Characterizing circular peptides in mixtures: sequence fragment assembly of cyclotides from a violet plant by MALDI-TOF/TOF mass spectrometry

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• 作者：Hossein Hashempour (1) (2)
  Johannes Koehbach (1)
  Norelle L. Daly (3)
  Alireza Ghassempour (2)
  Christian W. Gruber (1)
  
• 关键词：Viola ignobilis ; Circular ; Cystine ; knot ; Oxidative folding ; Vigno ; Peptidomics
• 刊名：Amino Acids
• 出版年：2013
• 出版时间：February 2013
• 年：2013
• 卷：44
• 期：2
• 页码：581-595
• 全文大小：1458KB
• 参考文献：1. Aboye TL, Clark RJ, Burman R, Roig MB, Craik DJ, G?ransson U (2011) Interlocking disulfides in circular proteins: toward efficient oxidative folding of cyclotides. Antioxid Redox Signal 14(1):77-6 CrossRef
  2. Barbeta BL, Marshall AT, Gillon AD, Craik DJ, Anderson MA (2008) Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc Natl Acad Sci USA 105(4):1221-225 CrossRef
  3. Claeson P, Goransson U, Johansson S, Luijendijk T, Bohlin L (1998) Fractionation protocol for the isolation of polypeptides from plant biomass. J Nat Prod 61(1):77-1 CrossRef
  4. Clark RJ, Daly NL, Craik DJ (2006) Structural plasticity of the cyclic-cystine-knot framework: implications for biological activity and drug design. Biochem J 394(Pt 1):85-3
  5. Colgrave ML, Craik DJ (2004) Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry 43(20):5965-975 CrossRef
  6. Colgrave ML, Kotze AC, Ireland DC, Wang CK, Craik DJ (2008) The anthelmintic activity of the cyclotides: natural variants with enhanced activity. ChemBioChem 9(12):1939-945 CrossRef
  7. Colgrave ML, Poth A, Kaas Q, Craik DJ (2010) A new ‘era-for cyclotide sequencing. Biopolymers 94(5):592-01 CrossRef
  8. Craik DJ, Daly NL, Bond T, Waine C (1999) Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J Mol Biol 294(5):1327-336 CrossRef
  9. Daly NL, Love S, Alewood PF, Craik DJ (1999) Chemical synthesis and folding pathways of large cyclic polypeptides: studies of the cystine knot polypeptide kalata B1. Biochemistry 38(32):10606-0614 CrossRef
  10. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB 3rd, Snoeyink J, Richardson JS, Richardson DC (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35(Web Server issue):W375–W383
  11. G?ransson U, Sjogren M, Svangard E, Claeson P, Bohlin L (2004) Reversible antifouling effect of the cyclotide cycloviolacin O2 against barnacles. J Nat Prod 67(8):1287-290 CrossRef
  12. G?ransson U, Herrmann A, Burman R, Haugaard-Jonsson LM, Rosengren KJ (2009) The conserved glu in the cyclotide cycloviolacin O2 has a key structural role. ChemBioChem 10(14):2354-360 CrossRef
  13. Gran L (1970) An oxytocic principle found in / Oldenlandia affinis DC. Medd Nor Farm Selsk 12:173-80
  14. Gruber CW (2010) Global cyclotide adventure: a journey dedicated to the discovery of circular peptides from flowering plants. Biopolymers 94(5):565-72 CrossRef
  15. Gruber CW, O’Brien M (2011) Uterotonic plants and their bioactive constituents. Planta Med 77(3):207-20 CrossRef
  16. Gruber CW, Cemazar M, Anderson MA, Craik DJ (2007a) Insecticidal plant cyclotides and related cystine knot toxins. Toxicon 49(4):561-75 CrossRef
  17. Gruber CW, Cemazar M, Clark RJ, Horibe T, Renda RF, Anderson MA, Craik DJ (2007b) A novel plant protein disulfide isomerase involved in the oxidative folding of cystine knot defense proteins. J Biol Chem 282(28):20435-0446 CrossRef
  18. Gruber CW, Elliott AG, Ireland DC, Delprete PG, Dessein S, G?ransson U, Trabi M, Wang CK, Kinghorn AB, Robbrecht E, Craik DJ (2008) Distribution and evolution of circular miniproteins in flowering plants. Plant Cell 20(9):2471-483 CrossRef
  19. Gründemann C, Koehbach J, Huber R, Gruber CW (2012) Do plant cyclotides have potential as immunosuppressant peptides? J Nat Prod 75(2):167-74 CrossRef
  20. Gunasekera S, Daly NL, Clark RJ, Craik DJ (2009) Dissecting the oxidative folding of circular cystine knot miniproteins. Antioxid Redox Signal 11(5):971-80 CrossRef
  21. Hashempour H, Ghassempour A, Daly NL, Spengler B, Rompp A (2011) Analysis of cyclotides in / Viola ignobilis by Nano liquid chromatography fourier transform mass spectrometry. Protein Pept Lett 18(7):747-52 CrossRef
  22. Henriques ST, Craik DJ (2010) Cyclotides as templates in drug design. Drug Discov Today 15(1-):57-4 CrossRef
  23. Jennings C, West J, Waine C, Craik D, Anderson M (2001) Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from / Oldenlandia affinis. Proc Natl Acad Sci USA 98(19):10614-0619 CrossRef
  24. Leta Aboye T, Clark RJ, Craik DJ, G?ransson U (2008) Ultra-stable peptide scaffolds for protein engineering-synthesis and folding of the circular cystine knotted cyclotide cycloviolacin O2. ChemBioChem 9(1):103-13 CrossRef
  25. Mulvenna JP, Sando L, Craik DJ (2005) Processing of a 22?kDa precursor protein to produce the circular protein tricyclon A. Structure?13(5):691-01 CrossRef
  26. Poth AG, Colgrave ML, Philip R, Kerenga B, Daly NL, Anderson MA, Craik DJ (2010) Discovery of cyclotides in the Fabaceae plant family provides new insights into the cyclization, evolution, and distribution of circular proteins. ACS Chem Biol 6(4):345-55 CrossRef
  27. Saska I, Gillon AD, Hatsugai N, Dietzgen RG, Hara-Nishimura I, Anderson MA, Craik DJ (2007) An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J Biol Chem 282(40):29721-9728 CrossRef
  28. Seydel P, Gruber CW, Craik DJ, D?rnenburg H (2007) Formation of cyclotides and variations in cyclotide expression in / Oldenlandia affinis suspension cultures. Appl Microb Biotechnol 77(2):275-84 CrossRef
  29. Simonsen SM, Sando L, Ireland DC, Colgrave ML, Bharathi R, G?ransson U, Craik DJ (2005) A continent of plant defense peptide diversity: cyclotides in Australian Hybanthus (Violaceae). Plant Cell 17(11):3176-189 CrossRef
  30. Tam JP, Lu YA, Yang JL, Chiu KW (1999) An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides. Proc Natl Acad Sci USA 96(16):8913-918 CrossRef
  31. Wang CK, Colgrave ML, Gustafson KR, Ireland DC, Goransson U, Craik DJ (2008a) Anti-HIV cyclotides from the Chinese medicinal herb / Viola yedoensis. J Nat Prod 71(1):47-2 CrossRef
  32. Wang CK, Kaas Q, Chiche L, Craik DJ (2008b) CyBase: a database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res 36(Database issue):D206–D210
  33. Wong CT, Taichi M, Nishio H, Nishiuchi Y, Tam JP (2011) Optimal oxidative folding of the novel antimicrobial cyclotide from / Hedyotis biflora requires high alcohol concentrations. Biochemistry 50(33):7275-283 CrossRef
  34. Yeshak MY, Burman R, Asres K, G?ransson U (2011) Cyclotides from an extreme habitat: characterization of cyclic peptides from / Viola abyssinica of the Ethiopian highlands. J Nat Prod 74(4):727-31 CrossRef
  
• 作者单位：Hossein Hashempour (1) (2)
  Johannes Koehbach (1)
  Norelle L. Daly (3)
  Alireza Ghassempour (2)
  Christian W. Gruber (1)
  
  1. Center for Physiology and Pharmacology, Medical University of Vienna, Schwarzspanierstrasse 17, 1090, Vienna, Austria
  2. Medicinal Plants and Drugs Research Institute, Shahid Beheshti University, G.C. Evin, Tehran, Iran
  3. School of Pharmacy and Molecular Sciences, Centre for Biodiscovery and Molecular Development of Therapeutics, Queensland Tropical Health Alliance, James Cook University, Cairns, 4878, Australia
  
• ISSN：1438-2199

文摘

Cyclotides are a very abundant class of plant peptides that display significant sequence variability around a conserved cystine-knot motif and a head-to-tail cyclized backbone conferring them with remarkable stability. Their intrinsic bioactivities combined with tools of peptide engineering make cyclotides an interesting template for the design of novel agrochemicals and pharmaceuticals. However, laborious isolation and purification prior to de novo sequencing limits their discovery and hence their use as scaffolds for peptide-based drug development. Here we extend the knowledge about their sequence diversity by analysing the cyclotide content of a violet species native to Western Asia and the Caucasus region. Using an experimental approach, which was named sequence fragment assembly by MALDI-TOF/TOF, it was possible to characterize 13 cyclotides from Viola ignobilis, whereof ten (vigno 1-0) display previously unknown sequences. Amino acid sequencing of various enzymatic digests of cyclotides allowed the accurate assembly and alignment of smaller fragments to elucidate their primary structure, even when analysing mixtures containing multiple peptides. As a model to further dissect the combinatorial nature of the cyclotide scaffold, we employed in vitro oxidative refolding of representative vigno cyclotides and confirmed the high dependency of folding yield on the inter-cysteine loop sequences. Overall this work highlights the immense structural diversity and plasticity of the unique cyclotide framework. The presented approach for the sequence analysis of peptide mixtures facilitates and accelerates the discovery of novel plant cyclotides.