Recent progress towards pharmaceutical applications of disulfide-rich cyclic peptides

Current Protein and Peptide Science

Volumn 14, Issue 6, 2013, Pages 532-542

  Schroeder, Christina I ^a   Swedberg, Joakim E ^a   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Conotoxins; Cyclic peptides; Cyclization; Cyclotides; Drug design; Pain

Indexed keywords

CONOTOXIN; CYCLOPEPTIDE; CYCLOTIDE; DISULFIDE;

ARTICLE; BIOLOGICAL ACTIVITY; CYCLIZATION; DRUG CLASSIFICATION; DRUG DESIGN; DRUG MECHANISM; DRUG NOMENCLATURE; DRUG SYNTHESIS; HUMAN; MEMBRANE BINDING; MOLECULAR DYNAMICS; NEUROPATHIC PAIN; NONHUMAN; PROTEIN ENGINEERING; STRUCTURE ACTIVITY RELATION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DEVELOPMENT; METABOLISM; NEURALGIA;

ANIMALS; CONOTOXINS; CYCLOTIDES; DISULFIDES; DRUG DISCOVERY; HUMANS; MODELS, MOLECULAR; NEURALGIA; PEPTIDES, CYCLIC; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84888246027     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/13892037113149990069     Document Type: Article

References (107)

1. Craik, D.J. Discovery and applications of the plant cyclotides. Toxicon, 2010, 56, 1092-1102.
2. Craik, D.J.; Henriques, S.T.; Mylne, J.S.; Wang, C.K. Cyclotide isolation and characterization. In: Methods in Enzymology, Hopwood, D., Ed. Academic Press: Maryland Heights, USA, 2012; Vol. 516, pp. 37-62.
3. Ireland, D.C.; Clark, R.J.; Daly, N.L.; Craik, D.J. Isolation, sequencing, and structure-activity relationships of cyclotides. J. Nat. Prod., 2010, 73, 1610-1622.
4. Colgrave, M.L.; Poth, A.G.; Kaas, Q.; Craik, D.J. A new "era" for cyclotide sequencing. Biopolymers Pept. Sci., 2010, 94, 592-601.
5. Kaas, Q.; Craik, D.J. Analysis and classification of circular proteins in CyBase. Biopolymers Pept. Sci., 2010, 94, 584-591.
6. Craik, D.J.; Conibear, A.C. The chemistry of cyclotides. J. Org. Chem., 2011, 76, 4805-4817.
7. Daly, N.; Gruber, C.; Göransson, U.; Craik, D. Cystine knot folding in cyclotides. In: Folding of disulfide proteins, Chang, R.J.Y.; Ventura, S., Eds.; Springer: New York, USA, 2011; Vol. 14, pp. 43-61.
8. Craik, D.J. Host-defense activities of cyclotides. Toxins, 2012, 4, 139-156.
9. Henriques, S.T.; Craik, D.J. Importance of the cell membrane on the mechanism of action of cyclotides. ACS Chem. Biol., 2012, 7, 626-636.
10. Craik, D.; Mylne, J.; Daly, N. Cyclotides: macrocyclic peptides with applications in drug design and agriculture. Cell. Mol. Life Sci., 2010, 67, 9-16.
11. Smith, A.B.; Daly, N.L.; Craik, D.J. Cyclotides: a patent review. Expert Opin. Ther. Pat., 2011, 21, 1657-1672.
12. Henriques, S.T.; Craik, D.J. Cyclotides as templates in drug design. Drug Discov. Today, 2010, 15, 57-64.
13. Craik, D.J.; Swedberg, J.E.; Mylne, J.S.; Cemazar, M. Cyclotides as a basis for drug design. Expert Opin. Drug Discov., 2012, 7, 179-194.
14. Dörnenburg, H.; Craik, D.J. Cyclotides. In: Encyclopedia of Industrial Biotechnology, Flickinger, M.C., Ed. John Wiley & Sons, Inc.: Sussex, UK, 2009, Vol. 13, pp. 1849-1866.
