Actin migration driven by directional assembly and disassembly of membrane-anchored actin filaments

Cell Reports

Volumn 12, Issue 4, 2015, Pages 648-660

  Katsuno, Hiroko ^a   Toriyama, Michinori ^a   Hosokawa, Yoichiroh ^a   Mizuno, Kensaku ^b   Ikeda, Kazushi ^a   Sakumura, Yuichi ^a,c   Inagaki, Naoyuki ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c AICHI PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; EMBRYO; FORCE; MATHEMATICAL MODEL; MEASUREMENT; MEMBRANE BINDING; MOLECULAR BIOLOGY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; ANIMAL; AXON; CELL CULTURE; METABOLISM; NERVE FIBER TRANSPORT; PROTEIN MULTIMERIZATION;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; AXONAL TRANSPORT; AXONS; CELLS, CULTURED; PROTEIN MULTIMERIZATION; RATS;

EID: 84940989776     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.048     Document Type: Article

References (72)

1. Allard, J., and Mogilner, A. (2013). Traveling waves in actin dynamics and cell motility. Curr. Opin. Cell Biol. 25, 107-115.
2. 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.
3. Asano, Y., Nagasaki, A., and Uyeda, T.Q. (2008). Correlated waves of actin filaments and PIP3 in Dictyostelium cells. Cell Motil. Cytoskeleton 65, 923-934.
4. Bamburg, J.R. (1999). Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185-230.
5. Bamburg, J.R., McGough, A., and Ono, S. (1999). Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol. 9, 364-370.
6. Black, M.M., and Lasek, R.J. (1979). Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res. 171, 401-413.
7. Bravo-Cordero, J.J., Magalhaes, M.A., Eddy, R.J., Hodgson, L., and Condeelis, J. (2013). Functions of cofilin in cell locomotion and invasion. Nat. Rev. Mol. Cell Biol. 14, 405-415.
8. Bray, J.J., Fernyhough, P., Bamburg, J.R., and Bray, D. (1992). Actin depolymerizing factor is a component of slow axonal transport. J. Neurochem. 58, 2081-2087.
9. Bretschneider, T., Anderson, K., Ecke, M., Müller-Taubenberger, A., Schroth-Diez, B., Ishikawa-Ankerhold, H.C., and Gerisch, G. (2009). The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. Biophys. J. 96, 2888-2900.
10. Brown, A. (2003). Axonal transport of membranous and nonmembranous cargoes: a unified perspective. J. Cell Biol. 160, 817-821.
11. Bryce, N.S., Clark, E.S., Leysath, J.L., Currie, J.D., Webb, D.J., and Weaver, A.M. (2005). Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr. Biol. 15, 1276-1285.
12. Bugyi, B., and Carlier, M.F. (2010). Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449-470.
13. Carlsson, A.E. (2010a). Actin dynamics: from nanoscale to microscale. Annu. Rev. Biophys. 39, 91-110.
14. Carlsson, A.E. (2010b). Dendritic actin filament nucleation causes traveling waves and patches. Phys. Rev. Lett. 104, 228102.
15. Case, L.B., and Waterman, C.M. (2011). Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PLoS ONE 6, e26631.
16. Chan, C.E., and Odde, D.J. (2008). Traction dynamics of filopodia on compliant substrates. Science 322, 1687-1691.
17. Craig, E.M., Van Goor, D., Forscher, P., and Mogilner, A. (2012). Membrane tension, myosin force, and actin turnover maintain actin treadmill in the nerve growth cone. Biophys. J. 102, 1503-1513.
18. Cramer, L.P., Briggs, L.J., and Dawe, H.R. (2002). Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and nonmigrating cells. Cell Motil. Cytoskeleton 51, 27-38.
19. Doubrovinski, K., and Kruse, K. (2008). Cytoskeletal waves in the absence of molecular motors. Europhys. Lett. 83, 18003.
20. Endo, M., Ohashi, K., Sasaki, Y., Goshima, Y., Niwa, R., Uemura, T., and Mizuno, K. (2003). Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin. J. Neurosci. 23, 2527-2537.
21. Flynn, K.C., Pak, C.W., Shaw, A.E., Bradke, F., and Bamburg, J.R. (2009). Growth cone-like waves transport actin and promote axonogenesis and neurite branching. Dev. Neurobiol. 69, 761-779.
22. Forscher, P., and Smith, S.J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
