Differential modulation of glutamatergic and cholinergic synapses by calcineurin in hippocampal CA1 fast-spiking interneurons

Brain Research

Volumn 1004, Issue 1-2, 2004, Pages 125-135

  Wang, Jin Hui ^a   Zhang, Mei J ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Calcineurin; Interneuron; Signaling cascade; Synaptic kinetics

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCINEURIN; CALMODULIN; GLUTAMATE RECEPTOR; GLUTAMIC ACID; NICOTINIC RECEPTOR;

ANIMAL CELL; ARTICLE; CHOLINERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; CALCINEURIN; HIPPOCAMPUS; INTERNEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CHOLINERGIC; RECEPTORS, GLUTAMATE; SYNAPSES; TUBOCURARINE;

EID: 1642343645     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.01.025     Document Type: Article

References (47)

1. Alger B.E. Gating of GABAergic inhibition in hippocampal pyramidal cells. Ann. N.Y. Acad. Sci. 627:1991;249-263.
2. Alkondon M., Pereira E.F., Eisenberg H.M., Albuquerque E.X. Nicotinic receptor activation in human cerebral cortical interneurons: a mechanism for inhibition and disinhibition of neuronal network. J. Neurosci. 20:2000;66-75.
3. Buhler A.V., Dunwiddie T.V. Regulation of the activity of hippocampal stratum oriens interneurons by a7-nicotinic acetylcholine receptors. Neuroscience. 106:2001;55-67.
4. Cameron A.M.et al. Calcineurin associated with the inositol 1,4,5-triphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell. 83:1995;463-472.
5. Carmant L., Woodhall G., Ouardouz M., Robitaille R., Lacaille J.C. Interneuron-specific Ca2+ responses linked to metabotropic and ionotropic glutamate receptors in rat hippocampal slices. Eur. J. Neurosci. 9:1997;1625-1635.
6. Cordeiro J.M., Meireles S.M., Vale M.G., Oliveira C.R., Goncalves P.P. Ca2+ regulation of the carrier-mediated gamma-aminobutyric acid release from isolated synaptic plasma membrane vesicles. Neurosci. Res. 38:2000;385-395.
7. Fenster C.P.et al. Regulation of a4b2 nicotinic receptor desensitization by calcium and protein kinase C. Mol. Pharmacol. 55:1999;432-443.
8. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470.
9. Fricker D., Miles R. Interneuron, spike timing, and perception. Neuron. 32:2001;771-774.
10. Gabbott P.L.A., Bacon S.J. Calcineurin immunoreactivity in prelimbic cortex (area 32) of the rat. Brain Res. 747:1997;352-356.
11. Goncalves P.P., Meireles S.M., Vale M.G. Regulation of the gamma-aminobutyric acid transport activity by protein phosphatases in synaptic plasma membranes. Neurosci. Res. 33:1999;41-47.
12. Goto S., Singer W., Gu Q. Immunocytochemical localization of calcineurin in adult and developing primary visual cortex of cats. Exp. Brain Res. 96:1993;377-386.
13. Hashimoto Y., Perrrino B.A., Soderling T.R. Identification of an autoinhibitory domain in calcineurin. J. Biol. Chem. 265:1990;1924-1927.
14. Jones S., Sudweeks S., Yakel J.L. Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci. 22:1999;555-561.
15. Khiroug L., Sokolova E., Giniatullin R.A., Nistri A. Recovery from desensitization of neuronal nicotinic acetylcholine receptors of rat chromaffin cells is modulated by intracellular calcium through distinct second messengers. J. Neurosci. 18:1998;2458-2466.
16. Klee C.B., Cohen P. Cohen P., Klee C.B. Calmodulin. 1988;225-248 Elsevier, Amsterdam.
17. Ko G., Kelly P.T. Nitric oxide acts as a postsynaptic signaling molecule in calcium/calmodulin-induced synaptic potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 19:1999;6784-6794.
18. Kornau H.-C., Seeburg P.H., Kennedy M.B. Interaction of ion channels and receptors with PDZ domain protein. Curr. Opin. Neurobiol. 7:1997;368-373.
19. Lacaille J.C., Mueller A.L., Kunkel D.D., Schwartzkroin P.A. Local circuit interactions between orien/alveaus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 7:1987;1979-1993.