15. Daly, N.; Rosengren, K.J.; Henriques, S.T.; Craik, D. NMR and protein structure in drug design: application to cyclotides and conotoxins. Eur. Biophys. J., 2011, 40, 359-370.
16. Kaas, Q.; Westermann, J.-C.; Craik, D.J. Conopeptide characterization and classifications: An analysis using ConoServer. Toxicon, 2010, 55, 1491-1509.
17. Akcan, M.; Craik, D.J. Conotoxin-based leads in drug design. In: Peptide Drug Discovery and Development, Castanho, M.; Santos, N.C., Eds.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2011; pp. 119-137.
18. Schroeder, C.I.; Craik, D.J. Therapeutic potential of conopeptides. Future Med. Chem., 2012, 4, 1243-1255.
19. Clark, R.J.; Akcan, M.; Kaas, Q.; Daly, N.L.; Craik, D.J. Cyclization of conotoxins to improve their biopharmaceutical properties. Toxicon, 2012, 59, 446-455.
20. Clark, R.J.; Craik, D.J. Engineering cyclic peptide toxins. In: Methods in Enzymology, Wittrup, K.D.; Gregory, L.V., Eds.; Academic Press: Maryland Heights, USA, 2012; Vol. 503, pp. 57-74.
21. Daly, N.L.; Craik, D.J. Conopeptides as novel options for pain management. Drugs of the Future, 2011, 36, 25-32.
22. Carstens, B.B.; Clark, R.J.; Daly, N.L.; Harvey, P.J.; Kaas, Q.; Craik, D.J. Engineering of conotoxins for the treatment of pain. Curr. Pharm. Des., 2011, 17, 4242-4253.
23. Cascales, L.; Craik, D.J. Naturally occurring circular proteins: distribution, biosynthesis and evolution. Org. Biomol. Chem., 2010, 8, 5035-5047.
24. Conlan, B.F.; Gillon, A.D.; Craik, D.J.; Anderson, M.A. Circular proteins and mechanisms of cyclization. Biopolymers Pept. Sci., 2010, 94, 573-583.
25. Thorstholm, L.; Craik, D.J. Discovery and applications of naturally occurring cyclic peptides. Drug Discovery Today: Technologies, 2012, 9, e13-e21.
26. Craik, D.J.; Allewell, N.M. Thematic minireview series on circular proteins. J. Biol. Chem., 2012, 287, 26999-27000.
27. Clark, R.J.; Craik, D.J. Native chemical ligation applied to the synthesis and bioengineering of circular peptides and proteins. Biopolymers Pept. Sci.,2010, 94, 414-422.
28. Conibear, A.C.; Craik, D.J. Chemical synthesis of naturallyoccurring cyclic mini-proteins from plants and animals. Isr. J. Chem., 2011, 51, 908-916.
29. Cemazar, M.; Kwon, S.; Mahatmanto, T.; Ravipati, A.S.; Craik, D.J. Discovery and applications of disulfide-rich cyclic peptides. Curr. Top. Med. Chem., 2012, 12, 1534-1545.
30. Craik, D.J. Protein folding: Turbo-charged crosslinking. Nat. Chem., 2012, 4, 600-602.
31. Daly, N.L.; Craik, D.J. Bioactive cystine knot proteins. Curr. Opin. Chem. Biol., 2011, 15, 362-368.
32. Craik, D.J. The folding of disulfide-rich proteins. Antioxid. Redox. Signal., 2011, 14, 61-64.
33. Westermann, J.-C.; Craik, D.J. Plant peptide toxins from nonmarine environments. In: Comprehensive Natural Products II, Mander, L.N.; Lui, H-W., Eds.; Elsevier: Oxford, UK, 2010; pp. 257-285.
34. Kaas, Q.; Westermann, J.-C.; Henriques, S.T.; Craik, D.J. Antimicrobial peptides in plants. In: Antimicrobial Peptides: Discovery, Design, and Novel Therapeutic Strategies, Wang, G., Ed. CABI: Oxfordshire, UK, 2010; pp. 40-71.
