Skip to main content
SpringerLink
Log in

Modulation of VGCCs by G-Protein Coupled Receptors and Their Second Messengers

  • Chapter
  • First Online:
Voltage-Gated Calcium Channels

Abstract

Voltage-gated calcium channels (VGCCs) are essential for transforming electrical signals such as action potentials into biochemical and eventually physiological responses through the control of intracellular calcium. They mediate the depolarization of cells and increase the intracellular Ca2+ levels to regulate a variety of physiological events including neurotransmission, secretion, enzyme activity, cellular differentiation, gene expression, smooth muscle contraction, and pacemaker activity. Deficits in VGCCs function can lead to epilepsy, migraine, ataxia, autism, cardiac arrythmias, and pain. Therefore, careful modulation of VGCCs is vital. In this chapter, we will discuss the modulation of VGCCs by different G protein-coupled receptors and their downstream effectors such as G proteins, lipids, kinases, and synaptic associated proteins focusing primarily on the central nervous system and heart. Moreover, we will describe the underlying mechanisms that G proteins and their downstream second messengers use to control VGCCs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

5-HT:

Serotonin

AA:

Arachidonic acid

AC:

Adenylyl cyclase

AGS:

Activator of G protein signaling

AID:

α interaction domain

AKAP:

A-kinase anchoring protein

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

AR:

adrenoceptor

BDNF:

Brain-derived neurotrophic factor

Ca2+:

Calcium

CaBP:

Ca2+ binding protein

CaM:

Calmodulin

CaMKII:

Ca2+/calmodulin-dependent protein kinase II

cAMP:

Cyclic adenosine monophosphate

CaS:

Ca2+ sensor

CB:

Cannabinoid receptor

cGMP:

Cyclic guanosine monophosphate

CNS:

Central nervous system

CRF:

Corticotropin-releasing factor

CTX:

Cholera toxin

D1R:

Dopamine D1 receptor 2

D2R:

Dopamine D2 receptor

DAG:

Diacylglycerol

DRG:

Dorsal root ganglion

ER:

Endoplasmatic reticulum

FGF:

Fibroblast growth factor

FGFR1:

Fibroblast growth factor type 1 receptor

FRET:

Fluorescence resonance energy transfer

GABA:

Gamma-aminobutyric acid

GDP:

Guanosine diphosphate

Ghrelin:

Growth hormone release inducing

GHS-R1a:

Growth hormone secretagogue receptor 1a

GID:

G protein interaction domain

GPCRs:

G protein-coupled receptors

GRK:

G protein coupled receptor kinase

GTP:

Guanosine triphosphate

HEK:

Human embryonic kidney

ICa:

Ca2+ current

IGF-1:

Insulin-like growth factor 1

IP3:

Inositol triphosphate

Kir:

Inward rectifying potassium channel

LPA:

Lysophosphatidic acid

LTD:

Long term depression

LTP:

Long-term potentiation

M1R:

Muscarinic receptor 1

MAPK:

Mitogen-activated protein kinase

mGluR:

Metabotropic glutamate receptor

NA:

noradrenaline

Na:

sodium

NCS-1:

Neural Ca2+ sensor-1

NO:

Nitric oxide

OAG:

1,2-Oleoylacetyl-glycerol

PDE:

Phosphodiesterase

PI3K:

Phosphatidylinositol 3-kinase

PIP2:

Phosphatidylinositol 4,5-bisphosphate

PKA:

Protein kinase A

PKC:

Protein kinase C

PKG:

Protein kinase G

PKI:

Protein kinase A inhibitor

PLC:

Phospholipase C

PMA:

Phorbol-myristate 13-acetate

PP:

protein phosphatase

PSD-95:

Postsynaptic density protein-95

PTK:

Protein tyrosine kinase

PTX:

Pertussis toxin

RGS:

Regulators of G protein signaling

ROCK:

Rho-associated protein kinase

SNAP-25:

Synaptosomal-associated protein

SNAREs:

Soluble N-ethylmaleimide-sensitive factor attachment protein receptors

SST:

Somatostatin receptor

Thr:

Threonine

VGCCs:

Voltage-gated calcium channels

VILIP-2:

Visinin-like protein-2

References

  • Agler, H. L., Evans, J., Colecraft, H. M., & Yue, D. T. (2003). Custom distinctions in the interaction of G-protein beta subunits with N-type (CaV2.2) versus P/Q-type (CaV2.1) calcium channels. The Journal of General Physiology, 121, 495–510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agler, H., Evans, J., Tay, L., Anderson, M., Colecraft, H., & Yue, D. (2005). G protein-gated inhibitory module of N-type (ca(v)2.2) ca2+ channels. Neuron, 46(6), 891–904.

    Article  CAS  PubMed  Google Scholar 

  • Altier, C., Khosravani, H., Evans, R. M., Hameed, S., Peloquin, J. B., Vartian, B. A., et al. (2006). ORL1 receptor-mediated internalization of N-type calcium channels. Nature Neuroscience, 9(1), 31–40.

    Article  CAS  PubMed  Google Scholar 

  • Alvarez, J. L., Rubio, L. S., & Vassort, G. (1996). Facilitation of T-type calcium current in bullfrog atrial cells: Voltage-dependent relief of a G protein inhibitory tone. The Journal of Physiology, 491(2), 321–334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrade, A., Denome, S., Jiang, Y., Marangoudakis, S., & Lipscombe, D. (2010). Opioid inhibition of N-type Ca2+ channels and spinal analgesia couple to alternative splicing. Nature Neuroscience, 13(10), 1249–1256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anliker, B., & Chun, J. (2004). Lysophospholipid G protein-coupled receptors. The Journal of Biological Chemistry, 279(20), 20555–20558.

    Article  CAS  PubMed  Google Scholar 

  • Arnot, M. I., Stotz, S. C., Jarvis, S. E., & Zamponi, G. W. (2000). Differential modulation of N-type 1B and P/Q-type 1A calcium channels by different G protein subunit isoforms. The Journal of Physiology, 527, 203–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnoult, C., Lemos, J. R., & Florman, H. M. (1997). Voltage-dependent modulation of T-type calcium channels by protein tyrosine phosphorylation. The EMBO Journal, 16(7), 1593–1599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnoult, C., Villaz, M., & Florman, H. M. (1998). Pharmacological properties of the T-type Ca2+ current mouse spermatogenic cells. Molecular Pharmacology, 53(6), 1104–1111.

    CAS  PubMed  Google Scholar 

  • Barrett, C., & Rittenhouse, A. (2000). Modulation of N-type calcium channel activity by G-proteins and protein kinase C. The Journal of General Physiology, 115(3), 277–286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrett, P. Q., Lu, H. K., Colbran, R., Czernik, A., & Pancrazio, J. J. (2000). Stimulation of unitary T-type Ca2+ channel currents by calmodulin-dependent protein kinase II. American Journal of Physiology. Cell Physiology, 279(6), 48–46.

    Article  Google Scholar 

  • Bean, B. P. (1989). Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature, 340, 153–156.

    Article  CAS  PubMed  Google Scholar 

  • Bear, M. F., Connors, B. W., & Paradiso, M. A. (2015). Neuroscience: Exploring the brain: Fourth edition. Jones & Bartlett Learning.

    Google Scholar 

  • Bernheim, L., Beech, D., & Hille, B. (1991). A diffusible second messenger mediates one of the pathways coupling receptors to calcium channels in rat sympathetic neurons. Neuron, 6(6), 859–867.

    Article  CAS  PubMed  Google Scholar 

  • Bkaily, G., Sculptoreanu, A., Wang, S., Nader, M., Hazzouri, K. M., Jacques, D., et al. (2005). Angiotensin II-induced increase of T-type Ca2+ current and decrease of L-type Ca2+ current in heart cells. Peptides, 26(8), 1410–1417.

    Article  CAS  PubMed  Google Scholar 

  • Bolshakov, V., & Siegelbaum, S. (1994). Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science, 264(5162), 1148–1152.

