Pmu1a, a novel spider toxin with dual inhibitory activity at pain targets hNa


Journal

The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646

Informations de publication

Date de publication:
07 2023
Historique:
revised: 07 02 2023
received: 31 08 2022
accepted: 10 03 2023
medline: 21 7 2023
pubmed: 14 3 2023
entrez: 13 3 2023
Statut: ppublish

Résumé

Venom-derived peptides targeting ion channels involved in pain are regarded as a promising alternative to current, and often ineffective, chronic pain treatments. Many peptide toxins are known to specifically and potently block established therapeutic targets, among which the voltage-gated sodium and calcium channels are major contributors. Here, we report on the discovery and characterization of a novel spider toxin isolated from the crude venom of Pterinochilus murinus that shows inhibitory activity at both hNa

Identifiants

pubmed: 36912793
doi: 10.1111/febs.16773
doi:

Substances chimiques

Voltage-Gated Sodium Channel Blockers 0
Spider Venoms 0
Peptides 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

3688-3702

Subventions

Organisme : Intramural Research Program of the National Cancer Institute
ID : ZIA BC 012003

Informations de copyright

© 2023 Federation of European Biochemical Societies.

Références

Cohen SP, Vase L & Hooten WM (2021) Chronic pain: an update on burden, best practices, and new advances. Lancet 397, 2082-2097.
Coussens NP, Sittampalam GS, Jonson SG, Hall MD, Gorby HE, Tamiz AP, McManus OB, Felder CC & Rasmussen K (2019) The opioid crisis and the future of addiction and pain therapeutics. J Pharmacol Exp Ther 371, 396-408.
Glare P, Aubrey KR & Myles PS (2019) Transition from acute to chronic pain after surgery. Lancet 393, 1537-1546.
Lewis RJ & Garcia ML (2003) Therapeutic potential of venom peptides. Nat Rev Drug Discov 2, 790-802.
King GF (2011) Venoms as a platform for human drugs: translating toxins into therapeutics. Expert Opin Biol Ther 11, 1469-1484.
Casewell NR, Wüster W, Vonk FJ, Harrison RA & Fry BG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28, 219-229.
Robinson SD, Undheim EAB, Ueberheide B & King GF (2017) Venom peptides as therapeutics: advances, challenges and the future of venom-peptide discovery. Expert Rev Proteomics 14, 931-939.
Wood JN, Boorman JP, Okuse K & Baker MD (2004) Voltage-gated sodium channels and pain pathways. J Neurobiol 61, 55-71.
Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y et al. (2006) An SCN9A channelopathy causes congenital inability to experience pain. Nature 444, 894-898.
Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, Abrahamsen B, Ostman J, Klugbauer N, Wood JN, Gardiner RM et al. (2006) SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52, 767-774.
Gonçalves TC, Benoit E, Partiseti M & Servent D (2018) The NaV1.7 channel subtype as an antinociceptive target for spider toxins in adult dorsal root ganglia neurons. Front Pharmacol 9, 1000.
McArthur JR, Munasinghe NR, Finol-Urdaneta RK, Adams DJ & Christie MJ (2021) Spider venom peptide Pn3a inhibition of primary afferent high voltage-activated calcium channels. Front Pharmacol 11, 633679.
McArthur JR, Wen J, Hung A, Finol-Urdaneta RK & Adams DJ (2022) μ-Theraphotoxin-Pn3a inhibition of CaV3.3 channels reveals a novel isoform-selective drug binding site. Elife 11, e74040.
Deuis JR, Dekan Z, Wingerd JS, Smith JJ, Munasinghe NR, Bhola RF, Imlach WL, Herzig V, Armstrong DA, Rosengren KJ et al. (2017) Pharmacological characterisation of the highly NaV1.7 selective spider venom peptide Pn3a. Sci Rep 7, 40883.
Nicolas S, Zoukimian C, Bosmans F, Montnach J, Diochot S, Cuypers E, De Waard S, Béroud R, Mebs D, Craik D et al. (2019) Chemical synthesis, proper folding, nav channel selectivity profile and analgesic properties of the spider peptide phlotoxin 1. Toxins 11, 367.
Todorovic SM & Jevtovic-Todorovic V (2011) T-type voltage-gated calcium channels as targets for the development of novel pain therapies: T-channels in nociceptive pathways. Br J Pharmacol 163, 484-495.
Bourinet E, Altier C, Hildebrand ME, Trang T, Salter MW & Zamponi GW (2014) Calcium-permeable ion channels in pain signaling. Physiol Rev 94, 81-140.
