Induction of long-term potentiation in vivo regulates alternate splicing to alter syntaxin 3 isoform expression in rat dentate gyms

Journal of Neurochemistry

Volumn 71, Issue 2, 1998, Pages 666-675

  Rodger, Jennifer ^a   Davis, Sabrina ^b   Laroche, Serge ^b   Mallet, Jacques ^a   Hicks, Andrew ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CNRS   (France)

Author keywords

Exocytosis; Hippocampus; Long term potentiation; Splicing; Synaptic plasticity; Syntaxins

Indexed keywords

BRAIN PROTEIN; MESSENGER RNA; SYNTAXIN 1B; SYNTAXIN 3A; SYNTAXIN 3B; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DENTATE GYRUS; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; QUANTITATIVE DIAGNOSIS; RAT;

ANIMALIA; STAPHYLOCOCCUS PHAGE 3A; VERTEBRATA;

EID: 0031784631     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.71020666.x     Document Type: Article

References (61)

1. Abraham W. C., Dragunow M., and Tate W. P. (1991) The role of immediate early genes in the stabilization of long-term potentiation. Mol. Neurobiol. 5, 297-314.
2. Bennett M. K., Calakos N., and Scheller R. H. (1992) Syntaxin: a synaptic protein implicated in the docking of vesicles at the active zone. Science 257, 255-259.
3. Bennett M. K., Garcia-Arraràs J. E., Elferinck L. A., Peterson K., Fleming A. M., Hazuka C. D., and Scheller R. H. (1993) The syntaxin family of vesicle transporters. Cell 74, 863-873.
4. Bezprozvanny I., Scheller R. H., and Tsien R. W. (1995) Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378, 623-626.
5. Bliss T. V. P. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-38.
6. Broadie K., Prokop A., Bellen H. J., O'Kane C. J., Schulze K. L., and Sweeney S. T. (1995) Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15, 663-673.
7. Brumell J. H., Volchuk A., Sengelov H., Borregaard N., Cieutat A. M., Bainton D. F., Grinstein S., and Klip A. (1995) Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments. J. Immunol. 155, 5750-5759.
8. Buelt M. K., Glidden B. J., and Storm D. R. (1994) Regulation of p68 RNA helicase by calmodulin and protein kinase C. J. Biol. Chem. 269, 29367-29370.
9. Bullock S., Lössner B., Krug M., Frey S., Rose S. P. R., and Matthias H. (1990) Posttetanic long-term potentiation in rat dentate area increases postsynaptic 411B immunoreactivity. J. Neurochem. 55, 708-713.
10. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270, 23667-23671.
11. Cole A. J., Saffen D. W., Baraban J. M., and Worley P. F. (1989) Rapid increase of an immediate-early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474-476.
12. Dascher C., Matteson J., and Balch W. E. (1994) Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J. Biol. Chem. 269, 29363-29366.
13. Davis S., Rodger J., Hicks A., Mallet J., and Laroche S. (1996) Brain structure and task-specific increase in expression of the gene encoding syntaxin 1B during learning in the rat: a potential molecular marker for learning-induced synaptic plasticity in neural networks. Eur. J. Neurosci. 8, 2068-2074.
14. Dragunow M., Goulding M., Faull R. L. M., Ralph R., Mee E., and Frith R. (1990) Induction of c-fos mRNA and protein in neurones and glia after traumatic brain injury: pharmacological characterization. Exp. Neurol. 107, 236-248.
15. Eastwood S. L., Burnet P. W., Beckwith J., Kerwin R. W., and Harrison P. J. (1994) AMPA glutamate receptors and their flip and flop mRNAs in human hippocampus. Neuroreport 5, 1325-1328.
16. Ehlers M. D., Tingley W. G., and Huganir R. L. (1995) Regulated subcellular distribution of the NR1 subunit of the NMDA receptor. Science 269, 1734-1737.
