Login Register Cart 0
Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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

Ion Channels-related Neuroprotection and Analgesia Mediated by Spider Venom Peptides

Author(s): Ana Caroline Nogueira Souza, Nancy Scardua Binda, Huemara Yuri Almeida, Célio José de Castro Júnior, Marcus Vinicius Gomez, Fabíola Mara Ribeiro and Juliana Figueira Da Silva*

Volume 24, Issue 5, 2023

Published on: 20 April, 2023

Page: [365 - 379] Pages: 15

DOI: 10.2174/1389203724666230328133102

Price: $65

conference banner
Abstract

Ion channels play critical roles in generating and propagating action potentials and in neurotransmitter release at a subset of excitatory and inhibitory synapses. Dysfunction of these channels has been linked to various health conditions, such as neurodegenerative diseases and chronic pain. Neurodegeneration is one of the underlying causes of a range of neurological pathologies, such as Alzheimer’s disease (AD), Parkinson’s disease (PD), cerebral ischemia, brain injury, and retinal ischemia. Pain is a symptom that can serve as an index of the severity and activity of a disease condition, a prognostic indicator, and a criterion of treatment efficacy. Neurological disorders and pain are conditions that undeniably impact a patient's survival, health, and quality of life, with possible financial consequences. Venoms are the best-known natural source of ion channel modulators. Venom peptides are increasingly recognized as potential therapeutic tools due to their high selectivity and potency gained through millions of years of evolutionary selection pressure. Spiders have been evolving complex and diverse repertoires of peptides in their venoms with vast pharmacological activities for more than 300 million years. These include peptides that potently and selectively modulate a range of targets, such as enzymes, receptors, and ion channels. Thus, components of spider venoms hold considerable capacity as drug candidates for alleviating or reducing neurodegeneration and pain. This review aims to summarize what is known about spider toxins acting upon ion channels, providing neuroprotective and analgesic effects.

Keywords: Ion channels, neuroprotection, analgesia, spider venom, spider toxins, spider peptides.

Next »
Graphical Abstract

[1]
Petkov, G.V. Ion channels.Pharmacology: Principles and Practice; Hacker, M.; Messer, W.; Bachmann, K., Eds.; Academic Press, 2009, pp. 387-427.
[http://dx.doi.org/10.1016/B978-0-12-369521-5.00016-6]
[2]
Mathie, A. Ion channels as novel therapeutic targets in the treatment of pain. J. Pharm. Pharmacol., 2010, 62(9), 1089-1095.
[http://dx.doi.org/10.1111/j.2042-7158.2010.01131.x] [PMID: 20796186]
[3]
Imbrici, P.; Camerino, D.C.; Tricarico, D. Major channels involved in neuropsychiatric disorders and therapeutic perspectives. Front. Genet., 2013, 4(76), 76.
[http://dx.doi.org/10.3389/fgene.2013.00076] [PMID: 23675382]
[4]
Lee, A.; Fakler, B.; Kaczmarek, L.K.; Isom, L.L. More than a pore: Ion channel signaling complexes. J. Neurosci., 2014, 34(46), 15159-15169.
[http://dx.doi.org/10.1523/JNEUROSCI.3275-14.2014] [PMID: 25392484]
[5]
MacDonald, M.; Ambrose, C.; Duyao, M.P.; Harper, P.S. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell, 1993, 72(6), 971-983.
[http://dx.doi.org/10.1016/0092-8674(93)90585-E] [PMID: 8458085]
[6]
Lang, A.E.; Lozano, A.M. Parkinson’s disease. N. Engl. J. Med., 1998, 339(15), 1044-1053.
[http://dx.doi.org/10.1056/NEJM199810083391506] [PMID: 9761807]
[7]
Goedert, M.; Spillantini, M.G. A century of Alzheimer’s disease. Science, 2006, 314(5800), 777-781.
[http://dx.doi.org/10.1126/science.1132814] [PMID: 17082447]
[8]
Kalogeris, T.; Baines, C.P.; Krenz, M.; Korthuis, R.J. Cell biology of ischemia/reperfusion injury. Int. Rev. Cell Mol. Biol., 2012, 298, 229-317.
[http://dx.doi.org/10.1016/B978-0-12-394309-5.00006-7] [PMID: 22878108]
[9]
Dugger, B.N.; Dickson, D.W. Pathology of neurodegenerative diseases. Cold Spring Harb. Perspect. Biol., 2017, 9(7), a028035.
[http://dx.doi.org/10.1101/cshperspect.a028035] [PMID: 28062563]
[10]
Yan, M.H.; Wang, X.; Zhu, X. Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic. Biol. Med., 2013, 62, 90-101.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.11.014] [PMID: 23200807]
[11]
Yang, X.; Wang, Y.; Wu, C.; Ling, E.A. Animal venom peptides as a treasure trove for new therapeutics against neurodegenerative disorders. Curr. Med. Chem., 2019, 26(25), 4749-4774.
[http://dx.doi.org/10.2174/0929867325666181031122438] [PMID: 30378475]
[12]
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]
[13]
Fayaz, A.; Croft, P.; Langford, R.M.; Donaldson, L.J.; Jones, G.T. Prevalence of chronic pain in the UK: A systematic review and meta-analysis of population studies. BMJ Open, 2016, 6(6), e010364.
[http://dx.doi.org/10.1136/bmjopen-2015-010364] [PMID: 27324708]
[14]
GBD 2019 Diseases and Injuries Collaborators*. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet, 2020, 396(10258), 1204-1222.
[http://dx.doi.org/10.1016/S0140-6736(20)30925-9] [PMID: 33069326]
[15]
Dubin, A.E.; Patapoutian, A. Nociceptors: The sensors of the pain pathway. J. Clin. Invest., 2010, 120(11), 3760-3772.
[http://dx.doi.org/10.1172/JCI42843] [PMID: 21041958]
[16]
Diochot, S. Pain-related toxins in scorpion and spider venoms: A face to face with ion channels. J. Venom. Anim. Toxins Incl. Trop. Dis., 2021, 27, e20210026.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2021-0026] [PMID: 34925480]
[17]
Saez, N.J.; Herzig, V. Versatile spider venom peptides and their medical and agricultural applications. Toxicon, 2019, 158, 109-126.
