Mammalian neuronal sodium channel blocker μ-conotoxin BuIIIB has a structured N-terminus that influences potency

ACS Chemical Biology

Volumn 8, Issue 6, 2013, Pages 1344-1351

  Kuang, Zhihe ^a,f   Zhang, Min Min ^b   Gupta, Kallol ^c   Gajewiak, Joanna ^b   Gulyas, Jozsef ^d   Balaram, Padmanabhan ^c   Rivier, Jean E ^d   Olivera, Baldomero M ^b   Yoshikami, Doju ^b   Bulaj, Grzegorz ^b   Norton, Raymond S ^e  

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

^b UNIVERSITY OF UTAH   (United States)

^c INDIAN INSTITUTE OF SCIENCE   (India)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e MONASH UNIVERSITY   (Australia)

^f JINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; MU BUIIIA; MU BUIIIB; SODIUM CHANNEL BLOCKING AGENT; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; DISULFIDE BOND; DRUG POTENCY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CONOTOXINS; DISULFIDES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NAV1.3 VOLTAGE-GATED SODIUM CHANNEL; SODIUM CHANNEL BLOCKERS; XENOPUS;

MAMMALIA; MUS; VERTEBRATA;

EID: 84879756585     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300674x     Document Type: Article

References (40)

1. Terlau, H. and Olivera, B. M. (2004) Conus venoms: a rich source of novel ion channel-targeted peptides Physiol. Rev. 84, 41-68
2. Norton, R. S. and Olivera, B. M. (2006) Conotoxins down under Toxicon 48, 780-798
3. Han, T. S., Teichert, R. W., Olivera, B. M., and Bulaj, G. (2008) Conus venoms-a rich source of peptide-based therapeutics Curr. Pharm. Des 14, 2462-2479
4. French, R. J. and Terlau, H. (2004) Sodium channel toxins-receptor targeting and therapeutic potential Curr Med Chem 11, 3053-3064
5. French, R. J., Yoshikami, D., Sheets, M. F., and Olivera, B. M. (2010) The tetrodotoxin receptor of voltage-gated sodium channels-perspectives from interactions with μ-conotoxins Mar. Drugs 8, 2153-2161
6. Cummins, T. R., Sheets, P. L., and Waxman, S. G. (2007) The roles of sodium channels in nociception: Implications for mechanisms of pain Pain 131, 243-257
7. Dib-Hajj, S. D., Cummins, T. R., Black, J. A., and Waxman, S. G. (2010) Sodium channels in normal and pathological pain Annu. Rev. Neurosci. 33, 325-347
8. Norton, R. S. (2010) μ-Conotoxins as leads in the development of new analgesics Molecules 15, 2825-2844
9. Cruz, L. J., Gray, W. R., Olivera, B. M., Zeikus, R. D., Kerr, L., Yoshikami, D., and Moczydlowski, E. (1985) Conus geographus toxins that discriminate between neuronal and muscle sodium channels J. Biol. Chem. 260, 9280-9288
10. + channels J. Biol. Chem. 278, 8717-8724
11. 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
12. Nielsen, K. J., Watson, M., Adams, D. J., Hammarstrom, A. K., Gage, P. W., Hill, J. M., Craik, D. J., Thomas, L., Adams, D., Alewood, P. F., and Lewis, R. J. (2002) Solution structure of μ-conotoxin PIIIA, a preferential inhibitor of persistent tetrodotoxin-sensitive sodium channels J. Biol. Chem. 277, 27247-27255
13. Safo, P., Rosenbaum, T., Shcherbatko, A., Choi, D. Y., Han, E., Toledo-Aral, J. J., Olivera, B. M., Brehm, P., and Mandel, G. (2000) Distinction among neuronal subtypes of voltage-activated sodium channels by μ-conotoxin PIIIA J. Neurosci. 20, 76-80
14. 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
15. 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
16. 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
17. 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
18. Lewis, R. J., Schroeder, C. I., Ekberg, J., Nielsen, K. J., Loughnan, M., Thomas, L., Adams, D. A., Drinkwater, R., Adams, D. J., and Alewood, P. F. (2007) Isolation and structure-activity of μ-conotoxin TIIIA, a potent inhibitor of tetrodotoxin-sensitive voltage-gated sodium channels Mol. Pharmacol. 71, 676-685
19. 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
20. V1.1 through 1.8 identify those responsible for action potentials in sciatic nerve Proc. Natl. Acad. Sci. U.S.A. 108, 10302-10307
21. Green, B. R., Catlin, P., Zhang, M. M., Fiedler, B., Bayudan, W., Morrison, A., Norton, R. S., Smith, B. J., Yoshikami, D., Olivera, B. M., and Bulaj, G. (2007) Conotoxins containing nonnatural backbone spacers: cladistic-based design, chemical synthesis, and improved analgesic activity Chem. Biol. 14, 399-407
22. McArthur, J. R., Singh, G., McMaster, D., Winkfein, R., Tieleman, D. P., and French, R. J. (2011) Interactions of key charged residues contributing to selective block of neuronal sodium channels by μ-conotoxin KIIIA Mol. Pharmacol. 80, 573-584
23. Holford, M., Zhang, M. M., Gowd, K. H., Azam, L., Green, B. R., Watkins, M., Ownby, J. P., Yoshikami, D., Bulaj, G., and Olivera, B. M. (2009) Pruning nature: Biodiversity-derived discovery of novel sodium channel blocking conotoxins from Conus bullatus Toxicon 53, 90-98
24. Catterall, W. A., Goldin, A. L., and Waxman, S. G. (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels Pharmacol. Rev. 57, 397-409
25. 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
26. Bhattacharyya, M., Gupta, K., Gowd, K. H., and Balaram, P. (2013) Rapid mass spectrometric determination disulfide connectivity in peptides and proteins Mol. Biosyst. 10.1039/C1033MB25534D
27. Ulrich, E. L., Akutsu, H., Doreleijers, J. F., Harano, Y., Ioannidis, Y. E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z., Nakatani, E., Schulte, C. F., Tolmie, D. E., Kent Wenger, R., Yao, H., and Markley, J. L. (2008) BioMagResBank Nucleic Acids Res. 36, D402-408
28. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank Nucleic Acids Res. 28, 235-242
29. Zhang, M. M., McArthur, J. R., Azam, L., Bulaj, G., Olivera, B. M., French, R. J., and Yoshikami, D. (2009) Synergistic and antagonistic interactions between tetrodotoxin and μ-conotoxin in blocking voltage-gated sodium channels Channels 3, 32-38
30. Zhang, M. M., Han, T. S., Olivera, B. M., Bulaj, G., and Yoshikami, D. (2010) μ-conotoxin KIIIA derivatives with divergent affinities versus efficacies in blocking voltage-gated sodium channels Biochemistry 49, 4804-4812
31. Zhang, M. M., Gruszczynski, P., Walewska, A., Bulaj, G., Olivera, B. M., and Yoshikami, D. (2010) Cooccupancy of the outer vestibule of voltage-gated sodium channels by μ-conotoxin KIIIA and saxitoxin or tetrodotoxin J. Neurophysiol. 104, 88-97
32. Markgraf, R., Leipold, E., Schirmeyer, J., Paolini-Bertrand, M., Hartley, O., and Heinemann, S. H. (2012) Mechanism and molecular basis for the sodium channel subtype specificity of μ-conopeptide CnIIIC Br. J. Pharmacol. 167, 576-586
33. Pallaghy, P. K., Duggan, B. M., Pennington, M. W., and Norton, R. S. (1993) Three-dimensional structure in solution of the calcium channel blocker ω-conotoxin J. Mol. Biol. 234, 405-420
34. Venkatachalam, C. M. (1968) Stereochemical criteria for polypeptides and proteins. V. Conformation of a system of three linked peptide units Biopolymers 6, 1425-1436
35. 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
36. V1.2/1.4 channels and blocks neuronal nicotinic acetylcholine receptors Br. J. Pharmacol. 166, 1654-1668
37. 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
38. Khoo, K. K., Gupta, K., Green, B. R., Zhang, M.-M., Watkins, M., Olivera, B. M., Balaram, P., Yoshikami, D., Bulaj, G., and Norton, R. S. (2012) Distinct disulfide isomers of μ-conotoxins KIIIA and KIIIB block voltage-gated sodium channels Biochemistry 51, 9826-9835
39. 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
40. 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