35. Conibear, A.C.; Daly, N.L.; Craik, D.J. Quantification of small cyclic disulfide-rich peptides. Biopolymers Pept. Sci., 2012, 98, 518-524.
36. Arnison, P.G.; Bibb, M.J.; Bierbaum, G.; Bowers, A.A.; Bugni, T.S.; Bulaj, G.; Camarero, J.A.; Campopiano, D.J.; Challis, G.L.; Clardy, J.; Cotter, P.D.; Craik, D.J.; Dawson, M.; Dittmann, E.; Donadio, S.; Dorrestein, P.C.; Entian, K.-D.; Fischbach, M.A.; Garavelli, J.S.; Goransson, U.; Gruber, C.W.; Haft, D.H.; Hemscheidt, T.K.; Hertweck, C.; Hill, C.; Horswill, A.R.; Jaspars, M.; Kelly, W.L.; Klinman, J.P.; Kuipers, O.P.; Link, A.J.; Liu, W.; Marahiel, M.A.; Mitchell, D.A.; Moll, G.N.; Moore, B.S.; Muller, R.; Nair, S.K.; Nes, I.F.; Norris, G.E.; Olivera, B.M.; Onaka, H.; Patchett, M.L.; Piel, J.; Reaney, M.J.T.; Rebuffat, S.; Ross, R.P.; Sahl, H.-G.; Schmidt, E.W.; Selsted, M.E.; Severinov, K.; Shen, B.; Sivonen, K.; Smith, L.; Stein, T.; Sussmuth, R.D.; Tagg, J.R.; Tang, G.-L.; Truman, A.W.; Vederas, J.C.; Walsh, C.T.; Walton, J.D.; Wenzel, S.C.; Willey, J.M.; van der Donk, W.A. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat. Prod. Rep., 2013, 30, 108-160.
37. Craik, D.J.; Daly, N.L.; Bond, T.; Waine, C. Plant cyclotides: A unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol., 1999, 294, 1327-1336.
38. Burman, R.; Gruber, C.W.; Rizzardi, K.; Herrmann, A.; Craik, D.J.; Gupta, M.P.; Göransson, U. Cyclotide proteins and precursors from the genus Gloeospermum: Filling a blank spot in the cyclotide map of Violaceae. Phytochemistry, 2010, 71, 13-20.
39. Tang, J.; Wang, C.K.; Pan, X.; Yan, H.; Zeng, G.; Xu, W.; He, W.; Daly, N.L.; Craik, D.J.; Tan, N. Isolation and characterization of cytotoxic cyclotides from Viola tricolor. Peptides, 2010, 31, 1434-1440.
40. Tang, J.; Wang, C.K.; Pan, X.; Yan, H.; Zeng, G.; Xu, W.; He, W.; Daly, N.L.; Craik, D.J.; Tan, N. Isolation and characterization of bioactive cyclotides from Viola labridorica. Helv. Chim. Acta, 2010, 93, 2287-2295.
41. He, W.; Chan, L.Y.; Zeng, G.; Daly, N.L.; Craik, D.J.; Tan, N. Isolation and characterization of cytotoxic cyclotides from Viola philippica. Peptides, 2011, 32, 1719-1723.
42. Poth, A.G.; Colgrave, M.L.; Philip, R.; Kerenga, B.; Daly, N.L.; Anderson, M.A.; Craik, D.J. Discovery of cyclotides in the Fabaceae pant family provides new insights into the cyclization, evolution, and distribution of circular proteins. ACS Chem. Biol., 2010, 6, 345-355.
43. Soares, J. Discovery of novel cyclotides. ACS Chem. Biol., 2012, 7, 6-11.
44. Poth, A.G.; Mylne, J.S.; Grassl, J.; Lyons, R.E.; Millar, A.H.; Colgrave, M.L.; Craik, D.J. Cyclotides associate with leaf vasculature and are the products of a novel precursor in Petunia (Solanaceae). J. Biol. Chem., 2012, 287, 27033-27046.