    Article  CAS  PubMed  Google Scholar 

  • Bonvallet, R., & Rougier, O. (1989). Existence of two calcium currents recorded at normal calcium concentrations in single frog atrial cells. Cell Calcium, 10(7), 499–508.

    Article  CAS  PubMed  Google Scholar 

  • Bucci, G., Mochida, S., & Stephens, G. (2011). Inhibition of synaptic transmission and G protein modulation by synthetic CaV2.2 Ca2+ channel peptides. The Journal of Physiology, 589(13), 3085–3101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carabelli, V., D’Ascenzo, M., Carbone, E., Grassi, C. (2002). Nitric oxide inhibits neuroendocrine Ca(V)1 L-channel gating via cGMP-dependent protein kinase in cell-attached patches of bovine chromaffin cells. The Journal of Physiology, 541(2), 351–366. https://doi.org/10.1113/jphysiol.2002.017749

  • Cairns, S., & Borrani, F. (2015). β-Adrenergic modulation of skeletal muscle contraction: Key role of excitation-contraction coupling. The Journal of Physiology, 593(21), 4713–4727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calin-Jageman, I., Yu, K., Hall, R., Mei, L., & Lee, A. (2007). Erbin enhances voltage-dependent facilitation of Ca(v)1.3 Ca2+ channels through relief of an autoinhibitory domain in the Ca(v)1.3 alpha1 subunit. The Journal of Neuroscience, 27(6), 1374–1385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell, V., Berrow, N. S., Fitzgerald, E. M., Brickley, K., & Dolphin, A. C. (1995). Inhibition of the interaction of G protein G(o) with calcium channels by the calcium channel beta-subunit in rat neurones. The Journal of Physiology, 485, 365–372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canti, C., Page, K. M., Stephens, G. J., & Dolphin, A. C. (1999). Identification of residues in the N terminus of alpha1B critical for inhibition of the voltage-dependent calcium channel by Gbeta gamma. The Journal of Neuroscience, 19, 6855–6864.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canti, C., Bogdanov, Y., & Dolphin, A. C. (2000). Interaction between G proteins and accessory subunits in the regulation of 1B calcium channels in Xenopus oocytes. The Journal of Physiology, 527, 419–432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carabelli, V., Lovallo, M., Magnelli, V., Zucker, H., & Carbone, E. (1996). Voltage-dependent modulation of single N-Type Ca2+ channel kinetics by receptor agonists in IMR32 cells. Biophysical Journal, 70(5), 2144–2154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cataldi, M., Gaudino, A., Lariccia, V., Russo, M., Amoroso, S., Di Renzo, G., et al. (2004). Imatinib-mesylate blocks recombinant T-type calcium channels expressed in human embryonic kidney-293 cells by a protein tyrosine kinase-independent mechanism. The Journal of Pharmacology and Experimental Therapeutics, 309(1), 208–215.

    Article  CAS  PubMed  Google Scholar 

  • Catterall, W. A. (1999). Interactions of presynaptic Ca2+ channels and snare proteins in neurotransmitter release. Annals of the New York Academy of Sciences, 868, 144–159.

    Article  CAS  PubMed  Google Scholar 

  • Catterall, W. A. (2000). Structure and regulation of voltage-gated Ca2+ channels. Annual Review of Cell and Developmental Biology, 16, 521–555.

    Article  CAS  PubMed  Google Scholar 

  • Cesetti, T., Hernández-Guijo, J., Baldelli, P., Carabelli, V., & Carbone, E. (2003). Opposite action of beta1- and beta2-adrenergic receptors on Ca(V)1 L-channel current in rat adrenal chromaffin cells. The Journal of Neuroscience, 23(1), 73–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chemin, J., Monteil, A., Perez-Reyes, E., Nargeot, J., & Lory, P. (2001). Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. The EMBO Journal, 20(24), 7033–7040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chemin, J., Mezghrani, A., Bidaud, I., Dupasquier, S., Marger, F., Barrère, C., et al. (2007). Temperature-dependent modulation of CaV3 T-type calcium channels by protein kinases C and A in mammalian cells. The Journal of Biological Chemistry, 282(45), 32710–32718.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., DeVivo, M., Dingus, J., Harry, A., Li, J., Sui, J., et al. (1995). A region of adenylyl cyclase 2 critical for regulation by G protein beta gamma subunits. Science, 268, 1166–1169.

    Article  CAS  PubMed  Google Scholar 

  • Chen, C., Xu, R., Clarke, I. J., Ruan, M., Loneragan, K., & Roh, S. G. (2000). Diverse intracellular signalling systems used by growth hormone-releasing hormone in regulating voltage-gated Ca2+ or K+ channels in pituitary somatotropes. Immunology and Cell Biology, 78(4), 356–368.

    Article  CAS  PubMed  Google Scholar 

  • Cooper, C., Arnot, M., Feng, Z., Jarvis, S., Hamid, J., & Zamponi, G. (2000). Cross-talk between G-protein and protein kinase C modulation of N-type calcium channels is dependent on the G-protein beta subunit isoform. The Journal of Biological Chemistry, 275(52), 40777–40781.

    Article  CAS  PubMed  Google Scholar 

  • Currie, K. P. M. (2010). G protein inhibition of CaV2 calcium channels. Channels, 4(6), 497–509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Currie, K., & Fox, A. (2002). Differential facilitation of N- and P/Q-type calcium channels during trains of action potential-like waveforms. The Journal of Physiology, 539(2), 419–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Waard, M., Witcher, D., Pragnell, M., Liu, H., & Campbell, K. (1995). Properties of the alpha 1-beta anchoring site in voltage-dependent Ca2+ channels. The Journal of Biological Chemistry, 270(20), 12056–12064.

    Article  PubMed  Google Scholar 

  • De Waard, M., Liu, H., Walker, D., Scott, V. E., Gurnett, C. A., & Campbell, K. P. (1997). Direct binding of G-protein betagamma complex to voltage-dependent calcium channels. Nature, 385, 446–450.

    Article  PubMed  Google Scholar 

  • De Waard, M., Hering, J., Weiss, N., & Feltz, A. (2005). How do G proteins directly control neuronal Ca2+ channel function? Trends in Pharmacological Sciences, 26(8), 427–436.

    Article  PubMed  Google Scholar 

  • Delmas, P., Coste, B., Gamper, N., & Shapiro, M. (2005). Phosphoinositide lipid second messengers: New paradigms for calcium channel modulation. Neuron, 47(2), 179–182.

    Article  CAS  PubMed  Google Scholar 

  • DeMaria, C., Soong, T., Alseikhan, B., Alvania, R., & Yue, D. (2001). Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature, 411(6836), 484–489.

    Article  CAS  PubMed  Google Scholar 

  • DePuy, S. D., Yao, J., Hu, C., McIntire, W., Bidaud, I., Lory, P., et al. (2006). The molecular basis for T-type Ca2+ channel inhibition by G protein beta2gamma2 subunits. Proceedings of the National Academy of Sciences, 103(39), 14590–14595.

    Article  CAS  Google Scholar 

  • Doering, C. J., Kisilevsky, A. E., Feng, Z. P., Arnot, M. I., Peloquin, J., Hamid, J., et al. (2004). A single G beta subunit locus controls cross-talk between protein kinase C and G protein regulation of N-type calcium channels. The Journal of Biological Chemistry, 279, 29709–29717.

    Article  CAS  PubMed  Google Scholar 

  • Dresviannikov, A., Page, K., Leroy, J., Pratt, W., & Dolphin, A. (2009). Determinants of the voltage dependence of G protein modulation within calcium channel beta subunits. Pflügers Archiv, 457(4), 743–756.

    Article  CAS  PubMed  Google Scholar 

  • Drolet, P., Bilodeau, L., Chorvatova, A., Laflamme, L., Gallo-Payet, N., & Payet, M. D. (1997). Inhibition of the T-type Ca2+ current by the dopamine D1 receptor in rat adrenal glomerulosa cells: Requirement of the combined action of the G betagamma protein subunit and cyclic adenosine 3′,5′-monophosphate. Molecular Endocrinology, 11(4), 503–514.

