Pre-synaptic kainate receptor-mediated facilitation of glutamate release involves PKA and Ca2+-calmodulin at thalamocortical synapses

Journal of Neurochemistry

Volumn 126, Issue 5, 2013, Pages 565-578

  Andrade Talavera, Yuniesky ^a   Duque Feria, Paloma ^a   Sihra, Talvinder S ^b   Rodríguez Moreno, Antonio ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

calcium calmodulin; kainate receptors; pre synaptic; slices; synaptosomes; thalamocortical

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; KAINIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SYNAPTIC TRANSMISSION; SYNAPTOSOME; THALAMOCORTICAL TRACT;

CALCIUM CALMODULIN; KAINATE RECEPTORS; PRE-SYNAPTIC; SLICES; SYNAPTOSOMES; THALAMOCORTICAL;

ALGORITHMS; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CEREBRAL CORTEX; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMATES; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, KAINIC ACID; RECEPTORS, PRESYNAPTIC; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTOSOMES; THALAMUS;

EID: 84883157591     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12310     Document Type: Article

References (45)

1. Agmon A., and, Connors B. W., (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365-379.
2. 2+-calmodulin at mossy fiber-CA3 synapses. J. Neurochem. 122, 891-899.
3. Banerjee A., Meredith R. M., Rodríguez-Moreno A., Mierau S., Auberson Y. P., and, Paulsen O., (2009) Double dissociation of spike timing-dependent potentiation and depresiõn by subunit-preferring NMDA receptor antagonists in mouse barrel cortex. Cereb. Cortex 19, 2959-2969.
4. Bekkers J. M., and, Stevens C. F., (1990) Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724-729.
5. Berridge M. J., (1998) Neuronal calcium signalling. Neuron 21, 13-26.
6. Bettler B., and, Mulle C., (1995) Review: neurotransmitter receptors II. AMPA and kainate receptors. Neuropharmacology 34, 123-139.
7. Cooper D. M., (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375, 517-529.
8. Crair M. C., and, Malenka R. C., (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375, 325-328.
9. Daw M. J., Bannister N. V., and, Isaac J. T., (2006) Rapid, activity-dependent plasticity in timing precision in neonatal barrel cortex. J. Neurosci. 26, 4178-4187.
10. Daw M. J., Scott H. L., and, Isaac J. T., (2007) Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Nat. Neurosci. 10, 493-502.
11. Feldman D. E., Nicoll R. A., and, Malenka R. C., (1999) Synaptic plasticity at thalamocortical synapses in developing rat somatoxensory cortex: LTP, LTD., and silent synapses. J. Neurobiol. 41, 92-101.
12. Fletcher E. J., and, Lodge D., (1996) New developments in the molecular pharmacology of AMPA and kainate receptors. Pharmacol. Ther. 70, 65-89.
13. c but not on cAMP mediates L-AP4 inhibition of glutamate release: PKC-mediated suppression of this inhibitory pathway. Eur. J. Neurosci. 8, 700-709.
14. 2+ mobilising mechanisms in cultured rat cerebellar granule cells. J. Physiol. 456, 667-680.
15. Jane D. E., Lodge D., and, Collingridge G. L., (2009) Kainate receptors: pharmacology, function and therapeutical potential. Neuropharmacology 56, 90-113.
16. Jouhanneau J.-S., Ball S. M., Molnar E., and, Isaac J. T. R., (2011) Mechanisms of bi-directional modulation of thalamocortical transmission in barrel cortex by presynaptic kainate receptors. Neuropharmacology 60, 832-841.
17. 2+ influx and EPSP in area CA1 of the rat hippocampus. J. Physiol. 509, 833-845.
18. Kamiya H., and, Ozawa S., (2000) Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre. J. Physiol. 523, 653-665.
19. 2+ entry is unchanged during hippocampal mossy fiber long-term potentiation. J. Neurosci. 22, 10524-10528.
20. Kerchner G. A., Wilding T. J., Li P., Zhuo M., and, Huettner J. E., (2001) Presynaptic kainate receptors regulate spinal sensory transmission. J. Neurosci. 21, 59-66.
21. Kidd F. L., Coumis U., Collingridge G. L., Crabtree J. W., and, Isaac J. T., (2002) A presynaptic kainate receptor is involved in regulating the dynamic properties of thalamo-cortical synapses during development. Neuron 34, 635-646.
22. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39, 327-341.
23. Lee C. C., and, Sherman S. M., (2008) Synaptic properties of thalamic and intracortical inputs to layer 4 of the first-and-higher order cortical areas in the auditory and somatosensory systems. J. Neurophysiol. 100, 317-326.
24. Malinow R., and, Tsien R. W., (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation. Nature 346, 177-180.
25. Manabe T., Willey D. J., Perkel D. J., and, Nicoll R. A., (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J. Neurophysiol. 70, 1451-1459.
26. Negrete-Díaz J. V., Sihra T. S., Delgado-García J. M., and, Rodríguez-Moreno A., (2006) Kainate receptor-mediated inhibition of glutamate release involves protein kinase A in the mouse hippocampus. J. Neurophysiol. 96, 1829-1837.
27. Negrete-Díaz J. V., Sihra T. S., Delgado-García J. M., and, Rodríguez-Moreno A., (2007) Kainate receptor-mediated presynaptic inhibition converges with presynaptic inhibition mediated by Group II mGluRs and long-term depression at the hippocampal mossy fiber-CA3 synapse. J. Neural Transm. 114, 1425-1431.
28. Nicholls D. G., and, Sihra T. S., (1986) Synaptosomes possess and exocytotic pull of glutamate. Nature 321, 115-118.
29. Perkinton M. S., and, Sihra T. S., (1999) A high-affinity presynaptic kainate-type glutamate receptor facilitates glutamate exocytosis from cerebral cortex nerve terminals (synaptosomes). Neuroscience 90, 1281-1292.
30. Petralia R. S., Wang Y. X., and, Wenthold R. J., (1994) Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349, 85-110.
31. Rodríguez-Moreno A., and, Paulsen O., (2008) Spike timing-dependent long-term depression requires presynaptic NMDA receptors. Nat. Neurosci. 11, 744-745.
32. Rodríguez-Moreno A., and, Sihra T. S., (2004) Presynaptic kainate receptor facilitation of glutamate release involves protein kinase A in the rat hippocampus. J. Physiol. 557, 733-745.
33. Rodríguez-Moreno A., and, Sihra T. S., (2007a) Metabotropic actions of kainate receptors in the CNS. J. Neurochem. 103, 2121-2135.
34. Rodríguez-Moreno A., and, Sihra T. S., (2007b) Kainate receptors with a metabotropic modus operandi. Trends Neurosci. 30, 630-637.
35. Rodríguez-Moreno A., Kohl M. M., Reeve J. E., Eaton T. R., Collins H. A., Anderson H. L., and, Paulsen O., (2011) Presynaptic induction and expression of timing-dependent long-term depression demonstrated by compartment-specific photorelease of a use-dependent NMDA receptor antagonist. J. Neurosci. 31, 8564-8569.
36. Schiffer H. H., Swanson G. T., and, Heinemann S. F., (1997) Rat GluR7 and carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19, 1141-1146.
37. Schmitz D., Frerking M., and, Nicoll R. A., (2000) Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27, 327-338.
38. Schmitz D., Mellor J., and, Nicoll R. A., (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291, 1972-1976.
39. 2+ store-dependent short-term plasticity at hippocampal mossy fibers. J. Neurosci. 28, 13139-13149.
40. Siegelbaum S. A., and, Kandel E. R., (1991) Learning-related synaptic plasticity: LTP and LTD. Curr. Opin. Neurobiol. 1, 113-120.
41. Sihra T. S., (1997) Protein phosphorylation and dephosphorylation in isolated nerve terminals (synaptosomes), in Regulatory Protein Modification. Techniques and Protocols (, Hemmings H. C. Jr, ed.), pp. 67-119. Humana, Totowa, New Jersy.
42. Tong G., Malenka R. C., and, Nicoll R. A., (1996) Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron 16, 1147-1157.
43. Wang S. J., and, Sihra T. S., (2003) Opposing facilitatory and inhibitory modulation of glutamate release elicited by cAMP production in cerebrocortical nerve terminals (synaptosomes). Neuropharmacology 44, 686-697.
44. Wang H., and, Storm D. R., (2003) Calmodulin-regulated adenylyl cyclases: cross-talk and plasticity in the central nervous system. Mol. Pharmacol. 63, 463-468.
45. Wong S. T., Athos J., Figueroa X. A., Pineda V. V., Schaefer M. L., Chavkin C. C., Muglia L. J., and, Storm D. R., (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23, 787-798.