A point mutant of GAP-43 induces enhanced short-term and long-term hippocampal plasticity

European Journal of Neuroscience

Volumn 15, Issue 12, 2002, Pages 1976-1982

  Hulo, S ^a   Alberi, S ^a   Laux, T ^b   Muller, Dominique ^a   Caroni, P ^b  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Facilitation; Long term potentiation; LTP; Neuromodulin; Phosphorylation; PKC; Transmitter release

Indexed keywords

NEUROMODULIN;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; GENE OVEREXPRESSION; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TEMPORAL SUMMATION; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GAP-43 PROTEIN; GENE EXPRESSION; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE; MICE, TRANSGENIC; NEURONS; ORGAN CULTURE TECHNIQUES; PHENOTYPE; PHORBOL 12,13-DIBUTYRATE; PHOSPHORYLATION; POINT MUTATION; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 0036460683     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02026.x     Document Type: Article

References (31)

1. Aigner, L., Arber, S., Kapfhammer, J.P., Laux, T., Schneider, C., Brenner, H.-R. & Caroni, P. (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell, 83, 269-278.
2. Aigner, L. & Caroni, P. (1993) Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J. Cell Biol., 123, 417-429.
3. Aigner, L. & Caroni, P. (1995) Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J. Cell Biol., 128, 647- 660.
4. Akers, R.F., Lovinger, D.M., Colley, P.A., Linden, D.J. & Routtenberg, A. (1986) Translocation of protein kinase C activity may mediate hippocampal long-term potentiation. Science, 231, 587-589.
5. Alexander, K.A., Cimler, B.M., Meier, K.E. & Storm, D.R. (1987) Regulation of calmodulin binding to P-57. J. Biol. Chem., 262, 6108-6113.
6. Benowitz, L.I. & Routtenberg, A. (1997) GAP-43: An intrinsic determinant of neuronal development and plasticity. Trends Neurosci., 20, 84-91.
7. Bliss, T.V.P. & Collingridge, G.L. (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 361, 31-39.
8. Capogna, M., Fankhauser, C., Gagliardini, V., Gähwiler, B.H. & Thompson, S.M. (1999) Excitatory synaptic transmission and its modulation by PKC is unchanged in the hippocampus of GAP-43-deficient mice. Eur. J. Neurosci., 11, 433-440.
9. Caroni, P., Aigner, L. & Schneider, C. (1997) Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction. J. Cell Biol., 136, 679-692.
10. Coggins, P.J. & Zwiers, H. (1989) Evidence for a single protein kinase C-mediated phosphorylation site in rat brain protein B-50. J. Neurochem., 53, 1895-1901.
11. Dekker, L.V., De Graan, P.N.E., Oestricher, A.B., Versteeg, D.H.G. & Gispen, W.H. (1989) Inhibition of noradrenaline release by antibodies to B-50 (GAP-43). Nature, 342, 74-76.
12. Dent, E.W. & Meiri, K.F. (1998) Distribution of phosphorylated GAP-43 (neuromodulin) in growth cones directly reflects growth cone behavior. J. Neurobiol., 35, 287-299.
13. Engert, F. & Bonhoeffer, T. (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature, 399, 66-70.
14. Frey, D., Laux, T., Xu, L., Schneider, C. & Caroni, P. (2000) Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J. Cell Biol., 149, 1443-1454.
15. Gianotti, C., Nunzi, M.G., Gispen, W.H. & Corradetti, R. (1992) Phosphorylation of the presynaptic protein b-50 (GAP-43) is increased during electrically induced long-term potentiation. Neuron, 8, 843-848.
16. Harding, D.I., Greensmith, L., Mason, M., Anderson, P.N. & Vrbova, G. (1999) Overexpression of GAP-43 induces prolonged sprouting and causes death of adult motoneurons. Eur. J. Neurosci., 11, 2237-2242.
17. Klein, R.L., McNamara, R.K., King, M.A., Lenox, R.H., Muzyczka, N. & Meyer, E.M. (1999) Generation of aberrant sprouting in the adult rat brain by GAP-43 somatic gene transfer. Brain Res., 832, 136-144.
18. Larson, J. & Lynch, G. (1986) Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science, 232, 985-988.
19. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D. & Caroni, P. (2000) GAP43, MARCKS, and CAP23 modulate PI (4,5) P (2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol., 149, 1455-1472.
20. Leahy, J.C., Luo, Y., Kent, C.S., Meiri, K.F. & Vallano, M.L. (1993) Demonstration of presynaptic protein kinase C activation following long-term potentiation in rat hippocampal slices. Neuroscience, 52, 563-574.
21. Maier, D.L., Mani, S., Donoval, S.L., Soppet, D., Tesarollo, L., McCasland, J.S. & Meiri, K.F. (1999) Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP) -43 knockout mice. Proc. Natl. Acad. Sci. USA, 96, 9397-9402.
22. Meiri, K.F., Saffell, J.L., Walsh, F.S. & Doherty, P. (1998) Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J. Neurosci., 18, 10429-10437.
23. Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G. & Kiss, J.Z. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron, 17, 413-422.
24. Neve, R.L., Coopersmith, R., McPhie, D.L., Santeufemio, C., Pratt, K.G., Murphy, C.J. & Lynn, S.D. (1998) The neuronal growth-associated protein GAP-43 interacts with rabaptin-5 and participates in endocytosis. J. Neurosci., 18, 7757-7767.
25. Oestreicher, A.B., De Graan, P.N.E., Gispen, W.H., Verhaagen, J. & Schrama, L.H. (1997) B-50, the growth associated protein-43: Modulation of cell morphology and communication in the nervous system. Progr. Neurobiol., 53, 627-686.
26. Ramakers, G.M., De Graan, P.N., Urban, I.J., Kraay, D., Tang, T., Pasinelli, P., Oestreicher, A.B. & Gispen, W.H. (1995) Temporal differences in the phosphorylation state of pre- and postsynaptic protein kinase C substrates B-50/GAP-43 and neurogranin during long-term potentiation. J. Biol. Chem, 270, 13892-13898.
27. Robinson, P.J. (1991) The role of protein kinase C and its neuronal substrates dephosphin, B-50, and MARCKS in neurotransmitter release. Mol. Neurobiol., 5, 87-130.
28. Routtenberg, A., Cantallops, I., Zaffuto, S., Serrano, P. & Namgung, U. (2000) Enhanced learning after genetic overexpression of a brain growth protein. Proc. Natl. Acad. Sci. USA, 97, 7657-7662.
29. Spencer, S.A., Schuh, S.M., Liu, W.S. & Willard, M.B. (1992) GAP-43, a protein associated with axon growth, is phosphorylated at 3 sites in cultured neurons and rat brain. J. Biol. Chem., 267, 9059-9064.
30. Strittmatter, S.M., Fankhauser, C., Huang, P.L., Mashimo, H. & Fishman, M.C. (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell, 80, 445-452.
31. Toni, N., Buchs, P.A., Nikonenko, I., Bron, C.R. & Muller, D. (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature, 402, 421-425.