Drugs from Slugs. Part II - Conopeptide bioengineering

Chemico-Biological Interactions

Volumn 200, Issue 2-3, 2012, Pages 92-113

  Bingham, Jon Paul ^a   Andrews, Elizabeth A ^a   Kiyabu, Shaun M ^a   Cabalteja, Chino C ^a  

^a UNIVERSITY OF HAWAII AT MANOA   (United States)

Author keywords

Bioengineering; Clinical drugs; Conopeptides; Peptide cyclization; Peptidomimetics; Therapeutic peptides

Indexed keywords

CONOPEPTIDE; CYSTEINE; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIBODY PRODUCTION; BINDING SITE; BIOENGINEERING; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CONJUGATION; CYCLIZATION; DISULFIDE BOND; HUMAN; HYDROPHOBICITY; ISOTOPE LABELING; MEDICAL RESEARCH; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATION; PEPTIDE SYNTHESIS; POLYMERIZATION; PROTEIN FOLDING; PROTEIN PROCESSING; REVIEW; SOLID PHASE SYNTHESIS; STRUCTURE ACTIVITY RELATION; TOXIC SLUG;

ANIMALS; CONUS SNAIL; MOLLUSK VENOMS; PEPTIDES; PROTEIN ENGINEERING;

GASTROPODA;

EID: 84868709357     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2012.09.021     Document Type: Review

References (189)

1. R. Halai, and D.J. Craik Conotoxins: natural product drug leads Nat. Prod. Rep. 26 2009 526 536
2. J.P. Bingham, E. Mitsunaga, and Z.L. Bergeron Drugs from slugs - past, present and future perspectives of omega-conotoxin research Chem. Biol. Interact. 183 2010 1 18
3. U. Dietrich, R. Durr, and J. Koch Peptides as drugs: from screening to application Curr. Pharm. Biotechnol. 2012 PMID: 22429133
4. F. Lazcano-Perez, S.A. Roman-Gonzalez, N. Sanchez-Puig, and R. Arreguin-Espinosa Bioactive peptides from marine organisms: a short overview Protein Pept. Lett. 2012 700 707
5. T.P. King, and K.M. Wittkowski Hyaluronidase and hyaluronan in insect venom allergy Int. Arch. Allergy Immunol. 156 2011 205 211
6. T. Pexton, T. Moeller-Bertram, J.M. Schilling, and M.S. Wallace Targeting voltage-gated calcium channels for the treatment of neuropathic pain: a review of drug development Expert Opin. Investig. Drugs 20 2011 1277 1284
7. C. Adessi, and C. Soto Converting a peptide into a drug: strategies to improve stability and bioavailability Curr. Med. Chem. 9 2002 963 978
8. L. Malavolta, and F.R. Cabral Peptides: important tools for the treatment of central nervous system disorders Neuropeptides 45 2011 309 316
9. R.A. Skidgel, and E.G. Erdos Angiotensin converting enzyme (ACE) and neprilysin hydrolyze neuropeptides: a brief history, the beginning and follow-ups to early studies Peptides 25 2004 521 525
10. S.H. Ferreira A bradykinin-potentiating factor (Bpf) present in the venom of Bothrops jararca Br. J. Pharmacol. Chemother. 24 1965 163 169
11. S.H. Ferreira, D.C. Bartelt, and L.J. Greene Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom Biochemistry 9 1970 2583 2593
12. R. DiBianco Adverse reactions with angiotensin converting enzyme (ACE) inhibitors Med. Toxicol. 1 1986 122 141
13. D.W. Cushman, and M.A. Ondetti History of the design of captopril and related inhibitors of angiotensin converting enzyme Hypertension 17 1991 589 592
14. I. Spence, D. Gillessen, R.P. Gregson, and R.J. Quinn Characterization of the neurotoxic constituents of Conus geographus (L) venom Life Sci. 21 1977 1759 1769
15. L.J. Cruz, W.R. Gray, and B.M. Olivera Purification and properties of a myotoxin from Conus geographus venom Arch. Biochem. Biophys. 190 1978 539 548
16. R.A. Balaji, A. Ohtake, K. Sato, P. Gopalakrishnakone, R.M. Kini, K.T. Seow, and B.H. Bay 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 2000 39516 39522
17. G.T. Haermanson Bioconjugation Techniques 1996 Elsevier San Diego pp. 3-26
18. L.J. Cruz, and B.M. Olivera Calcium channel antagonists. Omega-conotoxin defines a new high affinity site J. Biol. Chem. 261 1986 6230 6233
19. A. Nicke, M.L. Loughnan, E.L. Millard, P.F. Alewood, D.J. Adams, N.L. Daly, D.J. Craik, and R.J. Lewis Isolation, structure, and activity of GID, a novel alpha 4/7-conotoxin with an extended N-terminal sequence J. Biol. Chem. 278 2003 3137 3144
20. T.S. Kang, S. Vivekanandan, S.D. Jois, and R.M. Kini Effect of C-terminal amidation on folding and disulfide-pairing of alpha-conotoxin ImI Angew. Chem. Int. Ed. Engl. 44 2005 6333 6337
21. I.A. Sharpe, J. Gehrmann, M.L. Loughnan, L. Thomas, D.A. Adams, A. Atkins, E. Palant, D.J. Craik, D.J. Adams, P.F. Alewood, and R.J. Lewis Two new classes of conopeptides inhibit the alpha1-adrenoceptor and noradrenaline transporter Nat. Neurosci. 4 2001 902 907
