1,263
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Dopamine-mediated calcium channel regulation in synaptic suppression in L. stagnalis interneurons

, , &
Pages 153-173 | Received 19 Dec 2017, Accepted 21 Mar 2018, Published online: 08 May 2018

References

  • Altschul SF, Madden TL, Schäffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. doi:10.1093/nar/25.17.3389
  • Arnot MI, Stotz SC, Jarvis SE, et al. Differential modulation of N-type 1B and P/Q-type 1A calcium channels by different G protein subunit isoforms. J Physiol. 2000;527 (Pt 2):203–212. doi:10.1111/j.1469-7793.2000.00203.x
  • Audesirk TE. Characterization of pre- and postsynaptic dopamine receptors in Lymnaea. Comp Biochem Physiol C. 1989;93:115–119. doi:10.1016/0742-8413(89)90020-0
  • Barnes S, Syed NI, Bulloch AG, et al. Modulation of ionic currents by dopamine in an interneurone of the respiratory central pattern generator of Lymnaea stagnalis. J Exp Biol. 1994;189:37–54
  • Bean BP. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature. 1989;340:153–156. doi:10.1038/340153a0
  • Beech DJ, Bernheim L, Hille B. Pertussis toxin and voltage dependence distinguish multiple pathways modulating calcium channels of rat sympathetic neurons. Neuron. 1992;8:97–106. doi:10.1016/0896-6273(92)90111-P
  • Beedle AM, McRory JE, Poirot O, et al. Agonist-independent modulation of N-type calcium channels by ORL1 receptors. Nat Neurosci. 2004;7:118–125. doi:10.1038/nn1180
  • Bell HJ, Syed NI. Hypoxia-induced modulation of the respiratory CPG. Front Biosci. 2009;14:3825–3835. doi:10.2741/3491.
  • Bernheim L, Beech DJ, Hille B. A diffusible second messenger mediates one of the pathways coupling receptors to calcium channels in rat sympathetic neurons. Neuron. 1991;6:859–867. doi:10.1016/0896-6273(91)90226-P
  • Bissiere S, Humeau Y, Luthi A. Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci. 2003;6:587–592. doi:10.1038/nn1058
  • Blackmer T, Larsen EC, Bartleson C, et al. G protein betagamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat Neurosci. 2005;8:421–425. doi:10.1038/nn1423
  • Blackmer T, Larsen EC, Takahashi M, et al. G protein betagamma subunit-mediated presynaptic inhibition: regulation of exocytotic fusion downstream of Ca2+ entry. Science. 2001;292:293–297. doi:10.1126/science.1058803
  • Boland LM, Bean BP. Modulation of N-type calcium channels in bullfrog sympathetic neurons by luteinizing hormone-releasing hormone: kinetics and voltage dependence. J Neurosci. 1993;13:516–533
  • Brody DL, Patil PG, Mulle JG, et al. Bursts of action potential waveforms relieve G-protein inhibition of recombinant P/Q-type Ca2+ channels in HEK 293 cells. J Physiol. 1997;499 (Pt 3):637–644. doi:10.1113/jphysiol.1997.sp021956
  • Brown NA, Seabrook GR. Phosphorylation- and voltage-dependent inhibition of neuronal calcium currents by activation of human D2(short) dopamine receptors. Br J Pharmacol. 1995;115:459–466. doi:10.1111/j.1476-5381.1995.tb16355.x
  • Cabrera-Vera TM, Hernandez S, Earls LR, et al. RGS9-2 modulates D2 dopamine receptor-mediated Ca2+ channel inhibition in rat striatal cholinergic interneurons. Proc Natl Acad SciU S A. 2004;101:16339–16344. doi:10.1073/pnas.0407416101
