Aberrant spindle dynamics and cytokinesis in Dictyostelium discoideum cells that lack glycogen synthase kinase 3

European Journal of Cell Biology

Volumn 92, Issue 6-7, 2013, Pages 222-228

  Harwood, Adrian J ^a   Forde Thomas, Josephine E ^a   Williams, Hazel ^a   Samereier, Matthias ^b   Müller Taubenberger, Annette ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cytokinesis; Dictyostelium; Glycogen synthase kinase 3; Mitosis; Mitotic spindle

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3;

ARTICLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; DICTYOSTELIUM DISCOIDEUM; ENZYME ACTIVITY; MITOSIS SPINDLE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALIA; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; MAMMALIA;

CYTOKINESIS; DICTYOSTELIUM; GLYCOGEN SYNTHASE KINASE 3; MITOSIS; MITOTIC SPINDLE;

CHROMOSOME SEGREGATION; CYTOKINESIS; DICTYOSTELIUM; GLYCOGEN SYNTHASE KINASE 3; MUTATION; PROTEIN BINDING; PROTOZOAN PROTEINS; SPINDLE APPARATUS;

EID: 84883228695     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2013.05.001     Document Type: Article

References (40)

1. Bobinnec Y., Morin X., Debec A. Shaggy/GSK-3beta kinase localizes to the centrosome and to specialized cytoskeletal structures in Drosophila. Cell Motil. Cytoskeleton 2006, 63:313-320.
2. Cole A.R., Knebel A., Morrice N.A., Robertson L.A., Irving A.J., Connolly C.N., Sutherland C. GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem. 2004, 279:50176-50180.
3. Daunderer C., Schliwa M., Graf R. Dictyostelium discoideum: a promising centrosome model system. Biol. Cell. 1999, 91:313-320.
4. Effler J.C., Kee Y.S., Berk J.M., Tran M.N., Iglesias P.A., Robinson D.N. Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr. Biol. 2006, 16:1962-1967.
5. Fodde R., Kuipers J., Rosenberg C., Smits R., Kielman M., Gaspar C., van Es J.H., Breukel C., Wiegant J., Giles R.H., Clevers H. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 2001, 3:433-438.
6. Forde J.E., Dale T.C. Glycogen synthase kinase 3: a key regulator of cellular fate. Cell. Mol. Life Sci. 2007, 64:1930-1944.
7. Goold R.G., Owen R., Gordon-Weeks P.R. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 1999, 112(Pt 19):3373-3384.
8. Gräf R., Daunderer C., Schulz I. Molecular and functional analysis of the dictyostelium centrosome. Int. Rev. Cytol. 2004, 241:155-202.
9. Harwood A.J., Plyte S.E., Woodgett J., Strutt H., Kay R.R. Glycogen synthase kinase 3 regulates cell fate in Dictyostelium. Cell 1995, 80:139-148.
10. Müller-Taubenberger A., Ishikawa-Ankerhold H.C. Fluorescent reporters and methods to analyze fluorescent signals. Methods Mol. Biol. 2013, 983:93-112.
11. King J., Insall R.H. Parasexual genetics of Dictyostelium gene disruptions: identification of a ras pathway using diploids. BMC Genet. 2003, 4:12.
12. Kumar P., Chimenti M.S., Pemble H., Schonichen A., Thompson O., Jacobson M.P., Wittmann T. Multisite phosphorylation disrupts arginine-glutamate salt bridge networks required for binding of cytoplasmic linker-associated protein 2 (CLASP2) to end-binding protein 1 (EB1). J. Biol. Chem. 2012, 287:17050-17064.
13. Lovestone S., Hartley C.L., Pearce J., Anderton B.H. Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience 1996, 73:1145-1157.
14. Maiato H., DeLuca J., Salmon E.D., Earnshaw W.C. The dynamic kinetochore-microtubule interface. J. Cell Sci. 2004, 117:5461-5477.
15. McManus E.J., Sakamoto K., Armit L.J., Ronaldson L., Shpiro N., Marquez R., Alessi D.R. Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J. 2005, 24:1571-1583.
16. Mishima M., Tanaka K., Takeiri A., Harada A., Kubo C., Sone S., Nishimura Y., Tachibana Y., Okazaki M. Two structurally distinct inhibitors of glycogen synthase kinase 3 induced centromere positive micronuclei in human lymphoblastoid TK6 cells. Mutat. Res. 2008, 643:29-35.
17. Müller-Taubenberger A. Application of fluorescent protein tags as reporters in live-cell imaging studies. Methods Mol. Biol. 2006, 346:229-246.
