Intracellular Ca2+ and Ca2+/calmodulin-dependent kinase II mediate acute potentiation of neurotransmitter release by neurotrophin-3

Journal of Cell Biology

Volumn 149, Issue 4, 2000, Pages 783-791

  He, Xiang Ping ^a   Yang, Feng ^a   Xie, Zuo Ping ^a,c   Lu, Bai ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

Acetylcholine; Inositol 1, 4, 5 trisphosphate receptors; Neuromuscular junction; Ryanodine receptors; Synaptic transmission

Indexed keywords

CALCIUM; NEUROTROPHIN 3; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CARRIER PROTEINS; CELLS, CULTURED; COCULTURE TECHNIQUES; ELECTRIC CONDUCTIVITY; ENZYME ACTIVATION; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; NEUROTROPHIN 3; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SYNAPTIC TRANSMISSION; XENOPUS;

EID: 0034658075     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.4.783     Document Type: Article

References (49)

1. Alder, J., Z.-P. Xie, F. Valtorta, P. Greengard, and M.-M. Poo. 1992. Antibodies to synaptophysin interfere with transmitter secretion at neuromuscular synapses. Neuron. 9:759-768.
2. 2+ elevation in hippocampal neurons. Neuroreport. 4:1303-1306.
3. Berridge, M.J. 1998. Neuronal calcium signaling. Neuron. 21:13-26.
4. Cabelli, R.J., A. Horn, and C.J. Shatz. 1995. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science. 267:1662-1666.
5. Cabelli, R.J., D.L. Shelton, R.A. Segal, and C.J. Shatz. 1997. Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron. 19:63-76.
6. 2+/calmodulin kinase II: a bidirectional modulator of presynaptic plasticity. Neuron. 14:591-597.
7. Cochilla, A.J., and S. Alford. 1998. Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron. 20:1007-1016.
8. 2+/calmodulin-dependent protein kinase IV. Role in transcriptional regulation. J. Biol. Chem. 269:15520-15527.
9. Figurov, A., L. Pozzo-Miller, P. Olafsson, T. Wang, and B. Lu 1996. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature. 381:706-709.
10. Gafni, J., J.A. Munsch, T.H. Lam, M.C. Catlin, L.G. Costa, T.F. Molinski, and I.N. Pessah. 1997. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron. 19:723-733.
11. Gonzalez, M., F.P. Ruggiero, O. Chang, Y.J. Shi, M.M. Rich, S. Kraner, and R.J. Balice-Gordon. 1999. Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron. 24:567-583.
12. Gottschalk, W. A., H. Jiang, N. Tartaglia, L. Feng, A. Figurov, and B. Lu. 1999. Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn. Mem. 6:243-256.
13. Greengard, P., F. Valtorta, A.J. Czernik, and F. Benfenati. 1993. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:780-785.
14. Hunt, J.M., E.M. Silinsky, J.K. Hirsh, D. Ahn. and C. Solsona. 1990. The effects of TMB-8 on acetylcholine release from frog motor nerve: interactions with adenosine. Eur. J. Pharmacol. 178:259-266.
15. Ishida, A., I. Kameshita, S. Okuno, T. Kitani, and H. Fujisawa. 1995. A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun. 212:806-812.
16. Jin, P., L.C. Griffith, and R.K. Murphey. 1998. Presynaptic calcium/calmodulin-dependent protein kinase II regulates habituation of a simple reflex in adult Drosophila. J. Neurosci. 18:8955-8964.
17. Kaplan, D.R., and R.M. Stephens. 1994. Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25:1404-1417.
18. Kokaia, M., F. Asztely, K. Olofsdotter, C.B. Sindreu, D.M. Kullmann, and O. Lindvall. 1998. Endogenous neurotrophin-3 regulates short-term plasticity at lateral perforant path-granule cell synapses. J. Neurosci. 18:8730-8739.
19. Korte, M., P. Carroll, E. Wolf, G. Brem, H. Thoenen, and T. Bonhoeffer. 1995. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA. 92:8856-8860.
20. Li, Y.X., Y. Zhang, H.A. Lester, E.M. Schuman, and N. Davidson. 1998. Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci. 18:10231-10240.
21. Lin, J.-W., M. Sugimori, R.R. Llinas, T.L. McGuinness, and P. Greengard. 1990. Effects of synapsin 1 and calciurn/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. Proc. Natl. Acad. Sci. USA. 87:8257-8261.
