A tarantula-venom peptide antagonizes the TRPA1 nociceptor Ion channel by binding to the S1-S4 gating domain

Current Biology

Volumn 24, Issue 5, 2014, Pages 473-483

  Gui, Junhong ^a   Liu, Boyi ^a   Cao, Guan ^a   Lipchik, Andrew M ^b   Perez, Minervo ^b   Dekan, Zoltan ^c   Mobli, Mehdi ^c   Daly, Norelle L ^d   Alewood, Paul F ^c   Parker, Laurie L ^b   King, Glenn F ^c   Zhou, Yufeng ^a   Jordt, Sven Eric ^a   Nitabach, Michael N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARANEAE; TARANTULA; THRIXOPELMA PRURIENS;

PEPTIDE; SODIUM CHANNEL NAV1.2; SPIDER VENOM; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VOLTAGE GATED SODIUM CHANNEL BLOCKING AGENT; XENOPUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; FEMALE; GENE LIBRARY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; OOCYTE; PRECLINICAL STUDY; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DRUG EVALUATION, PRECLINICAL; FEMALE; GENE LIBRARY; HUMANS; MOLECULAR SEQUENCE DATA; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; OOCYTES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SPIDER VENOMS; TRANSIENT RECEPTOR POTENTIAL CHANNELS; VOLTAGE-GATED SODIUM CHANNEL BLOCKERS; XENOPUS PROTEINS;

EID: 84897663183     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.01.013     Document Type: Article

References (62)

