Cyclotides: From gene structure to promiscuous multifunctionality

Journal of Evidence-Based Complementary and Alternative Medicine

Volumn 17, Issue 1, 2012, Pages 40-53

  Pinto, Michelle F S ^a   Almeida, Renato G ^a   Porto, William F ^a   Fensterseifer, Isabel C M ^a   Lima, Loiane A ^a   Dias, Simoni C ^a   Franco, Octávio L ^a  

^a UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

cyclic peptides; cyclotides; cysteine; drug design; gene structure; structural properties

Indexed keywords

EID: 84855361816     PISSN: 21565872     EISSN: None     Source Type: Journal    
DOI: 10.1177/2156587211428077     Document Type: Review

References (81)

1. Chen B,Colgrave ML,Daly NL, et al.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;280:22395-22405.
2. Jennings CV,Rosengren KJ,Daly NL, et al.Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: do Mobius strips exist in nature?.Biochemistry. 2005;44:851-860.
3. Ireland DC,Colgrave ML,Craik DJ.A novel suite of cyclotides from Viola odorata: sequence variation and the implications for structure, function and stability.Biochem J. 2006;400:1-12.
4. Nguyen GK,Zhang S,Nguyen NT, et al.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.
5. Craik DJ.The folding of disulfide-rich proteins.Antioxid Redox Signal. 2011;14:61-64.
6. Craik DJ.Discovery and applications of the plant cyclotides.Toxicon. 2010;56:1092-1102.
7. Simonsen SM,Sando L,Ireland DC, et al.A continent of plant defense peptide diversity: cyclotides in Australian Hybanthus (Violaceae).Plant Cell. 2005;17:3176-3189.
8. Craik DJ,Daly NL,Mulvenna J, et al.Discovery, structure and biological activities of the cyclotides.Curr Protein Pept Sci. 2004;5:297-315.
9. Poth AG,Colgrave ML,Lyons RE, et al.Discovery of an unusual biosynthetic origin for circular proteins in legumes.Proc Natl Acad Sci U S A. 2011;108:10127-10132.
10. Pranting M,Loov C,Burman R, et al.The cyclotide cycloviolacin O2 from Viola odorata has potent bactericidal activity against Gram-negative bacteria.J Antimicrob Chemother. 2010;65:1964-1971.
11. Craik DJ,Daly NL.NMR as a tool for elucidating the structures of circular and knotted proteins.Mol Biosyst. 2007;3:257-265.
12. Daly NL,Clark RJ,Plan MR, et al.Kalata B8, a novel antiviral circular protein, exhibits conformational flexibility in the cystine knot motif.Biochem J. 2006;393:619-626.
13. Wu WJ,Raleigh DP.Local control of peptide conformation: stabilization of cis proline peptide bonds by aromatic proline interactions.Biopolymers. 1998;45:381-394.
14. Pelegrini PB,Quirino BF,Franco OL.Plant cyclotides: an unusual class of defense compounds.Peptides. 2007;28:1475-1481.
15. Heitz Aal.Solution structure of the squash trypsin inhibitor MCoTI-II: a new family for cyclic knottins.Biochemistry. 2001;40:7973-7983.
16. Thongyoo P,Roque-Rosell N,Leatherbarrow RJ, et al.Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides.Org Biomol Chem. 2008;6:1462-1470.
17. Craik DJ,Cemazar M,Daly NL.The cyclotides and related macrocyclic peptides as scaffolds in drug design.Curr Opin Drug Discov Devel. 2006;9:251-260.
18. Franco OL.Peptide promiscuity: an evolutionary concept for plant defense.FEBS Lett. 2011;585:995-1000.
19. Colgrave ML,Kotze AC,Ireland DC, et al.The anthelmintic activity of the cyclotides: natural variants with enhanced activity.Chembiochem. 2008;9:1939-1945.
20. Plan MR,Saska I,Cagauan AG, et al.Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail).J Agric Food Chem. 2008;56:5237-5241.
21. Tam JP,Lu YA,Yang JL, et al.An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides.Proc Natl Acad Sci U S A. 1999;96:8913-8918.
22. Wang CK,Colgrave ML,Gustafson KR, et al.Anti-HIV cyclotides from the Chinese medicinal herb Viola yedoensis.J Nat Prod. 2008;71:47-52.
23. Herrmann A,Burman R,Mylne JS, et al.The alpine violet, Viola biflora, is a rich source of cyclotides with potent cytotoxicity.Phytochemistry. 2008;69:939-952.
24. Trabi M,Craik DJ.Tissue-specific expression of head-to-tail cyclized miniproteins in Violaceae and structure determination of the root cyclotide Viola hederacea root cyclotide1.Plant Cell. 2004;16:2204-2216.
25. Jennings C,West J,Waine C, et al.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.
26. Plan MR,Rosengren KJ,Sando L, et al.Structural and biochemical characteristics of the cyclotide kalata B5 from Oldenlandia affinis.Biopolymers. 2010;94:647-658.
27. Dutton JL,Renda RF,Waine C, et al.Conserved structural and sequence elements implicated in the processing of gene-encoded circular proteins.J Biol Chem. 2004;279:46858-46867.
28. Zhang J,Liao B,Craik DJ, et al.Identification of two suites of cyclotide precursor genes from metallophyte Viola baoshanensis: cDNA sequence variation, alternative RNA splicing and potential cyclotide diversity.Gene. 2009;431:23-32.
29. Burman R,Svedlund E,Felth J, et al.Evaluation of toxicity and antitumor activity of cycloviolacin O2 in mice.Biopolymers. 2010;94:626-634.
30. Saska I,Gillon AD,Hatsugai N, et al.An asparaginyl endopeptidase mediates in vivo protein backbone cyclization.J Biol Chem. 2007;282:29721-29728.
31. Gillon AD,Saska I,Jennings CV, et al.Biosynthesis of circular proteins in plants.Plant J. 2008;53:505-515.
32. Kaas Q,Craik DJ.Analysis and classification of circular proteins in CyBase.Biopolymers. 2010;94:584-591.
33. Craik DJ,Mylne JS,Daly NL.Cyclotides: macrocyclic peptides with applications in drug design and agriculture.Cell Mol Life Sci. 2010;67:9-16.
34. Daly NL,Rosengren KJ,Craik DJ.Discovery, structure and biological activities of cyclotides.Adv Drug Deliv Rev. 2009;61:918-930.
35. Qin Q,McCallum EJ,Kaas Q, et al.Identification of candidates for cyclotide biosynthesis and cyclisation by expressed sequence tag analysis of Oldenlandia affinis.BMC Genomics. 2010;11:111.
36. Westermann JC,Craik DJ.Comprehensive Natural Products II: Chemistry and Biology. Mander LLiu HW, ed. Oxford, UK: Elsevier; 2010:257-285.
37. Mulvenna JP,Sando L,Craik DJ.Processing of a 22 kDa precursor protein to produce the circular protein tricyclon A.Structure. 2005;13:691-701.
38. Mulvenna JP,Mylne JS,Bharathi R, et al.Discovery of cyclotide-like protein sequences in graminaceous crop plants: ancestral precursors of circular proteins?.Plant Cell. 2006;18:2134-2144.
39. Craik DJ,Daly NL,Bond T, et al.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.
40. Trabi M,Mylne JS,Sando L, et al.Circular proteins from Melicytus (Violaceae) refine the conserved protein and gene architecture of cyclotides.Org Biomol Chem. 2009;7:2378-2388.
41. Gruber CW,Cemazar M,Clark RJ, et al.A novel plant protein-disulfide isomerase involved in the oxidative folding of cystine knot defense proteins.J Biol Chem. 2007;282:20435-20446.
42. Basse CW.Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation.Plant Physiol. 2005;138:1774-1784.
43. Poth AG,Colgrave ML,Philip R, et al.Discovery of cyclotides in the Fabaceae plant family provides new insights into the cyclization, evolution, and distribution of circular proteins.ACS Chem Biol. 2011;6:345-355.
44. D'aloisio E,Paolacci AR,Dhanapal AP, et al.The protein disulfide isomerase gene family in bread wheat (T. aestivum L.).BMC Plant Biol. 2010;10:101.
45. Xu W,Li L,Du L, et al.Various mechanisms in cyclopeptide production from precursors synthesized independently of non-ribosomal peptide synthetases.Acta Biochim Biophys Sin (Shanghai). 2011;10:757-762.
46. Saether O,Craik DJ,Campbell ID, et al.Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1.Biochemistry. 1995;34:4147-4158.
47. Rosengren KJ,Daly NL,Plan MR, et al.Twists, knots, and rings in proteins: structural definition of the cyclotide framework.J Biol Chem. 2003;278:8606-8616.
48. Gunasekera S,Foley FM,Clark RJ, et al.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.
49. Barbeta BL,Marshall AT,Gillon AD, et al.Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae.Proc Natl Acad Sci U S A. 2008;105:1221-1225.
50. Kamimori H,Hall K,Craik DJ, et al.Studies on the membrane interactions of the cyclotides kalata B1 and kalata B6 on model membrane systems by surface plasmon resonance.Anal Biochem. 2005;337:149-153.
51. Shenkarev ZO,Nadezhdin KD,Sobol VA, et al.Conformation and mode of membrane interaction in cyclotides: spatial structure of kalata B1 bound to a dodecylphosphocholine micelle.FEBS J. 2006;273:2658-2672.
52. Chagolla-Lopez A,Blanco-Labran A,Patthy A, et al.A novel α-amylase inhibitor from amaranth (Amaranthus hypocondriacus) seeds.J Biol Chem. 1994;269:23675-23680.
53. Nourse A,Trabi M,Daly NL, et al.A comparison of the self-association behavior of the plant cyclotides kalata B1 and kalata B2 via analytical ultracentrifugation.J Biol Chem. 2004;279:562-570.
54. Triebskorn R,Casper H,Scheil V, et al.Ultrastructural effects of pharmaceuticals (carbamazepine, clofibric acid, metoprolol, diclofenac) in rainbow trout (Oncorhynchus mykiss) and common carp (Cyprinus carpio).Anal Bioanal Chem. 2007;387:1405-1416.
55. Lindholm P,Goransson U,Johansson S, et al.Cyclotides: a novel type of cytotoxic agents.Mol Cancer Ther. 2002;1:365-369.
56. Huang YH,Colgrave ML,Daly NL, et al.The biological activity of the prototypic cyclotide kalata B1 is modulated by the formation of multimeric pores.J Biol Chem. 2009;284:20699-20707.
57. Colgrave ML,Huang YH,Craik DJ, et al.Cyclotide interactions with the nematode external surface.Antimicrob Agents Chemother. 2010;54:2160-2166.
58. Gran L,Sletten K,Skjeldal L.Cyclic peptides from Oldenlandia affinis DC. Molecular and biological properties.Chem Biodivers. 2008;5:2014-2022.
59. Craik DJ.Circling the enemy: cyclic proteins in plant defence.Trends Plant Sci. 2009;14:328-335.
60. Gustafson KR,McKee TC,Bokesch HR.Anti-HIV cyclotides.Curr Protein Pept Sci. 2004;5:331-340.
61. Hallock YF,Sowder RC,Pannell LK, et al.Cycloviolins A-D, anti-HIV macrocyclic peptides from Leonia cymosa.J Org Chem. 2000;65:124-128.
62. Bokesch HR,Pannell LK,Cochran PK, et al.A novel anti-HIV macrocyclic peptide from Palicourea condensata.J Nat Prod. 2001;64:249-250.
63. Gustafson KR,Walton LK,Sowder RC, et al.New circulin macrocyclic polypeptides from Chassalia parvifolia.J Nat Prod. 2000;63:176-178.
64. Rusconi S,Scozzafava A,Mastrolorenzo A, et al.An update in the development of HIV entry inhibitors.Curr Top Med Chem. 2007;7:1273-1289.
65. Henriques ST,Craik DJ.Cyclotides as templates in drug design.Drug Discov Today. 2010;15:57-64.
66. Ireland DC,Wang CK,Wilson JA, et al.Cyclotides as natural anti-HIV agents.Biopolymers. 2008;90:51-60.
67. Svangard E,Goransson U,Hocaoglu Z, et al.Cytotoxic cyclotides from Viola tricolor.J Nat Prod. 2004;67:144-147.
68. Herrmann A,Svangard E,Claeson P, et al.Key role of glutamic acid for the cytotoxic activity of the cyclotide cycloviolacin O2.Cell Mol Life Sci. 2006;63:235-245.
69. Dornenburg H.Cyclotide synthesis and supply: from plant to bioprocess.Biopolymers. 2010;94:602-610.
70. Camarero JA,Kimura RH,Woo YH, et al.Biosynthesis of a fully functional cyclotide inside living bacterial cells.Chembiochem. 2007;8:1363-1366.
71. Leta Aboye T,Clark RJ,Craik DJ, et al.Ultra-stable peptide scaffolds for protein engineering-synthesis and folding of the circular cystine knotted cyclotide cycloviolacin O2.Chembiochem. 2008;9:103-113.
72. Gunasekera S,Daly NL,Anderson MA, et al.Chemical synthesis and biosynthesis of the cyclotide family of circular proteins.IUBMB Life. 2006;58:515-524.
73. Kent S.Novel forms of chemical protein diversity: in nature and in the laboratory.Curr Opin Biotechnol. 2004;15:607-614.
74. Perler FB,Davis EO,Dean GE, et al.Protein splicing elements: inteins and exteins-a definition of terms and recommended nomenclature.Nucleic Acids Res. 1994;22:1125-1127.
75. Li L,Liu J,Diao Z, et al.Evaluation of specific delivery of chimeric phi29 pRNA/siRNA nanoparticles to multiple tumor cells.Mol Biosyst. 2009;5:1361-1368.
76. Thongyoo P,Jaulent AM,Tate EW, et al.Immobilized protease-assisted synthesis of engineered cysteine-knot microproteins.Chembiochem. 2007;8:1107-1109.
77. Camarero JA,Muir TW.Native chemical ligation of polypeptides.Curr Protoc Protein Sci. 2001;18:18-14.
78. Gunasekera S,Daly NL,Clark RJ, et al.Dissecting the oxidative folding of circular cystine knot miniproteins.Antioxid Redox Signal. 2009;11:971-980.
79. Clark RJ,Daly NL,Craik DJ.Structural plasticity of the cyclic-cystine-knot framework: implications for biological activity and drug design.Biochem J. 2006;394:85-93.
80. Cudic M,Fields GB.Extracellular proteases as targets for drug development.Curr Protein Pept Sci. 2009;10:297-307.
81. Sommerhoff CP,Schaschke N.Mast cell tryptase beta as a target in allergic inflammation: an evolving story.Curr Pharm Des. 2007;13:313-332.