  • Cantí C, Davies A, Berrow NS, et al. Evidence for two concentration-dependent processes for beta-subunit effects on alpha1B calcium channels. Biophys J. 2001;81:1439–1451. doi:10.1016/S0006-3495(01)75799-2
  • Capogna M, Gahwiler BH, Thompson SM. Presynaptic inhibition of calcium-dependent and -independent release elicited with ionomycin, gadolinium, and alpha-latrotoxin in the hippocampus. J Neurophysiol. 1996;75:2017–2028. doi:10.1152/jn.1996.75.5.2017
  • Chu HY, Ito W, Li J, Morozov A. Target-specific suppression of GABA release from parvalbumin interneurons in the basolateral amygdala by dopamine. J Neurosci. 2012;32:14815–14820. doi:10.1523/JNEUROSCI.2997-12.2012
  • De Waard M, Liu H, Walker D, et al. Direct binding of G-protein betagamma complex to voltage-dependent calcium channels. Nature. 1997;385:446–450. doi:10.1038/385446a0
  • DeBoer P, Abercrombie ED. Physiological release of striatal acetylcholine in vivo: modulation by D1 and D2 dopamine receptor subtypes. J Pharmacol Exp Therapeutics. 1996;277:775–783
  • Delmas P, Abogadie FC, Dayrell M, et al. G-proteins and G-protein subunits mediating cholinergic inhibition of N-type calcium currents in sympathetic neurons. Eur J Neurosci. 1998;10:1654–1666. doi:10.1046/j.1460-9568.1998.00170.x
  • Ding YS, Logan J, Bermel R, et al. Dopamine receptor-mediated regulation of striatal cholinergic activity: positron emission tomography studies with norchloro[18F]fluoroepibatidine. J Neurochem. 2000;74:1514–1521. doi:10.1046/j.1471-4159.2000.0741514.x
  • Dittman JS, Regehr WG. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci. 1996;16:1623–1633
  • Diverse-Pierluissi M, Remmers AE, Neubig RR, et al. Novel form of crosstalk between G protein and tyrosine kinase pathways. PNAS. 1997;94:5417–5421. doi:10.1073/pnas.94.10.5417
  • Dobson KS, Dmetrichuk JM, Spencer GE. Different receptors mediate the electrophysiological and growth cone responses of an identified neuron to applied dopamine. Neuroscience. 2006;141:1801–1810. doi:10.1016/j.neuroscience.2006.05.029
  • Dunlap K, Fischbach GD. Neurotransmitters decrease the calcium ocmponent of sensory neurone action potentials. Nature. 1978;276:837–839. doi:10.1038/276837a0
  • Eddy SR. Accelerated profile HMM searches. PLoS Comp Biol. 2011;7:e1002195. doi:10.1371/journal.pcbi.1002195.
  • Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi:10.1093/nar/gkh340
  • Elmslie KS, Kammermeier PJ, Jones SW. Calcium current modulation in frog sympathetic neurones: L-current is relatively insensitive to neurotransmitters. J Physiol. 1992;456:107–123. doi:10.1113/jphysiol.1992.sp019329
  • Elmslie KS, Zhou W, Jones SW. LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron. 1990;5:75–80. doi:10.1016/0896-6273(90)90035-E
  • Feng ZP, Arnot MI, Doering CJ, et al. Calcium channel beta subunits differentially regulate the inhibition of N-type channels by individual Gbeta isoforms. J Biol Chem. 2001;276:45051–45058. doi:10.1074/jbc.M107784200
  • Feng ZP, Grigoriev N, Munno D, et al. Development of Ca2+ hotspots between Lymnaea neurons during synaptogenesis. J Physiol. 2002;539:53–65. doi:10.1113/jphysiol.2001.013125
  • Feng ZP, Klumperman J, Lukowiak K, et al. In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J Neurosci. 1997;17:7839–7849
  • Feng ZP, Zhang Z, van Kesteren RE, et al. Transcriptome analysis of the central nervous system of the mollusc Lymnaea stagnalis. BMC Genomics. 2009;10:451. doi:10.1186/1471-2164-10-451
  • Forscher P, Oxford GS, Schulz D. Noradrenaline modulates calcium channels in avian dorsal root ganglion cells through tight receptor-channel coupling. J Physiol. 1986;379:131–144. doi:10.1113/jphysiol.1986.sp016244
  • Furukawa T, Miura R, Mori Y, et al. Differential interactions of the C terminus and the cytoplasmic I-II loop of neuronal Ca2+ channels with G-protein alpha and beta gamma subunits. II. Evidence for direct binding. J Biol Chem. 1998;273:17595–17603. doi:10.1074/jbc.273.28.17595
  • Gamper N, Reznikov V, Yamada Y, et al. Phosphatidylinositol [correction] 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+ channels. J Neurosci. 2004;24:10980–10992. doi:10.1523/JNEUROSCI.3869-04.2004
  • Gardzinski P, Lee DWK, Fei GH, et al. The role of synaptotagmin I C2A calcium-binding domain in synaptic vesicle clustering during synapse formation. J Physiol. 2007;581:75–90. doi:10.1113/jphysiol.2006.127472
  • Gerachshenko T, Blackmer T, Yoon EJ, et al. Gbetagamma acts at the C terminus of SNAP-25 to mediate presynaptic inhibition. Nat Neurosci. 2005;8:597–605. doi:10.1038/nn1439
  • Gerachshenko T, Schwartz E, Bleckert A, et al. Presynaptic G-protein-coupled receptors dynamically modify vesicle fusion, synaptic cleft glutamate concentrations, and motor behavior. J Neurosci. 2009;29:10221–10233. doi:10.1523/JNEUROSCI.1404-09.2009
  • Golard A, Siegelbaum SA. Kinetic basis for the voltage-dependent inhibition of N-type calcium current by somatostatin and norepinephrine in chick sympathetic neurons. J Neurosci. 1993;13:3884–3894
  • Guo C-H, Senzel A, Li K, et al. De novo protein synthesis of syntaxin-1 and dynamin-1 in long-term memory formation requires CREB1 gene transcription in Lymnaea stagnalis. Behav Genet. 2010;40:680–693. doi:10.1007/s10519-010-9374-9
  • Haas BJ, Papanicolaou A, Yassour M, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512. doi:10.1038/nprot.2013.084
  • Hamakawa T, Woodin MA, Bjorgum MC, et al. Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J Neurosci. 1999;19:9306–9312
  • Heidelberger R, Heinemann C, Neher E, et al. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 1994;371:513–515. doi:10.1038/371513a0
  • Herlitze S, Garcia DE, Mackie K, et al. Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature. 1996;380:258–262. doi:10.1038/380258a0
  • Hernadi L, Vehovszky A, Serfozo Z. Immunological and pharmacological identification of the dopamine D1 receptor in the CNS of the pond snail, Lymnaea stagnalis. Acta Biologica Hungarica. 2012;63 Suppl 2:151–159. doi:10.1556/ABiol.63.2012.Suppl.2.20
  • Hernandez-Lopez S, Tkatch T, Perez-Garci E, et al. D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J Neurosci. 2000;20:8987–8995
  • Higley MJ, Sabatini BL. Competitive regulation of synaptic Ca2+ influx by D2 dopamine and A2A adenosine receptors. Nat Neurosci. 2010;13:958–966. doi:10.1038/nn.2592
  • Huang X, Senatore A, Dawson TF, et al. G-proteins modulate invertebrate synaptic calcium channel (LCav2) differently from the classical voltage-dependent regulation of mammalian Cav2.1 and Cav2.2 channels. J Exp Biol. 2010;213:2094–2103. doi:10.1242/jeb.042242
  • Hui K, Fei GH, Saab BJ, et al. Neuronal calcium sensor-1 modulation of optimal calcium level for neurite outgrowth. Dev (Cambridge, England). 2007;134:4479–4489. doi:10.1242/dev.008979
  • Ikarashi Y, Takahashi A, Ishimaru H, et al. Regulation of dopamine D1 and D2 receptors on striatal acetylcholine release in rats. Brain Res Bulletin. 1997;43:107–115. doi:10.1016/S0361-9230(96)00351-6
  • Ikeda SR. Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature. 1996;380:255–258. doi:10.1038/380255a0
  • Jarvis SE, Zamponi GW. Masters or slaves? Vesicle release machinery and the regulation of presynaptic calcium channels. Cell Calcium. 2005;37:483–488. doi:10.1016/j.ceca.2005.01.017
  • Kammermeier PJ, Ruiz-Velasco V, Ikeda SR. A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Galpha q/11 and Gbeta gamma. J Neurosci. 2000;20:5623–5629
  • Kasai H, Aosaki T. Modulation of Ca-channel current by an adenosine analog mediated by a GTP-binding protein in chick sensory neurons. Pflugers Archiv : Eur J Physiol. 1989;414:145–149. doi:10.1007/BF00580956
  • Katz B, Miledi R. The effect of calcium on acetylcholine release from motor nerve terminals. Proc Royal Soc London Series B, Biol Sci. 1965;161:496–503. doi:10.1098/rspb.1965.0017
  • Kisilevsky AE, Mulligan SJ, Altier C, et al. D1 receptors physically interact with N-type calcium channels to regulate channel distribution and dendritic calcium entry. Neuron. 2008;58:557–570. doi:10.1016/j.neuron.2008.03.002
  • Kisilevsky AE, Zamponi GW. D2 dopamine receptors interact directly with N-type calcium channels and regulate channel surface expression levels. Channels (Austin, Tex). 2008;2:269–277. doi:10.4161/chan.2.4.6402
  • Knol JC, Roovers E, van Kesteren ER, et al. A G-protein beta subunit that is expressed in the central nervous system of the mollusc Lymnaea stagnalis identified through cDNA cloning. Biochim Et Biophys Acta. 1994;1222:129–133. doi:10.1016/0167-4889(94)90035-3
  • Knol JC, Weidemann W, Planta RJ, et al. Molecular cloning of G protein alpha subunits from the central nervous system of the mollusc Lymnaea stagnalis. FEBS Letters. 1992;314:215–219. doi:10.1016/0014-5793(92)81474-Z
  • Li D, Roberts R. WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell Mol Life Sci. 2001;58:2085–97. doi:10.1007/PL00000838
  • Lu Q, AtKisson MS, Jarvis SE, et al. Syntaxin 1A supports voltage-dependent inhibition of alpha1B Ca2+ channels by Gbetagamma in chick sensory neurons. J Neurosci. 2001;21:2949–2957
  • Lu TZ, Feng ZP. A sodium leak current regulates pacemaker activity of adult central pattern generator neurons in Lymnaea stagnalis. PloS One. 2011;6:e18745. doi:10.1371/journal.pone.0018745
  • Luebke JI, Dunlap K. Sensory neuron N-type calcium currents are inhibited by both voltage-dependent and -independent mechanisms. Pflugers Archiv : Eur J Physiol. 1994;428:499–507. doi:10.1007/BF00374571
  • Lukowiak K, Martens K, Orr M, et al. Modulation of aerial respiratory behaviour in a pond snail. Respir Physiol Neurobiol. 2006;154:61–72. doi:10.1016/j.resp.2006.02.009.
  • Magoski NS, Bauce LG, Syed NI, et al. Dopaminergic transmission between identified neurons from the mollusk, Lymnaea stagnalis. J Neurophysiol. 1995;74:1287–1300. doi:10.1152/jn.1995.74.3.1287
  • Magoski NS, Bulloch AG. Dopamine activates two different receptors to produce variability in sign at an identified synapse. J Neurophysiol. 1999;81:1330–1340. doi:10.1152/jn.1999.81.3.1330
  • Man-Son-Hing H, Zoran MJ, Lukowiak K, et al. A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature. 1989;341:237–239. doi:10.1038/341237a0
  • Marchetti C, Carbone E, Lux HD. Effects of dopamine and noradrenaline on Ca channels of cultured sensory and sympathetic neurons of chick. Pflugers Archiv: Eur J Physiol. 1986;406:104–111. doi:10.1007/BF00586670
  • Marowsky A, Yanagawa Y, Obata K, et al. A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron. 2005;48:1025–1037. doi:10.1016/j.neuron.2005.10.029
  • Martella G, Madeo G, Schirinzi T, et al. Altered profile and D2-dopamine receptor modulation of high voltage-activated calcium current in striatal medium spiny neurons from animal models of Parkinson's disease. Neuroscience. 2011;177:240–251. doi:10.1016/j.neuroscience.2010.12.057
  • Momiyama T, Koga E. Dopamine D2-like receptors selectively block N-type Ca2+ channels to reduce GABA release onto rat striatal cholinergic interneurones. J Physiol. 2001;533:479–492. doi:10.1111/j.1469-7793.2001.0479a.x
  • Moroz LI, Winlow W. Respiratory behaviour in Lymnaea stagnalis: pharmacological and cellular analyses. Acta Biologica Hungarica. 1992;43:421–429
  • Park D, Dunlap K. Dynamic regulation of calcium influx by G-proteins, action potential waveform, and neuronal firing frequency. J Neurosci. 1998;18:6757–6766
  • Pennock RL, Hentges ST. Desensitization-resistant and -sensitive GPCR-mediated inhibition of GABA release occurs by Ca2+-dependent and -independent mechanisms at a hypothalamic synapse. J Neurophysiol. 2016;115:2376–2388. doi:10.1152/jn.00535.2015
  • Photowala H, Blackmer T, Schwartz E, et al. G protein betagamma-subunits activated by serotonin mediate presynaptic inhibition by regulating vesicle fusion properties. Proc Natl Acad Sci U S A. 2006;103:4281–4286. doi:10.1073/pnas.0600509103
  • Qin N, Platano D, Olcese R, et al. 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. Proc Natl Acad Sci U S A. 1997;94:8866–8871. doi:10.1073/pnas.94.16.8866
  • Rane SG, Dunlap K. Kinase C activator 1,2-oleoylacetylglycerol attenuates voltage-dependent calcium current in sensory neurons. Proc Natl Acad Sci U S A. 1986;83:184–188. doi:10.1073/pnas.83.1.184
  • Ridgway RL, Syed NI, Lukowiak K, et al. Nerve growth factor (NGF) induces sprouting of specific neurons of the snail, Lymnaea stagnalis. J Neurobiol. 1991;22:377–390. doi:10.1002/neu.480220406
  • Sadamoto H, Takahashi H, Okada T, et al. De novo sequencing and transcriptome analysis of the central nervous system of mollusc Lymnaea stagnalis by deep RNA sequencing. PLoS One. 2012;7:e42546. doi:10.1371/journal.pone.0042546
  • Schiff ML, Siderovski DP, Jordan JD, et al. Tyrosine-kinase-dependent recruitment of RGS12 to the N-type calcium channel. Nature. 2000;408:723–727. doi:10.1038/35047093
  • Scholz KP, Miller RJ. Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron. 1992;8:1139–1150. doi:10.1016/0896-6273(92)90134-Y
  • Spencer GE, Lukowiak K, Syed NI. Transmitter-receptor interactions between growth cones of identified Lymnaea neurons determine target cell selection in vitro. J Neurosci. 2000;20:8077–8086
  • Stoof JC, De Vlieger TA, Lodder JC. Opposing roles for D-1 and D-2 dopamine receptors in regulating the excitability of growth hormone-producing cells in the snail Lymnaea stagnalis. Eur J Pharmacol. 1984;106:431–435. doi:10.1016/0014-2999(84)90735-0
  • Surmeier DJ, Bargas J, Hemmings HC, Jr, et al. Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron. 1995;14:385–397. doi:10.1016/0896-6273(95)90294-5
  • Syed NI, Bulloch AG, Lukowiak K. In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science. 1990;250:282–285. doi:10.1126/science.2218532
  • Syed NI, Winlow W. Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J Exp Biol. 1991;158:37–62
  • Südhof TC, Rizo J. Synaptic Vesicle Exocytosis. In Cold Spring Harb Perspect Biol. 2011;3(12):pii:a005637. doi:10.1101/cshperspect.a005637.
