Protein folding determinants: Structural features determining alternative disulfide pairing in α- and χ/λ-conotoxins

Biochemistry

Volumn 46, Issue 11, 2007, Pages 3338-3355

  Kang, Tse Siang ^a   Radić, Zoran ^b   Talley, Todd T ^b   Jois, Seetharama D S ^a,d   Taylor, Palmer ^b   Kini, R Manjunatha ^a,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF LOUISIANA AT MONROE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE DISULFIDE PAIRING; CONOTOXINS; GLOBULAR CONFORMATION; RIBBON CONFORMATION;

BINDING ENERGY; BIOCHEMISTRY; CONFORMATIONS; SUBSTITUTION REACTIONS; TOXIC MATERIALS;

PROTEIN FOLDING;

ACETYLCHOLINE; ALPHA CONOTOXIN; BINDING PROTEIN; CONOTOXIN; DISULFIDE; LAMBDA CONOTOXIN; LYSINE; PROLINE; UNCLASSIFIED DRUG; VENOM;

AMIDATION; AMINO ACID SUBSTITUTION; APLYSIA; ARTICLE; BINDING AFFINITY; BULINUS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONUS SNAIL; DEAMINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN STRUCTURE; STEREOSPECIFICITY;

AMINO ACID SEQUENCE; CONOTOXINS; DISULFIDES; ELECTROSTATICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; SEQUENCE ALIGNMENT;

APLYSIA; BULINUS;

EID: 33947424873     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061969o     Document Type: Article

References (58)

