Nanosecond Electric Pulses: A Novel Stimulus for Triggering Ca2+ Influx into Chromaffin Cells Via Voltage-Gated Ca2+ Channels
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Exposing bovine chromaffin cells to a single 5 ns, high-voltage (5 MV/m) electric pulse stimulates Ca(2+) entry into the cells via L-type voltage-gated Ca(2+) channels (VGCC), resulting in the release of catecholamine. In this study, fluorescence imaging was used to monitor nanosecond pulse-induced effects on intracellular Ca(2+) level ([Ca(2+)](i)) to investigate the contribution of other types of VGCCs expressed in these cells in mediating Ca(2+) entry. ω-Conotoxin GVIA and ω-agatoxin IVA, antagonists of N-type and P/Q-type VGCCs, respectively, reduced the magnitude of the rise in [Ca(2+)](i) elicited by a 5 ns pulse. ω-conotoxin MVIIC, which blocks N- and P/Q-type VGCCs, had a similar effect. Blocking L-, N-, and P\Q-type channels simultaneously with a cocktail of VGCC inhibitors abolished the pulse-induced [Ca(2+)](i) response of the cells, suggesting Ca(2+) influx occurs only via VGCCs. Lowering extracellular K(+) concentration from 5 to 2 mM or pulsing cells in Na(+)-free medium suppressed the pulse-induced rise in [Ca(2+)](i) in the majority of cells. Thus, both membrane potential and Na(+) entry appear to play a role in the mechanism by which nanoelectropulses evoke Ca(2+) influx. However, activation of voltage-gated Na(+) channels (VGSC) is not involved since tetrodotoxin (TTX) failed to block the pulse-induced rise in [Ca(2+)](i). These findings demonstrate that a single electric pulse of only 5 ns duration serves as a novel stimulus to open multiple types of VGCCs in chromaffin cells in a manner involving Na(+) transport across the plasma membrane. Whether Na(+) transport occurs via non-selective cation channels and/or through lipid nanopores remains to be determined.
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After the first threshold is surpassed, the Vm depolarizes the membrane sufficiently to trigger the formation of aqueous pores and stimulate other voltage-dependent processes such as ion channel activation and cytoskeletal disruption.
“After the first threshold is surpassed, it is thought that the Vm depolarizes the membrane sufficiently to trigger the formation of aqueous pores and stimulate other voltage-dependent processes such as ion channel activation and cytoskeletal disruption [62,65].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [65]
5-ns duration, high-intensity (50,000 V/cm) electric pulses were sufficient to open up the L-type Cav2+ channels, resulting in detectable calcium influx.
“This study concluded that 5-ns duration, high-intensity (50,000 V/cm) electric pulses were sufficient to open up the L-type Cav2+ channels, resulting in detectable calcium influx [65].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [65]
Ion channel activation and ion influx, and perhaps other effects such as cytoskeleton damage, can be used as biomarkers of responsiveness to TTFields.
“The results from electroporation studies further support that ion channel activation and ion influx, and perhaps other effects such as cytoskeleton damage, can be used as biomarkers of responsiveness to TTFields, given that these phenomena are observed after exposure to electric fields [27,46,62,65].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [65]
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Cites
Ion Channels/Excitable Membranes
(2011) · Springer eBooks · doi:10.1007/springerreference_33998 · Cited by 4,066 · see citing works
A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine
Fenwick, E. M., Marty, A., & Neher, E. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014393 · Cited by 812 · see citing works
Intracellular effect of ultrashort electrical pulses
Schoenbach, K. H., Beebe, S. J., & Buescher, E. S. (2001) · Bioelectromagnetics · doi:10.1002/bem.71 · Cited by 548 · see citing works
