Calcium signaling and exocytosis in adrenal chromaffin cells

García, Antonio G.; García-De-Diego, Antonio M.; Gandía, Luis; Borges, Ricardo; García-Sancho, Javier

doi:10.1152/physrev.00039.2005

Cited by 350Ion channel regulation and functionIon Channels and ReceptorsCalcium signaling and nucleotide metabolism

Calcium signaling and exocytosis in adrenal chromaffin cells

García, Antonio G., García-De-Diego, Antonio M., Gandía, Luis, Borges, Ricardo, García-Sancho, Javier·2006·Physiological Reviews

DOI 10.1152/physrev.00039.2005

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Abstract

At a given cytosolic domain of a chromaffin cell, the rate and amplitude of the Ca2+ concentration ([Ca2+]c) depends on at least four efficient regulatory systems: 1) plasmalemmal calcium channels, 2) endoplasmic reticulum, 3) mitochondria, and 4) chromaffin vesicles. Different mammalian species express different levels of the L, N, P/Q, and R subtypes of high-voltage-activated calcium channels; in bovine and humans, P/Q channels predominate, whereas in felines and murine species, L-type channels predominate. The calcium channels in chromaffin cells are regulated by G proteins coupled to purinergic and opiate receptors, as well as by voltage and the local changes of [Ca2+]c. Chromaffin cells have been particularly useful in studying calcium channel current autoregulation by materials coreleased with catecholamines, such as ATP and opiates. Depending on the preparation (cultured cells, adrenal slices) and the stimulation pattern (action potentials, depolarizing pulses, high K+, acetylcholine), the role of each calcium channel in controlling catecholamine release can change drastically. Targeted aequorin and confocal microscopy shows that Ca2+ entry through calcium channels can refill the endoplasmic reticulum (ER) to nearly millimolar concentrations, and causes the release of Ca2+ (CICR). Depending on its degree of filling, the ER may act as a sink or source of Ca2+ that modulates catecholamine release. Targeted aequorins with different Ca2+ affinities show that mitochondria undergo surprisingly rapid millimolar Ca2+ transients, upon stimulation of chromaffin cells with ACh, high K+, or caffeine. Physiological stimuli generate [Ca2+]c microdomains in which the local subplasmalemmal [Ca2+]c rises abruptly from 0.1 to approximately 50 microM, triggering CICR, mitochondrial Ca2+ uptake, and exocytosis at nearby secretory active sites. The fact that protonophores abolish mitochondrial Ca2+ uptake, and increase catecholamine release three- to fivefold, support the earlier observation. This increase is probably due to acceleration of vesicle transport from a reserve pool to a ready-release vesicle pool; this transport might be controlled by Ca2+ redistribution to the cytoskeleton, through CICR, and/or mitochondrial Ca2+ release. We propose that chromaffin cells have developed functional triads that are formed by calcium channels, the ER, and the mitochondria and locally control the [Ca2+]c that regulate the early and late steps of exocytosis.

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Single-cell amperometry measures the numbers of released catecholamine molecules during every individual exocytosis event.
“Single-cell amperometry measures the numbers of released catecholamine molecules during every individual exocytosis event (Garcia et al., 2006; Wightman et al., 1991).”
From Intestinal microbiota modulates adrenomedullary response through Nod1 sensing in chromaffin cells (2021) · cites this paper as Garcia et al., 2006