    CAS  PubMed  Google Scholar 

  • Dunlap, K., & Fischbach, G. (1978). Neurotransmitters decrease the calcium ocmponent of sensory neurone action potentials. Nature, 276(5690), 837–839.

    Article  CAS  PubMed  Google Scholar 

  • Elmslie, K. (2003). Neurotransmitter modulation of neuronal calcium channels. Journal of Bioenergetics and Biomembranes, 35(6), 477–489.

    Article  CAS  PubMed  Google Scholar 

  • Elmslie, K. S., & Jones, S. W. (1994). Concentration dependence of neurotransmitter effects on calcium current kinetics in frog sympathetic neurones. The Journal of Physiology, 481, 35–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emrick, M., Sadilek, M., Konoki, K., & Catterall, W. (2010). Beta-adrenergic-regulated phosphorylation of the skeletal muscle Ca(V)1.1 channel in the fight-or-flight response. Proceedings of the National Academy of Sciences of the United States of America, 107(43), 18712–18717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans, R. M., You, H., Hameed, S., Altier, C., Mezghrani, A., Bourinet, E., et al. (2010). Heterodimerization of ORL1 and opioid receptors and its consequences for N-type calcium channel regulation. The Journal of Biological Chemistry, 285(2), 1032–1040.

    Article  CAS  PubMed  Google Scholar 

  • Feng, Z., Arnot, M., Doering, C., & Zamponi, G. (2001). Calcium channel beta subunits differentially regulate the inhibition of N-type channels by individual Gbeta isoforms. The Journal of Biological Chemistry, 276(48), 45051–45058.

    Article  CAS  PubMed  Google Scholar 

  • Fern, R. J., Hahm, M. S., Lu, H. K., Liu, L. P., Gorelick, F. S., & Barrett, P. Q. (1995). Ca2+/calmodulin-dependent protein kinase II activation and regulation of adrenal glomerulosa Ca2+ signaling. The American Journal of Physiology, 269(6), 751–760.

    Google Scholar 

  • Forscher, P., Oxford, G. S., & Schulz, D. (1986). Noradrenaline modulates calcium channels in avian dorsal root ganglion cells through tight receptor-channel coupling. The Journal of Physiology, 379, 131–144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furukawa, T., Ito, H., Nitta, J., Tsujino, M., Adachi, S., Hiroe, M., et al. (1992). Endothelin-1 enhances calcium entry through T-type calcium channels in cultured neonatal rat ventricular myocytes. Circulation Research, 71(5), 1242–1253.

    Article  CAS  PubMed  Google Scholar 

  • Gamper, N., Reznikov, V., Yamada, Y., Yang, J., & Shapiro, M. (2004). Phosphatidylinositol [correction] 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+ channels. The Journal of Neuroscience, 24(48), 10980–10992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray, P., Scott, J., & Catterall, W. (1998). Regulation of ion channels by cAMP-dependent protein kinase and A-kinase anchoring proteins. Current Opinion in Neurobiology, 8(3), 330–334.

    Article  CAS  PubMed  Google Scholar 

  • Grazzini, E., Durroux, T., Payet, M. D., Bilodeau, L., Gallo-Payet, N., & Guillon, G. (1996). Membrane-delimited G protein-mediated coupling between V(1a) vasopressin receptor and dihydropyridine binding sites in rat glomerulosa cells. Molecular Pharmacology, 50(5), 1273–1283.

    CAS  PubMed  Google Scholar 

  • Gross, R. A., Moises, H. C., Uhler, M. D., & Macdonald, R. L. (1990a). Dynorphin a and cAMP-dependent protein kinase independently regulate neuronal calcium currents. Proceedings of the National Academy of Sciences of the United States of America, 87(18), 7025–7029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gross, R. A., Uhler, M. D., & Macdonald, R. L. (1990b). The cyclic AMP-dependent protein kinase catalytic subunit selectively enhances calcium currents in rat nodose neurones. The Journal of Physiology, 429(1), 483–496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haeseleer, F., Imanishi, Y., Maeda, T., Possin, D., Maeda, A., Lee, A., et al. (2004). Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nature Neuroscience, 7(10), 1079–1087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamid, J., Nelson, D., Spaetgens, R., Dubel, S., Snutch, T., & Zamponi, G. (1999). Identification of an integration center for cross-talk between protein kinase C and G protein modulation of N-type calcium channels. The Journal of Biological Chemistry, 274(10), 6195–6202.

    Article  CAS  PubMed  Google Scholar 

  • Harraz, O. F., & Welsh, D. G. (2013). Protein kinase A regulation of T-type Ca2+ channels in rat cerebral arterial smooth muscle. Journal of Cell Science, 126(13), 2944–2954.

    CAS  PubMed  Google Scholar 

  • Harvey, R., & Hell, J. (2013). CaV1.2 signaling complexes in the heart. Journal of Molecular and Cellular Cardiology, 58(1), 143–152.

    Article  CAS  PubMed  Google Scholar 

  • Heidelberger, R., Thoreson, W. B., & Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Progress in Retinal and Eye Research, 24(6), 682–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herlitze, S., Garcia, D. E., Mackie, K., Hille, B., Scheuer, T., & Catterall, W. A. (1996). Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature, 380(6571), 258–262. https://doi.org/10.1038/380258a0

  • Herlitze, S., Hockerman, G. H., Scheuer, T., & Catterall, W. A. (1997). Molecular determinants of inactivation and G protein modulation in the intracellular loop connecting domains I and II of the calcium channel alpha1A subunit. Proceedings of the National Academy of Sciences of the United States of America, 94(4), 1512–1516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herlitze, S., Zhong, H., Scheuer, T., & Catterall, W. A. (2001). Allosteric modulation of Ca2+ channels by G proteins, voltage-dependent facilitation, protein kinase C, and Ca(v)beta subunits. Proceedings of the National Academy of Sciences of the United States of America, 98(8), 4699–4704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hermosilla, T., Moreno, C., Itfinca, M., Altier, C., Armisén, R., Stutzin, A., et al. (2011). L-type calcium channel β subunit modulates angiotensin II responses in cardiomyocytes. Channels (Austin, Tex.), 5(3), 280–286.

    Article  CAS  Google Scholar 

  • Hernádez-López, S., Tkatch, T., Perez-Garci, E., Galarraga, E., Bargas, J., Hamm, H., et al. (2000). D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLCβ1-IP3-Calcineurin-signaling cascade. The Journal of Neuroscience, 20(24), 8987–8995.

    Article  Google Scholar 

  • Hernández-Ochoa, E., García-Ferreiro, R., & García, D. (2007a). G protein activation inhibits gating charge movement in rat sympathetic neurons. American Journal of Physiology. Cell Physiology, 292(6), C2226–C2238.

    Article  PubMed  Google Scholar 

  • Hernández-Ochoa, E., García-Ferreiro, R., & García, D. (2007b). G protein activation inhibits gating charge movement in rat sympathetic neurons. American Journal of Physiology. Cell Physiology, 292(6), 2226–2238.

    Article  Google Scholar 

  • Hildebrand, M. E., David, L. S., Hamid, J., Mulatz, K., Garcia, E., Zamponi, G. W., et al. (2007). Selective inhibition of Cav3.3 T-type calcium channels by Gαq/11-coupled muscarinic acetylcholine receptors. The Journal of Biological Chemistry, 282(29), 21043–21055.

    Article  CAS  PubMed  Google Scholar 

  • Hille, B. (1994). Modulation of ion-channel function by G-protein-coupled receptors. Trends in Neurosciences, 17(12), 531–536.

    Article  CAS  PubMed  Google Scholar 

  • Hille, B., Dickson, E., Kruse, M., Vivas, O., & Suh, B. (2015). Phosphoinositides regulate ion channels. Biochimica et Biophysica Acta, 1851(6), 844–856.

    Article  CAS  PubMed  Google Scholar 

  • Hockberger, P., Toselli, M., Swandulla, D., & Lux, H. D. (1989). A diacylglycerol analogue reduces neuronal calcium currents independently of protein kinase C activation. Nature, 338(6213), 340–342.

