Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Systematic Review Article

Role of Cav2.3 (R-type) Calcium Channel in Pain and Analgesia: A Scoping Review

Author(s): Marcella de Amorim Ferreira and Juliano Ferreira*

Volume 22, Issue 11, 2024

Published on: 15 August, 2023

Page: [1909 - 1922] Pages: 14

DOI: 10.2174/1570159X21666230811102700

Price: $65

Abstract

Background: Voltage-gated calcium channels (VGCCs) play an important role in pain development and maintenance. As Cav2.2 and Cav3.2 channels have been identified as potential drug targets for analgesics, the participation of Cav2.3 (that gives rise to R-type calcium currents) in pain and analgesia remains incompletely understood.

Objective: Identify the participation of Cav2.3 in pain and analgesia.

Methods: To map research in this area as well as to identify any existing gaps in knowledge on the potential role of Cav2.3 in pain signalling, we conducted this scoping review. We searched PubMed and SCOPUS databases, and 40 articles were included in this study. Besides, we organized the studies into 5 types of categories within the broader context of the role of Cav2.3 in pain and analgesia.

Results: Some studies revealed the expression of Cav2.3 in pain pathways, especially in nociceptive neurons at the sensory ganglia. Other studies demonstrated that Cav2.3-mediated currents could be inhibited by analgesic/antinociceptive drugs either indirectly or directly. Some articles indicated that Cav2.3 modulates nociceptive transmission, especially at the pre-synaptic level at spinal sites. There are studies using different rodent pain models and approaches to reduce Cav2.3 activity or expression and mostly demonstrated a pro-nociceptive role of Cav2.3, despite some contradictory findings and deficiencies in the description of study design quality. There are three studies that reported the association of single-nucleotide polymorphisms in the Cav2.3 gene (CACNA1E) with postoperative pain and opioid consumption as well as with the prevalence of migraine in patients.

Conclusion: Cav2.3 is a target for some analgesic drugs and has a pro-nociceptive role in pain.

