Age-related changes in synaptic phosphorylation and dephosphorylation

Advances in Cell Aging and Gerontology

Volumn 16, Issue , 2004, Pages 133-152

  Foster, Thomas C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33645189598     PISSN: 15663124     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1566-3124(04)16006-9     Document Type: Review

References (155)

1. M.A. Abdul-Ghani T.A. Valiante P.L. Carlen P.S. Pennefather Tyrosine kinase inhibitors enhance a Ca(2+)-activated K+ current (IAHP) and reduce IAHP suppression by a metabotropic glutamate receptor agonist in rat dentate granule neurones J. Physiol. 496 Pt 1 1996 139 144
2. T. Abel P.V. Nguyen M. Barad T.A. Deuel E.R. Kandel R. Bourtchouladze Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory Cell 88 1997 615 626
3. S. Alagarsamy M.J. Marino S.T. Rouse R.W.T. Gereau S.F. Heinemann P.J. Conn Activation of NMDA receptors reverses desensitization of mGluR5 in native and recombinant systems Nat. Neurosci. 2 1999 234 240
4. S. Alaluf E.R. Mulvihill R.A. McIlhinney Rapid agonist mediated phosphorylation of the metabotropic glutamate receptor 1 alpha by protein kinase C in permanently transfected BHK cells FEBS Lett. 367 1995 301 305
5. F.A. Antoni M. Palkovits J. Simpson S.M. Smith A.L. Leitch R. Rosie G. Fink J.M. Paterson Ca2+/calcineurin-inhibited adenylyl cyclase, highly abundant in forebrain regions, is important for learning and memory J. Neurosci. 18 1998 9650 9661
6. R. Anwyl Metabotropic glutamate receptors: electrophysiological properties and role in plasticity Brain Res. Brain Res. Rev. 29 1999 83 120
7. H.J. Armbrecht M.A. Boltz V.B. Kumar J.F. Flood J.E. Morley Effect of age on calcium-dependent proteins in hippocampus of senescence-accelerated mice Brain Res. 842 1999 287 293
8. S. Attucci G.V. Clodfelter O. Thibault J. Staton F. Moroni P.W. Landfield N.M. Porter Group I metabotropic glutamate receptor inhibition selectively blocks a prolonged Ca(2+) elevation associated with age-dependent excitotoxicity Neuroscience 112 2002 183 194
9. M.E. Bach M. Barad H. Son M. Zhuo Y.F. Lu R. Shih I. Mansuy R.D. Hawkins E.R. Kandel Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway Proc. Natl. Acad. Sci. USA 96 1999 5280 5285
10. T.G. Banke D. Bowie H. Lee R.L. Huganir A. Schousboe S.F. Traynelis Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase J. Neurosci. 20 2000 89 102
11. C.A. Barnes S.J. Mizumori D.M. Lovinger F.S. Sheu K. Murakami S.Y. Chan D.J. Linden R.B. Nelson A. Routtenberg Selective decline in protein F1 phosphorylation in hippocampus of senescent rats Neurobiol. Aging 9 1988 393 398
12. C.A. Barnes G. Rao G. Orr Age-related decrease in the Schaffer collateral-evoked EPSP in awake, freely behaving rats Neural Plast. 7 2000 167 178
13. A. Barria D. Muller V. Derkach L.C. Griffith T.R. Soderling Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation Science 276 1997 2042 2045
14. D.K. Bartschat T.E. Rhodes Protein kinase C modulates calcium channels in isolated presynaptic nerve terminals of rat hippocampus J. Neurochem. 64 1995 2064 2072
15. F. Battaini S. Elkabes S. Bergamaschi V. Ladisa L. Lucchi P.N. De Graan T. Schuurman W.C. Wetsel M. Trabucchi S. Govoni Protein kinase C activity, translocation, and conventional isoforms in aging rat brain Neurobiol. Aging 16 1995 137 148
16. Y. Ben-Ari L. Aniksztejn P. Bregestovski Protein kinase C modulation of NMDA currents: an important link for LTP induction Trends Neurosci. 15 1992 333 339
