Pre-synaptic GABAB receptors inhibit glutamate release through GIRK channels in rat cerebral cortex

Journal of Neurochemistry

Volumn 107, Issue 6, 2008, Pages 1506-1517

  Ladera, Carolina ^a   Del Carmen Godino, María ^a   Cabañero, María José ^b   Torres, Magdalena ^a   Watanabe, Masahiko ^c   Luján, Rafael ^b   Sánchez Prieto, José ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b Universidad de Castilla La Mancha   (Spain)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Ca2+ channels; Cerebrocortical nerve terminals; GABAB receptors; GIRK channels; Glutamate release; Tertiapin Q

Indexed keywords

CALCIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GLUTAMIC ACID; METABOTROPIC RECEPTOR; PRESYNAPTIC RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; IMMUNOGOLD STAINING; IMMUNOHISTOCHEMISTRY; NERVE ENDING; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; RAT; SYNAPSE;

ANIMALS; BEE VENOMS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELL MEMBRANE; CEREBRAL CORTEX; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GABA AGENTS; GLUTAMIC ACID; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; OMEGA-AGATOXIN IVA; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHLORIDE; PRESYNAPTIC TERMINALS; RATS; RECEPTORS, GABA; SYNAPTOSOMES;

RATTUS;

EID: 56749160443     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05712.x     Document Type: Article

References (51)