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Q‐ and L‐type Ca2+ channels dominate the control of secretion in bovine chromaffin cells
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R-Type Ca2+Channels Are Coupled to the Rapid Component of Secretion in Mouse Adrenal Slice Chromaffin Cells
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Inositol 1,4,5-trisphosphate-triggered Ca2+ release from bovine adrenal medullary secretory vesicles.
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Chromaffin cell calcium channel kinetics measured isotopically through fast calcium, strontium, and barium fluxes.
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The control of cytoskeletal actin and exocytosis in intact and permeabilized adrenal chromaffin cells: role of calcium and protein kinase C
Burgoyne, R. D., Morgan, A., & O’Sullivan, A. J. (1989) · Cellular Signalling · doi:10.1016/0898-6568(89)90051-x · Cited by 107 · see citing works
ATP modulation of calcium channels in chromaffin cells.
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Two types of Ca2+ currents are found in bovine chromaffin cells: facilitation is due to the recruitment of one type.
Artalejo, C. R., Dahmer, M. K., Perlman, R. L., & Fox, A. P. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018406 · Cited by 107 · see citing works
Release of LHRH is linearly related to the time integral of presynaptic Ca+ elevation above a threshold level in bullfrog sympathetic ganglia
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ω-Conotoxin GVIA blocks a Ca2+ current in bovine chromaffin cells that is not of the “classic” N type
Artalejo, C. R., Perlman, R. L., & Fox, A. P. (1992) · Neuron · doi:10.1016/0896-6273(92)90110-y · Cited by 105 · see citing works

