GSK3β/Axin-1/β-catenin complex is involved in semaphorin3A signaling

Journal of Neuroscience

Volumn 32, Issue 35, 2012, Pages 11905-11918

  Hida, Tomonobu ^a   Yamashita, Naoya ^a   Usui, Hiroshi ^a   Nakamura, Fumio ^a   Sasaki, Yukio ^a   Kikuchi, Akira ^b   Goshima, Yoshio ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; NEUROPILIN 1; SEMAPHORIN 3A;

ANIMAL CELL; ARTICLE; CHICK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FEMALE; GROWTH CONE; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; AXIN PROTEIN; BETA CATENIN; CELLS, CULTURED; CHICK EMBRYO; ENDOCYTOSIS; FEMALE; GANGLIA, SPINAL; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MICE; MUTAGENESIS, SITE-DIRECTED; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; RATS; SEMAPHORIN-3A; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 84865326421     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6139-11.2012     Document Type: Article

References (48)

1. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I (2002) Axin-mediated CKI phosphorylation of betacatenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 16:1066-1076.
2. Arimura N, Inagaki N, Chihara K, Ménager C, Nakamura N, Amano M, Iwamatsu A, Goshima Y, Kaibuchi K (2000) Phosphorylation of collapsing response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 275:23973-23980.
3. Bhat R, Xue Y, Berg S, Hellberg S, Ormö M, Nilsson Y, Radesäter AC, Jerning E, Markgren PO, Borgegård T, Nylöf M, Giménez-Cassina A, Hernández F, Lucas JJ, Díaz-Nido J, Avila J (2003) Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J Biol Chem 278:45937-45945.
4. Brown M, Jacobs T, Eickholt B, Ferrari G, Teo M, Monfries C, Qi RZ, Leung T, Lim L, Hall C (2004) β2-chimaerin, cyclin-dependent kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J Neurosci 24:8994-9004.
5. Carcea I, Ma'ayan A, Mesias R, Sepulveda B, Salton SR, Benson DL (2010) Flotillin-mediated endocytic events dictate cell type-specific responses to semaphorin 3A. J Neurosci 30:15317-15329.
6. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, Connolly CN, Sutherland C (2004) GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 279:50176-50180.
7. Eickholt BJ, Walsh FS, Doherty P (2002) An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J Cell Biol 157:211-217.
8. Fan J, Raper JA (1995) Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14:263-274.
9. Fang WQ, Ip JP, Li R, Ng YP, Lin SC, Chen Y, Fu AK, Ip NY (2011) Cdk5-mediated phosphorylation of Axin directs axon formation during cerebral cortex development. J Neurosci 31:13613-13624.
10. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM (2000) Semaphorin3A enhances endocytosis at sites of receptor-Factin colocalization during growth cone collapse. J Cell Biol 149:411-422.
11. Frame S, Cohen P, Biondi RM (2001) A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7:1321-1327.
12. 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.
13. Goshima Y, Kawakami T, Hori H, Sugiyama Y, Takasawa S, Hashimoto Y, Kagoshima-Maezono M, Takenaka T, Misu Y, Strittmatter SM (1997) A novel action of collapsin: collapsin-1 increases antero- and retrograde axoplasmic transport independently of growth cone collapse. J Neurobiol 33:316-328.
14. Goshima Y, Ito T, Sasaki Y, Nakamura F (2002) Semaphorins as signals for cell repulsion and invasion. J Clin Invest 109:993-998.
15. Guirland C, Suzuki S, Kojima M, Lu B, Zheng JQ (2004) Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42:51-62.
16. Hagen T, Vidal-Puig A (2002) Characterisation of the phosphorylation of beta-catenin at the GSK-3 priming site Ser45. Biochem Biophys Res Commun 294:324-328.
17. Hur EM, Zhou FQ (2010) GSK3 signalling in neural development. Nat Rev Neurosci 11:539-551.
18. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17:1371-1384.
19. Jho E, Lomvardas S, Costantini F (1999) A GSK3beta phosphorylation site in axin modulates interaction with beta-catenin and Tcf-mediated gene expression. Biochem Biophys Res Commun 266:28-35.
20. Kabayama H, Nakamura T, Takeuchi M, Iwasaki H, Taniguchi M, Tokushige N, Mikoshiba K (2009) Ca 2β induces macropinocytosis via F-actin depolymerization during growth cone collapse. Mol Cell Neurosci 40:27-38.
