GSK3β and PKCζ function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization

Molecular and Cellular Neuroscience

Volumn 32, Issue 1-2, 2006, Pages 118-132

  Higginbotham, Holden ^a   Tanaka, Teruyuki ^b   Brinkman, Brendan C ^b   Gleeson, Joseph G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atypical protein kinase C; Cell migration; Glycogen synthase kinase 3; Neuron; Slit

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE C ZETA; SLIT PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; GLYCOPROTEIN; NERVE PROTEIN; PROTEIN KINASE C; SLIT PROTEIN, VERTEBRATE;

ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL POLARITY; CELLULAR DISTRIBUTION; CENTROSOME; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOLECULAR STABILITY; MOUSE; NERVE CELL GROWTH; NERVE CELL MEMBRANE POTENTIAL; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REPOLARIZATION; ANIMAL; ASSOCIATION; CELL DIFFERENTIATION; CELL LINE; CELL MOTION; CYTOLOGY; CYTOSKELETON; METABOLISM; NERVE CELL; NEURITE; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PRENATAL DEVELOPMENT; STEM CELL; ULTRASTRUCTURE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; CELL NUCLEUS; CELL POLARITY; CENTROSOME; CUES; CYTOSKELETON; GLYCOGEN SYNTHASE KINASE 3; GLYCOPROTEINS; HUMANS; MICE; NERVE TISSUE PROTEINS; NEURITES; NEURONS; OLFACTORY BULB; ORGAN CULTURE TECHNIQUES; PROTEIN KINASE C; STEM CELLS;

EID: 33745068650     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2006.03.003     Document Type: Article

References (66)