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L-type CaV1.2 calcium channels: from in vitro findings to in vivo function.
Hofmann, F., Flockerzi, V., Kahl, S., & Wegener, J. (2014) · Physiological Reviews · doi:10.1152/physrev.00016.2013 · Cited by 330 · see citing works
Neurotoxicity of Brominated Flame Retardants: (In)direct Effects of Parent and Hydroxylated Polybrominated Diphenyl Ethers on the (Developing) Nervous System
Dingemans, M. M. L., van den Berg, M., & Westerink, R. H. S. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1003035 · Cited by 310 · see citing works
R1441C mutation in LRRK2 impairs dopaminergic neurotransmission in mice
Tong, Y., Pisani, A., Martella, G., Karouani, M., Yamaguchi, H., Pothos, E. N., & Shen, J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906334106 · Cited by 304 · see citing works
Hydroxylation Increases the Neurotoxic Potential of BDE-47 to Affect Exocytosis and Calcium Homeostasis in PC12 Cells
Dingemans, M. M. L., de Groot, A., van Kleef, R. G. D. M., Bergman, Å., van den Berg, M., Vijverberg, H. P. M., & Westerink, R. H. S. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11059 · Cited by 210 · see citing works
BDE-47 disrupts axonal growth and motor behavior in developing zebrafish
Chen, X., Huang, C., Wang, X., Chen, J., Bai, C., Chen, Y., Chen, X., Dong, Q., & Yang, D. (2012) · Aquatic Toxicology · doi:10.1016/j.aquatox.2012.04.014 · Cited by 135 · see citing works
A physiological view of the central and peripheral mechanisms that regulate the release of catecholamines at the adrenal medulla
de Diego, A. M. G., Gandı́a, L., & Garcı́a, A. G. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01807.x · Cited by 129 · see citing works
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Selective Uncoupling of Individual Mitochondria within a Cell Using a Mitochondria-Targeted Photoactivated Protonophore
Chalmers, S., Caldwell, S. T., Quin, C., Prime, T. A., James, A. M., Cairns, A. G., Murphy, M. P., McCarron, J. G., & Hartley, R. C. (2011) · Journal of the American Chemical Society · doi:10.1021/ja2077922 · Cited by 118 · see citing works
Arrestin-biased AT1R agonism induces acute catecholamine secretion through TRPC3 coupling
Liu, C.-H., Gong, Z., Liang, Z.-L., Liu, Z.-X., Yang, F., Sun, Y., Ma, M.-L., Wang, Y.-J., Ji, C.-R., Wang, Y.-H., et al. (2017) · Nature Communications · doi:10.1038/ncomms14335 · Cited by 115 · see citing works
Nanosecond Electric Pulses: A Novel Stimulus for Triggering Ca2+ Influx into Chromaffin Cells Via Voltage-Gated Ca2+ Channels
Craviso, G. L., Choe, S., Chatterjee, P., Chatterjee, I., & Vernier, P. T. (2010) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-010-9573-1 · Cited by 107 · see citing works
Glucose-Stimulated Calcium Dynamics in Islets of Langerhans in Acute Mouse Pancreas Tissue Slices
Stožer, A., Dolenšek, J., & Rupnik, M. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054638 · Cited by 106 · 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
Cav1.3 and BK Channels for Timing and Regulating Cell Firing
Vandael, D. H. F., Marcantoni, A., Mahapatra, S., Caro, A., Ruth, P., Zuccotti, A., Knipper, M., & Carbone, E. (2010) · Molecular Neurobiology · doi:10.1007/s12035-010-8151-3 · Cited by 103 · see citing works
Translating neurobehavioural endpoints of developmental neurotoxicity tests into in vitro assays and readouts
van Thriel, C., Westerink, R. H. S., Beste, C., Bale, A. S., Lein, P. J., & Leist, M. (2011) · NeuroToxicology · doi:10.1016/j.neuro.2011.10.002 · Cited by 103 · see citing works
The Endoplasmic Reticulum of Dorsal Root Ganglion Neurons Contains Functional TRPV1 Channels
Gallego‐Sandín, S., Rodrı́guez-Garcı́a, A., Alonso, M. T., & Garcı́a-Sancho, J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.019687 · Cited by 97 · see citing works
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Acute Enhancement of Synaptic Transmission and Chronic Inhibition of Synaptogenesis Induced by Perfluorooctane Sulfonate through Mediation of Voltage-dependent Calcium Channel
