Inhibition of glycogen synthase kinase 3β in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones

Molecular and Cellular Neuroscience

Volumn 23, Issue 4, 2003, Pages 626-637

  Owen, Rebecca ^a   Gordon Weeks, Phillip R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM; MICROTUBULE ASSOCIATED PROTEIN 5; PHOSPHOTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL SIZE; CHICKEN; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EFFECT; DRUG MECHANISM; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FILOPODIUM; GROWTH CONE; GROWTH RATE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NERVE CELL CULTURE; NERVE FIBER; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SENSORY NERVE;

EID: 0042661212     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-7431(03)00095-2     Document Type: Article

References (52)

1. Berridge M.J., Downes C.P., Hanley M.R. Neural and developmental actions of lithium a unifying hypothesis . Cell. 59:1989;411-419.
2. Bray D., Chapman K. Analysis of microspike movements on the neuronal growth cone. J. Neurosci. 5:1985;3204-3213.
3. Burstein D.E., Seeley P.J., Greene L.A. Lithium ion inhibits nerve growth factor-induced neurite outgrowth and phosphorylation of nerve growth factor-modulated microtubule-associated proteins. J. Cell Biol. 101:1985;862-870.
4. Challacombe J.F., Snow D.M., Letourneau P.C. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J. Neurosci. 17:1997;3085-3095.
5. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee C.L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 7:2000;793-803.
6. Cross D.A., Culbert A.A., Chalmers K.A., Facci L., Skaper S.D., Reith A.D. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J. Neurochem. 77:2001;94-102.
7. Dent E.W., Callaway J.L., Szebenyi G., Baas P.W., Kalil K. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J. Neurosci. 19:1999;8894-8908.
8. Dent E.W., Kalil K. Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21:2001;9757-9769.
9. Edelmann W., Zervas M., Costello P., Roback L., Fischer I., Hammarback J.A., Cowan J., Davies P., Wainer B., Kucherlapati R. Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc. Natl. Acad. Sci. USA. 93:1996;1270-1275.
10. Eickholt B.J., Walsh F.S., Doherty P. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157:2002;211-217.
11. Fan J., Mansfield S.G., Redmond T., Gordon-Weeks P.R., Raper J. The organization of F-actin and microtubules in growth cones exposed to a brain-derived collapsing factor. J. Cell Biol. 121:1993;867-878.
12. Gonzalez-Billault C., Demandt E., Wandosell F., Torres M., Bonaldo P., Stoykova A., Chowdhury K., Gruss P., Avila J., Sanchez M.P. Perinatal lethality of microtubule-associated protein 1B-deficient mice expressing alternative isoforms of the protein at low levels. Mol. Cell Neurosci. 16:2000;408-421.
13. Gonzalez-Billault C., Avila J., Caceres A. Evidence for the role of MAP1B in axon formation. Mol. Biol. Cell. 12:2001;2087-2098.
14. Gonzalez-Billault C., Owen R., Gordon-Weeks P.R., Avila J. Microtubule-associated protein 1B is involved in the initial stages of axonogenesis in peripheral nervous system cultured neurons. Brain Res. 943:2002;56-67.
15. Goold R.G., Owen R., Gordon-Weeks P.R. Glycogen synthase kinase 3β phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112:1999;3373-3384.
16. Goold R.G., Gordon-Weeks P.R. Microtubule associated protein 1B phosphorylation by glycogen synthase kinase 3β is induced during PC12 cell differentiation. J. Cell Sci. 114:2001;4273-4284.
17. Gordon-Weeks P.R., Fischer I. MAP1B expression and microtubule stability in growing and regenerating axons. Microsc. Res. Tech. 48:2000;63-74.
18. Grimes C.A., Jope R.S. The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog. Neurobiol. 65:2001;391-426.
19. Gundersen G.G., Kalnoski M.H., Bulinski J.C. Distinct populations of microtubules tyrosinated and nontyrosinated alpha-tubulins are distributed differently in vivo . Cell. 38:1984;779-789.
20. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell. 100:2000;525-535.
21. Hall A.C., Brennan A., Goold R.G., Cleverley K., Lucas F.R., Gordon-Weeks P.R., Salinas P.C. Valproate regulates GSK-3-mediated axonal remodelling and synapsin I clustering in developing neurons. Mol. Cell. Neurosci. 20:2002;257-270.
22. Hoeflich K.P., Luo J., Rubie E.A., Tsao M.S., Jin O., Woodgett J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature. 406:2000;86-90.
23. Hollander B.A., Bennett G.S. Lithium chloride alters cytoskeletal organization in growing, but not mature, cultured chick sensory neurons. J. Neurosci. Res. 28:1991;332-342.
24. Johnstone M., Goold R.G., Bei D., Fischer I., Gordon-Weeks P.R. Localisation of microtubule-associated protein 1B phosphorylation sites recognised by monoclonal antibody SMI-31. J. Neurochem. 69:1997;1417-1424.
25. Kilmartin J.V., Wright B., Milstein D. Rat monoclonal antitubulin antibodies derived by using as new non-secretory rat cell line. J. Cell Biol. 93:1982;576-582.
26. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA. 93:1996;8455-8459.
27. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
28. Leroy K., Brion J.P. Developmental expression and localization of glycogen synthase kinase-3β in rat brain. J. Chem. Neuroanat. 16:1999;279-293.
29. Lucas F.R., Salinas P.C. WNT-7a induces axonal remodelling and increases synapsin 1 levels in cerebellar neurons. Dev. Biol. 192:1997;31-44.
30. Lucas F.R., Goold R.G., Gordon-Weeks P.R., Salinas P.C. Inhibition of GSK-3β leading to the loss of phosphorylated MAP-1B is an early event in axonal remodelling induced by WNT-7a or lithium. J. Cell Sci. 111:1998;1351-1361.
31. Meixner A., Haverkamp S., Wassle H., Fuhrer S., Thalhammer J., Kropf N., Bittner R.E., Lassmann H., Wiche G., Propst F. MAP1B is required for axon guidance and is involved in the development of the central and peripheral nervous system. J. Cell Biol. 151:2000;1169-1178.
32. Noiges R., Eichinger R., Kutschera W., Fischer I., Nemeth Z., Wiche G., Propst F. Microtubule-associated protein 1A (MAP1A) and MAP1B light chains determine distinct functional properties . J. Neurosci. 22:2002;2106-2114.
33. Pedrotti B., Islam K. Dephosphorylated but not phosphorylated microtubule associated protein MAP1B binds to microfilaments. FEBS Lett. 388:1996;131-133.
34. Phiel C.J., Klein P.S. Molecular targets of lithium action. Annu. Rev. Pharmacol. Toxicol. 41:2001;789-813.
35. Ryves W.J., Harwood A.J. Lithium inhibits glycogen synthase kinase-3 by competition for magnesium. Biochem. Biophys. Res. Commun. 280:2001;720-725.
36. Sanchez S., Sayas C.L., Lim F., Diaz-Nido J., Avila J., Wandosell F. The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J. Neurochem. 78:2001;468-481.
37. Seidensticker M.J., Behrens J. Biochemical interactions in the wnt pathway. Biochim. Biophys. Acta. 1495:2000;168-182.
38. Stambolic V., Ruel L., Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6:1996;1664-1668.
39. Sternberger L.A., Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc. Natl. Acad. Sci. USA. 80:1983;6126-6130.
40. Suter D.M., Forscher P. Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J. Neurobiol. 44:2000;97-113.
41. Takahashi M., Tomizawa K., Kato R., Sato K., Uchida T., Fujita S.C., Imahori K. Localization and developmental changes of tau protein kinase I/glycogen synthase kinase-3β in rat brain. J. Neurochem. 63:1994;245-255.
42. Takahashi M., Yasutake K., Tomizawa K. Lithium inhibits neurite growth and tau protein kinase I/glycogen synthase kinase-3beta-dependent phosphorylation of juvenile tau in cultured hippocampal neurons. J. Neurochem. 73:1999;2073-2083.
43. Takei Y., Kondo S., Harada A., Inomata S., Noda T., Hirokawa N. Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene. J. Cell Biol. 137:1997;1615-1626.
44. Takei Y., Teng J., Harada A., Hirokawa N. Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J. Cell Biol. 150:2000;989-1000.
45. Tanaka E., Ho T., Kirschner M.W. The role of microtubule dynamics in growth cone motility and axonal growth. J. Cell Biol. 128:1995;139-155.
46. Teng J., Takei Y., Harada A., Nakata T., Chen J., Hirokawa N. Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J. Cell Biol. 155:2001;65-76.
47. Tögel M., Wiche G., Propst F. Novel features of the light chain of microtubule-associated protein MAP1B microtubule stabilization, self interaction, actin filament binding, and regulation by the heavy chain . J. Cell Biol. 143:1998;695-707.
48. Tsui H.T., Lankford K.L., Ris H., Klein W.L. Novel organization of microtubules in cultured central nervous system neurons formation of hairpin loops at ends of maturing neurites . J. Neurosci. 4:1984;3002-3013.
49. Williams R.S., Cheng L., Mudge A.W., Harwood A.J. A common mechanism of action for three mood-stabilizing drugs. Nature. 417:2002;292-295.
50. Williamson T.W., Gordon-Weeks P.R., Schachner M., Taylor J. Microtubule reorganization is obligatory for growth cone turning. Proc. Natl. Acad. Sci. USA. 93:1996;15221-15226.
51. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 9:1990;2431-2438.
52. Woods A., Sherwin T., Sasse R., MacRae T.H., Baines A.J., Gull K. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93:1989;491-500.