Nimodipine inhibits AP firing in cultured hippocampal neurons predominantly due to block of voltage-dependent potassium channels

General Physiology and Biophysics

Volumn 30, Issue SPECIAL, 2011, Pages

  Caro, Anton ^a   Tarabova, Bohumila ^a,c   Rojo Ruiz, Jonathan ^b   Lacinova, Lubica ^a  

^a INSTITUTE OF MOLECULAR PHYSIOLOGY AND GENETICS   (Slovakia)

^b UNIVERSITY OF TURIN   (Italy)

^c France   (Germany)

Author keywords

Action potential; Calcium current; Hippocampal neurons; Nimodipine; Potassium current

Indexed keywords

CALCIUM; CALCIUM CHANNEL L TYPE; ION; VOLTAGE GATED POTASSIUM CHANNEL; BARIUM; CALCIUM CHANNEL BLOCKING AGENT; NIMODIPINE; POTASSIUM; POTASSIUM CHANNEL BLOCKING AGENT;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CONTROLLED STUDY; DRUG INHIBITION; HIPPOCAMPUS; ION CURRENT; NERVE CELL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; RAT; WHOLE CELL PATCH; ANIMAL; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ELECTRIC CONDUCTIVITY; METABOLISM; NEWBORN; TIME;

MUS; RATTUS;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BARIUM; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC CONDUCTIVITY; HIPPOCAMPUS; NEURONS; NIMODIPINE; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; TIME FACTORS;

EID: 82255177148     PISSN: 02315882     EISSN: 13384325     Source Type: Journal    
DOI: 10.4149/gpb-2011-SI1-44     Document Type: Article

References (42)