1. L.J. Wu, T.B. Sweet, and D.E. Clapham International Union of Basic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family Pharmacol. Rev. 62 2010 381 404
2. C. Montell The TRP superfamily of cation channels Sci. STKE 2005 2005 re3
3. B. Nilius TRP channels in disease Biochim. Biophys. Acta 1772 2007 805 812
4. G.M. Story, A.M. Peier, A.J. Reeve, S.R. Eid, J. Mosbacher, T.R. Hricik, T.J. Earley, A.C. Hergarden, D.A. Andersson, and S.W. Hwang et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures Cell 112 2003 819 829
5. L.J. Macpherson, B.H. Geierstanger, V. Viswanath, M. Bandell, S.R. Eid, S. Hwang, and A. Patapoutian The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin Curr. Biol. 15 2005 929 934
6. D.M. Bautista, P. Movahed, A. Hinman, H.E. Axelsson, O. Sterner, E.D. Högestätt, D. Julius, S.E. Jordt, and P.M. Zygmunt Pungent products from garlic activate the sensory ion channel TRPA1 Proc. Natl. Acad. Sci. USA 102 2005 12248 12252
7. V. Meseguer, Y. Karashima, K. Talavera, D. D'Hoedt, T. Donovan-Rodríguez, F. Viana, B. Nilius, and T. Voets Transient receptor potential channels in sensory neurons are targets of the antimycotic agent clotrimazole J. Neurosci. 28 2008 576 586
8. K. Hill, and M. Schaefer TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine J. Biol. Chem. 282 2007 7145 7153
9. D.A. Andersson, C. Gentry, S. Moss, and S. Bevan Clioquinol and pyrithione activate TRPA1 by increasing intracellular Zn2+ Proc. Natl. Acad. Sci. USA 106 2009 8374 8379
10. D.M. Bautista, S.E. Jordt, T. Nikai, P.R. Tsuruda, A.J. Read, J. Poblete, E.N. Yamoah, A.I. Basbaum, and D. Julius TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents Cell 124 2006 1269 1282
11. S. Wang, Y. Dai, T. Fukuoka, H. Yamanaka, K. Kobayashi, K. Obata, X. Cui, M. Tominaga, and K. Noguchi Phospholipase C and protein kinase A mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain Brain 131 2008 1241 1251
12. Y. Dai, S. Wang, M. Tominaga, S. Yamamoto, T. Fukuoka, T. Higashi, K. Kobayashi, K. Obata, H. Yamanaka, and K. Noguchi Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain J. Clin. Invest. 117 2007 1979 1987
13. K. Nagata, A. Duggan, G. Kumar, and J. García-Añoveros Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing J. Neurosci. 25 2005 4052 4061
14. S. Du, I. Araki, H. Kobayashi, H. Zakoji, N. Sawada, and M. Takeda Differential expression profile of cold (TRPA1) and cool (TRPM8) receptors in human urogenital organs Urology 72 2008 450 455
15. T. Streng, H.E. Axelsson, P. Hedlund, D.A. Andersson, S.E. Jordt, S. Bevan, K.E. Andersson, E.D. Högestätt, and P.M. Zygmunt Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder Eur. Urol. 53 2008 391 399
16. S. Earley, A.L. Gonzales, and R. Crnich Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca2+-Activated K+ channels Circ. Res. 104 2009 987 994
17. C. Gratzke, P. Weinhold, O. Reich, M. Seitz, B. Schlenker, C.G. Stief, K.E. Andersson, and P. Hedlund Transient receptor potential A1 and cannabinoid receptor activity in human normal and hyperplastic prostate: relation to nerves and interstitial cells Eur. Urol. 57 2010 902 910
18. E.L. Andrade, S. Forner, A.F. Bento, D.F. Leite, M.A. Dias, P.C. Leal, J. Koepp, and J.B. Calixto TRPA1 receptor modulation attenuates bladder overactivity induced by spinal cord injury Am. J. Physiol. Renal Physiol. 300 2011 F1223 F1234
19. K. Obata, H. Katsura, T. Mizushima, H. Yamanaka, K. Kobayashi, Y. Dai, T. Fukuoka, A. Tokunaga, M. Tominaga, and K. Noguchi TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury J. Clin. Invest. 115 2005 2393 2401
20. D.S. da Costa, F.C. Meotti, E.L. Andrade, P.C. Leal, E.M. Motta, and J.B. Calixto The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation Pain 148 2010 431 437
21. M. Petrus, A.M. Peier, M. Bandell, S.W. Hwang, T. Huynh, N. Olney, T. Jegla, and A. Patapoutian A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition Mol. Pain 3 2007 40
22. A. Patapoutian, S. Tate, and C.J. Woolf Transient receptor potential channels: targeting pain at the source Nat. Rev. Drug Discov. 8 2009 55 68
23. S.R. Eid, E.D. Crown, E.L. Moore, H.A. Liang, K.C. Choong, S. Dima, D.A. Henze, S.A. Kane, and M.O. Urban HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity Mol. Pain 4 2008 48
24. J. Chen, S.K. Joshi, S. DiDomenico, R.J. Perner, J.P. Mikusa, D.M. Gauvin, J.A. Segreti, P. Han, X.F. Zhang, and W. Niforatos et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation Pain 152 2011 1165 1172
25. B. Kremeyer, F. Lopera, J.J. Cox, A. Momin, F. Rugiero, S. Marsh, C.G. Woods, N.G. Jones, K.J. Paterson, and F.R. Fricker et al. A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome Neuron 66 2010 671 680
26. E.L. Andrade, F.C. Meotti, and J.B. Calixto TRPA1 antagonists as potential analgesic drugs Pharmacol. Ther. 133 2012 189 204
27. F. Viana, and A. Ferrer-Montiel TRPA1 modulators in preclinical development Expert Opin. Ther. Pat. 19 2009 1787 1799
28. G.F. King Venoms as a platform for human drugs: translating toxins into therapeutics Expert Opin. Biol. Ther. 11 2011 1469 1484
29. S. Dutertre, and R.J. Lewis Use of venom peptides to probe ion channel structure and function J. Biol. Chem. 285 2010 13315 13320
30. K.J. Swartz, and R. MacKinnon Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites Neuron 18 1997 665 673
31. K.J. Swartz, and R. MacKinnon Mapping the receptor site for hanatoxin, a gating modifier of voltage-dependent K+ channels Neuron 18 1997 675 682
32. V. Tsetlin, Y. Utkin, and I. Kasheverov Polypeptide and peptide toxins, magnifying lenses for binding sites in nicotinic acetylcholine receptors Biochem. Pharmacol. 78 2009 720 731
33. T.P. Snutch Targeting chronic and neuropathic pain: the N-type calcium channel comes of age NeuroRx 2 2005 662 670
