Presynaptic R-type calcium channels contribute to fast excitatory synaptic transmission in the rat hippocampus
Open accessAbstract
The possibility that R-type calcium channels contribute to fast glutamatergic transmission in the hippocampus has been assessed using low concentrations of NiCl(2) and the peptide toxin SNX 482, a selective antagonist of the pore-forming alpha(1E) subunit of R-type calcium channel. EPSPs or EPSCs were recorded in the whole-cell configuration of the patch-clamp technique mainly from CA3 hippocampal neurons. Effects of both NiCl(2) and SNX 482 were tested on large (composite) EPSCs evoked by mossy and associative-commissural fiber stimulation. NiCl(2) effects were also tested on minimal EPSPs-EPSCs. Both substances reduced the amplitude of EPSPs-EPSCs. This effect was associated with an increase in the number of response failures of minimal EPSPs-EPSCs, an enhancement of the paired-pulse facilitation ratios of both minimal and composite EPSCs, and a reduction of the inverse squared coefficient of variation (CV(-2)). The reduction of CV(-2) was positively correlated with the decrease in EPSC amplitude. The inhibitory effect of NiCl(2) was occluded by SNX 482 but not by omega-conotoxin-MVIIC, a broad-spectrum antagonist thought to interact with N- and P/Q-type calcium channels, supporting a specific action of low concentrations of NiCl(2) on R-type calcium channels. Together, these observations indicate that both NiCl(2) and SNX 482 act at presynaptic sites and block R-type calcium channels with pharmacological properties similar to those encoded by the alpha(1E) gene. These channels are involved in fast glutamatergic transmission at hippocampal synapses.
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P/Q- and N-type Ca2+ channels are localized to active zones, and the related R-type Ca2+ channel may also be present.
“P/Q- (Cav2.1) and N-type Ca2+ channels (Cav2.2) are localized to active zones, and the related R-type Ca2+ channel (Cav2.3) may also be present (Gasparini et al., 2001; Li et al., 2007).”
From The Presynaptic Active Zone (2012) · cites this paper as Gasparini et al., 2001
The introduction states that N- and P/Q-type channels are localized at presynaptic release sites. The Discussion reports evidence favoring R-type channels on the same nerve endings, but it does not establish that R-type channels are at the active zones specifically; it notes that channels may be more or less close to them. Page numbers were not available in our copy. (LLM, conf=0.84)
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Cites
Co‐operative action of calcium ions in transmitter release at the neuromuscular junction
Dodge, F. A., & Rahamimoff, R. (1967) · The Journal of Physiology · doi:10.1113/jphysiol.1967.sp008367 · Cited by 1,315 · see citing works
The release of neural transmitter substances
Katz, B. (1969) · Medical Entomology and Zoology · Cited by 1,114 · see citing works
Roles of N-Type and Q-Type Ca 2+ Channels in Supporting Hippocampal Synaptic Transmission
Wheeler, D. B., Randall, A. D., & Tsien, R. W. (1994) · Science · doi:10.1126/science.7832825 · Cited by 954 · see citing works
Exocytotic Ca2+ channels in mammalian central neurons
Dunlap, K., Luebke, J. I., & Turner, T. J. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)80030-6 · Cited by 918 · see citing works
Randall, A. D., & Tsien, R. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02995.1995 · Cited by 816 · see citing works
Low-Threshold Calcium Currents in Central Nervous System Neurons
Huguenard, J. R. (1996) · Annual Review of Physiology · doi:10.1146/annurev.ph.58.030196.001553 · Cited by 767 · see citing works
Different types of calcium channels mediate central synaptic transmission
Takahashi, T., & Momiyama, A. (1993) · Nature · doi:10.1038/366156a0 · Cited by 755 · see citing works
Presynaptic inhibition of elicited neurotransmitter release
Wu, L., & Saggau, P. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01015-6 · Cited by 627 · see citing works
Zhang, J.-F., Randall, A. D., Ellinor, P. T., Horne, W. A., Sather, W. A., Tanabe, T., Schwarz, T. L., & Tsien, R. W. (1993) · Neuropharmacology · doi:10.1016/0028-3908(93)90003-l · Cited by 627 · see citing works
Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells.
