodia EMBO J. 27 2008 982 992 (Pubitemid 351508144)
13. K. Ohashi, and S. Fujiwara K. Mizuno LIM kinase has a dual role in regulating lamellipodium extension by decelerating the rate of actin retrograde flow and the rate of actin polymerization J. Biol. Chem. 286 2011 36340 36351
14. P. Hotulainen, and E. Paunola P. Lappalainen Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells Mol. Biol. Cell 16 2005 649 664 (Pubitemid 40165562)
15. C. Le Clainche, and M.F. Carlier Regulation of actin assembly associated with protrusion and adhesion in cell migration Physiol. Rev. 88 2008 489 513 (Pubitemid 351520086)
16. Y. Tardy, and J.L. McGrath C.F. Dewey Interpreting photoactivated fluorescence microscopy measurements of steady-state actin dynamics Biophys. J. 69 1995 1674 1682
17. J.L. McGrath, and Y. Tardy J.H. Hartwig Simultaneous measurements of actin filament turnover, filament fraction, and monomer diffusion in endothelial cells Biophys. J. 75 1998 2070 2078 (Pubitemid 28455203)
18. G. Carrero, and E. Crawford G. de Vries Characterizing fluorescence recovery curves for nuclear proteins undergoing binding events Bull. Math. Biol. 66 2004 1515 1545 (Pubitemid 39444482)
19. A. Mogilner, and L. Edelstein-Keshet Regulation of actin dynamics in rapidly moving cells: a quantitative analysis Biophys. J. 83 2002 1237 1258 (Pubitemid 34977700)
20. I.R. Kuznetsov, M. Herant, and M. Dembo Analysis of actin FLAP dynamics in the leading lamella PLoS ONE 5 2010 e10082
21. P.J. Michalski, and A.E. Carlsson The effects of filament aging and annealing on a model lamellipodium undergoing disassembly by severing Phys. Biol. 7 2010 026004
22. C.H. Schreiber, M. Stewart, and T. Duke Simulation of cell motility that reproduces the force-velocity relationship Proc. Natl. Acad. Sci. USA 107 2010 9141 9146
23. I.L. Novak, B.M. Slepchenko, and A. Mogilner Quantitative analysis of G-actin transport in motile cells Biophys. J. 95 2008 1627 1638
24. F. Huber, J. Käs, and B. Stuhrmann Growing actin networks form lamellipodium and lamellum by self-assembly Biophys. J. 95 2008 5508 5523
25. J.A. Ditlev, and N.M. Vacanti L.M. Loew An open model of actin dendritic nucleation Biophys. J. 96 2009 3529 3542
26. B. Stuhrmann, F. Huber, and J. Käs Robust organizational principles of protrusive biopolymer networks in migrating living cells PLoS ONE 6 2011 e14471
27. D. Zicha, and I.M. Dobbie G.A. Dunn Rapid actin transport during cell protrusion Science 300 2003 142 145 (Pubitemid 36423048)
28. M. Kapustina, and E. Vitriol K. Jacobson Modeling capping protein FRAP and CALI experiments reveals in vivo regulation of actin dynamics Cytoskeleton (Hoboken) 67 2010 519 534
29. M.B. Smith, and E. Karatekin D. Vavylonis Interactive, computer-assisted tracking of speckle trajectories in fluorescence microscopy: application to actin polymerization and membrane fusion Biophys. J. 101 2011 1794 1804
30. G.L. Ryan, and H.M. Petroccia D. Vavylonis Excitable actin dynamics in lamellipodial protrusion and retraction Biophys. J. 102 2012 1493 1502
31. H. Engelke, D. Heinrich, and J.O. Rädler Probing GFP-actin diffusion in living cells using fluorescence correlation spectroscopy Phys. Biol. 7 2010 046014
32. T. Kiuchi, and T. Nagai K. Mizuno Measurements of spatiotemporal changes in G-actin concentration reveal its effect on stimulus-induced actin assembly and lamellipodium extension J. Cell Biol. 193 2011 365 380
33. V.C. Abraham, and V. Krishnamurthi F. Lanni The actin-based nanomachine at the leading edge of migrating cells Biophys. J. 77 1999 1721 1732 (Pubitemid 29407343)
34. S.A. Koestler, and K. Rottner J.V. Small F- and G-actin concentrations in lamellipodia of moving cells PLoS ONE 4 2009 e4810
