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Current Neuropharmacology

Editor-in-Chief

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

Review Article

Animal Venom Peptides Cause Antinociceptive Effects by Voltage-gated Calcium Channels Activity Blockage

Author(s): Gabriela Trevisan* and Sara Marchesan Oliveira*

Volume 20, Issue 8, 2022

Published on: 24 March, 2022

Page: [1579 - 1599] Pages: 21

DOI: 10.2174/1570159X19666210713121217

Price: $65

Abstract

Pain is a complex phenomenon that is usually unpleasant and aversive. It can range widely in intensity, quality, and duration and has diverse pathophysiologic mechanisms and meanings. Voltage-gated sodium and calcium channels are essential to transmitting painful stimuli from the periphery until the dorsal horn of the spinal cord. Thus, blocking voltage-gated calcium channels (VGCCs) can effectively control pain refractory to treatments currently used in the clinic, such as cancer and neuropathic pain. VGCCs blockers isolated of cobra Naja naja kaouthia (α-cobratoxin), spider Agelenopsis aperta (ω-Agatoxin IVA), spider Phoneutria nigriventer (PhTx3.3, PhTx3.4, PhTx3.5, PhTx3.6), spider Hysterocrates gigas (SNX-482), cone snails Conus geographus (GVIA), Conus magus (MVIIA or ziconotide), Conus catus (CVID, CVIE and CVIF), Conus striatus (SO- 3), Conus fulmen (FVIA), Conus moncuri (MoVIA and MoVIB), Conus regularis (RsXXIVA), Conus eburneus (Eu1.6), Conus victoriae (Vc1.1.), Conus regius (RgIA), and spider Ornithoctonus huwena (huwentoxin-I and huwentoxin-XVI) venoms caused antinociceptive effects in different acute and chronic pain models. Currently, ziconotide is the only clinical used N-type VGCCs blocker peptide for chronic intractable pain. However, ziconotide causes different adverse effects, and the intrathecal route of administration also impairs its use in a more significant number of patients. In this sense, peptides isolated from animal venoms or their synthetic forms that act by modulating or blocking VGCCs channels seem to be a relevant prototype for developing new analgesics efficacious and well tolerated by patients.

Keywords: Chronic pain, nociception, ion channels, toxin, spider, cone snail.