Oliet, S., Malenka, R., & Nicoll, R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80336-0 · Cited by 600 · see citing works
Magee, J., & Johnston, D. (1995) · Journal of Physiology · doi:10.1113/jphysiol.1995.sp020862 · Cited by 577 · see citing works
Calcium control of transmitter release at a cerebellar synapse.
Mintz, I., Sabatini, B., & Regehr, W. (1995) · Neuron · doi:10.1016/0896-6273(95)90155-8 · Cited by 551 · see citing works
Wu, L., Westenbroek, R. E., Borst, J. G. G., Catterall, W. A., & Sakmann, B. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00726.1999 · Cited by 428 · see citing works
Newcomb, R., Szoke, B. G., Palma, A., Wang, G., Chen, X., Hopkins, W. F., Cong, R., Miller, J., Ürge, L., Tarczy‐Hornoch, K., et al. (1998) · Biochemistry · doi:10.1021/bi981255g · Cited by 396 · see citing works
Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus
Luebke, J. I., Dunlap, K., & Turner, T. J. (1993) · Neuron · doi:10.1016/0896-6273(93)90119-c · Cited by 381 · see citing works
Applicability of the coefficient of variation method for analyzing synaptic plasticity
Faber, D. S., & Korn, H. (1991) · Biophysical Journal · doi:10.1016/s0006-3495(91)82162-2 · Cited by 369 · see citing works
Kamiya, H., Shinozaki, H., & Yamamoto, C. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021395 · Cited by 327 · see citing works
Chavez-Noriega, L., & Stevens, C. F. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-01-00310.1994 · Cited by 300 · see citing works
Castillo, P. E., Weisskopf, M. G., & Nicoll, R. A. (1994) · Neuron · doi:10.1016/0896-6273(94)90269-0 · Cited by 298 · see citing works
Wu, L., & Saggau, P. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00645.1994 · Cited by 294 · see citing works
Exocytotic Ca2+ channels in mammalian central neurons
Dunlap, K. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93882-x · Cited by 294 · see citing works
Magee, J. C., & Carruth, M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.4.1895 · Cited by 293 · see citing works
R-type Ca 2+ currents evoke transmitter release at a rat central synapse
Wu, L., Borst, J. G. G., & Sakmann, B. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4720 · Cited by 277 · see citing works
Christie, B. R., Eliot, L. S., Ito, K., Miyakawa, H., & Johnston, D. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.6.2553 · Cited by 222 · see citing works
Augustine, G. J., & Charlton, M. P. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016347 · Cited by 217 · see citing works
Miledi, R., & Thies, R. E. (1971) · The Journal of Physiology · doi:10.1113/jphysiol.1971.sp009320 · Cited by 216 · see citing works
Gasparini, S., Saviane, C., Voronin, L. L., & Cherubini, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.170032297 · Cited by 187 · see citing works
Self-citationTottene, A., Volsen, S. G., & Pietrobon, D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00171.2000 · Cited by 170 · see citing works
Self-citationFunctional Diversity of P-Type and R-Type Calcium Channels in Rat Cerebellar Neurons
Tottene, A., Moretti, A., & Pietrobon, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06353.1996 · Cited by 164 · see citing works
Self-citationYokoyama, C., Westenbroek, R. E., Hell, J., Soong, T., Snutch, T., & Catterall, W. A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06419.1995 · Cited by 160 · see citing works
Dendritic Ca2+ Channels Characterized by Recordings from Isolated Hippocampal Dendritic Segments
Kavalali, E. T., Zhuo, M., Bito, H., & Tsien, R. W. (1997) · Neuron · doi:10.1016/s0896-6273(00)80305-0 · Cited by 148 · see citing works
The Status of Voltage-Dependent Calcium Channels in α1EKnock-Out Mice
Wilson, S. M., Tóth, P. T., Oh, S. B., Gillard, S. E., Volsen, S. G., Ren, D., Philipson, L. H., Lee, E. C., Fletcher, C., Tessarollo, L., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08566.2000 · Cited by 146 · see citing works