22. N. Jiang, and J. Ma Influence of disulfide connectivity, electrostatics, and hydrophobicity on the conformational variations of alpha-conotoxin GI single-disulfide analogues: simulations with polarizable force field J. Phys. Chem. B 114 2010 11241 11250
23. R.J. Lewis, C.I. Schroeder, J. Ekberg, K.J. Nielsen, M. Loughnan, L. Thomas, D.A. Adams, R. Drinkwater, D.J. Adams, and P.F. Alewood Isolation and structure-activity of mu-conotoxin TIIIA, a potent inhibitor of tetrodotoxin-sensitive voltage-gated sodium channels Mol. Pharmacol. 71 2007 676 685
24. T. Kimmerlin, and D. Seebach '100 years of peptide synthesis': ligation methods for peptide and protein synthesis with applications to beta-peptide assemblies J. Pept. Res. 65 2005 229 260
25. F. Albericio Orthogonal protecting groups for N(alpha)-amino and C-terminal carboxyl functions in solid-phase peptide synthesis Biopolymers 55 2000 123 139
26. G.B. Fields, and R.L. Noble Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids Int. J. Pept. Protein Res. 35 1990 161 214
27. B. Merrifield Concept and early development of solid-phase peptide synthesis Methods Enzymol. 289 1997 3 13
28. G. Barany, N. Kneib-Cordonier, and D.G. Mullen Solid-phase peptide synthesis: a silver anniversary report Int. J. Pept. Protein Res. 30 1987 705 739
29. A.G. Grant Synthetic Peptides: A User's Guide U.O.M.M.C. Allan Jacobson, Advances in Molecular Biology second ed. 2002 Oxford University Press Oxford, New York
30. G.R. Marshall Solid-phase synthesis: a paradigm shift J. Pept. Sci. 9 2003 534 544
31. W.C. Chan, and P.D. White Basic Principles in FMOC Solid Phase Peptide Synthesis 2000 Oxford University Press Inc. New York pp. 1-76
32. V.K. Sarin, S.B. Kent, J.P. Tam, and R.B. Merrifield Quantitative monitoring of solid-phase peptide synthesis by the ninhydrin reaction Anal. Biochem. 117 1981 147 157
33. J.P. Tam, and Y. Lu Coupling difficulty associated with interchain clustering and phase transition in solid phase peptide synthesis JACS 117 1995 12058 12063
34. A. Aletras, K. Barlos, D. Gatos, S. Koutsogianni, and P. Mamos Preparation of the very acid-sensitive Fmoc-Lys(Mtt)-OH. Application in the synthesis of side-chain to side-chain cyclic peptides and oligolysine cores suitable for the solid-phase assembly of MAPs and TASPs Int. J. Pept. Protein Res. 45 1995 488 496
35. B.L. Nilsson, L.L. Kiessling, and R.T. Raines High-yielding Staudinger ligation of a phosphinothioester and azide to form a peptide Org. Lett. 3 2001 9 12
36. M. Kohn, and R. Breinbauer The Staudinger ligation - a gift to chemical biology Angew. Chem. Int. Ed. Engl. 43 2004 3106 3116
37. M. Nakamura, Y. Ishida, T. Kohno, K. Sato, Y. Oba, and H. Nakamura Effects of modification at the fifth residue of mu-conotoxin GIIIA with bulky tags on the electrically stimulated contraction of the rat diaphragm J. Pept. Res. 64 2004 110 117
38. + channel analysis Biochem. Biophys. Res. Commun. 283 2001 374 378
39. T.S. Han, R.W. Teichert, B.M. Olivera, and G. Bulaj Conus venoms - a rich source of peptide-based therapeutics Curr. Pharm. Des. 14 2008 2462 2479
40. H. Terlau, and B.M. Olivera Conus venoms: a rich source of novel ion channel-targeted peptides Physiol. Rev. 84 2004 41 68
41. R.M. Hann, O.R. Pagan, L.M. Gregory, T. Jacome, and V.A. Eterovic The 9-arginine residue of alpha-conotoxin GI is responsible for its selective high affinity for the alphagamma agonist site on the electric organ acetylcholine receptor Biochemistry 36 1997 9051 9056
42. D.R. Groebe, W.R. Gray, and S.N. Abramson Determinants involved in the affinity of alpha-conotoxins GI and SI for the muscle subtype of nicotinic acetylcholine receptors Biochemistry 36 1997 6469 6474
43. A. Kolosov, L. Aurini, E.D. Williams, I. Cooke, and C.S. Goodchild Intravenous injection of leconotide, an omega conotoxin: synergistic antihyperalgesic effects with morphine in a rat model of bone cancer pain Pain Med. 12 2011 923 941
44. G. Berecki, L. Motin, A. Haythornthwaite, S. Vink, P. Bansal, R. Drinkwater, C.I. Wang, M. Moretta, R.J. Lewis, P.F. Alewood, M.J. Christie, and D.J. Adams Analgesic (omega)-conotoxins CVIE and CVIF selectively and voltage-dependently block recombinant and native N-type calcium channels Mol. Pharmacol. 77 2010 139 148
45. N.J. Ede Multiple parallel synthesis of peptides on SynPhase grafted supports J. Immunol. Methods 267 2002 3 11
46. C. Falciani, L. Lozzi, A. Pini, and L. Bracci Bioactive peptides from libraries Chem. Biol. 12 2005 417 426
47. B. Kundu Solid-phase strategies for the design and synthesis of heterocyclic molecules of medicinal interest Curr. Opin. Drug Discov. Devel. 6 2003 815 826