1. Azouz R., Jensen M. S., Yaari Y. (1996): Ionic basis of spike afer-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. 492, 211-223 (Pubitemid 26123645)
2. Bauer E. P., Schafe G. E., LeDoux J. E. (2002): NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components offear memory forma-tion in the lateral amygdala. J. Neurosci. 22, 5239-5249 (Pubitemid 37465637)
3. Bett G. C., Morales M. J., Strauss H. C., Rasmusson R. L. (2006): KChIP2b modulates the affinity and use-dependent block of Kv4.3 by nifedipine. Biochem. Biophys. Res. Commun. 340, 1167-1177 doi:10.1016/j.bbrc.2005.12.135 (Pubitemid 43083401)
4. Bliss T. V, Lomo T. (1973): Long-lasting potentiation of synaptic trans-mission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356
5. Campbell L. W., Hao S. Y., Tibault O., Blalock E. M., Landfield P. W. (1996): Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J. Neurosci. 16, 6286-6295 (Pubitemid 26314001)
6. Chen S., Yue C., Yaari Y. (2005): A transitional period of Ca2+-de-pendent spike aferdepolarization and bursting in developing rat CA1 pyramidal cells. J. Physiol. 567, 79-93 doi:10.1113/jphysiol.2005.084590 (Pubitemid 41167307)
7. Deisseroth K., Mermelstein P. G., Xia H., Tsien R. W. (2003): Signal-ing from synapse to nucleus: the logic behind the mechanisms. Curr. Opin. Neurobiol. 13, 354-365 doi:10.1016/S0959-4388(03)00076-X (Pubitemid 36805579)
8. Drigelova M., Tarabova B., Duburs G., Lacinova L. (2009): Te dihy-dropyridine analogue cerebrocrast blocks both T-type and L-type calcium currents. Can. J. Physiol. Pharmacol. 87, 923-932 doi:10.1139/Y09-086
9. Dudek S. M., Fields R. D. (2002): Somatic APs are sufficient for late-phase LTP-related cell signaling. Proc. Nat. Acad. Sci. U. S. A. 99, 3962-3967 doi:10.1073/pnas.062510599 (Pubitemid 34252213)
10. Frey U., Krug M., Reymann K. G, Matthies H. (1988): Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain. Res. 452, 57-65 doi:10.1016/0006- 8993(88)90008-X
11. Gao Z., Sun H., Chiu S. W., Lau C. P., Li G. R. (2005): Effects of diltiazem and nifedipine on transient outward and ultra-rapid delayed rectifierpotassium currents in human atrial myocytes. Br. J. Pharmacol. 144, 595-604 doi:10.1038/sj.bjp.0706113 (Pubitemid 40349467)
12. Grover L. M., Teyler T. J. (1990): Two components of long-term potentiation induced by differentpatterns ofafferent activation. Nature 347, 477-479 doi:10.1038/347477a0 (Pubitemid 20329988)
13. Gu N., Vervaeke K., Hu H., Storm J. F. (2005): Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium afer-hyperpolarization andexcitabilitycontrolin CA1 hippocampal pyramidal cells. J. Physiol. 566, 689-715 doi:10.1113/jphysiol.2005.086835 (Pubitemid 41122655)
14. Gu N., Vervaeke K., Storm J. F. (2007): BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J. Physiol. 580, 859-882 doi:10.1113/jphysiol.2006. 126367 (Pubitemid 46909039)
15. Hell J. W, Westenbroek R. E., Warner C., Ahlijanian M. K., Prystay W, Gilbert M. M., Snutch T. P., Catterall W. A. (1993): Identifi-cation and differential subcellular localization of the neuronal class C and class D L-type calcium channel a1 subunits. J. Cell Biol. 123, 949-962 doi:10.1083/jcb.123.4. 949 (Pubitemid 23333582)
16. Hoffman D. A., Magee J. C., Colbert C. M., Johnston D. (1997): K+ channel regulation of signal propagation in dendrites of hip-pocampal pyramidal neurons. Nature. 387, 869-875 doi:10.1038/42571 (Pubitemid 27289580)
17. Inoue Y., Hisatome I., Tsuboi M., Ahmmed G. U., Yatsuhashi T., Uchida K., Yamanouchi Y., Santo Y., Miake J., Tanaka Y., Hamada T., Watanabe M., Igawa O., Yoshida A., Shigemasa C., Makita N., Sato R. (1999): Effects ofamlodipine on native cardiac Na+ channels and cloned a-subunits of cardiac Na+ channels. Arzneimittelforschung 49, 394-397 (Pubitemid 29242641)
18. Kampa B. M., Letzkus J. J., Stuart G. J. (2006): Requirement of den-dritic calcium spikes for induction of spike-timing-dependent synaptic plasticity J. Physiol. 574, 283-290 doi:10.1113/jphysiol.2006.111062 (Pubitemid 43905812)
19. Kandel E. R. (2009): Te biology ofmemory: a forty-year perspec-tive. J. Neurosci. 29, 12748-12756 doi:10.1523/JNEUROSCI.3958-09.2009
20. Kim S., Yun H. M., Baik J. H., Chung K. C., Nah S. Y., Rhim H. (2007): Functional interaction of neuronal Cav1.3 L-type calcium channel with ryanodine receptor type 2 in the rat hippocampus. J. Biol. Chem. 282, 32877-32889 doi:10.1074/jbc.M701418200 (Pubitemid 350159320)
21. Lacinova L., Klugbauer N., Hofmann F. (2000): Regulation of the calcium channel a1G subunit by divalent cations and organic blockers. Neuropharmacology 39, 1254-1266 doi:10.1016/S0028-3908(99)00202-6 (Pubitemid 30173189)
22. Lacinova L., Moosmang S., Langwieser N., Hofmann F., Kleppisch T. (2008): Cav1.2 calcium channels modulate the spiking pat-tern of hippocampal pyramidal cells. Life Sci. 82, 41-49 doi:10.1016/j.lfs.2007.10.009 (Pubitemid 350251391)
23. Lin S., Wang Z., Fedida D. (2001): Influence of permeatingions on Kv1.5 channel block by nifedipine. Am. J. Physiol. Heart Circ. Physiol. 280, H1160-1172
24. 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 doi:10.1242/jcs.03399 (Pubitemid 46638513)
25. Magee J. C., Carruth M. (1999): Dendritic voltage-gated ion chan-nels regulate the AP firing mode ofhippocampal CA1 pyrami-dal neurons. J. Neurophysiol. 82, 1895-1901 (Pubitemid 29471277)
26. Moosmang S., Haider N., Klugbauer N., Adelsberger H., Langwi-eser N., Muller J., Stiess M., Marais E., Schulla V., Lacinova L., Goebbels S., Nave K. A., Storm D. R., Hofmann F., Kleppisch T. (2005): Role of hippocampal Cav1.2 Ca2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory. J. Neurosci. 25, 9883-9892 doi:10.1523/JNEUROSCI.1531-05.2005 (Pubitemid 41528025)
27. Moyer J. R., Jr., Tompson L. T., Black J. P., Disterhof J. F. (1992): Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J. Neurophysiol. 68, 2100-2109 (Pubitemid 23015511)
28. Moyer J. R., Jr., Disterhof J. F. (1994): Nimodipine decreases calcium APs in rabbit hippocampal CA1 neurons in an age-dependent and concentration-dependent manner. Hippocampus 4, 11-17 doi:10.1002/hipo.450040104 (Pubitemid 24168376)
29. Murphy T. H., Worley P. F., Nakabeppu Y., Christy B., Gastel J., Baraban J. M. (1991): Synaptic regulation of immediate early gene expression in primary cultures of cortical neurons. J. Neurochem. 57, 1862-1872 doi:10.1111/j.1471- 4159.1991.tb06396.x (Pubitemid 21922832)
30. Obermair G. J., Szabo Z., Bourinet E., Flucher B. E. (2004): Differential targeting of the L-type Ca2+ channel alpha 1C (CaV1.2) to synaptic and extrasynaptic compartments in hippocampal neurons. Eur. J. Neurosci. 19, 2109-2122 doi:10.1111/j.0953-816X.2004.03272.x (Pubitemid 38582200)
31. Perez-Reyes E., Van Deusen A. L., Vitko I. (2009): Molecular pharmacology of human Cav3.2 T-type Ca2+ channels: block by antihypertensives, antiarrhythmics, and their analogs. J. Pharmacol. Exp. Ter. 328, 621-627 doi:10.1124/jpet.108.145672
32. Salkoff L., Butler A., Ferreira G., Santi C., Wei A. (2006): High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7, 921-931 doi:10.1038/nrn1992
33. Schlick B., Flucher B. E., Obermair G J. (2010): Voltage-activated calcium channel expression profiles in mouse brain and cultured hippocampal neurons. Neuroscience 167, 786-798 doi:10.1016/j.neuroscience.2010.02.037
34. Sinnegger-Brauns M. J., Hetzenauer A., Huber I. G., Renstrom E., Wietzorrek G., Berjukov S., Cavalli M., Walter D., Koschak A., Waldschutz R., Hering S., Bova S., Rorsman P., Pongs O., Singewald N., Striessnig J. J. (2004): Isoform-specific regula-tion of mood behavior and pancreatic beta cell and cardiovas-cular function by L-type Ca2+ channels. J. Clin. Invest. 113, 1430-1439 (Pubitemid 39071698)
35. Spruston N., Schiller Y., Stuart G., Sakmann B. (1995): Activity-dependent AP invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297-300 doi:10.1126/science.7716524
36. Sun X., Gu X. Q., Haddad G G. (2003): Calcium influxviaL- andN-type calcium channels activates a transient large-conductance Ca2+-activated K+ current in mouse neocortical pyramidal neurons. J. Neurosci. 23, 3639-3648 (Pubitemid 36958472)
37. Tseng-Crank J., Foster C. D., Krause J. D., Mertz R., Godinot N., DiChiara T. J., Reinhart P. H. (1994): Cloning, expression, and distribution of functionally distinct Ca2+-activated K+ channel isoforms from human brain. Neuron 13, 1315-1330 doi:10.1016/0896-6273(94)90418-9
38. Veng L. M., Browning M. D (2002): Regionally selective alterations in expression of the a1D subunit (Cav1.3) of L-type calcium channels in the hippocampus of aged rats. Brain. Res. Mol. Brain Res. 107, 120-127 doi:10.1016/S0169-328X(02)00453-9 (Pubitemid 35335529)
39. West A. E., Chen W. G., Dalva M. B., Dolmetsch R. E., Kornhauser J. M., Shaywitz A. J., Takasu M. A., Tao X., Greenberg M. E. (2001): Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U. S. A. 98, 11024-11031 doi:10.1073/pnas.191352298 (Pubitemid 32928677)
40. Williams M. E., Washburn M. S., Hans M., Urrutia A., Brust P. F., Pro-danovich P., Harpold M. M., Stauderman K. A. (1999): Structure and functional characterization of a novel human low-voltage activated calcium channel. J. Neurochem. 72, 791-799 doi:10.1046/j.1471-4159.1999.0720791.x (Pubitemid 29055245)
41. Yatani A., Brown A. M. (1985): Te calcium channel blocker nitrendipine blocks sodium channels in neonatal rat cardiac myocytes. Circ. Res. 56, 868-875 (Pubitemid 15231510)
42. Zhang X. L., Gold M. S. (2009): Dihydropyridine block of voltage-dependent K+ currents in rat dorsal root ganglion neurons. Neuroscience 161, 184-194 doi:10.1016/j.neuroscience.2009.03.012