45. Jennings, C.; West, J.; Waine, C.; Craik, D.; Anderson, M. Biosynthesis and insecticidal properties of plant cyclotides: The cyclic knotted proteins from Oldenlandia affinis. Proc. Natl. Acad. Sci. U. S. A., 2001, 98, 10614-10619.
46. Poth, A.G.; Colgrave, M.L.; Lyons, R.E.; Daly, N.L.; Craik, D.J. Discovery of an unusual biosynthetic origin for circular proteins in legumes. Proc. Natl. Acad. Sci. U. S. A., 2011, 108, 10127-10132.
47. Nguyen, G.K.T.; Zhang, S.; Nguyen, N.T.K.; Nguyen, P.Q.T.; Chiu, M.S.; Hardjojo, A.; Tam, J.P. Discovery and characterization of novel cyclotides originated from chimeric precursors consisting of albumin-1 chain a and cyclotide domains in the Fabaceae family. J. Biol. Chem., 2011, 286, 24275-24287.
48. Mylne, J.S.; Chan, L.Y.; Chanson, A.H.; Daly, N.L.; Schaefer, H.; Bailey, T.L.; Nguyencong, P.; Cascales, L.; Craik, D.J. Cyclic peptides arising by evolutionary parallelism via asparaginylendopeptidase-mediated biosynthesis. Plant Cell, 2012, 24, 2765-2778.
49. Conlan, B.F.; Colgrave, M.L.; Gillon, A.D.; Guarino, R.; Craik, D.J.; Anderson, M.A. Insights into processing and cyclization events associated with biosynthesis of the cyclic peptide kalata B1. J. Biol. Chem., 2012, 287, 28037-28046.
50. Qin, Q.; McCallum, E.; Kaas, Q.; Suda, J.; Saska, I.; Craik, D.; Mylne, J. Identification of candidates for cyclotide biosynthesis and cyclisation by expressed sequence tag analysis of Oldenlandia affinis. BMC Genomics, 2010, 11, 111.
51. Mylne, J.S.; Wang, C.K.; van der Weerden, N.L.; Craik, D.J. Cyclotides are a component of the innate defense of Oldenlandia affinis. Biopolymers Pept. Sci., 2010, 94, 635-646.
52. Huang, Y.-H.; Colgrave, M.L.; Clark, R.J.; Kotze, A.C.; Craik, D.J. Lysine-scanning mutagenesis reveals an amendable face of the cyclotide kalata B1 for the optimization of nematocidal activity. J. Biol. Chem., 2010, 285, 10797-10805.
53. Colgrave, M.L.; Huang, Y.-H.; Craik, D.J.; Kotze, A.C. Cyclotide interactions with the nematode external surface. Antimicrob. Agents Chemother., 2010, 54, 2160-2166.
54. Pinto, M.F.S.; Fensterseifer, I.C.M.; Migliolo, L.; Sousa, D.A.; de Capdville, G.; Arboleda, J.W.; Colgrave, M.L.; Craik, D.J.; Magalhaes, B.S.; Dias, S.C.; Franco, O.L. Identification and structural characterization of a novel cyclotide with activity against an insect pest of sugar cane. J. Biol. Chem., 2011, 287, 134-147.
55. Sando, L.; Henriques, S.T.; Foley, F.; Simonsen, S.M.; Daly, N.L.; Hall, K.N.; Gustafson, K.R.; Aguilar, M.-I.; Craik, D.J. A synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor. Chembiochem, 2011, 12, 2456-2462.
56. Henriques, S.T.; Huang, Y.-H.; Rosengren, K.J.; Franquelim, H.G.; Carvalho, F.A.; Johnson, A.; Sonza, S.; Tachedjian, G.; Castanho, M.A.R.B.; Daly, N.L.; Craik, D.J. Decoding the membrane activity of the cyclotide kalata B1: The importance of phosphatidylethanolamine phospholipids and lipid organization on hemolytic and anti-HIV activities. J. Biol. Chem., 2011, 286, 24231-24241.
