Role of hydroxyprolines in the in vitro oxidative folding and biological activity of conotoxins

Biochemistry

Volumn 47, Issue 6, 2008, Pages 1741-1751

  Lopez Vera, Estuardo ^a,d   Walewska, Aleksandra ^a,c   Skalicky, Jack J ^b   Olivera, Baldomero M ^a   Bulaj, Grzegorz ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GDA SK   (Poland)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

GENE FAMILIES; OXIDATIVE FOLDING; PROLINE HYDROXYLATION;

COLLAGEN; HYDROXYLATION; PEPTIDES; PROTEIN FOLDING;

BIOACTIVITY;

ALPHA CONOTOXIN MII; COLLAGEN; CONOTOXIN; HYDROXYPROLINE; MU CONOTOXIN; OMEGA CONOTOXIN; OXYGENASE; PROLINE; PROTEIN DISULFIDE ISOMERASE; RECEPTOR; SODIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; CONUS SNAIL; HYDROXYLATION; IN VITRO STUDY; ISOMERIZATION; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANIMALS; CONOTOXINS; HYDROXYPROLINE; MICE; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; NEURONS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; PROTEIN FOLDING; RATS;

ANIMALIA; GASTROPODA;

EID: 38949200281     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701934m     Document Type: Article

References (84)