An R-Type Ca2+Current in Neurohypophysial Terminals Preferentially Regulates Oxytocin Secretion
Wang, G., Dayanithi, G., Newcomb, R., & Lémos, J. R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09235.1999 · Cited by 121 · see citing works
Albillos, A., Neher, E., & Moser, T. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08323.2000 · Cited by 110 · see citing works
Craig, P. J., Beattie, R., Folly, E. A., Reeves, M. B., Priestley, J. V., Carney, S. L., Sher, E., Perez‐Reyes, E., & Volsen, S. G. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00711.x · Cited by 82 · see citing works
Day, N. C., Shaw, P. J., McCormack, A. L., Craig, P. J., Smith, W., Beattie, R., Williams, T. L., Ellis, S. B., Ince, P. G., Harpold, M. M., et al. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00514-5 · Cited by 70 · see citing works
Voronin, L. L. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90332-a · Cited by 68 · see citing works
Self-citationThree novel types of voltage-dependent calcium channels in rat cerebellar neurons
Forti, L., Tottene, A., Moretti, A., & Pietrobon, D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05243.1994 · Cited by 58 · see citing works
Self-citationWu, L. G., & Saggau, P. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.5.1965 · Cited by 51 · see citing works
Isoforms of α1E voltage-gated calcium channels in rat cerebellar granule cells
Schramm, M., Vajna, R., Pereverzev, A., Tottene, A., Klöckner, U., Pietrobon, D., Hescheler, J., & Schneider, T. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00013-5 · Cited by 36 · see citing works
Self-citationAntagonists‐resistant calcium currents in rat embryo motoneurons
Magnelli, V., Baldelli, P., & Carbone, E. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00178.x · Cited by 27 · see citing works
Toxin-resistant calcium currents in embryonic mouse sensory neurons
Hilaire, C., Diochot, S., Desmadryl, G., Richard, S., & Valmier, J. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00101-2 · Cited by 23 · see citing works
Berretta, N., Rossokhin, A. V., Kasyanov, A. M., Sokolov, M., Cherubini, E., & Voronin, L. L. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00076-9 · Cited by 22 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Synaptic plasticity at hippocampal mossy fibre synapses
Nicoll, R. A., & Schmitz, D. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1786 · Cited by 653 · see citing works
Localization of Voltage-Gated Ion Channels IN Mammalian Brain
Trimmer, J. S., & Rhodes, K. J. (2004) · Annual Review of Physiology · doi:10.1146/annurev.physiol.66.032102.113328 · Cited by 442 · see citing works
CaV1.3 Channels Are Essential for Development and Presynaptic Activity of Cochlear Inner Hair Cells
Brandt, A., Striessnig, J., & Moser, T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10832.2003 · Cited by 415 · see citing works
Calcium-Permeable Ion Channels in Pain Signaling
Bourinet, E., Altier, C., Hildebrand, M. E., Trang, T., Salter, M. W., & Zamponi, G. W. (2014) · Physiological Reviews · doi:10.1152/physrev.00023.2013 · Cited by 335 · see citing works
Supramolecular Assemblies and Localized Regulation of Voltage-Gated Ion Channels
Dai, S., Hall, D. D., & Hell, J. W. (2009) · Physiological Reviews · doi:10.1152/physrev.00029.2007 · Cited by 330 · see citing works
Ziconotide: a review of its pharmacology and use in the treatment of pain
McGivern, J. G. (2007) · Neuropsychiatric Disease and Treatment · doi:10.2147/nedt.2007.3.1.69 · Cited by 311 · see citing works
Li, L., Bischofberger, J., & Jonas, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1709-07.2007 · Cited by 206 · see citing works
Functional Specialization of Presynaptic Cav2.3 Ca2+ Channels
Dietrich, D., Kirschstein, T., Kukley, M., Pereverzev, A., von der Brelie, C., Schneider, T., & Beck, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00430-6 · Cited by 202 · see citing works
Presynaptic Ca2+ channels: a functional patchwork.