[http://dx.doi.org/10.1016/j.toxicon.2018.11.298] [PMID: 30543821]
[18]
Uchitel, O.D. Toxins affecting calcium channels in neurons. Toxicon, 1997, 35(8), 1161-1191.
[http://dx.doi.org/10.1016/S0041-0101(96)00210-3] [PMID: 9278968]
[19]
Saez, N.J.; Senff, S.; Jensen, J.E.; Er, S.Y.; Herzig, V.; Rash, L.D.; King, G.F. Spider-venom peptides as therapeutics. Toxins, 2010, 2(12), 2851-2871.
[http://dx.doi.org/10.3390/toxins2122851] [PMID: 22069579]
[20]
Nasiripourdori, A.; Taly, V.; Grutter, T.; Taly, A. From toxins targeting ligand gated ion channels to therapeutic molecules. Toxins, 2011, 3(3), 260-293.
[http://dx.doi.org/10.3390/toxins3030260] [PMID: 22069709]
[21]
Langenegger, N.; Nentwig, W.; Kuhn-Nentwig, L. Spider venom: Components, modes of action, and novel strategies in transcriptomic and proteomic analyses. Toxins, 2019, 11(10), 611.
[http://dx.doi.org/10.3390/toxins11100611] [PMID: 31652611]
[22]
Rezende, L., Jr; Cordeiro, M.N.; Oliveira, E.B.; Diniz, C.R. Isolation of neurotoxic peptides from the venom of the ‘armed’ spider Phoneutria nigriventer. Toxicon, 1991, 29(10), 1225-1233.
[http://dx.doi.org/10.1016/0041-0101(91)90195-W] [PMID: 1801316]
[23]
de Lima, M.E.; Figueiredo, S.; Matavel, A.; Nunes, K.; Silva, C.; Almeida, F.; Diniz, M.; Cordeiro, M.; Stankiewicz, M.; Beirão, P. Phoneutria nigriventer venom and toxins: A review; Springer Science+ Business Media Dordrecht, 2015, pp. 1-24.
[24]
Cordeiro, M.N.; de Figueiredo, S.G.; Valentim, A.C.; Diniz, C.R.; von Eickstedt, V.R.D.; 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]
[25]
Pinheiro, A.C.N.; da Silva, A.J.; Prado, M.A.M.; Cordeiro, M.N.; Richardson, M.; Batista, M.C.; de Castro, Junior C.J.; Massensini, A.R.; Guatimosim, C.; Romano-Silva, M.A.; Kushmerick, C.; Gomez, M.V. Phoneutria spider toxins block ischemia-induced glutamate release, neuronal death, and loss of neurotransmission in hippocampus. Hippocampus, 2009, 19(11), 1123-1129.
[http://dx.doi.org/10.1002/hipo.20580] [PMID: 19370546]
[26]
Agostini, R.M.; do Nascimento Pinheiro, A.C.; Binda, N.S.; Romano Silva, M.A.; do Nascimento Cordeiro, M.; Richardson, M.; Sena Guimarães, A.L.; Gomez, M.V. Phoneutria spider toxins block ischemia-induced glutamate release and neuronal death of cell layers of the retina. Retina, 2011, 31(7), 1392-1399.
[http://dx.doi.org/10.1097/IAE.0b013e318205b249] [PMID: 21394062]
[27]
Binda, N.; Porto, P.C.C.; Agostini, R.; do Nascimento, P.A.; Nascimento, C.M.; Romano, S.M.; Figueira, S.J.; Rita, P.E.; da Silva, J.C.; de Castro, J.C.; Sena, G.A.; Gomez, M. PhTx3-4, a spider toxin calcium channel blocker, reduces NMDA-induced injury of the retina. Toxins, 2016, 8(3), 70.
[http://dx.doi.org/10.3390/toxins8030070] [PMID: 26978403]
[28]
Bazan, N.G. The metabolism of omega-3 polyunsaturated fatty acids in the eye: The possible role of docosahexaenoic acid and docosanoids in retinal physiology and ocular pathology. Prog. Clin. Biol. Res., 1989, 312, 95-112.
[PMID: 2529559]
[29]
Pellegrini-Giampietro, D.E.; Cherici, G.; Alesiani, M.; Carla, V.; Moroni, F. Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemia-induced neuronal damage. J. Neurosci., 1990, 10(3), 1035-1041.
[http://dx.doi.org/10.1523/JNEUROSCI.10-03-01035.1990] [PMID: 1969465]
[30]
Guatimosim, C.; Romano-Silva, M.A.; Cruz, J.S.; Beirão, P.S.L.; Kalapothakis, E.; Moraes-Santos, T.; Cordeiro, M.N.; Diniz, C.R.; Gomez, M.V.; Prado, M.A.M. A toxin from the spider Phoneutria nigriventer that blocks calcium channels coupled to exocytosis. Br. J. Pharmacol., 1997, 122(3), 591-597.
[http://dx.doi.org/10.1038/sj.bjp.0701381] [PMID: 9351520]
[31]
Prado, M.A.M.; Guatimosim, C.; Gomez, M.V.; Diniz, C.R.; Cordeiro, M.N.; Romano-Silva, M. A novel tool for the investigation of glutamate release from rat cerebrocortical synaptosomes: the toxin Tx3-3 from the venom of the spider Phoneutria nigriventer. Biochem. J., 1996, 314(1), 145-150.
[http://dx.doi.org/10.1042/bj3140145] [PMID: 8660275]
[32]
Gomez, M.V.; Kalapothakis, E.; Guatimosim, C.; Prado, M.A.M. Phoneutria nigriventer venom: A cocktail of toxins that affect ion channels. Cell. Mol. Neurobiol., 2002, 22(5/6), 579-588.
[http://dx.doi.org/10.1023/A:1021836403433] [PMID: 12585681]
[33]
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]
[34]
Cassola, A.C. Jaffe, H.; Fales, H.M.; Castro Afeche, S.; Magnoli, F.; Cipolla-Neto, J. ω-Phonetoxin-IIA: A calcium channel blocker from the spider Phoneutria nigriventer. Pflugers Arch., 1998, 436(4), 545-552.