« Previous Next »
Graphical Abstract

[1]
Basbaum, A.I.; Bautista, D.M.; Scherrer, G.; Julius, D. Cellular and molecular mechanisms of pain. Cell, 2009, 139(2), 267-284.
[http://dx.doi.org/10.1016/j.cell.2009.09.028] [PMID: 19837031]
[2]
Wang, H.; Woolf, C.J. Pain TRPs. Neuron, 2005, 46(1), 9-12.
[http://dx.doi.org/10.1016/j.neuron.2005.03.011] [PMID: 15820689]
[3]
Latremoliere, A.; Woolf, C.J. Central sensitization: A generator of pain hypersensitivity by central neural plasticity. J. Pain, 2009, 10(9), 895-926.
[http://dx.doi.org/10.1016/j.jpain.2009.06.012] [PMID: 19712899]
[4]
Dieleman, J.L.; Baral, R.; Birger, M.; Bui, A.L.; Bulchis, A.; Chapin, A.; Hamavid, H.; Horst, C.; Johnson, E.K.; Joseph, J.; Lavado, R.; Lomsadze, L.; Reynolds, A.; Squires, E.; Campbell, M.; DeCenso, B.; Dicker, D.; Flaxman, A.D.; Gabert, R.; Highfill, T.; Naghavi, M.; Nightingale, N.; Templin, T.; Tobias, M.I.; Vos, T. Murray, C.J.L. m.fl. US spending on personal health care and public health, 1996-2013. JAMA -. JAMA, 2016, 316(24), 2627-2646.
[http://dx.doi.org/10.1001/jama.2016.16885] [PMID: 28027366]
[5]
Raja, S.N.; Carr, D.B.; Cohen, M.; Finnerup, N.B.; Flor, H.; Gibson, S.; Keefe, F.J.; Mogil, J.S.; Ringkamp, M.; Sluka, K.A.; Song, X.J.; Stevens, B.; Sullivan, M.D.; Tutelman, P.R.; Ushida, T.; Vader, K. The revised International Association for the Study of Pain definition of pain: Concepts, challenges, and compromises. Pain, 2020, 161(9), 1976-1982.
[http://dx.doi.org/10.1097/j.pain.0000000000001939] [PMID: 32694387]
[6]
Loeser, J.D.; Treede, R.D. The Kyoto protocol of IASP Basic Pain Terminology. Pain, 2008, 137(3), 473-477.
[http://dx.doi.org/10.1016/j.pain.2008.04.025] [PMID: 18583048]
[7]
Freynhagen, R.; Parada, H.A.; Calderon-Ospina, C.A.; Chen, J.; Rakhmawati, E.D.; Fernández-Villacorta, F.J. Current understanding of the mixed pain concept: A brief narrative review. Curr. Med. Res. Opin., 2019, 35(1011), 1018-1117.
[8]
Cruccu, G.; Sommer, C.; Anand, P.; Attal, N.; Baron, R.; Garcia-Larrea, L.; Haanpaa, M.; Jensen, T.S.; Serra, J.; Treede, R.D. EFNS guidelines on neuropathic pain assessment: revised 2009. Eur. J. Neurol., 2010, 17(8), 1010-1018.
[http://dx.doi.org/10.1111/j.1468-1331.2010.02969.x] [PMID: 20298428]
[9]
Boezaart, A.P.; Smith, C.R.; Chembrovich, S.; Zasimovich, Y.; Server, A.; Morgan, G. Visceral versus somatic pain: An educational review of anatomy and clinical implications. Reg. Anesth. Pain Med., 2021, 46, 629-636.
[10]
Armitage, P.; Berry, G. The planning os statistical investigations: Statistical methods in medical research, 2nd ed; Blackwell: Oxford, 1987, pp. 179-185.
[11]
Khademi, H.; Kamangar, F.; Brennan, P.; Malekzadeh, R. Opioid therapy and its side effects: A review. Arch. Iran Med., 2016, 19, 870-876.
[12]
Greenwood-Van Meerveld, B.; Johnson, A.C.; Grundy, D. Gastrointestinal physiology and function. Handb. Exp. Pharmacol., 2017, 239, 1-16.
[http://dx.doi.org/10.1007/164_2016_118]
[13]
Abboud, C.; Duveau, A.; Bouali-Benazzouz, R.; Massé, K.; Mattar, J.; Brochoire, L. Animal models of pain: Diversity and benefits. J. Neurosci. Methods, 2021, 348, 108997.
[14]
Muley, M.M.; Krustev, E.; McDougall, J.J. Preclinical assessment of inflammatory pain. CNS Neurosci. Ther., 2016, 22(2), 88-101.
[http://dx.doi.org/10.1111/cns.12486] [PMID: 26663896]
[15]
Klinck, M.P.; Mogil, J.S.; Moreau, M.; Lascelles, B.D.X.; Flecknell, P.A.; Poitte, T.; Troncy, E. Translational pain assessment: Could natural animal models be the missing link? Pain, 2017, 158(9), 1633-1646.
[http://dx.doi.org/10.1097/j.pain.0000000000000978] [PMID: 28614187]
[16]