57. Hall, K.; Lee, T.-H.; Daly, N.L.; Craik, D.J.; Aguilar, M.-I. Gly6 of kalata B1 is critical for the selective binding to phosphatidylethanolamine membranes. Biochim. Biophys. Acta, 2012, 1818, 2354-2361.
58. Henriques, S.T.; Huang, Y.-H.; Castanho, M.A.R.B.; Bagatolli, L.A.; Sonza, S.; Tachedjian, G.; Daly, N.L.; Craik, D.J. Phosphatidylethanolamine binding is a conserved feature of cyclotide-membrane interactions. J. Biol. Chem., 2012, 287, 33629-33643.
59. Wang, C.K.; Wacklin, H.P.; Craik, D.J. Cyclotides insert into lipid bilayers to form membrane pores and destabilize the membrane through hydrophobic and phosphoethanolamine-specific interactions. J. Biol. Chem., 2012, 287, 43884-43898.
60. Aboye, T.L.; Clark, R.J.; Burman, R.; Roig, M.B.; Craik, D.J.; Göransson, U. Interlocking disulfides in circular proteins: Toward efficient oxidative folding of cyclotides. Antioxid. Redox. Signal., 2011, 14, 77-86.
61. Daly, N.L.; Chen, B.; Nguyencong, P.; Craik, D.J. Structure and activity of the leaf-specific cyclotide vhl-2. Aust. J. Chem., 2010, 63, 771-778.
62. Plan, M.R.; Rosengren, K.J.; Sando, L.; Daly, N.L.; Craik, D.J. Structural and biochemical characteristics of the cyclotide kalata B5 from Oldenlandia affinis. Biopolymers Pept. Sci., 2010, 94, 647-658.
63. Wang, C.K.L.; Clark, R.J.; Harvey, P.J.; Johan Rosengren, K.; Cemazar, M.; Craik, D.J. The role of conserved Glu residue on cyclotide stability and activity: A structural and functional study of kalata B12, a naturally occurring Glu to Asp mutant. Biochemistry, 2011, 50, 4077-4086.
64. Burman, R.; Svedlund, E.; Felth, J.; Hassan, S.; Herrmann, A.; Clark, R.J.; Craik, D.J.; Bohlin, L.; Claeson, P.; Göransson, U.; Gullbo, J. Evaluation of toxicity and antitumor activity of cycloviolacin O2 in mice. Biopolymers Pept. Sci., 2010, 94, 626-634.
65. Gunasekera, S.; Foley, F.M.; Clark, R.J.; Sando, L.; Fabri, L.J.; Craik, D.J.; Daly, N.L. Engineering stabilized vascular endothelial growth factor-A antagonists: Synthesis, structural characterization, and bioactivity of grafted analogues of cyclotides. J. Med. Chem., 2008, 51, 7697-7704.
66. Chan, L.Y.; Gunasekera, S.; Henriques, S.T.; Worth, N.F.; Le, S.-J.; Clark, R.J.; Campbell, J.H.; Craik, D.J.; Daly, N.L. Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds. Blood, 2011, 118, 6709-6717.
67. Eliasen, R.; Daly, N.L.; Wulff, B.S.; Andresen, T.L.; Conde-Frieboes, K.W.; Craik, D.J. Design, synthesis, structural and functional characterization of novel melanocortin agonists based on the cyclotide kalata B1. J. Biol. Chem., 2012, 287, 40493-40501.
68. Cascales, L.; Henriques, S.T.; Kerr, M.C.; Huang, Y.-H.; Sweet, M.J.; Daly, N.L.; Craik, D.J. Identification and characterization of a new family of cell-penetrating peptides: Cyclic cell-penetrating peptides. J. Biol. Chem., 2011, 286, 36932-36943.
69. Terlau, H.; Olivera, B.M. Conus venoms: A rich source of novel ion channel-targeted peptides. Physiol. Rev., 2004, 84, 41-68.