Chang, D. C., & Reese, T. S. (1990) · Biophysical Journal · doi:10.1016/s0006-3495(90)82348-1 · Cited by 524 · see citing works
Membrane Electroporation: A Molecular Dynamics Simulation
Tarek, M. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.050617 · Cited by 516 · see citing works
The molecular basis of electroporation
Tieleman, D. P. (2004) · BMC Biochemistry · doi:10.1186/1471-2091-5-10 · Cited by 440 · see citing works
Calcium bursts induced by nanosecond electric pulses
Vernier, P. T., Sun, Y. H., Marcu, L., Salemi, S., Craft, C. M., & Gundersen, M. A. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.08.140 · Cited by 400 · see citing works
Self-citationCalcium signaling and exocytosis in adrenal chromaffin cells
García, A. G., García-De-Diego, A. M., Gandía, L., Borges, R., & García-Sancho, J. (2006) · Physiological Reviews · doi:10.1152/physrev.00039.2005 · Cited by 349 · see citing works
Nanoelectropulse-driven membrane perturbation and small molecule permeabilization
Vernier, P. T., Sun, Y. H., & Gundersen, M. A. (2006) · BMC Cell Biology · doi:10.1186/1471-2121-7-37 · Cited by 320 · see citing works
Self-citationPakhomov, A. G., Kolb, J. F., White, J. A., Joshi, R. P., Xiao, S. H., & Schoenbach, K. H. (2007) · Bioelectromagnetics · doi:10.1002/bem.20354 · Cited by 294 · see citing works
Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane
Pakhomov, A. G., Bowman, A. M., Ibey, B. L., André, F. M., Pakhomova, O. N., & Schoenbach, K. H. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.05.035 · Cited by 289 · see citing works
Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells
Artalejo, C. R., Adams, M. E., & Fox, A. P. (1994) · Nature · doi:10.1038/367072a0 · Cited by 270 · see citing works
Stimulation of Capacitative Calcium Entry in HL-60 Cells by Nanosecond Pulsed Electric Fields
White, J. A., Blackmore, P. F., Schoenbach, K. H., & Beebe, S. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311135200 · Cited by 245 · see citing works
Plasma Membrane Voltage Changes during Nanosecond Pulsed Electric Field Exposure
Frey, W., White, J. A., Price, R. O., Blackmore, P. F., Joshi, R. P., Nuccitelli, R., Beebe, S. J., Schoenbach, K. H., & Kolb, J. F. (2006) · Biophysical Journal · doi:10.1529/biophysj.105.072777 · Cited by 242 · see citing works
Levine, Z. A., & Vernier, P. T. (2010) · The Journal of Membrane Biology · doi:10.1007/s00232-010-9277-y · Cited by 232 · see citing works
Self-citationMembrane permeabilization and cell damage by ultrashort electric field shocks
Pakhomov, A. G., Shevin, R. S., White, J. A., Kolb, J. F., Pakhomova, O. N., Joshi, R. P., & Schoenbach, K. H. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.05.003 · Cited by 197 · see citing works
Bovine adrenal chromaffin cells: high-yield purification and viability in suspension culture
Waymire, J. C., Bennett, W. F., Boehme, R. E., Hankins, L. L., Waymire, K. G., & Haycock, J. W. (1983) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(83)90026-2 · Cited by 178 · see citing works
Tekle, E., Oubrahim, H., Dzekunov, S. M., Kolb, J. F., Schoenbach, K. H., & Chock, P. B. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.054494 · Cited by 139 · see citing works
Nanosecond electric pulse-induced calcium entry into chromaffin cells
Vernier, P. T., Sun, Y. H., Chen, M.-T., Gundersen, M. A., & Craviso, G. L. (2008) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2008.02.003 · Cited by 104 · see citing works
Self-citationElectropermeabilization of endocytotic vesicles in B16 F1 mouse melanoma cells
Napotnik, T. B., Reberšek, M., Kotnik, T., Lebrasseur, É., Cabodevila, G., & Damijan Miklavčič, A. (2010) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-010-0599-9 · Cited by 67 · see citing works
Electrical activity in chromaffin cells of intact mouse adrenal gland.