Graphical Abstract

[1]
Scholz, J.; Finnerup, N.B.; Attal, N.; Aziz, Q.; Baron, R.; Bennett, M.I.; Benoliel, R.; Cohen, M.; Cruccu, G.; Davis, K.D.; Evers, S.; First, M.; Giamberardino, M.A.; Hansson, P.; Kaasa, S.; Korwisi, B.; Kosek, E.; Lavand’homme, P.; Nicholas, M.; Nurmikko, T.; Perrot, S.; Ra-ja, S.N.; Rice, A.S.C.; Rowbotham, M.C.; Schug, S.; Simpson, D.M.; Smith, B.H.; Svensson, P.; Vlaeyen, J.W.S.; Wang, S.J.; Barke, A.; Rief, W.; Treede, R.D. The IASP classification of chronic pain for ICD-11: Chronic neuropathic pain. Pain, 2019, 160(1), 53-59.
[http://dx.doi.org/10.1097/j.pain.0000000000001365] [PMID: 30586071]
[2]
Kosek, E.; Cohen, M.; Baron, R.; Gebhart, G.F.; Mico, J.A.; Rice, A.S.C.; Rief, W.; Sluka, A.K. Do we need a third mechanistic descriptor for chronic pain states? Pain, 2016, 157(7), 1382-1386.
[http://dx.doi.org/10.1097/j.pain.0000000000000507] [PMID: 26835783]
[3]
Bennett, D.L.H.; Woods, C.G. Painful and painless channelopathies. Lancet Neurol., 2014, 13(6), 587-599.
[http://dx.doi.org/10.1016/S1474-4422(14)70024-9] [PMID: 24813307]
[4]
Moran, M.M.; Szallasi, A. Targeting nociceptive transient receptor potential channels to treat chronic pain: Current state of the field.
[5]
IASP Terminology - IASP. Available from: http://www.iasp-pain.org/Education/Content.aspx?ItemNumber=1698&navItemNumber=576 [Accessed November 10, 2018]
[6]
Scholz, J.; Woolf, C.J. Can we conquer pain? Nat. Neurosci., 2002, 5(Suppl.), 1062-1067.
[http://dx.doi.org/10.1038/nn942] [PMID: 12403987]
[7]
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]
[8]
Park, J.; Luo, Z.D. Calcium channel functions in pain processing. Channels (Austin), 2010, 4(6), 510-517.
[http://dx.doi.org/10.4161/chan.4.6.12869] [PMID: 21150297]
[9]
Zamponi, G.W.; Lewis, R.J.; Todorovic, S.M.; Arneric, S.P.; Snutch, T.P. Role of voltage-gated calcium channels in ascending pain path-ways. Brain Res. Brain Res. Rev., 2009, 60(1), 84-89.
[http://dx.doi.org/10.1016/j.brainresrev.2008.12.021] [PMID: 19162069]
[10]
Bourinet, E.; Altier, C.; Hildebrand, M.E.; Trang, T.; Salter, M.W.; Zamponi, G.W. Calcium-permeable ion channels in pain signaling. Physiol. Rev., 2014, 94(1), 81-140.
[http://dx.doi.org/10.1152/physrev.00023.2013] [PMID: 24382884]
[11]
Jensen, T.S.; Baron, R.; Haanpää, M.; Kalso, E.; Loeser, J.D.; Rice, A.S.C.; Treede, R.D. A new definition of neuropathic pain. Pain, 2011, 152(10), 2204-2205.
[http://dx.doi.org/10.1016/j.pain.2011.06.017] [PMID: 21764514]
[12]
Treede, R.D.; Rief, W.; Barke, A.; Aziz, Q.; Bennett, M.I.; Benoliel, R.; Cohen, M.; Evers, S.; Finnerup, N.B.; First, M.B.; Giamberardino, M.A.; Kaasa, S.; Korwisi, B.; Kosek, E.; Lavand’homme, P.; Nicholas, M.; Perrot, S.; Scholz, J.; Schug, S.; Smith, B.H.; Svensson, P.; Vlaeyen, J.W.S.; Wang, S.J. Chronic pain as a symptom or a disease: The IASP Classification of Chronic Pain for the International Classi-fication of Diseases (ICD-11). Pain, 2019, 160(1), 19-27.
[http://dx.doi.org/10.1097/j.pain.0000000000001384] [PMID: 30586067]
[13]
Becker, S.; Navratilova, E.; Nees, F.; Van Damme, S. Emotional and motivational pain processing: Current state of knowledge and per-spectives in translational research. Pain Res. Manag., 2018, 2018, 5457870.
[http://dx.doi.org/10.1155/2018/5457870] [PMID: 30123398]
[14]
Ossipov, M.H.; Dussor, G.O.; Porreca, F. Central modulation of pain. J. Clin. Invest., 2010, 120(11), 3779-3787.
[http://dx.doi.org/10.1172/JCI43766] [PMID: 21041960]
[15]
James, S.L.; Abate, D.; Abate, K.H.; Abay, S.M.; Abbafati, C.; Abbasi, N. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: A systematic analysis for the Global Bur-den of Disease Study 2017. Lancet, 2018, 392(10159), 1789-1858.
[http://dx.doi.org/10.1016/S0140-6736(18)32279-7] [PMID: 30496104]
[16]
Turk, D.C.; Wilson, H.D.; Cahana, A. Treatment of chronic non-cancer pain. Lancet, 2011, 377(9784), 2226-2235.
[http://dx.doi.org/10.1016/S0140-6736(11)60402-9] [PMID: 21704872]
[17]
Ballantyne, J.C.; Kalso, E.; Stannard, C. WHO analgesic ladder: A good concept gone astray. BMJ, 2016, 352, i20.
[http://dx.doi.org/10.1136/bmj.i20] [PMID: 26739664]
[18]
Portenoy, R.K. Treatment of cancer pain; Elsevier B.V., 2011, p. 377.
[19]
Liu, W.C.; Zheng, Z.X.; Tan, K.H.; Meredith, G.J. Multidimensional treatment of cancer pain. Curr. Oncol. Rep., 2017, 19(2), 10.
[http://dx.doi.org/10.1007/s11912-017-0570-0] [PMID: 28220448]
[20]
Zamponi, G.W.; Striessnig, J.; Koschak, A.; Dolphin, A.C. The physiology, pathology, and pharmacology of voltage-gated calcium chan-nels and their future therapeutic potential. Pharmacol. Rev., 2015, 67(4), 821-870.
[http://dx.doi.org/10.1124/pr.114.009654] [PMID: 26362469]
[21]
Ertel, E.A.; Campbell, K.P.; Harpold, M.M.; Hofmann, F.; Mori, Y.; Perez-Reyes, E. Nomenclature of voltage-gated calcium channels. Neuron, 2000, 25(3), 533-535.
[22]
Catterall, W.A.; Perez-Reyes, E.; Snutch, T.P.; Striessnig, J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev., 2005, 57(4), 411-425.
[http://dx.doi.org/10.1124/pr.57.4.5] [PMID: 16382099]
[23]
Cain, S.M.; Snutch, T.P. Voltage-gated calcium channels and disease. Biofactors, 2011, 37(3), 197-205.
[http://dx.doi.org/10.1002/biof.158] [PMID: 21698699]
[24]
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]
[25]
Matthews, E.A.; Bee, L.A.; Stephens, G.J.; Dickenson, A.H. The Cav2.3 calcium channel antagonist SNX-482 reduces dorsal horn neu-ronal responses in a rat model of chronic neuropathic pain. Eur. J. Neurosci., 2007, 25(12), 3561-3569.
[http://dx.doi.org/10.1111/j.1460-9568.2007.05605.x] [PMID: 17610575]
[26]
Zamponi, G.W. Targeting voltage-gated calcium channels in neurological and psychiatric diseases. Nat. Rev. Drug Discov., 2016, 15(1), 19-34.
[http://dx.doi.org/10.1038/nrd.2015.5] [PMID: 26542451]
[27]
Catterall, W.A. Ion channel voltage sensors: Structure, function, and pathophysiology. Neuron, 2010, 67(6), 915-928.
[http://dx.doi.org/10.1016/j.neuron.2010.08.021] [PMID: 20869590]
[28]
Ellinor, P.T.; Yang, J.; Sather, W.A.; Zhang, J.F.; Tsien, R.W. Ca2+ channel selectivity at a single locus for high-affinity Ca2+ interactions. Neuron, 1995, 15(5), 1121-1132.
[http://dx.doi.org/10.1016/0896-6273(95)90100-0] [PMID: 7576655]
[29]
Yang, J.; Ellinor, P.T.; Sather, W.A.; Zhang, J.F.; Tsien, R.W. Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature, 1993, 366(6451), 158-161.
[http://dx.doi.org/10.1038/366158a0] [PMID: 8232554]
[30]
Tang, L.; Gamal El-Din, T.M.; Payandeh, J.; Martinez, G.Q.; Heard, T.M.; Scheuer, T.; Zheng, N.; Catterall, W.A. Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature, 2014, 505(7481), 56-61.
[http://dx.doi.org/10.1038/nature12775] [PMID: 24270805]
[31]
Fox a P, Nowycky MC, Tsien RW. Single-channel recordings of three types of calcium channels in chick sensory neurones. J. Physiol., 1987, 394, 149-172.
[32]
Weber, A.M.; Wong, F.K.; Tufford, A.R.; Schlichter, L.C.; Matveev, V.; Stanley, E.F. N-type Ca2+ channels carry the largest current: Im-plications for nanodomains and transmitter release. Nat. Neurosci., 2010, 13(11), 1348-1350.
[http://dx.doi.org/10.1038/nn.2657] [PMID: 20953196]
[33]
Doering, C.J.; Hamid, J.; Simms, B.; McRory, J.E.; Zamponi, G.W. Cav1.4 encodes a calcium channel with low open probability and uni-tary conductance. Biophys. J., 2005, 89(5), 3042-3048.
[http://dx.doi.org/10.1529/biophysj.105.067124] [PMID: 16085774]
[34]
Dai, S.; Hall, D.D.; Hell, J.W. Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol. Rev., 2009, 89(2), 411-452.
[http://dx.doi.org/10.1152/physrev.00029.2007] [PMID: 19342611]
[35]
Zamponi, G.W.; Bourinet, E.; Nelson, D.; Nargeot, J.; Snutch, T.P. Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature, 1997, 385(6615), 442-446.
[http://dx.doi.org/10.1038/385442a0] [PMID: 9009192]
[36]
Cavallo, F.; De Giovanni, C.; Nanni, P.; Forni, G.; Lollini, P.L. 2011: The immune hallmarks of cancer. Cancer Immunol. Immunother., 2011, 60(3), 319-326.
[http://dx.doi.org/10.1007/s00262-010-0968-0] [PMID: 21267721]
[37]
Hall, D.D.; Dai, S.; Tseng, P.Y.; Malik, Z.; Nguyen, M.; Matt, L.; Schnizler, K.; Shephard, A.; Mohapatra, D.P.; Tsuruta, F.; Dolmetsch, R.E.; Christel, C.J.; Lee, A.; Burette, A.; Weinberg, R.J.; Hell, J.W. Competition between α-actinin and Ca2⁺-calmodulin controls surface re-tention of the L-type Ca2⁺ channel Ca(V)1.2. Neuron, 2013, 78(3), 483-497.
[http://dx.doi.org/10.1016/j.neuron.2013.02.032] [PMID: 23664615]
[38]
Dolphin, A.C. The α2δ subunits of voltage-gated calcium channels. Biochim. Biophys. Acta, 2013, 1828(7), 1541-1549.
[http://dx.doi.org/10.1016/j.bbamem.2012.11.019] [PMID: 23196350]
[39]
Yizhar, O.; Matti, U.; Melamed, R.; Hagalili, Y.; Bruns, D.; Rettig, J. A2Δ Expression Sets Presynaptic Calcium Channel Abundance and Release Probability. Neuron, 2012, 2, 122-125.
[http://dx.doi.org/10.1038/nature11033]
[40]
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]
[41]