1. Abal M., Piel M., BoucksoN-Castaing V., Mogensen M., Sibarita J.B., and Bornens M. Microtubule release from the centrosome in migrating cells. J. Cell Biol. 159 (2002) 731-737
2. Ahmad F.J., and Baas P.W. Microtubules released from the neuronal centrosome are transported into the axon. J. Cell Sci. 108 pt. 8 (1995) 2761-2769
3. Anton E.S., Ghashghaei H.T., Weber J.L., McCann C., Fischer T.M., Cheung I.D., Gassmann M., Messing A., Klein R., Schwab M.H., Lloyd K.C., and Lai C. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat. Neurosci. 7 (2004) 1319-1328
4. Baird D.H., Myers K.A., Mogensen M., Moss D., and Baas P.W. Distribution of the microtubule-related protein ninein in developing neurons. Neuropharmacology 47 (2004) 677-683
5. Bellion A., Baudoin J.P., Alvarez C., Bornens M., and Metin C. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 25 (2005) 5691-5699
6. Bielas S.L., and Gleeson J.G. Cytoskeletal-associated proteins in the migration of cortical neurons. J. Neurobiol. 58 (2004) 149-159
7. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., and Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96 (1999) 795-806
8. Busson S., Dujardin D., Moreau A., Dompierre J., and De Mey J.R. Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells. Curr. Biol. 8 (1998) 541-544
9. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
10. de Anda F.C., Pollarolo G., Da Silva J.S., Camoletto P.G., Feiguin F., and Dotti C.G. Centrosome localization determines neuronal polarity. Nature 436 (2005) 704-708
11. Doetsch F., and Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14895-14900
12. Dominguez I., Itoh K., and Sokol S.Y. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8498-8502
13. Dujardin D.L., Barnhart L.E., Stehman S.A., Gomes E.R., Gundersen G.G., and Vallee R.B. A role for cytoplasmic dynein and LIS1 in directed cell movement. J. Cell Biol. 163 (2003) 1205-1211
14. Etienne-Manneville S., and Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106 (2001) 489-498
15. Etienne-Manneville S., and Hall A. Cdc42 regulates GSK-3 beta and adenomatous polyposis coli to control cell polarity. Nature 421 (2003) 753-756
16. Faulkner N.E., Dujardin D.L., Tai C.Y., Vaughan K.T., O'Connell C.B., Wang Y., and Vallee R.B. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2 (2000) 784-791
17. Feierbach B., and Chang F. Cytokinesis and the contractile ring in fission yeast. Curr. Opin. Microbiol. 4 (2001) 713-719
18. Fukata M., Watanabe T., Noritake J., Nakagawa M., Yamaga M., Kuroda S., Matsuura Y., Iwamatsu A., Perez F., and Kaibuchi K. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109 (2002) 873-885
19. Goold R.G., Owen R., and Gordon-Weeks P.R. Glycogen synthase kinase 3 beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112 Pt. 19 (1999) 3373-3384
20. Gregory W.A., Edmondson J.C., Hatten M.E., and Mason C.A. Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J. Neurosci. 8 (1988) 1728-1738
21. Gschwendt M., Dieterich S., Rennecke J., Kittstein W., Mueller H.J., and Johannes F.J. Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett. 392 (1996) 77-80
22. Hatten M.E. The role of migration in central nervous system neuronal development. Curr. Opin. Neurobiol. 3 (1993) 38-44
23. Hatten M.E. New directions in neuronal migration. Science 297 (2002) 1660-1663
24. He X., Saint-Jeannet J.P., Woodgett J.R., Varmus H.E., and Dawid I.B. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374 (1995) 617-622
25. Higginbotham H., Bielas S., Tanaka T., and Gleeson J.G. Transgenic mouse line with green-fluorescent protein-labeled Centrin 2 allows visualization of the centrosome in living cells. Transgenic Res. 13 (2004) 155-164
26. Jiang H., Guo W., Liang X., and Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3 beta and its upstream regulators. Cell 120 (2005) 123-135
27. Joberty G., Petersen C., Gao L., and Macara I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2 (2000) 531-539
28. Kidd T., Bland K.S., and Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96 (1999) 785-794
29. 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
30. Koonce M.P., Cloney R.A., and Berns M.W. Laser irradiation of centrosomes in newt eosinophils: evidence of centriole role in motility. J. Cell Biol. 98 (1984) 1999-2010
31. Leclerc S., Garnier M., Hoessel R., Marko D., Bibb J.A., Snyder G.L., Greengard P., Biernat J., Wu Y.Z., Mandelkow E.M., Eisenbrand G., and Meijer L. 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 (2001) 251-260
32. Li H.S., Chen J.H., Wu W., Fagaly T., Zhou L., Yuan W., Dupuis S., Jiang Z.H., Nash W., Gick C., Ornitz D.M., Wu J.Y., and Rao Y. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96 (1999) 807-818
33. Meijer L., Skaltsounis A.L., Magiatis P., Polychronopoulos P., Knockaert M., Leost M., Ryan X.P., Vonica C.A., Brivanlou A., Dajani R., Crovace C., Tarricone C., Musacchio A., Roe S.M., Pearl L., and Greengard P. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem. Biol. 10 (2003) 1255-1266
34. Mogensen M.M., Malik A., Piel M., BoucksoN-Castaing V., and Bornens M. Microtubule minus-end anchorage at centrosomal and noN-Centrosomal sites: the role of ninein. J. Cell Sci. 113 pt. 17 (2000) 3013-3023
35. Ohno S. Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 13 (2001) 641-648