Simms, B.A.; Zamponi, G.W. Neuronal voltage-gated calcium channels: Structure, function, and dysfunction. Neuron, 2014, 82(1), 24-45.
[http://dx.doi.org/10.1016/j.neuron.2014.03.016] [PMID: 24698266]
[17]
Zamponi, G.W.; Striessnig, J.; Koschak, A.; Dolphin, A.C. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol. Rev., 2015, 67(4), 821-870.
[http://dx.doi.org/10.1124/pr.114.009654] [PMID: 26362469]
[18]
Catterall, W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol., 2011, 3(8), a003947.
[http://dx.doi.org/10.1101/cshperspect.a003947] [PMID: 21746798]
[19]
Dolphin, A.C. Voltage-gated calcium channels and their auxiliary subunits: physiology and pathophysiology and pharmacology. J. Physiol., 2016, 594(19), 5369-5390.
[http://dx.doi.org/10.1113/JP272262] [PMID: 27273705]
[20]
Eldabe, S.; Batterham, A. Ziconotide monotherapy: A systematic review of randomised controlled trials. Curr. Neuropharmacol., 2016, 15, 217-231.
[21]
Wallace, M.S.; Rauck, R.; Fisher, R.; Charapata, S.G.; Ellis, D.; Dissanayake, S. Intrathecal ziconotide for severe chronic pain: Safety and tolerability results of an open-label, long-term trial. Anesth. Analg., 2008, 106(2), 628-637.
[http://dx.doi.org/10.1213/ane.0b013e3181606fad] [PMID: 18227325]
[22]
Mogil, J.S.; Davis, K.D.; Derbyshire, S.W. The necessity of animal models in pain research. Pain, 2010, 151(1), 12-17.
[http://dx.doi.org/10.1016/j.pain.2010.07.015] [PMID: 20696526]
[23]
Weiss, N.; Zamponi, G.W. Opioid receptor regulation of neuronal voltage-gated calcium channels. Cell. Mol. Neurobiol., 2021, 41(5), 839-847.
[http://dx.doi.org/10.1007/s10571-020-00894-3] [PMID: 32514826]
[24]
Fang, Z.; Park, C.K.; Li, H.Y.; Kim, H.Y.; Park, S.H.; Jung, S.J.; Kim, J.S.; Monteil, A.; Oh, S.B.; Miller, R.J. Molecular basis of Ca(v)2.3 calcium channels in rat nociceptive neurons. J. Biol. Chem., 2007, 282(7), 4757-4764.
[http://dx.doi.org/10.1074/jbc.M605248200] [PMID: 17145762]
[25]
Fang, Z.; Hwang, J.H.; Kim, J.S.; Jung, S.J.; Oh, S.B. R-type calcium channel isoform in rat dorsal root ganglion neurons. Korean J. Physiol. Pharmacol., 2010, 14(1), 45-49.
[http://dx.doi.org/10.4196/kjpp.2010.14.1.45] [PMID: 20221279]
[26]
Schneider, T.; Dibué, M.; Hescheler, J. How “pharmacoresistant” is cav2.3, the major component of voltage-gated R-type Ca2+ channels? Pharmaceuticals, 2013, 6(6), 759-776.
[http://dx.doi.org/10.3390/ph6060759] [PMID: 24276260]
[27]
Wormuth, C.; Lundt, A.; Henseler, C.; Müller, R.; Broich, K.; Papazoglou, A. Weiergräber, M. m.fl. Review: Cav2.3 R-type voltage-gated Ca2+ channels - Functional implications in convulsive and non-convulsive seizure activity. Open Neurol. J., 2016, 10(1), 99-126.
[http://dx.doi.org/10.2174/1874205X01610010099] [PMID: 27843503]
[28]
Tricco, A.C.; Lillie, E.; Zarin, W.; O’Brien, K.K.; Colquhoun, H.; Levac, D. PRISMA extension for scoping reviews (PRISMA-ScR): Checklist and explanation. Ann. Intern. Med., 2018, 169, 467-473.
[29]
Pham, M.T.; Rajić, A.; Greig, J.D.; Sargeant, J.M.; Papadopoulos, A.; McEwen, S.A. A scoping review of scoping reviews: Advancing the approach and enhancing the consistency. Res. Synth. Methods, 2014, 5(4), 371-385.
[http://dx.doi.org/10.1002/jrsm.1123] [PMID: 26052958]
[30]
Sena, E.; van der Worp, H.B.; Howells, D.; Macleod, M. How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci., 2007, 30(9), 433-439.
[http://dx.doi.org/10.1016/j.tins.2007.06.009] [PMID: 17765332]
[31]
Le Pichon, C.E.; Chesler, A.T. The functional and anatomical dissection of somatosensory subpopulations using mouse genetics. Front. Neuroanat., 2014, 8, 21.
[http://dx.doi.org/10.3389/fnana.2014.00021] [PMID: 24795573]
[32]
Martella, G.; Costa, C.; Pisani, A.; Cupini, L.M.; Bernardi, G.; Calabresi, P. Antiepileptic drugs on calcium currents recorded from cortical and PAG neurons: Therapeutic implications for migraine. Cephalalgia, 2008, 28(12), 1315-1326.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01682.x] [PMID: 18771493]
[33]
Kortus, S.; Srinivasan, C.; Forostyak, O.; Zapotocky, M.; Ueta, Y.; Sykova, E. Sodium-calcium exchanger and R-type Ca2+ channels mediate spontaneous [Ca2+]i oscillations in magnocellular neurones of the rat supraoptic nucleus. Cell Calcium, 2016, 59, 289-298.
[34]
Siwek, M.E.; Müller, R.; Henseler, C.; Broich, K.; Papazoglou, A.; Weiergräber, M. The CaV2.3 R-type voltage-gated Ca2+ channel in mouse sleep architecture. Sleep, 2014, 37(5), 881-892.
[http://dx.doi.org/10.5665/sleep.3652] [PMID: 24790266]
[35]
Lee, S.C.; Choi, S.; Lee, T.; Kim, H.L.; Chin, H.; Shin, H.S. Molecular basis of R-type calcium channels in central amygdala neurons of the mouse. Proc. Natl. Acad. Sci. USA, 2002, 99(5), 3276-3281.
[http://dx.doi.org/10.1073/pnas.052697799] [PMID: 11854466]
[36]
Castro, J.; Harrington, A.M.; Garcia-Caraballo, S.; Maddern, J.; Grundy, L.; Zhang, J.; Page, G.; Miller, P.E.; Craik, D.J.; Adams, D.J.; Brierley, S.M. α-Conotoxin Vc1.1 inhibits human dorsal root ganglion neuroexcitability and mouse colonic nociception via GABAB receptors. Gut, 2017, 66(6), 1083-1094.
[http://dx.doi.org/10.1136/gutjnl-2015-310971] [PMID: 26887818]
[37]
Gandla, J.; Lomada, S.K.; Lu, J.; Kuner, R.; Bali, K.K. miR-34c-5p functions as pronociceptive microRNA in cancer pain by targeting Cav2.3 containing calcium channels. Pain, 2017, 158(9), 1765-1779.
[http://dx.doi.org/10.1097/j.pain.0000000000000971] [PMID: 28614186]
[38]
Martin, L.; Ibrahim, M.; Gomez, K.; Yu, J.; Cai, S.; Chew, L.A. Conotoxin contulakin-G engages a neurotensin receptor 2/R-type calcium channel (Cav2.3) pathway to mediate spinal antinociception. Pain, 2021, 163(9), 1751-1762.
[39]
Murakami, M.; Suzuki, T.; Nakagawasai, O.; Murakami, H.; Murakami, S.; Esashi, A.; Taniguchi, R.; Yanagisawa, T.; Tan-No, K.; Miyoshi, I.; Sasano, H.; Tadano, T. Distribution of various calcium channel α1 subunits in murine DRG neurons and antinociceptive effect of ω-conotoxin SVIB in mice. Brain Res., 2001, 903(1-2), 231-236.
[http://dx.doi.org/10.1016/S0006-8993(01)02427-1] [PMID: 11382408]
[40]
Murakami, M.; Nakagawasai, O.; Suzuki, T.; Mobarakeh, I.I.; Sakurada, Y.; Murata, A.; Yamadera, F.; Miyoshi, I.; Yanai, K.; Tan-No, K.; Sasano, H.; Tadano, T.; Iijima, T. Antinociceptive effect of different types of calcium channel inhibitors and the distribution of various calcium channel α1 subunits in the dorsal horn of spinal cord in mice. Brain Res., 2004, 1024(1-2), 122-129.
[http://dx.doi.org/10.1016/j.brainres.2004.07.066] [PMID: 15451373]
[41]
Saegusa, H.; Kurihara, T.; Zong, S.; Minowa, O.; Kazuno, A.; Han, W.; Matsuda, Y.; Yamanaka, H.; Osanai, M.; Noda, T.; Tanabe, T. Altered pain responses in mice lacking α1E subunit of the voltage-dependent Ca2+ channel. Proc. Natl. Acad. Sci. USA, 2000, 97(11), 6132-6137.
[http://dx.doi.org/10.1073/pnas.100124197] [PMID: 10801976]
[42]
Qian, A.; Song, D.; Li, Y.; Liu, X.; Tang, D.; Yao, W.; Yuan, Y. Role of voltage gated Ca2+ channels in rat visceral hypersensitivity change induced by 2,4,6-trinitrobenzene sulfonic acid. Mol. Pain, 2013, 9, 1744-8069-9-15.
[http://dx.doi.org/10.1186/1744-8069-9-15] [PMID: 23537331]
[43]
Westenbroek, R.E.; Hoskins, L.; Catterall, W.A. Localization of Ca2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals. J. Neurosci., 1998, 18(16), 6319-6330.
[http://dx.doi.org/10.1523/JNEUROSCI.18-16-06319.1998] [PMID: 9698323]
[44]
Yang, L.; Zhang, F-X.; Huang, F.; Lu, Y-J.; Li, G-D.; Bao, L. Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur. J. Neurosci., 2004, 19, 871-883.
[45]
Yokoyama, T.; Westenbroek, I.R.E.; Hell, W.; Snutch, P. Biochemical properties and subcellular distribution neuronal class E E calcium channel alpha 1 subunit. J. Neurosci., 1995, 15(10), 6419-6432.
[46]
Needham, K.; Bron, R.; Hunne, B.; Nguyen, T.V.; Turner, K.; Nash, M. Identification of subunits of voltage-gated calcium channels and actions of pregabalin on intrinsic primary afferent neurons in the guinea-pig ileum. Neurogastroenterol. Motil., 2010, 22, e301-e308.
[47]
Nkambeu, B.; Ben Salem, J.; Beaudry, F. Eugenol and other vanilloids hamper Caenorhabditis elegans response to noxious heat. Neurochem. Res., 2021, 46(2), 252-264.
[http://dx.doi.org/10.1007/s11064-020-03159-z] [PMID: 33123873]
[48]
He, A.; Song, D.; Zhang, L.; Li, C. Unveiling the relative efficacy, safety and tolerability of prophylactic medications for migraine: Pairwise and network-meta analysis. J. Headache Pain, 2017, 18, 26.
[49]
Ling, H-Q.; Chen, Z-H.; He, L.; Feng, F.; Weng, C-G.; Cheng, S-J. Comparative efficacy and safety of 11 drugs as therapies for adults with neuropathic pain after spinal cord injury: a bayesian network analysis based on 20 randomized controlled trials. Front. Neurol., 2022, 13, 818522.
[50]
Hainsworth, A.H.; McNaughton, N.C.L.; Pereverzev, A.; Schneider, T.; Randall, A.D. Actions of sipatrigine, 202W92 and lamotrigine on R-type and T-type Ca2+ channel currents. Eur. J. Pharmacol., 2003, 467, 77-80.
[51]
Kuzmiski, J.B.; Barr, W.; Zamponi, G.W.; MacVicar, B.A. Topiramate inhibits the initiation of plateau potentials in CA1 neurons by depressing R-type calcium channels. Epilepsia, 2005, 46(4), 481-489.
[http://dx.doi.org/10.1111/j.0013-9580.2005.35304.x] [PMID: 15816941]
[52]
Wormuth, C.; Lundt, A.; Henseler, C.; Müller, R.; Broich, K.; Papazoglou, A. Weiergräber, M. m.fl. Review: Cav2.3 R-type voltage-gated Ca2+ channels - Functional implications in convulsive and non-convulsive seizure activity. Open Neurol. J., 2016, 10(1), 99-126.
[http://dx.doi.org/10.2174/1874205X01610010099] [PMID: 27843503]
[53]
Sng, B.L.; Sia, A.T.H.; Quek, K.; Woo, D.; Lim, Y. Incidence and risk factors for chronic pain after caesarean section under spinal anaesthesia. Anaesth. Intensive Care, 2009, 37(5), 748-752.
[http://dx.doi.org/10.1177/0310057X0903700513] [PMID: 19775038]
[54]
Marathe, A.; Allahabadi, S.; Abd-Elsayed, A.; Saulino, M.; Hagedorn, J.M.; Orhurhu, V.; Karri, J. Intrathecal baclofen monotherapy and polyanalgesia for treating chronic pain in patients with severe spasticity. Curr. Pain Headache Rep., 2021, 25(12), 79.
[http://dx.doi.org/10.1007/s11916-021-00994-9] [PMID: 34894303]
[55]
Kakuta, N.; Tsutsumi, Y.M.; Horikawa, Y.T.; Kawano, H.; Kinoshita, M.; Tanaka, K. Neurokinin-1 receptor antagonism, aprepitant, effectively diminishes post-operative nausea and vomiting while increasing analgesic tolerance in laparoscopic gynecological procedures. J. Med. Invest., 2011, 58, 246-251.
[56]
Gaskell, H.; Derry, S.; Moore, R.A. Treating chronic non-cancer pain in older people - more questions than answers? Maturitas, 2014, 79(1), 34-40.
[http://dx.doi.org/10.1016/j.maturitas.2014.06.013] [PMID: 25048719]
[57]
Ferrari, M.D.; Goadsby, P.J.; Roon, K.I.; Lipton, R.B. Triptans (serotonin, 5-HT1B/1D agonists) in migraine: Detailed results and methods of a meta-analysis of 53 trials. Cephalalgia, 2002, 22(8), 633-658.
[http://dx.doi.org/10.1046/j.1468-2982.2002.00404.x] [PMID: 12383060]
[58]
Mollenholt, P.; Rawal, N.; Gordh, T., Jr; Olsson, Y. Intrathecal and epidural somatostatin for patients with cancer. Analgesic effects and postmortem neuropathologic investigations of spinal cord and nerve roots. Anesthesiology, 1994, 81(3), 534-542.
[http://dx.doi.org/10.1097/00000542-199409000-00004] [PMID: 7916546]
[59]
Sang, C.N.; Barnabe, K.J.; Kern, S.E. Phase IA clinical trial evaluating the tolerability, pharmacokinetics, and analgesic efficacy of an intrathecally administered neurotensin a analogue in central neuropathic pain following spinal cord injury. Clin. Pharmacol. Drug Dev., 2016, 5, 250-258.
[60]
Chung, G.; Rhee, J.N.; Jung, S.J.; Kim, J.S.; Oh, S.B. Modulation of CaV2.3 calcium channel currents by eugenol. J. Dent. Res., 2008, 87(2), 137-141.
[http://dx.doi.org/10.1177/154405910808700201] [PMID: 18218839]
[61]
Mohammadreza, S.; Mackenzie, G.; Toni, W.; Slobodan, S. L- cysteine modulates visceral nociception mediated by the CaV2.3 R-type calcium channels. Pflugers Arch., 2022, 474(4), 435-445.
[62]
Leão, R.M.; Cruz, J.S.; Diniz, C.R.; Cordeiro, M.N.; Beirão, P.S.L. Inhibition of neuronal high-voltage activated calcium channels by the ω-Phoneutria nigriventer Tx3-3 peptide toxin. Neuropharmacology, 2000, 39(10), 1756-1767.
[http://dx.doi.org/10.1016/S0028-3908(99)00267-1] [PMID: 10884557]
[63]
Piekarz, A.D.; Due, M.R.; Khanna, M.; Wang, B.; Ripsch, M.S.; Wang, R.; Meroueh, S.O.; Vasko, M.R.; White, F.A.; Khanna, R. CRMP-2 peptide mediated decrease of high and low voltageactivated calcium channels, attenuation of nociceptor excitability, and anti-nociception in a model of AIDS therapy-induced painful peripheral neuropathy. Mol. Pain, 2012, 8, 1744-8069-8-54.
[http://dx.doi.org/10.1186/1744-8069-8-54] [PMID: 22828369]
[64]
Shan, Z.; Cai, S.; Yu, J.; Zhang, Z.; Vallecillo, T.G.; Serafini, M.J.; Thomas, A.M.; Pham, N.Y.N.; Bellampalli, S.S.; Moutal, A.; Zhou, Y.; Xu, G.B.; Xu, Y.M.; Luo, S.; Patek, M.; Streicher, J.M.; Gunatilaka, A.A.L.; Khanna, R. Reversal of peripheral neuropathic pain by the small-molecule natural product physalin F via block of CaV2.3 (R-type) and CaV2.2 (N-type) voltage-gated calcium channels. ACS Chem. Neurosci., 2019, 10(6), 2939-2955.
[http://dx.doi.org/10.1021/acschemneuro.9b00166] [PMID: 30946560]
[65]
Bourinet, E.; Soong, T.W.; Stea, A.; Snutch, T.P. Determinants of the G protein-dependent opioid modulation of neuronal calcium channels. Proc. Natl. Acad. Sci. USA, 1996, 93(4), 1486-1491.
[http://dx.doi.org/10.1073/pnas.93.4.1486] [PMID: 8643659]
[66]
Ottolia, M.; Platano, D.; Qin, N.; Noceti, F.; Birnbaumer, M.; Toro, L.; Birnbaumer, L.; Stefani, E.; Olcese, R. Functional coupling between human E-type Ca2+ channels and μ opioid receptors expressed in Xenopus oocytes. FEBS Lett., 1998, 427(1), 96-102.
[http://dx.doi.org/10.1016/S0014-5793(98)00401-3] [PMID: 9613607]
[67]
Berecki, G.; Motin, L.; Adams, D.J. Voltage-Gated R-Type Calcium Channel Inhibition via Human μ -, δ -, and κ -opioid Receptors Is Voltage-Independently Mediated by G βγ Protein Subunits. Mol. Pharmacol., 2016, 89(1), 187-196.
[http://dx.doi.org/10.1124/mol.115.101154] [PMID: 26490245]
[68]
Berecki, G.; McArthur, J.R.; Cuny, H.; Clark, R.J.; Adams, D.J. Differential Cav2.1 and Cav2.3 channel inhibition by baclofen and alpha-conotoxin Vc1.1 via GABAB receptor activation. J. Gen. Physiol., 2014, 143, 465-479.
[69]
Meza, U.; Thapliyal, A.; Bannister, R.A.; Adams, B.A. Neurokinin 1 receptors trigger overlapping stimulation and inhibition of CaV2.3 (R-type) calcium channels. Mol. Pharmacol., 2007, 71(1), 284-293.
[http://dx.doi.org/10.1124/mol.106.028530] [PMID: 17050807]
[70]
Morikawa, T.; Matsuzawa, Y.; Makita, K.; Katayama, Y. Antimigraine drug, zolmitriptan, inhibits high-voltage activated calcium currents in a population of acutely dissociated rat trigeminal sensory neurons. Mol. Pain, 2006, 2, 10.
[71]
Mehrke, G.; Pereverzev, A.; Grabsch, H.; Hescheler, J.; Schneider, T. Receptor-mediated modulation of recombinant neuronal class E calcium channels. FEBS Lett., 1997, 408(3), 261-270.
[http://dx.doi.org/10.1016/S0014-5793(97)00437-7] [PMID: 9188773]
[72]
Rozanski, G.M.; Nath, A.R.; Adams, M.E.; Stanley, E.F. Low voltage-activated calcium channels gate transmitter release at the dorsal root ganglion sandwich synapse. J. Physiol., 2013, 591(22), 5575-5583.
[http://dx.doi.org/10.1113/jphysiol.2013.260281] [PMID: 24000176]
[73]
Yang, L.; Topia, I.; Schneider, T.; Stephens, G.J. Phorbol ester modulation of Ca2+ channels mediates nociceptive transmission in dorsal horn neurones. Pharmaceuticals, 2013, 6, 777-787.
[74]
Dalmolin, G.D.; Bannister, K.; Gonçalves, L.; Sikandar, S.; Patel, R.; Cordeiro, M. Effect of the spider toxin Tx3-3 on spinal processing of sensory information in naive and neuropathic rats. Pain Rep., 2017, 2, e610.
[http://dx.doi.org/10.1097/PR9.0000000000000610] [PMID: 29392225]
[75]
Lirk, P. Modulators of calcium influx regulate membrane excitability in rat dorsal root ganglion neurons. Anesth. Analg., 2008, 107, 673-685.
[76]
Fuchs, A.; Rigaud, M.; Sarantopoulos, C.D.; Filip, P.; Hogan, Q.H. Contribution of calcium channel subtypes to the intracellular calcium signal in sensory neurons: The effect of injury. Anesthesiology, 2007, 107(1), 117-127.
[http://dx.doi.org/10.1097/01.anes.0000267511.21864.93] [PMID: 17585223]
[77]
McCallum, J.B. Subtype-specific reduction of voltage-gated calcium current in medium-sized dorsal root ganglion neurons after painful peripheral nerve injury. Neuroscience, 2011, 179(1), 244-255.
[http://dx.doi.org/10.1016/j.neuroscience.2011.01.049]
[78]
Matthews, E.A.; Bee, L.A.; Stephens, G.J.; Dickenson, A.H. The Cav2.3 calcium channel antagonist SNX-482 reduces dorsal horn neuronal responses in a rat model of chronic neuropathic pain. Eur. J. Neurosci., 2007, 25, 3561-3569.
[79]
Weiergräber, M.; Henry, M.; Südkamp, M.; de Vivie, E.R.; Hescheler, J.; Schneider, T. Ablation of Ca(v)2.3/E-type voltage-gated calcium channel results in cardiac arrhythmia and altered autonomic control within the murine cardiovascular system. Basic Res. Cardiol., 2005, 100(1), 1-13.
[http://dx.doi.org/10.1007/s00395-004-0488-1] [PMID: 15490203]
[80]
Yokoyama, K.; Kurihara, T.; Saegusa, H.; Zong, S.; Makita, K.; Tanabe, T. Blocking the R-type (Cav2.3) Ca2+ channel enhanced morphine analgesia and reduced morphine tolerance. Eur. J. Neurosci., 2004, 20, 3516-3519.
[81]
Ferreira, M.A.; Lückemeyer, D.D.; Macedo-Júnior, S.J.; Schran, R.G.; Silva, A.M.; Prudente, A.S.; Tonello, R.; Ferreira, J. Sex-dependent Cav2.3 channel contribution to the secondary hyperalgesia in a mice model of central sensitization. Brain Res., 2021, 1764, 147438.
[http://dx.doi.org/10.1016/j.brainres.2021.147438] [PMID: 33753067]
[82]
Newcomb, R.; Szoke, B.; Palma, A.; Wang, G.; Chen, X.; Hopkins, W.; Cong, R.; Miller, J.; Urge, L.; Tarczy-Hornoch, K.; Loo, J.A.; Dooley, D.J.; Nadasdi, L.; Tsien, R.W.; Lemos, J.; Miljanich, G. Selective peptide antagonist of the class E calcium channel from the venom of the tarantula Hysterocrates gigas. Biochemistry, 1998, 37(44), 15353-15362.
[http://dx.doi.org/10.1021/bi981255g] [PMID: 9799496]
[83]
Newcomb, R.; Chen, X.; Dean, R.; Dayanithi, G. SNX-482: A novel class E calcium channel antagonist from tarantula venom. Biochemistry, 2000, 37, 15353-15362.
[84]
Bourinet, E.; Stotz, S.C.; Spaetgens, R.L.; Dayanithi, G.; Lemos, J.; Nargeot, J.; Zamponi, G.W. Interaction of SNX482 with domains III and IV inhibits activation gating of alpha(1E) (Ca(V)2.3) calcium channels. Biophys. J., 2001, 81(1), 79-88.
[http://dx.doi.org/10.1016/S0006-3495(01)75681-0] [PMID: 11423396]
[85]
Bishop, K.M. Progress and promise of antisense oligonucleotide therapeutics for central nervous system diseases. Neuropharmacology, 2017, 120, 56-62.
[http://dx.doi.org/10.1016/j.neuropharm.2016.12.015] [PMID: 27998711]
[86]
Schoch, K.M.; Miller, T.M. Antisense oligonucleotides: Translation from mouse models to human neurodegenerative diseases. Neuron, 2017, 94(6), 1056-1070.
[http://dx.doi.org/10.1016/j.neuron.2017.04.010] [PMID: 28641106]
[87]
Terashima, T.; Xu, Q.; Yamaguchi, S.; Yaksh, T.L. Intrathecal P/Q- and R-type calcium channel blockade of spinal substance P release and c-Fos expression. Neuropharmacology, 2013, 75, 1-8.
[http://dx.doi.org/10.1016/j.neuropharm.2013.06.018] [PMID: 23810829]
[88]
Yang, L.; Stephens, G.J. Effects of neuropathy on high-voltage-activated Ca2+ current in sensory neurones. Cell Calcium, 2009, 46(4), 248-256.
[http://dx.doi.org/10.1016/j.ceca.2009.08.001] [PMID: 19726083]
[89]
Dalmolin, G.D.; Silva, C.R.; Rigo, F.K.; Gomes, G.M.; do Nascimento Cordeiro, M.; Richardson, M.; Silva, M.A.R.; Prado, M.A.M.; Gomez, M.V.; Ferreira, J. Antinociceptive effect of Brazilian armed spider venom toxin Tx3-3 in animal models of neuropathic pain. Pain, 2011, 152(10), 2224-2232.
[http://dx.doi.org/10.1016/j.pain.2011.04.015] [PMID: 21570770]
[90]
Percie du Sert, N.; Rice, A.S.C. Improving the translation of analgesic drugs to the clinic: Animal models of neuropathic pain. Br. J. Pharmacol., 2014, 171(12), 2951-2963.
[http://dx.doi.org/10.1111/bph.12645] [PMID: 24527763]
[91]
Hooijmans, C.R.; Rovers, M.M.; de Vries, R.B.M.; Leenaars, M.; Ritskes-Hoitinga, M.; Langendam, M.W. SYRCLE’s risk of bias tool for animal studies. BMC Med. Res. Methodol., 2014, 14(1), 43.
[http://dx.doi.org/10.1186/1471-2288-14-43] [PMID: 24667063]
[92]
Ide, S.; Nishizawa, D.; Fukuda, K.; Kasai, S.; Hasegawa, J.; Hayashida, M.; Minami, M.; Ikeda, K. Association between genetic polymorphisms in Cav2.3 (R-type) Ca2+ channels and fentanyl sensitivity in patients undergoing painful cosmetic surgery. PLoS One, 2013, 8(8), e70694.
[http://dx.doi.org/10.1371/journal.pone.0070694] [PMID: 23940630]
[93]
Amano, K.; Nishizawa, D.; Mieda, T.; Tsujita, M.; Kitamura, A.; Hasegawa, J.; Inada, E.; Hayashida, M.; Ikeda, K. Opposite associations between the rs3845446 single-nucleotide polymorphism of the CACNA1E gene and postoperative pain-related phenotypes in gastrointestinal surgery versus previously reported orthognathic surgery. J. Pain, 2016, 17(10), 1126-1134.
[http://dx.doi.org/10.1016/j.jpain.2016.07.001] [PMID: 27480382]
[94]
Ambrosini, A.; D’Onofrio, M.; Buzzi, M.G.; Arisi, I.; Grieco, G.S.; Pierelli, F.; Santorelli, F.M.; Schoenen, J. Possible involvement of the CACNA1E gene in migraine: A search for single nucleotide polymorphism in different clinical phenotypes. Headache, 2017, 57(7), 1136-1144.
[http://dx.doi.org/10.1111/head.13107] [PMID: 28573794]
[95]
Helbig, K.L.; Lauerer, R.J.; Bahr, J.C.; Souza, I.A.; Myers, C.T.; Schwarz, N. De novo pathogenic variants in CACNA1E cause developmental and epileptic encephalopathy with contractures, macrocephaly, and dyskinesias. Am. J. Hum. Genet., 2018, 103(5), 666-678.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy