The chemistry and biology of cyclotides

Current Opinion in Drug Discovery and Development

Volumn 10, Issue 2, 2007, Pages 176-184

  Craik, David J ^a   Čemažar, Maša ^a   Daly, Norelle L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Circular proteins; Cyclic peptides; Cystine knot; Drug design; Kalata B1; Protein engineering

Indexed keywords

CIRCULIN; CYCLOTIDE; CYCLOVIOLACIN H4; CYCLOVIOLACIN O2; INTEIN; KALATA B1; KALATA B2; KALATA B8; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; BIOLOGICAL ACTIVITY; BIOLOGY; CHEMISTRY; DISULFIDE BOND; DRUG DELIVERY SYSTEM; DRUG DESIGN; ENZYMATIC DEGRADATION; GENE EXPRESSION SYSTEM; HUMAN; NONHUMAN; PEPTIDE SYNTHESIS; PLANT CELL CULTURE; PLANT DEFENSE; PROTEIN ENGINEERING; PROTEIN STRUCTURE; REVIEW; SOLID;

ANIMALS; CYCLOTIDES; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PLANTS;

EID: 33947325235     PISSN: 13676733     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (44)

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2. Craik DJ, Daly NL, Mulvenna J, Plan MR, Trabi M: Discovery, structure and biological activities of the cyclotides. Curr Protein Peptide Sci (2004) 5(5):297-315.
3. Craik DJ, Čemažar M, Daly NL: The cyclotides and related macrocyclic peptides as scaffolds in drug design. Curr Opin Drug Discovery Dev (2006) 9(2):251-260.
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5. Witherup KM, Bogusky MJ, Anderson PS, Ramjit H, Ransom RW, Wood T, Sardana M: Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J Nat Prod (1994) 57(12):1619-1625.
6. Saether O, Craik DJ, Campbell ID, Sletten K, Juul J, Norman DG: Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry (1995) 34(13):4147-4158. • This paper describes the first 3-D structure of a cyclotide.
7. Gran L, Sandberg F, Sletten K: Oldenlandia affinis (R&S) DC. A plant containing uteroactive peptides used in African traditional medicine. J Ethnopharmacol (2000) 70(3):197-203. • An historical account of the discovery of the cyclotide kalata B1 in indigenous medicine.
8. Simonsen SM, Sando L, Ireland DC, Colgrave ML, Bharathi R, Göransson U, Craik DJ: A continent of plant defense peptide diversity: Cyclotides in Australian Hybanthus (Violaceae). Plant Cell (2005) 17(11):3176-3189.
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10. Craik DJ, Anderson MA, Barry DG, Clark RJ, Daly NL, Jennings CV, Mulvenna J: Discovery and structures of the cyclotides: Novel macrocyclic peptides from plants. Lett Peptide Sci (2002) 8(3-5):119-128.
11. Craik DJ, Čemažar M, Wang CK, Daly NL: The cyclotide family of circular miniproteins: Nature's combinatorial peptide template. Biopolymers (2006) 84(3):250-266. • A recent comprehensive review of the cyclotides.
12. Craik DJ, Simonsen S, Daly NL: The cyclotides: Novel macrocyclic peptides as scaffolds in drug design. Curr Opin Drug Discovery Dev (2002) 5(2):251-260.
13. Gunasekera S, Daly NL, Anderson MA, Craik DJ: Chemical synthesis and biosynthesis of the cyclotide family of circular proteins. IUBMB Life (2006) 58(9):515-524.
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. •• This article was the first to show that the cyclotides are encoded by genes and are produced via processing of a precursor protein.
15. Colgrave ML, Jones A, Craik DJ: Peptide quantification by matrixassisted laser desorption ionisation time-of-flight mass spectrometry: Investigations of the cyclotide kalata B1 in biological fluids. J Chromatogr A (2005) 1091(1-2):187-193.
16. Mulvenna JP, Wang C, Craik DJ: CyBase: A database of cyclic protein sequences and structure. Nucleic Acids Res (2006) 34(Database issue):D192-D194. • This paper introduces CyBase, which is a new database and information source for backbone-cyclized proteins.
17. Trabi M, Craik DJ: Circular proteins-no end in sight. Trends Biochem Sci (2002) 27(3):132-138.
18. Craik DJ, Daly NL, Saska I, Trabi M, Rosengren KJ: Structures of naturally occurring circular proteins from bacteria. J Bacteriol (2003) 185(14):4011-4021.
19. Chen B, Colgrave ML, Daly NL, Rosengren KJ, Gustafson KR, Craik DJ: 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.
20. 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):1-12.
21. Koltay A, Daly NL, Gustafson KR, Craik DJ: Structure of circulin B and implications for antimicrobial activity of the cyclotides. Int J Peptide Res Ther (2005) 11(1):99-106.
22. Chen B, Colgrave ML, Wang C, Craik DJ: Cycloviolacin H4, a hydrophobic cyclotide from Viola hederaceae. J Nat Prod (2006) 69(1):23-28.
23. Daly NL, Clark RJ, Plan MR, Craik DJ: Kalata B8, a novel antiviral circular protein, exhibits conformational flexibility in the cystine knot motif. Biochem J (2006) 393(Pt 3):619-626.
24. Jennings CV, Rosengren KJ, Daly NL, Plan M, Stevens J, Scanlon MJ, Waine C, Norman DG, Anderson MA, Craik DJ: Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: Do Möbius strips exist in nature? Biochemistry (2005) 44(3):851-860.