    Article  CAS  PubMed  Google Scholar 

  • Howe, A., & Surmeier, D. (1995). Muscarinic receptors modulate N-, P-, and L-type Ca2+ currents in rat striatal neurons through parallel pathways. The Journal of Neuroscience, 15(1), 458–469.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, C., DePuy, S. D., Yao, J., McIntire, W. E., & Barrett, P. Q. (2009). Protein kinase A activity controls the regulation of T-type CaV3.2 channels by Gbetagamma dimers. The Journal of Biological Chemistry, 284(12), 7465–7473.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hulme, J., Ahn, M., Hauschka, S., Scheuer, T., & Catterall, W. (2002). A novel leucine zipper targets AKAP15 and cyclic AMP-dependent protein kinase to the C terminus of the skeletal muscle Ca2+ channel and modulates its function. The Journal of Biological Chemistry, 277(6), 4079–4087.

    Article  CAS  PubMed  Google Scholar 

  • Hümmer, A., Delzeith, O., Gomez, S. R., Moreno, R. L., Mark, M. D., & Herlitze, S. (2003). Competitive and synergistic interactions of G protein beta(2) and Ca(2+) channel beta(1b) subunits with Ca(v)2.1 channels, revealed by mammalian two-hybrid and fluorescence resonance energy transfer measurements. The Journal of Biological Chemistry, 278(49), 49386–49400.

    Article  PubMed  Google Scholar 

  • Iftinca, M., Hamid, J., Chen, L., Varela, D., Tadayonnejad, R., Altier, C., et al. (2007). Regulation of T-type calcium channels by Rho-associated kinase. Nature Neuroscience, 10(7), 854–860.

    Article  CAS  PubMed  Google Scholar 

  • Ikeda, S. R. (1996). Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature, 380(6571), 255–258.

    Article  CAS  PubMed  Google Scholar 

  • Jenkins, M., Christel, C., Jiao, Y., Abiria, S., Kim, K., Usachev, Y., et al. (2010). Ca2+-dependent facilitation of Cav1.3 Ca2+ channels by densin and Ca2+/calmodulin-dependent protein kinase II. The Journal of Neuroscience, 30(15), 5125–5135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson, B., Scheuer, T., & Catterall, W. (2005). Convergent regulation of skeletal muscle Ca2+ channels by dystrophin, the actin cytoskeleton, and cAMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the United States of America, 102(11), 4191–4196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, S. W., & Elmslie, K. S. (1997). Transmitter modulation of neuronal calcium channels. The Journal of Membrane Biology, 155, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Kang, D., Hur, C. G., Park, J. Y., Han, J., & Hong, S. G. (2007). Acetylcholine increases Ca2+ influx by activation of CaMKII in mouse oocytes. Biochemical and Biophysical Research Communications, 360(2), 476–482.

    Article  CAS  PubMed  Google Scholar 

  • Kasai, H. (1992). Voltage- and time-dependent inhibition of neuronal calcium channels by a GTP-binding protein in a mammalian cell line. The Journal of Physiology, 448(1), 189–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katchman, A., Yang, L., Zakharov, S. I., Kushner, J., Abrams, J., Chen, B. X., et al. (2017). Proteolytic cleavage and PKA phosphorylation of α1C subunit are not required for adrenergic regulation of CaV1.2 in the heart. Proceedings of the National Academy of Sciences of the United States of America, 114(34), 9194–9199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katz, M., Subramaniam, S., Chomsky-Hecht, O., Tsemakhovich, V., Flockerzi, V., Klussmann, E., et al. (2021). Reconstitution of β-adrenergic regulation of Ca V 1.2: Rad-dependent and Rad-independent protein kinase A mechanisms. Proceedings of the National Academy of Sciences of the United States of America, 118(21), e2100021118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur, G., Pinggera, A., Ortner, N., Lieb, A., Sinnegger-Brauns, M., Yarov-Yarovoy, V., et al. (2015). A polybasic plasma membrane binding motif in the I-II linker stabilizes voltage-gated CaV1.2 calcium channel function. The Journal of Biological Chemistry, 290(34), 21086–21100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawai, F., & Miyachi, E. I. (2001). Modulation by cGMP of the voltage-gated currents in newt olfactory receptor cells. Neuroscience Research, 39(3), 327–337.

    Article  CAS  PubMed  Google Scholar 

  • Kawai, F., Kurahashi, T., & Kaneko, A. (1999). Adrenaline enhances odorant contrast by modulating signal encoding in olfactory receptor cells. Nature Neuroscience, 2(2), 133–138.

    Article  CAS  PubMed  Google Scholar 

  • Keja, J. A., Stoof, J. C., & Kits, K. S. (1992). Dopamine D2 receptor stimulation differentially affects voltage-activated calcium channels in rat pituitary melanotropic cells. The Journal of Physiology, 450(1), 409–435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, J. A., Park, J. Y., Kang, H. W., Huh, S. U., Jeong, S. W., & Lee, J. H. (2006). Augmentation of Cav3.2 T-type calcium channel activity by cAMP-dependent protein kinase A. The Journal of Pharmacology and Experimental Therapeutics, 318(1), 230–237.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H. H., Lee, K. H., Lee, D., Han, Y. E., Lee, S. H., Sohn, J. W., & Ho, W. K. (2015). Costimulation of AMPA and metabotropic glutamate receptors underlies phospholipase C activation by glutamate in hippocampus. The Journal of Neuroscience, 35(16), 6401–6412. https://doi.org/10.1523/JNEUROSCI.4208-14.2015

  • Kim, Y., Park, M. K., Uhm, D. Y., & Chung, S. (2007). Modulation of T-type Ca2+ channels by corticotropin-releasing factor through protein kinase C pathway in MN9D dopaminergic cells. Biochemical and Biophysical Research Communications, 358(3), 796–801.

    Article  CAS  PubMed  Google Scholar 

  • Kitano, J., Nishida, M., Itsukaichi, Y., Minami, I., Ogawa, M., Hirano, T., et al. (2003). Direct interaction and functional coupling between metabotropic glutamate receptor subtype 1 and voltage-sensitive Cav2.1 Ca2+ channel. The Journal of Biological Chemistry, 278(27), 25101–25108.

    Article  CAS  PubMed  Google Scholar 

  • Kobrinsky, E. M., Pearson, H. A., & Dolphin, A. C. (1994). Low- and high-voltage-activated calcium channel currents and their modulation in the dorsal root ganglion cell line ND7-23. Neuroscience, 58(3), 539–552.

    Article  CAS  PubMed  Google Scholar 

  • Kurejová, M., & Lacinová, L. (2006 Feb). Effect of protein tyrosine kinase inhibitors on the current through the CaV3.1 channel. Archives of Biochemistry and Biophysics, 446(1), 20–27.

    Article  PubMed  Google Scholar 

  • Lacinova, L., Mallmann, R. T., Jurkovičová-Tarabová, B., & Klugbauer, N. (2020). Modulation of voltage-gated CaV2.2 Ca2+ channels by newly identified interaction partners. Channels, 14(1), 380–392.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, H. K., & Elmslie, K. S. (2000). Reluctant gating of single N-type calcium channels during neurotransmitter-induced inhibition in bullfrog sympathetic neurons. The Journal of Neuroscience, 20, 3115–3128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, A., Wong, S. T., Gallagher, D., Li, B., Storm, D. R., Scheuer, T., et al. (1999). Ca2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature, 399(6732), 155–159.

    Article  CAS  PubMed  Google Scholar 

  • Lee, A., Scheuer, T., & Catterall, W. A. (2000). Ca2+/calmodulin-dependent facilitation and inactivation of P/Q-type Ca2+ channels. The Journal of Neuroscience, 20(18), 6830–6838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemke, T., Welling, A., Christel, C. J., Blaich, A., Bernhard, D., Lenhardt, P., et al. (2008). Unchanged β-adrenergic stimulation of cardiac L-type calcium channels in Cav1.2 phosphorylation site S1928A mutant mice. The Journal of Biological Chemistry, 283(50), 34738–34744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenglet, S., Louiset, E., Delarue, C., Vaudry, H., & Contesse, V. (2002). Activation of 5-HT(7) receptor in rat glomerulosa cells is associated with an increase in adenylyl cyclase activity and calcium influx through T-type calcium channels. Endocrinology, 143(5), 1748–1760.