48. A. Abell Advances in Amino Acids Mimetics and Peptidomimetics, vol. 1 1st ed. 2007 JAI Press London
49. M.R. Rajeev Kharb, Prabodh Chander Sharma, and Mohammad Shahar Yar Therapeutic improtance of peptidomimetics in medicinal chemistry J. Chem. Pharm. Res. 3 2011 173 186
50. N.J.H.-D. Sewald Peptides: Chemistry and Biology 2009 Wiley-VHC Verlag Weinheim
51. A.S. Ripka, and D.H. Rich Peptidomimetic design Curr. Opin. Chem. Biol. 2 1998 441 452
52. J.B. Baell, S.A. Forsyth, R.W. Gable, R.S. Norton, and R.J. Mulder Design and synthesis of type-III mimetics of omega-conotoxin GVIA J. Comput. Aided Mol. Des. 15 2001 1119 1136
53. Z. Dekan, C.I. Wang, R.K. Andrews, R.J. Lewis, and P.F. Alewood Conotoxin engineering: dual pharmacophoric noradrenaline transport inhibitor/integrin binding peptide with improved stability Org. Biomol. Chem. 2012
54. B.M. Olivera, J. Rivier, J.K. Scott, D.R. Hillyard, and L.J. Cruz Conotoxins J. Biol. Chem. 266 1991 22067 22070
55. S. Luo, T.A. Nguyen, G.E. Cartier, B.M. Olivera, D. Yoshikami, and J.M. McIntosh Single-residue alteration in alpha-conotoxin PnIA switches its nAChR subtype selectivity Biochemistry 38 1999 14542 14548
56. I.E. Kasheverov, M.N. Zhmak, C.A. Vulfius, E.V. Gorbacheva, D.Y. Mordvintsev, Y.N. Utkin, R. van Elk, A.B. Smit, and V.I. Tsetlin Alpha-conotoxin analogs with additional positive charge show increased selectivity towards Torpedo californica and some neuronal subtypes of nicotinic acetylcholine receptors FEBS J. 273 2006 4470 4481
57. + channel J. Biol. Chem. 275 2000 24639 24644
58. M. Chahine, L.Q. Chen, N. Fotouhi, R. Walsky, D. Fry, V. Santarelli, R. Horn, and R.G. Kallen Characterizing the mu-conotoxin binding site on voltage-sensitive sodium channels with toxin analogs and channel mutations Receptors Channels 3 1995 161 174
59. P. Buczek, O. Buczek, and G. Bulaj Total chemical synthesis and oxidative folding of delta-conotoxin PVIA containing an N-terminal propeptide Biopolymers 80 2005 50 57
60. J.P. Flinn, P.K. Pallaghy, M.J. Lew, R. Murphy, J.A. Angus, and R.S. Norton Roles of key functional groups in omega-conotoxin GVIA synthesis, structure and functional assay of selected peptide analogues Eur. J. Biochem. 262 1999 447 455
61. E. Lopez-Vera, A. Walewska, J.J. Skalicky, B.M. Olivera, and G. Bulaj Role of hydroxyprolines in the in vitro oxidative folding and biological activity of conotoxins Biochemistry 47 2008 1741 1751
62. M. Loughnan, T. Bond, A. Atkins, J. Cuevas, D.J. Adams, N.M. Broxton, B.G. Livett, J.G. Down, A. Jones, P.F. Alewood, and R.J. Lewis Alpha-conotoxin EpI, a novel sulfated peptide from Conus episcopatus that selectively targets neuronal nicotinic acetylcholine receptors J. Biol. Chem. 273 1998 15667 15674
63. J.L. Wolfender, F. Chu, H. Ball, F. Wolfender, M. Fainzilber, M.A. Baldwin, and A.L. Burlingame Identification of tyrosine sulfation in Conus pennaceus conotoxins alpha-PnIA and alpha-PnIB: further investigation of labile sulfo- and phosphopeptides by electrospray, matrix-assisted laser desorption/ionization (MALDI) and atmospheric pressure MALDI mass spectrometry J. Mass Spectrom. 34 1999 447 454
64. D.J. Craik, and D.J. Adams Chemical modification of conotoxins to improve stability and activity ACS Chem. Biol. 2 2007 457 468
65. B.M. Olivera, and L.J. Cruz Conotoxins, in retrospect Toxicon 39 2001 7 14
66. J.M. McIntosh, A.D. Santos, and B.M. Olivera Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes Annu. Rev. Biochem. 68 1999 59 88
67. A.H. Jin, N.L. Daly, S.T. Nevin, C.I. Wang, S. Dutertre, R.J. Lewis, D.J. Adams, D.J. Craik, and P.F. Alewood Molecular engineering of conotoxins: the importance of loop size to alpha-conotoxin structure and function J. Med. Chem. 51 2008 5575 5584
68. E.L. Millard, S.T. Nevin, M.L. Loughnan, A. Nicke, R.J. Clark, P.F. Alewood, R.J. Lewis, D.J. Adams, D.J. Craik, and N.L. Daly Inhibition of neuronal nicotinic acetylcholine receptor subtypes by alpha-conotoxin GID and analogues J. Biol. Chem. 284 2009 4944 4951
69. R.S. Norton Mu-conotoxins as leads in the development of new analgesics Molecules 15 2010 2825 2844
70. L. Azam, and J.M. McIntosh Alpha-conotoxins as pharmacological probes of nicotinic acetylcholine receptors Acta Pharmacol. Sin. 30 2009 771 783
71. B.R. Green, P. Catlin, M.M. Zhang, B. Fiedler, W. Bayudan, A. Morrison, R.S. Norton, B.J. Smith, D. Yoshikami, B.M. Olivera, and G. Bulaj Conotoxins containing nonnatural backbone spacers: cladistic-based design, chemical synthesis, and improved analgesic activity Chem. Biol. 14 2007 399 407