25. Nair SS, Romanuka J, Billeter M, Skjeldal L, Emmett MR, Nilsson CL, Marshall AG: Structural characterization of an unusually stable cyclic peptide, kalata B2 from Oldenlandia affinis. Biochim Biophys Acta (2006) 1764(10):1568-1576.
26. Herrmann A, Svangard E, Claeson P, Gullbo J, Bohlin L, Göransson U: Key role of glutamic acid for the cytotoxic activity of the cyclotide cycloviolacin O2. Cell Mol Life Sci (2006) 63(2):235-245.
27. Daly NL, Love S, Alewood PF, Craik DJ: Chemical synthesis and folding of large cyclic polypeptides: Studies of the cystine knot polypeptide kalata B1. Biochemistry (1999) 38(32):10606-10614.
28. Tam JP, Lu YA, Yang JL, Chiu KW: 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. • This paper describes the synthesis of cyclotides, using a thio-ester method, and their antimicrobial activity.
29. Kimura RH, Tran AT, Camarero JA: Biosynthesis of the cyclotide kalata B1 by using protein splicing. Angew Chem-Int Ed (2006) 45(6):973-976. •• This article describes the biosynthesis of cyclotide kalata B1 by using an engineered intein in vitro.
30. Seydel P, Dornenburg H: Establishment of in vitro plants, cell and tissue cultures from Oldenlandia affinis for the production of cyclic peptides. Plant Cell Tissue Organ Culture (2006) 85(3):247-255.
31. Clark RJ, Daly NL, Craik DJ: Structural plasticity of the cycliccystine-knot framework: Implications for biological activity and drug design. Biochem J (2006) 394(Pt 1):85-93. •• The first study to introduce non-native sequences into the cyclotide scaffold, demonstrating that the structure is maintained. It also shows that hemolytic activity can be removed from the cyclotide scaffold by effecting changes to a single loop.
32. Thongyoo P, Tate EW, Leatherbarrow RJ: Total synthesis of the macrocyclic cysteine knot microprotein MCoTI-II. Chem Commun (2006) (27):848-2850.
33. Craik DJ, Daly NL: Oxidative folding of the cystine knot motif in cyclotide proteins. Protein Peptide Lett (2005) 12(2):147-152.
34. Daly NL, Clark RJ, Craik DJ: 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.
35. Čemažar M, Daly NL, Haggblad S, Lo KP, Yulyaningsih E, Craik DJ: Knots in rings. The circular knotted protein Momordica cochinchinensis trypsin inhibitor-II folds via a stable two-disulfide intermediate. J Biol Chem (2006) 281(12):8224-8232.
36. Ireland DC, Colgrave ML, Nguyencong P, Daly NL, Craik DJ: Discovery and characterization of a linear cyclotide from Viola odorata: Implications for the processing of circular proteins. J Mol Biol (2006) 357(5):1522-1535. • This article describes the first naturally occurring linear version of a cyclotide and provides an insight into the processing mechanism.
37. Mulvenna JP, Sando L, Craik DJ: Processing of a 22 kDa precursor protein to produce the circular protein tricyclon A. Structure (2005) 13(5):691-701.
38. Basse CW: Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiol (2005) 138(3):1774- 1784.
39. Mulvenna JP, Mylne JS, Bharathi R, Burton RA, Shirley NJ, Fincher GB, Anderson MA, Craik DJ: Discovery of cyclotide-like protein sequences in graminaceous crop plants: Ancestral precursors of circular proteins? Plant Cell (2006) 18(9):2134-2144. • This study combines bioinformatics and expression analysis to report the discovery of sequences related to those of cyclotides in crop plants, such as rice, maize and wheat.
40. Kamimori H, Hall K, Craik DJ, Aguilar MI: 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.
41. Shenkarev ZO, Nadezhdin KD, Sobol VA, Sobol AG, Skjeldal L, Arseniev AS: Conformation and mode of membrane interaction in cyclotides. Spatial structure of kalata B1 bound to a dodecylphosphocholine micelle. FEBS J (2006) 273(12):2658-2672. •• This paper reports the structure of kalata B1 inserted into dodecylphosphocholine micelles and shows that the peptide binds via the hydrophobic residues in loops 2, 5 and 6.
42. Reiss S, Sieber M, Oberle V, Wentzel A, Spangenberg P, Claus R, Kolmar H, Losche W: Inhibition of platelet aggregation by grafting RGD and KGD sequences on the structural scaffold of small disulfide-rich proteins. Platelets (2006) 17(3):153-157. •• This paper reports the use of cystine-knot scaffolds as grafting templates and shows that significant improvements in activity of linear epitopes can be achieved upon grafting into the scaffolds.
43. Werle M, Schmitz T, Huang HL, Wentzel A, Kolmar H, Bernkop-Schnurch A: The potential of cystine-knot microproteins as novel pharmacophoric scaffolds in oral peptide drug delivery. J Drug Targeting (2006) 14(3):137-146. • This paper highlights the important features of cystine-knot scaffolds that may be beneficial in drug design candidates.
44. Colgrave ML, Craik DJ: Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: The importance of the cyclic cystine knot. Biochemistry (2004) 43(20):5965-5975.