Neonatal neuronal overexpression of glycogen synthase kinase-3β reduces brain size in transgenic mice

Neuroscience

Volumn 113, Issue 4, 2002, Pages 797-808

  Spittaels, K ^a   Van den Haute, C ^a   Van Dorpe, J ^a   Terwel, D ^a   Vandezande, K ^a   Lasrado, R ^a   Bruynseels, K ^a   Irizarry, M ^b   Verhoye, M ^c   Van Lint, J ^a   R Vandenheede, J ^a   Ashton, D ^d   Mercken, M ^d   Loos, R ^a   Hyman, B ^b   Van Der Linden, A ^c   Geerts, H ^d   Van Leuven, F ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

Glycogen synthase kinase 3 ; Microcephaly; Microtubule associated protein 2; Transgenic mice

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MICROTUBULE ASSOCIATED PROTEIN 2;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN SIZE; BRAIN WEIGHT; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOSKELETON; DENDRITE; FEMALE; GENE OVEREXPRESSION; HUMAN; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; SPINAL CORD; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PSYCHOMOTOR PERFORMANCE;

EID: 0037056024     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00236-1     Document Type: Article

References (60)

1. Avila J., Domínguez J., Díaz-Nido J. Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38:1994;13-25.
2. Bayer, S.A., Altman, J., 1991. Neocortical Development. Raven, New York.
3. Beck K.D., Powell-Braxton L., Widmer H.R., Valverde J., Hefti F. Igf1 gene disruption results in reduced brain size, CNS hypomyelinisation, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron. 14:1995;717-730.
4. Berezovska O., McLean P., Knowles R., Frosh M., Lu F.M., Lux S.E., Hyman B.T. Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience. 93:1999;433-439.
5. Berling B., Wille H., Röll B., Mandelkow E.-M., Garner C., Mandelkow E. Phosphorylation of microtubule-associated proteins MAP2a, b and MAP2c at Ser136 by proline-directed kinases in vivo and in vitro. Eur. J. Cell Biol. 64:1994;120-130.
6. Bollen M., Keppens F., Stalmans W. Specific features of glycogen metabolism in the liver. Biochem. J. 336:1998;19-31.
7. Caceres A., Mautino J., Kosik K.S. Suppression of MAP2 in cultured cerebeller macroneurons inhibits minor neurite formation. Neuron. 9:1992;607-618.
8. Cavalieri, B., 1966. Geometria Degli Indivisibili. Unione Tipografico, Torino.
9. Chan T.M., Exton J.H. A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Ann. Biochem. 71:1976;96-105.
10. Cheng C.M., Reinhardt R.R., Lee W.-H., Joncas G., Patel S.C., Bondy C.A. Insulin-like growth factor 1 regulates developing brain glucose metabolism. Proc. Natl. Acad. Sci. USA. 97:2000;10236-10241.
11. de la Pompa J.L., Wakeham A., Correia K.M., Samper E., Brown S., Aguilera R.J., Nakano T., Honjo T., Mak T.W., Rossant J., Conlon R.A. Conservation of the Notch signaling pathway in mammalian neurogenesis. Development. 124:1997;1139-1148.
12. Dominguez I., Itoh K., Sokol S.Y. Role of glycogen synthase kinase 3β as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc. Natl. Acad. Sci. USA. 92:1995;8498-8502.
13. 129 is required for the cAMP-mediated control of gene expression. J. Biol. Chem. 269:1994;32187-32193.
14. Franklin, K.B.J., Paxinos, G., 1997. The Mouse Brain in Stereotaxic Coordinates. Academic, San Diego, CA.
15. Fransen E., D'Hooghe R., Van Camp G., Verhoye M., Sijbers J., Reyniers E., Soriano P., Kamiguchi H., Willemsen R., Koekoek K.E., De Zeeuw C.I., De Deyn P.P., Van der Linden A., Lemmon V., Kooy R.F., Willems P. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet. 7:1998;999-1009.
16. García-Pérez J., Avila J., Díaz-Nido J. Implication of cyclin-dependent kinases and glycogen synthase kinase 3 in the phosphorylation of microtubule-associated protein 1B in developing neuronal cells. J. Neurosci. Res. 52:1998;445-452.
17. Gibb R., Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J. Neurosci. Methods. 79:1998;1-4.
18. Goold R.G., Owen R., Gordon-Weeks P.R. Glycogen synthase kinase 3β phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112:1999;3373-3384.
19. A (glycogen synthase kinase 3). J. Biol. Chem. 266:1991;8262-8267.
20. Guidato S., Tsai L.-H., Woodgett J., Miller C.C.J. Differential cellular phosphorylation of neurofilament heavy side-arm by glycogen synthase kinase 3 and cyclin-dependent kinase-5. J. Neurochem. 66:1996;1698-1706.
21. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell. 100:2000;525-535.
22. He H., Saint-Jeannet J.-P., Woodgett J.R., Varmus H.E., Dawid I.B. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature. 374:1995;617-622.
23. Hirokawa N., Funakoshi T., Sato-Harada R., Kanai Y. Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J. Cell Biol. 132:1996;667-679.
24. Hoshi M., Takashima A., Noguchi K., Murayama M., Sato M., Kondo S., Saitoh Y., Ishiguro K., Hoshino T., Imahori I. Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3β in brain. Proc. Natl. Acad. Sci. USA. 93:1996;2719-2723.
25. Ikeda S., Kishida S., Yamamoto H., Murai H., Koyama S., Kikuchi A. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes the GSK-3β-dependent phosphorylation of β-catenin. EMBO J. 17:1998;1371-1384.
26. Kooy F., Reyniers E., Verhoye M., Sijbers J., Cras P., Oostra B., Willems P., Van der Linden A. Neuroanatomy of the fragile X knockout mouse brain studied using in vivo high resolution magnetic resonance imaging (MRI). Eur. J. Hum. Genet. 7:1999;526-532.
27. Lamberty Y., Gower A.J. Age-related changes in spontaneous behavior and learning in NMRI mice from middle to old age. Phys. Behav. 51:1992;81-88.
28. Lendahl U. A growing family of Notch ligands. BioEssays. 20:1998;103-107.
29. Leroy K., Menu R., Conreur J.L., Dayanandan R., Lovestone S., Anderton B.H., Brion J.P. The function of the microtubule-associated protein tau is variable modulated by graded changes in glycogen synthase kinase-3β activity. FEBS Lett. 465:2000;34-38.
30. Li Z., Van Aelst L., Cline H.T. Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3:2000;217-225.
31. Lucas J.J., Hernández F., Gómez-Ramos P., Morán M.A., Hen R., Avila J. Decreased nuclear β-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mouse. EMBO J. 20:2001;27-39.
32. Mackie K., Sorkin B.C., Nairn A.C., Greengard P., Edelman G.M., Cunningham B.A. Identification of two protein kinases that phosphorylate the neural cell-adhesion molecule, N-CAM. J. Neurosci. 9:1989;1883-1896.
33. Marcus E.A., Kintner C., Harris W. The role of GSK-3β in regulating neuronal differentiation in Xenopus laevis. Mol. Cell Neurosci. 12:1998;269-280.
34. Moechars D., Dewachter I., Lorent K., Reversé D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., VandenHaute C., Checler F., Godaux E., Cordell B., Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem. 274:1999;6483-6492.
35. Moechars D., Lorent K., De Strooper B., Dewachter I., Van Leuven F. Expression in brain of amyloid precursor protein mutated in the α-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice. EMBO J. 15:1996;1265-1274.
36. Morris R. Thy-1, the enigmatic extrovert on the neuronal surface. BioAssay. 14:1992;715-722.
37. Morris R.J., Tiveron M.C., Xue G.P. The relation of the expression and function of the neuronal glycoprotein Thy-1 to axonal growth. Biochem. Soc. Trans. 20:1992;401-405.
38. Payen E., Verkerk T., Michalovich D., Dreyer S.D., Winterpacht A., Lee B., De Zeeuw C.I., Grosveld F., Galjart N. The centromeric/nucleolar chromatin protein Zfp-37 may function to specify neuronal nuclear domains. J. Biol. Chem. 273:1998;9099-9109.
39. Pellegri G., Rossier P., Magistretti P.J., Martin J.-L. Cloning, localization and induction of mouse brain glycogen synthase. Mol. Brain Res. 38:1996;191-199.
40. Perrimon N., Smouse D. Multiple functions of a Drosophila homeotic gene, zeste-white 3, during segmentation and neurogenesis. Dev. Biol. 135:1989;287-305.