35. L.P. Cramer, L.J. Briggs, and H.R. Dawe Use of fluorescently labeled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells Cell Motil. Cytoskeleton 51 2002 27 38 (Pubitemid 34101415)
36. B.W. Bernstein, and J.R. Bamburg ADF/cofilin: a functional node in cell biology Trends Cell Biol. 20 2010 187 195
37. C. Chan, C.C. Beltzner, and T.D. Pollard Cofilin dissociates Arp2/3 complex and branches from actin filaments Curr. Biol. 19 2009 537 545
38. J.L. Henty, and S.W. Bledsoe C.J. Staiger Arabidopsis actin depolymerizing factor4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells Plant Cell 23 2011 3711 3726
39. T. Kiuchi, and K. Ohashi K. Mizuno Cofilin promotes stimulus-induced lamellipodium formation by generating an abundant supply of actin monomers J. Cell Biol. 177 2007 465 476 (Pubitemid 46718275)
40. R.E. Mahaffy, and T.D. Pollard Kinetics of the formation and dissociation of actin filament branches mediated by Arp2/3 complex Biophys. J. 91 2006 3519 3528 (Pubitemid 44788285)
41. L. Cai, and A.M. Makhov J.E. Bear Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia Cell 134 2008 828 842
42. T.L. Hill Length dependence of rate constants for end-to-end association and dissociation of equilibrium linear aggregates Biophys. J. 44 1983 285 288
43. E. Andrianantoandro, and L. Blanchoin T.D. Pollard Kinetic mechanism of end-to-end annealing of actin filaments J. Mol. Biol. 312 2001 721 730 (Pubitemid 33116736)
44. K. Okada, and L. Blanchoin J.R. Bamburg Xenopus actin-interacting protein 1 (XAip1) enhances cofilin fragmentation of filaments by capping filament ends J. Biol. Chem. 277 2002 43011 43016 (Pubitemid 35285681)
45. V. Okreglak, and D.G. Drubin Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway J. Cell Biol. 188 2010 769 777
46. T. Tsuji, and T. Miyoshi N. Watanabe An order of magnitude faster AIP1-associated actin disruption than nucleation by the Arp2/3 complex in lamellipodia PLoS ONE 4 2009 e4921
47. E. Urban, and S. Jacob J.V. Small Electron tomography reveals unbranched networks of actin filaments in lamellipodia Nat. Cell Biol. 12 2010 429 435
48. C. Yang, and T. Svitkina Visualizing branched actin filaments in lamellipodia by electron tomography Nat. Cell Biol. 13 2011 1012 1013 author reply 1013-1014
49. M. Vinzenz, and M. Nemethova J.V. Small Actin branching in the initiation and maintenance of lamellipodia J. Cell Sci. 125 2012 2775 2785
50. C.A. Ydenberg, and B.A. Smith B.L. Goode Cease-fire at the leading edge: new perspectives on actin filament branching, debranching, and cross-linking Cytoskeleton 68 2011 596 602
51. C. Pack, and K. Saito M. Kinjo Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs Biophys. J. 91 2006 3921 3936 (Pubitemid 44788334)
52. D. Breitsprecher, and A.K. Kiesewetter J. Faix Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation EMBO J. 27 2008 2943 2954
53. S.D. Hansen, and R.D. Mullins VASP is a processive actin polymerase that requires monomeric actin for barbed end association J. Cell Biol. 191 2010 571 584
54. A. Ponti, and M. Machacek G. Danuser Two distinct actin networks drive the protrusion of migrating cells Science 305 2004 1782 1786 (Pubitemid 39249647)
55. Reference deleted in proof.
56. L. Amin, and E. Ercolini V. Torre The elementary events underlying force generation in neuronal lamellipodia Sci. Rep. 1 2011 153
57. K. Keren, and P.T. Yam J.A. Theriot Intracellular fluid flow in rapidly moving cells Nat. Cell Biol. 11 2009 1219 1224
58. E.M. Craig, and D. van Goor A. Mogilner Membrane tension, myosin force, and actin turnover maintain actin treadmill in the nerve growth cone Biophys. J. 102 2012 1503 1513