Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments

Journal of Neuroscience

Volumn 27, Issue 45, 2007, Pages 12211-12220

  Zhu, Ling Qiang ^a   Wang, Shao Hui ^a   Liu, Dan ^a   Yin, Yang Yang ^a   Tian, Qing ^a   Wang, Xiao Chuan ^a   Wang, Qun ^a   Chen, Jian Guo ^a   Wang, Jian Zhi ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Glutamate; Glycogen synthase kinase 3; Long term potentiation; Postsynaptic density; Synapse; Synapsin I

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM; LITHIUM CHLORIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; PROTEIN; PROTEIN PSD93; SYNAPSIN I; UNCLASSIFIED DRUG; WORTMANNIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMENTIA; DRUG MECHANISM; ENZYME ACTIVATION; HIPPOCAMPUS; IN VITRO STUDY; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSIENT EXPRESSION;

ANIMALS; ENZYME ACTIVATION; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; NEURAL INHIBITION; RATS; RATS, WISTAR; SYNAPSES;

EID: 36048937547     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3321-07.2007     Document Type: Article

References (67)

1. Berger TW, Yeckel M (1991) Long-term potentiation of entorhinal afferents to the hippocampus: enhanced propagation of activity through the trisynaptic pathway. In: Long-term potentiation: a debate of the current issues (Baudry M, Davis JL, eds), pp 327-356. Cambridge, MA: MIT.
2. Bliss TV, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
3. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
4. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Low P, Brodin L, Pieribone VA, Greengard P, Shupliakov O (2003) Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161:737-747.
5. Bortolotto ZA, Fitzjohn SM, Collingridge GL (1999) Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 9:299-304.
6. Bradford HF, Richards CD (1976) Specific release of endogenous glutamate from piriform cortex stimulated in vitro. Brain Res 105:168-172.
7. Canevari L, Richter-Levin G, Bliss TV (1994) LTP in the dentate gyrus is associated with a persistent NMDA receptor-dependent enhancement of synaptosomal glutamate release. Brain Res 667:115-117.
8. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
9. Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193.
10. Chin LS, Li L, Ferreira A, Kosik KS, Greengard P (1995) Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9230-9234.
11. De Sarno P, Bijur GN, Zmijewska AA, Li X, Jope RS (2006) In vivo regulation of GSK3 phosphorylation by cholinergic and NMDA receptors. Neurobiol Aging 27:413-422.
12. Do VH, Martinez CO, Martinez Jr JL, Derrick BE (2002) Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. J Neurophysiol 87:669-678.
13. Eastwood SL, Burnet PW, Harrison PJ (1995) Altered synaptophysin expression as a marker of synaptic pathology in schizophrenia. Neuroscience 66:309-319.
14. Engel T, Hernandez F, Avila J, Lucas JJ (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. Ferreira A, Chin LS, Li L, Lanier LM, Kosik KS, Greengard P (1998) Distinct roles of synapsin I and synapsin II during neuronal development. Mol Med 4:22-28.
16. Gardoni F, Caputi A, Cimino M, Pastorino L, Cattabeni F, Di Luca M (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J Neurochem 71:1733-1741.
17. Geinisman Y, Ganeshina O, Yoshida R, Berry RW, Disterhoft JF, Gallagher M (2004) Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum. Neurobiol Aging 25:407-416.
18. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
19. Grimes CA, Jope RS (2001) The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog Neurobiol 65:391-426.
20. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986a) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261:6084-6089.
21. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986b) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
22. Hernandez F, Borrell J, Guaza C, Avila J, Lucas JJ (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.
23. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
24. Hooper C, Markevich V, Plattner F, Killick R, Schofield E, Engel T, Hernandez F, Anderton B, Rosenblum K, Bliss T, Cooke SF, Avila J, Lucas JJ, Giese KP, Stephenson J, Lovestone S (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur J Neurosci 25:81-86.
25. Hou QL, Gao X, Lu Q, Zhang XH, Tu YY, Jin ML, Zhao GP, Yu L, Jing NH, Li BM (2006) SNAP-25 in hippocampal CA3 region is required for long-term memory formation. Biochem Biophys Res Commun 347:955-962.
26. Jope RS (2003) Lithium and GSK-3: one inhibitor, two inhibitory actions, multiple outcomes. Trends Pharmacol Sci 24:441-443.
27. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nature Protocols 1:2406-2415.
28. Kelly A, Lynch MA (2000) Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3 - kinase inhibitor, wortmannin. Neuropharmacology 39:643-651.
29. Larson J, Lynch G, Games D, Seubert P (1999) Alterations in synaptic transmission and long term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 840:23-35.
30. Lee VM, Balin BJ, Otvos Jr L, Trojanowski JQ (1991) A68: a major subunit of paired helical filaments and derivatized forms of normal Tau. Science 251:675-678.
31. Liu SJ, Zhang AH, Li HL, Wang Q, Deng HM, Netzer WJ, Xu H, Wang JZ (2003) Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87:1333-1344.
32. Liu SJ, Zhang JY, Li HL, Fang ZY, Wang Q, Deng HM, Gong CX, Grundke-Iqbal I, Iqbal K, Wang JZ (2004) Tau becomes a more favorable substrate for GSK-3 when it is prephosphorylated by PKA in rat brain. J Biol Chem 279:50078-50088.
33. Lucas FR, Salinas PC (1997) WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev Biol 192:31-44.
34. Lucas FR, Goold RG, Gordon-Weeks PR, Salinas PC (1998) Inhibition of GSK-3beta leading to the loss of phosphorylated MAP-1B is an early event in axonal remodelling induced by WNT-7a or lithium. J Cell Sci 111:1351-1361.
35. Luscher C, Malenka RC, Nicoll RA (1998) Monitoring glutamate release during LTP with glial transporter currents. Neuron 21:435-441.
36. Lynch MA, Errington ML, Clements MP, Bliss TV, Redini-Del Negro C, Laroche S (1990) Increases in glutamate release and phosphoinositide metabolism associated with long-term potentiation and classical conditioning. Prog Brain Res 83:251-256.
37. Marr D (1971) Atheory of archicortical function. Proc R Soc Lond B Biol Sci 262:23-81.
38. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
39. Mazarati AM, Hohmann JG, Bacon A, Liu H, Sankar R, Steiner RA, Wynick D, Wasterlain CG (2000) Modulation of hippocampal excitability and seizures by galanin. J Neurosci 20:6276-6281.
40. McGahon B, Lynch MA (1996) The synergism between metabotropic glutamate receptor activation and arachidonic acid on glutamate release is occluded by induction of long-term potentiation in the dentate gyrus. Neuroscience 72:847-855.
41. Meberg PJ, Miller MW (2003) Culturing hippocampal and cortical neurons. Methods Cell Biol 71:111-127.
42. Melloni Jr RH, Hemmendinger LM, Hamos JE, DeGennaro LJ (1993) Synapsin I gene expression in the adult rat brain with comparative analysis of mRNA and protein in the hippocampus. J Comp Neurol 327:507-520.
43. Morris RGM, Mcnaughton BL (1987) Memory storage in a distributed model of hippocampal formation. Trends Neurosci 10:408-414.
44. Nichols RA, Chilcote TJ, Czernik AJ, Greengard P (1992) Synapsin I regulates glutamate release from rat brain synaptosomes. J Neurochem 58:783-785.
45. Ordronneau P, Abdullah LH, Petrusz P (1991) An efficient enzyme immunoassay for glutamate using glutaraldehyde coupling of the hapten to microtiter plates. J Immunol Methods 142:169-176.
46. Paxinos G, Watson C. (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
47. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E, Wu D, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT, Collingridge GL (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53:703-717.
48. Pei JJ, Tananka T, Tung YC, Braak E, Iqbal K, Grundke-Iqbal I (1997) Distribution, levels, and activity of glycogen synthase-3 in the Alzheimer's disease brain. J Neuropathol Exp Neurol 56:70-78.
49. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
50. Plattner F, Angelo M, Giese KP (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281:25457-25465.
51. Rabenstein RL, Addy NA, Caldarone BJ, Asaka Y, Gruenbaum LM, Peters LL, Gilligan DM, Fitzsimonds RM, Picciotto MR (2005) Impaired synaptic plasticity and learning in mice lacking beta-adducin, an actin-regulating protein. J Neurosci 25:2138-2145.
52. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G, Hutton M, Ashe KH (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25:10637-10647.
53. Reisberg B, Doody R, Stoffler A, Schmitt F, Ferris S, Mobius HJ (2003) Memantine in moderate-to-severe Alzheimer's disease. N Engl J Med 348:1333-1341.
54. Richter-Levin G, Segal M (1991) The effects of serotonin depletion and raphe grafts on hippocampal electrophysiology and behavior. J Neurosci 11:1585-1596.
55. Rockenstein E, Torrance M, Adame A, Mante M, Bar-on P, Rose JB, Crews L, Masliah E (2007) Neuroprotective effects of regulators of the glycogen synthase kinase-3β signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation. J Neurosci 27:1981-1991.
56. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC (1995) Essential functions of synapsin I and II in synaptic vesicle regulation. Nature 375:488-493.
57. Salinas PC, Hall AC (1999) Lithium and synaptic plasticity. Bipolar Disord 1:87-90.
58. Sato K, Morimoto K, Suemaru S, Sato T, Yamada N (2000) Increased synapsin I immunoreactivity during long-term potentiation in rat hippocampus. Brain Res 872:219-222.
59. Scarpini E, Scheltens P, Feldman H (2003) Treatment of Alzheimer's disease: current status and new perspectives. Lancet Neurol 2:539-547.
60. Shirasaka Y, Wasterlain CG (1994) Chronic epileptogenicity following focal status epilepticus. Brain Res 655:33-44.
61. Son H, Yu IT, Hwang SJ, Kim JS, Lee SH, Lee YS, Kaang BK (2003) Lithium enhances long-term potentiation independently of hippocampal neurogenesis in the rat dentate gyrus. J Neurochem 85:872-881.
62. Terada S, Tsujimoto T, Takei Y, Takahashi T, Hirokawa N (1999) Impairment of inhibitory synaptic transmission in mice lacking synapsin I. J Cell Biol 145:1039-1048.
63. Teter B, Ashford JW (2002) Neuroplasticity in Alzheimer's disease. J Neurosci Res 70:402-437.
64. Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374-391.
65. Veliskova J, Velisek L (2007) Beta-estradiol increases dentate gyrus inhibition in female rats via augmentation of hilar neuropeptide Y. J Neurosci 27:6054-6063.
66. Walling SG, Nutt DJ, Lalies MD, Harley CW (2004) Orexin-A infusion in the locus ceruleus triggers norepinephrine (NE) release and NE-induced long-term potentiation in the dentate gyrus. J Neurosci 24:7421-7426.
67. Wang ZF, Li HL, Li XC, Zhang Q, Tian Q, Wang Q, Xu H, Wang JZ (2006) Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J Neurochem 98:1167-1175.