Control of growth cone motility and morphology by LIM kinase and slingshot via phosphorylation and dephosphorylation of cofilin

Journal of Neuroscience

Volumn 23, Issue 7, 2003, Pages 2527-2537

  Endo, Mitsuharu ^a   Ohashi, Kazumasa ^a   Sasaki, Yukio ^b   Goshima, Yoshio ^b   Niwa, Ryusuke ^c,d   Uemura, Tadashi ^c,d   Mizuno, Kensaku ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Actin depolymerizing factor; Cofilin; Growth cone guidance; LIM kinase; Neurite outgrowth; Slingshot

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; COFILIN; GENE PRODUCT; LIM KINASE; LIM KINASE 1; LIM PROTEIN; PHOSPHATASE; PROTEIN; PROTEIN ISL 1; PROTEIN LIN 11; PROTEIN MEC 3; PROTEIN SLINGSHOT; UNCLASSIFIED DRUG;

ACTIN FILAMENT; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHICK EMBRYO; CONTROLLED STUDY; CYTOSKELETON; DEPHOSPHORYLATION; DNA SEQUENCE; EMBRYO; ENZYME STRUCTURE; FILOPODIUM; GROWTH CONE; GROWTH CONE GUIDANCE; GROWTH CONE MOTILITY; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SPINAL GANGLION;

EID: 0037389872     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-07-02527.2003     Document Type: Article

References (52)