[http://dx.doi.org/10.1007/s004240050670] [PMID: 9683727]
[35]
Miranda, D.M.; Romano-Silva, M.A.; Kalapothakis, E.; Diniz, C.R.; Cordeiro, M.N.; Moraes-Santos, T.; De Marco, L.; Prado, M.A.M.; Gomez, M.V. Spider neurotoxins block the β scorpion toxin-induced calcium uptake in rat brain cortical synaptosomes. Brain Res. Bull., 2001, 54(5), 533-536.
[http://dx.doi.org/10.1016/S0361-9230(01)00443-9] [PMID: 11397544]
[36]
de Castro, Junior C.J.; Pinheiro, A.C.N.; Guatimosim, C.; Cordeiro, M.N.; Souza, A.H.; Richardson, M.; Romano-Silva, M.A.; Prado, M.A.M.; Gomez, M.V. Tx3-4 a toxin from the venom of spider Phoneutria nigriventer blocks calcium channels associated with exocytosis. Neurosci. Lett., 2008, 439(2), 170-172.
[http://dx.doi.org/10.1016/j.neulet.2008.05.019] [PMID: 18524484]
[37]
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]
[38]
Reis, H.J.; Prado, M.A.; Kalapothakis, E.; Cordeiro, M.N.; Diniz, C.R.; De Marco, L.A.; Gomez, M.V.; Romano-Silva, M.A. Inhibition of glutamate uptake by a polypeptide toxin (Phoneutriatoxin 3-4) from the spider Phoneutria nigriventer. Biochem. J., 1999, 343(Pt 2), 413-418.
[PMID: 10510308]
[39]
Reis, H.J.; Gomez, M.V.; Kalapothakis, E.; Diniz, C.R.; Cordeiro, M.N.; Prado, M.A.M.; Romano-Silva, M.A. Inhibition of glutamate uptake by Tx3-4 is dependent on the redox state of cysteine residues. Neuroreport, 2000, 11(10), 2191-2194.
[http://dx.doi.org/10.1097/00001756-200007140-00025] [PMID: 10923668]
[40]
Vieira, L.B.; Kushmerick, C.; Hildebrand, M.E.; Garcia, E.; Stea, A.; Cordeiro, M.N.; Richardson, M.; Gomez, M.V.; Snutch, T.P. Inhibition 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]
[41]
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 antinociceptive effects in mice. Br. J. Pharmacol., 2017, 174(1), 57-69.
[http://dx.doi.org/10.1111/bph.13652] [PMID: 27759880]
[42]
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]
[43]
Brownell, A.L.; Chen, Y.I.; Yu, M.; Wang, X.; Dedeoglu, A.; Cicchetti, F.; Jenkins, B.G.; Beal, M.F. 3-Nitropropionic acid-induced neurotoxicity - assessed by ultra high resolution positron emission tomography with comparison to magnetic resonance spectroscopy. J. Neurochem., 2004, 89(5), 1206-1214.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02408.x] [PMID: 15147513]
[44]
Antunes, F.T.T.; de Souza, A.H.; Caminski, E.S.; Greggio, S.; Venturin, G.T.; da Costa, J.C.; Taffarel, M.; Rebelo, I.N.; Gomez, M.V.; Correa, D.S.; Vilanova, F.N.; Regner, A.P.; Dallegrave, E. Neuroprotective effects of the CTK 01512-2 toxin against neurotoxicity induced by 3-nitropropionic acid in rats. Neurotoxicology, 2021, 87, 30-42.
[http://dx.doi.org/10.1016/j.neuro.2021.08.016] [PMID: 34478769]
[45]
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. Recombinant 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]
[46]
Caminski, E.S.; de Freitas, L.M.; Dallegrave, E.; Junior, C.A.S.; Gomez, M.V.; Pereira, E.M.R.; Antunes, F.T.T.; de Souza, A.H. Analgesic 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]
[47]
Joviano-Santos, J.V.; Valadão, P.A.C.; Magalhães-Gomes, M.P.S.; Fernandes, L.F.; Diniz, D.M.; Machado, T.C.G.; Soares, K.B.; Ladeira, M.S.; Miranda, A.S.; Massensini, A.R.; Gomez, M.V.; Guatimosim, C. Protective effect of a spider recombinant toxin in a murine model of Huntington’s disease. Neuropeptides, 2021, 85, 102111.
[http://dx.doi.org/10.1016/j.npep.2020.102111] [PMID: 33333486]
[48]
Hoffman, E.; Winder, S.J. A modified wire hanging apparatus for small animal muscle function testing. PLoS Curr., 2016, 8, 8.
[http://dx.doi.org/10.1371/currents.md.1e2bec4e78697b7b0ff80ea25a1d38be] [PMID: 28966868]
[49]
de Figueiredo, S.G.; de Lima, M.E.; Cordeiro, M.N.; Diniz, C.R.; Patten, D.; Halliwell, R.F.; Gilroy, J.; Richardson, M. Purification and amino acid sequence of a highly insecticidal toxin from the venom of the Brazilian spider Phoneutria nigriventer which inhibits NMDA-evoked currents in rat hippocampal neurones. Toxicon, 2001, 39(2-3), 309-317.
[http://dx.doi.org/10.1016/S0041-0101(00)00129-X] [PMID: 10978749]
[50]
Silva, F.R.; Batista, E.M.L.; Gomez, M.V.; Kushmerick, C.; Da Silva, J.F.; Cordeiro, M.N.; Vieira, L.B.; Ribeiro, F.M. The Phoneutria nigriventer spider toxin, PnTx4-5-5, promotes neuronal survival by blocking NMDA receptors. Toxicon, 2016, 112, 16-21.
[http://dx.doi.org/10.1016/j.toxicon.2016.01.056] [PMID: 26802625]
[51]
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]
[52]
Dalmolin, G.D.; Bannister, K.; Gonçalves, L.; Sikandar, S.; Patel, R.; Cordeiro, M.N.; Gomez, M.V.; Ferreira, J.; Dickenson, A.H. Effect of the spider toxin Tx3-3 on spinal processing of sensory information in naive and neuropathic rats: An in vivo electrophysiological study. Pain Rep., 2017, 2(4), e610.