72. K.K. Khoo, M.J. Wilson, B.J. Smith, M.M. Zhang, J. Gulyas, D. Yoshikami, J.E. Rivier, G. Bulaj, and R.S. Norton Lactam-stabilized helical analogues of the analgesic mu-conotoxin KIIIA J. Med. Chem. 54 2011 7558 7566
73. B. Hargittai, N.A. Sole, D.R. Groebe, S.N. Abramson, and G. Barany Chemical syntheses and biological activities of lactam analogues of alpha-conotoxin SI J. Med. Chem. 43 2000 4787 4792
74. K. Sato, C. Raymond, N. Martin-Moutot, T. Sasaki, A. Ohtake, K. Minami, C. Van Renterghem, M. Takahashi, and M.J. Seagar Binding of six chimeric analogs of omega-conotoxin MVIIA and MVIIC to N- and P/Q-type calcium channels Biochem. Biophys. Res. Commun. 269 2000 254 256
75. G. Hopping, R.L. Lewis, and P.F. Alewood Rapid access to omega conotoxin chimeras using native chemical ligation Aust. J. Chem. 62 2009 1333 1338
76. D.W. Keizer, P.J. West, E.F. Lee, D. Yoshikami, B.M. Olivera, G. Bulaj, and R.S. Norton Structural basis for tetrodotoxin-resistant sodium channel binding by mu-conotoxin SmIIIA J. Biol. Chem. 278 2003 46805 46813
77. K.J. Shon, B.M. Olivera, M. Watkins, R.B. Jacobsen, W.R. Gray, C.Z. Floresca, L.J. Cruz, D.R. Hillyard, H. Terlau, and D. Yoshikami Mu-conotoxin PIIIA, a new peptide for discriminating among tetrodotoxin-sensitive Na channel subtypes J. Neurosci. 18 1998 4473 4481
78. E. Drakopoulou, K. Uray, G. Mezö, M.R. Price, C. Vita, and F. Hudecz Synthesis and antibody recognition of mucin 1 (MUC1)-alpha-conotoxin chimera J. Pept. Sci. 6 2000 175 185
79. F.H.G. Mezô, E. Drakopoulou, C. Vita, V. Paál, and É. Rajnavölgyi Synthesis and immunological studies of alpha-conotoxin chimera containing an immunodominant epitope from the 268-284 region of HSV gD protein J. Pept. Res. 55 2000 7 17
80. I.E. Kasheverov, M.N. Zhmak, I.V. Maslennikov, Y.N. Utkin, and V.I. Tsetlin A comparative study on selectivity of alpha-conotoxins GI and ImI using their synthetic analogues and derivatives Neurochem. Res. 28 2003 599 606
81. A.S. Galanis, F. Albericio, and M. Grotli Enhanced microwave-assisted method for on-bead disulfide bond formation: synthesis of alpha-conotoxin MII Biopolymers 92 2009 23 34
82. B. Hargittai, and G. Barany Controlled syntheses of natural and disulfide-mispaired regioisomers of alpha-conotoxin SI J. Pept. Res. 54 1999 468 479
83. A.H. Jin, H. Brandstaetter, S.T. Nevin, C.C. Tan, R.J. Clark, D.J. Adams, P.F. Alewood, D.J. Craik, and N.L. Daly Structure of alpha-conotoxin BuIA: influences of disulfide connectivity on structural dynamics BMC Struct. Biol. 7 2007 28 41
84. E.L. Millard, N.L. Daly, and D.J. Craik Structure-activity relationships of alpha-conotoxins targeting neuronal nicotinic acetylcholine receptors Eur. J. Biochem. 271 2004 2320 2326
85. J.L. Dutton, P.S. Bansal, R.C. Hogg, D.J. Adams, P.F. Alewood, and D.J. Craik A new level of conotoxin diversity, a non-native disulfide bond connectivity in alpha-conotoxin AuIB reduces structural definition but increases biological activity J. Biol. Chem. 277 2002 48849 48857
86. + channel expressed in a human cell line Bioconjug. Chem. 17 2006 689 699
87. C.J. Armishaw, and P.F. Alewood Conotoxins as research tools and drug leads Curr. Protein Pept. Sci. 6 2005 221 240
88. R.G. Simmonds, D.E. Tupper, and J.R. Harris Synthesis of disulfide-bridged fragments of omega-conotoxins GVIA and MVIIA. Use of Npys as a protecting/activating group for cysteine in Fmoc syntheses Int. J. Pept. Protein Res. 43 1994 363 366
89. C.J. Armishaw, N. Singh, J.L. Medina-Franco, R.J. Clark, K.C. Scott, R.A. Houghten, and A.A. Jensen A synthetic combinatorial strategy for developing alpha-conotoxin analogs as potent alpha7 nicotinic acetylcholine receptor antagonists J. Biol. Chem. 15 2010 1809 1821
90. C.A. MacRaild, J. Illesinghe, B.J. van Lierop, A.L. Townsend, M. Chebib, B.G. Livett, A.J. Robinson, and R.S. Norton Structure and activity of (2,8)-dicarba-(3,12)-cystino alpha-ImI, an alpha-conotoxin containing a nonreducible cystine analogue J. Med. Chem. 52 2009 755 762
91. Z. Dekan, I. Vetter, N.L. Daly, D.J. Craik, R.J. Lewis, and P.F. Alewood Alpha-conotoxin ImI incorporating stable cystathionine bridges maintains full potency and identical three-dimensional structure J. Am. Chem. Soc. 133 2011 15866 15869
92. T.S. Han, M.M. Zhang, A. Walewska, P. Gruszczynski, C.R. Robertson, T.E. Cheatham 3rd, D. Yoshikami, B.M. Olivera, and G. Bulaj Structurally minimized mu-conotoxin analogues as sodium channel blockers: implications for designing conopeptide-based therapeutics ChemMedChem 4 2009 406 414
93. K.M. Kelly, A. Kume, R.L. Albin, and R.L. Macdonald Autoradiography of L-type and N-type calcium channels in aged rat hippocampus, entorhinal cortex, and neocortex Neurobiol. Aging 22 2001 17 23