Liao, C.-Y., Li, X.-Y., Wu, B., Duan, S., & Jiang, G.-B. (2008) · Environmental Science & Technology · doi:10.1021/es800018k · Cited by 96 · see citing works
Calcium Triggers Exocytosis from Two Types of Organelles in a Single Astrocyte
Liu, T., Sun, L., Xiong, Y., Shang, S., Guo, N., Teng, S., Wang, Y., Liu, B., Wang, C., Wang, L., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6401-10.2011 · Cited by 97 · see citing works
Transgene-free remote magnetothermal regulation of adrenal hormones
Rosenfeld, D., Senko, A. W., Moon, J., Yick, I., Varnavides, G., Gregureć, D., Koehler, F., Chiang, P., Christiansen, M. G., Maeng, L. Y., et al. (2020) · Science Advances · doi:10.1126/sciadv.aaz3734 · Cited by 95 · see citing works
Intracellular Ca 2+ - and Mn 2+ -Transport ATPases
Vangheluwe, P., Sepúlveda, M. R., Missiaen, L., Raeymaekers, L., Wuytack, F., & Vanoevelen, J. M. (2009) · Chemical Reviews · doi:10.1021/cr900013m · Cited by 89 · see citing works
L-type calcium channels in adrenal chromaffin cells: Role in pace-making and secretion
Marcantoni, A., Baldelli, P., Hernández-Guijo, J. M., Comunanza, V., Carabelli, V., & Carbone, E. (2007) · Cell Calcium · doi:10.1016/j.ceca.2007.04.015 · Cited by 89 · see citing works
Chromaffin Cells of the Adrenal Medulla: Physiology, Pharmacology, and Disease
Carbone, E., Borges, R., Eiden, L. E., Garcı́a, A. G., & Hernández‐Cruz, A. (2019) · Comprehensive physiology · doi:10.1002/cphy.c190003 · Cited by 105 · see citing works
Self-citation
Calcium channel types contributing to chromaffin cell excitability, exocytosis and endocytosis
Mahapatra, S., Calorio, C., Vandael, D. H. F., Marcantoni, A., Carabelli, V., & Carbone, E. (2012) · Cell Calcium · doi:10.1016/j.ceca.2012.01.005 · Cited by 79 · see citing works
Multiple Novel Modes of Action Involved in the In Vitro Neurotoxic Effects of Tetrabromobisphenol-A
Hendriks, H. S., van Kleef, R. G. D. M., van den Berg, M., & Westerink, R. H. S. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfs136 · Cited by 69 · see citing works
Neuronal Calcium Sensor-1 Regulation of Calcium Channels, Secretion, and Neuronal Outgrowth
Weiss, J. L., Hui, H., & Burgoyne, R. D. (2010) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-010-9588-7 · Cited by 68 · see citing works
CaV1.3-Driven SK Channel Activation Regulates Pacemaking and Spike Frequency Adaptation in Mouse Chromaffin Cells
Vandael, D. H. F., Zuccotti, A., Striessnig, J., & Carbone, E. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3715-12.2012 · Cited by 68 · see citing works
Platelet Granule Exocytosis: A Comparison with Chromaffin Cells
Fitch, J. L., & Flaumenhaft, R. C. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00077 · Cited by 65 · see citing works
Intricacies of the Molecular Machinery of Catecholamine Biosynthesis and Secretion by Chromaffin Cells of the Normal Adrenal Medulla and in Pheochromocytoma and Paraganglioma
Berends, A. M. A., Eisenhofer, G., Fishbein, L. M., van der Horst‐Schrivers, A. N. A., Kema, I. P., Links, T. P., Lenders, J. W. M., & Kerstens, M. N. (2019) · Cancers · doi:10.3390/cancers11081121 · Cited by 63 · see citing works
Compartmentalized cAMP signalling in regulated exocytic processes in non-neuronal cells
Szaszák, M., Frank, C., Rosenthal, W., & Klußmann, E. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.10.020 · Cited by 63 · see citing works
The high-affinity calcium sensor synaptotagmin-7 serves multiple roles in regulated exocytosis
MacDougall, D., Lin, Z., Chon, N. L., Jackman, S. L., Lin, H., Knight, J. D., & Anantharam, A. (2018) · The Journal of General Physiology · doi:10.1085/jgp.201711944 · Cited by 65 · see citing works
Reduced availability of voltage‐gated sodium channels by depolarization or blockade by tetrodotoxin boosts burst firing and catecholamine release in mouse chromaffin cells
Vandael, D. H. F., Ottaviani, M. M., Legros, C., Gabillard-Lefort, C., Guérineau, N. C., Allio, A., Carabelli, V., & Carbone, E. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.283374 · Cited by 60 · 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
Intravesicular Calcium Release Mediates the Motion and Exocytosis of Secretory Organelles