[http://dx.doi.org/10.1097/PR9.0000000000000610] [PMID: 29392225]
[53]
Pedron, C.; Antunes, F.T.T.; Rebelo, I.N.; Campos, M.M.; Correa, Á.P.; Klein, C.P.; de Oliveira, I.B.; do Nascimento, C.M.; Gomez, M.V.; de Souza, A.H. Phoneutria nigriventer Tx3-3 peptide toxin reduces fibromyalgia symptoms in mice. Neuropeptides, 2021, 85, 102094.
[http://dx.doi.org/10.1016/j.npep.2020.102094] [PMID: 33171335]
[54]
Nanou, E.; Catterall, W.A. Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron, 2018, 98(3), 466-481.
[http://dx.doi.org/10.1016/j.neuron.2018.03.017] [PMID: 29723500]
[55]
Kowalska, M.; Prendecki, M.; Piekut, T.; Kozubski, W.; Dorszewska, J. Migraine: Calcium channels and glia. Int. J. Mol. Sci., 2021, 22(5), 2688.
[http://dx.doi.org/10.3390/ijms22052688] [PMID: 33799975]
[56]
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]
[57]
Rita Pereira, E.M.; Souza, J.M.; Carobin, N.V.; Silva, J.F.; Santos, D.C.; Silva Júnior, C.A.; Binda, N.S.; Borges, M.H.; Pinto Nagem, R.A.; Kushmerick, C.; Ferreira, J.; Castro, Junior C.J.; Ribeiro, F.M.; Gomez, M.V. Phoneutria toxin PnTx3-5 inhibits TRPV1 channel with antinociceptive action in an orofacial pain model. Neuropharmacology, 2020, 162, 107826.
[http://dx.doi.org/10.1016/j.neuropharm.2019.107826] [PMID: 31647972]
[58]
Silva, J.F.; Binda, N.S.; Pereira, E.M.R.; Lavor, M.S.L.; Vieira, L.B.; Souza, A.H.; Rigo, F.K.; Ferrer, H.T.; Castro Júnior, C.J.; Ferreira, J.; Gomez, M.V. Analgesic effects of Phα1β toxin: A review of mechanisms of action involving pain pathways. J. Venom. Anim. Toxins Incl. Trop. Dis., 2021, 27, e20210001.
[http://dx.doi.org/10.1590/1678-9199-jvatitd-2021-0001] [PMID: 34868281]
[59]
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]
[60]
Souza, A.H.; Ferreira, J.; Cordeiro, M.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 Phα1β 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]
[61]
Diniz, D.M.; de Souza, A.H.; Pereira, E.M.; da Silva, J.F.; Rigo, F.K.; Romano-Silva, M.A.; Binda, N.; Castro-Junior, C.J.; 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]
[62]
Silva, R.B.M.; Sperotto, N.D.M.; Andrade, E.L.; Pereira, T.C.B.; Leite, C.E.; de Souza, A.H.; Bogo, M.R.; Morrone, F.B.; Gomez, M.V.; Campos, M.M. Spinal blockage of P/Q- or N-type voltage-gated calcium channels modulates functional and symptomatic changes related to haemorrhagic cystitis in mice. Br. J. Pharmacol., 2015, 172(3), 924-939.
[http://dx.doi.org/10.1111/bph.12966] [PMID: 25298144]
[63]
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]
[64]
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, M.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]
[65]
Wormwood, K.L.; Ngounou Wetie, A.G.; Gomez, M.V.; Ju, Y.; Kowalski, P.; Mihasan, M.; Darie, C.C. Structural characterization and disulfide assignment of spider peptide Phα1β by mass spectrometry. J. Am. Soc. Mass Spectrom., 2018, 29(5), 827-841.
[http://dx.doi.org/10.1007/s13361-018-1904-3] [PMID: 29663255]
[66]
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]
[67]
Rigo, F.K.; Rossato, M.F.; Borges, V.; da Silva, J.F.; Pereira, E.M.R.; de-Ávila, R.A.M.; Trevisan, G. 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]
[68]
Miljanich, G.P.; Ramachandran, J. Antagonists of neuronal calcium channels: Structure, function, and therapeutic implications. Annu. Rev. Pharmacol. Toxicol., 1995, 35(1), 707-734.
[http://dx.doi.org/10.1146/annurev.pa.35.040195.003423] [PMID: 7598513]
[69]
Skov, M.J.; Beck, J.C.; de Kater, A.W.; Shopp, G.M. Nonclinical safety of ziconotide: An intrathecal analgesic of a new pharmaceutical class. Int. J. Toxicol., 2007, 26(5), 411-421.
[http://dx.doi.org/10.1080/10915810701582970] [PMID: 17963128]
[70]
Staats, P.S.; Yearwood, T.; Charapata, S.G.; Presley, R.W.; Wallace, M.S.; Byas-Smith, M.; Fisher, R.; Bryce, D.A.; Mangieri, E.A.; Luther, R.R.; Mayo, M.; McGuire, D.; Ellis, D. Intrathecal ziconotide in the treatment of refractory pain in patients with cancer or AIDS: A randomized controlled trial. JAMA, 2004, 291(1), 63-70.
[http://dx.doi.org/10.1001/jama.291.1.63] [PMID: 14709577]
[71]
Rigo, F.K.; Dalmolin, G.D.; Trevisan, G.; Tonello, R.; Silva, M.A.; Rossato, M.F.; Klafke, J.Z.; Cordeiro, M.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]
[72]
Rosa, F.; Trevisan, G.; Rigo, F.K.; Tonello, R.; Andrade, E.L.; do Nascimento Cordeiro, M.; 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]
[73]
Liang, S.; Zhang, D.; Pan, X.; Chen, Q.; Zhou, P. Properties and amino acid sequence of huwentoxin-I, a neurotoxin purified from the venom of the Chinese bird spider Selenocosmia huwena. Toxicon, 1993, 31(8), 969-978.
