Large-scale study of phosphoproteins involved in long-term potentiation in the rat dentate gyrus in vivo

European Journal of Neuroscience

Volumn 27, Issue 11, 2008, Pages 2985-2998

  Chardonnet, Solenne ^a,b,c   Le Marechal, Pierre ^b,c   Cheval, Hélène ^a,b   Le Caer, Jean Pierre ^d   Decottignies, Paulette ^b,c   Laprevote, Olivier ^d   Laroche, Serge ^a,b   Davis, Sabrina ^a,b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CNRS   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

Author keywords

Hippocampus; Long term potentiation; Phosphorylation; Proteomics; Synaptic plasticity

Indexed keywords

PHOSPHOPROTEIN; PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL FUNCTION; DENTATE GYRUS; ELECTROSPRAY; EXOCYTOSIS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR INTERACTION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEOMICS; RAT; SYNAPTIC MEMBRANE; TIME OF FLIGHT MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; DENTATE GYRUS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLUORESCENT DYES; LONG-TERM POTENTIATION; MALE; MASS SPECTROMETRY; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; STAINING AND LABELING;

EID: 45149084714     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06280.x     Document Type: Article

References (92)

1. Ahmed, Z., Shaw, G., Sharma, V.P., Yang, C., McGowan, E. Dickson, D.W. (2007) Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J. Histochem. Cytochem., 55, 687 700.
2. Ahn, S., Kim, J., Lucaveche, C.L., Reedy, M.C., Luttrell, L.M., Lefkowitz, R.J. Daaka, Y. (2002) Src-dependent tyrosine phosphorylation regulates dynamin self-assembly and ligand-induced endocytosis of the epidermal growth factor receptor. J. Biol. Chem., 277, 26642 26651.
3. Albensi, B.C., Sullivan, P.G., Thompson, M.B., Scheff, S.W. Mattson, M.P. (2000) Cyclosporin ameliorates traumatic brain-injury-induced alterations of hippocampal synaptic plasticity. Exp. Neurol., 162, 385 389.
4. Alberi, S., Boda, B., Steiner, P., Nikonenko, I., Hirling, H. Muller, D. (2005) The endosomal protein NEEP21 regulates AMPA receptor-mediated synaptic transmission and plasticity in the hippocampus. Mol. Cell. Neurosci., 29, 313 319.
5. Alexander, C., Bilgin, N., Lindschau, C., Mesters, J.R., Kraal, B., Hilgenfeld, R., Erdmann, V.A. Lippmann, C. (1995) Phosphorylation of elongation factor Tu prevents ternary complex formation. J. Biol. Chem., 270, 14541 14547.
6. Anggono, V., Smillie, K.J., Graham, M.E., Valova, V.A., Cousin, M.A. Robinson, P.J. (2006) Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat. Neurosci., 9, 752 760.
7. Arimura, N., Menager, C., Kawano, Y., Yoshimura, T., Kawabata, S., Hattori, A., Fukata, Y., Amano, M., Goshima, Y., Inagaki, M., Morone, N., Usukura, J. Kaibuchi, K. (2005) Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol. Cell. Biol., 25, 9973 9984.
8. 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.
9. Bliss, T.V.P. Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31 39.
10. Blitzer, R.D., Connor, J.H., Brown, G.P., Wong, T., Shenolikar, S., Iyengar, R. Landau, E.M. (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science, 280, 1940 1942.
11. Bozon, B., Kelly, A., Josselyn, S.A., Silva, A.J., Davis, S. Laroche, S. (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R Soc. Lond. B Biol. Sci., 358, 805 814.
12. Brown, M., Jacobs, T., Eickholt, B., Ferrari, G., Teo, M., Monfries, C., Qi, R.Z., Leung, T., Lim, L. Hall, C. (2004) Alpha2-chimaerin, cyclin-dependent Kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J. Neurosci., 24, 8994 9004.
13. Bruel-Jungerman, E., Davis, S., Rampon, C. Laroche, S. (2006) Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J. Neurosci., 26, 5888 5893.
14. Chen, H.X., Otmakhov, N., Strack, S., Colbran, R.J. Lisman, J.E. (2001) Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J. Neurophysiol., 85, 1368 1376.
15. Chen, A., Liao, W.P., Lu, Q., Wong, W.S. Wong, P.T. (2007) Upregulation of dihydropyrimidinase-related protein 2, spectrin alpha II chain, heat shock cognate protein 70 pseudogene 1 and tropomodulin 2 after focal cerebral ischemia in rats - a proteomics approach. Neurochem. Int., 50, 1078 1086.
16. Chepkova, A.N., Sergeeva, O.A. Haas, H.L. (2006) Taurine rescues hippocampal long-term potentiation from ammonia-induced impairment. Neurobiol. Dis., 23, 512 521.
17. Colbran, R.J. Soderling, T.R. (1990) Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides. J. Biol. Chem., 265, 11213 11219.
18. Cole, A.R., Knebel, A., Morrice, N.A., Robertson, L.A., Irving, A.J., Connolly, C.N. Sutherland, C. (2004) GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem., 279, 50176 50180.
19. Collingridge, G.L., Isaac, J.T. Wang, Y.T. (2004) Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci., 5, 952 962.
20. Collins, M.O., Yu, L., Coba, M.P., Husi, H., Campuzano, I., Blackstock, W.P., Choudhary, J.S. Grant, S.G. (2005) Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem., 280, 5972 5982.
21. Cooke, S.F., Wu, J., Plattner, F., Errington, M., Rowan, M., Peters, M., Hirano, A., Bradshaw, K.D., Anwyl, R., Bliss, T.V.P. 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.
22. Coughenour, H.D., Spaulding, R.S. Thompson, C.M. (2004) The synaptic vesicle proteome: a comparative study in membrane protein identification. Proteomics, 4, 3141 3155.
23. Cousin, M.A. Robinson, P.J. (2001) The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci., 24, 659 665.
24. Davis, S., Vanhoutte, P., Pages, C., Caboche, J. Laroche, S. (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci., 20, 4563 4572.
25. Donella-Deana, A., James, P., Staudenmann, W., Cesaro, L., Marin, O., Brunati, A.M., Ruzzene, M. Pinna, L.A. (1996) Isolation from spleen of a 57-kDa protein substrate of the tyrosine kinase Lyn. Identification as a protein related to protein disulfide-isomerase and localisation of the phosphorylation sites. Eur. J. Biochem., 235, 18 25.
26. 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.
27. Elgersma, Y., Fedorov, N.B., Ikonen, S., Choi, E.S., Elgersma, M., Carvalho, O.M., Giese, K.P. Silva, A.J. (2002) Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron, 36, 493 505.
28. Franzen, B., Yang, Y., Sunnemark, D., Wickman, M., Ottervald, J., Oppermann, M. Sandberg, K. (2003) Dihydropyrimidinase related protein-2 as a biomarker for temperature and time dependent post mortem changes in the mouse brain proteome. Proteomics, 3, 1920 1929.
29. French, P.J., O'Connor, V., Jones, M.W., Davis, S., Errington, M.L., Voss, K., Truchet, B., Wotjak, C., Stean, T., Doyere, V., Maroun, M., Laroche, S. Bliss, T.V. (2001) Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo. Eur. J. Neurosci., 13, 968 976.
30. 2+/ calmodulin-dependent protein kinase II. J. Biol. Chem., 268, 7863 7867.
31. 2+/calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long-term potentiation. J. Biol. Chem., 270, 6119 6124.
32. Fukunaga, K., Muller, D. Miyamoto, E. (1996) CaM kinase II in long-term potentiation. Neurochem. Int., 28, 343 358.
33. Fukunaga, K., Muller, D., Ohmitsu, M., Bako, E., DePaoli-Roach, A.A. Miyamoto, E. (2000) Decreased protein phosphatase 2A activity in hippocampal long-term potentiation. J. Neurochem., 74, 807 817.
34. Giese, K.P., Fedorov, N.B., Filipkowski, R.K. Silva, A.J. (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science, 279, 870 873.
35. Goshe, M.B., Conrads, T.P., Panisko, E.A., Angell, N.H., Veenstra, T.D. Smith, R.D. (2001) Phosphoprotein isotope-coded affinity tag approach for isolating and quantitating phosphopeptides in proteome-wide analyses. Anal. Chem., 73, 2578 2586.
36. Graham, M.E., Anggono, V., Bache, N., Larsen, M.R., Craft, G.E. Robinson, P.J. (2007) The in vivo phosphorylation sites of rat brain dynamin I. J. Biol. Chem., 282, 14695 14707.
37. Greengard, P., Valtorta, F., Czernik, A.J. Benfenati, F. (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science, 259, 780 785.
38. Griffin, R., Nally, R., Nolan, Y., McCartney, Y., Linden, J. Lynch, M.A. (2006) The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem., 99, 1263 1272.
39. Gu, Y., Hamajima, N. Ihara, Y. (2000) Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry, 39, 4267 4275.
40. Halpain, S. Dehmelt, L. (2006) The MAP1 family of microtubule-associated proteins. Genome Biol., 7, 224.
41. Han, H.Q., Nichols, R.A., Rubin, M.R., Bahler, M. Greengard, P. (1991) Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb. Nature, 349, 697 700.
42. He, H., Chen, M., Scheffler, N.K., Gibson, B.W., Spremulli, L.L. Gottlieb, R.A. (2001) Phosphorylation of mitochondrial elongation factor Tu in ischemic myocardium: basis for chloramphenicol-mediated cardioprotection. Circ. Res., 89, 461 467.
43. Helme-Guizon, A., Davis, S., Israel, M., Lesbats, B., Mallet, J., Laroche, S. Hicks, A. (1998) Increase in syntaxin 1B and glutamate release in mossy fibre terminals following induction of LTP in the dentate gyrus: a candidate molecular mechanism underlying transsynaptic plasticity. Eur. J. Neurosci., 10, 2231 2237.
44. Hicks, A., Davis, S., Rodger, J., Helme-Guizon, A., Laroche, S. Mallet, J. (1997) Synapsin I and syntaxin 1B: key elements in the control of neurotransmitter release are regulated by neuronal activation and long-term potentiation in vivo. Neuroscience, 79, 329 340.
45. Hilfiker, S., Pieribone, V.A., Czernik, A.J., Kao, H.T., Augustine, G.J. Greengard, P. (1999) Synapsins as regulators of neurotransmitter release. Philos. Trans. R Soc. Lond. B Biol. Sci., 354, 269 279.
46. Horwood, J.M., Dufour, F., Laroche, S. Davis, S. (2006) Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur. J. Neurosci., 23, 3375 3384.
47. Izumi, Y., Katsuki, H. Zorumski, C.F. (1997) Monocarboxylates (pyruvate and lactate) as alternative energy substrates for the induction of long-term potentiation in rat hippocampal slices. Neurosci. Lett., 232, 17 20.
48. Jing-Ping, Z., Tian, Q.B., Sakagami, H., Kondo, H., Endo, S. Suzuki, T. (2005) p55 protein is a member of PSD scaffold proteins in the rat brain and interacts with various PSD proteins. Brain Res. Mol. Brain Res., 135, 204 216.
49. Kita, K., Okumura, N., Takao, T., Watanabe, M., Matsubara, T., Nishimura, O. Nagai, K. (2006) Evidence for phosphorylation of rat liver glucose-regulated protein 58, GRP58/ERp57/ER-60, induced by fasting and leptin. FEBS Lett., 580, 199 205.
50. Koch, A., Thiemann, M., Grabenbauer, M., Yoon, Y., McNiven, M.A. Schrader, M. (2003) Dynamin-like protein 1 is involved in peroxisomal fission. J. Biol. Chem., 278, 8597 8605.
51. Langkopf, A., Hammarback, J.A., Muller, R., Vallee, R.B. Garner, C.C. (1992) Microtubule-associated proteins 1A and LC2. Two proteins encoded in one messenger RNA. J. Biol. Chem., 267, 16561 16566.
52. Leenders, A.G. Sheng, Z.H. (2005) Modulation of neurotransmitter release by the second messenger-activated protein kinases: implications for presynaptic plasticity. Pharmacol. Ther., 105, 69 84.
53. Lengyel, I., Fieuw-Makaroff, S., Hall, A.L., Sim, A.T., Rostas, J.A. Dunkley, P.R. (2000) Modulation of the phosphorylation and activity of calcium/calmodulin-dependent protein kinase II by zinc. J. Neurochem., 75, 594 605.
54. Li, K.W., Hornshaw, M.P., Van Der Schors, R.C., Watson, R., Tate, S., Casetta, B., Jimenez, C.R., Gouwenberg, Y., Gundelfinger, E.D., Smalla, K.H. Smit, A.B. (2004a) Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology. J. Biol. Chem., 279, 987 1002.
55. Li, Z., Okamoto, K., Hayashi, Y. Sheng, M. (2004b) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119, 873 887.
56. Liao, L., Pilotte, J., Xu, T., Wong, C.C., Edelman, G.M., Vanderklish, P. Yates, J.R., III. (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics. J. Proteome. Res., 6, 1059 1071.
57. Liu, J.P., Sim, A.T. Robinson, P.J. (1994) Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science, 265, 970 973.
58. Lynch, G., Kessler, M., Halpain, S. Baudry, M. (1983) Biochemical effects of high-frequency synaptic activity studied with in vitro slices. Fed. Proc., 42, 2886 2890.
59. Marsin, A.S., Bertrand, L., Rider, M.H., Deprez, J., Beauloye, C., Vincent, M.F., Van den Berghe, G., Carling, D. Hue, L. (2000) Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol., 10, 1247 1255.
60. McNair, K., Davies, C.H. Cobb, S.R. (2006) Plasticity-related regulation of the hippocampal proteome. Eur. J. Neurosci., 23, 575 580.
61. McNair, K., Broad, J., Riedel, G., Davies, C.H. Cobb, S.R. (2007) Global changes in the hippocampal proteome following exposure to an enriched environment. Neuroscience, 145, 413 422.
62. Migaud, M., Charlesworth, P., Dempster, M., Webster, L.C., Watabe, A.M., Makhinson, M., He, Y., Ramsay, M.F., Morris, R.G., Morrison, J.H., O'Dell, T.J. Grant, S.G. (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature, 396, 433 439.
63. Migues, P.V., Lehmann, I.T., Fluechter, L., Cammarota, M., Gurd, J.W., Sim, A.T., Dickson, P.W. Rostas, J.A. (2006) Phosphorylation of CaMKII at Thr253 occurs in vivo and enhances binding to isolated postsynaptic densities. J. Neurochem., 98, 289 299.
64. Mimura, F., Yamagishi, S., Arimura, N., Fujitani, M., Kubo, T., Kaibuchi, K. Yamashita, T. (2006) Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J. Biol. Chem., 281, 15970 15979.
65. Montgomery, J.M., Selcher, J.C., Hanson, J.E. Madison, D.V. (2005) Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state. BMC Neurosci., 6, 48.
66. Munton, R.P., Tweedie-Cullen, R., Livingstone-Zatchej, M., Weinandy, F., Waidelich, M., Longo, D., Gehrig, P., Potthast, F., Rutishauser, D., Gerrits, B., Panse, C., Schlapbach, R. Mansuy, I.M. (2007) Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell. Proteomics, 6, 283 293.
67. 2+/ 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.
68. Nguyen, C. Bibb, J.A. (2003) Cdk5 and the mystery of synaptic vesicle endocytosis. J. Cell Biol., 163, 697 699.
69. Nielander, H.B., Onofri, F., Schaeffer, E., Menegon, A., Fesce, R., Valtorta, F., Greengard, P. Benfenati, F. (1997) Phosphorylation-dependent effects of synapsin IIa on actin polymerization and network formation. Eur. J. Neurosci., 9, 2712 2722.
70. Patel, M.S. Korotchkina, L.G. (2001) Regulation of mammalian pyruvate dehydrogenase complex by phosphorylation: complexity of multiple phosphorylation sites and kinases. Exp. Mol. Med., 33, 191 197.
71. 2+/calmodulin is inhibited by autophosphorylation of threonine within the calmodulin-binding domain. J. Biol. Chem., 265, 11204 11212.
72. Robinson, P.J., Liu, J.P., Powell, K.A., Fykse, E.M. Sudhof, T.C. (1994) Phosphorylation of dynamin I and synaptic-vesicle recycling. Trends Neurosci., 17, 348 353.
73. 2+ within toluene-permeabilized heart mitochondria. Biochim. Biophys. Acta, 1014, 263 270.
74. Sakai, J., Ishikawa, H., Kojima, S., Satoh, H., Yamamoto, S. Kanaoka, M. (2003) Proteomic analysis of rat heart in ischemia and ischemia-reperfusion using fluorescence two-dimensional difference gel electrophoresis. Proteomics, 3, 1318 1324.
75. Sastry, B.R., Maretic, H., Morishita, W. Xie, Z. (1990) Modulation of the induction of long-term potentiation in the hippocampus. Adv. Exp. Med. Biol., 268, 377 386.
76. 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.
77. Shevchenko, A., Wilm, M., Vorm, O. Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem., 68, 850 858.
78. Soderling, T.R. Derkach, V.A. (2000) Postsynaptic protein phosphorylation and LTP. Trends Neurosci., 23, 75 80.
79. Stanton, P.K. Schanne, F.A. (1986) Hippocampal long-term potentiation increases mitochondrial calcium pump activity in rat. Brain Res., 382, 185 188.
80. Steinberg, T.H., Agnew, B.J., Gee, K.R., Leung, W.Y., Goodman, T., Schulenberg, B., Hendrickson, J., Beechem, J.M., Haugland, R.P. Patton, W.F. (2003) Global quantitative phosphoprotein analysis using multiplexed proteomics technology. Proteomics, 3, 1128 1144.
81. Stevens, S.M., Jr., Zharikova, A.D. Prokai, L. (2003) Proteomic analysis of the synaptic plasma membrane fraction isolated from rat forebrain. Mol. Brain Res., 117, 116 128.
82. Sykova, E. Chvatal, A. (2000) Glial cells and volume transmission in the CNS. Neurochem. Int., 36, 397 409.
83. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T. Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem., 282, 11521 11529.
84. Trinidad, J.C., Thalhammer, A., Specht, C.G., Schoepfer, R. Burlingame, A.L. (2005) Phosphorylation state of postsynaptic density proteins. J. Neurochem., 92, 1306 1316.
85. Trinidad, J.C., Specht, C.G., Thalhammer, A., Schoepfer, R. Burlingame, A.L. (2006) Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Mol. Cell. Proteomics, 5, 914 922.
86. Veyrac, A., Giannetti, N., Charrier, E., Reymond-Marron, I., Aguera, M., Rogemond, V., Honnorat, J. Jourdan, F. (2005) Expression of collapsin response mediator proteins 1, 2 and 5 is differentially regulated in newly generated and mature neurons of the adult olfactory system. Eur. J. Neurosci., 21, 2635 2648.
87. Walikonis, R.S., Jensen, O.N., Mann, M., Provance, D.W. Jr, Mercer, J.A. Kennedy, M.B. (2000) Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci., 20, 4069 4080.
88. Williams, J.M., Thompson, V.L., Mason-Parker, S.E., Abraham, W.C. Tate, W.P. (1998) Synaptic activity-dependent modulation of mitochondrial gene expression in the rat hippocampus. Brain Res. Mol. Brain Res., 60, 50 56.
89. Wu, J., Rowan, M.J. Anwyl, R. (2006) Long-term potentiation is mediated by multiple kinase cascades involving CaMKII or either PKA or p42/44 MAPK in the adult rat dentate gyrus in vitro. J. Neurophysiol., 95, 3519 3527.
90. Ying, S.W., Futter, M., Rosenblum, K., Webber, M.J., Hunt, S.P., Bliss, T.V. Bramham, C.R. (2002) Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J. Neurosci., 22, 1532 1540.
91. Yoon, Y., Krueger, E.W., Oswald, B.J. McNiven, M.A. (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol., 23, 5409 5420.
92. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A. Kaibuchi, K. (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell, 120, 137 149.