34. I. Ibañez-Tallon, H. Wen, J.M. Miwa, J. Xing, A.B. Tekinay, F. Ono, P. Brehm, and N. Heintz Tethering naturally occurring peptide toxins for cell-autonomous modulation of ion channels and receptors in vivo Neuron 43 2004 305 311
35. Y. Wu, G. Cao, B. Pavlicek, X. Luo, and M.N. Nitabach Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin PLoS Biol. 6 2008 e273
36. R.E. Middleton, V.A. Warren, R.L. Kraus, J.C. Hwang, C.J. Liu, G. Dai, R.M. Brochu, M.G. Kohler, Y.D. Gao, and V.M. Garsky et al. Two tarantula peptides inhibit activation of multiple sodium channels Biochemistry 41 2002 14734 14747
37. B.T. Priest, K.M. Blumenthal, J.J. Smith, V.A. Warren, and M.M. Smith ProTx-I and ProTx-II: gating modifiers of voltage-gated sodium channels Toxicon 49 2007 194 201
38. T. Ohkubo, J. Yamazaki, and K. Kitamura Tarantula toxin ProTx-I differentiates between human T-type voltage-gated Ca2+ Channels Cav3.1 and Cav3.2 J. Pharmacol. Sci. 112 2010 452 458
39. M.M. Moran, M.A. McAlexander, T. Bíró, and A. Szallasi Transient receptor potential channels as therapeutic targets Nat. Rev. Drug Discov. 10 2011 601 620
40. D.A. Andersson, C. Gentry, S. Moss, and S. Bevan Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress J. Neurosci. 28 2008 2485 2494
41. B.F. Bessac, M. Sivula, C.A. von Hehn, J. Escalera, L. Cohn, and S.E. Jordt TRPA1 is a major oxidant sensor in murine airway sensory neurons J. Clin. Invest. 118 2008 1899 1910
42. A. Hinman, H.H. Chuang, D.M. Bautista, and D. Julius TRP channel activation by reversible covalent modification Proc. Natl. Acad. Sci. USA 103 2006 19564 19568
43. L.J. Macpherson, A.E. Dubin, M.J. Evans, F. Marr, P.G. Schultz, B.F. Cravatt, and A. Patapoutian Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines Nature 445 2007 541 545
44. M. Trevisani, J. Siemens, S. Materazzi, D.M. Bautista, R. Nassini, B. Campi, N. Imamachi, E. Andrè, R. Patacchini, and G.S. Cottrell et al. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1 Proc. Natl. Acad. Sci. USA 104 2007 13519 13524
45. J. Escalera, C.A. von Hehn, B.F. Bessac, M. Sivula, and S.E. Jordt TRPA1 mediates the noxious effects of natural sesquiterpene deterrents J. Biol. Chem. 283 2008 24136 24144
46. B. Xiao, A.E. Dubin, B. Bursulaya, V. Viswanath, T.J. Jegla, and A. Patapoutian Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels J. Neurosci. 28 2008 9640 9651
47. F. Bosmans, M.F. Martin-Eauclaire, and K.J. Swartz Deconstructing voltage sensor function and pharmacology in sodium channels Nature 456 2008 202 208
48. S. Sokolov, R.L. Kraus, T. Scheuer, and W.A. Catterall Inhibition of sodium channel gating by trapping the domain II voltage sensor with protoxin II Mol. Pharmacol. 73 2008 1020 1028
49. J.C. Rogers, Y. Qu, T.N. Tanada, T. Scheuer, and W.A. Catterall Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit J. Biol. Chem. 271 1996 15950 15962
50. W.A. Catterall Membrane potential-dependent binding of scorpion toxin to the action potential Na+ ionophore. Studies with a toxin derivative prepared by lactoperoxidase-catalyzed iodination J. Biol. Chem. 252 1977 8660 8668
51. L.R. Phillips, M. Milescu, Y. Li-Smerin, J.A. Mindell, J.I. Kim, and K.J. Swartz Voltage-sensor activation with a tarantula toxin as cargo Nature 436 2005 857 860
52. J.J. Smith, T.R. Cummins, S. Alphy, and K.M. Blumenthal Molecular interactions of the gating modifier toxin ProTx-II with NaV 1.5: implied existence of a novel toxin binding site coupled to activation J. Biol. Chem. 282 2007 12687 12697
53. H.W. Tedford, N. Gilles, A. Ménez, C.J. Doering, G.W. Zamponi, and G.F. King Scanning mutagenesis of omega-atracotoxin-Hv1a reveals a spatially restricted epitope that confers selective activity against insect calcium channels J. Biol. Chem. 279 2004 44133 44140
54. F. Maggio, and G.F. King Scanning mutagenesis of a Janus-faced atracotoxin reveals a bipartite surface patch that is essential for neurotoxic function J. Biol. Chem. 277 2002 22806 22813
55. J.M. Wang, S.H. Roh, S. Kim, C.W. Lee, J.I. Kim, and K.J. Swartz Molecular surface of tarantula toxins interacting with voltage sensors in K(v) channels J. Gen. Physiol. 123 2004 455 467
56. D. Ren, B. Navarro, H. Xu, L. Yue, Q. Shi, and D.E. Clapham A prokaryotic voltage-gated sodium channel Science 294 2001 2372 2375
57. J. Chen, M. Deng, Q. He, E. Meng, L. Jiang, Z. Liao, M. Rong, and S. Liang Molecular diversity and evolution of cystine knot toxins of the tarantula Chilobrachys jingzhao Cell. Mol. Life Sci. 65 2008 2431 2444
58. J.I. Fletcher, R. Smith, S.I. O'Donoghue, M. Nilges, M. Connor, M.E. Howden, M.J. Christie, and G.F. King The structure of a novel insecticidal neurotoxin, omega-atracotoxin-HV1, from the venom of an Australian funnel web spider Nat. Struct. Biol. 4 1997 559 566
59. X. Wang, M. Connor, R. Smith, M.W. Maciejewski, M.E. Howden, G.M. Nicholson, M.J. Christie, and G.F. King Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge Nat. Struct. Biol. 7 2000 505 513
60. J. Chen, L. Zhao, L. Jiang, E. Meng, Y. Zhang, X. Xiong, and S. Liang Transcriptome analysis revealed novel possible venom components and cellular processes of the tarantula Chilobrachys jingzhao venom gland Toxicon 52 2008 794 806
61. Z. Takacs, M. Toups, A. Kollewe, E. Johnson, L.G. Cuello, G. Driessens, M. Biancalana, A. Koide, C.G. Ponte, and E. Perozo et al. A designer ligand specific for Kv1.3 channels from a scorpion neurotoxin-based library Proc. Natl. Acad. Sci. USA 106 2009 22211 22216
62. J.W. Warmke, R.A. Reenan, P. Wang, S. Qian, J.P. Arena, J. Wang, D. Wunderler, K. Liu, G.J. Kaczorowski, and L.H. Van der Ploeg et al. Functional expression of Drosophila para sodium channels. Modulation by the membrane protein TipE and toxin pharmacology J. Gen. Physiol. 110 1997 119 133