1. Ananthanarayanan, V. S. (1983) Structural aspects of hydroxyproline- containing proteins, J. Biomol. Struct. Dyn. 1, 843-855.
2. Jenkins, C. L., and Raines, R. T. (2002) Insights on the conformational stability of collagen, Nat. Prod. Rep. 19, 49-59.
3. Berisio, R., Granata, V., Vitagliano, L., and Zagari, A. (2004) Imino acids and collagen triple helix stability: Characterization of collagen-like polypeptides containing Hyp-Hyp-Gly sequence repeats, J. Am. Chem. Soc. 126, 11402-11403.
4. Jenkins, C. L., Bretscher, L. E., Guzei, I. A., and Raines, R. T. (2003) Effect of 3-hydroxyproIine residues on collagen stability, J. Am. Chem. Soc. 125, 6422-6427.
5. Jenkins, C. L., McCloskey, A. I., Guzei, I. A., Eberhardt, E. S., and Raines, R. T. (2005) O-Acylation of hydroxyproline residues: Effect on peptide-bond isomerization and collagen stability, Biopolymers 80, 1-8.
6. Nishi, Y., Uchiyama, S., Doi, M., Nishiuchi, Y., Nakazawa, T., Ohkubo, T., and Kobayashi, Y. (2005) Different effects of 4-hydroxyproline and 4-fluoroproline on the stability of collagen triple helix, Biochemistry 44, 6034-6042.
7. 10: Hydroxyproline in the X-position decreases the melting temperature of the collagen triple helix, Arch. Biochem. Biophys. 219, 198-203.
8. Fields, G. B., and Prockop, D. J. (1996) Perspectives on the synthesis and application of triple-helical, collagen-model peptides, Biopolymers 40, 345-357.
9. Berg, R. A., and Prockop, D. J. (1973) The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen, Biochem. Biophys. Res. Commun. 52, 115-120.
10. Pokidysheva, E., Milbradt, A. G., Meier, S., Renner, C., Haussinger, D., Bachinger, H. P., Moroder, L., Grzesiek, S., Holstein, T. W., Ozbek, S., and Engel, J. (2004) The structure of the Cys-rich terminal domain of Hydra minicollagen, which is involved in disulfide networks of the nematocyst wall, J. Biol. Chem. 279, 30395-30401.
11. Buczek, O., Bulaj, G., and Olivera, B. M. (2005) Conotoxins and the posttranslational modification of secreted gene products, Cell. Mol. Life Sci. 62, 3067-3079.
12. Williamson, M. P. (1994) The structure and function of proline-rich regions in proteins, Biochem. J. 297 (Part 2), 249-260.
13. Cassab, G. I. (1998) Plant Cell Wall Proteins, Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 281-309.
14. Narvaez-Vasquez, J., Pearce, G., and Ryan, C. A. (2005) The plant cell wall matrix harbors a precursor of defense signaling peptides, Proc. Natl. Acad. Sci. U.S.A. 102, 12974-12977.
15. Ryan, C. A., and Pearce, G. (1998) Systemin: A polypeptide signal for plant defensive genes, Annu. Rev. Cell Dev. Biol. 14, 1-17.
16. Ryan, C. A., and Pearce, G. (2003) Systemins: A functionally defined family of peptide signals that regulate defensive genes in Solanaceae species, Proc. Natl. Acad. Sci. U.S.A. 100 (Suppl. 2), 14577-14580.
17. Pearce, G., and Ryan, C. A. (2003) Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene, J. Biol. Chem. 278, 30044-30050.
18. Esquerre-Tugaye, M. T. (1979) Cell Surfaces in Plant-Microorganism Interactions: I. A Structural Investigation of Cell Wall Hydroxyproline-rich Glycoproteins Which Accumulate in Fungus-infected Plants, Plant Physiol. 64, 314-319.
19. Esquerre-Tugaye, M. T., Lafitte, C., Mazau, D., Toppan, A., and Touze, A. (1979) Cell Surfaces in Plant-Microorganism Interactions: II. Evidence for the Accumulation of Hydroxyproline-rich Glycoproteins in the Cell Wall of Diseased Plants as a Defense Mechanism, Plant Physiol. 64, 320-326.
20. Craig, A. G., Bandyopadhyay, P., and Olivera, B. M. (1999) Posttranslationally modified neuropeptides from Conus venoms, Eur. J. Biochem. 264, 271-215.
21. Bulaj, G., Buczek, O., Goodsell, I., Jimenez, E. C., Kranski, J., Nielsen, J. S., Garrett, J. E., and Olivera, B. M. (2003) Efficient oxidative folding of conotoxins and the radiation of venomous cone snails, Proc. Natl. Acad. Sci. U.S.A. 100 (Suppl. 2), 14562-14568.
22. Prorok, M., Warder, S. E., Blandl, T., and Castellino, F. J. (1996) Calcium binding properties of synthetic γ-carboxyglutamic acid-containing marine cone snail "sleeper" peptides, conantokin-G and conantokin-T, Biochemistry 35, 16528-16534.
23. Rigby, A. C., Baleja, J. D., Li, L., Pedersen, L. G., Furie, B. C., and Furie, B. (1997) Role of γ-carboxyglutamic acid in the calcium-induced structural transition of conantokin G, a conotoxin from the marine snail Conus geographus, Biochemistry 36, 15677-15684.
24. Norton, R. S., and Olivera, B. M. (2006) Conotoxins down under, Toxicon 48, 780-798.
25. Terlau, H., and Olivera, B. M. (2004) Conus venoms: A rich source of novel ion channel-targeted peptides, Physiol. Rev. 84, 41-68.
26. Franco, A., Pisarewicz, K., Moller, C., Mora, D., Fields, G. B., and Mari, F. (2006) Hyperhydroxylation: A new strategy for neuronal targeting by venomous marine molluscs, Prog. Mol. Subcell. Biol. 43, 83-103.
27. Pisarewicz, K., Mora, D., Pflueger, F. C., Fields, G. B., and Mari, F. (2005) Polypeptide chains containing D-γ-hydroxyvaline, J. Am. Chem. Soc. 127, 6207-6215.
28. Aguilar, M. B., Lopez-Vera, E., Ortiz, E., Becerril, B., Possani, L. D., Olivera, B. M., and Heimer de la Cotera, E. P. (2005) A novel conotoxin from Conus delessertii with posttranslationally modified lysine residues, Biochemistry 44, 11130-11136.
29. 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.
30. Nielsen, J. S., Buczek, P., and Bulaj, G. (2004) Cosolvent-assisted oxidative folding of a bicyclic α-conotoxin ImI, J. Pept. Sci. 10, 249-256.
31. Fuller, E., Green, B. R., Catlin, P., Buczek, O., Nielsen, J. S., Olivera, B. M., and Bulaj, G. (2005) Oxidative folding of conotoxins sharing an identical disulfide bridging framework, FEBS J. 272, 1727-1738.
32. 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.
33. Green, B. R., and Bulaj, G. (2006) Oxidative folding of conotoxins in immobilized systems, Protein Pept. Lett. 13, 67-70.
34. Darlak, K., Wiegandt Long, D., Czerwinski, A., Darlak, M., Valenzuela, F., Spatola, A. F., and Barany, G. (2004) Facile preparation of disulfide-bridged peptides using the polymer-supported oxidant CLEAR-OX, J. Pept. Res. 63, 303-312.
35. Cartier, G. E., Yoshikami, D., Gray, W. R., Luo, S., Olivera, B. M., and McIntosh, J. M. (1996) A new α-conotoxin which targets α3β2 nicotinic acetylcholine receptors, J. Biol. Chem. 271, 7522-7528.
36. 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.
37. 2+ channels, Neuron 9, 69-77.
38. Jakubowski, J. A., Keays, D. A., Kelley, W. P., Sandall, D. W., Bingham, J. P., Livett, B. G., Gayler, K. R., and Sweedler, J. V. (2004) Determining sequences and post-translational modifications of novel conotoxins in Conus victoriae using cDNA sequencing and mass spectrometry, J. Mass Spectrom. 39, 548-557.
39. 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 α-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo, Biochemistry 42, 6904-6911.
40. Filloux, F., Karras, J., Imperial, J. S., Gray, W. R., and Olivera, B. M. (1994) The distribution of ω-conotoxin MVIIC-binding sites in rat brain measured by autoradiography, Neurosci. Lett. 178, 263-266.
41. Olivera, B. M., Miljanich, G. P., Ramachandran, J., and Adams, M. E. (1994) Calcium channel diversity and neurotransmitter release: The ω-conotoxins and ω-agatoxins, Annu. Rev. Biochem. 63, 823-867.
42. Kubo, S., Chino, N., Kimura, T., and Sakakibara, S. (1996) Oxidative folding of ω-conotoxin MVIIC: Effects of temperature and salt, Biopolymers 38, 733-744.
43. Price-Carter, M., Gray, W. R., and Goldenberg, D. P. (1996) Folding of ω-conotoxins. 1. Efficient disulfide-coupled folding of mature sequences in vitro, Biochemistry 35, 15537-15546.
44. Olivera, B. M., Cruz, L. J., de Santos, V., LeCheminant, G. W., Griffin, D., Zeikus, R., McIntosh, J. M., Galyean, R., Varga, J., Gray, W. R., et al. (1987) Neuronal calcium channel antagonists. Discrimination between calcium channel subtypes using ω-conotoxin from Conus magus venom, Biochemistry 26, 2086-2090.
45. Olivera, B. M., McIntosh, J. M., Cruz, L. J., Luque, F. A., and Gray, W. R. (1984) Purification and sequence of a presynaptic peptide toxin from Conus geographus venom, Biochemistry 23, 5087-5090.
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. Ellison, M., Gao, F., Wang, H. L., Sine, S. M., McIntosh, J. M., and Olivera, B. M. (2004) α-Conotoxins ImI and ImII target distinct regions of the human α7 nicotinic acetylcholine receptor and distinguish human nicotinic receptor subtypes, Biochemistry 43, 16019-16026.
48. Ellison, M., McIntosh, J. M., and Olivera, B. M. (2003) α-Conotoxins ImI and ImII. Similar α7 nicotinic receptor antagonists act at different sites, J. Biol. Chem. 278, 757-764.
49. + channels, J. Biol. Chem. 278, 2177-2183.
50. + channel antagonist, Biochemistry 43, 8625-8635.
51. Jimenez, E. C., Craig, A. G., Watkins, M., Hillyard, D. R., Gray, W. R., Gulyas, J., Rivier, J. E., Cruz, L. J., and Olivera, B. M. (1997) Bromocontryphan: Post-translational bromination of tryptophan, Biochemistry 36, 989-994.
52. Craig, A. G., Zafaralla, G., Cruz, L. J., Santos, A. D., Hillyard, D. R., Dykert, J., Rivier, J. E., Gray, W. R., Imperial, J., DelaCruz, R. G., Spooling, A., Terlau, H., West, P. J., Yoshikami, D., and Olivera, B. M. (1998) An O-glycosylated neuroexcitatory Conus peptide, Biochemistry 37, 16019-16025.
53. Walker, C. S., Steel, D., Jacobsen, R. B., Lirazan, M. B., Cruz, L. J., Hooper, D., Shetty, R., DelaCruz, R. C., Nielsen, J. S., Zhou, L. M., Bandyopadhyay, P., Craig, A. G., and Olivera, B. M. (1999) The T-superfamily of conotoxins, J. Biol. Chem. 274, 30664-30671.
54. Kang, J., Low, W., Norberg, T., Meisenhelder, J., Hansson, K., Stenflo, J., Zhou, G. P., Imperial, J., Olivera, B. M., Rigby, A. C., and Craig, A. G. (2004) Total chemical synthesis and NMR characterization of the glycopeptide tx5a, a heavily post-translationally modified conotoxin, reveals that the glycan structure is α-D-Gal-(1→3)-α-D-GalNAc, Eur. J. Biochem. 271, 4939-4949.
55. Jimenez, E. C., Shetty, R. P., Lirazan, M., Rivier, J., Walker, C., Abogadie, F. C., Yoshikami, D., Cruz, L. J., and Olivera, B. M. (2003) Novel excitatory Conus peptides define a new conotoxin superfamily, J. Neurochem. 85, 610-621.
56. Buczek, O., Yoshikami, D., Bulaj, G., Jimenez, E. C., and Olivera, B. M. (2005) Post-translational amino acid isomerization: A functionally important D-amino acid in an excitatory peptide, J. Biol. Chem. 280, 4247-4253.
57. Buczek, O., Yoshikami, D., Watkins, M., Bulaj, G., Jimenez, E. C., and Olivera, B. M. (2005) Characterization of D-amino-acid-containing excitatory conotoxins and redefinition of the I-conotoxin superfamily, FEBS J. 272, 4178-4188.
58. French, R. J., and Dudley, S. C., Jr. (1999) Pore-blocking toxins as probes of voltage-dependent channels, Methods Enzymol. 294, 575-605.
59. Becker, S., Prusak-Sochaczewski, E., Zamponi, G., Beck-Sickinger, A. G., Gordon, R. D., and French, R. J. (1992) Action of derivatives of μ-conotoxin GIIIA on sodium channels. Single amino acid substitutions in the toxin separately affect association and dissociation rates, Biochemistry 31, 8229-8238.
60. 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.
61. 2+ influx, Proc. Natl. Acad. Sci. U.S.A. 96, 5758-5763.
62. Sabareesh, V., Gowd, K. H., Ramasamy, P., Sudarslal, S., Krishnan, K. S., Sikdar, S. K., and Balaram, P. (2006) Characterization of contryphans from Conus loroisii and Conus amadis that target calcium channels, Peptides 27, 2647-2654.
63. Quiram, P. A., McIntosh, J. M., and Sine, S. M. (2000) Pairwise interactions between neuronal α(7) acetylcholine receptors and α-conotoxin PnIB, J. Biol. Chem. 275, 4889-4896.
64. Rabenstein, D. L., Shi, T., and Spain, S. M. (2000) Intramolecular catalysis of the cis-trans isomerization of proline peptide bonds in cyclic disulfide-containing peptides, J. Am. Chem. Soc. 122, 2401-2402.
65. Shi, T., Spain, S. M., and Rabenstein, D. L. (2006) A striking periodicity of the cis/trans isomerization of proline imide bonds in cyclic disulfide-bridged peptides, Angew. Chem., Int. Ed. 45, 1780-1783.
66. Flinn, J. P., Murphy, R., Boublik, J. H., Lew, M. J., Wright, C. E., and Angus, J. A. (1995) Synthesis and biological characterization of a series of analogues of ω-conotoxin GVIA, J. Pept. Sci. 1, 379-384.
67. Flinn, J. P., Pallaghy, P. K., Lew, M. J., Murphy, R., Angus, J. A., and Norton, R. S. (1999) Role of disulfide bridges in the folding, structure and biological activity of ω-conotoxin GVIA, Biochim. Biophys. Acta 1434, 177-190.
68. Flinn, J. P., Pallaghy, P. K., Lew, M. J., Murphy, R., Angus, J. A., and Norton, R. S. (1999) Roles of key functional groups in ω-conotoxin GVIA synthesis, structure and functional assay of selected peptide analogues, Eur. J. Biochem. 262, 447-455.
69. Lew, M. J., Flinn, J. P., Pallaghy, P. K., Murphy, R., Whorlow, S. L., Wright, C. E., Norton, R. S., and Angus, J. A. (1997) Structure-function relationships of ω-conotoxin GVIA. Synthesis, structure, calcium channel binding, and functional assay of alanine-substituted analogues, J. Biol. Chem. 272, 12014-12023.
70. Grathwohl, C., and Wuthrich, K. (1976) The X-Pro peptide bond as an NMR probe for conformational studies of flexible linear peptides, Biopolymers 15, 2025-2041.
71. Grathwohl, C., and Wuthrich, K. (1981) NMR studies of the rates of proline cis/trans isomerisation in oligopeptides, Biopolymers 20, 2623-2633.
72. Wu, W. J., and Raleigh, D. P. (1998) Local control of peptide conformation: Stabilization of eis proline peptide bonds by aromatic proline interactions, Biopolymers 45, 381-394.
73. Shi, T., Spain, S. M., and Rabenstein, D. L. (2004) Unexpectedly fast cis/trans isomerization of Xaa-Pro peptide bonds in disulfide-constrained cyclic peptides, J. Am. Chem. Soc. 126, 790-796.
74. Improta, R., Benzi, C., and Barone, V. (2001) Understanding the role of stereoelectronic effects in determining collagen stability. 1. A quantum mechanical study of proline, hydroxyproline, and fluoroproline dipeptide analogues in aqueous solution, J. Am. Chem. Soc. 123, 12568-12577.
75. Panasik, N., Jr., Eberhardt, E. S., Edison, A. S., Powell, D. R., and Raines, R. T. (1994) Inductive effects on the structure of proline residues, Int. J. Pept. Protein Res. 44, 262-269.
76. 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.
77. Pallaghy, P. K., He, W., Jimenez, E. C., Olivera, B. M., and Norton, R. S. (2000) Structures of the contryphan family of cyclic peptides. Role of electrostatic interactions in cis-trans isomerism, Biochemistry 39, 12845-12852.
78. Bottomley, M. J., Batten, M. R., Lumb, R. A., and Bulleid, N. J. (2001) Quality control in the endoplasmic reticulum: PDI mediates the ER retention of unassembled procollagen C-propeptides, Curr. Biol. 11, 1114-1118.
79. Lumb, R. A., and Bulleid, N. J. (2002) Is protein disulfide isomerase a redox-dependent molecular chaperone, EMBO J. 21, 6763-6770.
80. Koivunen, P., Salo, K. E., Myllyharju, J., and Ruddock, L. W. (2005) Three binding sites in protein-disulfide isomerase cooperate in collagen prolyl 4-hydroxylase tetramer assembly, J. Biol. Chem. 280, 5227-5235.
81. 2 sensing, Science 292, 464-468.
82. 2-regulated prolyl hydroxylation, Science 292, 468-472.
83. Min, J. H., Yang, H., Ivan, M., Gertler, F., Kaelin, W. G., Jr., and Pavletich, N. P. (2002) Structure of an HIF-1α-pVHL complex: Hydroxyproline recognition in signaling, Science 296, 1886-1889.
84. Hon, W. C., Wilson, M. I., Harlos, K., Claridge, T. D., Schofield, C. J., Pugh, C. W., Maxwell, P. H., Ratcliffe, P. J., Stuart, D. I., and Jones, E. Y. (2002) Structural basis for the recognition of hydroxyproline in HIF-1α by pVHL, Nature 417, 975-978.