17. C. Blackstone T.H. Murphy S.J. Moss J.M. Baraban R.L. Huganir Cyclic AMP and synaptic activity-dependent phosphorylation of AMPA-preferring glutamate receptors J. Neurosci. 14 1994 7585 7593
18. A.L. Boxer H. Moreno B. Rudy E.B. Ziff FGF-2 potentiates Ca(2+)-dependent inactivation of NMDA receptor currents in hippocampal neurons J. Neurophysiol. 82 1999 3367 3377
19. E.P. Brandon M. Zhuo Y.Y. Huang M. Qi K.A. Gerhold K.A. Burton E.R. Kandel G.S. McKnight R.L. Idzerda Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase Proc. Natl. Acad. Sci. USA 92 1995 8851 8855
20. E.P. Brandon R.L. Idzerda G.S. McKnight PKA isoforms, neural pathways, and behaviour: making the connection Curr. Opin. Neurobiol. 7 1997 397 403
21. Z. Cai J.A. Saugstad S.D. Sorensen K.J. Ciombor C. Zhang H. Schaffhauser F. Hubalek J. Pohl R.M. Duvoisin P.J. Conn Cyclic AMP-dependent protein kinase phosphorylates group III metabotropic glutamate receptors and inhibits their function as presynaptic receptors J. Neurochem. 78 2001 756 766
22. R.C. Carroll R.S. Zukin NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity Trends Neurosci. 25 2002 571 577
23. L. Chen L.Y. Huang Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation Nature 356 1992 521 523
24. F. Ciruela A. Giacometti R.A. McIlhinney Functional regulation of metabotropic glutamate receptor type 1c: a role for phosphorylation in the desensitization of the receptor FEBS Lett. 462 1999 278 282
25. V.M. Coghlan B.A. Perrino M. Howard L.K. Langeberg J.B. Hicks W.M. Gallatin J.D. Scott Association of protein kinase A and protein phosphatase 2B with a common anchoring protein Science 267 1995 108 111
26. M. Colledge R.A. Dean G.K. Scott L.K. Langeberg R.L. Huganir J.D. Scott Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex Neuron 27 2000 107 119
27. P.J. Colombo W.C. Wetsel M. Gallagher Spatial memory is related to hippocampal subcellular concentrations of calcium-dependent protein kinase C isoforms in young and aged rats Proc. Natl. Acad. Sci. USA 94 1997 14195 14199
28. L.B. Dale M. Bhattacharya P.H. Anborgh B. Murdoch M. Bhatia S. Nakanishi S.S. Ferguson G protein-coupled receptor kinase-mediated desensitization of metabotropic glutamate receptor 1A protects against cell death J. Biol. Chem. 275 2000 38213 38220
29. S. Davis H. Salin A. Helme-Guizon S. Dumas A. Stephan M. Corbex J. Mallet S. Laroche Dysfunctional regulation of alphaCaMKII and syntaxin 1B transcription after induction of LTP in the aged rat Eur. J. Neurosci. 12 2000 3276 3282
30. L. de Lecea J.R. Criado S. Rivera W. Wen E. Soriano S.J. Henriksen S.S. Taylor C.M. Gall J.G. Sutcliffe Endogenous protein kinase A inhibitor (PKIalpha) modulates synaptic activity J. Neurosci. Res. 53 1998 269 278
31. L.V. Dekker P.N. De Graan W.H. Gispen Transmitter release: target of regulation by protein kinase C? Prog. Brain Res. 89 1991 209 233
32. V. Derkach A. Barria T.R. Soderling Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors Proc. Natl. Acad. Sci. USA 96 1999 3269 3274
33. R. Dingledine K. Borges D. Bowie S.F. Traynelis The glutamate receptor ion channels Pharmacol. Rev. 51 1999 7 61
34. B.R. Douma E.A. Van der Zee P.G. Luiten Translocation of protein kinase Cgamma occurs during the early phase of acquisition of food rewarded spatial learning Behav. Neurosci. 112 1998 496 501
35. K.E. Eckles E.M. Dudek P.C. Bickford M.D. Browning Amelioration of age-related deficits in the stimulation of synapsin phosphorylation Neurobiol. Aging 18 1997 213 217