Nassar-Gentina, V., Pollard, H. B., & Rojas, E. (1988) · American Journal of Physiology · doi:10.1152/ajpcell.1988.254.5.c675 · Cited by 67 · see citing works
Albillos, A., Garcı́a, A. G., Olivera, B. M., & Gandı́a, L. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050231 · Cited by 66 · see citing works
Calcium dynamics in bovine adrenal medulla chromaffin cell secretory granules
Domingo, J. S., Vay, L., Camacho, M., Hernández‐SanMiguel, E., Fonteríz, R. I., Lobatón, C. D., Montero, M., Moreno, A., & Álvarez, J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06440.x · Cited by 58 · see citing works
López, M. G., Artalejo, A. R., Garcı́a, A. G., Neher, E., & Garcı́a-Sancho, J. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020496 · Cited by 52 · see citing works
Craviso, G. L., Chatterjee, P., Maalouf, G., Cerjanic, A. M., Yoon, J., Chatterjee, I., & Vernier, P. T. (2009) · IEEE Transactions on Dielectrics and Electrical Insulation · doi:10.1109/tdei.2009.5293941 · Cited by 46 · see citing works
Self-citationNanosecond pulse Generator using fast recovery diodes for cell electromanipulation
Kuthi, A., Gabrielsson, P., Behrend, M. R., Vernier, P. T., & Gundersen, M. A. (2005) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2005.852403 · Cited by 45 · see citing works
Self-citationFriedman, J. E., Lelkes, P. I., Lavie, E., Rosenheck, K., Schneeweiss, F. H. A., & Schneider, R. S. (1985) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1985.tb08775.x · Cited by 35 · see citing works
Mapping membrane-potential perturbations of chromaffin cells exposed to electric fields
Hassan, N., Chatterjee, I., Publicover, N. G., & Craviso, G. L. (2002) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2002.804210 · Cited by 27 · see citing works
Self-citationCraviso, G. L. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.02.031 · Cited by 24 · see citing works
Self-citationGarcı́a-Sancho, J., & Verkhratsky, A. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01812.x · Cited by 23 · see citing works
O'Farrell, M., & Marley, P. D. (1999) · Cell Calcium · doi:10.1054/ceca.1999.0025 · Cited by 20 · see citing works
Cheek, T. R., & Thorn, P. (2006) · Cell Calcium · doi:10.1016/j.ceca.2006.04.002 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Membrane Electroporation and Electropermeabilization: Mechanisms and Models
Kotnik, T., Rems, L., Tarek, M., & Miklavčič, D. (2019) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-052118-115451 · Cited by 813 · see citing works
Pall, M. L. (2013) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12088 · Cited by 440 · see citing works
Napotnik, T. B., Reberšek, M., Vernier, P. T., Mali, B. Č., & Damijan Miklavčič, A. (2016) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2016.02.011 · Cited by 195 · see citing works
Self-citationOxidative effects of nanosecond pulsed electric field exposure in cells and cell-free media
Pakhomova, O. N., Алексеевна, Х. В., Bowman, A. M., Rodaitė‐Riševičienė, R., Saulis, G., Xiao, S. H., & Pakhomov, A. G. (2012) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2012.08.004 · Cited by 189 · see citing works
In vitro electroporation detection methods – An overview
Napotnik, T. B., & Damijan Miklavčič, A. (2017) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2017.12.005 · Cited by 189 · see citing works
Primary pathways of intracellular Ca2+ mobilization by nanosecond pulsed electric field
Semenov, I., Xiao, S. H., & Pakhomov, A. G. (2012) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2012.11.032 · Cited by 166 · see citing works
Cancellation of cellular responses to nanoelectroporation by reversing the stimulus polarity
Pakhomov, A. G., Semenov, I., Xiao, S. H., Pakhomova, O. N., Gregory, B. W., Schoenbach, K. H., Cantu, J. C., Beier, H. T., Rajulapati, S. R., & Ibey, B. L. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1626-z · Cited by 133 · see citing works
Calcium-mediated pore expansion and cell death following nanoelectroporation
Pakhomova, O. N., Gregory, B. W., Semenov, I., & Pakhomov, A. G. (2014) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2014.06.015 · Cited by 107 · see citing works
Pulsed Electric Fields Can Create Pores in the Voltage Sensors of Voltage-Gated Ion Channels
Rems, L., Kasimova, M. A., Testa, I., & Delemotte, L. (2020) · Biophysical Journal · doi:10.1016/j.bpj.2020.05.030 · Cited by 96 · see citing works
Hanna, H., Denzi, A., Liberti, M., André, F. M., & Mir, L. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-12960-w · Cited by 86 · see citing works
Cell stimulation and calcium mobilization by picosecond electric pulses
Semenov, I., Xiao, S. H., Kang, D., Schoenbach, K. H., & Pakhomov, A. G. (2015) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2015.05.013 · Cited by 82 · see citing works
Pakhomov, A. G., Xiao, S. H., Pakhomova, O. N., Semenov, I., Kuipers, M. A., & Ibey, B. L. (2014) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2014.01.004 · Cited by 80 · see citing works
Permeabilizing Cell Membranes with Electric Fields
Aguilar, A. A., Ho, M. C., Chang, E., Carlson, K. W., Natarajan, A., Marciano, T., Bomzon, Z., & Patel, C. B. (2021) · Cancers · doi:10.3390/cancers13092283 · Cited by 76 · see citing works
Gianulis, E. C., Chantelle, L., Saulis, G., Novickij, V., Pakhomova, O. N., & Pakhomov, A. G. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2434-4 · Cited by 75 · see citing works
Nanosecond Pulsed Electric Field (nsPEF): Opening the Biotechnological Pandora’s Box
Ruiz-Fernández, A. R., Campos, L., Gutiérrez-Maldonado, S. E., Núñez, G., Villanelo, F., & Pérez‐Acle, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116158 · Cited by 74 · see citing works
Gianulis, E. C., Lee, J., Jiang, C., Xiao, S. H., Ibey, B. L., & Pakhomov, A. G. (2015) · Scientific Reports · doi:10.1038/srep13818 · Cited by 72 · see citing works
Pakhomov, A. G., Semenov, I., Casciola, M., & Xiao, S. H. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.04.016 · Cited by 68 · see citing works
Rossi, A., Pakhomova, O. N., Mollica, P. A., Casciola, M., Mangalanathan, U. M., Pakhomov, A. G., & Muratori, C. (2019) · Cancers · doi:10.3390/cancers11122034 · Cited by 68 · see citing works
Beier, H. T., & Ibey, B. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084614 · Cited by 66 · see citing works
Novel Passive Element Circuits for Microdosimetry of Nanosecond Pulsed Electric Fields
Merla, C., Denzi, A., Paffi, A., Casciola, M., d'Inzeo, G., Apollonio, F., & Liberti, M. (2012) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2012.2203133 · Cited by 66 · see citing works
Activation of intracellular phosphoinositide signaling after a single 600 nanosecond electric pulse
Tolstykh, G. P., Beier, H. T., Roth, C. C., Thompson, G. L., Payne, J. A., Kuipers, M. A., & Ibey, B. L. (2013) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2013.05.002 · Cited by 66 · see citing works
Burke, R. C., Bardet, S. M., Carr, L., Romanenko, S., Arnaud-Cormos, D., Leveque, P., & O'Connor, R. P. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.07.004 · Cited by 58 · see citing works
The interplay of excitation and electroporation in nanosecond pulse stimulation
Pakhomov, A. G., & Pakhomova, O. N. (2020) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2020.107598 · Cited by 58 · see citing works
Nanosecond pulsed electric field thresholds for nanopore formation in neural cells
Roth, C. C., Tolstykh, G. P., Payne, J. A., Kuipers, M. A., Thompson, G. L., DeSilva, M., & Ibey, B. L. (2013) · Journal of Biomedical Optics · doi:10.1117/1.jbo.18.3.035005 · Cited by 57 · see citing works
Damage-free peripheral nerve stimulation by 12-ns pulsed electric field
Casciola, M., Xiao, S. H., & Pakhomov, A. G. (2017) · Scientific Reports · doi:10.1038/s41598-017-10282-5 · Cited by 57 · see citing works
Mechanisms and immunogenicity of nsPEF-induced cell death in B16F10 melanoma tumors
Rossi, A., Pakhomova, O. N., Pakhomov, A. G., Weygandt, S., Bulysheva, A. A., Murray, L., Mollica, P. A., & Muratori, C. (2019) · Scientific Reports · doi:10.1038/s41598-018-36527-5 · Cited by 56 · see citing works
Resolving the spatial kinetics of electric pulse-induced ion release
Beier, H. T., Roth, C. C., Tolstykh, G. P., & Ibey, B. L. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.06.055 · Cited by 54 · see citing works
Excitation and injury of adult ventricular cardiomyocytes by nano- to millisecond electric shocks
Semenov, I., Grigoryev, S., Neuber, J., Zemlin, C. W., Pakhomova, O. N., Casciola, M., & Pakhomov, A. G. (2018) · Scientific Reports · doi:10.1038/s41598-018-26521-2 · Cited by 53 · see citing works
Modulation of intracellular Ca2+ levels in chromaffin cells by nanoelectropulses
Craviso, G. L., Choe, S., Chatterjee, I., & Vernier, P. T. (2011) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2011.11.016 · Cited by 52 · see citing works
Self-citationGianulis, E. C., Casciola, M., Xiao, S. H., Pakhomova, O. N., & Pakhomov, A. G. (2017) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2017.08.005 · Cited by 50 · see citing works
Hristov, K., Mangalanathan, U. M., Casciola, M., Pakhomova, O. N., & Pakhomov, A. G. (2018) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2018.08.017 · Cited by 48 · see citing works
Vernier, P. T., Levine, Z. A., Ho, M.-C., Xiao, S. H., Semenov, I., & Pakhomov, A. G. (2015) · The Journal of Membrane Biology · doi:10.1007/s00232-015-9788-7 · Cited by 47 · see citing works
Self-citationCichoń, N., Czarny, P. L., Bijak, M., Miller, E. D., Śliwiński, T., Szemraj, J., & Saluk, J. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/2181942 · Cited by 46 · see citing works
Coupling of pulsed electromagnetic fields (PEMF) therapy to molecular grounds of the cell.
Funk, R. H. W. (2018) · Europe PMC (PubMed Central) · Cited by 44 · see citing works
Excitation of murine cardiac myocytes by nanosecond pulsed electric field
Azarov, J. E., Semenov, I., Casciola, M., & Pakhomov, A. G. (2018) · Journal of Cardiovascular Electrophysiology · doi:10.1111/jce.13834 · Cited by 41 · see citing works
Semenov, I., Zemlin, C. W., Pakhomova, O. N., Xiao, S. H., & Pakhomov, A. G. (2015) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2015.06.018 · Cited by 39 · see citing works
Pakhomov, A. G., Gudvangen, E., Xiao, S. H., & Semenov, I. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107876 · Cited by 39 · see citing works
Muratori, C., Pakhomov, A. G., Gianulis, E. C., Meads, J., Casciola, M., Mollica, P. A., & Pakhomova, O. N. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.803049 · Cited by 38 · see citing works
Morotomi‐Yano, K., Akiyama, H., & Yano, K. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.10.061 · Cited by 35 · see citing works
Dermol‐Černe, J., Damijan Miklavčič, A., Reberšek, M., Mekuč, P., Bardet, S. M., Burke, R., Arnaud‐Cormos, D., Lévêque, P., & O'Connor, R. P. (2018) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2018.03.011 · Cited by 35 · see citing works
Probing Nanoelectroporation and Resealing of the Cell Membrane by the Entry of Ca2+ and Ba2+ Ions
Bo, W., Šilkūnas, M., Mangalanathan, U. M., Novickij, V., Casciola, M., Semenov, I., Xiao, S. H., Pakhomova, O. N., & Pakhomov, A. G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093386 · Cited by 32 · see citing works
Transprotein-Electropore Characterization: A Molecular Dynamics Investigation on Human AQP4
Marracino, P., Bernardi, M. D., Liberti, M., Signore, F. D., Trapani, E., Gárate, J. A., Burnham, C. J., Apollonio, F., & English, N. J. (2018) · ACS Omega · doi:10.1021/acsomega.8b02230 · Cited by 28 · see citing works
Guo, J., Ma, R., Su, B., Li, Y., Zhang, J., & Fang, J. (2016) · Scientific Reports · doi:10.1038/srep25949 · Cited by 27 · see citing works
Bagalkot, T. R., Leblanc, N., & Craviso, G. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-47929-4 · Cited by 27 · see citing works
Self-citationPall, M. L. (2022) · Current Alzheimer Research · doi:10.2174/1567205019666220202114510 · Cited by 25 · see citing works
Nanosecond pulsed electric field induces calcium mobilization in osteoblasts
Zhou, P., He, F., Han, Y., Liu, B., & Wei, S. (2018) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2018.06.009 · Cited by 25 · see citing works
Ruiz-Fernández, A. R., Campos, L., Villanelo, F., Gutiérrez-Maldonado, S. E., & Pérez‐Acle, T. (2021) · Membranes · doi:10.3390/membranes11070473 · Cited by 24 · see citing works
Liu, H., Zhao, Y., Yao, C., Schmelz, E. M., & Davalos, R. V. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107942 · Cited by 23 · see citing works
Xu, M., Xu, D., Dong, G., Ren, Z., Zhang, W., Aji, T., Zhao, Q., Chen, X., & Jiang, T. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.869316 · Cited by 23 · see citing works
Advances in applications of piezoelectronic electrons in cell regulation and tissue regeneration
Zhou, L., Yuan, T., Jin, F., Li, T., Qian, L., Wei, Z., Zheng, W., Ma, X., Wang, F., & Feng, Z. (2022) · Journal of Materials Chemistry B · doi:10.1039/d2tb01582j · Cited by 23 · see citing works
Doyon, P. R., & Johansson, O. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.06.028 · Cited by 23 · see citing works
2-ns Electrostimulation of Ca2+ Influx into Chromaffin Cells: Rapid Modulation by Field Reversal
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Self-citationYang, L., Craviso, G. L., Vernier, P. T., Chatterjee, I., & Leblanc, N. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181002 · Cited by 21 · see citing works
Self-citationZaklit, J., Craviso, G. L., Leblanc, N., Yang, L., Vernier, P. T., & Chatterjee, I. (2017) · The Journal of Membrane Biology · doi:10.1007/s00232-017-9983-9 · Cited by 21 · see citing works
Self-citationBagalkot, T. R., Terhune, R. C., Leblanc, N., & Craviso, G. L. (2018) · BioMed Research International · doi:10.1155/2018/9046891 · Cited by 20 · see citing works
Self-citationRems, L., Rainot, A., Wiczew, D., Szulc, N., & Tarek, M. (2023) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2023.108588 · Cited by 19 · see citing works
Claire Dalmay, A., de Ménorval, M., Français, O., Mir, L. M., & Pioufle, B. L. (2012) · Lab on a Chip · doi:10.1039/c2lc40857k · Cited by 19 · see citing works
Yoon, J., Leblanc, N., Zaklit, J., Vernier, P. T., Chatterjee, I., & Craviso, G. L. (2016) · The Journal of Membrane Biology · doi:10.1007/s00232-016-9902-5 · Cited by 18 · see citing works
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Gundersen, M. A., Vernier, P. T., Cronin, S. B., & Kerketta, S. (2020) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2020.2972934 · Cited by 18 · see citing works
Self-citationRuiz-Fernández, A. R., Rosemblatt, M. V., & Pérez‐Acle, T. (2022) · Annals of Medicine · doi:10.1080/07853890.2022.2087898 · Cited by 13 · see citing works
Yang, L., Pierce, S., Chatterjee, I., Craviso, G. L., & Leblanc, N. (2020) · PLoS ONE · doi:10.1371/journal.pone.0234114 · Cited by 13 · see citing works
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Craviso, G. L., Fisher, C., Chatterjee, I., & Vernier, P. T. (2014) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2014.08.006 · Cited by 12 · see citing works
Self-citationIbrahimi, N., Vallet, L., André, F. M., Rivaletto, M., Novac, B. M., Mir, L. M., & Pécastaing, L. (2023) · Bioelectricity · doi:10.1089/bioe.2022.0031 · Cited by 11 · see citing works
Chen, R., & Chen, X. (2013) · Surgery Current Research · doi:10.4172/2161-1076.s12-005 · Cited by 11 · see citing works
Mechanical Strain Regulates Osteoblast Proliferation Through Ca2+-CaMK-CREB Signal Pathway
Guo, Y., Lv, Q., Zou, X., Yan, Z., & Yan, Y.-X. (2016) · Chinese Medical Sciences Journal · doi:10.1016/s1001-9294(16)30033-5 · Cited by 11 · see citing works
Tolstykh, G. P., Cantu, J. C., Tarango, M., & Ibey, B. L. (2018) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2018.12.007 · Cited by 11 · see citing works
Zaklit, J., Chatterjee, I., Leblanc, N., & Craviso, G. L. (2019) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2019.04.006 · Cited by 11 · see citing works
Self-citationBaker, C., Willis, A., Milestone, W., Baker, M., Garner, A. L., & Joshi, R. P. (2024) · Scientific Reports · doi:10.1038/s41598-024-74659-z · Cited by 10 · see citing works
Yang, L., Pierce, S., Gould, T. W., Craviso, G. L., & Leblanc, N. (2022) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2022.109252 · Cited by 10 · see citing works
Self-citationMazzarda, F., Chittams-Miles, A. E., Pittaluga, J., Sozer, E. B., Vernier, P. T., & Muratori, C. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200881 · Cited by 10 · see citing works
Self-citationSozer, E. B., Semenov, I., & Vernier, P. T. (2024) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2024.108751 · Cited by 9 · see citing works
Self-citationZaklit, J., Cabrera, A., Shaw, A. J., Aoun, R., Vernier, P. T., Leblanc, N., & Craviso, G. L. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107830 · Cited by 8 · see citing works
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Bo, W., Tang, J., Ma, J., & Gong, Y. (2018) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2018.2840324 · Cited by 7 · see citing works
Kaynak, A., N’Guessan, K. F., Patel, P. H., Lee, J. H., Kogan, A. B., Narmoneva, D. A., & Qi, X. (2023) · Biomedicines · doi:10.3390/biomedicines11020466 · Cited by 7 · see citing works
Łapińska, Z., Novickij, V., Rembiałkowska, N., Szewczyk, A., Dubińska–Magiera, M., Kulbacka, J., & Saczko, J. (2023) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2023.108483 · Cited by 7 · see citing works
ns Pulsed Electric Field-Induced Action Potentials in the Circuital Model of an Axon
Lamberti, P., Compitiello, M., & Romeo, S. (2018) · IEEE Transactions on NanoBioscience · doi:10.1109/tnb.2018.2822840 · Cited by 7 · see citing works
Liu, J., Lu, Q., Liang, R., Guo, J., Wang, K., Dong, F., Wang, J., Zhang, J., & Fang, J. (2019) · Physical Review Applied · doi:10.1103/physrevapplied.11.024001 · Cited by 7 · see citing works
Napotnik, T. B., & Damijan Miklavčič, A. (2021) · Molecules · doi:10.3390/molecules26216571 · Cited by 6 · see citing works
Protein-Mediated Electroporation in a Cardiac Voltage-Sensing Domain Due to an nsPEF Stimulus
Ruiz-Fernández, A. R., Campos, L., Villanelo, F., Gárate, J. A., & Pérez‐Acle, T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411397 · Cited by 6 · see citing works
Modulating Ca2+ influx into adrenal chromaffin cells with short-duration nanosecond electric pulses
Yun, S. H., Mansurov, V., Yang, L., Yoon, J., Leblanc, N., Craviso, G. L., & Zaklit, J. (2024) · Biophysical Journal · doi:10.1016/j.bpj.2024.06.021 · Cited by 6 · see citing works
Self-citationPulse Power Ablation of Melanoma with Nanosecond Pulsed Electric Fields
Stephen, J., Wentia, E., Ren, W., & Che, X. (2011) · InTech eBooks · doi:10.5772/22850 · Cited by 6 · see citing works
Safety factor for electrostimulation with nanosecond pulses
Zemlin, C. W. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107882 · Cited by 6 · see citing works
Electric pulse shape impact on biological effects: A modeling study
Garner, A. L., Maciejewski, J. J., Vadlamani, A., & Byer, R. J. (2015) · IEEE Conference on Electrical Insulation and Dielectric Phenomena (CEIDP) · doi:10.1109/ceidp.2015.7352148 · Cited by 6 · see citing works
