Circling the enemy: cyclic proteins in plant defence

Trends in Plant Science

Volumn 14, Issue 6, 2009, Pages 328-335

  Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

VEGETABLE PROTEIN;

CHEMISTRY; COMBINATORIAL CHEMISTRY; CYCLIZATION; HYDROLYSIS; PHYSIOLOGY; REVIEW;

COMBINATORIAL CHEMISTRY TECHNIQUES; CYCLIZATION; HYDROLYSIS; PLANT PROTEINS;

HEXAPODA; RUBIACEAE; VIOLACEAE;

EID: 66649136413     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2009.03.003     Document Type: Review

References (85)

1. Craik D.J., et al. Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 294 (1999) 1327-1336
2. Saska I., et al. An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J. Biol. Chem. 282 (2007) 29721-29728
3. Gillon A.D., et al. Biosynthesis of circular proteins in plants. Plant J. 53 (2008) 505-515
4. Barbeta B.L., et al. Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 1221-1225
5. Craik D.J., et al. The chemistry and biology of cyclotides. Curr. Opin. Drug Discov. Devel. 10 (2007) 176-184
6. Leta Aboye T., et al. Ultra stable peptide scaffolds for protein engineering-synthesis and folding of the circular cystine knotted cyclotide cycloviolacin O2. ChemBioChem 9 (2008) 103-113
7. Thongyoo P., et al. Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides. Org. Biomol. Chem. 6 (2008) 1462-1470
8. Avrutina O., et al. Head-to-tail cyclized cystine-knot peptides by a combined recombinant and chemical route of synthesis. ChemBioChem 9 (2008) 33-37
9. Gruber C.W., et al. Distribution and evolution of circular miniproteins in flowering plants. Plant Cell 20 (2008) 2471-2483
10. Craik D.J. Seamless proteins tie up their loose ends. Science 311 (2006) 1563-1564
11. Trabi M., and Craik D.J. Circular proteins - no end in sight. Trends Biochem. Sci. 27 (2002) 132-138
12. Gran L. An oxytocic principle found in Oldenlandia affinis DC. Medd. Nor. Farm. Selsk. 12 (1970) 173-180
13. Gran L., et al. Oldenlandia affinis (R&S) DC. A plant containing uteroactive peptides used in African traditional medicine. J. Ethnopharmacol 70 (2000) 197-203
14. Gran L., et al. Cyclic peptides from Oldenlandia affinis DC. Molecular and biological properties. Chem. Biodivers 5 (2008) 2014-2022
15. Saether O., et al. Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry 34 (1995) 4147-4158
16. Craik D.J., et al. The cystine knot motif in toxins and implications for drug design. Toxicon 39 (2001) 43-60
17. Colgrave M.L., and Craik D.J. Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry 43 (2004) 5965-5975
18. Schöpke T., et al. Hämolytisch aktive komponenten aus Viola tricolor L. und Viola arvensis Murray. Sci. Pharm. 61 (1993) 145-153
19. Witherup K.M., et al. Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J. Nat. Prod 57 (1994) 1619-1625
20. Gustafson K.R., et al. Circulins A and B: novel HIV-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc. 116 (1994) 9337-9338
21. Claeson P., et al. Fractionation protocol for the isolation of polypeptides from plant biomass. J. Nat. Prod. 61 (1998) 77-81
22. Robbrecht E., and Manen J.F. The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF and atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Syst. Geogr. Plants 76 (2006) 85-146
23. Tokuoka T. Molecular phylogenetic analysis of Violaceae (Malpighiales) based on plastid and nuclear DNA sequences. J. Plant Res. 121 (2008) 253-260
24. Göransson U., et al. Seven novel macrocyclic polypeptides from Viola arvensis. J. Nat. Prod. 62 (1999) 283-286
25. Simonsen S.M., et al. A continent of plant defense peptide diversity: cyclotides in Australian Hybanthus (Violaceae). Plant Cell 17 (2005) 3176-3189
26. Plan M.R.R., et al. The cyclotide fingerprint in Oldenlandia affinis: elucidation of chemically modified, linear and novel macrocyclic peptides. ChemBioChem 8 (2007) 1001-1011
27. Seydel P., et al. Formation of cyclotides and variations in cyclotide expression in Oldenlandia affinis suspension cultures. Appl. Microbiol. Biotechnol. 77 (2007) 275-284
28. Dornenburg H. Plant cell culture technology-harnessing a biological approach for competitive cyclotides production. Biotechnol. Lett. 30 (2008) 1311-1321
29. 15N cyclotides by whole plant labeling. Biopolymers 90 (2008) 575-580
30. Trabi M., and Craik D.J. Tissue-specific expression of head-to-tail cyclized miniproteins in Violaceae and structure determination of the root cyclotide Viola hederacea root cyclotide1. Plant Cell 16 (2004) 2204-2216
31. Wang C.K., et al. CyBase: a database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res. 36 (2008) D206-D210
32. Gunasekera S., et al. Chemical synthesis and biosynthesis of the cyclotide family of circular proteins. IUBMB Life 58 (2006) 515-524
33. Pelegrini P.B., et al. Plant cyclotides: an unusual class of defense compounds. Peptides 28 (2007) 1475-1481
34. Gruber C.W., et al. Insecticidal plant cyclotides and related cystine knot toxins. Toxicon 49 (2007) 561-575
35. Goransson U., et al. Novel strategies for isolation and characterization of cyclotides: the discovery of bioactive macrocyclic plant polypeptides in the Violaceae. Curr. Protein Pept. Sci. 5 (2004) 317-329
36. Rosengren K.J., et al. Twists, knots, and rings in proteins. Structural definition of the cyclotide framework. J. Biol. Chem 278 (2003) 8606-8616
37. Herrmann A., et al. Key role of glutamic acid for the cytotoxic activity of the cyclotide cycloviolacin O2. Cell. Mol. Life Sci. 63 (2006) 235-245
38. Simonsen S.M., et al. Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem. 283 (2008) 9805-9813
39. Hernandez J.F., et al. Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure. Biochemistry 39 (2000) 5722-5730
40. Felizmenio-Quimio M.E., et al. Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J. Biol. Chem. 276 (2001) 22875-22882
41. Heitz A., et al. Solution structure of the squash trypsin inhibitor MCoTI-II. A new family for cyclic knottins. Biochemistry 40 (2001) 7973-7983
42. Chiche L., et al. Squash inhibitors: from structural motifs to macrocyclic knottins. Curr. Protein Pept. Sci. 5 (2004) 341-349
43. Ireland D.C., et al. Discovery and characterization of a linear cyclotide from Viola odorata: implications for the processing of circular proteins. J. Mol. Biol. 357 (2006) 1522-1535
44. Tan N.H., and Zhou J. Plant cyclopeptides. Chem. Rev. 106 (2006) 840-895
45. Jennings C., et al. Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10614-10619
46. Dutton J.L., et al. Conserved structural and sequence elements implicated in the processing of gene-encoded circular proteins. J. Biol. Chem. 279 (2004) 46858-46867
47. Zhang J., 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 431 (2008) 23-32
48. Herrmann A., et al. The alpine violet, Viola biflora, is a rich source of cyclotides with potent cytotoxicity. Phytochemistry 69 (2008) 939-952
49. Mulvenna J.P., et al. Processing of a 22 kDa precursor protein to produce the circular protein tricyclon A. Structure 13 (2005) 691-701
50. Muntz K., and Shutov A.D. Legumains and their functions in plants. Trends Plant Sci. 7 (2002) 340-344
51. Schaller A. A cut above the rest: the regulatory function of plant proteases. Planta 220 (2004) 183-197
52. Sheldon P.S., et al. Post-translational peptide bond formation during concanavalin A processing in vitro. Biochem. J. 320 (1996) 865-870
53. Gruber C.W., et al. A novel plant protein-disulfide isomerase involved in the oxidative folding of cystine knot defense proteins. J. Biol. Chem. 282 (2007) 20435-20446
54. Gruber C.W., et al. Biochemical and biophysical characterization of a novel plant protein disulfide isomerase. Biopolymers 92 (2009) 35-43
55. Gruber C.W., et al. Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem. Sci. 31 (2006) 455-464
56. Daly N.L., and Craik D.J. Acyclic permutants of naturally occurring cyclic proteins. Characterization of cystine knot and β-sheet formation in the macrocyclic polypeptide kalata B1. J. Biol. Chem 275 (2000) 19068-19075
57. Daly N.L., et al. Disulfide folding pathways of cystine knot proteins. Tying the knot within the circular backbone of the cyclotides. J. Biol. Chem 278 (2003) 6314-6322
58. Čemažar M., et al. Knots in rings. The circular knotted protein Momordica cochinchinensis trypsin inhibitor-II folds via a stable two-disulfide intermediate. J. Biol. Chem 281 (2006) 8224-8232
59. Gunasekera S., et al. Dissecting the oxidative folding of circular cystine knot miniproteins. Antioxid. Redox Signal. 11 (2008) 971-980
60. Tam J.P., 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. 96 (1999) 8913-8918
61. Jennings C.V., et al. Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: do Mobius strips exist in nature?. Biochemistry 44 (2005) 851-860
62. Plan M.R.R., et al. Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J. Agric. Food Chem. 56 (2008) 5237-5241
63. Göransson U., et al. Reversible antifouling effect of the cyclotide cycloviolacin O2 against barnacles. J. Nat. Prod. 67 (2004) 1287-1290
64. Colgrave M.L., et al. Cyclotides: natural, circular plant peptides that possess significant activity against gastrointestinal nematode parasites of sheep. Biochemistry 47 (2008) 5581-5589
65. Colgrave M.L., et al. Anthelmintic activity of cyclotides: in vitro studies with canine and human hookworms. Acta Trop. 109 (2009) 163-166
66. Kamimori H., 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. 337 (2005) 149-153
67. Shenkarev Z.O., et al. Conformation and mode of membrane interaction in cyclotides. Spatial structure of kalata B1 bound to a dodecylphosphocholine micelle. FEBS J 273 (2006) 2658-2672
68. Shenkarev Z.O., et al. Divalent cation coordination and mode of membrane interaction in cyclotides: NMR spatial structure of ternary complex Kalata B7/Mn21/DPC micelle. J. Inorg. Biochem. 102 (2008) 1246-1256
69. Skjeldal L., et al. Refined structure and metal binding site of the kalata B1 peptide. Arch. Biochem. Biophys. 399 (2002) 142-148
70. Barry D.G., et al. Linearization of a naturally occurring circular protein maintains structure but eliminates hemolytic activity. Biochemistry 42 (2003) 6688-6695
71. Simonsen S.M., et al. Capped acyclic permutants of the circular protein kalata B1. FEBS Lett. 577 (2004) 399-402
72. Mulvenna J.P., et al. Discovery of cyclotide-like protein sequences in graminaceous crop plants: ancestral precursors of circular proteins?. Plant Cell 18 (2006) 2134-2144
73. Basse C.W. Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiol. 138 (2005) 1774-1784
74. Craik D.J., et al. The cyclotides: novel macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Devel. 5 (2002) 251-260
75. Christmann A., et al. The cystine knot of a squash-type protease inhibitor as a structural scaffold for Esherichia coli cell surface display of conformationally constrained peptides. Protein Eng. 12 (1999) 797-806
76. Kolmar H. Alternative binding proteins: biological activity and therapeutic potential of cystine-knot miniproteins. FEBS J. 275 (2008) 2684-2690
77. Clark R.J., et al. Structural plasticity of the cyclic-cystine-knot framework: implications for biological activity and drug design. Biochem. J. 394 (2006) 85-93
78. Gunasekera S., et al. Engineering stabilized vascular endothelial growth factor-A antagonists: synthesis, structural characterization, and bioactivity of grafted analogues of cyclotides. J. Med. Chem. 51 (2008) 7697-7704
79. Greenwood K.P., et al. The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int. J. Biochem. Cell Biol. 39 (2007) 2252-2264
80. Daly N.L., et al. Chemical synthesis and folding pathways of large cyclic polypeptides: studies of the cystine knot polypeptide kalata B1. Biochemistry 38 (1999) 10606-10614
81. Kimura R.H., et al. Biosynthesis of the cyclotide kalata B1 by using protein splicing. Angew. Chem. Int. Ed. Engl. 45 (2006) 973-976
82. Camarero J.A., et al. Biosynthesis of a fully functional cyclotide inside living bacterial cells. ChemBioChem 8 (2007) 1363-1366
83. Thongyoo P., et al. Immobilized protease-assisted synthesis of engineered cysteine-knot microproteins. ChemBioChem 8 (2007) 1107-1109
84. Saska I., and Craik D.J. Protease-catalysed protein splicing: a new post-translational modification?. Trends Biochem. Sci. 33 (2008) 363-368
85. Saska I., et al. Quantitative analysis of backbone-cyclised peptides in plants. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 872 (2008) 107-114