    Article  CAS  PubMed  Google Scholar 

  • Leroy, J., Richards, M., Butcher, A., Nieto-Rostro, M., Pratt, W., Davies, A., et al. (2005). Interaction via a key tryptophan in the I-II linker of N-type calcium channels is required for beta1 but not for palmitoylated beta2, implicating an additional binding site in the regulation of channel voltage-dependent properties. The Journal of Neuroscience, 25(30), 6984–6996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y., Wang, F., Zhang, X., Qi, Z., Tang, M., Szeto, C., et al. (2012). ß-Adrenergic stimulation increases Cav3.1 activity in cardiac myocytes through protein kinase A. PLoS One, 7(7), e39965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Q., Zhang, Y., Wu, N., Yin, N., Sun, X. H., & Wang, Z. (2019). Activation of somatostatin receptor 5 suppresses T-type Ca2+ channels through NO/cGMP/PKG signaling pathway in rat retinal ganglion cells. Neuroscience Letters, 708, 134337.

    Article  CAS  PubMed  Google Scholar 

  • Lin, Z., Haus, S., Edgerton, J., & Lipscombe, D. (1997). Identification of functionally distinct isoforms of the N-type Ca2+ channel in rat sympathetic ganglia and brain. Neuron, 18, 153–166.

    Article  CAS  PubMed  Google Scholar 

  • Liu, B., Hill, S. J., & Khan, R. N. (2005). Oxytocin inhibits T-type calcium current of human decidual stromal cells. The Journal of Clinical Endocrinology and Metabolism, 90(7), 4191–4197.

    Article  CAS  PubMed  Google Scholar 

  • Liu, K., Jiang, D., Zhang, T., Tao, J., Shen, L., & Sun, X. (2011). Activation of growth hormone secretagogue type 1a receptor inhibits T-type Ca2+ channel currents through pertussis toxin-sensitive novel protein kinase C pathway in mouse spermatogenic cells. Cellular Physiology and Biochemistry, 27(5), 613–624.

    Article  PubMed  Google Scholar 

  • Liu, G., Papa, A., Katchman, A., Zakharov, S., Roybal, D., Hennessey, J., et al. (2020). Mechanism of adrenergic Ca V 1.2 stimulation revealed by proximity proteomics. Nature, 577(7792), 695–700.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lledo, P. M., Israel, J. M., & Vincent, J. D. (1990a). A guanine nucleotide-binding protein mediates the inhibition of voltage-dependent calcium currents by dopamine in rat lactotrophs. Brain Research, 528(1), 143–147.

    Article  CAS  PubMed  Google Scholar 

  • Lledo, P. M., Legendre, P., Israel, J. M., & Vincent, J. D. (1990b). Dopamine inhibits two characterized voltage-dependent calcium currents in identified rat lactotroph cells. Endocrinology, 127(3), 990–1001.

    Article  CAS  PubMed  Google Scholar 

  • Lledo, P. M., Homburger, V., Bockaert, J., & Vincent, J. D. (1992). Differential G protein-mediated coupling of D2 dopamine receptors to K+ and Ca2+ currents in rat anterior pituitary cells. Neuron, 8(3), 455–463.

    Article  CAS  PubMed  Google Scholar 

  • Louiset, E., Duparc, C., Lenglet, S., Gomez-Sanchez, C. E., & Lefebvre, H. (2017). Role of cAMP/PKA pathway and T-type calcium channels in the mechanism of action of serotonin in human adrenocortical cells. Molecular and Cellular Endocrinology, 441, 99–107.

    Article  CAS  PubMed  Google Scholar 

  • Lu, H. K., Fern, R. J., Nee, J. J., & Barrett, P. Q. (1994). Ca2+-dependent activation of T-type Ca2+ channels by calmodulin- dependent protein kinase II. The American Journal of Physiology, 267(1), 183–189.

    Google Scholar 

  • Lu, H. K., Fern, R. J., Luthin, D., Linden, J., Liu, L. P., Cohen, C. J., et al. (1996). Angiotensin II stimulates T-type Ca2+ channel currents via activation of a G protein, G(i). The American Journal of Physiology, 271(4), 1340–1349.

    Article  Google Scholar 

  • Mahapatra, S., Calorio, C., Vandael, D., Marcantoni, A., Carabelli, V., & Carbone, E. (2012). Calcium channel types contributing to chromaffin cell excitability, exocytosis and endocytosis. Cell Calcium, 51(3–4), 321–330.

    Article  CAS  PubMed  Google Scholar 

  • Mandy, L. R. C., & Rittenhouse, A. R. (2009). Arachidonic acid inhibition of L-type calcium (Ca V 1.3b) channels varies with accessory Ca Vβ subunits. The Journal of General Physiology, 133(4), 387–403.

    Article  Google Scholar 

  • Marchetti, C., & Brown, A. M. (1988). Protein kinase activator 1-oleoyl-2-acetyl-sn-glycerol inhibits two types of calcium currents in GH3 cells. The American Journal of Physiology, 254(1), 206–210.

    Article  Google Scholar 

  • Marchetti, C., Carbone, E., & Lux, H. D. (1986). Effects of dopamine and noradrenaline on Ca channels of cultured sensory and sympathetic neurons of chick. Pflügers Archiv, 406(2), 104–111.

    Article  CAS  PubMed  Google Scholar 

  • Margeta-Mitrovic, M., Grigg, J. J., Koyano, K., Nakajima, Y., & Nakajima, S. (1997). Neurotensin and substance P inhibit low- and high-voltage-activated Ca2+ channels in cultured newborn rat nucleus basalis neurons. Journal of Neurophysiology, 78(3), 1341–1352.

    Article  CAS  PubMed  Google Scholar 

  • Mark, M. D., Wittemann, S., & Herlitze, S. (2000). G protein modulation of recombinant P/Q-type calcium channels by regulators of G protein signalling proteins. The Journal of Physiology, 528(1), 65–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masland, R. (2012). The neuronal organization of the retina. Neuron, 76(2), 266–280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masuho, I., Skamangas, N., Muntean, B., & Martemyanov, K. (2021). Diversity of the Gβγ complexes defines spatial and temporal bias of GPCR signaling. Cell Systems, 12(4), 324–337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCarthy, R. T., Isales, C., & Rasmussen, H. (1993). T-type calcium channels in adrenal glomerulosa cells: GTP-dependent modulation by angiotensin II. Proceedings of the National Academy of Sciences of the United States of America, 90(8), 3260–3264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meves, H. (2005). The effect of prostaglandin E1 on ion currents of NG108-15 cells. Prostaglandins & Other Lipid Mediators, 76(1–4), 117–132.

    Article  CAS  Google Scholar 

  • Meza, U., & Adams, B. (1998). G-Protein-dependent facilitation of neuronal alpha1A, alpha1B, and alpha1E Ca channels. The Journal of Neuroscience, 18(14), 5240–5252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mochida, S. (2018). Presynaptic calcium channels. Neuroscience Research, 127, 33–44.

    Article  CAS  PubMed  Google Scholar 

  • Morikawa, H., Fukuda, K., Mima, H., Shoda, T., Kato, S., & Mori, K. (1998). Tyrosine kinase inhibitors suppress N-type and T-type Ca2+ channel currents in NG108-15 cells. Pflügers Archiv, 436(1), 127–132.

    Article  CAS  PubMed  Google Scholar 

  • Murali, S., Napier, I., Rycroft, B., & Christie, M. (2012). Opioid-related (ORL1) receptors are enriched in a subpopulation of sensory neurons and prolonged activation produces no functional loss of surface N-type calcium channels. The Journal of Physiology, 590(7), 1655–1667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy, B., & Scott, J. (1998). Functional anchoring of the cAMP-dependent protein kinase. Trends in Cardiovascular Medicine, 8(2), 89–95.

    Article  CAS  PubMed  Google Scholar 

  • Nanou, E., & Catterall, W. (2018). Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron, 98(3), 466–481.

    Article  CAS  PubMed  Google Scholar 

  • Nussinovitch, I., & Kleinhaus, A. L. (1992). Dopamine inhibits voltage-activated calcium channel currents in rat pars intermedia pituitary cells. Brain Research, 574(1–2), 49–55.

    Article  CAS  PubMed  Google Scholar 

  • Okamura, Y., Murata, Y., & Iwasaki, H. (2009). Voltage-sensing phosphatase: Actions and potentials. The Journal of Physiology, 587(3), 513–520.

    Article  CAS  PubMed  Google Scholar 

  • Oldham, W., & Hamm, H. (2008). Heterotrimeric G protein activation by G-protein-coupled receptors. Nature Reviews. Molecular Cell Biology, 9(1), 60–71.

    Article  CAS  PubMed  Google Scholar 

  • Olson, P. A., Tkatch, T., Hernandez-Lopez, S., Ulrich, S., Ilijic, E., Mugnaini, E., et al. (2005). G-protein-coupled receptor modulation of striatal Cav1.3 L-type Ca2+ channels is dependent on a shank-binding domain. The Journal of Neuroscience, 25(5), 1050–1062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osipenko, O. N., Várnai, P., Mike, A., Spät, A., & Vizi, E. S. (1994). Dopamine blocks T-type calcium channels in cultured rat adrenal. Endocrinology, 134(1), 511–514.

    Article  CAS  PubMed  Google Scholar 

  • Page, K., Cantí, C., Stephens, G., Berrow, N., & Dolphin, A. (1998). Identification of the amino terminus of neuronal Ca2+ channel alpha1 subunits alpha1B and alpha1E as an essential determinant of G-protein modulation. The Journal of Neuroscience, 18(13), 4815–4824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page, K., Heblich, F., Margas, W., Pratt, W., Nieto-Rostro, M., Chaggar, K., et al. (2010). N terminus is key to the dominant negative suppression of Ca(V)2 calcium channels: Implications for episodic ataxia type 2. The Journal of Biological Chemistry, 285(2), 835–844.

    Article  CAS  PubMed  Google Scholar 

  • Pan, J. Q., & Lipscombe, D. (2000). Alternative splicing in the cytoplasmic II-III loop of the N-type Ca channel alpha 1B subunit: Functional differences are beta subunit-specific. The Journal of Neuroscience, 20, 4769–4775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papa, A., Kushner, J., Hennessey, J. A., Katchman, A. N., Zakharov, S. I., Chen, B. X., et al. (2021). Adrenergic CaV1.2 activation via Rad phosphorylation converges at α1CI-II loop. Circulation Research, 128(1), 76–88.

    Article  CAS  PubMed  Google Scholar 

  • Park, J. Y., Jeong, S. W., Perez-Reyes, E., & Lee, J. H. (2003). Modulation of Cav3.2 T-type Ca2+ channels by protein kinase C. FEBS Letters, 547(1–3), 37–42.

    Article  CAS  PubMed  Google Scholar 

  • Park, J. Y., Kang, H. W., Moon, H. J., Huh, S. U., Jeong, S. W., Soldatov, N. M., et al. (2006). Activation of protein kinase C augments T-type Ca2+ channel activity without changing channel surface density. The Journal of Physiology, 577(2), 513–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patriarchi, T., Qian, H., Di Biase, V., Malik, Z., Chowdhury, D., Price, J., et al. (2016). Phosphorylation of Cav1.2 on S1928 uncouples the L-type Ca2+ channel from the β2 adrenergic receptor. The EMBO Journal, 35(12), 1330–1345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patriarchi, T., Buonarati, O., & Hell, J. (2018). Postsynaptic localization and regulation of AMPA receptors and Cav1.2 by β2 adrenergic receptor/PKA and Ca 2+/CaMKII signaling. The EMBO Journal, 37(20), e99771.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pemberton, K., Hill-Eubanks, L., & Penelope, J. S. (2000). Modulation of low-threshold T-type calcium channels by the five muscarinic receptor subtypes in NIH 3T3 cells. Pflügers Archiv, 440(3), 452–461.

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer-Linn, C., & Lasater, E. M. (1993). Dopamine modulates in a differential fashion T- and L-type calcium currents in bass retinal horizontal cells. The Journal of General Physiology, 102(2), 277–294.

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer-Linn, C. L., & Lasater, E. M. (1998). Multiple second-messenger system modulation of voltage-activated calcium currents in teleost retinal horizontal cells. Journal of Neurophysiology, 80(1), 377–388.

    Article  CAS  PubMed  Google Scholar 

  • Polo-Parada, L., Chan, S. A., & Smith, C. (2006). An activity-dependent increased role for L-type calcium channels in exocytosis is regulated by adrenergic signaling in chromaffin cells. Neuroscience, 143(2), 445–459.

    Article  CAS  PubMed  Google Scholar 

  • Pragnell, M., Sakamoto, J., Jay, S. D., & Campbell, K. P. (1991). Cloning and tissue-specific expression of the brain calcium channel beta-subunit. FEBS Letters, 291, 253–258.

    Article  CAS  PubMed  Google Scholar 

  • Pragnell, M., De Waard, M., Mori, Y., Tanabe, T., Snutch, T. P., & Campbell, K. P. (1994). Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit. Nature, 368, 67–70.

    Article  CAS  PubMed  Google Scholar 

  • Proft, J., & Weiss, N. (2015). G protein regulation of neuronal calcium channels: Back to the future. Molecular Pharmacology, 87(6), 890–906.

    Article  CAS  PubMed  Google Scholar 

  • Qian, W.-J., Yin, N., Gao, F., Miao, Y., Li, Q., Li, F., et al. (2017). Cannabinoid CB1 and CB2 receptors differentially modulate L- and T-type Ca2+ channels in rat retinal ganglion cells. Neuropharmacology, 124, 143–156.

    Article  CAS  PubMed  Google Scholar 

  • Qin, N., Platano, D., Olcese, R., Stefani, E., & Birnbaumer, L. (1997). Direct interaction of gbetagamma with a C-terminal Gbetagamma-binding domain of the Ca2+ channel alpha1 subunit is responsible for channel inhibition by G protein-coupled receptors. Proceedings of the National Academy of Sciences of the United States of America, 94, 8866–8871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rangel, A., Sánchez-Armass, S., & Meza, U. (2010). Protein kinase C-mediated inhibition of recombinant T-type CaV3.2 channels by neurokinin 1 receptors. Molecular Pharmacology, 77(2), 202–210.

    Article  CAS  PubMed  Google Scholar 

  • Rebolledo-Antúnez, S., Farías, J., Arenas, I., & García, D. (2009). Gating charges per channel of Ca(V)2.2 channels are modified by G protein activation in rat sympathetic neurons. Archives of Biochemistry and Biophysics, 486(1), 51–57.

    Article  PubMed  Google Scholar 

  • Rettig, J., Sheng, Z. H., Kim, D. K., Hodson, C. D., Snutch, T. P., & Catterall, W. A. (1996). Isoform-specific interaction of the alpha1A subunits of brain Ca2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proceedings of the National Academy of Sciences of the United States of America, 93, 7363–7368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts-Crowley, M., & Rittenhouse, A. (2018). Modulation of Ca V 1.3b L-type calcium channels by M 1 muscarinic receptors varies with Ca V β subunit expression. BMC Research Notes, 11(1), 681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenthal, W., Hescheler, J., Eckert, R., Offermanns, S., Schmidt, A., Hinsch, K. D., et al. (1990). Pertussis toxin-sensitive G-proteins: Participation in the modulation of voltage-dependent Ca2+ channels by hormones and neurotransmitters. Advances in Second Messenger and Phosphoprotein Research, 24, 89–94.