1. Agnew BJ, Minamide LS, Bamburg JR (1995) Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem 270:17582-17587.
2. Aizawa H, Wakatsuki S, Ishii A, Moriyama K, Sasaki Y, Ohashi K, SekineAizawa Y, Sehara-Fujisawa A, Mizuno K, Goshima Y, Yahara I (2001) Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 4:367-373.
3. Amano T, Tanabe K, Eto T, Narumiya S, Mizuno K (2001) LIM-kinase 2 induces formation of stress fibres, focal adhesions and membrane blebs, dependent on its activation by Rho-associated kinase-catalysed phosphorylation at threonine-505. Biochem J 354:149-159.
4. Amano T, Kaji N, Ohashi K, Mizuno K (2002) Mitosis-specific activation of LIM motif-containing protein kinase and roles of cofilin phosphorylation and dephosphorylation in mitosis. J Biol Chem 277:22093-22102.
5. Arber S, Barbayannis FA, Hanser H, Schneider C, Stanyon CA, Bernard O, Caroni P (1998) Regulation ofactin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393:805-809.
6. Bamburg JR (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15:185-230.
7. Bamburg JR, Bray D (1987) Distribution and cellular localization of actin depolymerizing factor. J Cell Biol 105:2817-2825.
8. Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, Mizuno K, Maekawa M, Ishizaki T, Narumiya S (2000) A critical role for a Rhoassociated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26:431-441.
9. 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.
10. Carlier MF, Ressad F, Pantaloni D (1999) Control of actin dynamics in cell motility: role of ADF/cofilin. J Biol Chem 274:33827-33830.
11. 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.
12. Chen H, Bernstein BW, Bamburg JR (2000) Regulating actin-filament dynamics in vivo. Trends Biochem Sci 25:19-23.
13. Condeelis J (2001) How is actin polymerization nucleated in vivo? Trends Cell Biol 11:288-293.
14. Dickson BJ (2001) Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11:103-110.
15. Edwards DC, Sanders LC, Bokoch GM, Gill GN (1999) Activation of LIMkinase by Pak1 couples Rac/Cdc42 GTPases signaling to actin cytoskeletal dynamics. Nat Cell Biol 1:253-259.
16. Fournier AE, Strittmatter SM (2001) Repulsive factors and axon regeneration in the CNS. Curr Opin Neurobiol 11:89-94.
17. Frangiskakis JM, Ewart AK, Morris CA, Mervis CB, Bertrand J, Robinson BF, Klein BP, Ensing GJ, Everett LA, Green ED, Proschel C, Gutowski NJ, Noble M, Atkinson DL, Odelberg SJ, Keating MT (1996) LIM-kinase 1 hemizygosity implicated in impaired visuospatial constructive cognition. Cell 86:59-69.
18. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM (1995) Collapsininduced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376:509-514.
19. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514.
20. Jin Z, Strittmatter SM (1997) Rac1 mediates collapsin-1-induced growth cone collapse. J Neurosci 17:6256-6263.
21. Kuhn TB, Meberg PJ, Brown MD, Bernstein BW, Minamide LS, Jensen JR, Okada K, Soda EA, Bamburg JR (2000) Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J Neurobiol 44:126-144.
22. Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1:173-180.
23. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, Narumiya S (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285:895-898.
24. McGrath JL, Osborn EA, Tardy YS, Dewey Jr CF, Hartwig JH (2000) Regulation of the actin cycle in vivo by actin filament severing. Proc Natl Acad Sci USA 97:6532-6537.
25. Meberg PJ (2000) Signal-regulated ADF/cofilin activity and growth cone motility. Mol Neurobiol 21:97-107.
26. Meberg PJ, Bamburg JR (2000) Increase in neurite outgrowth mediated by overexpression ofactin depolymerizing factor. J Neurosci 20:2459-2469.
27. Meng Y, Zhang Y, Tregoubov V, Janus C, Cruz L, Jackson M, Lu WY, MacDonald JF, Wang JY, Falls DL, Jia Z (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35:121-133.
28. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
29. Mizuno K, Okano I, Ohashi K, Nunoue K, Kuma K, Miyata T, Nakamura T (1994) Identification of a human cDNA encoding a novel protein kinase with two repeats of the LIM/double zinc finger motif. Oncogene 9:1605-1612.
30. Moon A, Drubin DG (1995) The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol Biol Cell 6:1423-1431.
31. Mori T, Okano I, Mizuno K, Tohyama M, Wanaka A (1997) Comparison of tissue distribution of two novel serine/threonine kinase genes containing the LIM motif (LIMK-1 and LIMK-2) in the developing rat. Mol Brain Res 45:247-254.
32. 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.
33. Moriyama K, Yahara I (2002) The actin-severing activity of cofilin is exerted by the interplay of three distinct sites on cofilin and essential for cell viability. Biochem J 365:147-155.
34. Mueller BK (1999) Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci 22:351-388.
35. 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 108:233-246.
36. Nunoue K, Ohashi K, Okano I, Mizuno K (1995) LIMK-1 and LIMK-2, two members of a LIM motif-containing protein kinase family. Oncogene 11:701-710.
37. Ohashi K, Toshima J, Tajinda K, Nakamura T, Mizuno K (1994) Molecular cloning of a chick lung cDNA encoding a novel protein kinase with N-terminal two LIM/double zinc finger motifs. J Biochem 111:636-642.
38. Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K (2000) Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275:3577-3582.
39. Okano I, Hiraoka J, Otera H, Nunoue K, Ohashi K, Iwashita S, Hirai M, Mizuno K (1995) Identification and characterization of a novel family of serine/threonine kinases containing two N-terminal LIM motifs. J Biol Chem 270:31321-31330.
40. Pollard T, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545-576.
41. Proschel C, Blouin MJ, Gutowski NJ, Ludwig R, Noble M (1995) Limk1 is predominantly expressed in neural tissues and phosphorylates serine, threonine and tyrosine residues in vitro. Oncogene 11:1271-1281.
42. Sasaki Y, Cheng C, Uchida Y, Nakajima O, Ohshima T, Yagi T, Taniguchi M, Nakayama T, Kishida R, Kudo Y, Ohno S, Nakamura F, Goshima Y (2002) Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35:907-920.
43. Song HI, Poo MM (2001) The cell biology of neuronal navigation. Nat Cell Biol 3:E81-E88.
44. Sumi T, Matsumoto K, Takai Y, Nakamura T (1999) Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42activated LIM-kinase-2. J Cell Biol 147:1519-1532.
45. Tanaka E, Sabry J (1995) Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
46. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
47. 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 12:1131-1145.
48. Toshima J, Toshima JY, Suzuki M, Noda T, Mizuno K (2001b) Cell-typespecific expression of a TESK1 promoter-linked lacZ gene in transgenic mice. Biochem Biophys Res Commun 286:566-573.
49. Toshima J, Toshima JY, Takeuchi K, Mori R, Mizuno K (2001c) Cofilin phosphorylation and actin reorganization activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells. Biol Chem 276:31449-31458.
50. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263-270.
51. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393:809-812.
52. Zebda N, Bernard O, Bailly M, Welti S, Lawrence DS, Condeelis IS (2000) Phosphorylation of ADF/cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J Cell Biol 151:1119-1128.