Distinct disulfide isomers of μ-conotoxins KIIIA and KIIIB block voltage-gated sodium channels

Biochemistry

Volumn 51, Issue 49, 2012, Pages 9826-9835

  Khoo, Keith K ^a,b,c   Gupta, Kallol ^d   Green, Brad R ^a   Zhang, Min Min ^e   Watkins, Maren ^e   Olivera, Baldomero M ^e   Balaram, Padmanabhan ^d   Yoshikami, Doju ^e   Bulaj, Grzegorz ^e   Norton, Raymond S ^a  

^a MONASH UNIVERSITY   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d INDIAN INSTITUTE OF SCIENCE   (India)

^e UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE PEPTIDES; CDNA SEQUENCE; COLLISION-INDUCED DISSOCIATION; CONOTOXINS; DISULFIDE BOND CONNECTIVITY; DISULFIDE BONDS; IN-VITRO; ISOFORMS; MINOR PRODUCTS; NUCLEAR MAGNETIC RESONANCE DATA; OXIDATIVE FOLDING; SODIUM CHANNEL; SODIUM CHANNEL BLOCKERS; SOLUTION STRUCTURES;

COVALENT BONDS; ISOMERS; PEPTIDES; SODIUM; TOXIC MATERIALS;

SULFUR COMPOUNDS;

COMPLEMENTARY DNA; CONOTOXIN; DISULFIDE; MU CONOTOXIN KIIIA; MU CONOTOXIN KIIIB; POLYPEPTIDE; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ALPHA HELIX; ARTICLE; CHEMICAL BINDING; CLONING; DIRECT MASS SPECTROMETRY COLLISION INDUCED DISSOCIATION FRAGMENTATION; DNA ISOLATION; DNA SEQUENCE; ELECTROPHYSIOLOGY; ISOMER; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OOCYTE; OXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RAT; SEQUENCE HOMOLOGY; XENOPUS;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; CONOTOXINS; DISULFIDES; ION CHANNEL GATING; ISOMERISM; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; SODIUM CHANNELS;

GASTROPODA;

EID: 84870872020     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301256s     Document Type: Article

References (53)