Miljanich GP (2004) Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem 11, 3029-3040.
Tranberg CE, Yang A, Vetter I, McArthur JR, Baell JB, Lewis RJ, Tuck KL & Duggan PJ (2012) ω-Conotoxin GVIA mimetics that bind and inhibit neuronal Cav2.2 ion channels. Mar Drugs 10, 2349-2368.
Adams DJ, Smith AB, Schroeder CI, Yasuda T & Lewis RJ (2003) ω-Conotoxin CVID inhibits a pharmacologically distinct voltage-sensitive calcium channel associated with transmitter release from preganglionic nerve terminals. J Biol Chem 278, 4057-4062.
McGivern JG (2007) Ziconotide: a review of its pharmacology and use in the treatment of pain. Neuropsychiatr Dis Treat 3, 69-85.
Harding EK & Zamponi GW (2022) Central and peripheral contributions of T-type calcium channels in pain. Mol Brain 15, 39.
Todorovic SM & Jevtovic-Todorovic V (2006) The role of T-type calcium channels in peripheral and central pain processing. CNS Neurol Disord Drug Targets 5, 639-653.
Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83, 117-161.
François A, Laffray S, Pizzoccaro A, Eschalier A & Bourinet E (2014) T-type calcium channels in chronic pain: mouse models and specific blockers. Pflugers Arch 466, 707-717.
Todorovic SM, Meyenburg A & Jevtovic-Todorovic V (2002) Mechanical and thermal antinociception in rats following systemic administration of mibefradil, a T-type calcium channel blocker. Brain Res 951, 336-340.
Flatters SJL & Bennett GJ (2004) Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain 109, 150-161.
Harding EK, Dedek A, Bonin RP, Salter MW, Snutch TP & Hildebrand ME (2021) The T-type calcium channel antagonist, Z944, reduces spinal excitability and pain hypersensitivity. Br J Pharmacol 178, 3517-3532.
Francois A, Kerckhove N, Meleine M, Alloui A, Barrere C, Gelot A, Uebele VN, Renger JJ, Eschalier A, Ardid D et al. (2013) State-dependent properties of a new T-type calcium channel blocker enhance CaV3.2 selectivity and support analgesic effects. Pain 154, 283-293.
Rose KE, Lunardi N, Boscolo A, Dong X, Erisir A, Jevtovic-Todorovic V & Todorovic SM (2013) Immunohistological demonstration of CaV3.2 T-type voltage-gated calcium channel expression in soma of dorsal root ganglion neurons and peripheral axons of rat and mouse. Neuroscience 250, 263-274.
François A, Schüetter N, Laffray S, Sanguesa J, Pizzoccaro A, Dubel S, Mantilleri A, Nargeot J, Noël J, Wood JN et al. (2015) The low-threshold calcium channel Cav3.2 determines low-threshold mechanoreceptor function. Cell Rep 10, 370-382.
Feng X-J, Ma L-X, Jiao C, Kuang H-X, Zeng F, Zhou X-Y, Cheng X-E, Zhu M-Y, Zhang D-Y, Jiang C-Y et al. (2019) Nerve injury elevates functional Cav3.2 channels in superficial spinal dorsal horn. Mol Pain 15, 1744806919836569.
Bourinet E, Alloui A, Monteil A, Barrère C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A et al. (2005) Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J 24, 315-324.
Marger F, Gelot A, Alloui A, Matricon J, Ferrer JFS, Barrere C, Pizzoccaro A, Muller E, Nargeot J, Snutch TP et al. (2011) T-type calcium channels contribute to colonic hypersensitivity in a rat model of irritable bowel syndrome. Proc Natl Acad Sci USA 108, 11268-11273.
King GF, Gentz MC, Escoubas P & Nicholson GM (2008) A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 52, 264-276.
King GF, Tedford HW & Maggio F (2002) Structure and function of insecticidal neurotoxins from Australian funnel-web spiders. J Toxicol Toxin Rev 21, 361-389.
Norton RS & Pallaghy PK (1998) The cystine knot structure of ion channel toxins and related polypeptides. Toxicon 36, 1573-1583.
Behrendt R, White P & Offer J (2016) Advances in Fmoc solid-phase peptide synthesis. J Pept Sci 22, 4-27.
Jordan JB, Poppe L, Haniu M, Arvedson T, Syed R, Li V, Kohno H, Kim H, Schnier PD, Harvey TS et al. (2009) Hepcidin revisited, disulfide connectivity, dynamics, and structure. J Biol Chem 284, 24155-24167.
Klint JK, Senff S, Rupasinghe DB, Er SY, Herzig V, Nicholson GM & King GF (2012) Spider-venom peptides that target voltage-gated sodium channels: pharmacological tools and potential therapeutic leads. Toxicon 60, 478-491.