Camacho, M., Machado, J. D., Álvarez, J., & Borges, R. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800552200 · Cited by 57 · see citing works
Self-citation
PDE type-4 inhibition increases L-type Ca2+ currents, action potential firing, and quantal size of exocytosis in mouse chromaffin cells
Marcantoni, A., Carabelli, V., Vandael, D. H. F., Comunanza, V., & Carbone, E. (2008) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-008-0584-4 · Cited by 55 · see citing works
Distinct fusion properties of synaptotagmin-1 and synaptotagmin-7 bearing dense core granules
Rao, T. C., Passmore, D. R., Peleman, A. R., Das, M., Chapman, E. R., & Anantharam, A. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-02-0702 · Cited by 55 · see citing works
Evaluating the Diffusion Coefficient of Dopamine at the Cell Surface During Amperometric Detection: Disk vs Ring Microelectrodes
Trouillon, R., Lin, Y., Mellander, L. J., Keighron, J. D., & Ewing, A. G. (2013) · Analytical Chemistry · doi:10.1021/ac400965d · Cited by 53 · see citing works
Privileged coupling between Ca2+ entry through plasma membrane store-operated Ca2+ channels and the endoplasmic reticulum Ca2+ pump
Alonso, M. T., Manjarrés, I. M., & Garcı́a-Sancho, J. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.08.021 · Cited by 53 · see citing works
Self-citation
Single‐Vesicle Electrochemistry Reveals Sex Difference in Vesicular Storage and Release of Catecholamine
Yue, Q., Wang, K., Guan, M., Zhao, Z., Li, X., Yu, P., & Mao, L. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202117596 · Cited by 51 · see citing works
Roles of Na+, Ca2+, and K+ channels in the generation of repetitive firing and rhythmic bursting in adrenal chromaffin cells
Lingle, C. J., Martinez-Espinosa, P. L., Guarina, L., & Carbone, E. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-2048-1 · Cited by 51 · see citing works
The role of mitochondrial potential in control of calcium signals involved in cell proliferation
Valero, R. A., Senovilla, L., Núñez, L., & Villalobos, C. (2008) · Cell Calcium · doi:10.1016/j.ceca.2007.12.002 · Cited by 51 · see citing works
Cysteinyl leukotriene 2 receptor‐mediated vascular permeability via transendothelial vesicle transport
Moos, M. P. W., Mewburn, J. D., Kan, F. W. K., Ishii, S., Abe, M., Sakimura, K., Noguchi, K., Shimizu, T., & Funk, C. D. (2008) · The FASEB Journal · doi:10.1096/fj.08-113274 · Cited by 50 · see citing works
Serotonin and Serotonin Transporters in the Adrenal Medulla: A Potential Hub for Modulation of the Sympathetic Stress Response
Brindley, R. L., Bauer, M. B., Blakely, R., & Currie, K. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00026 · Cited by 50 · see citing works
Pituitary Adenylate Cyclase-activating Peptide (PACAP) Recruits Low Voltage-activated T-type Calcium Influx under Acute Sympathetic Stimulation in Mouse Adrenal Chromaffin Cells*
Hill, J., Chan, S.-A., Kuri, B. A., & Smith, C. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.289389 · Cited by 44 · see citing works
Secretory granules in inositol 1,4,5‐trisphosphate‐dependent Ca 2+ signaling in the cytoplasm of neuroendocrine cells
Yoo, S. H. (2009) · The FASEB Journal · doi:10.1096/fj.09-132456 · Cited by 49 · see citing works
Novel model for “calcium paradox” in sympathetic transmission of smooth muscles: Role of cyclic AMP pathway
Bergantin, L. B., Souza, C. F., Ferreira, R. M., Smaili, S. S., Jurkiewicz, N. H., Caricati‐Neto, A., & Jurkiewicz, A. (2013) · Cell Calcium · doi:10.1016/j.ceca.2013.06.004 · Cited by 46 · see citing works
Calcium-Related Processes Involved in the Inhibition of Depolarization-Evoked Calcium Increase by Hydroxylated PBDEs in PC12 Cells
Dingemans, M. M. L., van den Berg, M., Bergman, Å., & Westerink, R. H. S. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp310 · Cited by 47 · see citing works
Cav1.3 Channels as Key Regulators of Neuron-Like Firings and Catecholamine Release in Chromaffin Cells
Vandael, D. H. F., Marcantoni, A., & Carbone, E. (2015) · Current Molecular Pharmacology · doi:10.2174/1874467208666150507105443 · Cited by 47 · see citing works