[http://dx.doi.org/10.1016/0041-0101(93)90256-I] [PMID: 8212049]
[74]
Qu, Y.; Liang, S.; Ding, J.; Liu, X.; Zhang, R.; Gu, X. Proton nuclear magnetic resonance studies on huwentoxin-I from the venom of the spider Selenocosmia huwena: 2. Three-dimensional structure in solution. J. Protein Chem., 1997, 16(6), 565-574.
[http://dx.doi.org/10.1023/A:1026314722607] [PMID: 9263120]
[75]
Schurr, A.; Rigor, B.M. The mechanism of cerebral hypoxic-ischemic damage. Hippocampus, 1992, 2(3), 221-228.
[http://dx.doi.org/10.1002/hipo.450020303] [PMID: 1308186]
[76]
Peng, K.; Chen, X.D.; Liang, S.P. The effect of Huwentoxin-I on Ca2+ channels in differentiated NG108-15 cells, a patch-clamp study. Toxicon, 2001, 39(4), 491-498.
[http://dx.doi.org/10.1016/S0041-0101(00)00150-1] [PMID: 11024489]
[77]
Liang, S. An overview of peptide toxins from the venom of the Chinese bird spider Selenocosmia huwena Wang. Toxicon, 2004, 43(5), 575-585.
[http://dx.doi.org/10.1016/j.toxicon.2004.02.005] [PMID: 15066414]
[78]
Wang, M.; Guan, X.; Liang, S. The cross channel activities of spider neurotoxin huwentoxin-I on rat dorsal root ganglion neurons. Biochem. Biophys. Res. Commun., 2007, 357(3), 579-583.
[http://dx.doi.org/10.1016/j.bbrc.2007.02.168] [PMID: 17451655]
[79]
Xiao, Y.; Bingham, J.P.; Zhu, W.; Moczydlowski, E.; Liang, S.; Cummins, T.R. Tarantula huwentoxin-IV inhibits neuronal sodium channels by binding to receptor site 4 and trapping the domain ii voltage sensor in the closed configuration. J. Biol. Chem., 2008, 283(40), 27300-27313.
[http://dx.doi.org/10.1074/jbc.M708447200] [PMID: 18628201]
[80]
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]
[81]
Wen tao, Z.; Gu yang, T.; Ying, R.; Mao cai, W.; Lin, L.; Chi miao, L.; Peng, H.; Jia 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]
[82]
Peng, K.; Shu, Q.; Liu, Z.; Liang, S. Function and solution structure of huwentoxin-IV, a potent neuronal tetrodotoxin (TTX)-sensitive sodium channel antagonist from Chinese bird spider Selenocosmia huwena. J. Biol. Chem., 2002, 277(49), 47564-47571.
[http://dx.doi.org/10.1074/jbc.M204063200] [PMID: 12228241]
[83]
Revell, J.D.; Lund, P.E.; Linley, J.E.; Metcalfe, J.; Burmeister, N.; Sridharan, S.; Jones, C.; Jermutus, L.; Bednarek, M.A. Potency optimization of Huwentoxin-IV on hNav1.7: A neurotoxin TTX-S sodium-channel antagonist from the venom of the Chinese bird-eating spider Selenocosmia huwena. Peptides, 2013, 44, 40-46.
[http://dx.doi.org/10.1016/j.peptides.2013.03.011] [PMID: 23523779]
[84]
Liu, Y.; Wu, Z.; Tang, D.; Xun, X.; Liu, L.; Li, X.; Nie, D.; Xiang, Y.; Yi, J.; Yi, J. Analgesic effects of Huwentoxin-IV on animal models of inflammatory and neuropathic pain. Protein Pept. Lett., 2013, 21(2), 153-158.
[http://dx.doi.org/10.2174/09298665113206660119] [PMID: 24188048]
[85]
Rahnama, S.; Deuis, J.R.; Cardoso, F.C.; Ramanujam, V.; Lewis, R.J.; Rash, L.D.; King, G.F.; Vetter, I.; Mobli, M. The structure, dynamics and selectivity profile of a NaV1.7 potency-optimised huwentoxin-IV variant. PLoS One, 2017, 12(3), e0173551.
[http://dx.doi.org/10.1371/journal.pone.0173551] [PMID: 28301520]
[86]
Liu, Z.; Cai, T.; Zhu, Q.; Deng, M.; Li, J.; Zhou, X.; Zhang, F.; Li, D.; Li, J.; Liu, Y.; Hu, W.; Liang, S. Structure and function of hainantoxin-III, a selective antagonist of neuronal tetrodotoxin-sensitive voltage-gated sodium channels isolated from the Chinese bird spider Ornithoctonus hainana. J. Biol. Chem., 2013, 288(28), 20392-20403.
[http://dx.doi.org/10.1074/jbc.M112.426627] [PMID: 23703613]
[87]
Dib-Hajj, S.D.; Yang, Y.; Waxman, S.G. Genetics and molecular pathophysiology of Na(v)1.7-related pain syndromes. Adv. Genet., 2008, 63, 85-110.
[http://dx.doi.org/10.1016/S0065-2660(08)01004-3] [PMID: 19185186]
[88]
Liu, Y.; Liu, Z.; Wang, Q.; Wang, Z.; Zhang, Y. HNTX-III alleviates inflammatory and neuropathic pain in animal models. Int. J. Pept. Res. Ther., 2019, 25(2), 799-806.
[http://dx.doi.org/10.1007/s10989-018-9729-2]
[89]
Xiao, Y.; Liang, S. Inhibition of neuronal tetrodotoxin-sensitive Na+ channels by two spider toxins: Hainantoxin-III and hainantoxin-IV. Eur. J. Pharmacol., 2003, 477(1), 1-7.
[http://dx.doi.org/10.1016/S0014-2999(03)02190-3] [PMID: 14512091]
[90]
Liu, Y.; Tang, J.; Zhang, Y.; Xun, X.; Tang, D.; Peng, D.; Yi, J.; Liu, Z.; Shi, X. Synthesis and analgesic effects of µ-TRTX-Hhn1b on models of inflammatory and neuropathic pain. Toxins, 2014, 6(8), 2363-2378.