36. Palazzo A.F., Joseph H.L., Chen Y.J., Dujardin D.L., Alberts A.S., Pfister K.K., Vallee R.B., and Gundersen G.G. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11 (2001) 1536-1541
37. Patel S., Yenush L., Rodriguez P.L., Serrano R., and Blundell T.L. Crystal structure of an enzyme displaying both inositol-polyphosphate-1-phosphatase and 3′-phosphoadenosine-5′-phosphate phosphatase activities: a novel target of lithium therapy. J. Mol. Biol. 315 (2002) 677-685
38. Rivas R.J., and Hatten M.E. Motility and cytoskeletal organization of migrating cerebellar granule neurons. J. Neurosci. 15 (1995) 981-989
39. Rosenblatt J., Cramer L.P., Baum B., and McGee K.M. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117 (2004) 361-372
40. Sameshima M., Imai Y., and Hashimoto Y. The position of the microtubule-organizing center relative to the nucleus is independent of the direction of cell migration in Dictyostelium discoideum. Cell Motil. Cytoskeleton 9 (1988) 111-116
41. Sanchez C., Perez M., and Avila J. GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur. J. Cell Biol. 79 (2000) 252-260
42. Schaar B.T., and McConnell S.K. Cytoskeletal coordination during neuronal migration. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13652-13657
43. Schliwa M., Euteneuer U., Graf R., and Ueda M. Centrosomes, microtubules and cell migration. Biochem. Soc. Symp. 65 (1999) 223-231
44. Shi S.H., Jan L.Y., and Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112 (2003) 63-75
45. Shi S.H., Cheng T., Jan L.Y., and Jan Y.N. APC and GSK-3 beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14 (2004) 2025-2032
46. Shu T., Ayala R., Nguyen M.D., Xie Z., Gleeson J.G., and Tsai L.H. Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44 (2004) 263-277
47. Solecki D.J., Model L., Gaetz J., Kapoor T.M., and Hatten M.E. Par6alpha signaling controls glial-guided neuronal migration. Nat. Neurosci. 7 (2004) 1195-1203
48. Standaert M.L., Galloway L., Karnam P., Bandyopadhyay G., Moscat J., and Farese R.V. Protein kinase C-zeta as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. J. Biol. Chem. 272 (1997) 30075-30082
49. Standaert M.L., Bandyopadhyay G., Sajan M.P., Cong L., Quon M.J., and Farese R.V. Okadaic acid activates atypical protein kinase C (zeta/lambda) in rat and 3T3/L1 adipocytes. An apparent requirement for activation of Glut4 translocation and glucose transport. J. Biol. Chem. 274 (1999) 14074-14078
50. Tabuse Y., Izumi Y., Piano F., Kemphues K.J., Miwa J., and Ohno S. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125 (1998) 3607-3614
51. Tanaka T., Serneo F.F., Higgins C., Gambello M.J., Wynshaw-Boris A., and Gleeson J.G. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165 (2004) 709-721
52. Tsai L.H., and Gleeson J.G. Nucleokinesis in neuronal migration. Neuron 46 (2005) 383-388
53. Ueda M., Graf R., MacWilliams H.K., Schliwa M., and Euteneuer U. Centrosome positioning and directionality of cell movements. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9674-9678
54. Vaughan K.T., Tynan S.H., Faulkner N.E., Echeverri C.J., and Vallee R.B. Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J. Cell Sci. 112 Pt. 10 (1999) 1437-1447
55. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., and Tessier-Lavigne M. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96 (1999) 771-784
56. Ward M., McCann C., DeWulf M., Wu J.Y., and Rao Y. Distinguishing between directional guidance and motility regulation in neuronal migration. J. Neurosci. 23 (2003) 5170-5177
57. Ward M.E., Jiang H., and Rao Y. Regulated formation and selection of neuronal processes underlie directional guidance of neuronal migration. Mol. Cell. Neurosci. 30 (2005) 378-387
58. Watts J.L., Etemad-Moghadam B., Guo S., Boyd L., Draper B.W., Mello C.C., Priess J.R., and Kemphues K.J. par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122 (1996) 3133-3140
59. White R.A., Pan Z., and Salisbury J.L. GFP-centrin as a marker for centriole dynamics in living cells. Microsc. Res. Tech. 49 (2000) 451-457
60. Wong K., Ren X.R., Huang Y.Z., Xie Y., Liu G., Saito H., Tang H., Wen L., Brady-Kalnay S.M., Mei L., Wu J.Y., Xiong W.C., and Rao Y. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107 (2001) 209-221
61. Wu W., Wong K., Chen J., Jiang Z., Dupuis S., Wu J.Y., and Rao Y. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400 (1999) 331-336
62. Yan X., Li F., Liang Y., Shen Y., Zhao X., Huang Q., and Zhu X. Human Nudel and NudE as regulators of cytoplasmic dynein in poleward protein transport along the mitotic spindle. Mol. Cell. Biol. 23 (2003) 1239-1250
63. Yoshimura T., Kawano Y., Arimura N., Kawabata S., Kikuchi A., and Kaibuchi K. GSK-3 beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120 (2005) 137-149
64. Yu W., Centonze V.E., Ahmad F.J., and Baas P.W. Microtubule nucleation and release from the neuronal centrosome. J. Cell Biol. 122 (1993) 349-359
65. Zhou F.Q., Zhou J., Dedhar S., Wu Y.H., and Snider W.D. NGF-induced axon growth is mediated by localized inactivation of GSK-3 beta and functions of the microtubule plus end binding protein APC. Neuron 42 (2004) 897-912
66. Zumbrunn J., Kinoshita K., Hyman A.A., and Nathke I.S. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 11 (2001) 44-49