Expression of a recombinant Phoneutria toxin active in calcium channels

Toxicon

Volumn 60, Issue 5, 2012, Pages 907-918

  Souza, I A ^a,c   Cino, E A ^b   Choy, W Y ^b   Cordeiro, M N ^d   Richardson, M ^d   Chavez Olortegui, C ^c   Gomez, M V ^c,e   Prado, M A M ^a,b,c   Prado, V F ^a,b,c  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d Ezequiel Dias Foundation   (Brazil)

^e IEP Santa Casa   (Brazil)

Author keywords

Bacterial expression; Calcium channel blocker; Circular dichroism; Knottin scaffold; Phoneutria nigriventer; Spider toxin

Indexed keywords

CALCIUM CHANNEL; KNOTTIN; RECOMBINANT PNTX3-4 PEPTIDE; RECOMBINANT PROTEIN; SCAFFOLD PROTEIN; SPIDER VENOM; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA CHAIN; BIOLOGICAL ACTIVITY; CIRCULAR DICHROISM; COMPUTER MODEL; MOLECULAR MODEL; NONHUMAN; PHONEUTRIA NIGRIVENTER; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; SOLUBILITY; SPIDER; TOXIN STRUCTURE;

ARANEAE; BACTERIA (MICROORGANISMS); PHONEUTRIA; PHONEUTRIA NIGRIVENTER;

EID: 84864032176     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2012.05.026     Document Type: Article

References (79)