36. M.D. Ehlers Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting Neuron 28 2000 511 525
37. M.D. Ehlers W.G. Tingley R.L. Huganir Regulated subcellular distribution of the NR1 subunit of the NMDA receptor Science 269 1995 1734 1737
38. D.I. Evans R.S. Jones G. Woodhall Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex J. Neurophysiol. 85 2001 571 579
39. A. Ferreira M. Rapoport The synapsins: beyond the regulation of neurotransmitter release Cell. Mol. Life Sci. 59 2002 589 595
40. E.H. Fisher E.G. Kreb Conversion of phosphorylase b to phosphorylase a in muscle extracts J. Biol. Chem. 216 1955 121 132
41. D.E. Fordyce J.M. Wehner Effects of aging on spatial learning and hippocampal protein kinase C in mice Neurobiol. Aging 14 1993 309 317
42. T.C. Foster Involvement of hippocampal synaptic plasticity in age-related memory decline Brain Res. Rev. 30 1999 236 249
43. T.C. Foster Regulation of synaptic plasticity in memory and memory decline with aging Prog. Brain Res. 138 2002 283 303
44. T.C. Foster C.M. Norris Age-associated changes in Ca(2+)-dependent processes: relation to hippocampal synaptic plasticity Hippocampus 7 1997 602 612
45. T.C. Foster A. Kumar Calcium dysregulation in the aging brain Neuroscientist 8 2002 297 301
46. T.C. Foster K.M. Sharrow J.R. Masse C.M. Norris A. Kumar Calcineurin links Ca2+ dysregulation with brain aging J. Neurosci. 21 2001 4066 4073
47. Foster, T.C., Sharrow, K.M., Kumar, A., Masse, J., 2003. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol. Aging 24, 839–852
48. E. Friedman H.Y. Wang Effect of age on brain cortical protein kinase C and its mediation of 5-hydroxytryptamine release J. Neurochem. 52 1989 187 192
49. J. Gao D. Yin Y. Yao T.D. Williams T.C. Squier Progressive decline in the ability of calmodulin isolated from aged brain to activate the plasma membrane Ca-ATPase Biochemistry 37 1998 9536 9548
50. D. Genoux U. Haditsch M. Knobloch A. Michalon D. Storm I.M. Mansuy Protein phosphatase 1 is a molecular constraint on learning and memory Nature 418 2002 970 975
51. R.W.T. Gereau S.F. Heinemann Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5 Neuron 20 1998 143 151
52. A. Ghetti S.F. Heinemann NMDA-dependent modulation of hippocampal kainate receptors by calcineurin and Ca(2+)/calmodulin-dependent protein kinase J. Neurosci. 20 2000 2766 2773
53. C. Gianotti A. Porta P.N. De Graan A.B. Oestreicher M.G. Nunzi B-50/GAP-43 phosphorylation in hippocampal slices from aged rats: effects of phosphatidylserine administration Neurobiol. Aging 14 1993 401 406
54. C.X. Gong T.J. Singh I. Grundke-Iqbal K. Iqbal Phosphoprotein phosphatase activities in Alzheimer disease brain J. Neurochem. 61 1993 921 927
55. C.X. Gong S. Shaikh J.Z. Wang T. Zaidi I. Grundke-Iqbal K. Iqbal Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain J. Neurochem. 65 1995 732 738
56. S. Govoni R.A. Rius F. Battaini M. Trabucchi Reduced cAMP-dependent phosphorylation in striatum and nucleus accumbens of aged rats: evidence of an altered functioning of D1 dopaminoceptive neurons J. Gerontol. 43 1988 B93 B97
57. I.A. Graef P.G. Mermelstein K. Stankunas J.R. Neilson K. Deisseroth R.W. Tsien G.R. Crabtree L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons Nature 401 1999 703 708
58. M. Grange-Midroit J.A. Garcia-Sevilla M. Ferrer-Alcon R. La Harpe C. Walzer J. Guimon G protein-coupled receptor kinases, beta-arrestin-2 and associated regulatory proteins in the human brain: postmortem changes, effect of age and subcellular distribution Brain Res. Mol. Brain Res. 101 2002 39 51
59. P. Greengard J. Jen A.C. Nairn C.F. Stevens Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons Science 253 1991 1135 1138
60. Q. Gu R.L. Moss 17 beta-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade J. Neurosci. 16 1996 3620 3629
61. X. He F. Yang Z. Xie B. Lu Intracellular Ca(2+) and Ca(2+)/calmodulin-dependent kinase II mediate acute potentiation of neurotransmitter release by neurotrophin-3 J. Cell Biol. 149 2000 783 792
62. V. Heidinger P. Manzerra X.Q. Wang U. Strasser S.P. Yu D.W. Choi M.M. Behrens Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons J. Neurosci. 22 2002 5452 5461
63. J.W. Hell C.T. Yokoyama L.J. Breeze C. Chavkin W.A. Catterall Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP-dependent protein kinase in hippocampal neurons EMBO J. 14 1995 3036 3044
64. S. Hilfiker V.A. Pieribone A.J. Czernik H.T. Kao G.J. Augustine P. Greengard Synapsins as regulators of neurotransmitter release Phil. Trans. R. Soc. Lond. B. Biol. Sci. 354 1999 269 279
65. S. Hilfiker A.J. Czernik P. Greengard G.J. Augustine Tonically active protein kinase A regulates neurotransmitter release at the squid giant synapse J. Physiol. 531 2001 141 146
66. J.P. Hodgkiss J.S. Kelly Only “de novo” long-term depression (LTD) in the rat hippocampus in vitro is blocked by the same low concentration of FK506 that blocks LTD in the visual cortex Brain Res. 705 1995 241 246
67. S. Hrabetova T.C. Sacktor Transient translocation of conventional protein kinase C isoforms and persistent downregulation of atypical protein kinase Mzeta in long-term depression Brain Res. Mol. Brain Res. 95 2001 146 152
68. C.C. Huang Y.C. Liang K.S. Hsu Characterization of the mechanism underlying the reversal of long term potentiation by low frequency stimulation at hippocampal CA1 synapses J. Biol. Chem. 276 2001 48108 48117
69. A. Hudmon H. Schulman Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function Annu. Rev. Biochem. 71 2002 473 510
70. A. Jouvenceau P. Dutar J.M. Billard Is activation of the metabotropic glutamate receptors impaired in the hippocampal CA1 area of the aged rat? Hippocampus 7 1997 455 459
71. K. Kameyama H.K. Lee M.F. Bear R.L. Huganir Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression Neuron 21 1998 1163 1175
72. F. Karege C. Lambercy M. Schwald T. Steimer M. Cisse Differential changes of cAMP-dependent protein kinase activity and 3H-cAMP binding sites in rat hippocampus during maturation and aging Neurosci. Lett. 315 2001 89 92
73. F. Karege M. Schwald C. Lambercy J.J. Murama M. Cisse A. Malafosse A non-radioactive assay for the cAMP-dependent protein kinase activity in rat brain homogenates and age-related changes in hippocampus and cortex Brain Res. 903 2001 86 93
74. C.A. La Porta R. Comolli Age-dependent modulation of PKC isoforms and NOS activity and expression in rat cortex, striatum, and hippocampus Exp. Gerontol. 34 1999 863 874
75. F.M. LaFerla Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease Nat. Rev. Neurosci. 3 2002 862 872
76. J.Y. Lan V.A. Skeberdis T. Jover S.Y. Grooms Y. Lin R.C. Araneda X. Zheng M.V. Bennett R.S. Zukin Protein kinase C modulates NMDA receptor trafficking and gating Nat. Neurosci. 4 2001 382 390
77. I.D. Laviada I. Galve-Roperh J.M. Malpartida A. Haro cAMP signalling mechanisms with aging in the Ceratitis capitata brain Mech. Ageing Dev. 97 1997 45 53
78. H.K. Lee K. Kameyama R.L. Huganir M.F. Bear NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus Neuron 21 1998 1151 1162
79. H.K. Lee M. Barbarosie K. Kameyama M.F. Bear R.L. Huganir Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity Nature 405 2000 955 959
80. B. Li N. Chen T. Luo Y. Otsu T.H. Murphy L.A. Raymond Differential regulation of synaptic and extra-synaptic NMDA receptors Nat. Neurosci. 5 2002 833 834
81. G.Y. Liao D.A. Wagner M.H. Hsu J.P. Leonard Evidence for direct protein kinase-C mediated modulation of N -methyl- d -aspartate receptor current Mol. Pharmacol. 59 2001 960 964
82. D.N. Lieberman I. Mody Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase Nature 369 1994 235 239
83. M.J. Lin S.Y. Lin-Shiau Enhanced spontaneous transmitter release at murine motor nerve terminals with cyclosporine Neuropharmacology 38 1999 195 198
84. R.C. Lin R.H. Scheller Mechanisms of synaptic vesicle exocytosis Annu. Rev. Cell Dev. Biol. 16 2000 19 49
85. J.W. Lin W. Ju K. Foster S.H. Lee G. Ahmadian M. Wyszynski Y.T. Wang M. Sheng Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization Nat. Neurosci. 3 2000 1282 1290
86. K.R. Magnusson Aging of glutamate receptors: correlations between binding and spatial memory performance in mice Mech. Ageing Dev. 104 1998 227 248
87. A.L. Mammen K. Kameyama K.W. Roche R.L. Huganir Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II J. Biol. Chem. 272 1997 32528 32533
88. H. Markram M. Segal Activation of protein kinase C suppresses responses to NMDA in rat CA1 hippocampal neurones J. Physiol. 457 1992 491 501
89. M.F. Matocha S.W. Fitzpatrick J.R. Atack S.I. Rapoport pp60c-src kinase expression in brain of adult rats in relation to age Exp. Gerontol. 25 1990 47 54
90. M. Mayford E.R. Kandel Genetic approaches to memory storage Trends Genet. 15 1999 463 470
91. Y. Mei K.R. Gawai Z. Nie V. Ramkumar R.H. Helfert Age-related reductions in the activities of antioxidant enzymes in the rat inferior colliculus Hear. Res. 135 1999 169 180
92. W. Meier-Ruge P. Iwangoff K. Reichlmeier P. Sandoz Neurochemical findings in the aging brain Adv. Biochem. Psychopharmacol. 23 1980 323 338
93. E.M. Meyer J.H. Judkins The development of age-related deficits in several presynaptic processes associated with brain [3H]acetylcholine release Mech. Ageing Dev. 72 1993 119 128
94. E.M. Meyer J.H. Judkins A.E. Momol E.O. Hardwick Effects of peroxidation and aging on rat neocortical ACh-release and protein kinase C Neurobiol. Aging 15 1994 63 67
95. R. Minakami N. Jinnai H. Sugiyama Phosphorylation and calmodulin binding of the metabotropic glutamate receptor subtype 5 (mGluR5) are antagonistic in vitro J. Biol. Chem. 272 1997 20291 20298
96. T. Mizutani S. Nakashima Y. Nozawa Changes in the expression of protein kinase C (PKC), phospholipases C (PLC) and D (PLD) isoforms in spleen, brain and kidney of the aged rat: RT-PCR and Western blot analysis Mech. Ageing Dev. 105 1998 151 172
97. N. Mons V. Enderlin R. Jaffard P. Higueret Selective age-related changes in the PKC-sensitive, calmodulin-binding protein, neurogranin, in the mouse brain J. Neurochem. 79 2001 859 867
98. R.M. Mulkey S. Endo S. Shenolikar R.C. Malenka Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression Nature 369 1994 486 488
99. P. Mullany S. Connolly M.A. Lynch Ageing is associated with changes in glutamate release, protein tyrosine kinase and Ca2+/calmodulin-dependent protein kinase II in rat hippocampus Eur. J. Pharmacol. 309 1996 311 315
100. M.M. Nicolle P.J. Colombo M. Gallagher M. McKinney Metabotropic glutamate receptor-mediated hippocampal phosphoinositide turnover is blunted in spatial learning-impaired aged rats J. Neurosci. 19 1999 9604 9610
101. C.M. Norris S. Halpain T.C. Foster Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging J. Neurophysiol. 80 1998 1567 1570
102. C.M. Norris E.M. Blalock K.C. Chen N.M. Porter P.W. Landfield Calcineurin enhances L-type Ca(2+) channel activity in hippocampal neurons: increased effect with age in culture Neuroscience 110 2002 213 225
103. L.R. Orlando A.W. Dunah D.G. Standaert A.B. Young Tyrosine phosphorylation of the metabotropic glutamate receptor mGluR5 in striatal neurons Neuropharmacology 43 2002 161 173
104. N. Otmakhov J.E. Lisman Postsynaptic application of a cAMP analogue reverses long-term potentiation in hippocampal CA1 pyramidal neurons J. Neurophysiol. 87 2002 3018 3032
105. A. Parent W. Rowe M.J. Meaney R. Quirion Increased production of inositol phosphates and diacylglycerol in aged cognitively impaired rats after stimulation of muscarinic, metabotropic-glutamate and endothelin receptors J. Pharmacol. Exp. Ther. 272 1995 1110 1116
106. K.D. Parfitt B.J. Hoffer M.D. Browning Norepinephrine and isoproterenol increase the phosphorylation of synapsin I and synapsin II in dentate slices of young but not aged Fisher 344 rats Proc. Natl. Acad. Sci. USA 88 1991 2361 2365
107. A. Pascale S. Govoni F. Battaini Age-related alteration of PKC, a key enzyme in memory processes: physiological and pathological examples Mol. Neurobiol. 16 1998 49 62
108. A. Pascale X. Nogues A. Marighetto J. Micheau F. Battaini S. Govoni R. Jaffard Cytosolic hippocampal PKC and aging: correlation with discrimination performance Neuroreport 9 1998 725 729
109. J.J. Pei E. Sersen K. Iqbal I. Grundke-Iqbal Expression of protein phosphatases (PP-1, PP-2A, PP-2B and PTP-1B) and protein kinases (MAP kinase and P34cdc2) in the hippocampus of patients with Alzheimer disease and normal aged individuals Brain Res. 655 1994 70 76
110. A. Pintor F. Tiburzi A. Pezzola M.T. Volpe Metabotropic glutamate receptor agonist (1S,3R-ACPD) increased frontal cortex dopamine release in aged but not in young rats Eur. J. Pharmacol. 359 1998 139 142
111. A. Pintor R.L. Potenza M.R. Domenici F. Tiburzi R. Reggio A. Pezzola P. Popoli Age-related decline in the functional response of striatal group I mGlu receptors Neuroreport 11 2000 3033 3038
112. N.E. Price M.C. Mumby Brain protein serine/threonine phosphatases Curr. Opin. Neurobiol. 9 1999 336 342
113. M. Qi M. Zhuo B.S. Skalhegg E.P. Brandon E.R. Kandel G.S. McKnight R.L. Idzerda Impaired hippocampal plasticity in mice lacking the Cbeta1 catalytic subunit of cAMP-dependent protein kinase Proc. Natl. Acad. Sci. USA 93 1996 1571 1576
114. M. Racchi S. Govoni S.B. Solerte C.L. Galli E. Corsini Dehydroepiandrosterone and the relationship with aging and memory: a possible link with protein kinase C functional machinery Brain Res. Brain Res. Rev. 37 2001 287 293
115. S. Rahman J.H. McLean A. Darby-King G. Paterno J.N. Reynolds R.S. Neuman Loss of cortical serotonin2A signal transduction in senescent rats: reversal following inhibition of protein kinase C Neuroscience 66 1995 891 901
116. G.M. Ramakers P. Pasinelli J.J. Hens W.H. Gispen P.N. De Graan Protein kinase C in synaptic plasticity: changes in the in situ phosphorylation state of identified pre- and postsynaptic substrates Prog. Neuropsychopharmacol. Biol. Psychiatry 21 1997 455 486
117. G.M. Ramakers K. Heinen W.H. Gispen P.N. de Graan Long term depression in the CA1 field is associated with a transient decrease in pre- and postsynaptic PKC substrate phosphorylation J. Biol. Chem. 275 2000 28682 28687
118. I.M. Raman G. Tong C.E. Jahr Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase Neuron 16 1996 415 421
119. L.A. Raymond C.D. Blackstone R.L. Huganir Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase Nature 361 1993 637 641
120. P.J. Robinson The role of protein kinase C and its neuronal substrates dephosphin, B-50, and MARCKS in neurotransmitter release Mol. Neurobiol. 5 1991 87 130
121. K.W. Roche R.J. O'Brien A.L. Mammen J. Bernhardt R.L. Huganir Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit Neuron 16 1996 1179 1188
122. K.W. Roche S. Standley J. McCallum C. Dune Ly M.D. Ehlers R.J. Wenthold Molecular determinants of NMDA receptor internalization Nat. Neurosci. 4 2001 794 802
123. J. Roeper C. Lorra O. Pongs Frequency-dependent inactivation of mammalian A-type K+ channel KV1.4 regulated by Ca2+/calmodulin-dependent protein kinase J. Neurosci. 17 1997 3379 3391
124. T.B. Romanczyk C.S. Weickert M.J. Webster M.M. Herman M. Akil J.E. Kleinman Alterations in trkB mRNA in the human prefrontal cortex throughout the lifespan Eur. J. Neurosci. 15 2002 269 280
125. C. Rosenmund D.W. Carr S.E. Bergeson G. Nilaver J.D. Scott G.L. Westbrook Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons Nature 368 1994 853 856
126. T. Sato T.S. Wilson L.F. Hughes H.R. Konrad M. Nakayama R.H. Helfert Age-related changes in levels of tyrosine kinase B receptor and fibroblast growth factor receptor 2 in the rat inferior colliculus: implications for neural senescence Neuroscience 103 2001 695 702
127. H. Schaffhauser Z. Cai F. Hubalek T.A. Macek J. Pohl T.J. Murphy P.J. Conn cAMP-dependent protein kinase inhibits mGluR2 coupling to G-proteins by direct receptor phosphorylation J. Neurosci. 20 2000 5663 5670
128. D.B. Scott T.A. Blanpied G.T. Swanson C. Zhang M.D. Ehlers An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing J. Neurosci. 21 2001 3063 3072
129. G. Segovia A. Porras A. Del Arco F. Mora Glutamatergic neurotransmission in aging: a critical perspective Mech. Ageing Dev. 122 2001 1 29
130. A.T. Sim H.G. Lloyd P.E. Jarvie M. Morrison J.A. Rostas P.R. Dunkley Synaptosomal amino acid release: effect of inhibiting protein phosphatases with okadaic acid Neurosci. Lett. 160 1993 181 184
131. A. Simonyi L.A. Miller G.Y. Sun Region-specific decline in the expression of metabotropic glutamate receptor 7 mRNA in rat brain during aging Brain Res. Mol. Brain Res. 82 2000 101 106
132. T.R. Soderling V.A. Derkach Postsynaptic protein phosphorylation and LTP Trends Neurosci. 23 2000 75 80
133. I. Song R.L. Huganir Regulation of AMPA receptors during synaptic plasticity Trends Neurosci. 25 2002 578 588
134. S. Staak T. Behnisch F. Angenstein Hippocampal long-term potentiation: transient increase but no persistent translocation of protein kinase C isoenzymes alpha and beta Brain Res. 682 1995 55 62
135. P. Svenningsson E.T. Tzavara J.M. Witkin A.A. Fienberg G.G. Nomikos P. Greengard Involvement of striatal and extrastriatal DARPP-32 in biochemical and behavioral effects of fluoxetine (Prozac) Proc. Natl. Acad. Sci. USA 99 2002 3182 3187
136. S.L. Swope S.I. Moss L.A. Raymond R.L. Huganir Regulation of ligand-gated ion channels by protein phosphorylation Adv. Second Messenger Phosphoprotein Res. 33 1999 49 78
137. C. Sze H. Bi B.K. Kleinschmidt-DeMasters C.M. Filley L.J. Martin N -Methyl- d -aspartate receptor subunit proteins and their phosphorylation status are altered selectively in Alzheimer's disease J. Neurol. Sci. 182 2001 151 159
138. W.G. Tingley M.D. Ehlers K. Kameyama C. Doherty J.B. Ptak C.T. Riley R.L. Huganir Characterization of protein kinase A and protein kinase C phosphorylation of the N -methyl- d -aspartate receptor NR1 subunit using phosphorylation site-specific antibodies J. Biol. Chem. 272 1997 5157 5166
139. M. Tokuda O. Hatase Regulation of neuronal plasticity in the central nervous system by phosphorylation and dephosphorylation Mol. Neurobiol. 17 1998 137 156
140. K. Tomizawa J. Ohta M. Matsushita A. Moriwaki S.T. Li K. Takei H. Matsui Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity J. Neurosci. 22 2002 2590 2597
141. N. Torii T. Kamishita Y. Otsu T. Tsumoto An inhibitor for calcineurin, FK506, blocks induction of long-term depression in rat visual cortex Neurosci. Lett. 185 1995 1 4
142. A.S. Undie H.Y. Wang E. Friedman Decreased phospholipase C-beta immunoreactivity, phosphoinositide metabolism, and protein kinase C activation in senescent F-344 rat brain Neurobiol. Aging 16 1995 19 28
143. J.R. Unnerstall A. Ladner Deficits in the activation and phosphorylation of hippocampal tyrosine hydroxylase in the aged Fischer 344 rat following intraventricular administration of 6-hydroxydopamine J. Neurochem. 63 1994 280 290
144. E.A. Van der Zee P.G. Luiten J.F. Disterhoft Learning-induced alterations in hippocampal PKC-immunoreactivity: a review and hypothesis of its functional significance Prog. Neuropsychopharmacol. Biol. Psychiatry 21 1997 531 572
145. M. Verona S. Zanotti T. Schafer G. Racagni M. Popoli Changes of synaptotagmin interaction with t-SNARE proteins in vitro after calcium/calmodulin-dependent phosphorylation J. Neurochem. 74 2000 209 221
146. T.W. Vickroy W.L. Malphurs M.L. Carriger Regulation of stimulus-dependent hippocampal acetylcholine release by okadaic acid-sensitive phosphoprotein phosphatases Neurosci. Lett. 191 1995 200 204
147. B. Vissel J.J. Krupp S.F. Heinemann G.L. Westbrook A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux Nat. Neurosci. 4 2001 587 596
148. V. Vogelsberg-Ragaglia T. Schuck J.Q. Trojanowski V.M. Lee PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus Exp. Neurol. 168 2001 402 412
149. M.R. Walton I. Dragunow Is CREB a key to neuronal survival? Trends Neurosci. 23 2000 48 53
150. L.Y. Wang M.W. Salter J.F. MacDonald Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases Science 253 1991 1132 1135
151. L.Y. Wang B.A. Orser D.L. Brautigan J.F. MacDonald Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A Nature 369 1994 230 232
152. Y.T. Wang X.M. Yu M.W. Salter Ca(2+)-independent reduction of N -methyl- d -aspartate channel activity by protein tyrosine phosphatase Proc. Natl. Acad. Sci. USA 93 1996 1721 1725
153. H.G. Wang N. Pathan I.M. Ethell S. Krajewski Y. Yamaguchi F. Shibasaki F. McKeon T. Bobo T.F. Franke J.C. Reed Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD Science 284 1999 339 343
154. J.B. Watson H. Khorasani A. Persson K.P. Huang F.L. Huang T.J. O'Dell Age-related deficits in long-term potentiation are insensitive to hydrogen peroxide: coincidence with enhanced autophosphorylation of Ca2+/calmodulin-dependent protein kinase II J. Neurosci. Res. 70 2002 298 308
155. J.L. Yakel Calcineurin regulation of synaptic function: from ion channels to transmitter release and gene transcription Trends Pharmacol. Sci. 18 1997 124 134