23. Garner, J.A., and Lasek, R.J. (1982). Cohesive axonal transport of the slow component b complex of polypeptides. J. Neurosci. 2, 1824-1835.
24. Gerisch, G., Bretschneider, T., Müller-Taubenberger, A., Simmeth, E., Ecke, M., Diez, S., and Anderson, K. (2004). Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys. J. 87, 3493-3503.
25. Gerisch, G., Schroth-Diez, B., Müller-Taubenberger, A., and Ecke, M. (2012). PIP3 waves and PTEN dynamics in the emergence of cell polarity. Biophys. J. 103, 1170-1178.
26. Ghosh, M., Song, X., Mouneimne, G., Sidani, M., Lawrence, D.S., and Condeelis, J.S. (2004). Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304, 743-746.
27. Giannone, G., Dubin-Thaler, B.J., Döbereiner, H.G., Kieffer, N., Bresnick, A.R., and Sheetz, M.P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
28. Goddette, D.W., and Frieden, C. (1986). The kinetics of cytochalasin D binding to monomeric actin. J. Biol. Chem. 261, 15970-15973.
29. Hatanaka, Y., and Yamauchi, K. (2013). Excitatory cortical neurons with multipolar shape establish neuronal polarity by forming a tangentially oriented axon in the intermediate zone. Cereb. Cortex 23, 105-113.
30. Hirokawa, N. (1998). Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279, 519-526.
31. Howard, J. (1997). Molecular motors: structural adaptations to cellular functions. Nature 389, 561-567, 561-567.
32. Inagaki, N., Toriyama, M., and Sakumura, Y. (2011). Systems biology of symmetry breaking during neuronal polarity formation. Dev. Neurobiol. 71, 584-593.
33. Kakumoto, T., and Nakata, T. (2013). Optogenetic control of PIP3: PIP3 is sufficient to induce the actin-based active part of growth cones and is regulated via endocytosis. PLoS ONE 8, e70861.
34. Kanegae, Y., Takamori, K., Sato, Y., Lee, G., Nakai, M., and Saito, I. (1996). Efficient gene activation system on mammalian cell chromosomes using recombinant adenovirus producing Cre recombinase. Gene 181, 207-212.
35. Kiuchi, T., Ohashi, K., Kurita, S., and Mizuno, K. (2007). Cofilin promotes stimulus-induced lamellipodium formation by generating an abundant supply of actin monomers. J. Cell Biol. 177, 465-476.
36. Knowles, G.C., and McCulloch, C.A. (1992). Simultaneous localization and quantification of relative G and F actin content: optimization of fluorescence labeling methods. J. Histochem. Cytochem. 40, 1605-1612.
37. Lowery, L.A., and Van Vactor, D. (2009). The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332-343.
38. MacGrath, S.M., and Koleske, A.J. (2012). Cortactin in cell migration and cancer at a glance. J. Cell Sci. 125, 1621-1626.
39. Madden, K., and Snyder, M. (1998). Cell polarity and morphogenesis in budding yeast. Annu. Rev. Microbiol. 52, 687-744.
40. Medeiros, N.A., Burnette, D.T., and Forscher, P. (2006). Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8, 215-226.
41. Mogilner, A., and Oster, G. (1996). Cell motility driven by actin polymerization. Biophys. J. 71, 3030-3045.
42. Mogilner, A., and Oster, G. (2003). Polymer motors: pushing out the front and pulling up the back. Curr. Biol. 13, R721-R733.
43. Morales, M., Colicos, M.A., and Goda, Y. (2000). Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27, 539-550.
44. Nolen, B.J., Tomasevic, N., Russell, A., Pierce, D.W., Jia, Z., McCormick, C.D., Hartman, J., Sakowicz, R., and Pollard, T.D. (2009). Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034.
45. Okabe, S., and Hirokawa, N. (1990). Turnover of fluorescently labelled tubulin and actin in the axon. Nature 343, 479-482.
46. Pavlov, D., Muhlrad, A., Cooper, J., Wear, M., and Reisler, E. (2007). Actin filament severing by cofilin. J. Mol. Biol. 365, 1350-1358.
47. Podolski, J.L., and Steck, T.L. (1988). Association of deoxyribonuclease I with the pointed ends of actin filaments in human red blood cell membrane skeletons. J. Biol. Chem. 263, 638-645.
48. Pollard, T.D. (2007). Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36, 451-477.
