Activation of pre-synaptic M-type K+ channels inhibits [ 3H]d-aspartate release by reducing Ca2+ entry through P/Q-type voltage-gated Ca2+channels

Journal of Neurochemistry

Volumn 109, Issue 1, 2009, Pages 168-181

  Luisi, Rosa ^b   Panza, Elisabetta ^b   Barrese, Vincenzo ^b   Iannotti, Fabio Arturo ^a,b   Viggiano, Davide ^a,b   Secondo, Agnese ^b   Canzoniero, Lorella Maria Teresa ^b   Martire, Maria ^c   Annunziato, Lucio ^b   Taglialatela, Maurizio ^a,b  

^a UNIVERSITY OF MOLISE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

Author keywords

Excitatory amino acid release; Intracellular Ca2+; K v7.2 subunits; M current; Retigabine; Synaptosomes

Indexed keywords

ASPARTIC ACID; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM ION; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KV7.2; POTASSIUM CHANNEL STIMULATING AGENT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; MALE; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTOSOME;

ANIMALS; CALCIUM; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, Q-TYPE; CHO CELLS; CRICETINAE; CRICETULUS; D-ASPARTIC ACID; ION CHANNEL GATING; KCNQ2 POTASSIUM CHANNEL; MALE; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; TRITIUM;

RATTUS;

EID: 61849162291     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05945.x     Document Type: Article

References (55)