70. Hu, S.-H.; Gehrmann, J.; Alewood, P.F.; Craik, D.J.; Martin, J.L. Crystal structure at 1.1 Å resolution of α-conotoxin PnIB: Comparison with α-conotoxins PnIA and GI. Biochemistry, 1997, 36, 11323-11330.
71. Scanlon, M.J.; Naranjo, D.; Thomas, L.; Alewood, P.F.; Lewis, R.J.; Craik, D.J. Solution structure and proposed binding mechanism of a novel potassium channel toxin kappa-conotoxin PVIIA. Structure, 1997, 5, 1585-1597.
72. Nielsen, K.J.; Thomas, L.; Lewis, R.J.; Alewood, P.F.; Craik, D.J. A consensus structure for ω-conotoxins with different selectivities for voltage-sensitive calcium channel subtypes: Comparison of MVIIA, SVIB and SNX-202. J. Mol. Biol., 1996, 263, 297-310.
73. Skjærbæk, N.; Nielsen, K.J.; Lewis, R.J.; Alewood, P.; Craik, D.J. Determination of the solution structures of conantokin-G and conantokin-T by CD and NMR spectroscopy. J. Biol. Chem., 1997, 272, 2291-2299.
74. Kaas, Q.; Westermann, J.-C.; Halai, R.; Wang, C.K.L.; Craik, D.J. ConoServer, a database for conopeptide sequences and structures. Bioinformatics, 2008, 24, 445-446.
75. Kaas, Q.; Yu, R.; Jin, A.-H.; Dutertre, S.; Craik, D.J. ConoServer: updated content, knowledge, and discovery tools in the conopeptide database. Nucleic Acids Res., 2012, 40, D325-D330.
76. Callaghan, B.; Haythornthwaite, A.; Berecki, G.; Clark, R.J.; Craik, D.J.; Adams, D.J. Analgesic α-conotoxins Vc1.1 and Rg1A inhibit N-type calcium channels in rat sensory neurons via GABAB receptor activation. J. Neurosci., 2008, 28, 10943-10951.
77. Luo, S.; Akondi, K.B.; Zhangsun, D.; Wu, Y.; Zhu, X.; Hu, Y.; Christensen, S.; Dowell, C.; Daly, N.L.; Craik, D.J.; Wang, C.-I.A.; Lewis, R.J.; Alewood, P.F.; Michael McIntosh, J. Atypical α-conotoxin LtIA from Conus litteratus targets a novel microsite of the α3β2 nicotinic receptor. J. Biol. Chem., 2010, 285, 12355-12366.
78. Daly, N.L.; Callaghan, B.; Clark, R.J.; Nevin, S.T.; Adams, D.J.; Craik, D.J. Structure and activity of α-conotoxin PeIA at nicotinic acetylcholine receptor subtypes and GABAB receptor-coupled Ntype calcium channels. J. Biol. Chem., 2011, 286, 10233-10237.
79. Franco, A.; Kompella, S.N.; Akondi, K.B.; Melaun, C.; Daly, N.L.; Luetje, C.W.; Alewood, P.F.; Craik, D.J.; Adams, D.J.; Marí, F. RegIIA: An α4/7-conotoxin from the venom of Conus regius that potently blocks α3β4 nAChRs. Biochem. Pharmacol., 2012, 83, 419-426.
80. Luo, S.; Zhangsun, D.; Wu, Y.; Zhu, X.; Hu, Y.; McIntyre, M.; Christensen, S.; Akcan, M.; Craik, D.J.; McIntosh, J.M. Characterization of a novel alpha-conotoxin from Conus textile that selectively targets α6/α3β2β3 nicotinic acetylcholine receptors. J. Biol. Chem., 2013, 288, 894-902.
81. 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.A.; Lewis, R.J.; Martin, J.L.; Noakes, P.G.; Craik, D.J.; Adams, D.J.; Alewood, P.F. Solving the α-conotoxin folding problem: Efficient selenium-directed on-resin generation of more potent and stable nicotinic acetylcholine receptor antagonists. J. Am. Chem. Soc., 2010, 132, 3514-3522.