94. 125I-alpha-conotoxin MII identifies a novel nicotinic acetylcholine receptor population in mouse brain Mol. Pharmacol. 57 2000 913 925
95. (125)I]Y0- alpha-conotoxin MII binding in rat mesostriatal dopamine pathway following continuous infusion of nicotine Neuroscience 137 2006 565 572
96. W.R. Gray, F.A. Luque, R. Galyean, E. Atherton, R.C. Sheppard, B.L. Stone, A. Reyes, J. Alford, M. McIntosh, and B.M. Olivera Conotoxin GI: disulfide bridges, synthesis, and preparation of iodinated derivatives Biochemistry 23 1984 2796 2802
97. B.M. Olivera, L.J. Cruz, V. De Santos, G.W. LeCheminant, D. Griffin, R. Zeikus, M. McIntosh, R. Galyean, J. Varga, W.R. Gray, and J. Rivier Neuronal calcium channel antagonists. Discrimination between calcium channel subtypes using omega-conotoxin from Conus magus venom Biochemistry 26 1987 2086 2090
98. 125I-omega-conotoxin GVIA binding in rat whole brain Neurochem. Res. 18 1993 1137 1144
99. D. Shields, R. Montenegro, and M. Ragusa Chemical stability of admixtures combining ziconotide with morphine or hydromorphone during simulated intrathecal administration Neuromodulation 8 2005 257 263
100. D.P. Goldenberg, R.E. Koehn, D.E. Gilbert, and G. Wagner Solution structure and backbone dynamics of an omega-conotoxin precursor Protein Sci. 10 2001 538 550
101. 2+ channels in the brain by positron emission tomography J. Labelled Compd. Radiopharm. 49 2006 269 283
102. R.A. Lampe, M.M. Lo, R.A. Keith, M.B. Horn, M.W. McLane, J.L. Herman, and R.C. Spreen Effects of site-specific acetylation on omega-conotoxin GVIA binding and function Biochemistry 32 1993 3255 3260
103. Y. Yanagawa, T. Abe, and M. Satake Mu-conotoxins share a common binding site with tetrodotoxin/saxitoxin on eel electroplax Na channels J. Neurosci. 7 1987 1498 1502
104. V. Tsetlin, Y. Utkin, and I. Kasheverov Polypeptide and peptide toxins, magnifying lenses for binding sites in nicotinic acetylcholine receptors Biochem. Pharmacol. 78 2009 720 731
105. 2+ channels on frog motor nerve terminals revealed by fluorescent omega-conotoxin J. Neurosci. 11 1991 1032 1039
106. 2+ channels are located on somata, dendrites, and a subpopulation of dendritic spines on live hippocampal pyramidal neurons J. Neurosci. 14 1994 6815 6824
107. O.T. Jones, and G.M. Bernstein Mapping N-type Calcium Channel Distributions with omega-Conotoxins 2001 Humana Press Inc. Towata, New Jersey
108. E.E. Mena, M.F. Gullak, M.J. Pagnozzi, K.E. Richter, J. Rivier, L.J. Cruz, and B.M. Olivera Conantokin-G: a novel peptide antagonist to the N-methyl-d-aspartic acid (NMDA) receptor Neurosci. Lett. 118 1990 241 244
109. Z. Sheng, Q. Dai, M. Prorok, and F.J. Castellino Subtype-selective antagonism of N-methyl-d-aspartate receptor ion channels by synthetic conantokin peptides Neuropharmacology 53 2007 145 156
110. M. Prorok, and F.J. Castellino The molecular basis of conantokin antagonism of NMDA receptor function Curr. Drug Targets 8 2007 633 642
111. V.D. Twede, G. Miljanich, B.M. Olivera, and G. Bulaj Neuroprotective and cardioprotective conopeptides: an emerging class of drug leads Curr. Opin. Drug Discov. Devel. 12 2009 231 239
112. L.M. Zhou, G.I. Szendrei, L.H. Fossom, M.L. Maccecchini, P. Skolnick, and L. Otvos Jr Synthetic analogues of conantokin-G: NMDA antagonists acting through a novel polyamine-coupled site J. Neurochem. 66 1996 620 628
113. R.C. Klein, and F.J. Castellino Inhibition of MK801 binding in adult rat brain sections by conantokin-G and conantokin-T Neurosci. Lett. 273 1999 171 174
114. J. Durand, L. Kojic, Y. Wang, P. Lee, M.S. Cynader, and Q. Gu Confocal imaging of N-methyl-d-aspartate receptors in living cortical neurons Neuroscience 97 2000 11 23
115. T.A. Benke, O.T. Jones, G.L. Collingridge, and K.J. Angelides N-Methyl-d-aspartate receptors are clustered and immobilized on dendrites of living cortical neurons Proc. Nat. Acad. Sci. USA 90 1993 7819 7823
116. V.A. Vishwanath, and J.M. McIntosh Synthesis of fluorescent analogs of alpha-conotoxin MII Bioconjug. Chem. 17 2006 1612 1617
117. A.J. Hone, P. Whiteaker, S. Christensen, Y. Xiao, E.L. Meyer, and J.M. McIntosh A novel fluorescent alpha-conotoxin for the study of alpha7 nicotinic acetylcholine receptors J. Neurochem. 111 2009 80 89
118. A.J. Hone, P. Whiteaker, J.L. Mohn, M.H. Jacob, and J.M. McIntosh Alexa Fluor 546-ArIB[V11L;V16A] is a potent ligand for selectively labeling alpha 7 nicotinic acetylcholine receptors J. Neurochem. 114 2010 994 1006