    CAS  PubMed  Google Scholar 

  • Rossier, M. F., Aptel, H. B. C., Python, C. P., Burnay, M. M., Vallotton, M. B., & Capponi, A. M. (1995). Inhibition of low threshold calcium channels by angiotensin II in adrenal glomerulosa cells through activation of protein kinase C. The Journal of Biological Chemistry, 270(25), 15137–15142.

    Article  CAS  PubMed  Google Scholar 

  • Roybal, D., Hennessey, J. A., & Marx, S. O. (2020). The quest to identify the mechanism underlying adrenergic regulation of cardiac Ca2+ channels. Channels, 14(1), 123.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanderson, J., & Dell’Acqua, M. (2011). AKAP signaling complexes in regulation of excitatory synaptic plasticity. The Neuroscientist, 17(3), 321–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandoval, A., Duran, P., Gandini, M., Andrade, A., Almanza, A., Kaja, S., et al. (2017). Regulation of L-type Ca V 1.3 channel activity and insulin secretion by the cGMP-PKG signaling pathway. Cell Calcium, 66, 1–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sang, L., Dick, I., & Yue, D. (2016). Protein kinase A modulation of CaV1.4 calcium channels. Nature Communications, 7, 12239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt, H., & Meves, H. (1995). Modulation of neuronal calcium channels by arachidonic acid and related substances. The Journal of Membrane Biology, 145(3), 233–244.

    Article  CAS  PubMed  Google Scholar 

  • Schrier, A. D., Wang, H., Talley, E. M., Perez-Reyes, E., & Barrett, P. Q. (2001). α1H T-type Ca2+ channel is the predominant subtype expressed in bovine and rat zona glomerulosa. The American Journal of Physiology, 280(2), 265–272.

    Article  Google Scholar 

  • Schroeder, J. E., & McCleskey, E. W. (1993). Inhibition of Ca2+ currents by a μ-opioid in a defined subset of rat sensory neurons. The Journal of Neuroscience, 13(2), 867–873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeder, J. E., Fischbach, P. S., & McCleskey, E. W. (1990). T-type calcium channels: Heterogeneous expression in rat sensory neurons and selective modulation by phorbol esters. The Journal of Neuroscience, 10(3), 947–951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeder, J. E., Fischbach, P. S., Zheng, D., & McCleskey, E. W. (1991). Activation of μ opioid receptors inhibits transient high- and low-threshold Ca 2+ currents, but spares a sustained current. Neuron, 6(1), 13–20.

    Article  CAS  PubMed  Google Scholar 

  • Scott, R. H., Wootton, J. F., & Dolphin, A. C. (1990). Modulation of neuronal T-type calcium channel currents by photoactivation of intracellular guanosine 5′-0(3-thio) triphosphate. Neuroscience, 38(2), 285–294.

    Article  CAS  PubMed  Google Scholar 

  • Sekiguchi, F., Aoki, Y., Nakagawa, M., Kanaoka, D., Nishimoto, Y., Tsubota-Matsunami, M., et al. (2013). AKAP-dependent sensitization of Cav3.2 channels via the EP 4 receptor/cAMP pathway mediates PGE2-induced mechanical hyperalgesia. British Journal of Pharmacology, 168(3), 734–745.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shan, H. Q., Hammarback, J. A., & Godwin, D. W. (2013). Ethanol inhibition of a T-type Ca2+ channel through activity of protein kinase C. Alcoholism, Clinical and Experimental Research, 37(8), 1333–1342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng, Z. H., Rettig, J., Takahashi, M., & Catterall, W. A. (1994). Identification of a syntaxin-binding site on N-type calcium channels. Neuron, 13, 1303–1313.

    Article  CAS  PubMed  Google Scholar 

  • Sheng, Z. H., Westenbroek, R. E., & Catterall, W. A. (1998). Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. Journal of Bioenergetics and Biomembranes, 30(4), 335–345.

    Article  CAS  PubMed  Google Scholar 

  • Si, W., Zhang, Y., Chen, K., Hu, D., Qian, Z., Gong, S., et al. (2018). Fibroblast growth factor type 1 receptor stimulation of T-type Ca 2+ channels in sensory neurons requires the phosphatidylinositol 3-kinase and protein kinase A pathways, independently of Akt. Cellular Signalling, 45, 93–101.

    Article  CAS  PubMed  Google Scholar 

  • Stanika, R., Flucher, B., & Obermair, G. (2015). Regulation of postsynaptic stability by the L-type calcium channel CaV1.3 and its interaction with PDZ proteins. Current Molecular Pharmacology, 8(1), 95–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stella, S. L., Hu, W. D., Vila, A., & Brecha, N. C. (2007). Adenosine inhibits voltage-dependent Ca2+ influx in cone photoreceptor terminals of the tiger salamander retina. Journal of Neuroscience Research, 85(5), 1126–1137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stotz, S., & Zamponi, G. (2001). Structural determinants of fast inactivation of high voltage-activated Ca(2+) channels. Trends in Neurosciences, 24(3), 176–182.

    Article  CAS  PubMed  Google Scholar 

  • Suh, B., Leal, K., & Hille, B. (2010). Modulation of high-voltage activated Ca(2+) channels by membrane phosphatidylinositol 4,5-bisphosphate. Neuron, 67(2), 224–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suh, B., Kim, D., Falkenburger, B., & Hille, B. (2012). Membrane-localized β-subunits alter the PIP2 regulation of high-voltage activated Ca2+ channels. Proceedings of the National Academy of Sciences of the United States of America, 109(8), 3161–3166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swartz, K. (1993). Modulation of Ca2+ channels by protein kinase C in rat central and peripheral neurons: Disruption of G protein-mediated inhibition. Neuron, 11(2), 305–320.

    Article  CAS  PubMed  Google Scholar 

  • Talavera, K., Staes, M., Janssens, A., Droogmans, G., & Nilius, B. (2004). Mechanism of arachidonic acid modulation of the T-type Ca2+ channel α1G. The Journal of General Physiology, 124(3), 225–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao, J., Hildebrand, M. E., Liao, P., Mui, C. L., Tan, G., Li, S., et al. (2008). Activation of corticotropin-releasing factor receptor 1 selectively inhibits CaV3.2 T-type calcium channels. Molecular Pharmacology, 73(6), 1596–1609.

    Article  CAS  PubMed  Google Scholar 

  • Tao, J., Zhang, Y., Li, S., Sun, W., & Soong, T. W. (2009). Tyrosine kinase-independent inhibition by genistein on spermatogenic T-type calcium channels attenuates mouse sperm motility and acrosome reaction. Cell Calcium, 45(2), 133–143.

    Article  CAS  PubMed  Google Scholar 

  • Tedford, H. W., Kisilevsky, A. E., Vieira, L. B., Varela, D., Chen, L., & Zamponi, G. W. (2010). Scanning mutagenesis of the I-II loop of the Cav2.2 calcium channel identifies residues Arginine 376 and Valine 416 as molecular determinants of voltage dependent G protein inhibition. Molecular Brain, 3, 6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tennakoon, M., Senarath, K., Kankanamge, D., Ratnayake, K., Wijayaratna, D., Olupothage, K., et al. (2021). Subtype-dependent regulation of Gβγ signalling. Cellular Signalling, 82, 109947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thoreson, W. B. (2021). Transmission at rod and cone ribbon synapses in the retina. Pflügers Archiv, 473(9), 1469–1491.

    Article  CAS  PubMed  Google Scholar 

  • Toselli, M., & Lux, H. D. (1989). Opposing effects of acetylcholine on the two classes of voltage-dependent calcium channels in hippocampal neurons. EXS, 57, 97–103.

    CAS  PubMed  Google Scholar 

  • Tseng, G. N., & Boyden, P. A. (1991). Different effects of intracellular Ca and protein kinase C on cardiac T and L Ca currents. The American Journal of Physiology, 261(2), 364–379.

    Google Scholar 

  • Vandael, D. H. F., Mahapatra, S., Calorio, C., Marcantoni, A., & Carbone, E. (2013). Cav1.3 and Cav1.2 channels of adrenal chromaffin cells: Emerging views on cAMP/cGMP-mediated phosphorylation and role in pacemaking. Biochimica et Biophysica Acta, 1828(7), 1608–1618.

    Article  CAS  PubMed  Google Scholar 

  • Waldner, D., Bech-Hansen, N., & Stell, W. (2018). Channeling vision: Ca V 1.4-A critical link in retinal signal transmission. BioMed Research International, 2018, 7272630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, F., Zhang, Y., Jiang, X., Zhang, Y., Zhang, L., Gong, S., et al. (2011). Neuromedin U inhibits T-type Ca2+ channel currents and decreases membrane excitability in small dorsal root ganglia neurons in mice. Cell Calcium, 49(1), 12–22.

    Article  PubMed  Google Scholar 

  • Wang, H., Wei, Y., Pu, Y., Jiang, D., Jiang, X., Zhang, Y., et al. (2019). Brain-derived neurotrophic factor stimulation of T-type Ca2+ channels in sensory neurons contributes to increased peripheral pain sensitivity. Science Signaling, 12(600), eaaw2300.

    Article  CAS  PubMed  Google Scholar 

  • Weiss, S., & Dascal, N. (2015). Molecular aspects of modulation of L-type calcium channels by protein kinase C. Current Molecular Pharmacology, 8(1), 43–53.

    Article  CAS  PubMed  Google Scholar 

  • Weiss, N., Tadmouri, A., Mikati, M., Ronjat, M., & De Waard, M. (2007). Importance of voltage-dependent inactivation in N-type calcium channel regulation by G-proteins. Pflügers Archiv, 454(1), 115–129.

    Article  CAS  PubMed  Google Scholar 

  • Welsby, P. J., Wang, H., Wolfe, J. T., Colbran, R. J., Johnson, M. L., & Barrett, P. Q. (2003). A mechanism for the direct regulation of T-type calcium channels by Ca 2+/calmodulin-dependent kinase II. The Journal of Neuroscience, 23(31), 10116–10121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wettschureck, N., & Offermanns, S. (2005). Mammalian G proteins and their cell type specific functions. Physiological Reviews, 85(4), 1159–1204.

    Article  CAS  PubMed  Google Scholar 

  • Williams, P. J., MacVicar, B. A., & Pittman, Q. J. (1990). Synaptic modulation by dopamine of calcium currents in rat pars intermedia. The Journal of Neuroscience, 10(3), 757–763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Witcher, D., De Waard, M., Liu, H., Pragnell, M., & Campbell, K. (1995). Association of native Ca2+ channel beta subunits with the alpha 1 subunit interaction domain. The Journal of Biological Chemistry, 270(30), 18088–18093.

    Article  CAS  PubMed  Google Scholar 

  • Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica, 108(1), 17–39.

    Article  PubMed  Google Scholar 

  • Wolfe, J. T., Wang, H., Perez-Reyes, E., & Barrett, P. Q. (2002). Stimulation of recombinant CaV3.2, T-type, Ca2+ channel currents by CaMKIIγC. The Journal of Physiology, 538(2), 343–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe, J. T., Wang, H., Howard, J., Garrison, J. C., & Barrett, P. Q. (2003). T-type calcium channel regulation by specific G-protein betagamma subunits. Nature, 424(6945), 209–213.

    Article  CAS  PubMed  Google Scholar 

  • Wu, X., Kushwaha, N., Albert, P., & Penington, N. (2002). A critical protein kinase C phosphorylation site on the 5-HT(1A) receptor controlling coupling to N-type calcium channels. The Journal of Physiology, 538(1), 41–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao, R., Zhu, W., Zheng, M., Chakir, K., Bond, R., Lakatta, E., et al. (2004). Subtype-specific beta-adrenoceptor signaling pathways in the heart and their potential clinical implications. Trends in Pharmacological Sciences, 25(7), 358–365.

    Article  CAS  PubMed  Google Scholar 

  • Yu, H., Seo, J. B., Jung, S. R., Koh, D. S., & Hille, B. (2015). Noradrenaline upregulates T-type calcium channels in rat pinealocytes. The Journal of Physiology, 593(4), 887–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue, J., Zhang, Y., Li, X., Gong, S., Tao, J., & Jiang, X. (2014). Activation of G-protein-coupled receptor 30 increases t-type calcium currents in trigeminal ganglion neurons via the cholera toxin-sensitive protein kinase a pathway. Die Pharmazie, 69(11), 804–808.

    CAS  PubMed  Google Scholar 

  • Zamponi, G., & Currie, K. (2013). Regulation of Ca(V)2 calcium channels by G protein coupled receptors. Biochimica et Biophysica Acta, 1828(7), 1629–1643.

    Article  CAS  PubMed  Google Scholar 

  • Zamponi, G. W., & Snutch, T. P. (1998). Modulation of voltage-dependent calcium channels by G proteins. Current Opinion in Neurobiology, 8, 351–356.

    Article  CAS  PubMed  Google Scholar 

  • Zamponi, G. W., Bourinet, E., Nelson, D., Nargeot, J., & Snutch, T. P. (1997). Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature, 385, 442–446.

    Article  CAS  PubMed  Google Scholar 

  • Zamponi, G., Striessnig, J., Koschak, A., & Dolphin, A. (2015). The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacological Reviews, 67(4), 821–870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Cribbs, L. L., & Satin, J. (2000). Arachidonic acid modulation of α1H, a cloned human T-type calcium channel. The American Journal of Physiology, 278(1), 184–193.

    Google Scholar 

  • Zhang, Y., Zhang, L., Wang, F., Zhang, Y., Wang, J., Qin, Z., et al. (2011). Activation of M3 muscarinic receptors inhibits T-type Ca2+ channel currents via pertussis toxin-sensitive novel protein kinase C pathway in small dorsal root ganglion neurons. Cellular Signalling, 23(6), 1057–1067.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Zhang, Y., Jiang, D., Reid, P. F., Jang, X., Qin, Z., et al. (2012). Alpha-cobratoxin inhibits T-type calcium currents through muscarinic M4 receptor and G o-protein βγ subunits-dependent protein kinase A pathway in dorsal root ganglion neurons. Neuropharmacology, 62(2), 1062–1072.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Qin, W., Qian, Z., Liu, X., Wang, H., Gong, S., et al. (2014). Peripheral pain is enhanced by insulin-like growth factor 1 through a G protein-mediated stimulation of T-type calcium channels. Science Signaling, 7(346), ra94.

    Article  PubMed  Google Scholar 

  • Zhang, Y., Ji, H., Wang, J., Sun, Y., Qian, Z., Jiang, X., et al. (2018). Melatonin-mediated inhibition of Cav3.2 T-type Ca2+ channels induces sensory neuronal hypoexcitability through the novel protein kinase C-eta isoform. Journal of Pineal Research, 64(4), 12476.

    Article  Google Scholar 

  • Zühlke, R., Pitt, G., Tsien, R., & Reuter, H. (2000). Ca2+-sensitive inactivation and facilitation of L-type Ca2+ channels both depend on specific amino acid residues in a consensus calmodulin-binding motif in the(alpha)1C subunit. The Journal of Biological Chemistry, 275(28), 21121–21129.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Behavioral Neuroscience, Ruhr-University Bochum, Bochum, Germany

    Melanie D. Mark & Jan Claudius Schwitalla

  2. Department of Zoology and Neurobiology, Ruhr-University Bochum, Bochum, Germany

    Stefan Herlitze

Authors
  1. Melanie D. Mark
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Claudius Schwitalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefan Herlitze
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada

    Gerald Werner Zamponi

  2. Department of Pathophysiology, Third Faculty of Medicine, Charles University, Prague, Czech Republic

    Norbert Weiss

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Mark, M.D., Schwitalla, J.C., Herlitze, S. (2022). Modulation of VGCCs by G-Protein Coupled Receptors and Their Second Messengers. In: Zamponi, G.W., Weiss, N. (eds) Voltage-Gated Calcium Channels . Springer, Cham. https://doi.org/10.1007/978-3-031-08881-0_7

Download citation

Publish with us

Policies and ethics

Search

Navigation