1. McIntosh, J. M., Santos, A. D., and Olivera, B. M. (1999) Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes, Annu. Rev. Biochem. 68, 59-88.
2. Arias, H. R. and Blanton, M. P. (2000) Alpha-conotoxins, Int. J. Biochem. Cell Biol. 32, 1017-1028.
3. Terlau, H., and Olivera, B. M. (2004) Conus venoms: a rich source of novel ion channel-targeted peptides, Physiol Rev. 84, 41-68.
4. Gehrmann, J., Alewood, P. F., and Craik, D. J. (1998) Structure determination of the three disulfide bond isomers of alpha-conotoxin GI: A model for the role of disulfide bonds in structural stability, J. Mol. Biol. 278, 401-415.
5. Zhang, R. M., and Snyder, G. H. (1991) Factors governing selective formation of specific disulfides in synthetic variants of alpha-conotoxin, Biochemistry, 30, 11343-11348.
6. Carlier, E., Fajloun, Z., Mansuelle, P., Fathallah, M., Mosbah, A., Oughideni, R., Sandoz, G., Di Luccio, E., Geib, S., Regaya, I., Brocard, J., Rochat, H., Darbon, H., Devaux, C., Sabatier, J. M., and de Waard, M. (2001) Disulfide bridge reorganization induced by proline mutations in maurotoxin, FEBS Lett. 489, 202-207.
7. Kini, R. M., and Evans, H. J. (1995) A novel approach to the design of potent bioactive peptides by incorporation of proline brackets: Antiplatelet effects of Arg-Gly-Asp peptides, FEBS Lett. 375, 15-17.
8. Luo, S., Kulak, J. M., Cartier, G. E., Jacobsen, R. B., Yoshikami, D., Olivera, B. M., and McIntosh, J. M. (1998) Alpha-conotoxin AuIB selectively blocks alpha3 beta4 nicotinic acetylcholine receptors and nicotine-evoked norepinephrine release, J. Neurosci. 18, 8571-8579.
9. Balaji, R. A., Ohtake, A., Sato, K., Gopalakrishnakone, P., Kini, R. M., Seow, K. T., and Bay, B. H. (2000) Lambda-conotoxins, a new family of conotoxins with unique disulfide pattern and protein folding. Isolation and characterization from the venom of Conus marmoreus, J. Biol. Chem. 275, 39516-39522.
10. McIntosh, J. M., Corpuz, G. O., Layer, R. T., Garrett, J. E., Wagstaff, J. D., Bulaj, G., Vyazovkina, A., Yoshikami, D., Cruz, L. J., and Olivera, B. M. (2000) Isolation and characterization of a novel conus peptide with apparent antinociceptive activity, J. Biol. Chem. 275, 32391-32397.
11. Sharpe, I. A., Gehrmann, J., Loughnan, M. L., Thomas, L., Adams, D. A., Atkins, A., Palant, E., Craik, D. J., Adams, D. J., Alewood, P. F., and Lewis, R. J. (2001) Two new classes of conopeptides inhibit the alpha1-adrenoceptor and noradrenaline transporter, Nat. Neurosci. 4, 902-907.
12. Kang, T. S., Vivekanandan, S., Jois, S. D., and Kini, R. M. (2005) Effect of C-terminal amidation on folding and disulfide-pairing of alpha-conotoxin ImI, Angew. Chem. Int. Ed Engl. 44, 6333-6337.
13. Hansen, S. B., Sulzenbacher, G., Huxford, T., Marchot, P., Taylor, P., and Bourne, Y. (2005) Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations, EMBO J. 24, 3635-3646.
14. Celie, P. H., Kasheverov, I. E., Mordvintsev, D. Y., Hogg, R. C., van Nierop, P., van Elk, R., Rossum-Fikkert, S. E., Zhmak, M. N., Bertrand, D., Tsetlin, V., Sixma, T. K., and Smit, A. B. (2005) Crystal structure of nicotinic acetylcholine receptor homolog AChBP in complex with an alpha-conotoxin PnIA variant, Nat. Struct. Mol. Biol. 12, 582-588.
15. Bax, A. D., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
16. Bax, A. D., and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy, J. Magn. Reson. 63, 207-213.
17. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-665.
18. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids; Wiley: New York.
19. Nicke, A., Loughnan, M. L., Millard, E. L., Alewood, P. F., Adams, D. J., Daly, N. L., Craik, D. J., and Lewis, R. J. (2003) Isolation, structure, and activity of GID, a novel alpha 4/7-conotoxin with an extended N-terminal sequence, J. Biol. Chem. 278, 3137-3144.
20. Broxton, N. M., Down, J. G., Gehrmann, J., Alewood, P. F., Satchell, D. G., and Livett, B. G. (1999) Alpha-conotoxin ImI inhibits the alpha-bungarotoxin-resistant nicotinic response in bovine adrenal chromaffin cells, J. Neurochem. 72, 1656-1662.
21. Ellison, M., McIntosh, J. M., and Olivera, B. M. (2003) Alpha-conotoxins ImI and ImII. Similar alpha 7 nicotinic receptor antagonists act at different sites, J. Biol. Chem. 278, 757-764.
22. Gehrmann, J., Daly, N. L., Alewood, P. F., and Craik, D. J. (1999) Solution structure of alpha-conotoxin ImI by 1H nuclear magnetic resonance, J. Med. Chem. 42, 2364-2372.
23. Gouda, H., and Hirono, S. (1999) Solution structure of alpha-conotoxin ImI determined by two-dimensional NMR spectroscopy Biochim. Biophys. Acta 1431, 384-394.
24. Johnson, D. S., Martinez, J., Elgoyhen, A. B., Heinemann, S. F., and McIntosh, J. M. (1995) Alpha-Conotoxin ImI exhibits subtype-specific nicotinic acetylcholine receptor blockade: preferential inhibition of homomeric alpha 7 and alpha 9 receptors, Mol. Pharmacol. 48, 194-199.
25. Lamthanh, H., Jegou-Matheron, C., Servent, D., Menez, A., and Lancelin, J. M. (1999) Minimal conformation of the alpha-conotoxin ImI for the alpha7 neuronal nicotinic acetylcholine receptor recognition: correlated CD, NMR and binding studies, FEBS Lett. 454, 293-298.
26. Maslennikov, I. V., Shenkarev, Z. O., Zhmak, M. N., Ivanov, V. T., Methfessel, C., Tsetlin, V. I., and Arseniev, A. S. (1999) NMR spatial structure of alpha-conotoxin ImI reveals a common scaffold in snail and snake toxins recognizing neuronal nicotinic acetyl-choline receptors, FEBS Lett. 444, 275-280.
27. McIntosh, J. M., Yoshikami, D., Mahe, E., Nielsen, D. B., Rivier, J. E., Gray, W. R., and Olivera, B. M. (1994) A nicotinic acetylcholine receptor ligand of unique specificity, alpha-conotoxin ImI, J. Biol. Chem. 269, 16733-16739.
28. Nielsen, J. S., Buczek, P., and Bulaj, G. (2004) Cosolvent-assisted oxidative folding of a bicyclic alpha-conotoxin ImI, J. Pept. Sci. 10, 249-256.
29. Quiram, P. A., and Sine, S. M. (1998) Structural elements in alpha-conotoxin ImI essential for binding to neuronal alpha7 receptors, J. Biol. Chem. 273, 11007-11011.
30. Quiram, P. A., and Sine, S. M. (1998) Identification of residues in the neuronal alpha7 acetylcholine receptor that confer selectivity for conotoxin ImI, J. Biol. Chem. 273, 11001-11006.
31. Quiram, P. A., Jones, J. J., and Sine, S. M. (1999) Pairwise interactions between neuronal alpha7 acetylcholine receptors and alpha-conotoxin ImI, J. Biol. Chem. 274, 19517-19524.
32. Rogers, J. P., Luginbuhl, P., Shen, G. S., McCabe, R. T., Stevens, R. C., and Wemmer, D. E. (1999) NMR solution structure of alpha-conotoxin ImI and comparison to other conotoxins specific for neuronal nicotinic acetylcholine receptors, Biochemistry 38, 3874-3882.
33. Utkin, Y. N., Zhmak, M. N., Methfessel, C., and Tsetlin, V. I. (1999) Aromatic substitutions in alpha-conotoxin ImI. Synthesis of iodinated photoactivatable derivative, Toxicon 37, 1683-1695.
34. Bellizzi, J. J., III, Widom, J., Kemp, C., Lu, J. Y., Das, A. K., Hofmann, S. L., and Clardy, J. (2000) The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis, Proc. Natl. Acad. Sci. U.S.A. 97, 4573-4578.
35. Brejc, K., van Dijk, W. J., Klaassen, R. V., Schuurmans, M., van Der, O. J., Smit, A. B., and Sixma, T. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors, Nature 411, 269-276.
36. Carugo, O., Cemazar, M., Zahariev, S., Hudaky, I., Gaspari, Z., Perczel, A., and Pongor, S. (2003) Vicinal disulfide turns, Protein Eng. 16, 637-639.
37. Ghosh, M., Anthony, C., Harlos, K., Goodwin, M. G., and Blake, C. (1995) The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 Å, Structure 3, 177-187.
38. Hunter, H. N., Fulton, D. B., Ganz, T., and Vogel, H. J. (2002) The solution structure of human hepcidin, a peptide hormone with antimicrobial activity that is involved in iron uptake and hereditary hemochromatosis, J. Biol. Chem. 277, 37597-37603.
39. Keitel, T., Diehl, A., Knaute, T., Stezowski, J. J., Hohne, W., and Gorisch, H. (2000) X-ray structure of the quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosai basis of substrate specificity, J. Mol. Biol. 297, 961-974.
40. Teplyakov, A., Polyakov, K., Obmolova, G., Strokopytov, B., Kuranova, I., Osterman, A., Grishin, N., Smulevitch, S., Zagnitko, O., and Galperina, O. (1992) Crystal structure of carboxypeptidase T from Thermoactinomyces vulgaris, Eur. J. Biochem. 208, 281-288.
41. Wang, X., Connor, M., Smith, R., Maciejewski, M. W., Howden, M. E., Nicholson, G. M., Christie, M. J., and King, G. F. (2000) Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge, Nat. Struct. Biol. 7, 505-513.
42. Yoon, H. J., Hashimoto, W., Miyake, O., Murata, K., and Mikami, B. (2001) Crystal structure of alginate lyase A1-III complexed with trisaccharide product at 2.0 Å resolution, J. Mol. Biol. 307, 9-16.
43. Zeng, H., Moise, L., Grant, M. A., and Hawrot, E. (2001) The solution structure of the complex formed between alpha-bungarotoxin and an 18-mer cognate peptide derived from the alpha 1 subunit of the nicotinic acetylcholine receptor from Torpedo californica, J. Biol. Chem. 276, 22930-22940.
44. Wishart, D. S., Sykes, B., D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy, Biochemistry 31, 1647-1651.
45. Kang, T. S., Jois, S. D., and Kini, R. M. (2006) Solution structures of two structural isoforms of CMrVIA chi/lambda-conotoxin, Biomacromolecules 7, 2337-2346.
46. Buczek, O., Olivera, B. M., and Bulaj, G. (2004) Propeptide does not act as an intramolecular chaperone but facilitates protein disulfide isomerase-assisted folding of a conotoxin precursor, Biochemistry 43, 1093-1101.
47. Loughnan, M. L., Nicke, A., Jones, A., Adams, D. J., Alewood, P. F., and Lewis, R. J. (2004) Chemical and functional identification and characterization of novel sulfated alpha-conotoxins from the cone snail Conus anemone, J. Med. Chem. 47, 1234-1241.
48. Hansen, S. B., Talley, T. T., Radic, Z., and Taylor, P. (2004) Structural and ligand recognition characteristics of an acetylcholine-binding protein from Aplysia californica, J. Biol. Chem. 279, 24197-24202.
49. Loughnan, M., Bond, T., Atkins, A., Cuevas, J., Adams, D. J., Broxton, N. M., Livett, B. G., Down, J. G., Jones, A., Alewood, P. F., and Lewis, R. J. (1998) Alpha-conotoxin EpI, a novel sulfated peptide from Conus episcopatus that selectively targets neuronal nicotinic acetylcholine receptors, J. Biol. Chem. 273, 15667-15674.
50. Fainzilber, M., Hasson, A., Oren, R., Burlingame, A. L., Gordon, D., Spira, M. E., and Zlotkin, E. (1994) New mollusc-specific alpha-conotoxins block Aplysia neuronal acetylcholine receptors, Biochemistry 33, 9523-9529.
51. Cartier, G. E., Yoshikami, D., Gray, W. R., Luo, S., Olivera, B. M., and McIntosh, J. M. (1996) A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors, J. Biol. Chem. 271, 7522-7528.
52. Martinez, J. S., Olivera, B. M., Gray, W. R., Craig, A. G., Groebe, D. R., Abramson, S. N., and McIntosh, J. M. (1995) Alpha-conotoxin EI, a new nicotinic acetylcholine receptor antagonist with novel selectivity, Biochemistry 34, 14519-14526.
53. McIntosh, J. M., Dowell, C., Watkins, M., Garrett, J. E., Yoshikami, D., and Olivera, B. M. (2002) Alpha-conotoxin GIC from Conus geographus, a novel peptide antagonist of nicotinic acetylcholine receptors, J. Biol. Chem. 277, 33610-33615.
54. Sandall, D. W., Satkunanathan, N., Keays, D. A., Polidano, M. A., Liping, X., Pham, V., Down, J. G., Khalil, Z., Livett, B. G., and Gayler, K. R. (2003) A novel alpha-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo, Biochemistry 42, 6904-6911.
55. Azam, L., Dowell, C., Watkins, M., Stitzel, J. A., Olivera, B. M., and McIntosh, J. M. (2005) Alpha-conotoxin BuIA, & novel peptide from Conus bullatus, distinguishes among neuronal nicotinic acetylcholine receptors, J. Biol. Chem. 280, 80-87.
56. Chi, S. W., Kim, D. H., Olivera, B. M., McIntosh, J. M., and Han, K. H. (2006) Solution conformation of a neuronal nicotinic acetylcholine receptor antagonist alpha-conotoxin OmIA that discriminates alpha3 vs. alpha6 nAChR subtypes, Biochem. Biophys. Res. Commun. 345, 248-254.
57. Gray, W. R., Luque, A., Olivera, B. M., Barrett, J., and Cruz, L. J. (1981) Peptide toins from Conus geographus venom, J. Biol. Chem. 256, 4734-4740.
58. Zafaralla, G. C., Ramilo, C., Gray, W. R., Karlstrom, R., Olivera, B. M., and Cruz, L. J. (1988) Phylogenetic specificity of cholinergic ligands: alpha-conotoxin SI, Biochemistry 27, 7102-7105.