17. Flor P. J., Gomeza J., Tones M. A., Kuhn R., Pin J.-P., and Knöpfel T. (1996) The C-terminal domain of the mGluR1 metabotropic glutamate receptor affects sensitivity to agonists. J. Neurochem. 67, 58-63.
18. Frey U. and Morris R. G. M. (1997) Synaptic tagging and long-term potentiation. Nature 385, 533-536.
19. Frey U., Krug M., Reymann K. G., and Matthies H. (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phase of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452, 57-65.
20. Garner A. S. and Large T. H. (1994) Isoforms of the avian TrkC receptor: a novel kinase insertion dissociates transformation and process outgrowth from survival. Neuron 13, 457-472.
21. Genetics Computer Group (1994) Program Manual for the Wisconsin Package. Genetics Computer Group, Madison, Wisconsin.
22. Gesemann M., Cavalli V., Denzer A. J., Brancaccio A., Schumacher B., and Ruegg M. A. (1996) Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16, 755-767.
23. A receptor γ2-subunit mRNAs in the chick brain. Eur. J. Neurosci. 4, 271-277.
24. Guivarch D., Vernier P., and Vincent J. D. (1995) Sex steroid hormones change the differential distribution of the isoforms of the D2 dopamine receptor messenger RNA in the rat brain. Neuroscience 69, 159-166.
25. Hanson P. I., Otto H., Barton N., and Jahn R. (1995) N-Ethylmaleimide-sensitive fusion protein and alpha-SNAP induce a conformational change in syntaxin. J. Biol. Chem. 270, 16955-16961.
26. Harris E. W. and Cotman C. W. (1986) Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl-D-aspartate. Neurosci. Lett. 70, 132-137.
27. A receptor β2 subunit. J. Neurochem. 62, 10-16.
28. Helme-Guizon A., Davis S., Israel M., Lesbats B., Mallet J., Laroche S., and 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. (in press).
29. Hicks A., Davis S., Rodger J., Helme-Guizon A., Laroche S., and 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.
30. Hirata K., Sawada S., and Yamamoto C. (1991) Enhancement of transmitter release accompanying with long-term potentiation in synapses between mossy fibers and CA3 neurons in hippocampus. Neurosci. Lett. 11, 73-76.
31. Ibaraki K., Horikawa H. P. M., Monta T., Mori H., Sakimura K., Mishina M., Saisu H., and Abe T. (1995) Identification of four different forms of syntaxin 3. Biochem. Biophys. Res. Commun. 211, 997-1005.
32. Idriss H., Kumar A., Casas-Finet J. R., Guo H., Damuni Z., and Wilson S. H. (1994) Regulation of in vitro nucleic acid strand annealing activity of heterogeneous nuclear ribonucleoprotein protein A1 by reversible phosphorylation. Biochemistry 33, 11382-11390.
33. Jaffe D. and Johnston D. (1990) Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule. J. Neurophysiol. 64, 948-960.
34. Kee Y., Lin R. C., Hsu S. C., and Scheller R. H. (1995) Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation. Neuron 14, 991-998.
35. Krug M., Lossner B., and Ott T. (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res. Bull. 13, 39-42.
36. Landwehrmeyer G. B., Standaert D. G., Testa C. M., Penney J. J., and Young A. B. (1995) NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J. Neurosci. 15, 5297-5307.
37. Laroche S., Doyère V., and Bloch V. (1989) Linear relation between the magnitude of long-term potentiation in the dentate gyrus and associative learning in the rat. A demonstration using commissural inhibition and local infusion of an N-methyl-D-aspartate receptor antagonist. Neuroscience 28, 375-386.
38. Laurie D. J. and Seeburg P. H. (1994) Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14, 3180-3194.
39. Levêque C., El Far O., Martin-Moutot N., Sato K., Kato R., Takahashi M., and Seagar M. J. (1994) Purification of the N-type calcium channel in association with syntaxin and synaptotagmin. A complex implicated in synaptic vesicle exocytosis. J. Biol. Chem. 269, 6306-6312.
40. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375, 594-599.
41. Mermoud J. E., Cohen P. T., and Lamond A. I. (1994) Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J. 13, 5679-5688.
42. Morgans C. W., Brandstätter J. H., Kellerman J., Betz H., and Wässle H. (1996) A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J. Neurosci. 16, 6713-6721.
43. Mosbacher J., Schoepfer R., Monyer H., Burnashev N., Seeburg P. H., and Ruppersberg J. P. (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059-1062.
44. Otani S. and Abraham W. C. (1989) Inhibition of protein-synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats. Neurosci. Lett. 106, 175-180.
45. Qian Z., Gilbert M. E., Colicos M. A., Kandel E. R., and Kuhl D. (1993) Tissue-plasminogen activator is induced as an immediate early gene during seizure, kindling and long-term potentiation. Nature 361, 453-457.
46. Ruiz-Montasell B., Aguado F., Majo G., Chapman E. R., Canals J. M., Marsal J., and Blasi J. (1996) Differential distribution of syntaxin isoforms 1A and 1B in the rat central nervous system. Eur. J. Neurosci. 8, 2544-2552.
47. Sambrook J., Fritsch E. F., and Maniatis T. (1989) Molecular Cloning, A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
48. Sheng Z.-H., Rettig J., Takahashi M., and Catterall W. A. (1994) Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13, 1303-1313.
49. Sheng Z. H., Rettig J., Cook T., and Catterall W. A. (1996) Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379, 451-454.
50. Siebert P. D. and Kellogg D. E. (1995) PCR MIMICs: competitive DNA fragments for use in quantitative PCR, in PCR 2: A Practical Approach (McPherson M. J., Hames B. D., and Taylor G. R., eds), pp. 135-148. IRL Press, Oxford.
51. Spring J., Kato M., and Bernfield M. (1993) Epimorphin is related to a new class of neuronal and yeast vesicle targeting proteins. Trends Biochem. Sci. 18, 124-125.
52. Südhof T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
53. Thomas K. L., Laroche S., Errington M. L., Bliss T. P. V., and Hunt S. P. (1994a) Spatial and temporal changes in signal transduction pathways during LTP. Neuron 13, 737-745.
54. Thomas K. L., Davis S., Laroche S., and Hunt S. P. (1994b) Regulation of the expression of NR1 NMDA glutamate receptor subunits during hippocampal LTP. Neuroreport 6, 119-123.
55. Tingley W. G., Roche K. W., Thompson A. K., and Huganir R. L. (1993) Regulation of NMDA receptor pnosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70-73.
56. Tolle T. R., Berthele A., Laurie D. J., Seeburg P. H., and Zieglgansberger W. (1995) Cellular and subcellular distribution of NMDAR1 splice variant mRNA in the rat lumbar spinal cord. Eur. J. Neurosci. 7, 1235-1244.
57. Wisden W., Errington M. L., Williams S., Dunnett S. B., Waters C., Hitchcock D., Evan G., Bliss T. V. P., and Hunt S. P. (1990) Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4, 603-614.
58. Worley P. F., Bhat R. V., Baraban J. M., Erickson C. A., McNaughton B. L., and Barnes C. A. (1993) Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J. Neurosci. 13, 4776-4786.
59. Xiang Z., Greenwood A., Kairiss E., and Brown T. (1994) Quantal mechanism of long-term potentiation in hippocampal mossy-fiber synapses. J. Neurophysiol. 71, 2552-2556.
60. Yamagata K., Kaufman W. E., Lanahan A., Papavlou M., Barnes C. A., Andreasson K. I., and Worley P. F. (1994) Egr3/Pilot, a zinc finger transcription factor, is rapidly regulated by activity in brain neurons and colocalises with Egrl/zif268. Learn. Mem. 1, 140-152.
61. Zalutsky R. A. and Nicoll R. A. (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248, 1619-1624.