Reid, C., Bekkers, J., & Clements, J. (2003) · Trends in Neurosciences · doi:10.1016/j.tins.2003.10.003 · Cited by 196 · see citing works
Metz, A. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0624-05.2005 · Cited by 182 · see citing works
Timing and Efficacy of Ca2+Channel Activation in Hippocampal Mossy Fiber Boutons
Bischofberger, J., Geiger, J. R. P., & Jónás, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10593.2002 · Cited by 158 · see citing works
Function and dysfunction of synaptic calcium channels: insights from mouse models
Pietrobon, D. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.010 · Cited by 159 · see citing works
Self-citationCalcium Channels and Short-term Synaptic Plasticity
Catterall, W. A., Leal, K., & Nanou, E. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.r112.411645 · Cited by 146 · see citing works
The Role of Neurotrophins in Neurotransmitter Release
Tyler, W. J., Perrett, S. P., & Pozzo‐Miller, L. D. (2002) · The Neuroscientist · doi:10.1177/1073858402238511 · Cited by 140 · see citing works
Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network
Bischofberger, J., Engel, D., Frotscher, M., & Jónás, P. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0093-2 · Cited by 117 · see citing works
α 1E -Containing Ca 2+ channels are involved in synaptic plasticity
Breustedt, J., Vogt, K. E., Miller, R. J., Nicoll, R. A., & Schmitz, D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2035117100 · Cited by 113 · see citing works
Striessnig, J., & Koschak, A. (2008) · Channels · doi:10.4161/chan.2.4.5847 · Cited by 100 · see citing works
Matthews, E. A., Bee, L., Stephens, G. J., & Dickenson, A. H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05605.x · Cited by 88 · see citing works
Parajuli, L. K., Nakajima, C., Kulik, Á., Matsui, K., Schneider, T., Shigemoto, R., & Fukazawa, Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1142-12.2012 · Cited by 79 · see citing works
Gundlfinger, A., Bischofberger, J., Johenning, F. W., Torvinen, M., Schmitz, D., & Breustedt, J. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.132613 · Cited by 77 · see citing works
Tigaret, C. M., Olivo, V., Sadowski, J. H. L. P., Ashby, M. C., & Mellor, J. R. (2016) · Nature Communications · doi:10.1038/ncomms10289 · Cited by 78 · see citing works
The Cellular Building Blocks of Breathing
Ramirez, J., Doi, A., Garcia, A. J., Elsen, F. P., Koch, H., & Wei, A. D. (2012) · Comprehensive physiology · doi:10.1002/cphy.c110033 · Cited by 76 · see citing works
Control of low-threshold exocytosis by T-type calcium channels
Weiss, N., & Zamponi, G. W. (2012) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2012.07.031 · Cited by 65 · see citing works
T-type channel-mediated neurotransmitter release
Carbone, E., Calorio, C., & Vandael, D. H. F. (2014) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1489-z · Cited by 62 · see citing works
Daniel, H., Rancillac, A., & Crépel, F. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063263 · Cited by 62 · see citing works
Straface, E., Matarrese, P., Gambardella, L., Vona, R., Sgadari, A., Silveri, M. C., & Malorni, W. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.03.094 · Cited by 58 · see citing works