20. Liu Q.-S., Berg D.K. Actin filaments and the opposing action of CaM kinase II and calcineurin in regulating a7-containing nicotinic receptors on chick ciliary ganglion neurons. J. Neurosci. 19:1999;10280-10288.
21. Liu X.-B., Jones E.G. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not r-aminobutyric acid GABAergic synapses in thalamus and cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 93:1996;7332-7336.
22. Luscher C., Frerking M. Restless AMPA receptors: implications for synaptic transmission and plasticity. Trends Neurosci. 24:2001;665-670.
23. Luscher C.et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron. 24:1999;649-658.
24. Marty A., Neher E. Sakmann B., Neher E. Single Channel Recording. 1995;31-52 Plenum, New York.
25. McBain C.J., Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum-radiatum interneurons of rat hippocampus. J. Physiol. (Lond.). 462:1993;373-392.
26. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev., Neurosci. 2:2001;11-23.
27. McBain C.J., Freund T.F., Mody I. Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. TINS. 22:1999;228-235.
28. McQuistion A.R., Madison D. Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J. Neurosci. 19:1999;2887-2896.
29. Nusser Z.et al. Cell type and pathway dependence of synaptic AMPA receptor number and variability in hippocampus. Neuron. 21:1998;545-559.
30. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. 88:1991;11285-11289.
31. Oliva A.A., Jiang M., Lam T., Smith K.L., Swann J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20:2000;3354-3368.
32. Ouardouz M., Lacaille J.-C. Mechanisms of selective long-term potentiation of excitatory synapses in stratum orien/laves interneurons of rat. J. Neurophysiol. 73:1995;810-819.
33. Porter J.T.et al. Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J. Neurosci. 19:1999;5228-5235.
34. Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70:1990;165-198.
35. Ross S.T., Soltesz I. Long-term plasticity in interneurons of dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 98:2001;8874-8879.
36. Sanes J.R., Lichtman J.W. Can molecules explain long-term potentiation? Nat. Neurosci. 2:1999;597-604.
37. Shao Z., Yakel J.L. Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices. J. Physiol. (Lond.). 527:2000;507-513.
38. Sik A., Hajos N., Culacsi A., Mody I., Freund T.F. The absence of a major Ca2+ signaling pathway in GABAergic neurons of the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 95:1998;3245-3250.
39. Sitges M., Dunkley P.R., Chiu L.M. A role for calcium/calmodulin kinases in the regulation of GABA exocytosis. Neurochem. Res. 20:1995;245-252.
40. Stelzer A., Kay A.R., Wong R.K. GABAA-receptor function in hippocampal cells is maintained by phosphorylation factors. Science. 241:1988;339-341.
41. Storchak L.G., Kravchuk M.V., Himmelreich N.H. Okadaic acid and cyclosporin A modulate [3H]GABA release from rat brain synaptosomes. Neurochem. Int. 38:2001;445-451.
42. Sudweeks S.N., Yakel J.L. Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J. Physiol. (Lond.). 527:2000;515-528.
43. Toth K., McBain C.J. Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat. Neurosci. 1:1998;572-578.
44. Trussell L.O., Thio L.L., Zorumski C.F., Fischbach G.D. Rapid desensitization of glutamate receptors in vertebrate central neurons. Proc. Natl. Acad. Sci. U. S. A. 85:1988;4562-4566.
45. Wang J.-H., Kelly P.T. Postsynaptic calcineurin activity down-regulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CA1 neurons. J. Neurosci. 17:1997;4600-4611.
46. Wang J.-H., Kelly P.T. Ca2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. J. Physiol. (Lond.). 533:2001;407-422.
47. Wong R.K.S., Traub R.D., Miles R. Cellular basis of neuronal synchrony in epilepsy. Adv. Neurol. 44:1986;583-592.