1. Khoo, K. K. and Norton, R. S. (2012) Role of disulfide bonds in peptide and protein conformation. In Amino Acids, Peptides and Proteins in Organic Chemistry (Hughes, A. B., Ed.) pp 395-417, Wiley-VCH, Weinheim, Germany.
2. Trivedi, M. V., Laurence, J. S., and Siahaan, T. J. (2009) The role of thiols and disulfides on protein stability Curr. Protein Pept. Sci. 10, 614-625
3. Gilbert, H. F. (1995) Thiol/disulfide exchange equilibria and disulfide bond stability Methods Enzymol. 251, 8-28
4. Holmgren, A. and Bjornstedt, M. (1995) Thioredoxin and thioredoxin reductase Methods Enzymol. 252, 199-208
5. Buczek, O., Green, B. R., and Bulaj, G. (2007) Albumin is a redox-active crowding agent that promotes oxidative folding of cysteine-rich peptides Biopolymers 88, 8-19
6. Armishaw, C. J., Daly, N. L., Nevin, S. T., Adams, D. J., Craik, D. J., and Alewood, P. F. (2006) α-Selenoconotoxins, a new class of potent α7 neuronal nicotinic receptor antagonists J. Biol. Chem. 281, 14136-14143
7. Walewska, A., Zhang, M. M., Skalicky, J. J., Yoshikami, D., Olivera, B. M., and Bulaj, G. (2009) Integrated oxidative folding of cysteine/selenocysteine containing peptides: Improving chemical synthesis of conotoxins Angew. Chem., Int. Ed. 48, 2221-2224
8. Paul, M. and Donk, W. A. v. d. (2005) Chemical and enzymatic synthesis of lanthionines Mini-Rev. Org. Chem. 2, 23-37
9. Knerr, P. J., Tzekou, A., Ricklin, D., Qu, H., Chen, H., van der Donk, W. A., and Lambris, J. D. (2011) Synthesis and activity of thioether-containing analogues of the complement inhibitor compstatin ACS Chem. Biol. 6, 753-760
10. Muttenthaler, M., Andersson, A., de Araujo, A. D., Dekan, Z., Lewis, R. J., and Alewood, P. F. (2010) Modulating oxytocin activity and plasma stability by disulfide bond engineering J. Med. Chem. 53, 8585-8596
11. Platt, R. J., Han, T. S., Green, B. R., Smith, M. D., Skalicky, J., Gruszczynski, P., White, H. S., Olivera, B., Bulaj, G., and Gajewiak, J. (2012) Stapling mimics noncovalent interactions of γ-carboxyglutamates in conantokins, Peptidic antagonists of N-methyl- d -aspartic acid receptors J. Biol. Chem. 287, 20727-20736
12. MacRaild, C. A., Illesinghe, J., van Lierop, B. J., Townsend, A. L., Chebib, M., Livett, B. G., Robinson, A. J., and Norton, R. S. (2009) Structure and activity of (2,8)-dicarba-(3,12)-cystino α-ImI, an α-conotoxin containing a nonreducible cystine analogue J. Med. Chem. 52, 755-762
13. Robinson, A. J., van Lierop, B. J., Garland, R. D., Teoh, E., Elaridi, J., Illesinghe, J. P., and Jackson, W. R. (2009) Regioselective formation of interlocked dicarba bridges in naturally occurring cyclic peptide toxins using olefin metathesis Chem. Commun. 4293-4295
14. Gray, W. R. (1993) Disulfide structures of highly bridged peptides: A new strategy for analysis Protein Sci. 2, 1732-1748
15. Gupta, K., Kumar, M., and Balaram, P. (2010) Disulfide bond assignments by mass spectrometry of native natural peptides: Cysteine pairing in disulfide bonded conotoxins Anal. Chem. 82, 8313-8319
16. Ye, M., Khoo, K. K., Xu, S., Zhou, M., Boonyalai, N., Perugini, M. A., Shao, X., Chi, C., Galea, C. A., Wang, C., and Norton, R. S. (2012) A helical conotoxin from Conus imperiali s has a novel cysteine framework and defines a new superfamily J. Biol. Chem. 287, 14973-14983
17. Poppe, L., Hui, J. O., Ligutti, J., Murray, J. K., and Schnier, P. D. (2012) PADLOC: A powerful tool to assign disulfide bond connectivities in peptides and proteins by NMR spectroscopy Anal. Chem. 84, 262-266
18. Jordan, J. B., Poppe, L., Haniu, M., Arvedson, T., Syed, R., Li, V., Kohno, H., Kim, H., Schnier, P. D., Harvey, T. S., Miranda, L. P., Cheetham, J., and Sasu, B. J. (2009) Hepcidin revisited, disulfide connectivity, dynamics, and structure J. Biol. Chem. 284, 24155-24167
19. Lauth, X., Babon, J. J., Stannard, J. A., Singh, S., Nizet, V., Carlberg, J. M., Ostland, V. E., Pennington, M. W., Norton, R. S., and Westerman, M. E. (2005) Bass hepcidin synthesis, solution structure, antimicrobial activities and synergism, and in vivo hepatic response to bacterial infections J. Biol. Chem. 280, 9272-9282
20. Mobli, M. and King, G. F. (2010) NMR methods for determining disulfide-bond connectivities Toxicon 56, 849-854
21. Walewska, A., Skalicky, J. J., Davis, D. R., Zhang, M. M., Lopez-Vera, E., Watkins, M., Han, T. S., Yoshikami, D., Olivera, B. M., and Bulaj, G. (2008) NMR-based mapping of disulfide bridges in cysteine-rich peptides: Application to the μ-conotoxin SxIIIA J. Am. Chem. Soc. 130, 14280-14286
22. Khoo, K. K., Feng, Z. P., Smith, B. J., Zhang, M. M., Yoshikami, D., Olivera, B. M., Bulaj, G., and Norton, R. S. (2009) Structure of the analgesic μ-conotoxin KIIIA and effects on the structure and function of disulfide deletion Biochemistry 48, 1210-1219
23. Hill, J. M., Alewood, P. F., and Craik, D. J. (1996) Three-dimensional solution structure of μ-conotoxin GIIIB, a specific blocker of skeletal muscle sodium channels Biochemistry 35, 8824-8835
24. Keizer, D. W., West, P. J., Lee, E. F., Yoshikami, D., Olivera, B. M., Bulaj, G., and Norton, R. S. (2003) Structural basis for tetrodotoxin-resistant sodium channel binding by μ-conotoxin SmIIIA J. Biol. Chem. 278, 46805-46813
25. Lancelin, J. M., Kohda, D., Tate, S., Yanagawa, Y., Abe, T., Satake, M., and Inagaki, F. (1991) Tertiary structure of conotoxin GIIIA in aqueous solution Biochemistry 30, 6908-6916
26. Shon, K. J., Olivera, B. M., Watkins, M., Jacobsen, R. B., Gray, W. R., Floresca, C. Z., Cruz, L. J., Hillyard, D. R., Brink, A., Terlau, H., and Yoshikami, D. (1998) μ-Conotoxin PIIIA, a new peptide for discriminating among tetrodotoxin-sensitive Na channel subtypes J. Neurosci. 18, 4473-4481
27. Yao, S., Zhang, M. M., Yoshikami, D., Azam, L., Olivera, B. M., Bulaj, G., and Norton, R. S. (2008) Structure, dynamics, and selectivity of the sodium channel blocker μ-conotoxin SIIIA Biochemistry 47, 10940-10949
28. Han, T. S., Zhang, M. M., Walewska, A., Gruszczynski, P., Robertson, C. R., Cheatham, T. E., III, Yoshikami, D., Olivera, B. M., and Bulaj, G. (2009) Structurally minimized μ-conotoxin analogues as sodium channel blockers: Implications for designing conopeptide-based therapeutics ChemMedChem 4, 406-414
29. Stevens, M., Peigneur, S., Dyubankova, N., Lescrinier, E., Herdewijn, P., and Tytgat, J. (2012) Design of bioactive peptides from naturally occurring μ-conotoxin structures J. Biol. Chem. 287, 31382-31392
30. Bhattacharyya, M., Gupta, K., Gowd, K. H., and Balaram, P. (2012) Rapid mass spectrometric determination of disulfide folds in peptides and proteins: A robust solution for a long standing problem in protein chemistry Mol. Biosyst. submitted
31. Bulaj, G., West, P. J., Garrett, J. E., Watkins, M., Zhang, M. M., Norton, R. S., Smith, B. J., Yoshikami, D., and Olivera, B. M. (2005) Novel conotoxins from Conus striatus and Conus kinoshitai selectively block TTX-resistant sodium channels Biochemistry 44, 7259-7265
32. Biggs, J. S., Watkins, M., Puillandre, N., Ownby, J. P., Lopez-Vera, E., Christensen, S., Moreno, K. J., Bernaldez, J., Licea-Navarro, A., Corneli, P. S., and Olivera, B. M. (2010) Evolution of Conus peptide toxins: Analysis of Conus californicus Reeve, 1844 Mol. Phylogenet. Evol. 56, 1-12
33. Bartels, C., Xia, T. H., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer-supported NMR spectral-analysis of biological macromolecules J. Biomol. NMR 6, 1-10
34. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., and Clore, G. M. (2003) The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160, 65-73
35. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8, 477-486
36. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 51-55, 29-32
37. Zhang, M. M., Green, B. R., Catlin, P., Fiedler, B., Azam, L., Chadwick, A., Terlau, H., McArthur, J. R., French, R. J., Gulyas, J., Rivier, J. E., Smith, B. J., Norton, R. S., Olivera, B. M., Yoshikami, D., and Bulaj, G. (2007) Structure/function characterization of μ-conotoxin KIIIA, an analgesic, nearly irreversible blocker of mammalian neuronal sodium channels J. Biol. Chem. 282, 30699-30706
38. West, P. J., Bulaj, G., Garrett, J. E., Olivera, B. M., and Yoshikami, D. (2002) μ-Conotoxin SmIIIA, a potent inhibitor of tetrodotoxin-resistant sodium channels in amphibian sympathetic and sensory neurons Biochemistry 41, 15388-15393
39. V1.1 through 1.8 identify those responsible for action potentials in sciatic nerve Proc. Natl. Acad. Sci. U.S.A. 108, 10302-10307
40. Norton, R. S. (2010) μ-Conotoxins as leads in the development of new analgesics Molecules 15, 2825-2844
41. Corpuz, G. P., Jacobsen, R. B., Jimenez, E. C., Watkins, M., Walker, C., Colledge, C., Garrett, J. E., McDougal, O., Li, W., Gray, W. R., Hillyard, D. R., Rivier, J., McIntosh, J. M., Cruz, L. J., and Olivera, B. M. (2005) Definition of the M-conotoxin superfamily: Characterization of novel peptides from molluscivorous Conus venoms Biochemistry 44, 8176-8186
42. Jacob, R. B. and McDougal, O. M. (2010) The M-superfamily of conotoxins: A review Cell. Mol. Life Sci. 67, 17-27
43. Yanagawa, Y., Abe, T., Satake, M., Odani, S., Suzuki, J., and Ishikawa, K. (1988) A novel sodium channel inhibitor from Conus geographus: Purification, structure, and pharmacological properties Biochemistry 27, 6256-6262
44. Cruz, L. J., Kupryszewski, G., LeCheminant, G. W., Gray, W. R., Olivera, B. M., and Rivier, J. (1989) μ-Conotoxin GIIIA, a peptide ligand for muscle sodium channels: Chemical synthesis, radiolabeling, and receptor characterization Biochemistry 28, 3437-3442
45. Hidaka, Y., Sato, K., Nakamura, H., Kobayashi, J., Ohizumi, Y., and Shimonishi, Y. (1990) Disulfide pairings in geographutoxin I, a peptide neurotoxin from Conus geographus FEBS Lett. 264, 29-32
46. V1.2/1.4 channels and blocks neuronal nicotinic acetylcholine receptors Br. J. Pharmacol. 166, 1654-1668
47. V1.4 Angew. Chem., Int. Ed. 51, 4058-4061
48. Bulaj, G. and Olivera, B. M. (2008) Folding of conotoxins: Formation of the native disulfide bridges during chemical synthesis and biosynthesis of Conus peptides Antioxid. Redox Signaling 10, 141-155
49. Safavi-Hemami, H., Gorasia, D. G., Steiner, A. M., Williamson, N. A., Karas, J. A., Gajewiak, J., Olivera, B. M., Bulaj, G., and Purcell, A. W. (2012) Modulation of conotoxin structure and function is achieved through a multienzyme complex in the venom glands of cone snails J. Biol. Chem. 287, 34288-34303
50. Dutton, J. L., Bansal, P. S., Hogg, R. C., Adams, D. J., Alewood, P. F., and Craik, D. J. (2002) A new level of conotoxin diversity, a non-native disulfide bond connectivity in α-conotoxin AuIB reduces structural definition but increases biological activity J. Biol. Chem. 277, 48849-48857
51. Gehrmann, J., Alewood, P. F., and Craik, D. J. (1998) Structure determination of the three disulfide bond isomers of α-conotoxin GI: A model for the role of disulfide bonds in structural stability J. Mol. Biol. 278, 401-415
52. Khoo, K. K., Wilson, M. J., Smith, B. J., Zhang, M. M., Gulyas, J., Yoshikami, D., Rivier, J. E., Bulaj, G., and Norton, R. S. (2011) Lactam-stabilized helical analogues of the analgesic μ-conotoxin KIIIA J. Med. Chem. 54, 7558-7566
53. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.