Wang, K., Lin, M. T., Adelman, J. P., & Maylie, J. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.004 · Cited by 57 · see citing works
Calcium channel blockers in the treatment of disease
Elmslie, K. S. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.10872 · Cited by 57 · see citing works
Myoga, M. H., & Regehr, W. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5252-10.2011 · Cited by 56 · see citing works
Kamp, M. A., Krieger, A., Henry, M., Hescheler, J., Weiergräber, M., & Schneider, T. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03984.x · Cited by 47 · see citing works
Page, A. J., O’Donnell, T. A., & Blackshaw, L. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.09.016 · Cited by 46 · see citing works
Structure, biophysics, and circuit function of a “giant” cortical presynaptic terminal
Vandael, D., & Jonas, P. (2024) · Science · doi:10.1126/science.adg6757 · Cited by 45 · see citing works
Berecki, G., McArthur, J. R., Cuny, H., Clark, R. J., & Adams, D. J. (2014) · The Journal of General Physiology · doi:10.1085/jgp.201311104 · Cited by 44 · see citing works
Mori, Y. (2002) · Trends in Cardiovascular Medicine · doi:10.1016/s1050-1738(02)00173-1 · Cited by 42 · see citing works
Berrou, L., Klein, H., Bernatchez, G., & Parent, L. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)73914-3 · Cited by 41 · see citing works
Melatonin inhibits voltage-sensitive Ca2+ channel-mediated neurotransmitter release
Choi, T.-Y., Kwon, J., Durrance, E. S., Jo, S., Choi, S., & Kim, K. (2014) · Brain Research · doi:10.1016/j.brainres.2014.02.023 · Cited by 39 · see citing works
Wang, S., Polo‐Parada, L., & Landmesser, L. T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3809-09.2009 · Cited by 39 · see citing works
Long, P., Mercer, A., Begum, R., Stephens, G. J., Sihra, T. S., & Jovanovic, J. N. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m805322200 · Cited by 38 · see citing works
Cohen, R., & Atlas, D. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.027 · Cited by 37 · see citing works
Differential Modulation of CaV2.3 Ca2+ Channels by Gαq/11-Coupled Muscarinic Receptors
Bannister, R. A., Melliti, K., & Adams, B. (2004) · Molecular Pharmacology · doi:10.1124/mol.65.2.381 · Cited by 36 · see citing works
van de Bovenkamp‐Janssen, M. C., Scheenen, W. J. J. M., Kuijpers, F. J., Kozicz, T., Veening, J. G., van Luijtelaar, E. L. J. M., McEnery, M. W., & Roubos, E. W. (2004) · Journal of Neurobiology · doi:10.1002/neu.10291 · Cited by 36 · see citing works
Coincidence detection of convergent perforant path and mossy fibre inputs by CA3 interneurons
Calixto, E., Galván, E. J., Card, J. P., & Barrionuevo, G. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.152751 · Cited by 34 · see citing works
Shcheglovitov, A., Vitko, I., Lazarenko, R. M., Orestes, P., Todorovic, S. M., & Perez‐Reyes, E. (2012) · The Journal of General Physiology · doi:10.1085/jgp.201110699 · Cited by 35 · see citing works
Boscia, F., Elkjaer, M. L., Illés, Z., & Kukley, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.685703 · Cited by 33 · see citing works
Joksovic, P. M., Weiergräber, M., Lee, W., Struck, H., Schneider, T., & Todorovic, S. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5574-08.2009 · Cited by 34 · see citing works
Regulation of Voltage-Gated Calcium Channels by Synaptic Proteins
