Characterization of a novel BmαTX47 toxin modulating sodium channels: The crucial role of expression vectors in toxin pharmacological activity

Toxins

Volumn 6, Issue 3, 2014, Pages 816-829

  Li, Tian ^a   Xu, Lingna ^a   Liu, Honglian ^a   He, Yawen ^a   Liang, Songping ^b   Li, Wenxin ^a   Wu, Yingliang ^a  

^a WUHAN UNIVERSITY   (China)

^b HUNAN NORMAL UNIVERSITY   (China)

Author keywords

Bm TX47; Buthus martensii karsch; pET 14b vector; pET 28a vector; Recombinant expression; Sodium channels

Indexed keywords

ALPHA TX47 TOXIN; RECOMBINANT PROTEIN; SCORPION VENOM; SODIUM CHANNEL; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.4; SODIUM CHANNEL NAV1.5; UNCLASSIFIED DRUG;

ARTICLE; BUTHUS MARTENSII; CONTROLLED STUDY; DNA LIBRARY; DNA SEQUENCE; ELECTROPHYSIOLOGY; EXPRESSION VECTOR; HUMAN; HUMAN CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PURIFICATION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SCORPION; SCREENING; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; GENE EXPRESSION; GENETIC VECTORS; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PLASMIDS; SCORPION VENOMS; SCORPIONS; SEQUENCE ALIGNMENT; SODIUM CHANNELS;

EID: 84894630909     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins6030816     Document Type: Article

References (45)