49. Pollard, T.D., and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
50. Rizvi, S.A., Neidt, E.M., Cui, J., Feiger, Z., Skau, C.T., Gardel, M.L., Kozmin, S.A., and Kovar, D.R. (2009). Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chem. Biol. 16, 1158-1168.
51. Ruthel, G., and Banker, G. (1998). Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: a novel form of axonal transport? Cell Motil. Cytoskeleton 40, 160-173.
52. Ruthel, G., and Banker, G. (1999). Role of moving growth cone-like "wave"structures in the outgrowth of cultured hippocampal axons and dendrites. J. Neurobiol. 39, 97-106.
53. Ryan, G.L., Watanabe, N., and Vavylonis, D. (2012). A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. Cytoskeleton (Hoboken) 69, 195-206.
54. Sampath, P., and Pollard, T.D. (1991). Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30, 1973-1980.
55. Scott, D.A., Das, U., Tang, Y., and Roy, S. (2011). Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron 70, 441-454.
56. Shimada, T., Toriyama, M., Uemura, K., Kamiguchi, H., Sugiura, T., Watanabe, N., and Inagaki, N. (2008). Shootin1 interacts with actin retrograde flow and L1-CAM to promote axon outgrowth. J. Cell Biol. 181, 817-829.
57. Suter, D.M., Errante, L.D., Belotserkovsky, V., and Forscher, P. (1998). The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227-240.
58. Toriyama, M., Shimada, T., Kim, K.B., Mitsuba, M., Nomura, E., Katsuta, K., Sakumura, Y., Roepstorff, P., and Inagaki, N. (2006). Shootin1: a protein involved in the organization of an asymmetric signal for neuronal polarization. J. Cell Biol. 175, 147-157.
59. Toriyama, M., Sakumura, Y., Shimada, T., Ishii, S., and Inagaki, N. (2010). A diffusion-based neurite length-sensing mechanism involved in neuronal symmetry breaking. Mol. Syst. Biol. 6, 394.
60. Toriyama, M., Kozawa, S., Sakumura, Y., and Inagaki, N. (2013). Conversion of a signal into forces for axon outgrowth through Pak1-mediated shootin1 phosphorylation. Curr. Biol. 23, 529-534.
61. Vale, R.D., Funatsu, T., Pierce, D.W., Romberg, L., Harada, Y., and Yanagida, T. (1996). Direct observation of single kinesin molecules moving along microtubules. Nature 380, 451-453.
62. Vallee, R.B., and Bloom, G.S. (1991). Mechanisms of fast and slow axonal transport. Annu. Rev. Neurosci. 14, 59-92.
63. Van Goor, D., Hyland, C., Schaefer, A.W., and Forscher, P. (2012). The role of actin turnover in retrograde actin network flow in neuronal growth cones. PLoS ONE 7, e30959.
64. Vicker, M.G. (2002a). Eukaryotic cell locomotion depends on the propagation of self-organized reaction-diffusion waves and oscillations of actin filament assembly. Exp. Cell Res. 275, 54-66.
65. Vicker, M.G. (2002b). F-actin assembly in Dictyostelium cell locomotion and shape oscillations propagates as a self-organized reaction-diffusion wave. FEBS Lett. 510, 5-9.
66. Wang, E., and Goldberg, A.R. (1978). Binding of deoxyribonuclease I to actin: a new way to visualize microfilament bundles in nonmuscle cells. J. Histochem. Cytochem. 26, 745-749.
67. Watanabe, N., and Mitchison, T.J. (2002). Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295, 1083-1086.
68. Weiner, O.D., Marganski, W.A., Wu, L.F., Altschuler, S.J., and Kirschner, M.W. (2007). An actin-based wave generator organizes cell motility. PLoS Biol. 5, e221.
69. Whitelam, S., Bretschneider, T., and Burroughs, N.J. (2009). Transformation from spots to waves in a model of actin pattern formation. Phys. Rev. Lett. 102, 198103.
70. Willard, M., Wiseman, M., Levine, J., and Skene, P. (1979). Axonal transport of actin in rabbit retinal ganglion cells. J. Cell Biol. 81, 581-591.
71. Wilson, C.A., Tsuchida, M.A., Allen, G.M., Barnhart, E.L., Applegate, K.T., Yam, P.T., Ji, L., Keren, K., Danuser, G., and Theriot, J.A. (2010). Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465, 373-377.
72. Yildiz, A., Forkey, J.N., McKinney, S.A., Ha, T., Goldman, Y.E., and Selvin, P.R. (2003). Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300, 2061-2065.