[http://dx.doi.org/10.3390/toxins6082363] [PMID: 25123556]
[91]
Gonçalves, T.C.; Boukaiba, R.; Molgó, J.; Amar, M.; Partiseti, M.; Servent, D.; Benoit, E. Direct evidence for high affinity blockade of NaV1.6 channel subtype by huwentoxin-IV spider peptide, using multiscale functional approaches. Neuropharmacology, 2018, 133, 404-414.
[http://dx.doi.org/10.1016/j.neuropharm.2018.02.016] [PMID: 29474819]
[92]
Escoubas, P.; De Weille, J.R.; Lecoq, A.; Diochot, S.; Waldmann, R.; Champigny, G.; Moinier, D.; Ménez, A.; Lazdunski, M. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J. Biol. Chem., 2000, 275(33), 25116-25121.
[http://dx.doi.org/10.1074/jbc.M003643200] [PMID: 10829030]
[93]
Escoubas, P.; Bernard, C.; Lambeau, G.; Lazdunski, M.; Darbon, H. Recombinant production and solution structure of PcTx1, the specific peptide inhibitor of ASIC1a proton-gated cation channels. Protein Sci., 2003, 12(7), 1332-1343.
[http://dx.doi.org/10.1110/ps.0307003] [PMID: 12824480]
[94]
Chen, X.; Kalbacher, H.; Gründer, S. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J. Gen. Physiol., 2006, 127(3), 267-276.
[http://dx.doi.org/10.1085/jgp.200509409] [PMID: 16505147]
[95]
Chen, X.; Gründer, S. Permeating protons contribute to tachyphylaxis of the acid-sensing ion channel (ASIC) 1a. J. Physiol., 2007, 579(3), 657-670.
[http://dx.doi.org/10.1113/jphysiol.2006.120733] [PMID: 17204502]
[96]
Waldmann, R.; Champigny, G.; Bassilana, F.; Heurteaux, C.; Lazdunski, M. A proton-gated cation channel involved in acid-sensing. Nature, 1997, 386(6621), 173-177.
[http://dx.doi.org/10.1038/386173a0] [PMID: 9062189]
[97]
Hoagland, E.N.; Sherwood, T.W.; Lee, K.G.; Walker, C.J.; Askwith, C.C. Identification of a calcium permeable human acid-sensing ion channel 1 transcript variant. J. Biol. Chem., 2010, 285(53), 41852-41862.
[http://dx.doi.org/10.1074/jbc.M110.171330] [PMID: 21036899]
[98]
Sherwood, T.W.; Lee, K.G.; Gormley, M.G.; Askwith, C.C. Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J. Neurosci., 2011, 31(26), 9723-9734.
[http://dx.doi.org/10.1523/JNEUROSCI.1665-11.2011] [PMID: 21715637]
[99]
Tan, J.; Ye, X.; Xu, Y.; Wang, H.; Sheng, M.; Wang, F. Acid-sensing ion channel 1a is involved in retinal ganglion cell death induced by hypoxia. Mol. Vis., 2011, 17, 3300-3308.
[PMID: 22194656]
[100]
Gu, X.S.; Wang, F.; Zhang, C.Y.; Mao, C.J.; Yang, J.; Yang, Y.P.; Liu, S.; Hu, L.F.; Liu, C.F. Neuroprotective effects of paeoniflorin on 6-OHDA-lesioned rat model of Parkinson’s disease. Neurochem. Res., 2016, 41(11), 2923-2936.
[http://dx.doi.org/10.1007/s11064-016-2011-0] [PMID: 27447883]
[101]
Stankowska, D.L.; Mueller, B.H., II; Oku, H.; Ikeda, T.; Dibas, A. Neuroprotective effects of inhibitors of acid-sensing ion channels (ASICs) in optic nerve crush model in rodents. Curr. Eye Res., 2018, 43(1), 84-95.
[http://dx.doi.org/10.1080/02713683.2017.1383442] [PMID: 29111855]
[102]
Dibas, A.; Millar, C.; Al-Farra, A.; Yorio, T. Neuroprotective effects of Psalmotoxin-1, an acid-sensing ion channel (ASIC) inhibitor, in ischemia reperfusion in mouse eyes. Curr. Eye Res., 2018, 43(7), 921-933.
[http://dx.doi.org/10.1080/02713683.2018.1454478] [PMID: 29595330]
[103]
McCarthy, C.A.; Rash, L.D.; Chassagnon, I.R.; King, G.F.; Widdop, R.E. PcTx1 affords neuroprotection in a conscious model of stroke in hypertensive rats via selective inhibition of ASIC1a. Neuropharmacology, 2015, 99, 650-657.
[http://dx.doi.org/10.1016/j.neuropharm.2015.08.040] [PMID: 26320544]
[104]
Cristofori-Armstrong, B.; Rash, L.D. Acid-sensing ion channel (ASIC) structure and function: Insights from spider, snake and sea anemone venoms. Neuropharmacology, 2017, 127, 173-184.
[http://dx.doi.org/10.1016/j.neuropharm.2017.04.042] [PMID: 28457973]
[105]
Chassagnon, I.R.; McCarthy, C.A.; Chin, Y.K.Y.; Pineda, S.S.; Keramidas, A.; Mobli, M.; Pham, V.; De Silva, T.M.; Lynch, J.W.; Widdop, R.E.; Rash, L.D.; King, G.F. Potent neuroprotection after stroke afforded by a double-knot spider-venom peptide that inhibits acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA, 2017, 114(14), 3750-3755.
[http://dx.doi.org/10.1073/pnas.1614728114] [PMID: 28320941]
[106]
Xiong, Z.G.; Zhu, X.M.; Chu, X.P.; Minami, M.; Hey, J.; Wei, W.L.; MacDonald, J.F.; Wemmie, J.A.; Price, M.P.; Welsh, M.J.; Simon, R.P. Neuroprotection in Ischemia. Cell, 2004, 118(6), 687-698.
[http://dx.doi.org/10.1016/j.cell.2004.08.026] [PMID: 15369669]
[107]
Gao, J.; Duan, B.; Wang, D.G.; Deng, X.H.; Zhang, G.Y.; Xu, L.; Xu, T.L. Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron, 2005, 48(4), 635-646.
[http://dx.doi.org/10.1016/j.neuron.2005.10.011] [PMID: 16301179]
[108]
Pignataro, G.; Simon, R.P.; Xiong, Z.G. Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain, 2007, 130(Pt 1), 151-158.
[PMID: 17114797]
[109]
Cherki, R.S.; Kolb, E.; Langut, Y.; Tsveyer, L.; Bajayo, N.; Meir, A. Two tarantula venom peptides as potent and differential NaV channels blockers. Toxicon, 2014, 77, 58-67.
[http://dx.doi.org/10.1016/j.toxicon.2013.10.029] [PMID: 24211312]
[110]
Murray, J.K.; Biswas, K.; Holder, J.R.; Zou, A.; Ligutti, J.; Liu, D.; Poppe, L.; Andrews, K.L.; Lin, F.F.; Meng, S.Y.; Moyer, B.D.; McDonough, S.I.; Miranda, L.P. Sustained inhibition of the Na V 1.7 sodium channel by engineered dimers of the domain II binding peptide GpTx-1. Bioorg. Med. Chem. Lett., 2015, 25(21), 4866-4871.
[http://dx.doi.org/10.1016/j.bmcl.2015.06.033] [PMID: 26112439]
[111]
Deuis, J.; Wingerd, J.; Winter, Z.; Durek, T.; Dekan, Z.; Sousa, S.; Zimmermann, K.; Hoffmann, T.; Weidner, C.; Nassar, M.; Alewood, P.; Lewis, R.; Vetter, I. Analgesic effects of GpTx-1, PF-04856264 and CNV1014802 in a mouse model of NaV1.7-mediated pain. Toxins, 2016, 8(3), 78.
[http://dx.doi.org/10.3390/toxins8030078] [PMID: 26999206]
[112]
Chen, C.; Xu, B.; Shi, X.; Zhang, M.; Zhang, Q.; Zhang, T.; Zhao, W.; Zhang, R.; Wang, Z.; Li, N.; Fang, Q. GpTx-1 and [Ala5, Phe6, Leu26, Arg28]GpTx-1, two peptide Na V 1.7 inhibitors: analgesic and tolerance properties at the spinal level. Br. J. Pharmacol., 2018, 175(20), 3911-3927.
[http://dx.doi.org/10.1111/bph.14461] [PMID: 30076786]
[113]
Suchyna, T.M.; Johnson, J.H.; Hamer, K.; Leykam, J.F.; Gage, D.A.; Clemo, H.F.; Baumgarten, C.M.; Sachs, F. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J. Gen. Physiol., 2000, 115(5), 583-598.
[http://dx.doi.org/10.1085/jgp.115.5.583] [PMID: 10779316]
[114]
Spassova, M.A.; Hewavitharana, T.; Xu, W.; Soboloff, J.; Gill, D.L. A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc. Natl. Acad. Sci. USA, 2006, 103(44), 16586-16591.
[http://dx.doi.org/10.1073/pnas.0606894103] [PMID: 17056714]
[115]
Alessandri-Haber, N.; Dina, O.A.; Chen, X.; Levine, J.D. TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J. Neurosci., 2009, 29(19), 6217-6228.
[http://dx.doi.org/10.1523/JNEUROSCI.0893-09.2009] [PMID: 19439599]
[116]
Park, S.P.; Kim, B.M.; Koo, J.Y.; Cho, H.; Lee, C.H.; Kim, M.; Na, H.S.; Oh, U. A tarantula spider toxin, GsMTx4, reduces mechanical and neuropathic pain. Pain, 2008, 137(1), 208-217.
[http://dx.doi.org/10.1016/j.pain.2008.02.013] [PMID: 18359568]
[117]
Bae, C.; Sachs, F.; Gottlieb, P.A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry, 2011, 50(29), 6295-6300.
[http://dx.doi.org/10.1021/bi200770q] [PMID: 21696149]
[118]
Alcaino, C.; Knutson, K.; Gottlieb, P.A.; Farrugia, G.; Beyder, A. Mechanosensitive ion channel Piezo2 is inhibited by D-GsMTx4. Channels (Austin), 2017, 11(3), 245-253.
[http://dx.doi.org/10.1080/19336950.2017.1279370] [PMID: 28085630]
[119]
Zhang, M.; Wang, Y.; Geng, J.; Zhou, S.; Xiao, B. Mechanically activated Piezo channels mediate touch and suppress acute mechanical pain response in mice. Cell Rep., 2019, 26(6), 1419-1431.
[http://dx.doi.org/10.1016/j.celrep.2019.01.056] [PMID: 30726728]
[120]
Middleton, R.E.; Warren, V.A.; Kraus, R.L.; Hwang, J.C.; Liu, C.J.; Dai, G.; Brochu, R.M.; Kohler, M.G.; Gao, Y.D.; Garsky, V.M.; Bogusky, M.J.; Mehl, J.T.; Cohen, C.J.; Smith, M.M. Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry, 2002, 41(50), 14734-14747.
[http://dx.doi.org/10.1021/bi026546a] [PMID: 12475222]
[121]
Priest, B.T.; Blumenthal, K.M.; Smith, J.J.; Warren, V.A.; Smith, M.M. ProTx-I and ProTx-II: Gating modifiers of voltage-gated sodium channels. Toxicon, 2007, 49(2), 194-201.
[http://dx.doi.org/10.1016/j.toxicon.2006.09.014] [PMID: 17087985]
[122]
Flinspach, M.; Xu, Q.; Piekarz, A.D.; Fellows, R.; Hagan, R.; Gibbs, A.; Liu, Y.; Neff, R.A.; Freedman, J.; Eckert, W.A.; Zhou, M.; Bonesteel, R.; Pennington, M.W.; Eddinger, K.A.; Yaksh, T.L.; Hunter, M.; Swanson, R.V.; Wickenden, A.D. Insensitivity to pain induced by a potent selective closed-state Nav1.7 inhibitor. Sci. Rep., 2017, 7(1), 39662.