Cardoso FC, Castro J, Grundy L, Schober G, Garcia-Caraballo S, Zhao T, Herzig V, King GF, Brierley SM & Lewis RJ (2021) A spider-venom peptide with multitarget activity on sodium and calcium channels alleviates chronic visceral pain in a model of irritable bowel syndrome. Pain 162, 569-581.
Dos Santos RG, Van Renterghem C, Martin-Moutot N, Mansuelle P, Cordeiro MN, Diniz CR, Mori Y, De Lima ME & Seagar M (2002) Phoneutria nigriventer ω-phonetoxin IIA blocks the Cav2 family of calcium channels and interacts with ω-conotoxin-binding sites. J Biol Chem 277, 13856-13862.
Wang M, Guan X & Liang S (2007) The cross channel activities of spider neurotoxin huwentoxin-I on rat dorsal root ganglion neurons. Biochem Biophys Res Commun 357, 579-583.
Liang S, Zhang D, Pan X, Chen Q & Zhou P (1993) Properties and amino acid sequence of huwentoxin-I, a neurotoxin purified from the venom of the Chinese bird spider Selenocosmia huwena. Toxicon 31, 969-978.
Jiang L, Peng L, Chen J, Zhang Y, Xiong X & Liang S (2008) Molecular diversification based on analysis of expressed sequence tags from the venom glands of the Chinese bird spider Ornithoctonus huwena. Toxicon 51, 1479-1489.
Liu Z, Dai J, Dai L, Deng M, Hu Z, Hu W & Liang S (2006) Function and solution structure of huwentoxin-X, a specific blocker of N-type calcium channels, from the Chinese bird spider Ornithoctonus huwena. J Biol Chem 281, 8628-8635.
Bindokas VP & Adams ME (1989) Omega-Aga-I: a presynaptic calcium channel antagonist from venom of the funnel web spider, Agelenopsis aperta. J Neurobiol 20, 171-188.
Adams E, Bindokas VP, Hasegawa L & Venema VJ (1990) Omega-agatoxins: novel calcium channel antagonists of two subtypes from funnel web spider (Agelenopsis aperta) venom. J Biol Chem 265, 861-867.
Ertel EA, Warren VA, Adams ME, Griffin PR, Cohen CJ & Smith MM (1994) Type III omega-agatoxins: a family of probes for similar binding sites on L- and N-type calcium channels. Biochemistry 33, 5098-5108.
Yan L & Adams ME (2000) The spider toxin ω-Aga IIIA defines a high affinity site on neuronal high voltage-activated calcium channels. J Biol Chem 275, 21309-21316.
Leão RM, Cruz JS, Diniz CR, Cordeiro MN & Beirão PSL (2000) Inhibition of neuronal high-voltage activated calcium channels by the ω-Phoneutria nigriventer Tx3-3 peptide toxin. Neuropharmacology 39, 1756-1767.
Cordeiro MN, de Figueiredo SG, Valentim AC, Diniz CR, von Eickstedt VRD, Gilroy J & Richardson M (1993) Purification and amino acid sequences of six Tx3 type neurotoxins from the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (keys.). Toxicon 31, 35-42.
Vieira LB, Kushmerick C, Hildebrand ME, Garcia E, Stea A, Cordeiro MN, Richardson M, Gomez MV & Snutch TP (2005) Inhibition of high voltage-activated calcium channels by spider toxin PnTx3-6. J Pharmacol Exp Ther 314, 1370-1377.
Vieira LB, Pimenta AMC, Richardson M, Bemquerer MP, Reis HJ, Cruz JS, Gomez MV, Santoro MM, Ferreira-de-Oliveira R, Figueiredo SG et al. (2007) Leftward shift in the voltage-dependence for Ca2+ currents activation induced by a new toxin from Phoneutria reidyi (Aranae, Ctenidae) venom. Cell Mol Neurobiol 27, 129-146.
Richardson M, Pimenta AMC, Bemquerer MP, Santoro MM, Beirao PSL, Lima ME, Figueiredo SG, Bloch C, Vasconcelos EAR, Campos FAP et al. (2006) Comparison of the partial proteomes of the venoms of Brazilian spiders of the genus Phoneutria. Comp Biochem Physiol C Toxicol Pharmacol 142, 173-187.
Newcomb R, Palma A, Fox J, Gaur S, Lau K, Chung D, Cong R, Bell JR & Horne B (1995) SNX-325, a novel calcium antagonist from the spider Segestria florentina. Biochemistry 34, 8341-8347.
Herzig V, Chen Y-C, Chin YK-Y, Dekan Z, Chang Y-W, Yu H-M, Alewood PF, Chen C-C & King GF (2022) The tarantula toxin ω-Avsp1a specifically inhibits human CaV3.1 and CaV3.3 via the extracellular S3-S4 loop of the domain 1 voltage-sensor. Biomedicine 10, 1066.
Gonzales J, Demetrio de Souza Franca P, Jiang Y, Pirovano G, Kossatz S, Guru N, Yarilin D, Agwa AJ, Schroeder CI, Patel S et al. (2019) Fluorescence imaging of peripheral nerves by a Nav1.7-targeted inhibitor cystine knot peptide. Bioconjug Chem 30, 2879-2888.
Lim WK, Rösgen J & Englander SW (2009) Urea, but not guanidinium, destabilizes proteins by forming hydrogen bonds to the peptide group. Proc Natl Acad Sci USA 106, 2595-2600.