Viola, C., Gould, T. W., Procacci, N. M., Leblanc, N., Zaklit, J., & Craviso, G. L. (2023) · PLoS ONE · doi:10.1371/journal.pone.0283736 · Cited by 4 · see citing works
Self-citationNapotnik, T. B., Cimperman, T., & Rems, L. (2025) · Scientific Reports · doi:10.1038/s41598-025-06989-5 · Cited by 3 · see citing works
Subcellular Biological Effects of Nanosecond Pulsed Electric Fields
Kolb, J. F., & Stacey, M. W. (2011) · NATO science for peace and security series. A, Chemistry and biology · doi:10.1007/978-94-007-2852-3_28 · Cited by 3 · see citing works
Merla, C., Paffi, A., Apollonio, F., Lévêque, P., & Liberti, M. (2011) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2011.6090079 · Cited by 2 · see citing works
Cantu, J. C., Tolstykh, G. P., Tarango, M., Beier, H. T., & Ibey, B. L. (2021) · The Journal of Membrane Biology · doi:10.1007/s00232-020-00160-z · Cited by 2 · see citing works
Elementary Concepts and Definitions
Brosseau, C. (2023) · Studies in mechanobiology, tissue engineering and biomaterials · doi:10.1007/978-3-031-37981-9_2 · Cited by 2 · see citing works
Ultra short waves alleviate ulcerative colitis via TRPV2 mediated-macrophage polarization
Ning, Y., Wang, Y., Guo, M., Mai, J., Sun, W., Ge, Z., Han, K., Wang, C., Qin, L., Wang, X., et al. (2026) · iScience · doi:10.1016/j.isci.2026.115929 · Cited by 1 · see citing works
Morotomi‐Yano, K., & Yano, K. (2015) · Cited by 1 · see citing works
[Mechanism of ablation with nanosecond pulsed electric field].
Cen, C., Chen, X., & Zheng, S. (2015) · PubMed Central · doi:10.3785/j.issn.1008-9292.2015.11.13 · Cited by 1 · see citing works
Effects of usEPs on Plasma Membranes—Pores, Channels, and Repair
Beebe, S. J. (2021) · Series in bioengineering · doi:10.1007/978-981-10-5113-5_2 · Cited by 1 · see citing works
Application and Characterization Osteo Nanoporation under Electrical Stimuli
Sarkar, S., & Mk, G. (2015) · Gene Technology · doi:10.4172/2329-6682.1000123
Shckorbatov, Y. (2018) · International Conference on Ultrawideband and Ultrashort Impulse Signals · doi:10.1109/uwbusis.2018.8520259
Ruiz-Fernández, Á., Gallo-Méndez, I., Campos, L. R. S., Ceballos-Ulloa, F., Barria-Urenda, M., Garate, J. A., Araya-Secchi, R., & Pérez-Acle, T. (2025) · Protein Science · doi:10.1002/pro.70285
Yang, L., Zaklit, J., Gould, T. W., Craviso, G. L., & Leblanc, N. (2026) · The Journal of Membrane Biology · doi:10.1007/s00232-026-00370-x
Self-citation
- Authors
- Craviso, G. L., Choe, S., Chatterjee, P., Chatterjee, I., & Vernier, P. T.
- Affiliations
- University of Nevada, Reno (US)
- University of Southern California (US)
- Corresponding author
- Craviso, Gale L.
- Venue
- Cellular and Molecular Neurobiology
- Published
- 2010-11
- Volume
- 30
- Issue
- 8
- Pages
- 1259-1265
- ISSN
- 0272-4340 (ISSN-L)
- 1573-6830
- PMC
- PMC11498812
- OpenAlex
- W2003802737
- Cited by
- 107
- References
- 32
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 3 · 2023: 10 · 2022: 6 · 2021: 9 · 2020: 7 · 2019: 6 · 2018: 12 · 2017: 13 · 2016: 6 · 2015: 8 · 2014: 5 · 2013: 5 · 2012: 6
- FWCI
- 1.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cellular and Molecular Neurobiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Agence Nationale pour la Gestion des Déchets Radioactifs
- Air Force Office of Scientific Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- nanosecond pulsed electric fields, chromaffin cells, voltage-gated calcium channels, L-type calcium channels, N-type calcium channels, P/Q-type calcium channels, intracellular calcium influx, catecholamine release, omega-conotoxin GVIA, omega-agatoxin IVA, omega-conotoxin MVIIC, sodium transport, membrane potential, tetrodotoxin
- MeSH terms
- Animals, Calcium, Calcium Channel Blockers, Cattle, Electricity, Extracellular Space, Membrane Potentials, Sodium, Time Factors, Calcium Channels, Ion Channel Gating, Chromaffin Cells, Calcium Signaling
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