1. Catterall, W.A. Voltage-gated sodium channels at 60: Structure, function and pathophysiology. J. Physiol. 2012, 590, 2577-2589.
2. Catterall, W.A.; Goldin, A.L.; Waxman, S.G. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 2005, 57, 397-409.
3. Beneski, D.A.; Catterall, W.A. Covalent labeling of protein components of the sodium channel with a photoactivable derivative of scorpion toxin. Proc. Natl. Acad. Sci. USA 1980, 77, 639-643.
4. Yang, N.; Horn, R. Evidence for voltage-dependent S4 movement in sodium channels. Neuron 1995, 15, 213-218.
5. Yang, N.; George, A.L., Jr.; Horn, R. Molecular basis of charge movement in voltage-gated sodium channels. Neuron 1996, 16, 113-122.
6. Chanda, B.; Bezanilla, F. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J. Gen. Physiol. 2002, 120, 629-645.
7. Catterall, W.A.; Cestele, S.; Yarov-Yarovoy, V.; Yu, F.H.; Konoki, K.; Scheuer, T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49, 124-141.
8. Bosmans, F.; Tytgat, J. Voltage-gated sodium channel modulation by scorpion alpha-toxins. Toxicon 2007, 49, 142-158.
9. Chen, H.; Gordon, D.; Heinemann, S.H. Modulation of cloned skeletal muscle sodium channels by the scorpion toxins Lqh II, Lqh III, and Lqh alphaIT. Pflugers Arch. 2000, 439, 423-432.
10. Leipold, E.; Lu, S.; Gordon, D.; Hansel, A.; Heinemann, S.H. Combinatorial interaction of scorpion toxins Lqh-2, Lqh-3, and LqhalphaIT with sodium channel receptor sites-3. Mol. Pharmacol. 2004, 65, 685-691.
11. Gilles, N.; Blanchet, C.; Shichor, I.; Zaninetti, M.; Lotan, I.; Bertrand, D.; Gordon, D. A scorpion alpha-like toxin that is active on insects and mammals reveals an unexpected specificity and distribution of sodium channel subtypes in rat brain neurons. J. Neurosci. 1999, 19, 8730-8739.
12. Krimm, I.; Gilles, N.; Sautiere, P.; Stankiewicz, M.; Pelhate, M.; Gordon, D.; Lancelin, J.M. NMR structures and activity of a novel alpha-like toxin from the scorpion Leiurus quinquestriatus hebraeus. J. Mol. Biol. 1999, 285, 1749-1763.
13. Zilberberg, N.; Froy, O.; Loret, E.; Cestele, S.; Arad, D.; Gordon, D.; Gurevitz, M. Identification of structural elements of a scorpion alpha-neurotoxin important for receptor site recognition. J. Biol. Chem. 1997, 272, 14810-14816.
14. Chen, H.; Heinemann, S.H. Interaction of scorpion alpha-toxins with cardiac sodium channels: Binding properties and enhancement of slow inactivation. J. Gen. Physiol. 2001, 117, 505-518.
15. Kahn, R.; Karbat, I.; Ilan, N.; Cohen, L.; Sokolov, S.; Catterall, W.A.; Gordon, D.; Gurevitz, M. Molecular requirements for recognition of brain voltage-gated sodium channels by scorpion alpha-toxins. J. Biol. Chem. 2009, 284, 20684-20691.
16. Gur, M.; Kahn, R.; Karbat, I.; Regev, N.; Wang, J.; Catterall, W.A.; Gordon, D.; Gurevitz, M. Elucidation of the molecular basis of selective recognition uncovers the interaction site for the core domain of scorpion alpha-toxins on sodium channels. J. Biol. Chem. 2011, 286, 35209-35217.
17. + channel voltage sensor. Proc. Natl. Acad. Sci. USA 2011, 108, 15426-15431.
18. Sun, Y.M.; Bosmans, F.; Zhu, R.H.; Goudet, C.; Xiong, Y.M.; Tytgat, J.; Wang, D.C. Importance of the conserved aromatic residues in the scorpion alpha-like toxin BmK M1: The hydrophobic surface region revisited. J. Biol. Chem. 2003, 278, 24125-24131.
19. Wang, C.G.; Gilles, N.; Hamon, A.; Le Gall, F.; Stankiewicz, M.; Pelhate, M.; Xiong, Y.M.; Wang, D.C.; Chi, C.W. Exploration of the functional site of a scorpion alpha-like toxin by site-directed mutagenesis. Biochemistry 2003, 42, 4699-4708.
20. Dai, H.; Yin, S.; Li, T.; Cao, Z.; Ji, Y.; Wu, Y.; Li, W. Recombinant expression, purification, and characterization of scorpion toxin BmalphaTX14. Protein Expr. Purif. 2012, 82, 325-331.
21. Han, S.; Yi, H.; Yin, S.J.; Chen, Z.Y.; Liu, H.; Cao, Z.J.; Wu, Y.L.; Li, W.X. Structural basis of a potent peptide inhibitor designed for Kv1.3 channel, a therapeutic target of autoimmune disease. J. Biol. Chem. 2008, 283, 19058-19065.
22. Chen, Z.; Hu, Y.; Han, S.; Yin, S.; He, Y.; Wu, Y.; Cao, Z.; Li, W. ImKTx1, a new Kv1.3 channel blocker with a unique primary structure. J. Biochem. Mol. Toxicol. 2011, 25, 244-251.
23. Chen, Z.Y.; Zeng, D.Y.; Hu, Y.T.; He, Y.W.; Pan, N.; Ding, J.P.; Cao, Z.J.; Liu, M.L.; Li, W.X.; Yi, H. et al. Structural and functional diversity of acidic scorpion potassium channel toxins. PLoS One 2012, 7, e35154.