82. de Araujo, A.D.; Callaghan, B.; Nevin, S.T.; Daly, N.L.; Craik, D.J.; Moretta, M.; Hopping, G.; Christie, M.J.; Adams, D.J.; Alewood, P.F. Total synthesis of the analgesic conotoxin MrVIB through selenocysteine-assisted folding. Angew. Chem. Int. Ed. Engl., 2011, 50, 6527-6529.
83. Dekan, Z.; Vetter, I.; Daly, N.L.; Craik, D.J.; Lewis, R.J.; Alewood, P.F. α-Conotoxin ImI incorporating stable cystathionine bridges maintains full potency and identical three-dimensional structure. J. Am. Chem. Soc., 2011, 133, 15866-15869.
84. Halai, R.; Clark, R.J.; Nevin, S.T.; Jensen, J.E.; Adams, D.J.; Craik, D.J. Scanning mutagenesis of α-conotoxin Vc1.1 reveals residues crucial for activity at the α9α10 nicotinic acetylcholine receptor. J. Biol. Chem., 2009, 284, 20275-20284.
85. Schroeder, C.I.; Nielsen, K.J.; Adams, D.A.; Loughnan, M.; Thomas, L.; Alewood, P.F.; Lewis, R.J.; Craik, D.J. Effects of Lys2 to Ala2 substitutions on the structure and potency of omegaconotoxins MVIIA and CVID. Biopolymers Pept. Sci., 2012, 98, 345-356.
86. Schroeder, C.I.; Adams, D.; Thomas, L.; Alewood, P.F.; Lewis, R.J. N-and c-terminal extensions of μ-conotoxins increase potency and selectivity for neuronal sodium channels. Biopolymers Pept. Sci., 2012, 98, 161-165.
87. Yu, R.; Craik, D.J.; Kaas, Q. Blockade of neuronal α7-nAChR by α-conotoxin ImI explained by computational scanning and energy calculations. PLoS Comput. Biol., 2011, 7, e1002011.
88. Yu, R.; Kaas, Q.; Craik, D.J. Delineation of the unbinding pathway of α-conotoxin ImI from the α7 nicotinic acetylcholine receptor. J. Phys. Chem. B, 2012, 116, 6097-6105.
89. Colgrave, M.L.; Craik, D.J. Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: The importance of the cyclic cystine knot. Biochemistry, 2004, 43, 5965-5975.
90. Clark, R.J.; Fischer, H.; Dempster, L.; Daly, N.L.; Rosengren, K.J.; Nevin, S.T.; Meunier, F.A.; Adams, D.J.; Craik, D.J. Engineering stable peptide toxins by means of backbone cyclization: Stabilization of the α-conotoxin MII. Proc. Natl. Acad. Sci. U. S. A., 2005, 102, 13767-13772.
91. Clark, R.J.; Jensen, J.; Nevin, S.T.; Callaghan, B.P.; Adams, D.J.; Craik, D.J. The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angew. Chem. Int. Ed. Engl., 2010, 49, 6545-6548.
92. Armishaw, C.J.; Dutton, J.L.; Craik, D.J.; Alewood, P.F. Establishing regiocontrol of disulfide bond isomers of α-conotoxin ImI via the synthesis of N-to-C cyclic analogs. Biopolymers Pept. Sci., 2010, 94, 307-313.
93. Lovelace, E.S.; Gunasekera, S.; Alvarmo, C.; Clark, R.J.; Nevin, S.T.; Grishin, A.A.; Adams, D.J.; Craik, D.J.; Daly, N.L. Stabilization of α-conotoxin AuIB: Influences of disulfide connectivity and backbone cyclization. Antioxid. Redox. Signal., 2010, 14, 87-95.
94. Halai, R.; Callaghan, B.; Daly, N.L.; Clark, R.J.; Adams, D.J.; Craik, D.J. Effects of cyclization on stability, structure, and activity of α-conotoxin RgIA at the α9α10 nicotinic acetylcholine receptor and GABAB receptor. J. Med. Chem., 2011, 54, 6984-6992.