[http://dx.doi.org/10.1038/srep39662] [PMID: 28045073]
[123]
Schmalhofer, W.A.; Calhoun, J.; Burrows, R.; Bailey, T.; Kohler, M.G.; Weinglass, A.B.; Kaczorowski, G.J.; Garcia, M.L.; Koltzenburg, M.; Priest, B.T. ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol. Pharmacol., 2008, 74(5), 1476-1484.
[http://dx.doi.org/10.1124/mol.108.047670] [PMID: 18728100]
[124]
Chernov-Rogan, T.; Li, T.; Lu, G.; Verschoof, H.; Khakh, K.; Jones, S.W.; Beresini, M.H.; Liu, C.; Ortwine, D.F.; McKerrall, S.J.; Hackos, D.H.; Sutherlin, D.; Cohen, C.J.; Chen, J. Mechanism-specific assay design facilitates the discovery of Nav1.7-selective inhibitors. Proc. Natl. Acad. Sci. USA, 2018, 115(4), E792-E801.
[http://dx.doi.org/10.1073/pnas.1713701115] [PMID: 29311306]
[125]
Xu, H.; Li, T.; Rohou, A.; Arthur, C.P.; Tzakoniati, F.; Wong, E.; Estevez, A.; Kugel, C.; Franke, Y.; Chen, J.; Ciferri, C.; Hackos, D.H.; Koth, C.M.; Payandeh, J. Structural basis of Nav1.7 inhibition by a gating-modifier spider toxin. Cell, 2019, 176(4), 702-715.e14.
[http://dx.doi.org/10.1016/j.cell.2018.12.018] [PMID: 30661758]
[126]
Torres-Pérez, J.V.; Adamek, P.; Palecek, J.; Vizcaychipi, M.; Nagy, I.; Varga, A. The NAv1.7 blocker protoxin II reduces burn injury-induced spinal nociceptive processing. J. Mol. Med., 2018, 96(1), 75-84.
[http://dx.doi.org/10.1007/s00109-017-1599-0] [PMID: 29063143]
[127]
Bladen, C.; Hamid, J.; Souza, I.A.; Zamponi, G.W. Block of T-type calcium channels by protoxins I and II. Mol. Brain, 2014, 7(1), 36.
[http://dx.doi.org/10.1186/1756-6606-7-36] [PMID: 24886690]
[128]
Moyer, B.D.; Murray, J.K.; Ligutti, J.; Andrews, K.; Favreau, P.; Jordan, J.B.; Lee, J.H.; Liu, D.; Long, J.; Sham, K.; Shi, L.; Stöcklin, R.; Wu, B.; Yin, R.; Yu, V.; Zou, A.; Biswas, K.; Miranda, L.P. Pharmacological characterization of potent and selective NaV1.7 inhibitors engineered from Chilobrachys jingzhao tarantula venom peptide JzTx-V. PLoS One, 2018, 13(5), e0196791.
[http://dx.doi.org/10.1371/journal.pone.0196791] [PMID: 29723257]
[129]
Murray, J.K.; Wu, B.; Tegley, C.M.; Nixey, T.E.; Falsey, J.R.; Herberich, B.; Yin, L.; Sham, K.; Long, J.; Aral, J.; Cheng, Y.; Netirojjanakul, C.; Doherty, L.; Glaus, C.; Ikotun, T.; Li, H.; Tran, L.; Soto, M.; Salimi-Moosavi, H.; Ligutti, J.; Amagasu, S.; Andrews, K.L.; Be, X.; Lin, M.H.J.; Foti, R.S.; Ilch, C.P.; Youngblood, B.; Kornecook, T.J.; Karow, M.; Walker, K.W.; Moyer, B.D.; Biswas, K.; Miranda, L.P. Engineering NaV1.7 inhibitory JzTx-V peptides with a potency and basicity profile suitable for antibody conjugation to enhance pharmacokinetics. ACS Chem. Biol., 2019, 14(4), 806-818.
[http://dx.doi.org/10.1021/acschembio.9b00183] [PMID: 30875193]
[130]
Zeng, X.; Deng, M.; Lin, Y.; Yuan, C.; Pi, J.; Liang, S. Isolation and characterization of Jingzhaotoxin-V, a novel neurotoxin from the venom of the spider Chilobrachys jingzhao. Toxicon, 2007, 49(3), 388-399.
[http://dx.doi.org/10.1016/j.toxicon.2006.10.012] [PMID: 17157888]
[131]
Wu, B.; Murray, J.K.; Andrews, K.L.; Sham, K.; Long, J.; Aral, J.; Ligutti, J.; Amagasu, S.; Liu, D.; Zou, A.; Min, X.; Wang, Z.; Ilch, C.P.; Kornecook, T.J.; Lin, M.H.J.; Be, X.; Miranda, L.P.; Moyer, B.D.; Biswas, K. Discovery of tarantula venom-derived NaV1.7-inhibitory JzTx-V peptide 5-Br-Trp24 analogue AM-6120 with systemic block of histamine-induced pruritis. J. Med. Chem., 2018, 61(21), 9500-9512.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00736] [PMID: 30346167]
[132]
Godoy, L.; Liberato, J.; Celani, M.; Gobbo-Neto, L.; Lopes, N.; dos Santos, W. Disease modifying effects of the spider toxin Parawixin2 in the experimental epilepsy model. Toxins, 2017, 9(9), 262.
[http://dx.doi.org/10.3390/toxins9090262] [PMID: 28841161]
[133]
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.; Oliveira, I.S.; Boldrini-França, J.; Pucca, M.B.; Baldo, M.A.; Arantes, E.C. From animal poisons 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]
[134]
Smallwood, T.B.; Clark, R.J. Advances in venom peptide drug discovery: Where are we at and where are we heading? Expert Opin. Drug Discov., 2021, 16(10), 1163-1173.
[http://dx.doi.org/10.1080/17460441.2021.1922386] [PMID: 33914674]
[135]
Ambure, P.; Roy, K. CADD modeling of multi-target drugs against Alzheimer’s disease. Curr. Drug Targets, 2017, 18(5), 522-533.
[http://dx.doi.org/10.2174/1389450116666150907104855] [PMID: 26343117]

Rights & Permissions Print Cite
Article Metrics
40
5
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy