A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment

Journal of Cell Science

Volumn 116, Issue 4, 2003, Pages 637-646

  Wakefield, James G ^a   Stephens, David J ^a   Tavaré, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

GSK 3; Microtubule; Mitotic spindle; PKB

Indexed keywords

ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3; HISTONE H2B; LITHIUM; PROTEIN KINASE B;

CELL CYCLE; CENTROSOME; CHROMOSOME ANALYSIS; CHROMOSOME STRUCTURE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MAMMAL CELL; METAPHASE CHROMOSOME; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

CELL CYCLE PROTEINS; CENTROSOME; CHROMOSOME SEGREGATION; CHROMOSOMES; ENZYME INHIBITORS; EUKARYOTIC CELLS; GLYCOGEN SYNTHASE KINASE 3; HELA CELLS; HUMANS; LITHIUM; METAPHASE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT;

MAMMALIA;

EID: 0037442990     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00273     Document Type: Review

References (37)

1. Ahkmanova, A., Hoogenraad, C. C., Drabek, K., Stepanova, T., Dortland, B., Verkerk, T., Vermeulen, W., Burgering, B. M., de Zeeuw, C. I., Grosveld, F. and Galjart, N. (2001). Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
2. Alessi, D. R. and Cohen, P. (1998). Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8, 55-62.
3. Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R., Reese, C. B. and Cohen, P. (1997). Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 7, 261-269.
4. Andersen, C. B., Roth, R. A. and Conti, M. (1998). Protein kinase B/Akt induces resumption of meiosis in Xenopus oocytes. J. Biol. Chem. 273, 18705-18718.
5. Ault, J. G., DeMarco, A. J., Salmon, E. D. and Rieder, C. L. (1991). Studies on the ejection properties of asters: astral microtubule turnover influences the oscillatory behavior and positioning of mono-oriented chromosomes. J. Cell Sci. 99, 701-710.
6. Cassimeris, L. (1999). Accessory protein regulation of microtubule dynamics throughout the cell cycle. Curr. Opin. Cell Biol. 11, 134-141.
7. 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 Cox, L. et al. (2000). Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen and gene transcription. Chem. Biol. 7, 793-803.
8. Compton, D. A. (2000). Spindle assembly in animal cells. Annu. Rev. Biochem. 69, 95-114.
9. Corthesy-Theulaz, I., Pauloin, A. and Rfeffer, S. R. (1992). Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol. 118, 1333-1345.
10. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. and Hemmings, B. A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
11. Damiens, E., Baratte, B., Marie, D., Eisenbrand, G. and Meijer, L. (2001). Anti-mitotic properties of indirubin-3′-monoxime, a CDK/GSK-3 inhibitor: induction of endoreplication following prophase arrest Oncogene 20, 3786-3797.
12. Embi, N., Rylatt, D. and Cohen, P. (1980). Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase Eur. J. Biochem. 107, 519-526.
13. Ferkey, D. M. and Kimelman, D. (2000). GSK-3: new thoughts on an old enzyme. Dev. Biol. 225, 471-479.
14. Fodde, R., Kuipers, J., Rosenberg, C., Smits, R., Kielman, M., Gaspar, C., van Es, J. H., Breukel, C., Wiegant, J., Giles, R. H. and Clevers, H. (2001). Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3, 433-438.
15. Frame, S. and Cohen, P. (2001). GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1-16.
16. Goold, R. G., Owen, R. and Gordon-Weeks, P. R. (1999). Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112, 3373-3384.
17. Inoue, S. and Salmon, E. D. (1995). Force generation by microtubule assembly/ disassembly in mitosis and related movements. Mol. Biol. Cell. 6, 1619-1640.
18. Jordan, M. A., Wendell, K., Gardiner, S., Derry, W. B., Copp, H. and Wilson, L. (1996). Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res. 56, 816-825.
19. Kand, T., Sullivan, K. E and Wahl, G. M. (1998). Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385.
20. Kaplan, K. B., Burds, A. A., Swedlow, J. R., Bekir, S. S., Sorger, P. K. and Nathke, I. S. (2001). A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat. Cell Biol. 3, 429-432.
21. Khodjakov, A., Cole, R. W., Oakley, B. R. and Rieder, C. L. (2000). Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 10, 59-67.
22. Klein, P. S. and Melton, D. A. (1996). A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459.
23. Krylova, O., Messenger, M. J. and Salinas, P. C. (2000). Dishevelled-1 regulates microtubule stability: a new function mediated by glycogen synthasekinase-3beta. J. Cell Biol. 151, 83-94.
24. Leclerc, S., Garnier, M., Hoessel, R., Marko, D., Bibb, J. A., Snyder, G. L., Greengard, P., Biernat, J., Mandelkow, E. M., Eisenbrand, G. and Meijer, L. (2001). Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276, 251-260.
25. Lovestone, S., Hartley, C. L., Pearce, J. and Anderton, B. H. (1996). Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience 73, 1145-1157.
26. Nigg, E. A. (2001). Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32.
27. Okumura, E., Fukuhara, T., Yoshida, H., Hanada, Si. S., Kozutsumi, R., Mori, M., Tachibana, K. and Kishimoto, M. (2002). Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat. Cell Biol. 4, 111-116.
28. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S. and Polakis, P. (1996). Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
29. Sanchez, C., Perez, M. and Avila, J. (2000). GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur. J. Cell Biol, 79, 252-260.
30. Shtivelman, E., Sussman, J. and Stokoe, D. (2002). A Role for PI 3-Kinase and PKB Activity in the G2/M Phase of the Cell Cycle. Curr. Biol. 12, 919-924.
31. Siegfried, E., Chou, T. B. and Perrimon, N. (1992). Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167-1179.
32. Stambolic, V., Ruel, L. and Woodgett, J. R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6, 1664-1668.
33. Stein, G. S., Stein, J. L., Lian, J. B., Last, T. J., Owen, T. and McCabe, L. (1994). Synchronisation of normal diploid and transformed Mammalian cells. In Cell Biology: A Laboratory Handbook (ed. J. Celis), pp. 282-287. San Diego: Academic Press.
34. Utton, M. A., Vandecandelaere, A., Wagner, U., Reynolds, C. H., Gibb, G. M., Miller, C. C., Bayley, P. M. and Anderton, B. H. (1997). Phosphorylation of tau by glycogen synthase kinase 3beta affects the ability of tau to promote microtubule self-assembly. Biochem. J. 323, 741-747.
35. Wagner, U., Utton, M., Gallo, J. M. and Miller, C. C. (1996). Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organisation. J. Cell Sci. 109, 1537-1543.
36. Zhou, J., Panda, D., Landen, J. W., Wilson, L. and Joshi, H. C. (2002). Minor alteration of microtubule dynamics causes loss of tension across kinetochore pairs and activates the spindle checkpoint. J. Biol. Chem. 277, 17200-17208.
37. Zumbrunn, J., Kinoshita, K., Hyman, A. A. and Nathke, I. S. (2001). Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 11, 44-49.