Westenbroek, R.E.; Sakurai, T.; Elliott, E.M.; Hell, J.W.; Starr, T.V.; Snutch, T.P.; Catterall, W.A. Immunochemical identification and sub-cellular distribution of the alpha 1A subunits of brain calcium channels. J. Neurosci., 1995, 15(10), 6403-6418.
[http://dx.doi.org/10.1523/JNEUROSCI.15-10-06403.1995] [PMID: 7472404]
[42]
Wheeler, D A R, RW T Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science (80-), 1994, 264, 107-111.
[43]
Kisilevsky, A.E.; Mulligan, S.J.; Altier, C.; Iftinca, M.C.; Varela, D.; Tai, C.; Chen, L.; Hameed, S.; Hamid, J.; Macvicar, B.A.; Zamponi, G.W. D1 receptors physically interact with N-type calcium channels to regulate channel distribution and dendritic calcium entry. Neuron, 2008, 58(4), 557-570.
[http://dx.doi.org/10.1016/j.neuron.2008.03.002] [PMID: 18498737]
[44]
Randall, A.; Tsien, R.W. Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons. J. Neurosci., 1995, 15(4), 2995-3012.
[http://dx.doi.org/10.1523/JNEUROSCI.15-04-02995.1995] [PMID: 7722641]
[45]
Bourinet, E.; Soong, T.W.; Sutton, K.; Slaymaker, S.; Mathews, E.; Monteil, A.; Zamponi, G.W.; Nargeot, J.; Snutch, T.P. Splicing of alpha 1A subunit gene generates phenotypic variants of P- and Q-type calcium channels. Nat. Neurosci., 1999, 2(5), 407-415.
[http://dx.doi.org/10.1038/8070] [PMID: 10321243]
[46]
Richards, K.S.; Swensen, A.M.; Lipscombe, D.; Bommert, K. Novel CaV2.1 clone replicates many properties of Purkinje cell CaV2.1 current. Eur. J. Neurosci., 2007, 26(10), 2950-2961.
[http://dx.doi.org/10.1111/j.1460-9568.2007.05912.x] [PMID: 18001290]
[47]
Adams, M.E.; Mintz, I.M.; Reily, M.D.; Thanabal, V.; Bean, B.P. Structure and properties of omega-agatoxin IVB, a new antagonist of P-type calcium channels. Mol. Pharmacol., 1993, 44(4), 681-688.
[PMID: 8232218]
[48]
McCleskey, E.W.; Fox, A.P.; Feldman, D.H.; Cruz, L.J.; Olivera, B.M.; Tsien, R.W.; Yoshikami, D. Omega-conotoxin: Direct and persis-tent blockade of specific types of calcium channels in neurons but not muscle. Proc. Natl. Acad. Sci. USA, 1987, 84(12), 4327-4331.
[http://dx.doi.org/10.1073/pnas.84.12.4327] [PMID: 2438698]
[49]
Olivera, B.M.; Cruz, L.J.; de Santos, V.; LeCheminant, G.W.; Griffin, D.; Zeikus, R.; McIntosh, J.M.; Galyean, R.; Varga, J.; Gray, W.R. Neuronal calcium channel antagonists. Discrimination between calcium channel subtypes using omega-conotoxin from Conus magus ven-om. Biochemistry, 1987, 26(8), 2086-2090.
[http://dx.doi.org/10.1021/bi00382a004] [PMID: 2441741]
[50]
Soong, T.W.; Stea, A.; Hodson, C.D.; Dubel, S.J.; Vincent, S.R.; Snutch, T.P. Structure and functional expression of a member of the low voltage-activated calcium channel family. Science, 1993, 260(5111), 1133-1136.
[http://dx.doi.org/10.1126/science.8388125] [PMID: 8388125]
[51]
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]
[52]
Newcomb, R.; Szoke, B.; Palma, A.; Wang, G.; Chen, Xh.; 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 ven-om of the tarantula Hysterocrates gigas. Biochemistry, 1998, 37(44), 15353-15362.
[http://dx.doi.org/10.1021/bi981255g] [PMID: 9799496]
[53]
Tottene, A.; Volsen, S.; Pietrobon, D. alpha(1E) subunits form the pore of three cerebellar R-type calcium channels with different pharma-cological and permeation properties. J. Neurosci., 2000, 20(1), 171-178.
[http://dx.doi.org/10.1523/JNEUROSCI.20-01-00171.2000] [PMID: 10627594]
[54]
Perez-reyes, E; Snutch, TP; Barrett, PQ; Lee, J; Zorumski, CF; Todorovic, SM Molecular physiology of low-voltage-activated t-type calci-um channels., 2007, 117-161.
[55]
Boroujerdi, A.; Zeng, J.; Sharp, K.; Kim, D.; Steward, O.; Luo, D.Z. Calcium channel alpha-2-delta-1 protein upregulation in dorsal spinal cord mediates spinal cord injury-induced neuropathic pain states. Pain, 2011, 152(3), 649-655.
[http://dx.doi.org/10.1016/j.pain.2010.12.014] [PMID: 21239111]
[56]
Luo, Z.D.; Calcutt, N.A.; Higuera, E.S.; Valder, C.R.; Song, Y-H.; Svensson, C.I.; Myers, R.R. Injury type-specific calcium channel alpha 2 delta-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J. Pharmacol. Exp. Ther., 2002, 303(3), 1199-1205.
[http://dx.doi.org/10.1124/jpet.102.041574] [PMID: 12438544]
[57]
Li, C-Y.; Song, Y-H.; Higuera, E.S.; Luo, Z.D. Spinal dorsal horn calcium channel alpha2delta-1 subunit upregulation contributes to pe-ripheral nerve injury-induced tactile allodynia. J. Neurosci., 2004, 24(39), 8494-8499.
[http://dx.doi.org/10.1523/JNEUROSCI.2982-04.2004] [PMID: 15456823]
[58]
Field, M.J.; Li, Z.; Schwarz, J.B. Ca2+ channel alpha2-delta ligands for the treatment of neuropathic pain. J. Med. Chem., 2007, 50(11), 2569-2575.
[http://dx.doi.org/10.1021/jm060650z] [PMID: 17489571]
[59]
Rosenberg, J.M.; Harrell, C.; Ristic, H.; Werner, R.A.; de Rosayro, A.M. The effect of gabapentin on neuropathic pain. Clin. J. Pain, 1997, 13(3), 251-255.
[http://dx.doi.org/10.1097/00002508-199709000-00011] [PMID: 9303258]
[60]
Gee, N.S.; Brown, J.P.; Dissanayake, V.U.K.; Offord, J.; Thurlow, R.; Woodruff, G.N. The novel anticonvulsant drug, gabapentin (Neu-rontin), binds to the alpha2delta subunit of a calcium channel. J. Biol. Chem., 1996, 271(10), 5768-5776.
[http://dx.doi.org/10.1074/jbc.271.10.5768] [PMID: 8621444]
[61]
Bauer, C.S.; Rahman, W.; Tran-van-Minh, A.; Lujan, R.; Dickenson, A.H.; Dolphin, A.C. The anti-allodynic α(2)δ ligand pregabalin inhibits the trafficking of the calcium channel α(2)δ-1 subunit to presynaptic terminals in vivo. Biochem. Soc. Trans., 2010, 38(2), 525-528.
[http://dx.doi.org/10.1042/BST0380525] [PMID: 20298215]
[62]
Bauer, C.S.; Nieto-Rostro, M.; Rahman, W.; Tran-Van-Minh, A.; Ferron, L.; Douglas, L.; Kadurin, I.; Sri Ranjan, Y.; Fernandez-Alacid, L.; Millar, N.S.; Dickenson, A.H.; Lujan, R.; Dolphin, A.C. The increased trafficking of the calcium channel subunit alpha2delta-1 to presyn-aptic terminals in neuropathic pain is inhibited by the alpha2delta ligand pregabalin. J. Neurosci., 2009, 29(13), 4076-4088.
[http://dx.doi.org/10.1523/JNEUROSCI.0356-09.2009] [PMID: 19339603]
[63]
Hendrich, J.; Bauer, C.S.; Dolphin, A.C. Chronic pregabalin inhibits synaptic transmission between rat dorsal root ganglion and dorsal horn neurons in culture. Channels (Austin), 2012, 6(2), 124-132.
[http://dx.doi.org/10.4161/chan.19805] [PMID: 22627148]
[64]
Bayer, K.; Ahmadi, S.; Zeilhofer, H.U. Gabapentin may inhibit synaptic transmission in the mouse spinal cord dorsal horn through a pref-erential block of P/Q-type Ca2+ channels. Neuropharmacology, 2004, 46(5), 743-749.
[http://dx.doi.org/10.1016/j.neuropharm.2003.11.010] [PMID: 14996552]
[65]
Matthews, E.A.; Dickenson, A.H. Effects of spinally delivered N- and P-type voltage-dependent calcium channel antagonists on dorsal horn neuronal responses in a rat model of neuropathy. Pain, 2001, 92(1-2), 235-246.
[http://dx.doi.org/10.1016/S0304-3959(01)00255-X] [PMID: 11323145]
[66]
McGivern, J.G. Targeting N-type and T-type calcium channels for the treatment of pain. Drug Discov. Today, 2006, 11(5-6), 245-253.
[http://dx.doi.org/10.1016/S1359-6446(05)03662-7] [PMID: 16580601]
[67]
Dogrul, A.; Gardell, L.R.; Ossipov, M.H.; Tulunay, F.C.; Lai, J.; Porreca, F. Reversal of experimental neuropathic pain by T-type calcium channel blockers. Pain, 2003, 105(1-2), 159-168.
[http://dx.doi.org/10.1016/S0304-3959(03)00177-5] [PMID: 14499432]
[68]
Shannon, H.E.; Eberle, E.L.; Peters, S.C. Comparison of the effects of anticonvulsant drugs with diverse mechanisms of action in the formalin test in rats. Neuropharmacology, 2005, 48(7), 1012-1020.
[http://dx.doi.org/10.1016/j.neuropharm.2005.01.013] [PMID: 15857628]
[69]
Flatters, S.J.L.; Bennett, G.J. Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain, 2004, 109(1-2), 150-161.
[http://dx.doi.org/10.1016/j.pain.2004.01.029] [PMID: 15082137]
[70]
Kerckhove, N.; Pereira, B.; Soriot-Thomas, S.; Alchaar, H.; Deleens, R.; Hieng, V.S.; Serra, E.; Lanteri-Minet, M.; Arcagni, P.; Picard, P.; Lefebvre-Kuntz, D.; Maindet, C.; Mick, G.; Balp, L.; Lucas, C.; Creach, C.; Letellier, M.; Martinez, V.; Navez, M.; Delbrouck, D.; Kuhn, E.; Piquet, E.; Bozzolo, E.; Brosse, C.; Lietar, B.; Marcaillou, F.; Hamdani, A.; Leroux-Bromberg, N.; Perier, Y.; Vergne-Salle, P.; Gov, C.; Delage, N.; Gillet, D.; Romettino, S.; Richard, D.; Mallet, C.; Bernard, L.; Lambert, C.; Dubray, C.; Duale, C.; Eschalier, A. Efficacy and safety of a T-type calcium channel blocker in patients with neuropathic pain: A proof-of-concept, randomized, double-blind and con-trolled trial. Eur. J. Pain, 2018, 22(7), 1321-1330.
[http://dx.doi.org/10.1002/ejp.1221] [PMID: 29577519]
[71]
Hord, A.H.; Denson, D.D.; Chalfoun, A.G.; Azevedo, M.I. The effect of systemic zonisamide (Zonegran) on thermal hyperalgesia and mechan-ical allodynia in rats with an experimental mononeuropathy. Anesth. Analg., 2003, 96, 1700-1706.
[72]
Drake, M.E., Jr; Greathouse, N.I.; Renner, J.B.; Armentbright, A.D. Open-label zonisamide for refractory migraine. Clin. Neuropharmacol., 2004, 27(6), 278-280.
[http://dx.doi.org/10.1097/01.wnf.0000150866.98887.77] [PMID: 15613932]
[73]
Takahashi, Y.; Hashimoto, K.; Tsuji, S. Successful use of zonisamide for central poststroke pain. J. Pain, 2004, 5(3), 192-194.
[http://dx.doi.org/10.1016/j.jpain.2004.01.002] [PMID: 15106132]
[74]
Todorovic, S.; Meyenburg, A.; Jevtovic-Todorovic, V. Mechanical and thermal antinociception in rats following systemic administration of mibefradil, a T-type calcium channel blocker. Brain Res., 2002, 336-340.
[75]
SoRelle, R. Withdrawal of posicor from market. Circulation, 1998, 98(9), 831-832.
[http://dx.doi.org/10.1161/01.CIR.98.9.831] [PMID: 9738634]
[76]
Kumar, R.; Mehra, R.; Ray, S.B. L-type calcium channel blockers, morphine and pain: Newer insights. Indian J. Anaesth., 2010, 54(2), 127-131.
[http://dx.doi.org/10.4103/0019-5049.63652] [PMID: 20661350]
[77]
Michaluk, J.; Karolewicz, B.; Antkiewicz-Michaluk, L.; Vetulani, J. Effects of various Ca2+ channel antagonists on morphine analgesia, tolerance and dependence, and on blood pressure in the rat. Eur. J. Pharmacol., 1998, 352(2-3), 189-197.
[http://dx.doi.org/10.1016/S0014-2999(98)00373-2] [PMID: 9716354]
[78]
Kawashiri, T.; Egashira, N.; Kurobe, K.; Tsutsumi, K.; Yamashita, Y.; Ushio, S.; Yano, T.; Oishi, R. L type Ca2+ channel blockers prevent oxaliplatin-induced cold hyperalgesia and TRPM8 overexpression in rats. Mol. Pain, 2012, 8, 7.
[http://dx.doi.org/10.1186/1744-8069-8-7] [PMID: 22292988]
[79]
Ray, S.B.; Mehra, R.D. Potentiation of opioid-induced analgesia by l-type calcium channel blockers: Need for clinical trial in cancer pain. Indian J. Anaesth., 2008, 52, 367-372.
[80]
Yamamoto, S.; Suzuki, Y.; Ono, H.; Kume, K.; Ohsawa, M. N- and L-type calcium channels blocker cilnidipine ameliorates neuropathic pain. Eur. J. Pharmacol., 2016, 793, 66-75.
[http://dx.doi.org/10.1016/j.ejphar.2016.11.001] [PMID: 27823932]
[81]
Skerratt, S.E.; West, C.W. Ion channel therapeutics for pain. Channels (Austin), 2015, 9(6), 344-351.
[http://dx.doi.org/10.1080/19336950.2015.1075105] [PMID: 26218246]
[82]
Schroeder, C.I. Lewis, R.J. ω-Conotoxins GVIA. MVIIA and CVID: SAR and Clinical Potential. Mar Drugs, 2006, 4, 193.
[83]
Saegusa, H.; Kurihara, T.; Zong, S.; Kazuno, A.; Matsuda, Y.; Nonaka, T.; Han, W.; Toriyama, H.; Tanabe, T. Suppression of inflammato-ry and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel. EMBO J., 2001, 20(10), 2349-2356.
[http://dx.doi.org/10.1093/emboj/20.10.2349] [PMID: 11350923]
[84]
Hatakeyama, S.; Wakamori, M.; Ino, M.; Miyamoto, N.; Takahashi, E.; Yoshinaga, T.; Sawada, K.; Imoto, K.; Tanaka, I.; Yoshizawa, T.; Nishizawa, Y.; Mori, Y.; Niidome, T.; Shoji, S. Differential nociceptive responses in mice lacking the α(1B) subunit of N-type Ca2+ chan-nels. Neuroreport, 2001, 12(11), 2423-2427.
[http://dx.doi.org/10.1097/00001756-200108080-00027] [PMID: 11496122]
[85]
Snutch, T.P. Targeting chronic and neuropathic pain: The N-type calcium channel comes of age. NeuroRx, 2005, 2(4), 662-670.
[http://dx.doi.org/10.1602/neurorx.2.4.662] [PMID: 16489373]
[86]
Vanegas, H.; Schaible, H. Effects of antagonists to high-threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain, 2000, 85(1-2), 9-18.
[http://dx.doi.org/10.1016/S0304-3959(99)00241-9] [PMID: 10692598]
[87]
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 alpha 1E 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]
[88]
Sanford, M. Intrathecal ziconotide: A review of its use in patients with chronic pain refractory to other systemic or intrathecal analgesics. CNS Drugs, 2013, 27(11), 989-1002.
[http://dx.doi.org/10.1007/s40263-013-0107-5] [PMID: 23999971]
[89]
Santicioli, P.; Del Bianco, E.; Tramontana, M.; Geppetti, P.; Maggi, C.A. Release of calcitonin gene-related peptide like-immunoreactivity induced by electrical field stimulation from rat spinal afferents is mediated by conotoxin-sensitive calcium channels. Neurosci. Lett., 1992, 136(2), 161-164.
[http://dx.doi.org/10.1016/0304-3940(92)90039-A] [PMID: 1322515]
[90]
Maggi, C.A.; Tramontana, M.; Cecconi, R.; Santicioli, P. Neurochemical evidence for the involvement of N-type calcium channels in transmitter secretion from peripheral endings of sensory nerves in guinea pigs. Neurosci. Lett., 1990, 114(2), 203-206.
[http://dx.doi.org/10.1016/0304-3940(90)90072-H] [PMID: 1697665]
[91]
Sluka, K.A. Blockade of calcium channels can prevent the onset of secondary hyperalgesia and allodynia induced by intradermal injection of capsaicin in rats. Pain, 1997, 71(2), 157-164.
[http://dx.doi.org/10.1016/S0304-3959(97)03354-X] [PMID: 9211477]
[92]
Nebe, J.; Vanegas, H.; Schaible, H.G. Spinal application of ω-conotoxin GVIA, an N-type calcium channel antagonist, attenuates enhance-ment of dorsal spinal neuronal responses caused by intra-articular injection of mustard oil in the rat. Exp. Brain Res., 1998, 120(1), 61-69.
[http://dx.doi.org/10.1007/s002210050378] [PMID: 9628404]
[93]
Scott, D.A.; Wright, C.E.; Angus, J.A. Actions of intrathecal ω-conotoxins CVID, GVIA, MVIIA, and morphine in acute and neuropathic pain in the rat. Eur. J. Pharmacol., 2002, 451(3), 279-286.
[http://dx.doi.org/10.1016/S0014-2999(02)02247-1] [PMID: 12242089]
[94]
E. Brookes, M.; Eldabe, S.; Batterham, A. Ziconotide monotherapy: A systematic review of randomised controlled trials. Curr. Neuropharmacol., 2016, 15, 217-231.
[http://dx.doi.org/10.2174/1570159x14666160210142056]
[95]
Schmidtko, A.; Lötsch, J.; Freynhagen, R.; Geisslinger, G. Ziconotide for treatment of severe chronic pain. Lancet, 2010, 375(9725), 1569-1577.
[http://dx.doi.org/10.1016/S0140-6736(10)60354-6] [PMID: 20413151]
[96]
Malmberg, A.B.; Yaksh, T.L. Voltage-sensitive calcium channels in spinal nociceptive processing: Blockade of N- and P-type channels inhibits formalin-induced nociception. J. Neurosci., 1994, 14(8), 4882-4890.
[http://dx.doi.org/10.1523/JNEUROSCI.14-08-04882.1994] [PMID: 8046458]
[97]
Malmberg, A.B.; Yaksh, T.L. Effect of continuous intrathecal infusion of ω-conopeptides, N-type calcium-channel blockers, on behavior and antinociception in the formalin and hot-plate tests in rats. Pain, 1995, 60(1), 83-90.
[http://dx.doi.org/10.1016/0304-3959(94)00094-U] [PMID: 7715945]
[98]
Bowersox, S.S.; Gadbois, T.; Singh, T.; Pettus, M.; Wang, Y.X.; Luther, R.R. Selective N-type neuronal voltage-sensitive calcium channel blocker, SNX-111, produces spinal antinociception in rat models of acute, persistent and neuropathic pain. J. Pharmacol. Exp. Ther., 1996, 279(3), 1243-1249.
[PMID: 8968347]
[99]
Chaplan, S.R.; Pogrel, J.W.; Yaksh, T.L. Role of voltage-dependent calcium channel subtypes in experimental tactile allodynia. J. Pharmacol. Exp. Ther., 1994, 269(3), 1117-1123.
[PMID: 8014856]
[100]
Pope, J.E.; Deer, T.R. Ziconotide: A clinical update and pharmacologic review. Expert Opin. Pharmacother., 2013, 14(7), 957-966.
[http://dx.doi.org/10.1517/14656566.2013.784269] [PMID: 23537340]
[101]
Yamamoto, T.; Sakashita, Y. Differential effects of intrathecally administered N- and P-type voltage-sensitive calcium channel blockers upon two models of experimental mononeuropathy in the rat. Brain Res., 1998, 794(2), 329-332.
[http://dx.doi.org/10.1016/S0006-8993(98)00306-0] [PMID: 9622667]
[102]
Wang, Y.X.; Pettus, M.; Gao, D.; Phillips, C.; Scott Bowersox, S. Effects of intrathecal administration of ziconotide, a selective neuronal N-type calcium channel blocker, on mechanical allodynia and heat hyperalgesia in a rat model of postoperative pain. Pain, 2000, 84(2-3), 151-158.
[http://dx.doi.org/10.1016/S0304-3959(99)00197-9] [PMID: 10666519]
[103]
White, D.M.; Cousins, M.J. Effect of subcutaneous administration of calcium channel blockers on nerve injury-induced hyperalgesia. Brain Res., 1998, 801(1-2), 50-58.
[http://dx.doi.org/10.1016/S0006-8993(98)00539-3] [PMID: 9729273]
[104]
Delhaas, E.M.; Huygen, F.J.P.M. Complications associated with intrathecal drug delivery systems. BJA Educ., 2020, 20(2), 51-57.
[http://dx.doi.org/10.1016/j.bjae.2019.11.002] [PMID: 33456930]
[105]
Ver Donck, A.; Collins, R.; Rauck, R.L.; Nitescu, P. An open-label, multicenter study of the safety and efficacy of intrathecal ziconotide for severe chronic pain when delivered via an external pump. Neuromodulation, 2008, 11(2), 103-111.
[http://dx.doi.org/10.1111/j.1525-1403.2008.00150.x] [PMID: 22151042]
[106]
Deer, T.; Krames, E.S.; Hassenbusch, S.J.; Burton, A.; Caraway, D.; Dupen, S.; Eisenach, J.; Erdek, M.; Grigsby, E.; Kim, P.; Levy, R.; McDowell, G.; Mekhail, N.; Panchal, S.; Prager, J.; Rauck, R.; Saulino, M.; Sitzman, T.; Staats, P.; Stanton-Hicks, M.; Stearns, L.; Willis, K.D.; Witt, W.; Follett, K.; Huntoon, M.; Liem, L.; Rathmell, J.; Wallace, M.; Buchser, E.; Cousins, M.; Ver Donck, A. Polyanalgesic con-sensus conference 2007: Recommendations for the management of pain by intrathecal (intraspinal) drug delivery: Report of an interdisci-plinary expert panel. Neuromodulation, 2007, 10(4), 300-328.
[http://dx.doi.org/10.1111/j.1525-1403.2007.00128.x] [PMID: 22150890]
[107]
Manda, P.; Kushwaha, A.S.; Kundu, S.; Shivakumar, H.N.; Jo, S.B.; Murthy, S.N. Delivery of ziconotide to cerebrospinal fluid via intrana-sal pathway for the treatment of chronic pain. J. Control. Release, 2016, 224, 69-76.
[http://dx.doi.org/10.1016/j.jconrel.2015.12.044] [PMID: 26732557]
[108]
Yu, S.; Li, Y.; Chen, J.; Zhang, Y.; Tao, X.; Dai, Q.; Wang, Y.; Li, S.; Dong, M. TAT-modified w-conotoxin MVIIA for crossing the blood-brain barrier. Mar. Drugs, 2019, 17(5), E286.
[http://dx.doi.org/10.3390/md17050286] [PMID: 31083641]
[109]
Smith, M.T.; Cabot, P.J.; Ross, F.B.; Robertson, A.D.; Lewis, R.J. The novel N-type calcium channel blocker, AM336, produces potent dose-dependent antinociception after intrathecal dosing in rats and inhibits substance P release in rat spinal cord slices. Pain, 2002, 96(1-2), 119-127.
[http://dx.doi.org/10.1016/S0304-3959(01)00436-5] [PMID: 11932068]
[110]
Kolosov, A.; Aurini, L.; Williams, E.D.; Cooke, I.; Goodchild, C.S. Intravenous injection of leconotide, an omega conotoxin: Synergistic antihyperalgesic effects with morphine in a rat model of bone cancer pain. Pain Med., 2011, 12(6), 923-941.
[http://dx.doi.org/10.1111/j.1526-4637.2011.01118.x] [PMID: 21539704]
[111]
Kolosov, A.; Goodchild, C.S.; Cooke, I. CNSB004 (Leconotide) causes antihyperalgesia without side effects when given intravenously: A comparison with ziconotide in a rat model of diabetic neuropathic pain. Pain Med., 2010, 11(2), 262-273.
[http://dx.doi.org/10.1111/j.1526-4637.2009.00741.x] [PMID: 20002322]
[112]
Harvey, A.L. Toxins and drug discovery. Toxicon, 2014, 92, 193-200.
[http://dx.doi.org/10.1016/j.toxicon.2014.10.020] [PMID: 25448391]
[113]
Wen, L.; Yang, S.; Qiao, H.; Liu, Z.; Zhou, W.; Zhang, Y.; Huang, P. SO-3, a new O-superfamily conopeptide derived from Conus striatus, selectively inhibits N-type calcium currents in cultured hippocampal neurons. Br. J. Pharmacol., 2005, 145(6), 728-739.
[http://dx.doi.org/10.1038/sj.bjp.0706223] [PMID: 15880145]
[114]
Lu, B.S.; Yu, F.; Zhao, D.; Huang, P.T.; Huang, C.F. Conopeptides from Conus striatus and Conus textile by cDNA cloning. Peptides, 1999, 20(10), 1139-1144.
[http://dx.doi.org/10.1016/S0196-9781(99)00116-3] [PMID: 10573284]
[115]
Dai, Q.; Liu, F.; Zhou, Y.; Lu, B.; Yu, F.; Huang, P. The synthesis of SO-3, a conopeptide with high analgesic activity derived from Conus striatus. J. Nat. Prod., 2003, 66(9), 1276-1279.
[http://dx.doi.org/10.1021/np030099y] [PMID: 14510617]
[116]
Yan, L.D.; Liu, Y.L.; Zhang, L.; Dong, H.J.; Zhou, P.L.; Su, R.B.; Gong, Z.H.; Huang, P.T. Spinal antinociception of synthetic omega-conotoxin SO-3, a selective N-type neuronal voltage-sensitive calcium channel blocker, and its effects on morphine analgesia in chemical stimulus tests in rodent. Eur. J. Pharmacol., 2010, 636(1-3), 73-81.
[http://dx.doi.org/10.1016/j.ejphar.2010.03.036] [PMID: 20361956]
[117]
Lee, S.; Kim, Y.; Back, S.K.; Choi, H.W.; Lee, J.Y.; Jung, H.H.; Ryu, J.H.; Suh, H.W.; Na, H.S.; Kim, H.J.; Rhim, H.; Kim, J.I. Analgesic effect of highly reversible ω-conotoxin FVIA on N type Ca2+ channels. Mol. Pain, 2010, 6, 97.
[http://dx.doi.org/10.1186/1744-8069-6-97] [PMID: 21172037]
[118]
Berecki, G.; Motin, L.; Haythornthwaite, A.; Vink, S.; Bansal, P.; Drinkwater, R.; Wang, C.I.; Moretta, M.; Lewis, R.J.; Alewood, P.F.; Christie, M.J.; Adams, D.J. Analgesic (ω)-conotoxins CVIE and CVIF selectively and voltage-dependently block recombinant and native N-type calcium channels. Mol. Pharmacol., 2010, 77(2), 139-148.
[http://dx.doi.org/10.1124/mol.109.058834] [PMID: 19892914]
[119]
Sousa, S.R.; McArthur, J.R.; Brust, A.; Bhola, R.F.; Rosengren, K.J.; Ragnarsson, L.; Dutertre, S.; Alewood, P.F.; Christie, M.J.; Adams, D.J.; Vetter, I.; Lewis, R.J. Novel analgesic ω-conotoxins from the vermivorous cone snail Conus moncuri provide new insights into the evolution of conopeptides. Sci. Rep., 2018, 8(1), 13397.
[http://dx.doi.org/10.1038/s41598-018-31245-4] [PMID: 30194442]
[120]
Bernáldez, J.; Román-González, S.A.; Martínez, O.; Jiménez, S.; Vivas, O.; Arenas, I.; Corzo, G.; Arreguín, R.; García, D.E.; Possani, L.D.; Licea, A. A Conus regularis conotoxin with a novel eight-cysteine framework inhibits CaV2.2 channels and displays an anti-nociceptive activity. Mar. Drugs, 2013, 11(4), 1188-1202.
[http://dx.doi.org/10.3390/md11041188] [PMID: 23567319]
[121]
Liu, Z.; Bartels, P.; Sadeghi, M.; Du, T.; Dai, Q.; Zhu, C.; Yu, S.; Wang, S.; Dong, M.; Sun, T.; Guo, J.; Peng, S.; Jiang, L.; Adams, D.J.; Dai, Q. A novel α-conopeptide Eu1.6 inhibits N-type (CaV2.2) calcium channels and exhibits potent analgesic activity. Sci. Rep., 2018, 8(1), 1004.
[http://dx.doi.org/10.1038/s41598-017-18479-4] [PMID: 29343689]
[122]
Callaghan, B.; Adams, D.J. Analgesic α-conotoxins Vc1.1 and RgIA inhibit N-type calcium channels in sensory neurons of α9 nicotinic receptor knockout mice. Channels (Austin), 2010, 4(1), 51-54.
[http://dx.doi.org/10.4161/chan.4.1.10281] [PMID: 20368690]
[123]
Klimis, H.; Adams, D.J.; Callaghan, B.; Nevin, S.; Alewood, P.F.; Vaughan, C.W.; Mozar, C.A.; Christie, M.J. A novel mechanism of inhi-bition of high-voltage activated calcium channels by α-conotoxins contributes to relief of nerve injury-induced neuropathic pain. Pain, 2011, 152(2), 259-266.
[http://dx.doi.org/10.1016/j.pain.2010.09.007] [PMID: 20889259]
[124]
Callaghan, B.; Haythornthwaite, A.; Berecki, G.; Clark, R.J.; Craik, D.J.; Adams, D.J. Analgesic α-conotoxins Vc1.1 and Rg1A inhibit N-type calcium channels in rat sensory neurons via GABAB receptor activation. J. Neurosci., 2008, 28(43), 10943-10951.
[http://dx.doi.org/10.1523/JNEUROSCI.3594-08.2008] [PMID: 18945902]
[125]
Romero, H.K.; Christensen, S.B.; Di Cesare Mannelli, L.; Gajewiak, J.; Ramachandra, R.; Elmslie, K.S.; Vetter, D.E.; Ghelardini, C.; Iado-nato, S.P.; Mercado, J.L.; Olivera, B.M.; McIntosh, J.M. Inhibition of α9α10 nicotinic acetylcholine receptors prevents chemotherapy-induced neuropathic pain. Proc. Natl. Acad. Sci. USA, 2017, 114(10), E1825-E1832.
[http://dx.doi.org/10.1073/pnas.1621433114] [PMID: 28223528]
[126]
Bordon, K.C.F.; Cologna, C.T.; Fornari-Baldo, E.C.; Pinheiro-Júnior, E.L.; Cerni, F.A.; Amorim, F.G.; Anjolette, F.A.P.; Cordeiro, F.A.; Wiezel, G.A.; Cardoso, I.A.; Ferreira, I.G.; de Oliveira, I.S.; Boldrini-França, J.; Pucca, M.B.; Baldo, M.A.; Arantes, E.C. From animal poi-sons and venoms to medicines: Achievements, challenges and perspectives in drug discovery. Front. Pharmacol., 2020, 11, 1132.
[http://dx.doi.org/10.3389/fphar.2020.01132] [PMID: 32848750]
[127]
Chen, J.Q.; Zhang, Y.Q.; Dai, J.; Luo, Z.M.; Liang, S.P. Antinociceptive effects of intrathecally administered huwentoxin-I, a selective N-type calcium channel blocker, in the formalin test in conscious rats. Toxicon, 2005, 45(1), 15-20.
[http://dx.doi.org/10.1016/j.toxicon.2004.08.018] [PMID: 15581678]
[128]
Wen Tao, Z.; Gu Yang, T.; Ying, R.; Mao Cai, W.; Lin, L.; Chi Miao, L.; Peng, H.; Joa Qin, C. The antinociceptive efficacy of HWTX-I epidurally administered in rheumatoid arthritis rats. Int. J. Sports Med., 2011, 32(11), 869-874.
[http://dx.doi.org/10.1055/s-0031-1280775] [PMID: 22052031]
[129]
Deng, M.; Luo, X.; Xiao, Y.; Sun, Z.; Jiang, L.; Liu, Z.; Zeng, X.; Chen, H.; Tang, J. Zeng, W.; Songping Liang, Huwentoxin-XVI, an anal-gesic, highly reversible mammalian N-type calcium channel antagonist from Chinese Tarantula ornithoctonus huwena. Neuropharmacology, 2014, 79, 657-667.
[http://dx.doi.org/10.1016/j.neuropharm.2014.01.017] [PMID: 24467846]
[130]
Gewehr, C.; Oliveira, S.M.; Rossato, M.F.; Trevisan, G.; Dalmolin, G.D.; Rigo, F.K.; de Castro Júnior, C.J.; Cordeiro, M.N.; Ferreira, J.; Gomez, M.V. Mechanisms involved in the nociception triggered by the venom of the armed spider Phoneutria nigriventer. PLoS Negl. Trop. Dis., 2013, 7(4), e2198.
[http://dx.doi.org/10.1371/journal.pntd.0002198] [PMID: 23638210]
[131]
ordeiro, Mdo, M. N.; de Figueiredo, S.G.; Valentim, Ado.C.; Diniz, C.R.; von Eickstedt, V.R.; Gilroy, J.; Richardson, M. Purification and amino acid sequences of six Tx3 type neurotoxins from the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keys). Toxicon, 1993, 31(1), 35-42.
[http://dx.doi.org/10.1016/0041-0101(93)90354-L] [PMID: 8446961]
[132]
Vieira, L.B.; Kushmerick, C.; Reis, H.J.; Diniz, C.R.; Cordeiro, M.N.; Prado, M.A.M.; Kalapothakis, E.; Romano-Silva, M.A.; Gomez, M.V. PnTx3-6 a spider neurotoxin inhibits K+-evoked increase in [Ca2+](i) and Ca2+-dependent glutamate release in synaptosomes. Neurochem. Int., 2003, 42(4), 277-282.
[http://dx.doi.org/10.1016/S0197-0186(02)00130-4] [PMID: 12470700]
[133]
Vieira, L.B.; Kushmerick, C.; Hildebrand, M.E.; Garcia, E.; Stea, A.; Cordeiro, M.N.; Richardson, M.; Gomez, M.V.; Snutch, T.P. Inhibi-tion of high voltage-activated calcium channels by spider toxin PnTx3-6. J. Pharmacol. Exp. Ther., 2005, 314(3), 1370-1377.
[http://dx.doi.org/10.1124/jpet.105.087023] [PMID: 15933156]
[134]
Souza, A.H.; Ferreira, J.; Cordeiro, M.D.N.; Vieira, L.B.; De Castro, C.J.; Trevisan, G.; Reis, H.; Souza, I.A.; Richardson, M.; Prado, M.A.M.; Prado, V.F.; Gomez, M.V. Analgesic effect in rodents of native and recombinant Ph alpha 1beta toxin, a high-voltage-activated calcium channel blocker isolated from armed spider venom. Pain, 2008, 140(1), 115-126.
[http://dx.doi.org/10.1016/j.pain.2008.07.014] [PMID: 18774645]
[135]
Souza, A.H.; Ferreira, J.; Cordeiro, M.D.N.; Vieira, L.B.; De Castro, C.J.; Trevisan, G.; Reis, H.; Souza, I.A.; Richardson, M.; Prado, M.A.M.; Prado, V.F.; Gomez, M.V. Analgesic effect in rodents of native and recombinant Ph α 1β toxin, a high-voltage-activated calcium channel blocker isolated from armed spider venom. Pain, 2008, 140(1), 115-126.
[http://dx.doi.org/10.1016/j.pain.2008.07.014] [PMID: 18774645]
[136]
de Souza, A.H.; Castro, C.J., Jr; Rigo, F.K.; de Oliveira, S.M.; Gomez, R.S.; Diniz, D.M.; Borges, M.H.; Cordeiro, M.N.; Silva, M.A.; Fer-reira, J.; Gomez, M.V. An evaluation of the antinociceptive effects of Phα1β a neurotoxin from the spider Phoneutria nigriventer, and ω-conotoxin MVIIA, a cone snail Conus magus toxin, in rat model of inflammatory and neuropathic pain. Cell. Mol. Neurobiol., 2013, 33(1), 59-67.
[http://dx.doi.org/10.1007/s10571-012-9871-x] [PMID: 22869352]
[137]
Iftinca, M.; Defaye, M.; Altier, C. TRPV1-targeted drugs in development for human pain conditions. Drugs, 2021, 81(1), 7-27.
[http://dx.doi.org/10.1007/s40265-020-01429-2] [PMID: 33165872]
[138]
Castro-Junior, C.J. Milano, J.; Souza, A.H.; Silva, J.F.; Rigo, F.K.; Dalmolin, G.; Cordeiro, M.N.; Richardson, M.; Barros, A.G.; Gomez, R.S.; Silva, M.A.; Kushmerick, C.; Ferreira, J.; Gomez, M.V. Phα1β toxin prevents capsaicin-induced nociceptive behavior and mechanical hypersensitivity without acting on TRPV1 channels. Neuropharmacology, 2013, 71, 237-246.
[http://dx.doi.org/10.1016/j.neuropharm.2013.04.001] [PMID: 23597507]
[139]
Palhares, M.R.; Silva, J.F.; Rezende, M.J.S.; Santos, D.C.; Silva-Junior, C.A.; Borges, M.H.; Ferreira, J.; Gomez, M.V.; Castro-Junior, C.J. Synergistic antinociceptive effect of a calcium channel blocker and a TRPV1 blocker in an acute pain model in mice. Life Sci., 2017, 182, 122-128.
[http://dx.doi.org/10.1016/j.lfs.2017.06.018] [PMID: 28629730]
[140]
Diniz, D.M.; de Souza, A.H.; Pereira, E.M.R.; da Silva, J.F.; Rigo, F.K.; Romano-Silva, M.A.; Binda, N.; Castro, C.J., Jr; Cordeiro, M.N.; Ferreira, J.; Gomez, M.V. Effects of the calcium channel blockers Phα1β and ω-conotoxin MVIIA on capsaicin and acetic acid-induced visceral nociception in mice. Pharmacol. Biochem. Behav., 2014, 126, 97-102.
[http://dx.doi.org/10.1016/j.pbb.2014.09.017] [PMID: 25268314]
[141]
Koivisto, A.; Jalava, N.; Bratty, R.; Pertovaara, A. TRPA1 antagonists for pain relief. Pharmaceuticals (Basel), 2018, 11(4), E117.
[http://dx.doi.org/10.3390/ph11040117] [PMID: 30388732]
[142]
Tonello, R.; Fusi, C.; Materazzi, S.; Marone, I.M.; De Logu, F.; Benemei, S.; Gonçalves, M.C.; Coppi, E.; Castro-Junior, C.J.; Gomez, M.V.; Geppetti, P.; Ferreira, J.; Nassini, R. The peptide Phα1β from spider venom, acts as a TRPA1 channel antagonist with antinocicep-tive effects in mice. Br. J. Pharmacol., 2017, 174(1), 57-69.
[http://dx.doi.org/10.1111/bph.13652] [PMID: 27759880]
[143]
Rigo, F.K.; Trevisan, G.; De Prá, S.D-T.; Cordeiro, M.N.; Borges, M.H.; Silva, J.F.; Santa Cecilia, F.V.; de Souza, A.H. de Oliveira Ada-mante, G.; Milioli, A.M.; de Castro Junior, C.J.; Ferreira, J.; Gomez, M.V. The spider toxin Phα1β recombinant possesses strong analgesic activity. Toxicon, 2017, 133, 145-152.
[http://dx.doi.org/10.1016/j.toxicon.2017.05.018] [PMID: 28526335]
[144]
Antunes, F.T.T.; Angelo, S.G.; Dallegrave, E.; Picada, J.N.; Marroni, N.P.; Schemitt, E.; Ferraz, A.G.; Gomez, M.V.; de Souza, A.H. Re-combinant peptide derived from the venom the Phoneutria nigriventer spider relieves nociception by nerve deafferentation. Neuropeptides, 2020, 79, 101980.
[http://dx.doi.org/10.1016/j.npep.2019.101980] [PMID: 31711615]
[145]
Rigo, F.K.; Rossato, M.F.; Borges, V.; da Silva, J.F.; Pereira, E.M.R.; de Ávila, R.A.M.; Trevisan, G.; Dos Santos, D.C.; Diniz, D.M.; Silva, M.A.R.; de Castro, C.J.; Cunha, T.M.; Ferreira, J.; Gomez, M.V. Analgesic and side effects of intravenous recombinant Phα1β. J. Venom. Anim. Toxins Incl. Trop. Dis., 2020, 26, e20190070.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2019-0070] [PMID: 32362927]
[146]
de Souza, A.H.; Lima, M.C.; Drewes, C.C.; da Silva, J.F.; Torres, K.C.L.; Pereira, E.M.R.; de Castro Junior, C.J.; Vieira, L.B.; Cordeiro, M.N.; Richardson, M.; Gomez, R.S.; Romano-Silva, M.A.; Ferreira, J.; Gomez, M.V. Antiallodynic effect and side effects of Phα1β a neu-rotoxin from the spider Phoneutria nigriventer: Comparison with ω-conotoxin MVIIA and morphine. Toxicon, 2011, 58(8), 626-633.
[http://dx.doi.org/10.1016/j.toxicon.2011.09.008] [PMID: 21967810]
[147]
Tonello, R. Trevisan, G.; Luckemeyer, D.; Castro-Junior, C.J.; Gomez, M.V.; Ferreira, J. Phα1β a dual blocker of TRPA1 and Cav2.2, as an adjuvant drug in opioid therapy for postoperative pain. Toxicon, 2020, 188, 80-88.
[http://dx.doi.org/10.1016/j.toxicon.2020.10.007] [PMID: 33038354]
[148]
Tonello, R.; Rigo, F.; Gewehr, C.; Trevisan, G.; Pereira, E.M.R.; Gomez, M.V.; Ferreira, J. Action of Phα1β a peptide from the venom of the spider Phoneutria nigriventer, on the analgesic and adverse effects caused by morphine in mice. J. Pain, 2014, 15(6), 619-631.
[http://dx.doi.org/10.1016/j.jpain.2014.02.007] [PMID: 24607814]
[149]
Rigo, F.K.; Dalmolin, G.D.; Trevisan, G.; Tonello, R.; Silva, M.A.; Rossato, M.F.; Klafke, J.Z. Cordeiro, Mdo.N.; Castro Junior, C.J.; Montijo, D.; Gomez, M.V.; Ferreira, J. Effect of ω-conotoxin MVIIA and Phα1β on paclitaxel-induced acute and chronic pain. Pharmacol. Biochem. Behav., 2013, 114-115, 16-22.
[http://dx.doi.org/10.1016/j.pbb.2013.10.014] [PMID: 24148893]
[150]
Rigo, F.K.; Trevisan, G.; Rosa, F.; Dalmolin, G.D.; Otuki, M.F.; Cueto, A.P.; de Castro Junior, C.J.; Romano-Silva, M.A. Cordeiro, Mdo.N.; Richardson, M.; Ferreira, J.; Gomez, M.V. Spider peptide Phα1β induces analgesic effect in a model of cancer pain. Cancer Sci., 2013, 104(9), 1226-1230.
[http://dx.doi.org/10.1111/cas.12209] [PMID: 23718272]
[151]
de Souza, A.H.; da Costa Lopes, A.M.; Castro, C.J., Jr; Pereira, E.M.R.; Klein, C.P.; da Silva, C.A., Jr; da Silva, J.F.; Ferreira, J.; Gomez, M.V. The effects of Phα1β a spider toxin, calcium channel blocker, in a mouse fibromyalgia model. Toxicon, 2014, 81, 37-42.
[http://dx.doi.org/10.1016/j.toxicon.2014.01.015] [PMID: 24491352]
[152]
Rosa, F.; Trevisan, G.; Rigo, F.K.; Tonello, R.; Andrade, E.L. Cordeiro, Mdo.N.; Calixto, J.B.; Gomez, M.V.; Ferreira, J. Phα1β a peptide from the venom of the spider Phoneutria nigriventer shows antinociceptive effects after continuous infusion in a neuropathic pain model in rats. Anesth. Analg., 2014, 119(1), 196-202.
[http://dx.doi.org/10.1213/ANE.0000000000000249] [PMID: 24836473]
[153]
Silva, R.B.M.; Greggio, S.; Venturin, G.T.; da Costa, J.C.; Gomez, M.V.; Campos, M.M. Beneficial effects of the calcium channel blocker CTK 01512-2 in a mouse model of multiple sclerosis. Mol. Neurobiol., 2018, 55(12), 9307-9327.
[http://dx.doi.org/10.1007/s12035-018-1049-1] [PMID: 29667130]
[154]
Tenza-Ferrer, H. Magno, L.A.V.; Romano-Silva, M.A.; da Silva, J.F.; Gomez, M.V. Phα1β spider toxin reverses glial structural plasticity upon peripheral inflammation. Front. Cell. Neurosci., 2019, 13, 306.
[http://dx.doi.org/10.3389/fncel.2019.00306] [PMID: 31354431]
[155]
da Silva Junior, C.A.; de Castro Junior, C.J.; Pereira, E.M.R.; Binda, N.S.; da Silva, J.F.; do Nascimento Cordeiro, M.; Diniz, D.M.; Cecilia, F.S.; Ferreira, J.; Gomez, M.V. The inhibitory effect of Phα1β toxin on diabetic neuropathic pain involves the CXCR4 chemokine receptor. Pharmacol. Rep., 2020, 72(1), 47-54.
[http://dx.doi.org/10.1007/s43440-019-00002-3] [PMID: 32016848]
[156]
De Prá, S.D.T.; Antoniazzi, C.T.D.; Ferro, P.R.; Kudsi, S.Q.; Camponogara, C.; Fialho, M.F.P.; Rigo, F.K.; Gomez, M.V.; Bochi, G.V.; Moresco, R.N.; Oliveira, S.M.; Trevisan, G. Nociceptive mechanisms involved in the acute and chronic phases of a complex regional pain syndrome type 1 model in mice. Eur. J. Pharmacol., 2019, 859, 172555.
[http://dx.doi.org/10.1016/j.ejphar.2019.172555] [PMID: 31326377]
[157]
Caminski, E.S.; de Freitas, L.M.; Dallegrave, E.; Junior, C.A.D.S.; Gomez, M.V.; Pereira, E.M.R.; Antunes, F.T.T.; de Souza, A.H. Analge-sic effects of the CTK 01512-2 toxin in different models of orofacial pain in rats. Pharmacol. Rep., 2020, 72(3), 600-611.
[http://dx.doi.org/10.1007/s43440-020-00108-z] [PMID: 32399819]
[158]
Ricardo, C.V.P.; Figueira da Silva, J.; Buzelin, M.A.; Antônio da Silva Júnior, C.; Carvalho Dos Santos, D.; Montijo Diniz, D.; Binda, N.S.; Borges, M.H.; Senna Guimarães, A.L.; Rita Pereira, E.M.; Gomez, M.V. Calcium channels blockers toxins attenuate abdominal hyperalge-sia and inflammatory response associated with the cerulein-induced acute pancreatitis in rats. Eur. J. Pharmacol., 2021, 891, 173672.
[http://dx.doi.org/10.1016/j.ejphar.2020.173672] [PMID: 33190801]
[159]
Zamponi, G.W.; Lory, P.; Perez-Reyes, E. Role of voltage-gated calcium channels in epilepsy. Pflugers Arch., 2010, 460(2), 395-403.
[http://dx.doi.org/10.1007/s00424-009-0772-x] [PMID: 20091047]
[160]
Khosravani, H.; Zamponi, G.W. Voltage-gated calcium channels and idiopathic generalized epilepsies. Physiol. Rev., 2006, 86(3), 941-966.
[http://dx.doi.org/10.1152/physrev.00002.2006] [PMID: 16816142]
[161]
Cao, Y.Q. Voltage-gated calcium channels and pain. Pain, 2006, 126(1-3), 5-9.
[http://dx.doi.org/10.1016/j.pain.2006.10.019] [PMID: 17084979]
[162]
Jacus, M.O.; Uebele, V.N.; Renger, J.J.; Todorovic, S.M. Presynaptic Cav3.2 channels regulate excitatory neurotransmission in nociceptive dorsal horn neurons. J. Neurosci., 2012, 32(27), 9374-9382.
[http://dx.doi.org/10.1523/JNEUROSCI.0068-12.2012] [PMID: 22764245]
[163]
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]
[164]
François, A.; Laffray, S.; Pizzoccaro, A.; Eschalier, A.; Bourinet, E. T-type calcium channels in chronic pain: Mouse models and specific blockers. Pflugers Arch., 2014, 466(4), 707-717.
[http://dx.doi.org/10.1007/s00424-014-1484-4] [PMID: 24590509]
[165]
Scroggs, R.S.; Fox, A.P. Calcium current variation between acutely isolated adult rat dorsal root ganglion neurons of different size. J. Physiol., 1992, 445, 639-658.
[http://dx.doi.org/10.1113/jphysiol.1992.sp018944] [PMID: 1323671]
[166]
Talley, E.M.; Cribbs, L.L.; Lee, J.H.; Daud, A.; Perez-Reyes, E.; Bayliss, D.A. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci., 1999, 19(6), 1895-1911.
[http://dx.doi.org/10.1523/JNEUROSCI.19-06-01895.1999] [PMID: 10066243]
[167]
Todorovic, S.M.; Lingle, C.J. Pharmacological properties of T-type Ca2+ current in adult rat sensory neurons: Effects of anticonvulsant and anesthetic agents. J. Neurophysiol., 1998, 79(1), 240-252.
[http://dx.doi.org/10.1152/jn.1998.79.1.240] [PMID: 9425195]
[168]
Jagodic, M.M.; Pathirathna, S.; Joksovic, P.M.; Lee, W.; Nelson, M.T.; Naik, A.K.; Su, P.; Jevtovic-Todorovic, V.; Todorovic, S.M. Up-regulation of the T-type calcium current in small rat sensory neurons after chronic constrictive injury of the sciatic nerve. J. Neurophysiol., 2008, 99(6), 3151-3156.
[http://dx.doi.org/10.1152/jn.01031.2007] [PMID: 18417624]
[169]
Jagodic, M.M.; Pathirathna, S.; Nelson, M.T.; Mancuso, S.; Joksovic, P.M.; Rosenberg, E.R.; Bayliss, D.A.; Jevtovic-Todorovic, V.; Todo-rovic, S.M. Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J. Neurosci., 2007, 27(12), 3305-3316.
[http://dx.doi.org/10.1523/JNEUROSCI.4866-06.2007] [PMID: 17376991]
[170]
Wen, X-J.; Xu, S-Y.; Chen, Z-X.; Yang, C-X.; Liang, H.; Li, H. The roles of T-type calcium channel in the development of neuropathic pain following chronic compression of rat dorsal root ganglia. Pharmacology, 2010, 85(5), 295-300.
[http://dx.doi.org/10.1159/000276981] [PMID: 20453553]
[171]
Yue, J.; Liu, L.; Liu, Z.; Shu, B.; Zhang, Y. Upregulation of T-type Ca2+ channels in primary sensory neurons in spinal nerve injury. Spine, 2013, 38(6), 463-470.
[http://dx.doi.org/10.1097/BRS.0b013e318272fbf8] [PMID: 22972512]
[172]
Okubo, K.; Takahashi, T.; Sekiguchi, F.; Kanaoka, D.; Matsunami, M.; Ohkubo, T.; Yamazaki, J.; Fukushima, N.; Yoshida, S.; Kawabata, A. Inhibition of T-type calcium channels and hydrogen sulfide-forming enzyme reverses paclitaxel-evoked neuropathic hyperalgesia in rats. Neuroscience, 2011, 188, 148-156.
[http://dx.doi.org/10.1016/j.neuroscience.2011.05.004] [PMID: 21596106]
[173]
Shin, S.M.; Cai, Y.; Itson-Zoske, B.; Qiu, C.; Hao, X.; Xiang, H.; Hogan, Q.H.; Yu, H. Enhanced T-type calcium channel 3.2 activity in sensory neurons contributes to neuropathic-like pain of monosodium iodoacetate-induced knee osteoarthritis. Mol. Pain, 2020, 16, 1744806920963807.
[http://dx.doi.org/10.1177/1744806920963807] [PMID: 33054557]
[174]
Takahashi, T.; Aoki, Y.; Okubo, K.; Maeda, Y.; Sekiguchi, F.; Mitani, K.; Nishikawa, H.; Kawabata, A. Upregulation of Ca(v)3.2 T-type calcium channels targeted by endogenous hydrogen sulfide contributes to maintenance of neuropathic pain. Pain, 2010, 150(1), 183-191.
[http://dx.doi.org/10.1016/j.pain.2010.04.022] [PMID: 20546998]
[175]
Bourinet, E.; Alloui, A.; Monteil, A.; Barrère, C.; Couette, B.; Poirot, O.; Pages, A.; McRory, J.; Snutch, T.P.; Eschalier, A.; Nargeot, J. Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J., 2005, 24(2), 315-324.
[http://dx.doi.org/10.1038/sj.emboj.7600515] [PMID: 15616581]
[176]
Messinger, R.B.; Naik, A.K.; Jagodic, M.M.; Nelson, M.T.; Lee, W.Y.; Choe, W.J.; Orestes, P.; Latham, J.R.; Todorovic, S.M.; Jevtovic-Todorovic, V. In vivo silencing of the CaV3. 2 T-type calcium channels in sensory neurons alleviates hyperalgesia in rats with streptozo-cin-induced diabetic neuropathy. Pain, 2009, 145(1-2), 184-195.
[http://dx.doi.org/10.1016/j.pain.2009.06.012] [PMID: 19577366]
[177]
Dajas-Bailador, F.; Costa, G.; Dajas, F.; Emmett, S. Effects of α-erabutoxin, α-bungarotoxin, α-cobratoxin and fasciculin on the nicotine-evoked release of dopamine in the rat striatum in vivo. Neurochem. Int., 1998, 33(4), 307-312.
[http://dx.doi.org/10.1016/S0197-0186(98)00033-3] [PMID: 9840221]
[178]
Zeng, H.; Hawrot, E. NMR-based binding screen and structural analysis of the complex formed between α-cobratoxin and an 18-mer cog-nate peptide derived from the α 1 subunit of the nicotinic acetylcholine receptor from Torpedo californica. J. Biol. Chem., 2002, 277(40), 37439-37445.
[http://dx.doi.org/10.1074/jbc.M205483200] [PMID: 12133834]
[179]
Zhang, L.; Zhang, Y.; Jiang, D.; Reid, P.F.; Jiang, X.; Qin, Z.; Tao, J. Alpha-cobratoxin inhibits T-type calcium currents through muscarinic M4 receptor and Gο-protein βγ subunits-dependent protein kinase A pathway in dorsal root ganglion neurons. Neuropharmacology, 2012, 62(2), 1062-1072.
[http://dx.doi.org/10.1016/j.neuropharm.2011.10.017] [PMID: 22074645]
[180]
Chen, Z.X.; Zhang, H.L.; Gu, Z.L.; Chen, B.W.; Han, R.; Reid, P.F.; Raymond, L.N.; Qin, Z.H. A long-form α-neurotoxin from cobra ven-om produces potent opioid-independent analgesia. Acta Pharmacol. Sin., 2006, 27(4), 402-408.
[http://dx.doi.org/10.1111/j.1745-7254.2006.00293.x] [PMID: 16539838]
[181]
Joksimovic, S.L.; Joksimovic, S.M.; Manzella, F.M.; Asnake, B.; Orestes, P.; Raol, Y.H.; Krishnan, K.; Covey, D.F.; Jevtovic-Todorovic, V.; Todorovic, S.M. Novel neuroactive steroid with hypnotic and T-type calcium channel blocking properties exerts effective analgesia in a rodent model of post-surgical pain. Br. J. Pharmacol., 2020, 177(8), 1735-1753.
[http://dx.doi.org/10.1111/bph.14930] [PMID: 31732978]
[182]
Hess, P.; Lansman, J.B.; Tsien, R.W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antag-onists. Nature, 1984, 311(5986), 538-544.
[http://dx.doi.org/10.1038/311538a0] [PMID: 6207437]
[183]
Hardingham, G.E.; Chawla, S.; Johnson, C.M.; Bading, H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature, 1997, 385(6613), 260-265.
[http://dx.doi.org/10.1038/385260a0] [PMID: 9000075]
[184]
Greenberg, M.E.; Ziff, E.B.; Greene, L.A. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science (80-), 1986, 234,, 80-83.
[http://dx.doi.org/10.1126/science.3749894]
[185]
Morgan, J.I.; Curran, T. Role of ion flux in the control of c-fos expression. Nature, 1986, 322(6079), 552-555.
[http://dx.doi.org/10.1038/322552a0] [PMID: 2426600]
[186]
D’Arco, M.; Dolphin, A.C. L-type calcium channels: On the fast track to nuclear signaling. Sci. Signal., 2012, 5(237), pe34.
[http://dx.doi.org/10.1126/scisignal.2003355] [PMID: 22894834]
[187]
Deisseroth, K.; Mermelstein, P.G.; Xia, H.; Tsien, R.W. Signaling from synapse to nucleus: The logic behind the mechanisms. Curr. Opin. Neurobiol., 2003, 13(3), 354-365.
[http://dx.doi.org/10.1016/S0959-4388(03)00076-X] [PMID: 12850221]
[188]
Fossat, P.; Sibon, I.; Le Masson, G.; Landry, M.; Nagy, F. L-type calcium channels and NMDA receptors: A determinant duo for short-term nociceptive plasticity. Eur. J. Neurosci., 2007, 25(1), 127-135.
[http://dx.doi.org/10.1111/j.1460-9568.2006.05256.x] [PMID: 17241274]
[189]
Roca-Lapirot, O.; Radwani, H.; Aby, F.; Nagy, F.; Landry, M.; Fossat, P. Calcium signalling through L-type calcium channels: Role in pathophysiology of spinal nociceptive transmission. Br. J. Pharmacol., 2018, 175(12), 2362-2374.
[http://dx.doi.org/10.1111/bph.13747] [PMID: 28214378]
[190]
Berridge, M.J. Neuronal calcium signaling. RE:view, 1998, 21, 13-26.
[191]
Obermair, G.J.; Szabo, Z.; Bourinet, E.; Flucher, B.E. Differential targeting of the L-type Ca2+ channel α 1C (CaV1.2) to synaptic and ex-trasynaptic compartments in hippocampal neurons. Eur. J. Neurosci., 2004, 19(8), 2109-2122.
[http://dx.doi.org/10.1111/j.0953-816X.2004.03272.x] [PMID: 15090038]
[192]
Fossat, P.; Dobremez, E.; Bouali-Benazzouz, R.; Favereaux, A.; Bertrand, S.S.; Kilk, K.; Léger, C.; Cazalets, J.R.; Langel, U.; Landry, M.; Nagy, F. Knockdown of L calcium channel subtypes: Differential effects in neuropathic pain. J. Neurosci., 2010, 30(3), 1073-1085.
[http://dx.doi.org/10.1523/JNEUROSCI.3145-09.2010] [PMID: 20089916]
[193]
Clark, N.C.; Nagano, N.; Kuenzi, F.M.; Jarolimek, W.; Huber, I.; Walter, D.; Wietzorrek, G.; Boyce, S.; Kullmann, D.M.; Striessnig, J.; Seabrook, G.R. Neurological phenotype and synaptic function in mice lacking the CaV1.3 alpha subunit of neuronal L-type voltage-dependent Ca2+ channels. Neuroscience, 2003, 120(2), 435-442.
[http://dx.doi.org/10.1016/S0306-4522(03)00329-4] [PMID: 12890513]
[194]
Favereaux, A.; Thoumine, O.; Bouali-Benazzouz, R.; Roques, V.; Papon, M-A.; Salam, S.A.; Drutel, G.; Léger, C.; Calas, A.; Nagy, F.; Landry, M. Bidirectional integrative regulation of Cav1.2 calcium channel by microRNA miR-103: Role in pain. EMBO J., 2011, 30(18), 3830-3841.
[http://dx.doi.org/10.1038/emboj.2011.249] [PMID: 21804529]
[195]
Oliveira, S.M.; Silva, C.R.; Trevisan, G.; Villarinho, J.G.; Cordeiro, M.N.; Richardson, M.; Borges, M.H.; Castro, C.J., Jr; Gomez, M.V.; Ferreira, J. Antinociceptive effect of a novel armed spider peptide Tx3-5 in pathological pain models in mice. Pflugers Arch., 2016, 468(5), 881-894.
[http://dx.doi.org/10.1007/s00424-016-1801-1] [PMID: 26898377]
[196]
Quijada, L.; Germany, A.; Hernández, C.E.; Contreras, E. Effects of calcium channel antagonists and Bay K 8644 on the analgesic re-sponse to pentazocine and U 50488H. Gen. Pharmacol., 1992, 23(5), 837-842.
[http://dx.doi.org/10.1016/0306-3623(92)90234-B] [PMID: 1385259]
[197]
Zbuzek, K.; Avenue, S.O. Vlasta Cohen and Wen-hsien Wu UMD-New Jersey Medical Department of Anesthesiology. 1997, 60
[198]
Dobremez, E.; Bouali-Benazzouz, R.; Fossat, P.; Monteils, L.; Dulluc, J.; Nagy, F.; Landry, M. Distribution and regulation of L-type calci-um channels in deep dorsal horn neurons after sciatic nerve injury in rats. Eur. J. Neurosci., 2005, 21(12), 3321-3333.
[http://dx.doi.org/10.1111/j.1460-9568.2005.04177.x] [PMID: 16026470]
[199]
Filos, K.S.; Goudas, L.C.; Patroni, O.; Tassoudis, V. Analgesia with epidural nimodipine. Lancet, 1993, 342(8878), 1047.
[http://dx.doi.org/10.1016/0140-6736(93)92899-5] [PMID: 8105273]
[200]
Santillán, R.; Hurlé, M.A.; Armijo, J.A.; de los Mozos, R.; Flórez, J. Nimodipine-enhanced opiate analgesia in cancer patients requiring morphine dose escalation: A double-blind, placebo-controlled study. Pain, 1998, 76(1-2), 17-26.
[http://dx.doi.org/10.1016/S0304-3959(98)00019-0] [PMID: 9696455]
[201]
Antkiewicz-Michaluk, L.; Michaluk, J. Romańska, I.; Vetulani, J. Reduction of morphine dependence and potentiation of analgesia by chronic co-administration of nifedipine. Psychopharmacology (Berl.), 1993, 111(4), 457-464.
[http://dx.doi.org/10.1007/BF02253536] [PMID: 7870987]
[202]
Dierssen, M.; Flórez, J.; Hurlé, M.A. Calcium channel modulation by dihydropyridines modifies sufentanil-induced antinociception in acute and tolerant conditions. Naunyn Schmiedebergs Arch. Pharmacol., 1990, 342(5), 559-565.
[http://dx.doi.org/10.1007/BF00169046] [PMID: 1708855]
[203]
Verma, V.; Mediratta, P.K.S.K.; Sharma, K.K. Potentiation of analgesia and reversal of tolerance to morphine by calcium channel blockers. Indian J. Exp. Biol., 2001, 39(7), 636-642.
[PMID: 12019755]
[204]
Ray, S.B.; Mishra, P.; Verma, D.; Gupta, A.; Wadhwa, S. Nimodipine is more effective than nifedipine in attenuating morphine tolerance on chronic co-administration in the rat tail-flick test. Indian J. Exp. Biol., 2008, 46(4), 219-228.
[PMID: 18512330]
[205]
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]
[206]
Hagiwara, K.; Nakagawasai, O.; Murata, A.; Yamadera, F.; Miyoshi, I.; Tan-No, K.; Tadano, T.; Yanagisawa, T.; Iijima, T.; Murakami, M. Analgesic action of loperamide, an opioid agonist, and its blocking action on voltage-dependent Ca2+ channels. Neurosci. Res., 2003, 46(4), 493-497.
[http://dx.doi.org/10.1016/S0168-0102(03)00126-3] [PMID: 12871771]
[207]
Wu, L.G.; Borst, J.G.; Sakmann, B. R-type Ca2+ currents evoke transmitter release at a rat central synapse. Proc. Natl. Acad. Sci. USA, 1998, 95(8), 4720-4725.
[http://dx.doi.org/10.1073/pnas.95.8.4720] [PMID: 9539805]
[208]
Myoga, M.H.; Regehr, W.G. Calcium microdomains near R-type calcium channels control the induction of presynaptic long-term potentia-tion at parallel fiber to purkinje cell synapses. J. Neurosci., 2011, 31(14), 5235-5243.
[http://dx.doi.org/10.1523/JNEUROSCI.5252-10.2011] [PMID: 21471358]
[209]
Saegusa, H.; Matsuda, Y.; Tanabe, T. Effects of ablation of N- and R-type Ca2+ channels on pain transmission. Neurosci. Res., 2002, 43(1), 1-7.
[http://dx.doi.org/10.1016/S0168-0102(02)00017-2] [PMID: 12074836]
[210]
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]
[211]
da Silva, J.F.; Castro-Junior, C.J.; Oliveira, S.M.; Dalmolin, G.D.; Silva, C.R.; Vieira, L.B.; Diniz, D.M. Cordeiro, Mdo.N.; Ferreira, J.; Souza, A.H.; Gomez, M.V. Characterization of the antinociceptive effect of PhTx3-4, a toxin from Phoneutria nigriventer, in models of thermal, chemical and incisional pain in mice. Toxicon, 2015, 108, 53-61.
[http://dx.doi.org/10.1016/j.toxicon.2015.09.043] [PMID: 26435340]
[212]
Dos Santos, R.G.; Van Renterghem, C.; Martin-Moutot, N.; Mansuelle, P.; Cordeiro, M.N.; Diniz, C.R.; Mori, Y.; De Lima, M.E.; Seagar, M. Phoneutria nigriventer omega-phonetoxin IIA blocks the Cav2 family of calcium channels and interacts with omega-conotoxin-binding sites. J. Biol. Chem., 2002, 277(16), 13856-13862.
[http://dx.doi.org/10.1074/jbc.M112348200] [PMID: 11827974]
[213]
Dubel, S.J.; Starr, T.V.; Hell, J.; Ahlijanian, M.K.; Enyeart, J.J.; Catterall, W.A.; Snutch, T.P. Molecular cloning of the alpha-1 subunit of an omega-conotoxin-sensitive calcium channel. Proc. Natl. Acad. Sci. USA, 1992, 89(11), 5058-5062.
[http://dx.doi.org/10.1073/pnas.89.11.5058] [PMID: 1317580]
[214]
Lee, S. Pharmacological inhibition of voltage-gated Ca2+ channels for chronic pain relief. Curr. Neuropharmacol., 2013, 11(6), 606-620.
[http://dx.doi.org/10.2174/1570159X11311060005] [PMID: 24396337]
[215]
Plomp, J.J.; van den Maagdenberg, A.M.J.M.; Molenaar, P.C.; Frants, R.R.; Ferrari, M.D. Mutant P/Q-type calcium channel electrophysiol-ogy and migraine. Curr. Opin. Investig. Drugs, 2001, 2(9), 1250-1260.
[PMID: 11717812]
[216]
van den Maagdenberg, A.M.J.M.; Pietrobon, D.; Pizzorusso, T.; Kaja, S.; Broos, L.A.M.; Cesetti, T.; van de Ven, R.C.; Tottene, A.; van der Kaa, J.; Plomp, J.J.; Frants, R.R.; Ferrari, M.D.A. Cacna1a knockin migraine mouse model with increased susceptibility to cortical spread-ing depression. Neuron, 2004, 41(5), 701-710.
[http://dx.doi.org/10.1016/S0896-6273(04)00085-6] [PMID: 15003170]
[217]
Nimmrich, V.; Gross, G. P/Q-type calcium channel modulators. Br. J. Pharmacol., 2012, 167(4), 741-759.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02069.x] [PMID: 22670568]
[218]
Nebe, J. Vanegas, H.; Neugebauer, V.; Schaible, H.G. ω-agatoxin IVA, a P-type calcium channel antagonist, reduces nociceptive pro-cessing in spinal cord neurons with input from the inflamed but not from the normal knee joint--an electrophysiological study in the rat in vivo. Eur. J. Neurosci., 1997, 9(10), 2193-2201.
[http://dx.doi.org/10.1111/j.1460-9568.1997.tb01386.x] [PMID: 9421179]
[219]
Nebe, J.; Ebersberger, A.; Vanegas, H.; Schaible, H.G. Effects of ω-agatoxin IVA, a P-type calcium channel antagonist, on the development of spinal neuronal hyperexcitability caused by knee inflammation in rats. J. Neurophysiol., 1999, 81(6), 2620-2626.
[http://dx.doi.org/10.1152/jn.1999.81.6.2620] [PMID: 10368382]
[220]
Marinelli, S.; Eleuteri, C.; Vacca, V.; Strimpakos, G.; Mattei, E.; Severini, C.; Pavone, F.; Luvisetto, S. Effects of age-related loss of P/Q-type calcium channels in a mice model of peripheral nerve injury. Neurobiol. Aging, 2015, 36(1), 352-364.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.07.025] [PMID: 25150573]
[221]
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]
[222]
Luvisetto, S.; Marinelli, S.; Panasiti, M.S.; D’Amato, F.R.; Fletcher, C.F.; Pavone, F.; Pietrobon, D. Pain sensitivity in mice lacking the Ca(v)2.1alpha1 subunit of P/Q-type Ca2+ channels. Neuroscience, 2006, 142(3), 823-832.
[http://dx.doi.org/10.1016/j.neuroscience.2006.06.049] [PMID: 16890369]
[223]
Fukumoto, N.; Obama, Y.; Kitamura, N.; Niimi, K.; Takahashi, E.; Itakura, C.; Shibuya, I. Hypoalgesic behaviors of P/Q-type voltage-gated Ca2+ channel mutant mouse, rolling mouse Nagoya. Neuroscience, 2009, 160(1), 165-173.
[http://dx.doi.org/10.1016/j.neuroscience.2009.02.032] [PMID: 19248821]
[224]
Pietrobon, D; Moskowitz, M.A. PH75CH23-pietrobon pathophysiology of migraine. 2012.

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