Glycogen synthase kinase-3 inhibition is integral to long-term potentiation

European Journal of Neuroscience

Volumn 25, Issue 1, 2007, Pages 81-86

  Hooper, Claudie ^a   Markevich, Vladimir ^b   Plattner, Florian ^c   Killick, Richard ^a   Schofield, Emma ^a   Engel, Tobias ^d   Hernandez, Felix ^d   Anderton, Brian ^a   Rosenblum, Kobi ^e   Bliss, Tim ^f   Cooke, Sam F ^d   Avila, Jesús ^d   Lucas, José J ^d   Giese, Karl Peter ^a   Stephenson, John ^a   Lovestone, Simon ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^e UNIVERSITY OF HAIFA   (Israel)

^f NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Alzheimer's disease; GSK 3; Mice; Notch; Wnt

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CARBONATE; SERINE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; COGNITIVE DEFECT; CONTROLLED STUDY; DEMENTIA; DENTATE GYRUS; DRUG BLOOD LEVEL; ENZYME INHIBITION; GENE OVEREXPRESSION; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE;

ANIMALS; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; FUNCTIONAL LATERALITY; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; SERINE; SYNAPTOPHYSIN; SYNAPTOSOMES; TIME FACTORS;

EID: 33846259727     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05245.x     Document Type: Article

References (38)

1. Ahmad-Annuar, A., Ciani, L., Simeonidis, I., Herreros, J., Fredj, N.B., Rosso, S.B., Hall, A., Brickley, S. & Salinas, P.C. (2006) Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J. Cell Biol., 174, 127-139.
2. Barria, A., Muller, D., Derkach, V., Griffith, L.C. & Soderling, T.R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science, 276, 2042-2045.
3. Bortolotto, Z.A. & Collingridge, G.L. (2000) A role for protein kinase C in a form of metaplasticity that regulates the induction of long-term potentiation at CA1 synapses of the adult rat hippocampus. Eur. J. Neurosci., 12, 4055-4062.
4. Bullock, B.P. & Habener, J.F. (1998) Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affinity, conformation, and increases net charge. Biochemistry, 37, 3795-3809.
5. Carlisle, H.J. & Kennedy, M.B. (2005) Spine architecture and synaptic plasticity. TINS, 28, 182-187.
6. Chalecka-Franaszek, E. & Chuang, D.M. (1999) Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Natl Acad. Sci. USA, 96, 8745-8750.
7. Chen, J., Park, C.S. & Tang, S.J. (2006) Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J. Biol. Chem., 281, 11910-11916.
8. Cook, D., Fry, M.J., Hughes, K., Sumathipala, R., Woodgett, J. & Dale, T.C. (1996) Wingless inactivates glycogen synthase kinase-3 via an intraccellular signalling pathway which involves a protein kinase. EMBO J., 15, 4526-4536.
9. Cooke, S.F., Wu, J., Plattner, F., Errington, M., Rowan, M., Peters, M., Hirano, A., Bradshaw, K.D., Anwyl, R., Bliss, T.V. & Giese, K.P. (2006) Autophosphorylation of alphaCaMKII is not a general requirement for NMDA receptor-dependent LTP in the adult mouse. J. Physiol., 574, 805-818.
10. Costa, R.M., Drew, C. & Silva, A.J. (2005) Notch to remember. TINS, 28, 429-435.
11. De Strooper, B., Annaert, W., Cupers, P., Saftig, P., Craessaerts, K., Mumm, J.S., Schroeter, E.H., Schrijvers, V., Wolfe, M.S., Ray, W.J., Goate, A. & Kopan, R. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature, 398, 518-522.
12. Eagar, T.N., Tang, Q., Wolfe, M., He, Y., Pear, W.S. & Bluestone, J.A. (2004) Notch 1 signaling regulates peripheral T cell activation. Immunity, 20, 407-415.
13. Ehrlich, I. & Malinow, R. (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci., 24, 916-927.
14. Engel, T., Hernandez, F., Avila, J. & Lucas, J.J. (2006) Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci., 26, 5083-5090.
15. Espinosa, L., Ingles-Esteve, J., Aguilera, C. & Bigas, A. (2003) Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. J. Biol. Chem., 278, 32227-32235.
16. Facci, L., Stevens, D.A. & Skaper, S.D. (2003) Glycogen synthase kinase-3 inhibitors protect central neurons against excitotoxicity. Neuroreport, 14, 1467-1470.
17. Ferrer, I., Gomez-Isla, T., Puig, B., Freixes, M., Ribe, E., Dalfo, E. & Avila, J. (2005) Current advances on different kinases involved in tau phosphorylation, and implications in Alzheimer's disease and tauopathies. Curr. Alzheimer Res., 2, 3-18.
18. Franco, B., Bogdanik, L., Bobinnec, Y., Debec, A., Bockaert, J., Parmentier, M.L. & Grau, Y. (2004) Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila. J. Neurosci., 24, 6573-6577.
19. Grimes, C.A. & Jope, R.S. (2001) CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J. Neurochem., 78, 1219-1232.
20. Hansen, T.V., Rehfeld, J.F. & Nielsen, F.C. (2004) GSK-3beta reduces cAMP-induced cholecystokinin gene expression by inhibiting CREB binding. Neuroreport, 15, 841-845.
21. Hernandez, F., Borrell, J., Guaza, C., Avila, J. & Lucas, J.J. (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem., 83, 1529-1533.
22. Hye, A., Kerr, F., Archer, N., Foy, C., Poppe, M., Brown, R., Hamilton, G., Powell, J., Anderton, B. & Lovestone, S. (2005) Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease. Neurosci. Lett., 373, 1-4.
23. Impey, S., Mark, M., Villacres, E.C., Poser, S., Chavkin, C. & Storm, D.R. (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron, 16, 973-982.
24. Jope, R.S. & Johnson, G.V. (2004) The glamour and gloom of glycogen synthase kinase-3. TIBS, 29, 95-102.
25. Kelly, S., Zhao, H., Hua, S.G., Cheng, D., Qiao, Y., Luo, J., Martin, K., Steinberg, G.K., Harrison, S.D. & Yenari, M.A. (2004) Glycogen synthase kinase 3beta inhibitor Chir025 reduces neuronal death resulting from oxygen-glucose deprivation, glutamate excitotoxicity, and cerebral ischemia. Exp. Neurol., 188, 378-386.
26. Koivisto, L., Hakkinen, L., Matsumoto, K., McCulloch, C.A., Yamada, K.M. & Larjava, H. (2004) Glycogen synthase kinase-3 regulates cytoskeleton and translocation of Rac1 in long cellular extensions of human keratinocytes. Exp. Cell Res., 293, 68-80.
27. Lau, K.F., Miller, C.C., Anderton, B.H. & Shaw, P.C. (1999) Expression analysis of glycogen synthase kinase-3 in human tissues. J. Pept. Res., 54, 85-91.
28. Leroy, K. & Brion, J.P. (1999) Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J. Chem. Neuroanat., 16, 279-293.
29. Lisman, J. (2003) Long-term potentiation: outstanding questions and attempted synthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, 829-842.
30. Lucas, J.J., Hernandez, F., Gomez-Ramos, P., Moran, M.A., Hen, R. & Avila, J. (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J., 20, 27-39.
31. Nayak, A.S., Moore, C.I. & Browning, M.D. (1996) Ca2+/calmodulin- dependent protein kinase II phosphorylation of the presynaptic protein synapsin I is persistently increased during long-term potentiation. Proc. Natl Acad. Sci. USA, 93, 15451-15456.
32. Opazo, P., Watabe, A.M., Grant, S.G. & O'Dell, T.J. (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J. Neurosci., 23, 3679-3688.
33. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S. & Polakis, P. (1996) Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science, 272, 1023-1026.
34. Sanna, P.P., Cammalleri, M., Berton, F., Simpson, C., Lutjens, R., Bloom, F.E. & Francesconi, W. (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J. Neurosci., 22, 3359-3365.
35. Stambolic, V. & Woodgett, J.R. (1994) Mitogen inactivation of glycogen synthase kinase-3β in intact cells via serine 9 phosphorylation. Biochem. J., 303, 701-704.
36. Wang, Y., Chan, S.L., Miele, L., Yao, P.J., Mackes, J., Ingram, D.K., Mattson, M.P. & Furukawa, K. (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proc. Natl Acad. Sci. USA, 101, 9458-9462.
37. Yao, W.D., Gainetdinov, R.R., Arbuckle, M.I., Sotnikova, T.D., Cyr, M., Beaulieu, J.M., Torres, G.E., Grant, S.G. & Caron, M.G. (2004) Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron, 41, 625-638.
38. Yao, H.B., Shaw, P.C., Wong, C.C. & Wan, D.C. (2002) Expression of glycogen synthase kinase-3 isoforms in mouse tissues and their transcription in the brain. J. Chem. Neuroanat., 23, 291-297.