Regulating filopodial dynamics through actin-depolymerizing factor/cofilin

Anatomical Science International

Volumn 79, Issue 4, 2004, Pages 173-183

  Fass, Joseph ^a   Gehler, Scott ^b   Sarmiere, Patrick ^a   Letourneau, Paul ^b   Bamburg, James R ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Actin depolymerizing factor; Cofilin; Filopodia; Growth cone

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; COFILIN; F ACTIN;

ACTIN MYOSIN INTERACTION; FILOPODIUM; GROWTH CONE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

EID: 10944222221     PISSN: 14476959     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1447-073x.2004.00087.x     Document Type: Review

References (84)

1. Amano M, Ito M, Kimura K et al. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271, 20 246-9.
2. Arber S, Barbayannis FA, Hanser H et al. (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805-9.
3. Bamburg JR, McGough A, Ono S (1999) Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9 364-70.
4. Bray D, Chapman K (1985) Analysis of microspike movements on the neuronal growth cone. J Neurosci 5, 3204-13.
5. Bridgman PC (2002) Growth cones contain myosin II bipolar filament arrays. Cell Motil Cytoskeleton 52, 91-6.
6. Bridgman PC, Dailey ME (1989) The organization of myosin and actin in rapid frozen nerve growth cones. J Cell Biol 108, 95-109.
7. Bridgman PC, Dave S, Asnes CF, Tullio AN, Adelstein RS (2001) Myosin IIB is required for growth cone motility. J Neurosci 21 6159-69.
8. Brown J, Bridgman PC (2003a) Role of myosin II in axon outgrowth. J Histochem Cytochem 51, 421-8.
9. Brown ME, Bridgman PC (2003b) Retrograde flow rate is increased in growth cones from myosin IIB knockout mice. J Cell Sci 116, 1087-94.
10. Brown ME, Bridgman PC (2004) Myosin function in nervous and sensory systems. J Neurobiol 58, 118-30.
11. Carlier MF, Laurent V, Santolini J et al. (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: Implication in actin-based motility. J Cell Biol 136 1307-22.
12. Cheung A, Dantzig JA, Hollingworth S et al. (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4, 83-8.
13. Cohan CS, Welnhofer EA, Zhao L, Matsumura F, Yamashiro S (2001) Role of the actin bundling protein fascin in growth cone morphogenesis: Localization in filopodia and lamellipodia. Cell Motil Cytoskeleton 48, 109-20.
14. Dawe HR, Minamide LS, Bamburg JR, Cramer LP (2003) ADF/cofilin controls cell polarity during fibroblast migration. Curr Biol 13, 252-7.
15. DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE (2002) Spatial regulation of actin dynamics: A tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115, 4649-60.
16. DesMarais V, Macaluso F, Condeelis J, Bailly M (2004) Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 117, 3499-510.
17. Diefenbach TJ, Latham VM, Yimlamai D, Liu CA, Herman IM, Jay DG (2002) Myosin 1c and myosin IIB serve opposing roles in lamellipodial dynamics of the neuronal growth cone. J Cell Biol 158, 1207-17.
18. Egan MF, Kojima M, Callicott JH et al. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-69.
19. Endo M, Ohashi K, Sasaki Y et al. (2003) Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 23 2527-37.
20. Evans LL, Hammer J, Bridgman PC (1997) Subcellular localization of myosin V in nerve growth cones and outgrowth from dilute-lethal neurons. J Cell Sci 110, 439-49.
21. 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, 1505-16.
22. Gallo G, Letourneau PC (1998) Localized sources of neurotrophins initiate axon collateral sprouting. J Neurosci 18 5403-14.
23. Gallo G, Letourneau PC (1999) Axon guidance: A balance of signals sets axons on the right track. Curr Biol 9, R490-2.
24. Gallo G, Letourneau PC (2004) Regulation of growth cone actin filaments by guidance cues. J Neurobiol 58, 92-102.
25. Gallo G, Lefcort FB, Letourneau PC (1997) The trkA receptor mediates growth cone turning toward a localized source of nerve growth factor. J Neurosci 17, 5445-54.
26. Gehler S, Gallo G, Veien E, Letourneau PC (2004a) p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci 24, 4363-72.
27. Gehler S, Shaw AE, Sarmiere PD, Bamburg JR, Letourneau PC (2004b) BDNF regulation of growth cone filopodial dynamics is mediated through ADF/cofilin. J Neurosci (in press).
28. 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, 743-6.
29. Gohla A, Bokoch GM (2002) 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol 12, 1704-10.
30. Goldberg DJ, Burmeister DW (1986) Stages in axon formation: Observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol 103, 1921-31.
31. Gomez TM, Robles E, Poo M, Spitzer NC (2001) Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291, 1983-7.
32. Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72, 77-98.
33. Hariri AR, Goldberg TE, Mattay VS et al. (2003) Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 23, 6690-4.
34. Heidemann SR, Lamoureux P, Buxbaum RE (1990) Growth cone behavior and production of traction force. J Cell Biol 111, 1949-57.
35. Hirose M, Ishizaki T, Watanabe N et al. (1998) Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141, 1625-36.
36. Ichetovkin I, Han J, Pang KM, Knecht DA, Condeelis JS (2000) Actin filaments are severed by both native and recombinant dictyostelium cofilin but to different extents. Cell Motil Cytoskeleton 45, 293-306.
37. Ichetovkin I, Grant W, Condeelis J (2002) Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr Biol 12, 79-84.
38. Jay DG (2000) The clutch hypothesis revisited: Ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. J Neurobiol 44, 114-25.
39. Kimura K, Ito M, Amano M et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-8.
40. Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers J (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279, 35 557-63.
41. Lappalainen P, Drubin DG (1997) Cofilin promotes rapid actin filament turnover in vivo. Nature 388, 78-82.
42. Lebrand C, Dent EW, Strasser GA et al. (2004) Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37-49.
43. Letourneau PC (1996) The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurosci 4, 111-23.
44. Lin CH, Forscher P (1995) Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763-71.
45. Lin CH, Espreafico EM, Mooselker MS, Forscher P (1996) Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-82.
46. Mallavarapu A, Mitchison T (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146, 1097-106.
47. Matsutani S, Yamamoto N (2004) Brain-derived neurotrophic factor induces rapid morphological changes in dendritic spines of olfactory bulb granule cells in cultured slices through the modulation of glutamatergic signaling. Neuroscience 123, 695-702.
48. Meberg PJ (2000) Signal-regulated ADF/cofilin activity and growth cone motility. Mol Neurobiol 21, 97-107.
49. Meberg PJ, Bamburg JR (2000) Increase in neurite outgrowth mediated by overexpression of actin depolymerizing factor. J Neurosci 20, 2459-69.
50. Meberg PJ, Ono S, Minamide LS, Takahashi M, Bamburg JR (1998) Actin depolymerizing factor and cofilin phosphorylation dynamics: Response to signals that regulate neurite extension. Cell Motil Cytoskeleton 39, 172-90.
51. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1, 761-72.
52. Mogilner A, Oster G (2003) Force generation by actin polymerization II: The elastic ratchet and tethered filaments. Biophys J 84, 1591-605.
53. Nagata-Ohashi K, Ohta Y, Goto K et al. (2004) A pathway of neuregulin-induced activation of cofilin-phosphatase Slingshot and cofilin in lamellipodia. J Cell Biol 165, 465-71.
54. Niwa R, Nagata-Ohashi K, Takeichi M, Mizuno K, Uemura T (2002) Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108, 233-46.
55. Ohta Y, Kousaka K, Nagata-Ohashi K et al. (2003) Differential activities, subcellular distribution and tissue expression patterns of three members of Slingshot family phosphatases that dephosphorylate cofilin. Genes Cells 8, 811-24.
56. Okabe S, Hirokawa N (1991) Actin dynamics in growth cones. J Neurosci 11, 1918-29.
57. Pollard TD, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29, 545-76.
58. Rosenblatt J, Agnew BJ, Abe H, Bamburg JR, Mitchison TJ (1997) Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J Cell Biol 136, 1323-32.
59. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D (1991) Microtubule behavior during guidance of pioneer neuron growth cones in situ. J Cell Biol 115, 381-95.
60. Sala C (2002) Molecular regulation of dendritic spine shape and function. Neurosignals 11, 213-23.
61. Samstag Y, Nebl G (2003) Interaction of cofilin with the serine phosphatases PP1 and PP2A in normal and neoplastic human T lymphocytes. Adv Enzyme Regul 43, 197-211.
62. Sarmiere PD, Bamburg JR (2004) Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol 58, 103-17.
63. Schaefer AW, Kabir N, Forscher P (2002) Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol 158, 139-52.
64. Shimada A, Mason CA, Morrison ME (1998) TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J Neurosci 18, 8559-70.
65. Smith CL (1994) Cytoskeletal movements and substrate interactions during initiation of neurite outgrowth by sympathetic neurons in vitro. J Neurosci 14, 384-98.
66. Steketee MB, Tosney KW (2002) Three functionally distinct adhesions in filopodia: Shaft adhesions control lamellar extension. J Neurosci 22, 8071-83.
67. Steketee M, Balazovich K, Tosney KW (2001) Filopodial initiation and a novel filament-organizing center, the focal ring. Mol Biol Cell 12, 2378-95.
68. Straight AF, Cheung A, Limouze J et al. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299, 1743-7.
69. Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM (2004) Arp2/3 is a negative regulator of growth cone translocation. Neuron 43, 81-94.
70. Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44, 97-113.
71. Suter DM, Errante LD, Belotserkovsky V, Forscher P (1998) The lg superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J Cell Biol 141, 227-40.
72. Svitkina TM, Bulanova EA, Chaga OY et al. (2003) Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160, 409-21.
73. Theriot JA (1997) Accelerating on a treadmill: ADF/cofilin promotes rapid actin filament turnover in the dynamic cytoskeleton. J Cell Biol 136, 1165-8.
74. Toshima J, Toshima JY, Amano T, Yang N, Narumiya S, Mizuno K (2001a) Cofilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol Biol Cell 12, 1131-45.
75. Toshima J, Toshima JY, Takeuchi K, Mori R, Mizuno K (2001b) Cofilin phosphorylation and actin reorganization activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells. J Biol Chem 276, 31 449-58.
76. Upadhyaya A, van Oudenaarden A (2004) Actin polymerization: Forcing flat faces forward. Curr Biol 14, R467-9.
77. Wang FS, Wolenski JS, Cheney RE, Mooseker MS, Jay DG (1996) Function of myosin-V in filopodial extension of neuronal growth cones. Science 273, 660-3.
78. Wang FS, Liu CW, Diefenbach TJ, Jay DG (2003) Modeling the role of myosin 1c in neuronal growth cone turning. Biophys J 85 3319-28.
79. Welnhofer EA, Zhao L, Cohan CS (1997) Actin dynamics and organization during growth cone morphogenesis in Helisoma neurons. Cell Motil Cytoskeleton 37, 54-71.
80. Wylie SR, Chantler PD (2001) Separate but linked functions of conventional myosins modulate adhesion and neurite outgrowth. Nat Cell Biol 3, 88-92.
81. Wylie SR, Wu P-J, Patel H, Chantler PD (1998) A conventional myosin motor drives neurite outgrowth. Proc Natl Acad Sci USA 95 12 967-72.
82. Yang N, Higuchi O, Ohashi K et al. (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393, 809-12.
83. Zheng JQ, Wan JJ, Poo MM (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16, 1140-9.
84. Zhou FQ, Cohan CS (2004) How actin filaments and microtubules steer growth cones to their targets. J Neurobiol 58, 84-91.