Disulfide-depleted selenoconopeptides: Simplified oxidative folding of cysteine-rich peptides

ACS Medicinal Chemistry Letters

Volumn 1, Issue 4, 2010, Pages 140-144

  Han, Tiffany S ^a   Zhang, Min Min ^a   Gowd, Konkallu Hanumae ^a   Walewska, Aleksandra ^a,b   Yoshikami, Doju ^a   Olivera, Baldomero M ^a   Bulaj, Grzegorz ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF GDA SK   (Poland)

Author keywords

Conotoxins; diselenide bridges; disulfide rich peptides; oxidative folding; selenocysteines

Indexed keywords

CYSTEINE; DISULFIDE; NEUROTOXIN; PEPTIDE DERIVATIVE; SELENOCONOPEPTIDE; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.4; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ARTICLE; DISULFIDE BOND; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN FOLDING;

EID: 77953251331     PISSN: None     EISSN: 19485875     Source Type: Journal    
DOI: 10.1021/ml900017q     Document Type: Article

References (45)

1. Tedford, H. W.; Sollod, B. L.; Maggio, F.; King, G. F. Australian funnel-web spiders: master insecticide chemists Toxicon 2004, 43, 601-18
2. Escoubas, P.; Sollod, B.; King, G. F. Venom landscapes: mining the complexity of spider venoms via a combined cDNA and mass spectrometric approach Toxicon 2006, 47, 650-63
3. Bulaj, G. Integrating the discovery pipeline for novel compounds targeting ion channels Curr. Opin. Chem. Biol. 2008, cr12, 441-7
4. Lewis, R. J.; Garcia, M. L. Therapeutic potential of venom peptides Nat. Rev. Drug Discovery 2003, 2, 790-802
5. Olivera, B. M.; Teichert, R. W. Diversity of the neurotoxic Conus peptides: a model for concerted pharmacological discovery Mol. Interventions 2007, 7, 251-60
6. Beeton, C. E.; Gutman, G. A.; Chandy, K. G. Targets and Therapeutic Properties of Venom Peptides. In Handbook of Biologically Active Peptides; Kastin, A. J., Ed.; Academic Press: New York, 2005; pp 403 ? 414.
7. Miljanich, G. P. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain Curr. Med. Chem. 2004, 11, 3029-40
8. Livett, B. G.; Gayler, K. R.; Khalil, Z. Drugs from the sea: conopeptides as potential therapeutics Curr. Med. Chem. 2004, 11, 1715-23
9. Han, T. S.; Teichert, R. W.; Olivera, B. M.; Bulaj, G. Conus Venoms'a Rich Source of Peptide-Based Therapeutics Curr. Pharm. Des. 2008, 14, 2462-2479
10. Escoubas, P.; King, G. F. Venomics as a drug discovery platform Expert Rev. Proteomics 2009, 6, 221-4
11. Olivera, B. M. Conus peptides: biodiversity-based discovery and exogenomics J. Biol. Chem. 2006, 281, 31173-7
12. Duda, T. F., Jr.; Palumbi, S. R. Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 6820-3
13. Jakubowski, J. A.; Keays, D. A.; Kelley, W. P.; Sandall, D. W.; Bingham, J. P.; Livett, B. G.; Gayler, K. R.; Sweedler, J. V. Determining sequences and post-translational modifications of novel conotoxins in Conus victoriae using cDNA sequencing and mass spectrometry J. Mass Spectrom. 2004, 39, 548-57
14. Gowd, K. H.; Dewan, K. K.; Iengar, P.; Krishnan, K. S.; Balaram, P. Probing peptide libraries from Conus achatinus using mass spectrometry and cDNA sequencing: identification of delta and omega-conotoxins J. Mass Spectrom. 2008, 43, 791-805
15. Miranda, L. P.; Alewood, P. F. Challenges for protein chemical synthesis in the 21st century: bridging genomics and proteomics Biopolymers 2000, 55, 217-26
16. Bulaj, G.; Walewska, A. Oxidative Folding of Single-stranded Disulfide-rich Peptides. In Oxidative Folding of Peptides and Proteins; Buchner, J.; Moroder, L., Eds.; Royal Society of Chemistry: Cambridge, 2009, pp 274 ? 296.
17. Darlak, K.; Wiegandt Long, D.; Czerwinski, A.; Darlak, M.; Valenzuela, F.; Spatola, A. F.; Barany, G. Facile preparation of disulfide-bridged peptides using the polymer-supported oxidant CLEAR-OX J. Pept. Res. 2004, 63, 303-12
18. Green, B. R.; Bulaj, G. Oxidative folding of conotoxins in immobilized systems Protein Pept. Lett. 2006, 13, 67-70
19. Zhang, J.; Diamond, S.; Arvedson, T.; Sasu, B. J.; Miranda, L. P. Oxidative folding of hepcidin at acidic pH Biopolymers 2010, 94, 257-64
20. Besse, D.; Moroder, L. Synthesis of selenocysteine peptides and their oxidation to diselenide-bridged compounds J. Pept. Sci. 1997, 3, 442-53
21. Moroder, L. Isosteric replacement of sulfur with other chalcogens in peptides and proteins J. Pept. Sci. 2005, 11, 187-214
22. Pegoraro, S.; Fiori, S.; Cramer, J.; Rudolph-Bohner, S.; Moroder, L. The disulfide-coupled folding pathway of apamin as derived from diselenide-quenched analogs and intermediates Protein Sci. 1999, 8, 1605-13
23. Armishaw, C. J.; Daly, N. L.; Nevin, S. T.; Adams, D. J.; Craik, D. J.; Alewood, P. F. Alpha-selenoconotoxins, a new class of potent ?7 neuronal nicotinic receptor antagonists J. Biol. Chem. 2006, 281, 14136-43
24. Muttenthaler, M.; Alewood, P. F. Selenopeptide chemistry J. Pept. Sci. 2008, 14, 1223-39
25. Walewska, A.; Zhang, M. M.; Skalicky, J. J.; Yoshikami, D.; Olivera, B. M.; Bulaj, G. Integrated oxidative folding of cysteine/selenocysteine containing peptides: improving chemical synthesis of conotoxins Angew. Chem., Int. Ed. Engl. 2009, 48, 2221-4
26. Muttenthaler, M.; Nevin, S. T.; Grishin, A. A.; Ngo, S. T.; Choy, P. T.; Daly, N. L.; Hu, S. H.; Armishaw, C. J.; Wang, C. I.; Lewis, R. J.; Martin, J. L.; Noakes, P. G.; Craik, D. J.; Adams, D. J.; Alewood, P. F. Solving the ?-conotoxin folding problem: efficient selenium-directed on-resin generation of more potent and stable nicotinic acetylcholine receptor antagonists J. Am. Chem. Soc. 2010, 132, 3514-22
27. Gowd, K. H.; Yarotskyy, V.; Elmslie, K. S.; Skalicky, J. J.; Olivera, B. M.; Bulaj, G. Site-Specific Effects of Diselenide Bridges on the Oxidative Folding of a Cystine Knot Peptide, ?-Selenoconotoxin GVIA Biochemistry 2010, 49, 2741-52
28. Pegoraro, S.; Fiori, S.; Rudolph-Bohner, S.; Watanabe, T. X.; Moroder, L. Isomorphous replacement of cystine with selenocystine in endothelin: oxidative refolding, biological and conformational properties of [Sec3,Sec11,Nle7]- endothelin-1 J. Mol. Biol. 1998, 284, 779-92
29. Zhu, Q.; Liang, S.; Martin, L.; Gasparini, S.; Menez, A.; Vita, C. Role of disulfide bonds in folding and activity of leiurotoxin I: just two disulfides suffice Biochemistry 2002, 41, 11488-94
30. Savarin, P.; Romi-Lebrun, R.; Zinn-Justin, S.; Lebrun, B.; Nakajima, T.; Gilquin, B.; Menez, A. Structural and functional consequences of the presence of a fourth disulfide bridge in the scorpion short toxins: solution structure of the potassium channel inhibitor HsTX1 Protein Sci. 1999, 8, 2672-85
31. Han, T. S.; Zhang, M. M.; Walewska, A.; Gruszczynski, P.; Robertson, C. R.; Cheatham, T. E., 3rd; Yoshikami, D.; Olivera, B. M.; Bulaj, G. Structurally Minimized μ-Conotoxin Analogues as Sodium Channel Blockers: Implications for Designing Conopeptide-Based Therapeutics ChemMedChem 2009, 4, 406-414
32. Price-Carter, M.; Hull, M. S.; Goldenberg, D. P. Roles of individual disulfide bonds in the stability and folding of an omega-conotoxin Biochemistry 1998, 37, 9851-61
33. Khoo, K. K.; Feng, Z. P.; Smith, B. J.; Zhang, M. M.; Yoshikami, D.; Olivera, B. M.; Bulaj, G.; Norton, R. S. Structure of the Analgesic μ-Conotoxin KIIIA and Effects on the Structure and Function of Disulfide Deletion Biochemistry 2009, 48, 2110-19
34. Dy, C. Y.; Buczek, P.; Imperial, J. S.; Bulaj, G.; Horvath, M. P. Structure of conkunitzin-S1, a neurotoxin and Kunitz-fold disulfide variant from cone snail Acta Crystallogr., Sect. D: Biol. Crystallogr. 2006, 62, 980-90
35. Bayrhuber, M.; Vijayan, V.; Ferber, M.; Graf, R.; Korukottu, J.; Imperial, J.; Garrett, J. E.; Olivera, B. M.; Terlau, H.; Zweckstetter, M.; Becker, S. Conkunitzin-S1 is the first member of a new Kunitz-type neurotoxin family. Structural and functional characterization J. Biol. Chem. 2005, 280, 23766-70
36. Olivera, B. M.; Bulaj, G.; Garrett, J. E.; Terlau, H.; Imperial, J. Peptide Toxins from the Venoms of Cone Snails and Other Toxoglossan gastropods. In Animal Toxins: State of the Art; De Lima, M. E., Ed.; Editora UFMG: Terreo, 2009; pp 25 ? 48.
37. Bulaj, G.; West, P. J.; Garrett, J. E.; Watkins, M.; Zhang, M. M.; Norton, R. S.; Smith, B. J.; Yoshikami, D.; Olivera, B. M. Novel conotoxins from Conus striatus and Conus kinoshitai selectively block TTX-resistant sodium channels Biochemistry 2005, 44, 7259-65
38. 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.; Bulaj, G. Structure/function characterization of μ-conotoxin KIIIA, an analgesic, nearly irreversible blocker of mammalian neuronal sodium channels J. Biol. Chem. 2007, 282, 30699-706
39. Schroll, A. L.; Hondal, R. J. Further development of new deprotection chemistry for cysteine and selenocysteine side chain protecting groups Adv. Exp. Med. Biol. 2009, 611, 135-6
40. Harris, K. M.; Flemer, S., Jr.; Hondal, R. J. Studies on deprotection of cysteine and selenocysteine side-chain protecting groups J. Pept. Sci. 2007, 13, 81-93
41. Fuller, E.; Green, B. R.; Catlin, P.; Buczek, O.; Nielsen, J. S.; Olivera, B. M.; Bulaj, G. Oxidative folding of conotoxins sharing an identical disulfide bridging framework FEBS J. 2005, 272, 1727-38
42. Bulaj, G. Formation of disulfide bonds in proteins and peptides Biotechnol. Adv. 2005, 23, 87-92
43. Walewska, A.; Skalicky, J. J.; Davis, D. R.; Zhang, M. M.; Lopez-Vera, E.; Watkins, M.; Han, T. S.; Yoshikami, D.; Olivera, B. M.; Bulaj, G. NMR-Based Mapping of Disulfide Bridges in Cysteine-Rich Peptides: Application to the μ-Conotoxin SxIIIA J. Am. Chem. Soc. 2008, 130, 14280-6
44. Mobli, M.; de Araujo, A. D.; Lambert, L. K.; Pierens, G. K.; Windley, M. J.; Nicholson, G. M.; Alewood, P. F.; King, G. F. Direct visualization of disulfide bonds through diselenide proxies using 77Se NMR spectroscopy Angew. Chem., Int. Ed. 2009, 48, 9312-4
45. Brust, A.; Tickle, A. E. High-throughput synthesis of conopeptides: a safety-catch linker approach enabling disulfide formation in 96-well format J. Pept. Sci. 2007, 13, 133-41