24. Karbat, I.; Kahn, R.; Cohen, L.; Ilan, N.; Gilles, N.; Corzo, G.; Froy, O.; Gur, M.; Albrecht, G.; Heinemann, S.H. et al. The unique pharmacology of the scorpion alpha-like toxin Lqh3 is associated with its flexible C-tail. FEBS J. 2007, 274, 1918-1931.
25. Li, S.; Ma, Y.; Jang, S.; Wu, Y.; Liu, H.; Cao, Z.; Li, W. A HindIII BAC library construction of Mesobuthus martensii Karsch (Scorpiones:Buthidae): An important genetic resource for comparative genomics and phylogenetic analysis. Genes Genet. Syst. 2009, 84, 417-424.
26. Ma, Y.; Zhao, R.; He, Y.; Li, S.; Liu, J.; Wu, Y.; Cao, Z.; Li, W. Transcriptome analysis of the venom gland of the scorpion Scorpiops jendeki: Implication for the evolution of the scorpion venom arsenal. BMC Genomics 2009, 10, 290.
27. He, Y.; Zhao, R.; Di, Z.; Li, Z.; Xu, X.; Hong, W.; Wu, Y.; Zhao, H.; Li, W.; Cao, Z. Molecular diversity of Chaerilidae venom peptides reveals the dynamic evolution of scorpion venom components from Buthidae to non-Buthidae. J. Proteomics 2013, 89, 1-14.
28. Gong, J.; Kini, R.M.; Gwee, M.C.; Gopalakrishnakone, P.; Chung, M.C., Makatoxin I, A novel toxin isolated from the venom of the scorpion Buthus martensi Karsch, exhibits nitrergic actions. J. Biol. Chem. 1997, 272, 8320-8324.
29. Chen, H.; Lu, S.; Leipold, E.; Gordon, D.; Hansel, A.; Heinemann, S.H. Differential sensitivity of sodium channels from the central and peripheral nervous system to the scorpion toxins Lqh-2 and Lqh-3. Eur. J. Neurosci. 2002, 16, 767-770.
30. Liu, L.H.; Bosmans, F.; Maertens, C.; Zhu, R.H.; Wang, D.C.; Tytgat, J. Molecular basis of the mammalian potency of the scorpion alpha-like toxin, BmK M1. FASEB J. 2005, 19, 594-596.
31. + channel selectivity of the scorpion alpha-like toxin BmK M1. J. Mol. Biol. 2005, 353, 788-803.
32. Weinberger, H.; Moran, Y.; Gordon, D.; Turkov, M.; Kahn, R.; Gurevitz, M. Positions under positive selection--key for selectivity and potency of scorpion alpha-toxins. Mol. Biol. Evol. 2010, 27, 1025-1034.
33. Chen, R.; Chung, S.H. Binding modes and functional surface of anti-mammalian scorpion alpha-toxins to sodium channels. Biochemistry 2012, 51, 7775-7782.
34. Durek, T.; Vetter, I.; Wang, C.I.; Motin, L.; Knapp, O.; Adams, D.J.; Lewis, R.J.; Alewood, P.F. Chemical engineering and structural and pharmacological characterization of the alpha-scorpion toxin OD1. ACS Chem. Biol. 2013, 8, 1215-1222.
35. Wang, K.; Yin, S.J.; Lu, M.; Yi, H.; Dai, C.; Xu, X.J.; Cao, Z.J.; Wu, Y.L.; Li, W.X. Functional analysis of the alpha-neurotoxin, BmalphaTX14, derived from the Chinese scorpion, Buthus martensii Karsch. Biotechnol. Lett. 2006, 28, 1767-1772.
36. Zhu, S.; Peigneur, S.; Gao, B.; Lu, X.; Cao, C.; Tytgat, J. Evolutionary diversification of Mesobuthus alpha-scorpion toxins affecting sodium channels. Mol. Cell. Proteomics 2012, 11, doi:10.1074/mcp.M111.012054.
37. + channels: Primary structure and function of two isoforms and alternatively spliced variants. Am. J. Physiol.-Heart Circ. Physiol. 2002, 282, H1007-H1017.
38. Yu, J.B.; Ji, P.; Zha, X.M.; Shen, W.D.; Wu, X.F. Cloning and expression of Buthus martensii Karsch scorpion toxin gene (BmK IT3) in Escherichia coli. Sheng Wu Gong Cheng Xue Bao 2002, 18, 106-108.
39. + channels. Biochimie 2013, 95, 1732-1740.
40. Zilberberg, N.; Gordon, D.; Pelhate, M.; Adams, M.E.; Norris, T.M.; Zlotkin, E.; Gurevitz, M. Functional expression and genetic alteration of an alpha scorpion neurotoxin. Biochemistry 1996, 35, 10215-10222.
41. Karbat, I.; Frolow, F.; Froy, O.; Gilles, N.; Cohen, L.; Turkov, M.; Gordon, D.; Gurevitz, M. Molecular basis of the high insecticidal potency of scorpion alpha-toxins. J. Biol. Chem. 2004, 279, 31679-31686.
42. Karbat, I.; Turkov, M.; Cohen, L.; Kahn, R.; Gordon, D.; Gurevitz, M.; Frolow, F. X-ray structure and mutagenesis of the scorpion depressant toxin LqhIT2 reveals key determinants crucial for activity and anti-insect selectivity. J. Mol. Biol. 2007, 366, 586-601.
43. Sun, Y.M.; Liu, W.; Zhu, R.H.; Goudet, C.; Tytgat, J.; Wang, D.C. Roles of disulfide bridges in scorpion toxin BmK M1 analyzed by mutagenesis. J. Pept. Res. 2002, 60, 247-256.
44. Chen, Z.Y.; Hu, Y.T.; Yang, W.S.; He, Y.W.; Feng, J.; Wang, B.; Zhao, R.M.; Ding, J.P.; Cao, Z.J.; Li, W.X. et al. Hg1, novel peptide inhibitor specific for Kv1.3 channels from first scorpion Kunitz-type potassium channel toxin family. J. Biol. Chem. 2012, 287, 13813-13821.
45. Zhao, R.; Dai, H.; Qiu, S.; Li, T.; He, Y.; Ma, Y.; Chen, Z.; Wu, Y.; Li, W.; Cao, Z. SdPI, the first functionally characterized Kunitz-type trypsin inhibitor from scorpion venom. PLoS One 2011, 6, e27548.