PACAP signaling in stress: insights from the chromaffin cell
Eiden, L. E., Emery, A. C., Zhang, L., & Smith, C. B. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-2062-3 · Cited by 47 · see citing works
Modulation of cell viability, oxidative stress, calcium homeostasis, and voltage- and ligand-gated ion channels as common mechanisms of action of (mixtures of) non-dioxin-like polychlorinated biphenyls and polybrominated diphenyl ethers
Westerink, R. H. S. (2013) · Environmental Science and Pollution Research · doi:10.1007/s11356-013-1759-x · Cited by 46 · see citing works
Impaired chromaffin cell excitability and exocytosis in autistic Timothy syndrome TS2‐neo mouse rescued by L‐type calcium channel blockers
Calorio, C., Gavello, D., Guarina, L., Salio, C., Sassoé‐Pognetto, M., Riganti, C., Bianchi, F. T., Hofer, N. T., Tuluc, P., Obermair, G. J., et al. (2019) · The Journal of Physiology · doi:10.1113/jp277487 · Cited by 46 · see citing works
Nanosecond electric pulse-induced increase in intracellular calcium in adrenal chromaffin cells triggers calcium-dependent catecholamine release
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
Pharmacological implications of the Ca2+/ cAMP signaling interaction: from risk for antihypertensive therapy to potential beneficial for neurological and psychiatric disorders
Caricati‐Neto, A., Garcı́a, A. G., & Bergantin, L. B. (2015) · Pharmacology Research & Perspectives · doi:10.1002/prp2.181 · Cited by 45 · see citing works
Self-citation
Calcium channels in chromaffin cells: focus on L and T types
Marcantoni, A., Carabelli, V., Comunanza, V., Hoddah, H., & Carbone, E. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01815.x · Cited by 45 · see citing works
Differential Co-release of Two Neurotransmitters from a Vesicle Fusion Pore in Mammalian Adrenal Chromaffin Cells
Zhang, Q., Liu, B., Wu, Q., Liu, B., Li, Y., Sun, S., Wang, Y., Wu, X., Chai, Z., Jiang, X., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.031 · Cited by 43 · see citing works
Depolarization preconditioning produces cytoprotection against veratridine-induced chromaffin cell death
Orozco, C., de Diego, A. M. G., Arias, E., Hernández-Guijo, J. M., de Diego, A. M. G., Villarroya, M., & López, M. G. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.08.084 · Cited by 41 · see citing works
Stabilizers of Neuronal and Mitochondrial Calcium Cycling as a Strategy for Developing a Medicine for Alzheimer's Disease
Fernández‐Morales, J., Arranz-Tagarro, J.-A., Calvo‐Gallardo, E., Maroto, M., Padín, J. F., & Garcı́a, A. G. (2012) · ACS Chemical Neuroscience · doi:10.1021/cn3001069 · Cited by 40 · see citing works
Self-citation
The F-actin cortical network is a major factor influencing the organization of the secretory machinery in chromaffin cells
Torregrosa‐Hetland, C. J., Villanueva, J., Giner, D., López‐Font, I., Nadal, Á., Quesada, I., Viniegra, S., Expósito-Romero, G., Gil, A., González‐Vélez, V., et al. (2011) · Journal of Cell Science · doi:10.1242/jcs.078600 · Cited by 40 · see citing works
Differential Effects of 20 Non-Dioxin-Like PCBs on Basal and Depolarization-Evoked Intracellular Calcium Levels in PC12 Cells
Langeveld, W. T., Meijer, M., & Westerink, R. H. S. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfr346 · Cited by 38 · see citing works
Hydrogen sulfide stimulates catecholamine secretion in rainbow trout (Oncorhynchus mykiss)
Perry, S. F., McNeill, B., Elia, E., Nagpal, A., & Vulesevic, B. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00185.2008 · Cited by 38 · see citing works
Calcium entry-calcium refilling (CECR) coupling between store-operated Ca2+ entry and sarco/endoplasmic reticulum Ca2+-ATPase
Manjarrés, I. M., Alonso, M. T., & Garcı́a-Sancho, J. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.01.007 · Cited by 38 · see citing works
Self-citation
Testing Pancreatic Islet Function at the Single Cell Level by Calcium Influx with Associated Marker Expression
Kenty, J. H.-R., & Melton, D. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122044 · Cited by 38 · see citing works
Cav1.3 and Cav1.2 channels of adrenal chromaffin cells: Emerging views on cAMP/cGMP-mediated phosphorylation and role in pacemaking
Vandael, D. H. F., Mahapatra, S., Calorio, C., Marcantoni, A., & Carbone, E. (2012) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2012.11.013 · Cited by 37 · see citing works
Effect of cytosolic Mg2+ on mitochondrial Ca2+ signaling
Szanda, G., Rajki, A., Gallego‐Sandín, S., Garcı́a-Sancho, J., & Spät, A. (2008) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-008-0551-0 · Cited by 37 · see citing works
Self-citation
L-type calcium channels are preferentially coupled to endocytosis in bovine chromaffin cells
Rosa, J. M., de Diego, A. M. G., Gandı́a, L., & de Diego, A. M. G. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.03.207 · Cited by 36 · see citing works
Self-citation
Histogenesis and morphofunctional characteristics of chromaffin cells
Díaz‐Flores, L., Gutiérrez, R., Varela, H., Valladares, F., Álvarez‐Argüelles, H., & Borges, R. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01811.x · Cited by 36 · see citing works
Self-citation
Single-Vesicle Catecholamine Release Has Greater Quantal Content and Faster Kinetics in Chromaffin Cells from Hypertensive, as Compared with Normotensive, Rats
Miranda‐Ferreira, R., de Pascual, R., de Diego, A. M. G., Caricati‐Neto, A., Gandı́a, L., Jurkiewicz, A., & de Diego, A. M. G. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.128819 · Cited by 36 · see citing works
Self-citation
Inhibition of Ca2+ Channels and Adrenal Catecholamine Release by G Protein Coupled Receptors
Currie, K. (2010) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-010-9596-7 · Cited by 35 · see citing works
Role of the Endoplasmic Reticulum and Mitochondria on Quantal Catecholamine Release from Chromaffin Cells of Control and Hypertensive Rats
Miranda-Ferreira, R., de Pascual, R., Caricati-Neto, A., Gandía, L., Jurkiewicz, A., & García, A. G. (2009) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.147413 · Cited by 35 · see citing works
Self-citation
The effect of CdSe–ZnS quantum dots on calcium currents and catecholamine secretion in mouse chromaffin cells
Gosso, S., Gavello, D., Giachello, C. N., Franchino, C., Carbone, E., & Carabelli, V. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.08.031 · Cited by 35 · see citing works
Mitochondrial Na+/Ca2+-Exchanger Blocker CGP37157 Protects against Chromaffin Cell Death Elicited by Veratridine
Nicolau, S. M., de Diego, A. M. G., Cortés, L., Egea, J., Gonzalez, J., Mosquera, M., López, M. G., Hernández-Guijo, J. M., & de Diego, A. M. G. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.154765 · Cited by 35 · see citing works
Functional Chromaffin Cell Plasticity in Response to Stress: Focus on Nicotinic, Gap Junction, and Voltage-Gated Ca2+ Channels
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Authors: García, A. G., García-De-Diego, A. M., Gandía, L., Borges, R., & García-Sancho, J.
ORCID: Borges, Ricardo
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2006-10
Volume: 86
Issue: 4
Pages: 1093-1131
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00039.2005
OpenAlex: W2137229430
Cited by: 349
References: 426
Citations by year: 2026: 6 · 2025: 9 · 2024: 14 · 2023: 10 · 2022: 22 · 2021: 9 · 2020: 15 · 2019: 13 · 2018: 16 · 2017: 22 · 2016: 11 · 2015: 12 · 2014: 18 · 2013: 19 · 2012: 23
FWCI: 1.91
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords: calcium signaling, exocytosis, catecholamine release, calcium channels, P/Q-type calcium channels, L-type calcium channels, calcium-induced calcium release, endoplasmic reticulum, mitochondrial calcium uptake, chromaffin granules, opioid receptors, purinergic receptors, G proteins, aequorin, vesicle trafficking, cytoskeleton, adrenal medulla, confocal microscopy
MeSH terms: Adrenal Glands, Animals, Exocytosis, Humans, Chromaffin Cells, Calcium Signaling

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Calcium signaling and exocytosis in adrenal chromaffin cells

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