  • The UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2017;45:D158–D169. doi:10.1093/nar/gkw1099
  • Tritsch NX, Sabatini BL. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron. 2012;76:33–50. doi:10.1016/j.neuron.2012.09.023
  • Wells CA, Zurawski Z, Betke KM, et al. Gbetagamma inhibits exocytosis via interaction with critical residues on soluble N-ethylmaleimide-sensitive factor attachment protein-25. Mol Pharmacol. 2012;82;1136–1149. doi:10.1124/mol.112.080507
  • Werkman TR, Lodder JC, De Vlieger TA, et al. Further pharmacological characterization of a D-2-like dopamine receptor on growth hormone producing cells in Lymnaea stagnalis. Eur J Pharmacol. 1987;139:155–161. doi:10.1016/0014-2999(87)90247-0
  • Williams S, Serafin M, Muhlethaler M, et al. Facilitation of N-type calcium current is dependent on the frequency of action potential-like depolarizations in dissociated cholinergic basal forebrain neurons of the guinea pig. J Neurosci. 1997;17:1625–1632
  • Winlow W, Syed NI. The respiratory central pattern generator of Lymnaea. Acta Biologica Hungarica. 1992;43:399–408
  • Woodin MA, Hamakawa T, Takasaki M, et al. Trophic factor-induced plasticity of synaptic connections between identified Lymnaea neurons. Learning Memory (Cold Spring Harbor, NY). 1999;6:307–316.
  • Woodin MA, Munno DW, et al. Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetylcholine receptors. J Neurosci. 2002;22:505–514
  • Yan Z, Song WJ, Surmeier J. D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J Neurophysiol. 1997;77:1003–1015. doi:10.1152/jn.1997.77.2.1003
  • Yoon EJ, Hamm HE, Currie KP. G protein betagamma subunits modulate the number and nature of exocytotic fusion events in adrenal chromaffin cells independent of calcium entry. J Neurophysiol. 2008;100:2929–2939. doi:10.1152/jn.90839.2008
  • Zamponi GW, Bourinet E, Nelson D, Nargeot J, Snutch TP. Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature. 1997;385:442–446. doi:10.1038/385442a0
  • Zamponi GW, Currie KP. Regulation of Ca(V)2 calcium channels by G protein coupled receptors. Biochim Et Biophys Acta. 2013;1828:1629–1643. doi:10.1016/j.bbamem.2012.10.004
  • Zamponi GW, Snutch TP. Decay of prepulse facilitation of N type calcium channels during G protein inhibition is consistent with binding of a single Gbeta subunit. Proc Natl Acad Sci U S A. 1998;95:4035–4039. doi:10.1073/pnas.95.7.4035
  • Zucker RS, Regehr WG. Short-term synaptic plasticity. Ann Rev Physiol. 2002;64:355–405. doi:10.1146/annurev.physiol.64.092501.114547
  • Zurawski Z, Rodriguez S, Hyde K, et al. Gbetagamma Binds to the extreme C Terminus of SNAP25 to mediate the action of Gi/o-Coupled G protein-coupled receptors. Mol Pharmacol. 2016;89:75–83. doi:10.1124/mol.115.101600