1. Aiuchi T., Daimatsu T., Nakaya K. Nakamura Y. (1982) Fluorescence changes of rhodamine 6G associated with changes in membrane potential in synaptosomes. Biochim. Biophys. Acta 685, 289 296.
2. Arriza J. L., Fairman W. A., Wadiche J. I., Murdoch G. H., Kavanaugh M. P. Amara S. G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559 5569.
3. + current in a vertebrate neurone. Nature 28, 673 676.
4. Caminos E., Garcia-Pino E., Martinez-Galan J. R. Juiz J. M. (2007) The potassium channel KCNQ5/Kv7.5 is localized in synaptic endings of auditory brainstem nuclei of the rat. J. Comp. Neurol. 505, 363 378.
5. 2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12, 261 269.
6. Chung H. J., Jan Y. N. Jan L. Y. (2006) Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc. Natl Acad. Sci. USA 103, 8870 8875.
7. Cooper E. C., Aldape K. D., Abosch A., Barbaro N. M., Berger M. S., Peacock W. S., Jan Y. N. Jan L. Y. (2000) Colocalization andcoassembly of two human brain M-Type potassium channel subunits that are mutated in epilepsy. Proc. Natl Acad. Sci. USA 97, 4914 4919.
8. Cooper E. C., Harrington E., Jan Y. N. Jan L. Y. (2001) M Channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J. Neurosci. 21, 9529 9540.
9. + channel. J. Neurosci. 24, 1236 1244.
10. + channels: electrifying regulators of synaptic terminal excitability. Trends Neurosci. 27, 210 217.
11. Dougherty J. J., Wu J. Nichols R. A. (2003) Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J. Neurosci. 23, 6740 6747.
12. Dunkley P. R., Jarvie P. E., Heath J. W., Kidd G. J. E. Rostas J. A. P. (1986) A rapid method for the isolation of synaptosomes on Percoll gradients. Brain Res. 372, 115 129.
13. 2+ entry, and spontaneous transmitter release. Neuron 29, 197 208.
14. 2+ stores can regulate exocytosis in adrenal chromaffin cells. J. Neurosci. 19, 3711 3722.
15. Fremeau R. T. Jr., Voglmaier S., Seal R. P. Edwards R. H. (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 27, 98 103.
16. Geiger J., Weber Y. G., Landwehrmeyer B., Sommer C. Lerche H. (2006) Immunohistochemical analysis of KCNQ3 potassium channels in mouse brain. Neurosci. Lett. 400, 101 104.
17. 2+ channels in rat brain. J. Biol. Chem. 279, 36445 3653.
18. Kornhuber J., Bleich S., Wiltfang J., Maler M. Parsons C. G. (1999) Flupirtine shows functional NMDA receptor antagonism by enhancing Mg2+ block via activation of voltage independent potassium channels. Rapid communication. J. Neural Transm. 106, 857 867.
19. Ladera C., Godino Mdel C., Martín R., Luján R., Shigemoto R., 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.
20. Loane D. J., Lima P. A. Marrion N. V. (2007) Co-assembly of N-type Ca2+ and BK channels underlies functional coupling in rat brain. J. Cell Sci. 120, 985 995.
21. Main M. J., Cryan J. E., Dupere J. R., Cox B., Clare J. J. Burbidge S. A. (2000) Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol. Pharmacol. 58, 253 262.
22. Mandalà M., Serck-Hanssen G., Martino G. Helle K. B. (1999) The fluorescent cationic dye rhodamine 6G as a probe for membrane potential in bovine aortic endothelial cells. Anal. Biochem. 274, 1 6.
23. Martínez-Serrano A. Satrústegui J. (1989) Caffeine-sensitive calcium stores in presynaptic nerve endings: a physiological role? Biochem. Biophys. Res. Commun. 161, 965 971.
24. Martire M., Castaldo P., D'Amico M., Preziosi P., Annunziato L. Tagliatatela M. (2004) M channels containing KCNQ2 subunits modulate norepinephrine, aspartate, and GABA release from hippocampal nerve terminals. J. Neurosci. 24, 592 597.
25. 3H]dopamine release triggered by depolarization and pre-synaptic muscarinic receptor activation from rat striatal synaptosomes. J. Neurochem. 102, 179 193.
26. Miceli F., Soldovieri M. V., Martire M. Taglialatela M. (2008) Molecular pharmacology and therapeutic potential of neuronal Kv7-modulating drugs. Curr. Opin. Pharmacol. 8, 65 74.
27. 2+channels in single nerve terminals. J. Biol. Chem. 277, 47796 47803.
28. Millán C., Castro E., Torres M., Shigemoto R. Sánchez- Prieto J. (2003) Co-expression of metabotropic glutamate receptor 7 and N-type Ca(2+) channels in single cerebrocortical nerve terminals of adult rats. J. Biol. Chem. 278, 23955 23962.
29. Mollard P., Seward E. P. Nowycky M. C. (1995) Activation of nicotinic receptors triggers exocytosis from bovine chromaffin cells in the absence of membrane depolarization. Proc. Natl Acad. Sci. USA 92, 3065 3069.
30. Otto J. F., Kimball M. M. Wilcox K. S. (2002) Effects of the anticonvulsant retigabine on cultured cortical neurons: changes in electroresponsive properties and synaptic transmission. Mol. Pharmacol. 61, 921 927.