22. Liou, J.C., and W.M. Fu. 1997. Regulation of quantal secretion from developing motoneurons by postsynaptic activity-dependent release of NT-3. J. Neurosci. 17:2459-2468.
23. Liou, J.C., R.S. Yang, and W.M. Fu. 1997. Regulation of quantal secretion by neurotrophic factors at developing motoneurons in Xenopus cell cultures. J. Physiol. 503:129-139.
24. Llinas, R., T.L. McGuinness, C.S. Leonard, M. Sugimori, and P. Greengard. 1985. Intra-terminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc. Natl. Acad. Sci. USA. 82:3035-3039.
25. Lohof, A.M., N.Y. Ip. and M.M. Poo. 1993. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature. 363:350-353.
26. Lu, B., and A. Figurov. 1997. Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 8:1-12.
27. Lu, B., P. Greengard, and M.-M. Poo. 1992. Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron. 8:521-529.
28. Ma, L., G. Reis, L.F. Parada, and E.M. Schuman. 1999. Neuronal NT-3 is not required for synaptic transmission or long-term potentiation in area CA1 of the adult rat hippocampus. Learn. Mem. 6:267-275.
29. Marsh, H.N., and H.C. Palfrey. 1996. Neurotrophin-3 and brain-derived neurotrophic factor activate multiple signal transduction events but are not survival factors for hippocampal pyramidal neurons. J. Neurochem. 67:952-963.
30. McAllister, A.K., D.C. Lo, and L.C. Katz. 1995. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron. 15:791-803.
31. McAllister, A.K., L.C. Katz, and D.C. Lo. 1997. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron. 18:767-778.
32. McAllister, A.M., L.C. Katz, and D.C. Lo. 1999. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22:295-318
33. Molhet, J.P., P. Fossier, F.M. Meunier, J. Stinnakre, L. Taue, and G. Baux. 1998. Cyclic ADP-ribose and calcium-induced calcium release regulate neurotransmitter release at a cholinergic synapse of Aplysia. J. Physiol. 507:405-414.
34. Nichols, R.A., T.S. Sihra, A.J. Czernik, A.C. Nairn, and P. Greengard. 1990. Calcium/calmodulin-dependenl protein kinase II increases glutamate and noradrenaline release from synaptosomes. Nature. 343:647-651.
35. Patterson, S.L., T. Abel, T.A. Deuel, K.C. Martin, J.C. Rose, and E.R. Kandel. 1996. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1137-1145.
36. Riddle, D.R., D.C. Lo, and L.C. Katz. 1995. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature. 378:189-191.
37. 2+ oscillations in cultured hippocampal neurons. Brain Res. 778:318-328.
38. Segal, R.A., and M.E. Greenberg. 1996. Intracellualr signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19:463-189.
39. Smith, A.B., and T.C. Cunnane. 1996. Ryanodine-sensitive calcium stores involved in neurotransmitter release from sympathetic nerve terminals of the guinea-pig. J. Physiol. 497:657-664.
40. Song, H.J., G. Ming, L.E. Fon, E. Belloechio, R.H. Edwards, and M.M. Poo. 1997. Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron. 18:815-826.
41. Song, H., G. Ming, Z. He, M. Lehmann, M. Tessier-Lavigne, and M. Poo. 1998. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science. 281:1515-1518.
42. 2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. J. Neurophysiol. 76:2097-2101.
43. Stoop, R., and M.M. Poo. 1995. Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling. Science. 267:695-699.
44. Stoop, R., and M.M. Poo. 1996. Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J. Neurosci. 16:3256-3264.
45. 2+-ATPasc. Proc. Natl. Acad. Sci. USA. 87:2466-2470.
46. Tokumitsu, H., T. Chijiwa, M. Hagiwara, A. Mizutani, M. Terasawa, and H. Hidaka. 1990. KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 265:4315-4320.
47. Wang, T., K.W. Xie, and B. Lu. 1995. Neurotrophins promote maturation of developing neuromuscular synapses. J. Neurosci. 15:4796-4805.
48. Wang, X.H., and M.M. Poo. 1997. Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron. 19:825-835.
49. Xie, K., T. Wang, P. Olafsson, K. Mizuno, and B. Lu. 1997. Activity-dependent expression of NT-3 in muscle cells in culture: implication in the development of neuromuscular junctions. J. Neurosci. 17:2947-2958.