95. Akcan, M.; Stroud, M.R.; Hansen, S.J.; Clark, R.J.; Daly, N.L.; Craik, D.J.; Olson, J.M. Chemical re-engineering of chlorotoxin improves bioconjugation properties for tumor imaging and targeted therapy. J. Med. Chem., 2011, 54, 782-787.
96. Colgrave, M.L.; Korsinczky, M.J.L.; Clark, R.J.; Foley, F.; Craik, D.J. Sunflower trypsin inhibitor-1, proteolytic studies on a trypsin inhibitor peptide and its analogs. Biopolymers Pept. Sci., 2010, 94, 665-672.
97. Yuan, C.; Chen, L.; Meehan, E.; Daly, N.; Craik, D.; Huang, M.; Ngo, J. Structure of catalytic domain of matriptase in complex with sunflower trypsin inhibitor-1. BMC Struct. Biol., 2011, 11, 30.
98. Mylne, J.S.; Colgrave, M.L.; Daly, N.L.; Chanson, A.H.; Elliott, A.G.; McCallum, E.J.; Jones, A.; Craik, D.J. Albumins and their processing machinery are hijacked for cyclic peptides in sunflower. Nat. Chem. Biol., 2011, 7, 257-259.
99. Marx, U.C.; Korsinczky, M.L.J.; Schirra, H.J.; Jones, A.; Condie, B.; Otvos, L.; Craik, D.J. Enzymatic cyclization of a potent Bowman-Birk protease inhibitor, sunflower trypsin inhibitor-1, and solution structure of an acyclic precursor peptide. J. Biol. Chem., 2003, 278, 21782-21789.
100. Schirra, H.J.; Guarino, R.F.; Anderson, M.A.; Craik, D.J. Selective removal of individual disulfide bonds within a potato type II serine proteinase inhibitor from Nicotiana alata reveals differential stabilization of the reactive-site loop. J. Mol. Biol., 2010, 395, 609-626.
101. Dunse, K.M.; Kaas, Q.; Guarino, R.F.; Barton, P.A.; Craik, D.J.; Anderson, M.A. Molecular basis for the resistance of an insect chymotrypsin to a potato type II proteinase inhibitor. Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 15016-15021.
102. Zhu, S.; Gao, B.; Harvey, P.J.; Craik, D.J. Dermatophytic defensin with antiinfective potential. Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 8495-8500.
103. Andersson, H.; Figueredo, S.; Haugaard-Kedström, L.; Bengtsson, E.; Daly, N.; Qu, X.; Craik, D.; Ouellette, A.; Rosengren, K.J. The α-defensin salt-bridge induces backbone stability to facilitate folding and confer proteolytic resistance. Amino Acids, 2012, 43, 1471-1483.
104. Conibear, A.C.; Rosengren, K.J.; Harvey, P.J.; Craik, D.J. Structural characterization of the cyclic cystine ladder motif of θ-defensins. Biochemistry, 2012, 51, 9718-9726.
105. Clark, Richard J.; Tan, Chia C.; Preza, Gloria C.; Nemeth, E.; Ganz, T.; Craik, David J. Understanding the structure/activity relationships of the iron regulatory peptide hepcidin. Chem. Biol., 2011, 18, 336-343.
106. Haugaard-Kedström, L.M.; Shabanpoor, F.; Hossain, M.A.; Clark, R.J.; Ryan, P.J.; Craik, D.J.; Gundlach, A.L.; Wade, J.D.; Bathgate, R.A.D.; Rosengren, K.J. Design, synthesis, and characterization of a single-chain peptide antagonist for the relaxin-3 receptor RXFP3. J. Am. Chem. Soc., 2011, 133, 4965-4974.
107. Craik, D.J.; Fairlie, D.P.; Liras, S.; Price, D. The future of peptidebased drugs. Chem. Biol. Drug Des., 2013, 81, 136-147.