Discovery and applications of disulfide-rich cyclic peptides

Current Topics in Medicinal Chemistry

Volumn 12, Issue 14, 2012, Pages 1534-1545

  Cemazar, Masa ^a   Kwon, Soohyun ^a   Mahatmanto, Tunjung ^a   Ravipati, Anjaneya S ^a   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Chlorotoxin; Conotoxin; Cyclic peptides; Cyclotide; Kalata B1

Indexed keywords

CHLOROTOXIN; CIRCULIN DERIVATIVE; CONOTOXIN; CYCLOPEPTIDE; CYCLOPSYCHOTRIDE A; CYCLOTIDE; CYCLOVIOLACIN DERIVATIVE; DISULFIDE; KALATA DERIVATIVE; NATURAL PRODUCT; PALICOUREIN; PSYLE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGICAL ACTIVITY; CYCLIZATION; DRUG DESIGN; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NEUROPATHIC PAIN; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN STRUCTURE; PROTEIN TARGETING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; DISULFIDES; DRUG DISCOVERY; GLIOMA; HUMANS; MODELS, MOLECULAR; NEURALGIA; NEUROTOXINS; PEPTIDES, CYCLIC;

EID: 84866952842     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802612802652484     Document Type: Article

References (116)

1. Kovarik, J.M.; Kaplan, B.; Silva, H.T.; Kahan, B.D.; Dantal, J.; McMahon, L.; Berthier, S.; Hsu, C.H.; Rordorf, C. Pharmacokinetics of an everolimus-cyclosporine immunosuppressive regimen over the first 6 months after kidney transplantation. Am. J. Transplant., 2003, 3(5), 606-613.
2. Veber, D.F.; Johnson, S.R.; Cheng, H.Y.; Smith, B.R.; Ward, K.W.; Kopple, K.D. Molecular properties that influence the oral bioavailability of drug candidates. J. Med. Chem., 2002, 45(12), 2615-2623.
3. Trabi, M.; Craik, D.J. Circular proteins-no end in sight. Trends Biochem. Sci., 2002, 27 (3), 132-138.
4. Craik, D. J., Chemistry-Seamless proteins tie up their loose ends. Science 2006, 311(5767), 1563-1564.
5. Cascales, L.; Craik, D.J. Naturally occurring circular proteins: distribution, biosynthesis and evolution. Org. Biomol. Chem., 2010, 8(22), 5035-5047.
6. 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(5), 1327-1336.
7. Craik, D.J.; Daly, N.L.; Waine, C. The cystine knot motif in toxins and implications for drug design. Toxicon 2001, 39(1), 43-60.
8. Craik, D.J.; Cemazar, M.; Daly, N.L. The cyclotides and related macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Devel., 2006, 9(2), 251-260.
9. 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(9), 1610-1622.
10. Craik, D.J.; Conibear, A.C. The chemistry of cyclotides. J. Org. Chem., 2011, 76(12), 4805-4817.
11. Gran, L. An oxytocic principle found in Oldenlandia affinis DC. Meddelelser Norsk Farmasøytisk Selskap 1970, 12, 173-180.
12. Saether, O.; Craik, D.J.; Campbell, I.D.; Sletten, K.; Juul, J.; Norman, D.G. Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide Kalata B1. Biochemistry, 1995, 34(13), 4147-4158.
13. Gruber, C.W.; Cemazar, M.; Anderson, M.A.; Craik, D.J. Insecticidal plant cyclotides and related cystine knot toxins. Toxicon, 2007, 49(4), 561-575.
14. 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. USA, 2001, 98(19), 10614-10619.
15. Colgrave, M.L.; Kotze, A.C.; Kopp, S.; McCarthy, J.S.; Coleman, G.T.; Craik, D.J. Anthelmintic activity of cyclotides: In vitro studies with canine and human hookworms. Acta Trop., 2009, 109 (2), 163-166.
16. Gustafson, K.R.; Sowder, R.C.; Henderson, L.E.; Parsons, I.C.; Kashman, Y.; Cardellina, J.H.; McMahon, J.B.; Buckheit Jr, R.W.; Pannell, L.K.; Boyd, M.R. Circulins A and B. Novel human immunodeficiency virus (HIV)-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc., 1994, 116(20), 9337-9338.
17. Pranting, M.; Loov, C.; Burman, R.; Goransson, U.; Andersson, D.I. The cyclotide cycloviolacin O2 from Viola odorata has potent bactericidal activity against Gram-negative bacteria. J. Antimicrob. Chemother., 2010, 65(9), 1964-1971.
18. Tam, J.P.; Lu, Y.A.; Yang, J.L.; Chiu, K.W. An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides. Proc. Natl. Acad. Sci. USA, 1999, 96(16), 8913-8918.
19. Goransson, U.; Sjogren, M.; Svangard, E.; Claeson, P.; Bohlin, L. Reversible antifouling effect of the cyclotide cycloviolacin O2 against barnacles. J. Nat. Prod. 2004, 67(8), 1287-1290.
20. Svangard, E.; Goransson, U.; Hocaoglu, Z.; Gullbo, J.; Larsson, R.; Claeson, P.; Bohlin, L. Cytotoxic cyclotides from Viola tricolor. J. Nat. Prod., 2004, 67(2), 144-147.
21. Kamimori, H.; Hall, K.; Craik, D.J.; Aguilar, M.I. Studies on the membrane interactions of the cyclotides kalata B1 and kalata B6 on model membrane systems by surface plasmon resonance. Anal. Biochem., 2005, 337(1), 149-153.
22. 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 (27), 24231-24241.
23. Hall, K.; Lee, T.H.; Daly, N.L.; Craik, D.J.; Aguilar, M.I. Gly(6) of kalata B1 is critical for the selective binding to phosphatidylethanolamine membranes. Biochim. Biophys. Acta, 2012, (in press)
24. Gustafson, K.R.; Walton, L.K.; Sowder, R.C.; Johnson, D.G.; Pannell, L.K.; Cardellina, J.H.; Boyd, M.R. New circulin macrocyclic polypeptides from Chassalia parvifolia. J. Nat. Prod. 2000, 63(2), 176-178.
25. Hallock, Y.F.; Sowder, R.C.; Pannell, L.K.; Hughes, C.B.; Johnson, D.G.; Gulakowski, R.; Cardellina, J.H.; Boyd, M.R. Cycloviolins A-D, anti-HIV macrocyclic peptides from Leonia cymosa. J. Org. Chem., 2000, 65(1), 124-128.
26. Colgrave, M.L.; Kotze, A.C.; Ireland, D.C.; Wang, C.K.; Craik, D.J. The anthelmintic activity of the cyclotides: Natural variants with enhanced activity. Chembiochem, 2008, 9(12), 1939-1945.
27. Chen, B.; Colgrave, M.L.; Daly, N.L.; Rosengren, K.J.; Gustafson, K.R.; Craik, D.J. Isolation and characterization of novel cyclotides from Viola hederaceae-Solution structure and anti-HIV activity of vhl-1, a leaf-specific expressed cyclotide. J. Biol. Chem., 2005, 280(23), 22395-22405.
28. Wang, C.K.L.; Colgrave, M.L.; Gustafson, K.R.; Ireland, D.C.; Goransson, U.; Craik, D.J. Anti-HIV cyclotides from the Chinese medicinal herb Viola yedoensis. J. Nat. Prod., 2008, 71(1), 47-52.
29. Plan, M.R.R.; Saska, I.; Cagauan, A.G.; Craik, D.J. Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J. Agric. Food Chem., 2008, 56(13), 5237-5241.
30. Svangard, E.; Burman, R.; Gunasekera, S.; Lovborg, H.; Gullbo, J.; Goransson, U. Mechanism of action of cytotoxic cyclotides: Cycloviolacin O2 disrupts lipid membranes. J. Nat. Prod., 2007, 70(4), 643-647.
31. Ireland, D.C.; Colgrave, M.L.; Craik, D.J. A novel suite of cyclotides from Viola odorata: Sequence variation and the implications for structure, function and stability. Biochem. J., 2006, 400, 1-12.
32. Ireland, D.C.; Wang, C.K.L.; Wilson, J.A.; Gustafson, K.R.; Craik, D.J. Cyclotides as natural anti-HIV agents. Biopolymers, 2008, 90(1), 51-60.
33. Jennings, C.V.; Rosengren, K.J.; Daly, N.L.; Plan, M.; Stevens, J.; Scanlon, M.J.; Waine, C.; Norman, D. G.; Anderson, M.A.; Craik, D.J. Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: Do Mobius strips exist in nature? Biochemistry, 2005, 44(3), 851-860.
34. Daly, N.L.; Clark, R.J.; Plan, M.R.; Craik, D.J. Kalata B8, a novel antiviral circular protein, exhibits conformational flexibility in the cystine knot motif. Biochem. J., 2006, 393, 619-626.
35. Hernandez, J.F.; Gagnon, J.; Chiche, L.; Nguyen, T.M.; Andrieu, J.P.; Heitz, A.; Hong, T.T.; Pham, T.T. C.; Nguyen, D.L. Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure. Biochemistry, 2000, 39(19), 5722-5730.
36. Bokesch, H.R.; Pannell, L.K.; Cochran, P.K.; Sowder, R.C.; McKee, T.C.; Boyd, M.R. A novel anti-HIV macrocyclic peptide from Palicourea condensata. J. Nat. Prod., 2001, 64(2), 249-250.
37. Gerlach, S.L.; Rathinakumar, R.; Chakravarty, G.; Goransson, U.; Wimley, W.C.; Darwin, S.P.; Mondal, D. Anticancer and chemosensitizing abilities of cycloviolacin O2 from Viola odorata and psyle cyclotides from Psychotria leptothyrsa. Biopolymers, 2010, 94(5), 617-625.
38. Mulvenna, J.R.; Sando, L.; Craik, D.J. Processing of a 22 kDa precursor protein to produce the circular protein tricyclon A. Structure, 2005, 13(5), 691-701.
39. Lindholm, P.; Goransson, U.; Johansson, S.; Claeson, P.; Gullbo, J.; Larsson, R.; Bohlin, L.; Backlund, A. Cyclotides: A novel type of cytotoxic agents. Mol. Cancer Ther., 2002, 1(6), 365-369.
40. Herrmann, A.; Burman, R.; Mylne, J.S.; Karlsson, G.; Gullbo, J.; Craik, D.J.; Clark, R.J.; Goransson, U. The alpine violet, Viola biflora, is a rich source of cyclotides with potent cytotoxicity. Phytochemistry, 2008, 69(4), 939-952.
41. Mulvenna, J.P.; Wang, C.; Craik, D.J. CyBase: a database of cyclic protein sequence and structure. Nucleic Acids Res., 2006, 34 (Database issue), D192-194.
42. Wang, C.K.L.; Kaas, Q.; Chiche, L.; Craik, D.J. CyBase: A database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res., 2008, 36, D206-D210.
43. Claeson, P.; Goransson, U.; Johansson, S.; Luijendijk, T.; Bohlin, L. Fractionation Protocol for the Isolation of Polypeptides from Plant Biomass. J. Nat. Prod., 1998, 61(1), 77-81.
44. 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. USA, 2011, 108(25), 10127.
45. Gruber, C.W.; Elliott, A.G.; Ireland, D.C.; Delprete, P.G.; Dessein, S.; Goransson, U.; Trabi, M.; Wang, C. K.; Kinghorn, A.B.; Robbrecht, E.; Craik, D.J. Distribution and evolution of circular miniproteins in flowering plants. Plant Cell, 2008, 20(9), 2471-2483.
46. Poth, A.G.; Colgrave, M.L.; Philip, R.; Kerenga, B.; Daly, N.L.; Anderson, J.P.; Craik, D.J. Discovery of cyclotides in the Fabaceae plant family provides new insights into the cyclization, evolution, and distribution of circular proteins. ACS Chem. Biol., 2010, A-K.
47. 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(20), 5965-5975.
48. Dutton, J.L.; Renda, R.F.; Waine, C.; Clark, R.J.; Daly, N.L.; Jennings, C.V.; Anderson, M.A.; Craik, D.J. Conserved structural and sequence elements implicated in the processing of geneencoded circular proteins. J. Biol. Chem., 2004, 279(45), 46858-46867.
49. Mulvenna, J.P.; Mylne, J.S.; Bharathi, R.; Burton, R.A.; Shirley, N.J.; Fincher, G.B.; Anderson, M.A.; Craik, D.J. Discovery of cyclotide-like protein sequences in graminaceous crop plants: Ancestral precursors of circular proteins? Plant Cell, 2006, 18(9), 2134-2144.
50. Craik, D.J.; Mylne, J.S.; Daly, N.L. Cyclotides: macrocyclic peptides with applications in drug design and agriculture. Cell. Mol. Life Sci., 2010, 67(1), 9-16.
51. Giang, K.T.N.; Zhang, S.; Ngan, T.K.N.; Phuong, Q.T.N.; 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(27), 24275-24287.
52. Kaas, Q.; Craik, D.J. Analysis and classification of circular proteins in CyBase. Biopolymers, 2010, 94(5), 584-591.
53. Schneider, T.D.; Stephens, R.M., Sequence logos: A new way to display consensus sequences. Nucleic Acids Res., 1990, 18(20), 6097-6100.
54. Crooks, G.E.; Hon, G.; Chandonia, J.M.; Brenner, S.E. WebLogo: A sequence logo generator. Genome Res., 2004, 14(6), 1188-1190.
55. Pelegrini, P.B.; Quirino, B.F.; Franco, O.L. Plant cyclotides: An unusual class of defense compounds. Peptides 2007, 28(7), 1475-1481.
56. 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. J. Biol. Chem., 2011, 286(42), 36932-36943.
57. Luckett, S.; Garcia, R.S.; Barker, J.J.; Konarev, A.V.; Shewry, P.R.; Clarke, A.R.; Brady, R.L. High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J. Mol. Biol., 1999, 290(2), 525-533.
58. Korsinczky, M.L.J.; Schirra, H.J.; Rosengren, K.J.; West, J.; Condie, B.A.; Otvos, L.; Anderson, M.A.; Craik, D.J. Solution structures by H-1 NMR of the novel cyclic trypsin inhibitor SFTI-1 from sunflower seeds and an acyclic permutant. J. Mol. Biol., 2001, 311(3), 579-591.
59. Swedberg, J.E.; de Veer, S.J.; Sit, K.C.; Reboul, C.F.; Buckle, A.M.; Harris, J.M. Mastering the canonical loop of serine protease inhibitors: Enhancing potency by optimising the internal hydrogen bond network. PLoS ONE, 2011, 6(4).
60. Yuan, C.; Chen, L.; Meehan, E.J.; Daly, N.; Craik, D.J.; Huang, M.; Ngo, J.C. Structure of catalytic domain of Matriptase in complex with Sunflower trypsin inhibitor-1. BMC Struct. Biol., 2011, 11(1), 30.
61. Simonsen, S.M.; Sando, L.; Rosengren, K.J.; Wang, C.K.; Colgrave, M.L.; Daly, N.L.; Craik, D.J. Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem., 2008, 283(15), 9805-9813.
62. Bernkop-Schnurch, A. The use of inhibitory agents to overcome the enzymatic barrier to perorally administered therapeutic peptides and proteins. J. Control. Release, 1998, 52(1-2), 1-16.
63. Gilon, C.; Halle, D.; Chorev, M.; Selinger, Z.; Byk, G., Backbone cyclization: A new method for conferring conformational constraint on peptides. Biopolymers, 1991, 31(6), 745-750.
64. Craik, D.J.; Clark, R.J.; Daly, N.L. Potential therapeutic applications of the cyclotides and related cystine knot miniproteins. Expert Opin. Investig. Drugs, 2007, 16(5), 595-604.
65. Barry, D.G.; Daly, N.L.; Clark, R.J.; Sando, L.; Craik, D.J. Linearization of a naturally occurring circular protein maintains structure but eliminates hemolytic activity. Biochemistry, 2003, 42(22), 6688-6695.
66. 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(24), 7697-7704.
67. Thongyoo, P.; Bonomelli, C.; Leatherbarrow, R.J.; Tate, E.W. Potent inhibitors of β-tryptase and human leukocyte elastase based on the MCoTI-II scaffold. J. Med. Chem., 2009, 52, 6197-6200.
68. Thongyoo, P.; Roque-Rosell, N.; Leatherbarrow, R.J.; Tate, E.W. Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides. Org. Biomol. Chem., 2008, 6(8), 1462-1470.
69. 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(25), 6709-6717.
70. Sommerhoff, C.P.; Avrutina, O.; Schmoldt, H.U.; Gabrijelcic-Geiger, D.; Diederichsen, U.; Kolmar, H. Engineered cystine knot miniproteins as potent inhibitors of human mast cell tryptase β. J. Mol. Biol., 2010, 395(1), 167-175.
71. Agyei, D.; Danquah, M.K. Industrial-scale manufacturing of pharmaceutical-grade bioactive peptides. Biotechnol. Adv., 2011, 29(3), 272-277.
72. Korhonen, H. Milk-derived bioactive peptides: From science to applications. J. Funct. Foods, 2009,1(2), 177-187.
73. Huang, Y.H.; Colgrave, M.L.; Daly, N.L.; Keleshian, A.; Martinac, B.; Craik, D.J. The biological activity of the prototypic cyclotide kalata b1 is modulated by the formation of multimeric pores. J. Biol. Chem., 2009, 284(31), 20699-20707.
74. Gruber, C.W.; Muttenthaler, M.; Freissmuth, M. Ligand-based peptide design and combinatorial peptide libraries to target G protein-coupled receptors. Curr. Pharm. Des., 2010, 16(28), 3071-3088.
75. Hartmann, R.; Meisel, H. Food-derived peptides with biological activity: From research to food applications. Curr. Opin. Biotechnol., 2007, 18(2), 163-169.
76. Bachovchin, D.A.; Cravatt, B.F. The pharmacological landscape and therapeutic potential of serine hydrolases. Nat. Rev. Drug Discov., 2012, 11(1), 52-68.
77. Jones, A.T.; Sayers, E.J. Cell entry of cell penetrating peptides and tales of tails wagging dogs. J. Control. Release 2012 (in press)
78. Greenwood, K.P.; Daly, N.L.; Brown, D.L.; Stow, J.L.; Craik, D.J. The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int. J. Biochem. Cell Biol., 2007, 39(12), 2252-2264.
79. Contreras, J.; Elnagar, A.Y.; Hamm-Alvarez, S.F.; Camarero, J.A. Cellular uptake of cyclotide MCoTI-I follows multiple endocytic pathways. J. Control. Release, 2011, 155(2), 134-143.
80. Daly, N.L.; Clark, R.J.; Craik, D.J. Disulfide folding pathways of cystine knot proteins-Tying the knot within the circular backbone of the cyclotides. J. Biol. Chem., 2003, 278(8), 6314-6322.
81. Daly, N.L.; Love, S.; Alewood, P.F.; Craik, D.J. Chemical synthesis and folding pathways of large cyclic polypeptide: Studies of the cystine knot polypeptide kalata B1. Biochemistry, 1999, 38(32), 10606-10614.
82. Dawson, P.E.; Muir, T.W.; Clark-Lewis, I.; Kent, S.B. Synthesis of proteins by native chemical ligation. Science, 1994, 266(5186), 776-779.
83. Camarero, J.A.; Muir, T.W. Chemoselective backbone cyclization of unprotected peptides. Chem. Commun. (Camb.) 1997, (15), 1369-1370.
84. Gunasekera, S.; Daly, N.L.; Anderson, M.A.; Craik, D.J. Chemical synthesis and biosynthesis of the cyclotide family of circular proteins. IUBMB Life, 2006, 58(9), 515-524.
85. Camarero, J.A.; Kimura, R.H.; Woo, Y.H.; Shekhtman, A.; Cantor, J. Biosynthesis of a fully functional cyclotide inside living bacterial cells. Chembiochem., 2007, 8(12), 1363-1366.
86. Dornenburg, H. Cyclotide synthesis and supply: From plant to bioprocess. Biopolymers, 2010, 94(5), 602-610.
87. Weale, A. Ethical arguments relevant to the use of GM crops. New Biotechnology, 2010, 27(5), 582-587.
88. Veronese, F.M.; Pasut, G. PEGylation, successful approach to drug delivery. Drug Discov. Today, 2005, 10 (21), 1451-1458.
89. Clark, R.J.; Akcan, M.; Kaas, Q.; Daly, N.L.; Craik, D.J. Cyclization of conotoxins to improve their biopharmaceutical properties. Toxicon, 2012, 59(4), 446-455.
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 alpha-conotoxin MII. Proc. Natl. Acad. Sci. USA, 2005, 102(39), 13767-13772.
91. Olivera, B.M.; Gray, W.R.; Zeikus, R.; McIntosh, J.M.; Varga, J.; Rivier, J.; de Santos, V.; Cruz, L.J., Peptide neurotoxins from fishhunting cone snails. Science, 1985, 230(4732), 1338-1343.
92. 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 (Database issue), D325-330.
93. Kaas, Q.; Westermann, J.C.; Craik, D.J. Conopeptide characterization and classifications: an analysis using ConoServer. Toxicon, 2010, 55(8), 1491-1509.
94. 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 (12), 1585-1597.
95. Miljanich, G.P. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr. Med. Chem., 2004, 11(23), 3029-3040.
96. Skjaerbaek, 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(4), 2291-2299.
97. Nicke, A.; Loughnan, M.L.; Millard, E.L.; Alewood, P.F.; Adams, D.J.; Daly, N.L.; Craik, D.J.; Lewis, R. J. Isolation, structure, and activity of GID, a novel alpha 4/7-conotoxin with an extended Nterminal sequence. J. Biol. Chem. 2003, 278(5), 3137-3144.
98. Marx, U.C.; Daly, N.L.; Craik, D.J. NMR of conotoxins: structural features and an analysis of chemical shifts of post-translationally modified amino acids. Magn. Reson. Chem., 2006, 44 Spec No, S41-50.
99. Armishaw, C.J.; Daly, N.L.; Nevin, S.T.; Adams, D.J.; Craik, D.J.; Alewood, P.F. Alpha-selenoconotoxins, a new class of potent alpha7 neuronal nicotinic receptor antagonists. J. Biol. Chem. 2006, 281(20), 14136-14143.
100. 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(37), 6545-6548.
101. Gelly, J.C.; Gracy, J.; Kaas, Q.; Le-Nguyen, D.; Heitz, A.; Chiche, L. The KNOTTIN website and database: A new information system dedicated to the knottin scaffold. Nucleic Acids Res., 2004, 32, D156-D159.
102. DeBin, J.A.; Maggio, J.E.; Strichartz, G.R. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am. J. Physiol., 1993, 264 (2 Pt 1), C361-369.
103. Ullrich, N.; Gillespie, G.Y.; Sontheimer, H. Human astrocytoma cells express a unique chloride current. Neuroreport, 1996, 7(5), 1020-1024.
104. Ullrich, N.; Sontheimer, H. Biophysical and pharmacological characterization of chloride currents in human astrocytoma cells. Am. J. Physiol., 1996, 270(5 Pt 1), C1511-1521.
105. Soroceanu, L.; Gillespie, Y.; Khazaeli, M.B.; Sontheimer, H. Use of chlorotoxin for targeting of primary brain tumors. Cancer Res., 1998, 58(21), 4871-4879.
106. Lyons, S. A.; O'Neal, J.; Sontheimer, H. Chlorotoxin, a scorpionderived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia, 2002, 39(2), 162-173.
107. Deshane, J.; Garner, C.C.; Sontheimer, H. Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2. J. Biol. Chem., 2003, 278(6), 4135-4144.
108. Wiranowska, M.; Colina, L.O.; Johnson, J.O. Clathrin-mediated entry and cellular localization of chlorotoxin in human glioma. Cancer Cell Int., 2011, 11, 27.
109. Mamelak, A.N.; Rosenfeld, S.; Bucholz, R.; Raubitschek, A.; Nabors, L.B.; Fiveash, J.B.; Shen, S.; Khazaeli, M.B.; Colcher, D.; Liu, A.; Osman, M.; Guthrie, B.; Schade-Bijur, S.; Hablitz, D.M.; Alvarez, V. L.; Gonda, M.A. Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J. Clin. Oncol., 2006, 24(22), 3644-3650.
110. Veiseh, O.; Sun, C.; Gunn, J.; Kohler, N.; Gabikian, P.; Lee, D.; Bhattarai, N.; Ellenbogen, R.; Sze, R.; Hallahan, A.; Olson, J.; Zhang, M. Optical and MRI multifunctional nanoprobe for targeting gliomas. Nano Lett., 2005, 5(6), 1003-1008.
111. Veiseh, M.; Gabikian, P.; Bahrami, S.B.; Veiseh, O.; Zhang, M.; Hackman, R.C.; Ravanpay, A.C.; Stroud, M.R.; Kusuma, Y.; Hansen, S.J.; Kwok, D.; Munoz, N.M.; Sze, R.W.; Grady, W.M.; Greenberg, N.M.; Ellenbogen, R.G.; Olson, J.M. Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res., 2007, 67(14), 6882-6888.
112. 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.
113. Jacoby, D.B.; Dyskin, E.; Yalcin, M.; Kesavan, K.; Dahlberg, W.; Ratliff, J.; Johnson, E.W.; Mousa, S.A. Potent pleiotropic antiangiogenic effects of TM601, a synthetic chlorotoxin peptide. Anticancer Res., 2010, 30 (1), 39-46.
114. Kesavan, K.; Ratliff, J.; Johnson, E.W.; Dahlberg, W.; Asara, J.M.; Misra, P.; Frangioni, J.V.; Jacoby, D.B. Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and antiangiogenic effects. J. Biol. Chem., 2010, 285(7), 4366-4374.
115. Takano, S.; Togawa, A.; Yoshitomi, H.; Shida, T.; Kimura, F.; Shimizu, H.; Yoshidome, H.; Ohtsuka, M.; Kato, A.; Tomonaga, T.; Nomura, F.; Miyazaki, M. Annexin II overexpression predicts rapid recurrence after surgery in pancreatic cancer patients undergoing gemcitabine-adjuvant chemotherapy. Ann. Surg. Oncol., 2008, 15(11), 3157-3168.
116. Ling, Q.; Jacovina, A.T.; Deora, A.; Febbraio, M.; Simantov, R.; Silverstein, R.L.; Hempstead, B.; Mark, W. H.; Hajjar, K.A. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J. Clin. Invest., 2004, 113(1), 38-48.