Weiss, N., & Zamponi, G. W. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-2888-2_33 · Cited by 32 · see citing works
Voltage-gated calcium channels: Determinants of channel function and modulation by inorganic cations
Neumaier, F., Dibué, M., Hescheler, J., & Schneider, T. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.12.003 · Cited by 31 · see citing works
Sarihi, A., Mirnajafi‐Zadeh, J., Jiang, B., Sohya, K., Safari, M.-S., Kourosh‐Arami, M., Yanagawa, Y., & Tsumoto, T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1386-12.2012 · Cited by 31 · see citing works
Scheuber, A., Miles, R., & Poncer, J. C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1664-04.2004 · Cited by 30 · see citing works
Shcheglovitov, A., Vitko, I., Lazarenko, R. M., Orestes, P., Todorovic, S. M., & Perez‐Reyes, E. (2012) · The Journal of General Physiology · doi:10.1085/jgp.2011106991395c · Cited by 29 · see citing works
Kohlmeier, K. A., & Leonard, C. S. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04640.x · Cited by 27 · see citing works
Tokunaga, T., Miyazaki, K.-I., Koseki, M., Mobarakeh, J. I., Ishizuka, T., & Yawo, H. (2004) · Hippocampus · doi:10.1002/hipo.10202 · Cited by 25 · see citing works
A System for Performing High Throughput Assays of Synaptic Function
Hempel, C., Sivula, M., Levenson, J., Rose, D. M., Li, B., Sirianni, A., Xia, E., Ryan, T. A., Gerber, D., & Cottrell, J. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025999 · Cited by 27 · see citing works
R-type calcium channels in myenteric neurons of guinea pig small intestine
Bian, X., Zhou, X., & Galligan, J. J. (2004) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00532.2003 · Cited by 25 · see citing works
Distinct roles for Cav2.1–2.3 in activity-dependent synaptic dynamics
Ricoy, U. M., & Frerking, M. E. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00335.2013 · Cited by 22 · see citing works
Suzuki, E., & Okada, T. (2008) · Brain Research · doi:10.1016/j.brainres.2008.09.101 · Cited by 21 · see citing works
Meza, U., Thapliyal, A., Bannister, R. A., & Adams, B. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.028530 · Cited by 21 · see citing works
Ramachandran, S., Rodgriguez, S., Potcoava, M. C., & Alford, S. T. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2207-21.2022 · Cited by 19 · see citing works
Nanou, E., Jin, Y., Whitehead, N. P., Kim, M. J., Froehner, S. C., Scheuer, T., & Catterall, W. A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1524650113 · Cited by 19 · see citing works
Dynamic Modulation of Phasic and Asynchronous Glutamate Release in Hippocampal Synapses
Chang, C. Y., & Mennerick, S. J. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00683.2009 · Cited by 19 · see citing works
Kang, S. J., Liu, M., Shi, T., Zhao, M., Kaang, B., & Zhuo, M. (2013) · Molecular Pain · doi:10.1186/1744-8069-9-58 · Cited by 18 · see citing works
Old proteins, developing roles: The regulation of calcium channels by synaptic proteins
Davies, J. N., & Zamponi, G. W. (2008) · Channels · doi:10.4161/chan.2.2.6214 · Cited by 17 · see citing works
Suzuki, E., & Okada, T. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.06.1472 · Cited by 16 · see citing works
How “Pharmacoresistant” is Cav2.3, the Major Component of Voltage-Gated R-type Ca2+ Channels?
