GSK3 regulates mitotic chromosomal alignment through CRMP4

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Ong Tone, Stephan ^a   Dayanandan, Bama ^b   Fournier, Alyson E ^a   Mandato, Craig A ^b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 4; GLYCOGEN SYNTHASE KINASE 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CHROMOSOME ANALYSIS; CONTROLLED STUDY; CYTOSKELETON; GENE EXPRESSION REGULATION; MICROTUBULE; MITOSIS; NONHUMAN; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; WILD TYPE;

CHROMOSOMES; CYTOSKELETON; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HELA CELLS; HUMANS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MUSCLE PROTEINS; PHENOTYPE; PHOSPHORYLATION; PLASMIDS; RNA, SMALL INTERFERING;

EID: 79960131915     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014345     Document Type: Article

References (55)

1. Decordier I, Cundari E, Kirsch-Volders M (2008) Survival of aneuploid, micronucleated and/or polyploid cells: crosstalk between ploidy control and apoptosis. Mutat Res 651: 30-39.
2. Frame S, Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1-16.
3. Wakefield J, Stephens D, Tavare J (2003) A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. Journal of Cell Science 116: 637-646.
4. Cohen P, Goedert M (2004) GSK3 inhibitors: development and therapeutic potential. Nature reviews Drug discovery 3: 479-487.
5. Tighe A, Ray-Sinha A, Staples O, Taylor S (2007) GSK-3 inhibitors induce chromosome instability. BMC Cell Biol 8: 34.
6. Ciani L, Krylova O, Smalley MJ, Dale TC, Salinas PC (2004) A divergent canonical WNT-signaling pathway regulates microtubule dynamics: dishevelled signals locally to stabilize microtubules. The Journal of Cell Biology 164: 243-253.
7. Wang JZ, Wu Q, Smith A, Grundke-Iqbal I, Iqbal K (1998) Tau is phosphorylated by GSK-3 at several sites found in Alzheimer disease and its biological activity markedly inhibited only after it is prephosphorylated by Akinase. FEBS Lett 436: 28-34.
8. Goold RG, Owen R, Gordon-Weeks PR (1999) Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. Journal of Cell Science 112(Pt 19): 3373-3384.
9. 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.
10. Wang LH, Strittmatter SM (1996) A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 16: 6197-6207.
11. Gaetano C, Matsuo T, Thiele CJ (1997) Identification and characterization of a retinoic acid-regulated human homologue of the unc-33-like phosphoprotein gene (hUlip) from neuroblastoma cells. J Biol Chem 272: 12195-12201.
12. Byk T, Ozon S, Sobel A (1998) The Ulip family phosphoproteins-common and specific properties. Eur J Biochem 254: 14-24.
13. Quinn CC, Gray GE, Hockfield S (1999) A family of proteins implicated in axon guidance and outgrowth. J Neurobiol 41: 158-164.
14. Quach TT, Duchemin A-M, Rogemond V, Aguera M, Honnorat J, et al. (2004) Involvement of collapsin response mediator proteins in the neurite extension induced by neurotrophins in dorsal root ganglion neurons. Mol Cell Neurosci 25: 433-443.
15. Minturn JE, Fryer HJ, Geschwind DH, Hockfield S (1995) TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J Neurosci 15: 6757-6766.
16. Byk T, Dobransky T, Cifuentes-Diaz C, Sobel A (1996) Identification and molecular characterization of Unc-33-like phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product. J Neurosci 16: 688-701.
17. Inatome R, Tsujimura T, Hitomi T, Mitsui N, Hermann P, et al. (2000) Identification of CRAM, a novel unc-33 gene family protein that associates with CRMP3 and protein-tyrosine kinase(s) in the developing rat brain. J Biol Chem 275: 27291-27302.
18. Quinn CC, Chen E, Kinjo TG, Kelly G, Bell AW, et al. (2003) TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. Journal of Neuroscience 23: 2815-2823.
19. Yuasa-Kawada J, Suzuki R, Kano F, Ohkawara T, Murata M, et al. (2003) Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 17: 2329-2343.
20. Alabed YZ, Pool M, Ong Tone S, Fournier AE (2007) Identification of CRMP4 as a convergent regulator of axon outgrowth inhibition. Journal of Neuroscience 27: 1702-1711.
21. Pan S, Chao Y, Chen H, Hung P, Lin P, et al. (2009) Long form collapsin response mediator protein-1 (LCRMP-1) expression is associated with clinical outcome and lymph node metastasis in non-small cell lung cancer patients. Lung Cancer.
22. Hedgecock EM, Culotti JG, Thomson JN, Perkins LA (1985) Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol 111: 158-170.
23. Yoshimura T, Arimura N, Kawano Y, Kawabata S, Wang S, et al. (2005) Ras regulates neuronal polarity via the PI3-kinase/Akt/GSK-3b/CRMP-2 pathway. Biochemical and Biophysical Research Communications. pp 7.
24. Gu Y, Ihara Y (2000) Evidence that collapsin response mediator protein-2 is involved in the dynamics of microtubules. J Biol Chem 275: 17917-17920.
25. Shih JY, Yang SC, Hong TM, Yuan A, Chen JJ, et al. (2001) Collapsin response mediator protein-1 and the invasion and metastasis of cancer cells. J Natl Cancer Inst 93: 1392-1400.
26. Arimura N, Ménager C, Kawano Y, Yoshimura T, Kawabata S, et al. (2005) Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol Cell Biol 25: 9973-9984.
27. Fukata Y, Itoh TJ, Kimura T, Ménager C, Nishimura T, et al. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4: 583-591.
28. Rosslenbroich V, Dai L, Baader SL, Noegel AA, Gieselmann V, et al. (2005) Collapsin response mediator protein-4 regulates F-actin bundling. Experimental Cell Research 310: 434-444.
29. Glotzer M (2001) Animal cell cytokinesis. Annu Rev Cell Dev Biol 17: 351-386.
30. Narumiya S, Yasuda S (2006) Rho GTPases in animal cell mitosis. Current Opinion in Cell Biology 18: 199-205.
31. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, et al. (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.
32. Cole AR, Causeret F, Yadirgi G, Hastie CJ, McLauchlan H, et al. (2006) Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. J Biol Chem 281: 16591-16598.
33. Tighe A, Ray-Sinha A, Staples OD, Taylor SS (2007) GSK-3 inhibitors induce chromosome instability. BMC Cell Biol 8: 34.
34. Lampson MA, Kapoor TM (2005) The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat Cell Biol 7: 93-98.
35. Jeffery JM, Urquhart AJ, Subramaniam VN, Parton RG, Khanna KK (2010) Centrobin regulates the assembly of functional mitotic spindles. Oncogene 29: 2649-2658.
36. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, et al. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
37. Cole AR, Causeret F, Yadirgi G, Hastie CJ, McLauchlan H, et al. (2006) Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. J Biol Chem 281: 16591-16598.
38. Goshima G, Wollman R, Stuurman N, Scholey JM, Vale RD (2005) Length control of the metaphase spindle. Curr Biol 15: 1979-1988.
39. Dewar H, Tanaka K, Nasmyth K, Tanaka TU (2004) Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428: 93-97.
40. Lampson MA, Renduchitala K, Khodjakov A, Kapoor TM (2004) Correcting improper chromosome-spindle attachments during cell division. Nat Cell Biol 6: 232-237.
41. Maure J-F, Kitamura E, Tanaka TU (2007) Mps1 kinase promotes sisterkinetochore bi-orientation by a tension-dependent mechanism. Curr Biol 17: 2175-2182.
42. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, et al. (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome biorientation by altering kinetochore-spindle pole connections. Cell 108: 317-329.
43. Alabed YZ, Pool M, Ong Tone S, Sutherland C, Fournier AE (2010) GSK3beta regulates myelin-dependent axon outgrowth inhibition through CRMP4. J Neurosci 30: 5635-5643.
44. Lovestone S, Hartley CL, Pearce J, Anderton BH (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.
45. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, et al. (2001) Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104: 923-935.
46. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, et al. (2001) A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 3: 429-432.
47. Watanabe T, Noritake J, Kakeno M, Matsui T, Harada T, et al. (2009) Phosphorylation of CLASP2 by GSK-3{beta} regulates its interaction with IQGAP1, EB1 and microtubules. Journal of Cell Science 122: 2969-2979.
48. Meraldi P, Honda R, Nigg EA (2004) Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr Opin Genet Dev 14: 29-36.
49. Marumoto T, Zhang D, Saya H (2005) Aurora-A - a guardian of poles. Nat Rev Cancer 5: 42-50.
50. Fumoto K, Lee PC, Saya H, Kikuchi A (2008) AIP regulates stability of Aurora- A at early mitotic phase coordinately with GSK-3beta. Oncogene 27: 4478-4487.
51. Diehl JA, Cheng M, Roussel MF, Sherr CJ (1998) Glycogen synthase kinase- 3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
52. Massagué J (2004) G1 cell-cycle control and cancer. Nature 432: 298-306.
53. Pizarro JG, Folch J, Esparza JL, Jordan J, Pallàs M, et al. (2008) A molecular study of pathways involved in the inhibition of cell proliferation in neuroblastoma B65 cells by the GSK-3 inhibitors lithium and SB-415286. J Cell Mol Med.
54. Yüce O, Piekny A, Glotzer M (2005) An ECT2-centralspindlin complex regulates the localization and function of RhoA. The Journal of Cell Biology 170: 571-582.
55. Minturn JE, Geschwind DH, Fryer HJ, Hockfield S (1995) Early postmitotic neurons transiently express TOAD-64, a neural specific protein. J Comp Neurol 355: 369-379.