1. Agostini R.M., do Nascimento Pinheiro A.C., Binda N.S., Romano Silva M.A., Cordeiro M.N., Richardson M., Sena Guimaraes A.L., Gomez M.V. Phoneutria spider toxins block ischemia-induced glutamate release and neuronal death of cell layers of the retina. Retina 2011, 31:1392-1399.
2. Alonso D., Khalil Z., Satkunanthan N., Livett B.G. Drugs from the sea: conotoxins as drug leads for neuropathic pain and other neurological conditions. Mini. Rev. Med. Chem. 2003, 3:785-787.
3. Arundine M., Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003, 34:325-337.
4. Butt T.R., Edavettal S.C., Hall J.P., Mattern M.R. SUMO fusion technology for difficult-to-express proteins. Protein Expr. Purif. 2005, 43:1-9.
5. Cardoso F.C., Pacifico L.G., Carvalho D.C., Victoria J.M., Neves A.L., Chavez-Olortegui C., Gomez M.V., Kalapothakis E. Molecular cloning and characterization of Phoneutria nigriventer toxins active on calcium channels. Toxicon 2003, 41:755-763.
6. + channels. Toxicon 2003, 41:305-313.
7. 2+]i in rat cortical synaptosomes. Cell Mol. Biol. (Noisy. -le-grand) 2010, 56(Suppl.):OL1223-OL1230.
8. Cassola A.C., Jaffe H., Fales H.M., Afeche S.C., Magnoli F., Cipolla-Neto J. Omega-Phonetoxin-IIA: a calcium channel blocker from the spider Phoneutria nigriventer. Pflugers Arch. 1998, 436:545-552.
9. Castellino F.J., Prorok M. Conantokins: inhibitors of ion flow through the N-methyl-D-aspartate receptor channels. Curr. Drug Targets 2000, 1:219-235.
10. Che N., Wang L., Gao Y., An C. Soluble expression and one-step purification of a neurotoxin Huwentoxin-I in Escherichia coli. Protein Expr. Purif. 2009, 65:154-159.
11. Cordeiro M.N., de Figueiredo S.G., Valentim A.C., Diniz C.R., von E.V., 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, 31:35-42.
12. Dalmolin G.D., Silva C.R., Rigo F.K., Gomes G.M., Cordeiro M.N., Richardson M., Silva M.A., Prado M.A., Gomez M.V., Ferreira J. Antinociceptive effect of Brazilian armed spider venom toxin Tx3-3 in animal models of neuropathic pain. Pain 2011, 152:2224-2232.
13. de Castro Junior C.J., Pinheiro A.C., Guatimosim C., Cordeiro M.N., Souza A.H., Richardson M., Romano-Silva M.A., Prado M.A., Gomez M.V. Tx3-4 a toxin from the venom of spider Phoneutria nigriventer blocks calcium channels associated with exocytosis. Neurosci. Lett. 2008, 439:170-172.
14. de Souza A.H., Lima M.C., Drewes C.C., da Silva J.F., Torres K.C., Pereira E.M., de Castro C.J.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 Phalpha1beta, a neurotoxin from the spider Phoneutria nigriventer: comparison with omega-conotoxin MVIIA and morphine. Toxicon 2011.
15. Diniz M.R., Theakston R.D., Crampton J.M., Cordeiro M.N., Pimenta A.M., De Lima M.E., Diniz C.R. Functional expression and purification of recombinant Tx1, a sodium channel blocker neurotoxin from the venom of the Brazilian " armed" spider, Phoneutria nigriventer. Protein Expr. Purif. 2006, 50:18-24.
16. Doering C.J., Zamponi G.W. Molecular pharmacology of high voltage-activated calcium channels. J. Bioenerg. Biomembr. 2003, 35:491-505.
17. Domin H., Zieba B., Golembiowska K., Kowalska M., Dziubina A., Smialowska M. Neuroprotective potential of mGluR5 antagonist MTEP: effects on kainate-induced excitotoxicity in the rat hippocampus. Pharmacol. Rep. 2010, 62:1051-1061.
18. Dos Santos R.G., Van R.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, 277:13856-13862.
19. Dunkley P.R., Jarvie P.E., Robinson P.J. A rapid Percoll gradient procedure for preparation of synaptosomes. Nat. Protoc. 2008, 3:1718-1728.
20. Escoubas P. Molecular diversification in spider venoms: a web of combinatorial peptide libraries. Mol. Divers. 2006, 10:545-554.
21. Fahnert B. Folding-promoting agents in recombinant protein production. Methods Mol. Biol. 2004, 267:53-74.
22. Fahnert B., Lilie H., Neubauer P. Inclusion bodies: formation and utilisation. Adv. Biochem. Eng. Biotechnol. 2004, 89:93-142.
23. Favreau P., Le G.F., Benoit E., Molgo J. A review on conotoxins targeting ion channels and acetylcholine receptors of the vertebrate neuromuscular junction. Acta Physiol. Pharmacol. Ther. Latinoam. 1999, 49:257-267.
24. Gomez M.V., Kalapothakis E., Guatimosim C., Prado M.A. Phoneutria nigriventer venom: a cocktail of toxins that affect ion channels. Cell Mol. Neurobiol. 2002, 22:579-588.
