The Drosophila microtubule associated protein Futsch is phosphorylated by Shaggy/Zeste-white 3 at an homologous GSK3β phosphorylation site in MAP1B

Molecular and Cellular Neuroscience

Volumn 33, Issue 2, 2006, Pages 188-199

  Gögel, Stefanie ^a   Wakefield, Sarah ^a   Tear, Guy ^a   Klämbt, Christian ^b   Gordon Weeks, Phillip R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; FUTSCH PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 5; PROTEIN; UNCLASSIFIED DRUG; ZESTE WHITE 3 PROTEIN;

ARTICLE; DROSOPHILA; HEAVY CHAIN; MICROTUBULE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SYNAPTOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIBODY SPECIFICITY; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; EPITOPES; GLYCOGEN SYNTHASE KINASE 3; MAMMALS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTATION; NERVE GROWTH FACTORS; NEUROMUSCULAR JUNCTION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY;

VERTEBRATA;

EID: 33748929447     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2006.07.004     Document Type: Article

References (50)

1. Bettencourt D.C., Schwarzel M., Schulze S., Niyyati M., Heisenberg M., and Kretzschmar D. Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila. Mol. Biol. Cell 16 (2005) 2433-2442
2. Bobinnec Y., Morin X., and Debec A. Shaggy/GSK-3β kinase localizes to the centrosome and to specialized cytoskeletal structures in Drosophila. Cell Motil. Cytoskeleton 63 (2006) 313-320
3. Bourouis M. Targeted increase in shaggy activity levels blocks wingless signaling. Genesis 34 (2002) 99-102
4. Bourouis M., Heitzler P., el Messal M., and Simpson P. Mutant Drosophila embryos in which all cells adopt a neural fate. Nature 341 (1989) 442-444
5. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
6. Ciani L., Krylova O., Smalley M.J., Dale T.C., and Salinas P.C. A divergent canonical WNT-signaling pathway regulates microtubule dynamics: dishevelled signals locally to stabilize microtubules. J. Cell Biol. 164 (2004) 243-253
7. Couso J.P., and Martinez A.A. Notch is required for wingless signaling in the epidermis of Drosophila. Cell 79 (1994) 259-272
8. Del Rio J.A., Gonzalez-Billault C., Urena J.M., Jimenez E.M., Barallobre M.J., Pascual M., Pujadas L., Simo S., La Torre A., Wandosell F., Avila J., and Soriano E. MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr. Biol. 14 (2004) 840-850
9. Dent E.W., and Gertler F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40 (2003) 209-227
10. Díaz-Nido J., Serrano L., Mendez E., and Avila J. A casein kinase II-related activity is involved in phosphorylation of microtubule-associated protein MAP-1B during neuroblastoma cell differentiation. J. Cell Biol. 106 (1988) 2057-2065
11. DiTella M.C., Feiguin F., Carri N., Kosik K.S., and Caceres A. MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J. Cell Sci. 109 Pt. 2 (1996) 467-477
12. Franco B., Bogdanik L., Bobinnec Y., Debec A., Bockaert J., Parmentier M.L., and Grau Y. Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila. J. Neurosci. 24 (2004) 6573-6577
13. Fujita S.C., Zipursky S.L., Benzer S., Ferrus A., and Shotwell S.L. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 7929-7933
14. Gonzalez-Billault C., Avila J., and Caceres A. Evidence for the role of MAP1B in axon formation. Mol. Biol. Cell 12 (2001) 2087-2098
15. Gonzalez-Billault C., Owen R., Gordon-Weeks P.R., and 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
16. Gonzalez-Billault C., Jimenez-Mateos E.M., Caceres A., Díaz-Nido J., Wandosell F., and Avila J. Microtubule-associated protein 1B function during normal development, regeneration, and pathological conditions in the nervous system. J. Neurobiol. 58 (2004) 48-59
17. Goold R.G., and 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
18. Goold R.G., and Gordon-Weeks P.R. NGF activates the phosphorylation of MAP1B by GSK3β through the TrkA receptor and not the p75(NTR) receptor. J. Neurochem. 87 (2003) 935-946
19. Goold R.G., and Gordon-Weeks P.R. Glycogen synthase kinase 3β and the regulation of axon growth. Biochem. Soc. Trans. 32 (2004) 809-811
20. Goold R.G., and Gordon-Weeks P.R. The MAP kinase pathway is upstream of the activation of GSK3β that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth. Mol. Cell. Neurosci. 28 (2005) 524-534
21. Goold R.G., Owen R., and 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
22. Gordon-Weeks P.R., and Fischer I. MAP1B expression and microtubule stability in growing and regenerating axons. Microsc. Res. Tech. 48 (2000) 63-74
23. Hall A.C., Lucas F.R., and Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100 (2000) 525-535
24. Hammarback J.A., Obar R.A., Hughes S.M., and Vallee R.B. MAP1B is encoded as a polyprotein that is processed to form a complex N-terminal microtubule-binding domain. Neuron 7 (1991) 129-139
25. Horton R.M., Hunt H.D., Ho S.N., Pullen J.K., and Pease R.L. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77 (1989) 61-68
26. Hummel T., Schimmelpfeng K., and Klambt C. Commissure formation in the embryonic CNS of Drosophila. Dev. Biol. 209 (1999) 381-398
27. Hummel T., Krukkert K., Roos J., Davis G., and Klambt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26 (2000) 357-370
28. Johnstone M., Goold R.G., Bei D., Fischer I., and Gordon-Weeks P.R. Localisation of microtubule-associated protein 1B phosphorylation sites recognised by monoclonal antibody SMI-31. J. Neurochem. 69 (1997) 1417-1424
29. Kalil K., and Dent E.W. Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr. Opin. Neurobiol. 15 (2005) 521-526
30. Kawauchi T., Chihama K., Nabeshima Y., and Hoshino M. The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J. 22 (2003) 4190-4201
31. Kawauchi T., Chihama K., Nishimura Y.V., Nabeshima Y., and Hoshino M. MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem. Biophys. Res. Commun. 331 (2005) 50-55
32. Klein P.S., and Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 8455-8459
33. Lucas F.R., Goold R.G., Gordon-Weeks P.R., and 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
34. Mack T.G., Koester M.P., and Pollerberg G.E. The microtubule-associated protein MAP1B is involved in local stabilization of turning growth cones. Mol. Cell. Neurosci. 15 (2000) 51-65
35. Meixner A., Haverkamp S., Wassle H., Fuhrer S., Thalhammer J., Kropf N., Bittner R.E., Lassmann H., Wiche G., and 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
36. Owen R., and Gordon-Weeks P.R. Inhibition of glycogen synthase kinase 3β in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol. Cell. Neurosci. 23 (2003) 626-637
37. Packard M., Koo E.S., Gorczyca M., Sharpe J., Cumberledge S., and Budnik V. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111 (2002) 319-330
38. Reichmuth C., Becker S., Benz M., Debel K., Reisch D., Heimbeck G., Hofbauer A., Klagges B., Pflugfelder G.O., and Buchner E. The sap47 gene of Drosophila melanogaster codes for a novel conserved neuronal protein associated with synaptic terminals. Brain Res. Mol. Brain Res. 32 (1995) 45-54
39. Roos J., Hummel T., Ng N., Klambt C., and Davis G.W. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26 (2000) 371-382
40. Ruel L., Bourouis M., Heitzler P., Pantesco V., and Simpson P. Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature 362 (1993) 557-560
41. Ruel L., Pantesco V., Lutz Y., Simpson P., and Bourouis M. Functional significance of a family of protein kinases encoded at the shaggy locus in Drosophila. EMBO J. 12 (1993) 1657-1669
42. Ruiz-Canada C., Ashley J., Moeckel-Cole S., Drier E., Yin J., and Budnik V. New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 42 (2004) 567-580
43. Schuster C.M., Davis G.W., Fetter R.D., and Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity: I. Fasciclin II controls synaptic stabilization and growth. Neuron 17 (1996) 641-654
44. Stambolic V., Ruel L., and Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6 (1996) 1664-1668
45. Takei Y., Kondo S., Harada A., Inomata S., Noda T., and 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
46. Takei Y., Teng J., Harada A., and Hirokawa N. Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J. Cell Biol. 150 (2000) 989-1000
47. Teng J., Takei Y., Harada A., Nakata T., Chen J., and Hirokawa N. Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J. Cell Biol. 155 (2001) 65-76
48. Tögel M., Wiche G., and 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
49. Tögel M., Eichinger R., Wiche G., and Propst F. A 45 amino acid residue domain necessary and sufficient for proteolytic cleavage of the MAP1B polyprotein precursor. FEBS Lett. 451 (1999) 15-18
50. Trivedi N., Marsh P., Goold R.G., Wood-Kaczmar A., and Gordon-Weeks P.R. Glycogen synthase kinase-3β phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J. Cell Sci. 118 (2005) 993-1005