Enhanced phosphorylation of the postsynaptic protein kinase C substrate RC3/neurogranin during long-term potentiation

Brain Research

Volumn 749, Issue 2, 1997, Pages 181-187

  Chen, Shu Jen ^a,c   Sweatt, J David ^a   Klann, Eric ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

calmodulin; hippocampus; learning and memory; postsynaptic protein; protein kinase C substrate; synaptic plasticity

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROGRANIN; PROTEIN KINASE C; PROTEIN KINASE INHIBITOR;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MEMORY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANIMALS; CALMODULIN; CALMODULIN-BINDING PROTEINS; ELECTRIC STIMULATION; HIPPOCAMPUS; KINETICS; LONG-TERM POTENTIATION; NERVE TISSUE PROTEINS; NEUROGRANIN; PHOSPHORYLASE KINASE; PHOSPHORYLATION; PRESYNAPTIC TERMINALS; PROTEIN KINASE C; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0031049691     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)01159-6     Document Type: Article

References (33)

1. Akers, R.F., Lovinger, D.M., Colley, P.A., Linden, D.J., and Routtenberg, A., Translocation of protein kinase C may mediate hippocampal long-term potentiation, Science, 231 (186) 587-589.
2. Baudier, J., Bronner, C., Kligman, D. and Cole, D.R., Protein kinase C substrates from bovine brain, J. Biol. Chem., 264 (1989) 1824-1828.
3. Baudier, J., Deloulme, J.C., Van Dorsselaer, A., Black, D. and Matthes, H.W.D., Purification and characterization of a brain-specific protein kinase C substrate, neurogranin (p. 17), J. Biol. Chem., 266 (1991) 229-237.
4. Bradford, M.M., A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteindye binding, Anal. Biochem., 72 (1976) 248-252.
5. Coggins, P.J., Stanisz, J., Nagy, A. and Zwiers, H., Indentification of a calmodulin-binding, B-50-immunoreactive C-kinase substrate (BICKS) in bovine brain, Neurosci. Res. Commun., 8 (1991) 49-56.
6. Cohen, R.W., Margulies, J.E., Coulter, P.M. II and Watson, J.B., Functional consequences of expression of the neuron-specific protein kinase C substrate RC3 (neurogranin) in Xenopus, oocytes, Brain Res., 627 (1993) 147-152.
7. Deloulme, J.C., Sensenbrenner, M. and Baudier, J., A rapid purification method for neurogranin, a brain specific calmodulin-binding protein kinase C substrate, FEBS Lett., 282 (1991) 183-188.
8. Fedorov, N.B., Pasinelli, P., Oestreicher, A.B., De Graan, P.N.E. and Reymann, K.G., Antibodies to postsynaptic PKC substrate neurogranin prevent long-term potentiation in hippocampal CA1 neurons, Eur. J. Neurosci., 7 (1995) 819-822.
9. 2+/calmodulin-dependent protein kinase II, J. Biol. Chem., 268 (1993) 7863-7867.
10. 2+ is absent, J. Biol. Chem., 270 (1995) 6741-6750.
11. Gerendasy, D.D., Herron, S.R., Watson, J.B. and Sutcliffe, J.G., Mutational and biophysical studies suggest that RC3/neurogranin regulates calmodulin availability, J. Biol. Chem., 269 (1994) 22420-22426.
12. Gianotti, C., Nunzi, M.G., Gispen, W.H. and Corradetti, R., Phosphorylation of the presynaptic protein B50 (GAP43) is increased during electrically induced long-term potentiation, Neuron, 8 (1992) 843-848.
13. Gonzalez, A., Klann, E., Sessoms, J.S. and Chen, S.-J., Use of the synthetic peptide neurogranin (28-43) as a selective protein kinase C substrate in assays of tissue homogenate, Anal. Biochem., 215 (1993) 184-189.
14. Hu, G.-Y., Hvalby, O., Walaas, S.I., Albert, K.A., Skjeflo, P., Andersen, P. and Greengard, P., Protein kinase C injection into hippocampal pyramidal cells elicits features of long-term potentiation, Nature, 328 (1987) 426-429.
15. Klann, E., Chen, S.-J. and Sweatt, J.D., Persistent protein kinase activation in the maintenance phase of long-term potentiation, J. Biol. Chem., 266 (1991) 24253-24256.
16. Klann, E., Chen, S.-J. and Sweatt, J.D., Increased phosphorylation of a 17 kDa protein kinase C substrate (P17) in long-term potentiation, J. Neurochem., 58 (1992) 1576-1579.
17. Klann, E., Chen, S.-J. and Sweatt, J.D., Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a novel peptide substrate, Proc. Natl. Acad. Sci. USA, 90 (1993) 8337-8341.
18. Lisman, J., The CaMKII hypothesis for the storage of synaptic memory, Trends Neurosci., 17 (1994) 406-412
19. 2+/calmodulin-dependent protein kinase, J. Biol. Chem., 267 (1992) 12197-12201.
20. Malinow, R., Madison, D.V. and Tsien, R.W., Persistent protein kinase activity underlying long-term potentiation, Nature, 335 (1988) 820-824.
21. Meiri, K.F. and Gordon-Weeks, P.R., GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and is a component of a membrane skeleton subcellular fraction, J. Neurosci., 10 (1990) 256-266.
22. Nestler, E.J. and Greengard, P., Protein Phosphorylation in the Nervous System, 1984, Wiley, New York.
23. Pasinelli, P., Ramakers, G.M.J., Urban, I.J.A., Hens, J.J.H., Oestreicher, A.B., De Graan, P.N.E. and Gispen, W.H. Long-term potentiation and synaptic protein phosphorylation, Behav. Brain Res., 66 (1995) 53-59.
24. Paudel, H.K., Zwiers, H. and Wang, J.H., Phosphorylase kinase phosphorylates the calmodulin-binding regulatory regions of neuronal tissue-specific proteins B-50 (GAP-43) and neurogranin, J. Biol. Chem., 268 (1993) 6207-6213.
25. Ramakers, G.M.J., De Graan, P.N.E., Urban, U.A., Kraay, D., Tang, T., Pasinelli, P., Oestreicher, A.B. and Gispen, W.H., Temporal differences in the phosphorylation state of pre-and postsynaptic kinase C substrates B-50/GAP-43 and neurogranin during long-term potentiation, J. Biol. Chem., 270 (1995) 13892-13898.
26. Raymond, L.A., Blackstone, C.D. and Huganir, R.L., Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity, Trends Neurosci., 16 (1993) 147-153.
27. Represa, A., Deloulme, J.C., Sensenbrenner, M., Ben-Ari, Y. and Baudier, J., Neurogranin: immunolocalization of a brain-specific protein kinase C substrate, J. Neurosci., 10 (1990) 3782-3792.
28. Sacktor, T.C., Osten, P., Valsamis, H., Jiang, X., Naik, M.U. and Sublette, E., Persistent activation of the z isoform of protein kinase C in the maintenance of long-term potentiation, Proc. Natl. Acad. Sci. USA, 90 (1993) 8342-8346.
29. Shearman, M.S., Ogita, K., Kikkawa, U. and Nishizuka, Y., A rapid method for the resolution of protein kinase C subspecies from rat brain tissue, Methods Enzymol., 168 (1989) 347-351.
30. van Lockeren Campagne, M., Oestreicher, A.B., van Bergen en Henegouwen, P.M.P. and Gispen, W.H., Ultrastructural immunocytochemical localization of B-50/GAP-43, a protein kinase C substrate in isolated presynaptic nerve terminals and nerve growth cones, J. Neurocytol., 18 (1989) 479-489.
31. Wang, J.-H. and Feng, D.-P., Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region, Proc. Natl. Acad. Sci. USA, 89 (1992) 2576-2580.
32. Watson, J.B., Battenberg, E.F., Wong, K.K., Bloom, F.E. and Sutcliffe, J.G., Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein, J. Neurosci. Res., 26 (1990) 397-408.
33. Watson, J.B., Sutcliffe, J.G. and Fisher, R.S., Localization of the protein kinase C phosphorylation/calmodulin-binding substrate RC3 in dendritic spines of neostriatal neurons, Proc. Natl. Acad. Sci. USA, 89 (1992) 8581-8585.