41. Redmond L., Oh S.-R., Hicks C., Weinmaster G., Gosh A. Nuclear Notch 1 signaling and the regulation of dendritic development. Nat. Neurosci. 3:2000;30-40.
42. Sánchez C., Tompa P., Szücs K., Friedrich P., Avila J. Phosphorylation and dephosphorylation in the proline-rich C-terminal domain of microtubule-associated protein 2. Eur. J. Biochem. 241:1996;765-771.
43. Sanchez S., Sayas C.L., Lim F., Diaz-Nido J., Avila J., Wandosell F. The inhibition of phophatidylinositol-3-kinase induces neurite retraction and activates GSK3. J. Neurochem. 78:2001;468-481.
44. Sarter M., Bodewitz G., Stephens D.N. Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology. 94:1988;491-495.
45. Sayas C.L., Moreno-Flores M.T., Avila J., Wandosell F. The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like tau phosphorylation. J. Biol. Chem. 274:1999;37046-37052.
46. Scanga S.E., Ruel L., Binari R.C., Snow B., Stambolic V., Bouchard D., Peters M., Calvieri B., Mak T.W., Woodgett J.R., Manoukian A.S. The conserved PI3′K/PTEN/Akt signalling pathway regulates both cell size and survival in Drosophila. Oncogene. 19:2000;3971-3977.
47. Sharma N., Kress Y., Shafit-Zagardo B. Antisense MAP-2 oligonucleotides induce changes in microtubule assembly and neuritic elongation in pre-existing neurites of rat cortical neurons. Cell Motil. Cytoskeleton. 27:1994;234-247.
48. Sijbers J., Scheunders P., Verhoye M., Van der Linden A., Van Dyck D., Raman E. Watershed-based segmentation of 3D MR data for volume quantization. Magn. Reson. Imaging. 15:1997;679-688.
49. Simpson P., El Messal M., Moscoso de Prado J., Ripoll P. Stripes of positional homologies across the wing blade of Drosophila melanogaster. Development. 103:1988;391-401.
50. Smith D.J., Stevens M.E., Sudanagunta S.P., Bronson R.T., Makhinson M., Watabe A.M., O'Dell T.J., Fung J., Weier H.-U.G., Cheng J.-F., Rubin E.M. Functional screening of 2 Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat. Genet. 16:1997;28-36.
51. Spittaels K., Van den Haute C., Van Dorpe J., Bruynseels K., Vandezande K., Laenen I., Geerts H., Mercken M., Sciot R., Van Lommel A., Loos R., Van Leuven F. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am. J. Pathol. 155:1999;2153-2165.
52. Spittaels K., Van den Haute C., Van Dorpe J., Geerts H., Mercken M., Bruynseels K., Lasrado R., Vandezande K., Laenen I., Boon T., Van Lint J., Vandenheede J., Moechars D., Loos R., Van Leuven F. Glycogen synthase kinase-3β phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem. 275:2000;41340-413498.
53. Stambolic V., Woodgett J.R. Mitogen inactivation of glycogen synthase kinase-3β in intact cells via serine 9 phosphorylation. Biochem. J. 303:1994;701-704.
54. Tesseur I., Van Dorpe J., Spittaels K., Van den Haute C., Moechars D., Van Leuven F. Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein Tau in the brain of transgenic mice. Am. J. Pathol. 156:2000;951-964.
55. Van den Haute C., Spittaels K., Van Dorpe J., Lasrado R., Vandenzande K., Laenen I., Geerts H., Van Leuven F. Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol. Dis. 8:2001;32-44.
56. Van Dorpe J., Smeijers L., Dewachter I., Nuyens D., Spittaels K., Van den Haute C., Mercken M., Moechars D., Laenen I., Kuiperi C., Bruynseels K., Tesseur I., Loos R., Vanderstichele H., Checler F., Van Leuven F. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the London mutant of human APP in neurons. Am. J. Pathol. 157:2000;1283-1298.
57. Verdu J., Buratovich M.A., Wilder E.L., Birnbaum M.J. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1:1999;500-506.
58. West M. New stereologic methods for counting neurons. Neurobiol. Aging. 14:1993;275-285.
59. West M.J., Gundersen H.J.G. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296:1990;1-22.
60. Woodgett J.R. A common denominator linking glycogen metabolism, nuclear oncogenes and development. TIBS. 16:1991;177-181.