119. O.H. Laitinen, H.R. Nordlund, V.P. Hytonen, and M.S. Kulomaa Brave new (strept)avidins in biotechnology Trends Biotechnol. 25 2007 269 277
120. D.S. Wilbur, P.M. Pathare, D.K. Hamlin, P.S. Stayton, R. To, L.A. Klumb, K.R. Buhler, and R.L. Vessella Development of new biotin/streptavidin reagents for pretargeting Biomol. Eng. 16 1999 113 118
121. A. Skerra, and T.G. Schmidt Applications of a peptide ligand for streptavidin: the Strep-tag Biomol. Eng. 16 1999 79 86
122. E.A. Bayer, and M. Wilchek Application of avidin-biotin technology to affinity-based separations J. Chromatogr. 510 1990 3 11
123. P.E. Swanson Foundations of immunohistochemistry. A practical review Am. J. Clin. Pathol. 90 1988 333 339
124. L.J. Cruz, W.R. Gray, B.M. Olivera, R.D. Zeikus, and L. Kerr Conus geographus toxins that discriminate between neuronal and muscle sodium channels J. Biol. Chem. 260 1985 9280 9288
125. S. Becker, E. Prusak-Sochaczewski, G. Zamponi, A.G. Beck-Sickinger, R.D. Gordon, and R.J. French Action of derivatives of mu-conotoxin GIIIA on sodium channels. Single amino acid substitutions in the toxin separately affect association and dissociation rates Biochemistry 31 1992 8229 8238
126. K. Sato, Y. Ishida, K. Wakamatsu, R. Kato, H. Honda, Y. Ohizumi, H. Nakamura, M. Ohya, J.M. Lancelin, and D. Kohda Active site of mu-conotoxin GIIIA, a peptide blocker of muscle sodium channels J. Biochem. 266 1991 16989 16991
127. M. Nakamura, Y. Niwa, Y. Ishida, T. Kohno, K. Sato, Y. Oba, and H. Nakamura Modification of Arg-13 of μ-conotoxin GIIIA with piperidinyl-Arg analogs and their relation to the inhibition of sodium channels FEBS Lett. 503 2001 107 110
128. W.S.D. Bowman, and A. McCormack Affinity purification of rat cortical and chicken forebrain synaptosomes using a biotinylated derivative of omega-CgTx GVIA Neuropharmacology 34 1995 743 752
129. Y. Sugiura, A. Woppmann, G.P. Miljanich, and C.P. Ko A novel omega-conopeptide for the presynaptic localization of calcium channels at the mammalian neuromuscular junction J. Neurocytol. 24 1995 15 27
130. N. Nemoto, S. Kubo, T. Yoshida, N. Chino, T. Kimura, S. Sakakibara, Y. Kyogoku, and Y. Kobayashi Solution structure of omega-conotoxin MVIIC determined by NMR Biochem. Biophys. Res. Commun. 207 1995 695 700
131. K.H. Gowd, T.S. Han, V. Twede, J. Gajewiak, M.D. Smith, M. Watkins, R.J. Platt, G. Toledo, H.S. White, B.M. Olivera, and G. Bulaj Conantokins derived from the Asprella Clade Impart conRl-B, an N-methyl d-aspartate receptor antagonist with a unique selectivity profile for NR2B subunits Biochemistry 51 2012 4685 4692
132. G.E. Cartier, D. Yoshikami, W.R. Gray, S. Luo, B.M. Olivera, and J.M. McIntosh A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors J. Biol. Chem. 271 1996 7522 7528
133. J.M. Hill, C.J. Oomen, L.P. Miranda, J.P. Bingham, P.F. Alewood, and D.J. Craik Three-dimensional solution structure of alpha-conotoxin MII by NMR spectroscopy: effects of solution environment on helicity Biochemistry 37 1998 15621 15630
134. L. Zhang, and G. Bulaj Converting peptides into drug leads by lipidation Curr. Med. Chem. 19 2012 1602 1618
135. F.M. Veronese, and A. Mero The impact of PEGylation on biological therapies BioDrugs 22 2008 315 329
136. W. Cheng, and L.Y. Lim Design, synthesis, characterization and in-vivo activity of a novel salmon calcitonin conjugate containing a novel PEG-lipid moiety J. Pharm. Pharmacol. 62 2010 296 304
137. I.F. Toth, N. Filinn, A. Hillery, W.A. Gibbons, and P. Artursson Lipidic conjugates of luteinizing hormone releasing hormone and thyrotropin releasing hormone that release and protect the native hormones in homogenates of human intestinal epithelial (Caco-2) cells Int. J. Pharm. 105 1994 241 247
138. K. Tanaka, T. Fujita, Y. Yamamoto, M. Murakami, A. Yamamoto, and S. Muranishi Enhancement of intestinal transport of thyrotropin-releasing hormone via a carrier-mediated transport system by chemical modification with lauric acid Biochim. Biophys. Acta 1283 1996 119 126
139. J.T. Blanchfield, O.P. Gallagher, C. Cros, R.J. Lewis, P.F. Alewood, and I. Toth Oral absorption and in vivo biodistribution of alpha-conotoxin MII and a lipidic analogue Biochem. Biophys. Res. Commun. 361 2007 97 102
140. C.N. Carrigan, and B. Imperiali The engineering of membrane-permeable peptides Anal. Biochem. 341 2005 290 298
141. F. Borras-Cuesta, A. Petit-Camurdan, and Y. Fedon Engineering of immunogenic peptides by co-linear synthesis of determinants recognized by B and T cells Eur. J. Immunol. 17 1987 1213 1215
142. B.G. Stiles, and J.D. Ashcom Characterization of alpha-conotoxin interactions with the nicotinic acetylcholine receptor and monoclonal antibodies Biochem. J. 328 1997 245 250