21. Kim WY, Zhou FQ, Zhou J, Yokota Y, Wang YM, Yoshimura T, Kaibuchi K, Woodgett JR, Anton ES, Snider WD (2006) Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52:981-996.
22. Luo W, Lin SC (2004) Axin: a master scaffold for multiple signaling pathways. Neurosignals 13:99-113.
23. MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26.
24. Mann F, Rougon G (2007) Mechanisms of axon guidance: membrane dynamics and axonal transport in semaphorin signalling. J Neurochem 102:316-323.
25. Nakamura F, Ugajin K, Yamashita N, Okada T, Uchida Y, Taniguchi M, Ohshima T, Goshima Y (2009) Increased proximal bifurcation of CA1 pyramidal apical dendrites in sema3A mutant mice. J Comp Neurol 516:360-375.
26. Pasterkamp RJ, Giger RJ (2009) Semaphorin function in neural plasticity and disease. Curr Opin Neurobiol 19:263-274.
27. Piper M, Salih S, Weinl C, Holt CE, Harris WA (2005) Endocytosisdependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation. Nat Neurosci 8:179-186.
28. Quinn CC, Wadsworth WG (2008) Axon guidance: asymmetric signaling orients polarized outgrowth. Trends Cell Biol 18:597-603.
29. 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.
30. Scales TM, Lin S, Kraus M, Goold RG, Gordon-Weeks PR (2009) Nonprimed and DYRK1A-primed GSK3 beta-phosphorylation sites on MAP1B regulate microtubule dynamics in growing axons. J Cell Sci 122:2424-2435.
31. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S, Timm J, Mintzlaff S, Abraham C, Bock N, Kietzmann S, Goedde A, Toksöz E, Droege A, Krobitsch S, Korn B, et al. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122:957-968.
32. Sutherland C (2011) What are the bona fide GSK3 substrates? Int J Alzheimers Dis 2011:505607.
33. Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP, Gumper I, Sabatini DD, De Robertis EM (2010) Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143:1136-1148.
34. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69.
35. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
36. Thomas GM, Frame S, Goedert M, Nathke I, Polakis P, Cohen P (1999) A GSK3-binding peptide from FRAT1 selectively inhibits the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett 458:247-251.
37. Tojima T, Itofusa R, Kamiguchi H (2010) Asymmetric clathrin-mediated endocytosis drives repulsive growth cone guidance. Neuron 66:370-377.
38. Tran TS, Kolodkin AL, Bharadwaj R (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23:263-292.
39. Tran TS, Rubio ME, Clem RL, Johnson D, Case L, Tessier-Lavigne M, Huganir RL, Ginty DD, Kolodkin AL (2009) Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 462:1065-1069.
40. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, Nakamura F, Takei K, Ihara Y, Mikoshiba K, Kolattukudy P, Honnorat J, Goshima Y (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10:165-179.
41. Willert K, Shibamoto S, Nusse R (1999) Wnt-induced dephosphorylation of axin releases beta-catenin from the axin complex. Genes Dev 13:1768-1773.
42. Yamamoto H, Kishida S, Kishida M, Ikeda S, Takada S, Kikuchi A (1999) Phosphorylation of axin, a Wnt signal negative regulator, by glycogen synthase kinase-3beta regulates its stability. J Biol Chem 274:10681-10684.
43. Yamamoto H, Komekado H, Kikuchi A (2006) Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of betacatenin. Dev Cell 11:213-223.
44. Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, Taniguchi M, Honnorat J, Thomasset N, Takei K, Takahashi T, Kolattukudy P, Goshima Y (2007) Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27:12546-12554.
45. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, Perry WL 3rd, Lee JJ, Tilghman SM, Gumbiner BM, Costantini F (1997) The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181-192.
46. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, Okamura H, Woodgett J, He X (2005) A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438:873-877.
47. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912.
48. Zhou Y, Gunput RA, Pasterkamp RJ (2008) Semaphorin signaling: progress made and promises ahead. Trends Biochem Sci 33:161-170.