25. Goncaves J.M., Ferreira J., Prado M.A., Cordeiro M.N., Richardson M., Pinheiro A.C., Silva M.A., Junior C.J., Souza A.H., Gomez M.V. The effect of spider toxin PhTx3-4, omega-conotoxins MVIIA and MVIIC on glutamate uptake and on capsaicin-induced glutamate release and [Ca2+]i in spinal cord synaptosomes. Cell Mol. Neurobiol. 2011, 31:277-283.
26. Gracy J., Chiche L. Optimizing structural modeling for a specific protein scaffold: knottins or inhibitor cystine knots. BMC. Bioinform. 2010, 11:535.
27. Gracy J., Chiche L. Structure and modeling of knottins, a promising molecular scaffold for drug discovery. Curr. Pharm. Des. 2011, 17:4337-4350.
28. Guatimosim C., Romano-Silva M.A., Cruz J.S., Beirao P.S., Kalapothakis E., Moraes-Santos T., Cordeiro M.N., Diniz C.R., Gomez M.V., Prado M.A. A toxin from the spider Phoneutria nigriventer that blocks calcium channels coupled to exocytosis. Br. J. Pharmacol. 1997, 122:591-597.
29. Guzman L.M., Belin D., Carson M.J., Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 1995, 177:4121-4130.
30. Heading C.E. Conus peptides and neuroprotection. Curr. Opin. Investig. Drugs 2002, 3:915-920.
31. Johnson T.M., Quick M.W., Sakai T.T., Krishna N.R. Expression of functional recombinant scorpion beta-neurotoxin Css II in E. coli. Peptides 2000, 21:767-772.
32. Jones R.M., Bulaj G. Conotoxins - new vistas for peptide therapeutics. Curr. Pharm. Des. 2000, 6:1249-1285.
33. Kalapothakis E., Penaforte C.L., Beirao P.S., Romano-Silva M.A., Cruz J.S., Prado M.A., Guimaraes P.E., Gomez M.V., Prado V.F. Cloning of cDNAS encoding neurotoxic peptides from the spider Phoneutria nigriventer. Toxicon 1998, 36:1843-1850.
34. Kalapothakis E., Penaforte C.L., Leao R.M., Cruz J.S., Prado V.F., Cordeiro M.N., Diniz C.R., Romano-Silva M.A., Prado M.A., Gomez M.V., Beirao P.S. Cloning, cDNA sequence analysis and patch clamp studies of a toxin from the venom of the armed spider (Phoneutria nigriventer). Toxicon 1998, 36:1971-1980.
35. Kozlov S., Grishin E. Classification of spider neurotoxins using structural motifs by primary structure features. Single residue distribution analysis and pattern analysis techniques. Toxicon 2005, 46:672-686.
36. 2+ oscillation frequency in GH3 cells. J. Neurochem. 1999, 72:1472-1481.
37. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010, 460:525-542.
38. Leao R.M., Cruz J.S., Diniz C.R., Cordeiro M.N., Beirao P.S. Inhibition of neuronal high-voltage activated calcium channels by the omega-phoneutria nigriventer Tx3-3 peptide toxin. Neuropharmacology 2000, 39:1756-1767.
39. Lewis R.J. Conotoxin venom peptide therapeutics. Adv. Exp. Med. Biol. 2009, 655:44-48.
40. Lewis R.J., Nielsen K.J., Craik D.J., Loughnan M.L., Adams D.A., Sharpe I.A., Luchian T., Adams D.J., Bond T., Thomas L., Jones A., Matheson J.L., Drinkwater R., Andrews P.R., Alewood P.F. Novel omega-conotoxins from Conus catus discriminate among neuronal calcium channel subtypes. J. Biol. Chem. 2000, 275:35335-35344.
41. Li R.A., Tomaselli G.F. Using the deadly mu-conotoxins as probes of voltage-gated sodium channels. Toxicon 2004, 44:117-122.
42. Lilie H., Schwarz E., Rudolph R. Advances in refolding of proteins produced in E. coli. Curr. Opin. Biotechnol. 1998, 9:497-501.
43. Lipton S.A. Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat. Rev. Drug Discov. 2006, 5:160-170.
44. Lipton S.A. Pathologically-activated therapeutics for neuroprotection: mechanism of NMDA receptor block by memantine and S-nitrosylation. Curr. Drug Targets 2007, 8:621-632.
45. Livett B.G., Gayler K.R., Khalil Z. Drugs from the sea: conopeptides as potential therapeutics. Curr. Med. Chem. 2004, 11:1715-1723.
46. Malakhov M.P., Mattern M.R., Malakhova O.A., Drinker M., Weeks S.D., Butt T.R. SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J. Struct. Funct. Genomics 2004, 5:75-86.
47. Marblestone J.G., Edavettal S.C., Lim Y., Lim P., Zuo X., Butt T.R. Comparison of SUMO fusion technology with traditional gene fusion systems: enhanced expression and solubility with SUMO. Protein Sci. 2006, 15:182-189.
48. Meng E., Cai T.F., Li W.Y., Zhang H., Liu Y.B., Peng K., Liang S., Zhang D.Y. Functional expression of spider neurotoxic peptide huwentoxin-I in E. coli. PLoS. One 2011, 6:e21608.
49. +-evoked release of [3H]adenine nucleotides from rat brain cortical synaptosomes. Neurosci. Lett. 1998, 258:57-59.
50. Miranda D.M., Romano-Silva M.A., Kalapothakis E., Diniz C.R., Cordeiro M.N., Santos T.M., Prado M.A., Gomez M.V. Phoneutria nigriventer toxins block tityustoxin-induced calcium influx in synaptosomes. Neuroreport 1998, 9:1371-1373.
51. Misawa S., Kumagai I. Refolding of therapeutic proteins produced in Escherichia coli as inclusion bodies. Biopolymers 1999, 51:297-307.
52. Moura J.R., Prado M.A., Gomez M.V., Kalapothakis E., Diniz C.R., Cordeiro M.N., Romano-Silva M.A. Investigation of the effect of PhTx2, from the venom of the spider Phoneutria nigriventer, on the release of [3H]-acetylcholine from rat cerebrocortical synaptosomes. Toxicon 1998, 36:1189-1192.
53. Penaforte C.L., Prado V.F., Prado M.A., Romano-Silva M.A., Guimaraes P.E., De M.L., Gomez M.V., Kalapothakis E. Molecular cloning of cDNAs encoding insecticidal neurotoxic peptides from the spider Phoneutria nigriventer. Toxicon 2000, 38:1443-1449.
54. Pinheiro A.C., da Silva A.J., Prado M.A., 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, 19:1123-1129.
55. Prado M.A., Guatimosim C., Gomez M.V., Diniz C.R., Cordeiro M.N., Romano-Silva M.A. 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(Pt 1):145-150.
56. Prinz W.A., Aslund F., Holmgren A., Beckwith J. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J. Biol. Chem. 1997, 272:15661-15667.
57. Reis H.J., Gomez M.V., Kalapothakis E., Diniz C.R., Cordeiro M.N., Prado M.A., Romano-Silva M.A. Inhibition of glutamate uptake by Tx3-4 is dependent on the redox state of cysteine residues. Neuroreport 2000, 11:2191-2194.
58. 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.
59. Sanger F., Nicklen S., Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 1977, 74:5463-5467.
60. Sattler R., Tymianski M. Molecular mechanisms of calcium-dependent excitotoxicity. J. Mol. Med. (Berl) 2000, 78:3-13.
61. Sharp P.M., Li W.H. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987, 15:1281-1295.
62. Shu Q., Lu S.Y., Gu X.C., Liang S.P. The structure of spider toxin huwentoxin-II with unique disulfide linkage: evidence for structural evolution. Protein Sci. 2002, 11:245-252.
63. Singh S.M., Panda A.K. Solubilization and refolding of bacterial inclusion body proteins. J. Biosci. Bioeng. 2005, 99:303-310.
64. 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., 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, 140:115-126.
65. Sreerama N., Venyaminov S.Y., Woody R.W. Estimation of the number of helical and strand segments in proteins using CD spectroscopy. Protein Sci. 1999, 8:370-380.
66. Sreerama N., Woody R.W. Estimation of protein secondary structure from CD spectra: comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set. Anal. Biochem. 2000, 287:252-260.
67. Stewart C., Bailey J., Manoil C. Mutant membrane protein toxicity. J. Biol. Chem. 1998, 273:28078-28084.
68. Studier F.W., Rosenberg A.H., Dunn J.J., Dubendorff J.W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990, 185:60-89.
69. Thomas J.G., Ayling A., Baneyx F. Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins from E. coli. To fold or to refold. Appl. Biochem. Biotechnol. 1997, 66:197-238.
70. Torres F.S., Silva C.N., Lanza L.F., Santos A.V., Pimenta A.M., De Lima M.E., Diniz M.R. Functional expression of a recombinant toxin - rPnTx2-6-active in erectile function in rat. Toxicon 2010, 56:1172-1180.
71. Van Stokkum I.H.M., Spoelder H.J.W., Bloemendal M., Van Grondelle R., Groen F.C.A. Estimation of protein secondary structure and error analysis from CD spectra. Anal. Biochem. 1990, 191:110-118.
72. Vassilevski A.A., Kozlov S.A., Grishin E.V. Molecular diversity of spider venom. Biochem. (Mosc. ) 2009, 74:1505-1534.
73. 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, 314:1370-1377.
74. 2+-dependent glutamate release in synaptosomes. Neurochem. Int. 2003, 42:277-282.
75. 2+ currents activation induced by a new toxin from Phoneutria reidyi (Aranae, Ctenidae) venom. Cell Mol. Neurobiol. 2007, 27:129-146.
76. Wen S., Wilson D.T., Kuruppu S., Korsinczky M.L., Hedrick J., Pang L., Szeto T., Hodgson W.C., Alewood P.F., Nicholson G.M. Discovery of an MIT-like atracotoxin family: spider venom peptides that share sequence homology but not pharmacological properties with AVIT family proteins. Peptides 2005, 26:2412-2426.
77. Wetlaufer D.B., Branca P.A., Chen G.X. The oxidative folding of proteins by disulfide plus thiol does not correlate with redox potential. Protein Eng. 1987, 1:141-146.
78. Williams J.A., Day M., Heavner J.E. Ziconotide: an update and review. Expert Opin. Pharmacother. 2008, 9:1575-1583.
79. Yan L., Adams M.E. The spider toxin omega-Aga IIIA defines a high affinity site on neuronal high voltage-activated calcium channels. J. Biol. Chem. 2000, 275:21309-21316.