1. Aguado C., Colón J., Ciruela F. et al. (2008) Cell type-specific subunit composition of G-protein-gated potassium channels in the cerebellum. J. Neurochem. 105, 497 511.
2. B receptors to the same channels in the hippocampus. Science 234, 1261 1265.
3. Barrie A. P., Nicholls D. G., Sánchez-Prieto J. Shira T. S. (1991) An ion channels locus for the protein kinase C potentiation of transmitter glutamate release from guinea pig cerebrocortical synaptosomes. J. Neurochem. 57, 1398 1404.
4. Brager D. H., Luther P. H., Erdelyi F., Szabo G. Alger B. E. (2003) Regulation of exocytosis from visualized GABAergic boutons in hippocampal slices. J. Neurosci. 23, 10475 10486.
5. Colmers W. F. Pittman Q. J. (1989) Pre-synaptic inhibition by neuropeptide Y and baclofen in hippocampus:insensitivity to pertussis treatmen. Brain Res. 498, 99 104.
6. Colmers W. F. Williams J. T. (1998) Pertussis toxin pre-treatment discriminates between pre- and postsynaptic actions of baclofen in rat dorsal raphe nucleus in vitro. Neurosci. Lett. 93, 300 306.
7. +-channels. Cell. Signal. 9, 551 573.
8. Dittman J. Regher W. G. (1996) Contributions of calcium-dependent and calcium-independent mechanisms to pre-synaptic inhibition at a cerebellar synapse. J. Neurosci. 16, 1623 1633.
9. Drake C. T., Bausch S. B., Milner T. A. Chavkin C. (1997) GIRK1 immunoreactivity is present predominantly in dendrites, dendritic spines, and somata in the CA1 region of the hippocampus. Proc. Natl Acad. Sci. USA 94, 1007 1012.
10. B receptors in the hippocampus have different pharmacological properties. Neuron 1, 585 591.
11. +-current in voltage clamp CA3 pyramidal cells in hippocampal cultures. Proc. Natl Acad. Sci. USA 82, 1558 1562.
12. Grosse G., Eulitz D., Thiele T. et al. (2003) Axonal sorting of Kir3.3 defines a GABA-containing neuron in the CA3 region of rodent hippocampus. Mol. Cell. Neurosci. 24, 709 724.
13. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440 3450.
14. 2+] but not in cAMP mediates L-AP4 inhibition of glutamate release: PKC-mediated suppression of this inhibitory pathway. Eur. J. Neurosci. 8, 700 709.
15. B-mediated pre-synaptic inhibition of excitatory transmission and synaptic vesicle dynamics in cultured hippocampal neurons. Neuron 18, 143 152.
16. Jeong S. W. Ikeda S. R. (1998) G protein alpha subunit G alpha z couples neurotransmitter receptors to ion channels in sympathetic neurons. Neuron 21, 1201 1212.
17. + channels. Biochemistry 38, 14286 14293.
18. B-receptor subtypes assamble into functional heteromeric complexes. Nature 396, 683 686.
19. Koyrakh L., Luján R., Colón J., Karschin C., Kurachi Y., Karschin A. Wickman K. (2005) Molecular and Cellular diversity of neuronal G-protein gated potassium channels. J. Neurosci. 25, 11468 11478.
20. B(2) in the rat hippocampus. J. Neurosci. 23, 11026 11035.
21. B receptors in hippocampal pyramidal cells. J. Neurosci. 26, 4289 4297.
22. Ladera C., Godino M. C., Martín R., Luján R., Shigemoto M., Ciruela F., Torres M. Sánchez-Prieto J. (2007) The coexistence of multiple receptors in a single nerve terminal provides evidence for pre-synaptic integration. J. Neurochem. 103, 2314 2326.
23. López-Bendito G., Shigemoto R., Kulik A., Fairen A. Lujan R. (2004) Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14, 836 848.
24. B2 relative to synaptic sites in the rat developing cerebellum. Eur. J. Neurosci. 23, 1479 1490.
25. Luján R., Aguado C., Marker C. Wickman K. (2005) The Subcellular Localization of GABAB Receptors is Regulated in the Cerebellum of GIRK3 Knock-out Mice. Program No. 959.4. 2005 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC. Available online at: http://sfn.scholarone.com/itin2005/main.html?new_page_id=126&abstract_id= 5596&p_num=959.4&is_tech=0 (last accessed 15 May 2008).
26. Lüscher C., Jan L. Y., Stoffel M., Malenka R. C. Nicoll R. (1997) G-protein-coupled inwardly rectifying channels (GIRKs) mediate postsynaptic but not pre-synaptic transmitter actions in hippocampal neurons. Neuron 19, 687 695.
27. Marker C. L., Luján R., Loh H. H. Wickman K. (2005) Spinal G-protein-gated potassium channels contribute in a dose-dependent manner to the analgesic effect of mu- and delta- but not kappa-opioids. J. Neurosci. 25, 3551 3559.
28. Millán C. Sánchez-Prieto J. (2002) Differential coupling of N and P/Q-type calcium channels to glutamate exocytosis in the rat cerebral cortex. Neurosci. Lett. 330, 29 32.
29. 2+ entry in single nerve terminals. J. Biol. Chem. 277, 14092 14101.
30. 2+ channels in single cerebrocortical nerve terminals from adult rats. J. Biol. Chem. 278, 23955 23962.
31. Mintz I. M., Sabatini B. L. Regehr W. G. (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675 688.
32. Newberry N. R. Nicoll R. A. (1984) Direct hiperpolarising action of baclofen on hippocampal pyramidal cells. Nature 308, 450 452.
33. Olivera B. M., Gray W. R., Zeikus R., McIntosh J. M., Varga J., Rivier J., de Santos V. Cruz L. J. (1985) Peptides neurotoxins from fish-hunting cone snails. Science 230, 1338 1343.
34. B receptor modulation of glutamate exocytosis from rat recebrocortical nerve terminals: receptor decoupling by protein kinase C. J. Neurochem. 70, 1513 1522.
35. + channels protein (GIRK1) are present in the soma and dendrites as well as in nerve terminals of specific neurons in the brain. J. Neurosci. 16, 1990 2001.
36. 2+ channels subunit modulation. J. Neurosci. 21, 3721 3728.
37. B receptor activation at a glutamatergic synapse. Nature 424, 775 778.
38. Scanziani M., Capogna M., Gähwiler B. H. Thompson S. M. (1992) Pre-synaptic inhibition of miniature excitatory synaptic currests by baclofen and adenosine in the hippocampus. Neuron 9, 919 927.
39. Sodickson D. L. Bean B. P. (1998) Neurotransmitter activation of inwardly rectifying potassium current in dissociated hippocampal CA3 neurons: interactions among multiple receptors. J. Neurosci. 18, 8153 8162.
40. + activation of muscarinic K channel by a G protein-independent mechanism. J. Gen. Physiol. 108, 381 391.
41. 2+ channels and synaptic transmission. Nature 361, 165 168.
42. B receptor. J. Neurosci. 18, 3138 3146.
43. B receptor mediated inhibition of calcium channels in isolated nerve terminals. Neurochem. Int. 24, 349 361.
44. Thompson S. M. Gähwiler B. H. (1992) Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 451, 329 345.
45. Thompson S. M., Capogna M. Scanziani M. (1993) Pre-synaptic inhibition in the hippocampus. Trends Neurosci. 16, 222 227.
46. Turner L. O. Dunlap K. (1995) Pharmacological characterization of pre-synaptic calcium channels using subsecond biochemical measurements of synaptosomal neurosecretion. Neuropharmacology 34, 1469 1478.
47. B receptors: synaptic functions and mechanisms of diversity. Curr. Opinion in Neurobiol. 17, 298 303.
48. Vázquez E. Sánchez-Prieto J. (1997) Pre-synaptic modulation of glutamate release targets different calcium channels in rat cerebrocortical nerve terminals. Eur. J. Neurosci. 9, 2009 2018.
49. B receptors variants. Neuron 50, 589 601.
50. Wischmeyer E., Doring F., Wischmeyer E., Spauchus A., Thomzig A., Veh R. Karschin A. (1997) Subunit interaction in the assembly of neuronal Kir3.0 inwardly rectifying K+ channels. Mol. Cell. Neurosci. 9, 194 206.
51. 2+ influx. J. Physiol. 485, 649 657.