143. J.M. Carter Techniques for conjugation of synthetic peptides to carrier molecules Methods Mol. Biol. 36 1994 155 191
144. B.G. Stiles, and F.W. Sexton Immunoreactivity, epitope mapping and protection studies with anti-conotoxin GI sera and various conotoxins Toxicon 30 1992 367 377
145. D. Tombaccini, O.M. Adeyemo, H.B. Pollard, and G. Feuerstein Monoclonal antibodies against the presynaptic calcium channel antagonist omega-conotoxin GVI A from cone snail poison FEBS Lett. 261 1990 71 75
146. O.M. Adeyemo, S. Shapira, D. Tombaccini, H.B. Pollard, G. Feuerstein, and A.L. Siren A goldfish model for evaluation of the neurotoxicity of omega-conotoxin GVIA and screening of monoclonal antibodies Toxicol. Appl. Pharmacol. 108 1991 489 496
147. 5]mu-conotoxin GIIIA sitespecifically conjugated with bovine serum albumin Biochem. Biophys. Res. Commun. 290 2002 1037 1041
148. L. Maus, J.P. Spatz, and R. Fiammengo Quantification and reactivity of functional groups in the ligand shell of PEGylated gold nanoparticles via a fluorescence-based assay Langmuir 25 2009 7910 7917
149. L. Maus, O. Dick, H. Bading, J.P. Spatz, and R. Fiammengo Conjugation of peptides to the passivation shell of gold nanoparticles for targeting of cell-surface receptors ACS Nano 4 2010 6617 6628
150. D.W. Sandall, N. Satkunanathan, D.A. Keays, M.A. Polidano, X. Liping, V. Pham, J.G. Down, Z. Khalil, B.G. Livett, and K.R. Gayler 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 2003 6904 6911
151. N. Satkunanathan, B. Livett, K. Gayler, D. Sandall, J. Down, and Z. Khalil Alpha-conotoxin Vc1.1 alleviates neuropathic pain and accelerates functional recovery of injured neurones Brain Res. 1059 2005 149 158
152. R.J. Lewis Conotoxin venom peptide therapeutics Adv. Exp. Med. Biol. 655 2009 44 48
153. S.T. Nevin, R.J. Clark, H. Klimis, M.J. Christie, D.J. Craik, and D.J. Adams Are alpha9alpha10 nicotinic acetylcholine receptors a pain target for alpha-conotoxins? Mol. Pharmacol. 72 2007 1406 1410
154. B.B. Carstens, R.J. Clark, N.L. Daly, P.J. Harvey, Q. Kaas, and D.J. Craik Engineering of conotoxins for the treatment of pain Curr. Pharm. Des. 17 2011 4242 4253
155. M.R. Plan, K.J. Rosengren, L. Sando, N.L. Daly, and D.J. Craik Structural and biochemical characteristics of the cyclotide kalata B5 from Oldenlandia affinis Biopolymers 94 2010 647 658
156. R.J. Clark, and D.J. Craik Native chemical ligation applied to the synthesis and bioengineering of circular peptides and proteins Biopolymers 94 2010 414 422
157. R.J. Clark, J. Jensen, S.T. Nevin, B.P. Callaghan, D.J. Adams, and D.J. Craik The engineering of an orally active conotoxin for the treatment of neuropathic pain Angew. Chem. Int. Ed. Engl. 49 2010 6545 6548
158. C.J. Armishaw, J.L. Dutton, D.J. Craik, and P.F. Alewood Establishing regiocontrol of disulfide bond isomers of alpha-conotoxin ImI via the synthesis of N-to-C cyclic analogs Biopolymers 94 2010 307 313
159. E.S. Lovelace, S. Gunasekera, C. Alvarmo, R.J. Clark, S.T. Nevin, A.A. Grishin, D.J. Adams, D.J. Craik, and N.L. Daly Stabilization of alpha-conotoxin AuIB: influences of disulfide connectivity and backbone cyclization Antioxid. Redox Signal. 14 2011 87 95
160. R. Halai, B. Callaghan, N.L. Daly, R.J. Clark, D.J. Adams, and D.J. Craik Effects of cyclization on stability, structure, and activity of alpha-conotoxin RgIA at the alpha9alpha10 nicotinic acetylcholine receptor and GABA(B) receptor J. Med. Chem. 54 2011 6984 6992
161. J.P. Bingham, N.M. Broxton, B.G. Livett, J.G. Down, A. Jones, and E.G. Moczydlowski Optimizing the connectivity in disulfide-rich peptides: alpha-conotoxin SII as a case study Anal. Biochem. 338 2005 48 61
162. E.S. Lovelace, C.J. Armishaw, M.L. Colgrave, M.E. Wahlstrom, P.F. Alewood, N.L. Daly, and D.J. Craik Cyclic MrIA: a stable and potent cyclic conotoxin with a novel topological fold that targets the norepinephrine transporter J. Med. Chem. 49 2006 6561 6568
163. P.E. Dawson, T.W. Muir, I. Clark-Lewis, and S.B. Kent Synthesis of proteins by native chemical ligation Science 266 1994 776 779
164. T.M. Hackeng, J.H. Griffin, and P.E. Dawson Protein synthesis by native chemical ligation: expanded scope by using straight forward methodology Proc. Natl. Acad. Sci. USA 96 1999 10068 10073
165. A. Dirksen, and P.E. Dawson Expanding the scope of chemoselective peptide ligations in chemical biology Curr. Opin. Chem. Biol. 12 2008 760 766
166. J.P. Tam, J. Xu, and K.D. Eom Methods and strategies of peptide ligation Biopolymers 60 2001 194 205
167. T.W. Muir, P.E. Dawson, and S.B. Kent Protein synthesis by chemical ligation of unprotected peptides in aqueous solution Methods Enzymol. 289 1997 266 298
168. Z. Dekan, F.A. Paczkowski, R.J. Lewis, and P.F. Alewood Synthesis and in vitro biological activity of cyclic lipophilic chi-conotoxin MrIA analogues Int. J. Pept. Res. Ther. 13 2007 307 312
169. L.S. Wermelinger, R.B. Geraldo, F.S. Frattani, C.R. Rodrigues, M.A. Juliano, H.C. Castro, and R.B. Zingali Integrin inhibitors from snake venom: exploring the relationship between the structure and activity of RGD-peptides Arch. Biochem. Biophys. 482 2009 25 32
170. C.Y. Koh, and R.M. Kini From snake venom toxins to therapeutics- cardiovascular examples Toxicon 59 2012 497 506
171. T. Yamamoto, and A. Takahara Recent updates of N-type calcium channel blockers with therapeutic potential for neuropathic pain and stroke Curr. Top. Med. Chem. 9 2009 377 395
172. B. Callaghan, A. Haythornthwaite, G. Berecki, R.J. Clark, D.J. Craik, and D.J. Adams Analgesic alpha-conotoxins Vc1.1 and Rg1A inhibit N-type calcium channels in rat sensory neurons via GABAB receptor activation J. Neurosci. 28 2008 10943 10951
173. C. Contet, B.L. Kieffer, and K. Befort Mu opioid receptor: a gateway to drug addiction Curr. Opin. Neurobiol. 14 2004 370 378
174. R.J. Clark, H. Fischer, S.T. Nevin, D.J. Adams, and D.J. Craik The synthesis, structural characterization, and receptor specificity of the alpha-conotoxin Vc1.1 J. Biol. Chem. 281 2006 23254 23263
175. I.E. Kasheverov, M.N. Zhmak, A.Y. Khruschov, and V.I. Tsetlin Design of new alpha-conotoxins: from computer modeling to synthesis of potent cholinergic compounds Mar. Drugs 9 2011 1698 1714
176. A.D. de Araujo, B. Callaghan, S.T. Nevin, N.L. Daly, D.J. Craik, M. Moretta, G. Hopping, M.J. Christie, D.J. Adams, and P.F. Alewood Total synthesis of the analgesic conotoxin MrVIB through selenocysteine-assisted folding Angew Chem. Int. Ed. Engl. 50 2011 6527 6529
177. Y.N. Utkin, M.N. Zhmak, C. Methfessel, and V.I. Tsetlin Aromatic substitutions in alpha-conotoxin ImI. Synthesis of iodinated photoactivatable derivative Toxicon 37 1999 1683 1695
178. P.A. Quiram, and S.M. Sine Structural elements in alpha-conotoxin ImI essential for binding to neuronal alpha7 receptors J. Biol. Chem. 273 1998 11007 11011
179. A.d. Araujo, B. Callaghan, S.T. Nevin, N.L. Daly, D.J. Craik, M. Moretta, G. Hopping, M.J. Christie, D.J. Addams, and P.F. Alewood Total synthesis of the analgesic conotoxin MrVIB through selenocystine-assisted folding Angew. Chem. Int. Ed. 50 2011 11007 11011
180. J.M. McIntosh, A. Hasson, M.E. Spira, W.R. Gray, W. Li, M. Marsh, D.R. Hillyard, and B.M. Olivera A new family of conotoxins that blocks voltage-gated sodium channels J. Biol. Chem. 270 1995 16796 16802
181. G. Bulaj, P.J. West, J.E. Garrett, M. Watkins, M.M. Zhang, R.S. Norton, B.J. Smith, D. Yoshikami, and B.M. Olivera Novel conotoxins from Conus striatus and Conus kinoshitai selectively block TTX-resistant sodium channels Biochemistry 44 2005 7259 7265
182. J.T. Blanchfield, J.L. Dutton, R.C. Hogg, O.P. Gallagher, D.J. Craik, A. Jones, D.J. Adams, R.J. Lewis, P.F. Alewood, and I. Toth Synthesis, structure elucidation, in vitro biological activity, toxicity, and Caco-2 cell permability of lipophilic analogues of alpha-conotoxin MII J. Med. Chem. 46 2003 1266 1272
183. W.R. Gray, B.M. Olivera, and L.J. Cruz Peptide toxins from venomous Conus snails Annu. Rev. Biochem. 57 1988 665 700
184. 2+ channels in hippocampal CA1 neurons Science 244 1989 1189 1193
185. P.K. Bandyopadhyay, C.J. Colledge, C.S. Walker, L.M. Zhou, D.R. Hillyard, and B.M. Olivera Conantokin-G precursor and its role in gamma-carboxylation by a vitamin K-dependent carboxylase from a Conus snail J. Biol. Chem. 273 1998 5447 5450
186. R.J. Clark, M. Akcan, Q. Kaas, N.L. Daly, and D.J. Craik Cyclization of conotoxins to improve their biopharmaceutical properties Toxicon 59 2012 446 455
187. R. Halai, R.J. Clark, S.T. Nevin, J.E. Jensen, D.J. Adams, and D.J. Craik Scanning mutagenesis of alpha-conotoxin Vc1.1 reveals residues crucial for activity at the alpha9alpha10 nicotinic acetylcholine receptor J. Biol. Chem. 284 2009 20275 20284
188. K.J. Nielsen, D. Adams, L. Thomas, T. Bond, P.F. Alewood, D.J. Craik, and R.J. Lewis Structure-activity relationships of omega-conotoxins MVIIA, MVIIC and 14 loop splice hybrids at N and P/Q-type calcium channels J. Mol. Biol. 289 1999 1405 1421
189. T.P. Snutch, Substituted piperazine and piperidine calcium channel blockers, in: A. Patents (Ed.), Australia, 2001.