31. Pan Z., Kao T., Horvath Z., Lemos J., Sul J. Y., Cranstoun S. D., Bennett V., Scherer S. S. Cooper E. C. (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26, 2599 2613.
32. Parekh A. B., Fleig A. Penner R. (1997) The store-operated calcium current I(CRAC): nonlinear activation by InsP3 and dissociation from calcium release. Cell 89, 973 980.
33. Peretz A., Sheinin A., Yue C. et al. (2007) Pre- and postsynaptic activation of M-channels by a novel opener dampens neuronal firing and transmitter release. J. Neurophysiol. 97, 283 295.
34. Raiteri M., Sala R., Fassio A., Rossetto O. Bonanno G. (2000) Entrapping of impermeant probes of different size into nonpermeabilized synaptosomes as a method to study presynaptic mechanisms. J. Neurochem. 74, 423 431.
35. Raiteri L., Stigliani S., Zedda L., Raiteri M. Bonanno G. (2002) Multiple mechanisms of transmitter release evoked by "pathologically" elevated extracellular [K+]: involvement of transporter reversal and mitochondrial calcium. J. Neurochem. 80, 706 714.
36. + concentrations. J. Neurochem. 103, 952 961.
37. Rundfeldt C. Netzer R. (2000) The novel anticonvulsant retigabine activates M-currents in Chinese hamster ovary-cells tranfected with human KCNQ2/3 subunits. Neurosci. Lett. 282, 73 76.
38. Savić N. Sciancalepore M. (1998) Intracellular calcium stores modulate miniature GABA-mediated synaptic currents in neonatal rat hippocampal neurons. Eur. J. Neurosci. 10, 3379 3386.
39. Schrøder R. L., Jespersen T., Christophersen P., Strøbaek D., Jensen B. S. Olesen S. P. (2001) KCNQ4 channel activation by BMS-204352 and retigabine. Neuropharmacology 40, 888 898.
40. Shah M. M., Mistry M., Marsh S. J., Brown D. A. Delmas P. (2002) Molecular correlates of the M-current in cultured rat hippocampal neurons. J. Physiol. 544 (Pt 1 29 37.
41. Shah M. M., Migliore M., Valencia I., Cooper E. C. Brown D. A. (2008) Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc. Natl Acad. Sci. USA 105, 7869 7874.
42. Soldovieri M. V., Miceli F., Bellini G., Coppola G., Pascotto A. Taglialatela M. (2007) Correlating the clinical and genetic features of benign familial neonatal seizures (BFNS) with the functional consequences of underlying mutations. Channels 1, 228 233.
43. Taglialatela M., Secondo A., Fresi A., Rosati B., Pannaccione A., Castaldo P., Giorgio G., Wanke E. Annunziato L. (2001) Inhibition of depolarization-induced [3H]noradrenaline release from SH-SY5Y human neuroblastoma cells by some second-generation H(1) receptor antagonists through blockade of store-operated Ca(2+) channels (SOCs). Biochem. Pharmacol. 62, 1229 1238.
44. Tatulian L., Delmas P., Abogadie F. C. Brown D. A. (2001) Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anti-convulsant drug retigabine. J. Neurosci. 21, 5535 5545.
45. Taverna E., Saba E., Rowe J., Francolini M., Clementi F. Rosa P. (2004) Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes. J. Biol. Chem. 279, 5127 5134.
46. Taylor S. C. Peers C. (1999) Store-operated Ca2+ influx and voltage-gated Ca2+ channels coupled to exocytosis in pheochromocytoma (PC12) cells. J. Neurochem. 73, 874 880.
47. Treiman M., Caspersen C. Christensen S. B. (1998) A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca(2+)-ATPases. Trends Pharmacol. Sci. 19, 131 135.
48. Turner T. J. Dunlap K. (1995) Pharmacological characterization of presynaptic calcium channels using subsecond biochemical measurements of synaptosomal neurosecretion. Neuropharmacology 34, 1469 1478.
49. Umemiya M. Berger A. J. (1995) Single-channel properties of four calcium channel types in rat motoneurons. J. Neurosci. 15, 2218 2224.
50. Usachev Y. M. Thayer S. A. (1999) Ca2+ influx in resting rat sensory neurones that regulates and is regulated by ryanodine-sensitive Ca2+ stores. J. Physiol. 519, 115 130.
51. Vervaeke K., Gu N., Agdestein C., Hu H. Storm J. F. (2006) Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release. J. Physiol. 576, 235 256.
52. Wang H. S., Pan Z., Shi W., Brown B. S., Wymore R. S., Cohen I. S., Dixon J. E. McKinnon D. (1998) KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890 1893.
53. Witzmann F. A., Arnold R. J., Bai F. et al. (2005) A proteomic survey of rat cerebral cortical synaptosomes. Proteomics 5, 2177 2201.
54. 2+/calmodulin impacts on their ability to support exocytosis in chromaffin cells. J. Neurosci. 27, 5236 5248.
55. Zaczek R., Chorvat R. J., Saye J. A., Pierdomenico M. E., Maciag C. M., Logue A. R., Fisher B. N., Rominger D. H. Earl R. A. (1998) Two new potent neurotransmitter release enhancers, 10,10-bis(4-pyridinylmethyl)-9(10H)- anthracenone and 10,10-bis(2-fluoro-4 pyridinylmethyl)-9(10H)-anthracenone: comparison to linopirdine. J. Pharmacol. Exp. Ther. 285, 724 730.