18. Neujahr R., Albrecht R., Köhler J., Matzner M., Schwartz J.M., Westphal M., Gerisch G. Microtubule-mediated centrosome motility and the positioning of cleavage furrows in multinucleate myosin II-null cells. J. Cell Sci. 1998, 111(Pt 9):1227-1240.
19. Niewöhner J., Weber I., Maniak M., Müller-Taubenberger A., Gerisch G. Talin-null cells of Dictyostelium are strongly defective in adhesion to particle and substrate surfaces and slightly impaired in cytokinesis. J. Cell Biol. 1997, 138:349-361.
20. Ong Tone S., Dayanandan B., Fournier A.E., Mandato C.A. GSK3 regulates mitotic chromosomal alignment through CRMP4. PLoS One 2010, 5:e14345.
21. Plyte S.E., Feoktistova A., Burke J.D., Woodgett J.R., Gould K.L. Schizosaccharomyces pombe skp1+ encodes a protein kinase related to mammalian glycogen synthase kinase 3 and complements a cdc14 cytokinesis mutant. Mol. Cell. Biol. 1996, 16:179-191.
22. Rehberg M., Gräf R. Dictyostelium EB1 is a genuine centrosomal component required for proper spindle formation. Mol. Biol. Cell 2002, 13:2301-2310.
23. Roos U.P., Camenzind R. Spindle dynamics during mitosis in Dictyostelium discoideum. Eur. J. Cell Biol. 1981, 25:248-257.
24. Ryves W.J., Fryer L., Dale T., Harwood A.J. An assay for glycogen synthase kinase 3 (GSK-3) for use in crude cell extracts. Anal. Biochem. 1998, 264:124-127.
25. Sanchez C., Perez M., Avila J. GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur. J. Cell Biol. 2000, 79:252-260.
26. Schilde C., Araki T., Williams H., Harwood A., Williams J.G. GSK3 is a multifunctional regulator of Dictyostelium development. Development 2004, 131:4555-4565.
27. Schlesinger A., Shelton C.A., Maloof J.N., Meneghini M., Bowerman B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 1999, 13:2028-2038.
28. Schliwa M., van Blerkom J. Structural interaction of cytoskeletal components. J. Cell Biol. 1981, 90:222-235.
29. Schulz I., Erle A., Gräf R., Kruger A., Lohmeier H., Putzler S., Samereier M., Weidenthaler S. Identification and cell cycle-dependent localization of nine novel, genuine centrosomal components in Dictyostelium discoideum. Cell Motil. Cytoskeleton 2009, 66:915-928.
30. Shero J.H., Hieter P. A suppressor of a centromere DNA mutation encodes a putative protein kinase (MCK1). Genes Dev. 1991, 5:549-560.
31. Strmecki L., Bloomfield G., Araki T., Dalton E., Skelton J., Schilde C., Harwood A., Williams J.G., Ivens A., Pears C. Proteomic and microarray analyses of the Dictyostelium Zak1-GSK-3 signaling pathway reveal a role in early development. Eukaryot Cell 2007, 6:245-252.
32. Teo R., Lewis K.J., Forde J.E., Ryves W.J., Reddy J.V., Rogers B.J., Harwood A.J. Glycogen synthase kinase-3 is required for efficient Dictyostelium chemotaxis. Mol. Biol. Cell 2010, 21:2788-2796.
33. Tighe A., Ray-Sinha A., Staples O.D., Taylor S.S. GSK-3 inhibitors induce chromosome instability. BMC Cell Biol. 2007, 8:34.
34. Tikhonenko I., Nag D.K., Martin N., Koonce M.P. Kinesin-5 is not essential for mitotic spindle elongation in Dictyostelium. Cell Motil. Cytoskeleton 2008, 65:853-862.
35. Wakefield J.G., Stephens D.J., Tavare J.M. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J. Cell Sci. 2003, 116:637-646.
36. Watanabe T., Noritake J., Kakeno M., Matsui T., Harada T., Wang S., Itoh N., Sato K., Matsuzawa K., Iwamatsu A., Galjart N., Kaibuchi K. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 2009, 122:2969-2979.
37. Wehland J., Willingham M.C. A rat monoclonal antibody reacting specifically with the tyrosylated form of alpha-tubulin. II. Effects on cell movement, organization of microtubules, and intermediate filaments, and arrangement of Golgi elements. J. Cell Biol. 1983, 97:1476-1490.
38. Wojcik E.J. A mitotic role for GSK-3beta kinase in Drosophila. Cell Cycle 2008, 7:3699-3708.
39. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 1990, 9:2431-2438.
40. Zumbrunn J., Kinoshita K., Hyman A.A., Näthke I.S. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 2001, 11:44-49.