Schneider, T., Dibué, M., & Hescheler, J. (2013) · Pharmaceuticals · doi:10.3390/ph6060759 · Cited by 17 · see citing works
Calcium control of gene regulation in rat hippocampal neuronal cultures
Pinato, G., Pegoraro, S., Iacono, G. L., Ruaro, M. E., & Torre, V. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21820 · Cited by 14 · see citing works
Jackson, R. E., & Burrone, J. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00021 · Cited by 14 · see citing works
Woodhall, G. L., Ayman, G., & Jones, R. S. G. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.06.002 · Cited by 14 · see citing works
Naidoo, V., Dai, X., & Galligan, J. J. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01596.x · Cited by 12 · see citing works
“Resistant” Channels Reluctantly Reveal Their Roles
Brenowitz, S. D., & Regehr, W. G. (2003) · Neuron · doi:10.1016/s0896-6273(03)00470-7 · Cited by 12 · see citing works
Ohura, S., & Kamiya, H. (2018) · eNeuro · doi:10.1523/eneuro.0254-18.2018 · Cited by 11 · see citing works
Reciprocal modulation of Cav2.3 voltage‐gated calcium channels by copper( II ) ions and kainic acid
Neumaier, F., Akhtar‐Schäfer, I., Lüke, J. N., Dibué, M., Hescheler, J., & Schneider, T. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14546 · Cited by 10 · see citing works
Shin, M.-C., Nonaka, K., Yamaga, T., Wakita, M., Akaike, H., & Akaike, N. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00571.2017 · Cited by 10 · see citing works
Frolov, R., & Weckström, M. (2016) · Advances in Protein Chemistry and Structural Biology · doi:10.1016/bs.apcsb.2015.11.001 · Cited by 8 · see citing works
Zn2+-induced changes in Cav2.3 channel function: An electrophysiological and modeling study
Neumaier, F., Alpdogan, S., Hescheler, J., & Schneider, T. (2020) · The Journal of General Physiology · doi:10.1085/jgp.202012585 · Cited by 9 · see citing works
P- and R-type Ca2+ channels regulating spinal glycinergic nerve terminals
Nonaka, K., Murayama, N., Maeda, M., Shoudai, K., Shin, M.-C., & Akaike, N. (2010) · Toxicon · doi:10.1016/j.toxicon.2010.01.020 · Cited by 8 · see citing works
Muscarinic modulation of Cav2.3 (R-type) calcium channels is antagonized by RGS3 and RGS3T
Toro-Castillo, C., Thapliyal, A., González-Ochoa, H. O., Adams, B., & Meza, U. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00219.2006 · Cited by 8 · see citing works
Rajagopal, S., Burton, B. K., Fields, B. L., El, I. O., & Kamatchi, G. L. (2017) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2017.04.002 · Cited by 8 · see citing works
Neumaier, F., Schneider, T., & Albanna, W. (2020) · Channels · doi:10.1080/19336950.2020.1829842 · Cited by 8 · see citing works
Yamazaki, K., Shigetomi, E., Ikeda, R., Nishida, M., Kiyonaka, S., Mori, Y., & Kato, F. (2006) · Brain Research · doi:10.1016/j.brainres.2006.05.077 · Cited by 7 · see citing works
Vesicular release of glutamate utilizes the proton gradient between the vesicle and synaptic cleft
Brown, J. T. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00015 · Cited by 7 · see citing works
Salvador‐Recatalà, V., & Greenberg, R. M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.144725 · Cited by 6 · see citing works
Rodriguez‐Tapia, E., Naidoo, V., DeVries, M., Perez-Medina, A. L., & Galligan, J. J. (2016) · Experimental Physiology · doi:10.1113/ep086027 · Cited by 6 · see citing works
The Cellular Building Blocks of Breathing
Ramirez, J., Doi, A., Garcia, A. J., Elsen, F. P., Koch, H., & Wei, A. D. (2012) · Comprehensive physiology · doi:10.1002/j.2040-4603.2012.tb00469.x · Cited by 6 · see citing works
Calcium channel blockers and calcium channels
Ertel, E. A., & Godfraind, T. (2004) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-7859-3_2 · Cited by 5 · see citing works
Jackson, R. E., Compans, B., & Burrone, J. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.830583 · Cited by 4 · see citing works
Lundt, A., Soós, J., Seidel, R., Henseler, C., Müller, R., Ginde, V. R., Arshaad, M. I., Ehninger, D., Hescheler, J., Sachinidis, A., et al. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14591 · Cited by 4 · see citing works
Moravčíková, L., Moravčík, R., Ježová, D., Lacinová, Ľ., & Dremencov, E. (2020) · Pharmacological Reports · doi:10.1007/s43440-020-00183-2 · Cited by 4 · see citing works
Castro, A., Andrade, A., Vergara, P., Segovia, J., Aguilar, J., Felix, R., & Delgado‐Lezama, R. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.21952 · Cited by 4 · see citing works
Striessnig, J., & Koschak, A. (2007) · Springer eBooks · doi:10.1007/0-387-27526-6_23 · Cited by 4 · see citing works
Voltage-Gated Calcium Channels
Zamponi, G. W., Gandini, M. A., & Snutch, T. P. (2019) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190860509.013.7 · Cited by 3 · see citing works
High-Voltage-Activated Calcium Channels in Epilepsy
Rossignol, E. (2024) · Oxford University Press eBooks · doi:10.1093/med/9780197549469.003.0046 · Cited by 3 · see citing works
Characterization of excitatory synaptic transmission in the retrosplenial cortex of adult mice
Wan, J., Ma, Y., Chen, X., Tao, W., Hao, S., Geng, W., Wu, Y., & Zhuo, M. (2025) · Molecular Pain · doi:10.1177/17448069251335500 · Cited by 2 · see citing works
Disruption of Ca V 2.3 channels in the brain of the 5xFAD mice
Aguado, C., Alfaro‐Ruiz, R., Martín‐Belmonte, A., Puertas‐Avendaño, R., Fernández, M., Martínez-Poyato, M. L., Portero-Campillo, E., Pozuelo-Montero, M., Moreno‐Martínez, A. E., Alonso-Gómez, P., et al. (2025) · Journal of Alzheimer s Disease · doi:10.1177/13872877251396963 · Cited by 2 · see citing works
Splicing and Editing to Fine-Tune Activity of High Voltage-Activated Calcium Channels
Huang, H. Y., Hu, Z., Yeow, S. Q. Z., & Soong, T. W. (2022) · Springer eBooks · doi:10.1007/978-3-031-08881-0_3 · Cited by 2 · see citing works
Reciprocal Regulation of Neuronal Calcium Channels by Synaptic Proteins
Weiss, N., & Zamponi, G. W. (2013) · Springer eBooks · doi:10.1007/978-94-007-6334-0_3 · Cited by 2 · see citing works
McGivern, J. G., & Worley, J. F. (2007) · Elsevier eBooks · doi:10.1016/b0-08-045044-x/00066-3 · Cited by 2 · see citing works
Murphy, J. G., Gutzmann, J. J., Lin, L., Hu, J., Petralia, R. S., Wang, Y., & Hoffman, D. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2021.110264 · Cited by 1 · see citing works
Mover affects a subpool of primed synaptic vesicles in the mouse calyx of Held
Pofantis, H. (2019) · doi:10.53846/goediss-7598 · Cited by 1 · see citing works
Ramachandran, S., Rodgriguez, S., Potcoava, M., & Alford, S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.02.429388 · Cited by 1 · see citing works
- Authors
- Gasparini, S., Kasyanov, A. M., Pietrobon, D., Voronin, L. L., & Cherubini, E.
- Affiliations
- Scuola Internazionale Superiore di Studi Avanzati (IT)
- University of Padua (IT)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-11-15
- Volume
- 21
- Issue
- 22
- Pages
- 8715-8721
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762258
- OpenAlex
- W2152544375
- Cited by
- 114
- References
- 43
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2022: 5 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 2 · 2016: 4 · 2015: 2 · 2014: 7 · 2013: 4 · 2012: 10
- FWCI
- 2.46
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- SDL (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- R-type calcium channels, presynaptic calcium channels, hippocampus, CA3 neurons, EPSC, EPSPS, nickel chloride, SNX-482, alpha1E subunit, paired-pulse facilitation, synaptic variability, mossy fibers, omega-conotoxin MVIIC
- MeSH terms
- Animals, Calcium Channel Blockers, Hippocampus, Synaptic Transmission, Neurons, Nickel, Spider Venoms, Rats, Wistar, Presynaptic Terminals, Mossy Fibers, Hippocampal, Excitatory Postsynaptic Potentials, Calcium Channels, R-Type, Rats, In Vitro Techniques
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