Kim D, Song I, Keum S, Lee T, Jeong M-J, Kim S-S, McEnery MW & Shin H-S (2001) Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking α1G T-type Ca2+ channels. Neuron 31, 35-45.
Choi S, Yu E, Hwang E & Llinás RR (2016) Pathophysiological implication of CaV3.1 T-type Ca 2+ channels in trigeminal neuropathic pain. Proc Natl Acad Sci USA 113, 2270-2275.
Timic Stamenic T, Feseha S, Valdez R, Zhao W, Klawitter J & Todorovic SM (2019) Alterations in oscillatory behavior of central medial thalamic neurons demonstrate a key role of CaV3.1 isoform of T-channels during isoflurane-induced anesthesia. Cereb Cortex 29, 4679-4696.
Sakkaki S, Gangarossa G, Lerat B, Françon D, Forichon L, Chemin J, Valjent E, Lerner-Natoli M & Lory P (2016) Blockade of T-type calcium channels prevents tonic-clonic seizures in a maximal electroshock seizure model. Neuropharmacology 101, 320-329.
Astori S, Wimmer RD, Prosser HM, Corti C, Corsi M, Liaudet N, Volterra A, Franken P, Adelman JP & Lüthi A (2011) The Ca(V)3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proc Natl Acad Sci USA 108, 13823-13828.
Bourinet E & Zamponi GW (2017) Block of voltage-gated calcium channels by peptide toxins. Neuropharmacology 127, 109-115.
Rogart RB, Cribbs LL, Muglia LK, Kephart DD & Kaiser MW (1989) Molecular cloning of a putative tetrodotoxin-resistant rat heart Na+ channel isoform. Proc Natl Acad Sci USA 86, 8170-8174.
Caldwell JH, Schaller KL, Lasher RS, Peles E & Levinson SR (2000) Sodium channel Na(v)1.6 is localized at nodes of ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 97, 5616-5620.
Mueller A, Dekan Z, Kaas Q, Agwa AJ, Starobova H, Alewood PF, Schroeder CI, Mobli M, Deuis JR & Vetter I (2020) Mapping the molecular surface of the analgesic NaV1.7-selective peptide Pn3a reveals residues essential for membrane and channel interactions. ACS Pharmacol Transl Sci 3, 535-546.
Sekiguchi F & Kawabata A (2013) T-type calcium channels: functional regulation and implication in pain signaling. J Pharmacol Sci 122, 244-250.
McMahon KL, Tran HNT, Deuis JR, Lewis RJ, Vetter I & Schroeder CI (2020) Discovery, pharmacological characterisation and NMR structure of the novel μ-conotoxin SxIIIC, a potent and irreversible NaV channel inhibitor. Biomedicine 8, E391.
Wüthrich K (1986) NMR of Proteins and Nucleic Acids. Wiley, New York, NY.
Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J & Laue ED (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696.
Güntert P (2004) Automated NMR structure calculation with CYANA. In Protein NMR Techniques (Kristina Downing A, ed.), pp. 353-378. Humana Press, New Jersey.
Koradi R, Billeter M & Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14, 51-55.
Waterhouse AM, Procter JB, Martin DMA, Clamp M & Barton GJ (2009) Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191.
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC & Ferrin TE (2004) UCSF Chimera?A visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.

Auteurs

Julien Giribaldi (J)

IBMM, CNRS, ENSCM, Université de Montpellier, France.
Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA.

Jean Chemin (J)

Institute of Functional Genomics, CNRS, INSERM, Montpellier University, France.

Marie Tuifua (M)

IBMM, CNRS, ENSCM, Université de Montpellier, France.

Jennifer R Deuis (JR)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld, Australia.

Rosanna Mary (R)

IBMM, CNRS, ENSCM, Université de Montpellier, France.

Irina Vetter (I)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld, Australia.
School of Pharmacy, The University of Queensland, Woolloongabba, Qld, Australia.

David T Wilson (DT)

Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Qld, Australia.

Norelle L Daly (NL)

Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Qld, Australia.

Christina I Schroeder (CI)

Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USA.
Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld, Australia.

Emmanuel Bourinet (E)

Institute of Functional Genomics, CNRS, INSERM, Montpellier University, France.

Sébastien Dutertre (S)

IBMM, CNRS, ENSCM, Université de Montpellier, France.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH