Discovery of Cyclotides from Australasian Plants
Meng-Wei Kan A and David J. Craik A BA Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld 4072, Australia.
B Corresponding author. Email: d.craik@imb.uq.edu.au
Meng-Wei Kan grew up in Taiwan and moved to Australia in 1998. She undertook her Ph.D. in medicinal chemistry at the School of Chemistry and Molecular Biosciences at The University of Queensland (UQ) and joined David Craik’s group at the Institute for Molecular Bioscience (IMB) as a senior research administration officer in 2013. Her research interests are in applications of peptide chemistry in medicine and agriculture, with a particular focus on cyclic peptides, including cyclotides. |
David Craik is a Professor of Chemistry at the Institute for Molecular Bioscience (IMB), The University of Queensland (UQ). He obtained his Ph.D. in organic chemistry from La Trobe University in Australia and undertook post-doctoral studies at Florida State and Syracuse Universities, USA, before taking up a lectureship at the Victorian College of Pharmacy in 1983. He moved to UQ in 1995 to set up a biomolecular NMR laboratory and is currently an Australian Research Council Laureate Fellow. His research focuses on applications of cyclic peptides, toxins, and NMR in drug design. He is a Fellow of the Australian Academy of Science and has received numerous awards for his research, including the Hirschmann Award from the American Chemical Society. |
Australian Journal of Chemistry 73(4) 287-299 https://doi.org/10.1071/CH19658
Submitted: 19 December 2019 Accepted: 17 January 2020 Published: 24 March 2020
Abstract
This article is part of a special issue celebrating the contributions of Professor Paul Alewood to peptide science. We begin by providing a summary of collaborative projects between the Alewood and Craik groups at The University of Queensland and highlighting the impacts of some of these studies. In particular, studies on the discovery, synthesis, structures, and bioactivities of disulfide-rich toxins from animal venoms have led to a greater understanding of the biology of ion channels and to applications of these bioactive peptides in drug design. The second part of the article focuses on plant-derived disulfide-rich cyclic peptides, known as cyclotides, and includes an analysis of the geographical distribution of Australasian plant species that contain cyclotides as well as an analysis of the diversity of cyclotide sequences found in Australasian plants. This should provide a useful resource for researchers to access native cyclotides and explore their chemistry and biology.
References
[1] J. R. Ball, D. J. Craik, P. F. Alewood, S. Morrison, P. R. Andrews, I. A. Nicholls, Aust. J. Chem. 1989, 42, 2171.| Crossref | GoogleScholarGoogle Scholar |
[2] K. J. Nielsen, D. Alewood, J. Andrews, S. B. Kent, D. J. Craik, Protein Sci. 1994, 3, 291.
| Crossref | GoogleScholarGoogle Scholar | 8003965PubMed |
[3] I. A. Nicholls, D. J. Craik, P. F. Alewood, Biochem. Biophys. Res. Commun. 1994, 205, 98.
| Crossref | GoogleScholarGoogle Scholar | 7999141PubMed |
[4] J. M. Hill, P. F. Alewood, D. J. Craik, Biochemistry 1996, 35, 8824.
| Crossref | GoogleScholarGoogle Scholar | 8688418PubMed |
[5] S. H. Hu, J. Gehrmann, L. W. Guddat, P. F. Alewood, D. J. Craik, J. L. Martin, Structure 1996, 4, 417.
| Crossref | GoogleScholarGoogle Scholar | 8740364PubMed |
[6] K. J. Nielsen, L. Thomas, R. J. Lewis, P. F. Alewood, D. J. Craik, J. Mol. Biol. 1996, 263, 297.
| Crossref | GoogleScholarGoogle Scholar | 8913308PubMed |
[7] R. Lewis, P. Alewood, M. Dooley, J. Martin, R. Drinkwater, D. J. Craik, P. Andrews, Today’s Life Sci. 1996, 8, 16.
[8] N. Skjærbæk, K. J. Nielsen, R. J. Lewis, P. Alewood, D. J. Craik, J. Biol. Chem. 1997, 272, 2291.
| Crossref | GoogleScholarGoogle Scholar | 8999936PubMed |
[9] J. M. Hill, P. F. Alewood, D. J. Craik, Structure 1997, 5, 571.
| Crossref | GoogleScholarGoogle Scholar | 9115446PubMed |
[10] S. H. Hu, J. Gehrmann, P. F. Alewood, D. J. Craik, J. L. Martin, Biochemistry 1997, 36, 11323.
| Crossref | GoogleScholarGoogle Scholar | 9298951PubMed |
[11] M. J. Scanlon, D. Naranjo, L. Thomas, P. F. Alewood, R. J. Lewis, D. J. Craik, Structure 1997, 5, 1585.
| Crossref | GoogleScholarGoogle Scholar | 9438859PubMed |
[12] J. Gehrmann, P. F. Alewood, D. J. Craik, J. Mol. Biol. 1998, 278, 401.
| Crossref | GoogleScholarGoogle Scholar | 9571060PubMed |
[13] J. M. Hill, C. J. Oomen, L. P. Miranda, J. P. Bingham, P. F. Alewood, D. J. Craik, Biochemistry 1998, 37, 15621.
| Crossref | GoogleScholarGoogle Scholar | 9843366PubMed |
[14] K. J. Nielsen, N. Skjaerbaek, M. Dooley, D. A. Adams, M. Mortensen, P. R. Dodd, D. J. Craik, P. F. Alewood, R. J. Lewis, J. Med. Chem. 1999, 42, 415.
| Crossref | GoogleScholarGoogle Scholar | 9986713PubMed |
[15] K. J. Nielsen, D. A. Adams, P. F. Alewood, R. J. Lewis, L. Thomas, T. Schroeder, D. J. Craik, Biochemistry 1999, 38, 6741.
| Crossref | GoogleScholarGoogle Scholar | 10346894PubMed |
[16] N. L. Daly, S. Love, P. F. Alewood, D. J. Craik, Biochemistry 1999, 38, 10606.
| Crossref | GoogleScholarGoogle Scholar | 10441158PubMed |
[17] J. Gehrmann, N. L. Daly, P. F. Alewood, D. J. Craik, J. Med. Chem. 1999, 42, 2364.
| Crossref | GoogleScholarGoogle Scholar | 10395477PubMed |
[18] K. J. Nielsen, D. Adams, L. Thomas, T. Bond, P. F. Alewood, D. J. Craik, R. J. Lewis, J. Mol. Biol. 1999, 289, 1405.
| Crossref | GoogleScholarGoogle Scholar | 10373375PubMed |
[19] D. J. Adams, P. F. Alewood, D. J. Craik, R. Drinkwater, R. J. Lewis, Drug Dev. Res. 1999, 46, 219.
| Crossref | GoogleScholarGoogle Scholar |
[20] R. C. Hogg, L. P. Miranda, D. J. Craik, R. J. Lewis, P. F. Alewood, D. J. Adams, J. Biol. Chem. 1999, 274, 36559.
| Crossref | GoogleScholarGoogle Scholar | 10593955PubMed |
[21] J. M. Hill, A. R. Atkins, M. L. Loughnan, A. Jones, D. A. Adams, R. C. Martin, R. J. Lewis, D. J. Craik, P. F. Alewood, Eur. J. Biochem. 2000, 267, 4642.
| Crossref | GoogleScholarGoogle Scholar | 10903496PubMed |
[22] J. M. Hill, P. F. Alewood, D. J. Craik, Eur. J. Biochem. 2000, 267, 4649.
| Crossref | GoogleScholarGoogle Scholar | 10903497PubMed |
[23] R. J. Lewis, K. J. Nielsen, D. J. Craik, M. L. Loughnan, D. A. Adams, I. A. Sharpe, T. Luchian, D. J. Adams, T. Bond, L. Thomas, A. Jones, J.-L. Matheson, R. Drinkwater, P. R. Andrews, P. F. Alewood, J. Biol. Chem. 2000, 275, 35335.
| Crossref | GoogleScholarGoogle Scholar | 10938268PubMed |
[24] J. A. Wilce, S. G. Love, S. J. Richardson, P. F. Alewood, D. J. Craik, J. Biol. Chem. 2001, 276, 25997.
| Crossref | GoogleScholarGoogle Scholar | 11352912PubMed |
[25] I. A. Sharpe, J. Gehrmann, M. L. Loughnan, L. Thomas, D. A. Adams, A. Atkins, E. Palant, D. J. Craik, D. J. Adams, P. F. Alewood, R. J. Lewis, Nat. Neurosci. 2001, 4, 902.
| Crossref | GoogleScholarGoogle Scholar | 11528421PubMed |
[26] J. Blanchfield, J. Dutton, R. Hogg, D. Craik, D. Adams, R. Lewis, P. Alewood, I. Toth, Lett. Pept. Sci. 2002, 8, 235.
| Crossref | GoogleScholarGoogle Scholar |
[27] K. J. Rosengren, D. Wilson, N. L. Daly, P. F. Alewood, D. J. Craik, Biochemistry 2002, 41, 3294.
| Crossref | GoogleScholarGoogle Scholar | 11876637PubMed |
[28] K. J. Nielsen, M. Watson, D. J. Adams, A. K. Hammarstrom, P. W. Gage, J. M. Hill, D. J. Craik, L. Thomas, D. Adams, P. F. Alewood, R. J. Lewis, J. Biol. Chem. 2002, 277, 27247.
| Crossref | GoogleScholarGoogle Scholar | 12006587PubMed |
[29] J. L. Dutton, P. S. Bansal, R. C. Hogg, D. J. Adams, P. F. Alewood, D. J. Craik, J. Biol. Chem. 2002, 277, 48849.
| Crossref | GoogleScholarGoogle Scholar | 12376538PubMed |
[30] A. Nicke, M. L. Loughnan, E. L. Millard, P. F. Alewood, D. J. Adams, N. L. Daly, D. J. Craik, R. J. Lewis, J. Biol. Chem. 2003, 278, 3137.
| Crossref | GoogleScholarGoogle Scholar | 12419800PubMed |
[31] J. T. Blanchfield, J. L. Dutton, R. C. Hogg, O. P. Gallagher, D. J. Craik, A. Jones, D. J. Adams, R. J. Lewis, P. F. Alewood, I. Toth, J. Med. Chem. 2003, 46, 1266.
| Crossref | GoogleScholarGoogle Scholar | 12646037PubMed |
[32] D. Alewood, K. Nielsen, P. F. Alewood, D. J. Craik, P. Andrews, M. Nerrie, S. White, T. Domagala, F. Walker, J. Rothacker, A. W. Burgess, E. C. Nice, Growth Factors 2005, 23, 97.
| Crossref | GoogleScholarGoogle Scholar | 16019431PubMed |
[33] K. P. R. Nilsson, E. S. Lovelace, C. E. Caesar, N. Tynngård, P. F. Alewood, H. M. Johansson, I. A. Sharpe, R. J. Lewis, N. L. Daly, D. J. Craik, Biopolymers: Pept. Sci. 2005, 80, 815.
| Crossref | GoogleScholarGoogle Scholar |
[34] P. S. Bansal, P. A. Grieve, R. J. Marschke, N. L. Daly, E. McGhie, D. J. Craik, P. F. Alewood, Biochem. Biophys. Res. Commun. 2006, 340, 1098.
| Crossref | GoogleScholarGoogle Scholar | 16403439PubMed |
[35] C. J. Armishaw, N. L. Daly, S. T. Nevin, D. J. Adams, D. J. Craik, P. F. Alewood, J. Biol. Chem. 2006, 281, 14136.
| Crossref | GoogleScholarGoogle Scholar | 16500898PubMed |
[36] J. S. Imperial, P. S. Bansal, P. F. Alewood, N. L. Daly, D. J. Craik, A. Sporning, H. Terlau, E. Lopez-Vera, P. K. Bandyopadhyay, B. M. Olivera, Biochemistry 2006, 45, 8331.
| Crossref | GoogleScholarGoogle Scholar | 16819832PubMed |
[37] E. S. Lovelace, C. J. Armishaw, M. L. Colgrave, M. E. Wahlstrom, P. F. Alewood, N. L. Daly, D. J. Craik, J. Med. Chem. 2006, 49, 6561.
| Crossref | GoogleScholarGoogle Scholar | 17064074PubMed |
[38] A. H. Jin, H. Brandstaetter, S. T. Nevin, C. C. Tan, R. J. Clark, D. J. Adams, P. F. Alewood, D. J. Craik, N. L. Daly, BMC Struct. Biol. 2007, 7, 28.
| Crossref | GoogleScholarGoogle Scholar | 17445276PubMed |
[39] S. Dutertre, D. Croker, N. L. Daly, A. Andersson, M. Muttenthaler, N. G. Lumsden, D. J. Craik, P. F. Alewood, G. Guillon, R. J. Lewis, J. Biol. Chem. 2008, 283, 7100.
| Crossref | GoogleScholarGoogle Scholar | 18174156PubMed |
[40] A. H. Jin, N. L. Daly, S. T. Nevin, C. I. Wang, S. Dutertre, R. J. Lewis, D. J. Adams, D. J. Craik, P. F. Alewood, J. Med. Chem. 2008, 51, 5575.
| Crossref | GoogleScholarGoogle Scholar | 18754612PubMed |
[41] J. S. Imperial, P. Chen, A. Sporning, H. Terlau, N. L. Daly, D. J. Craik, P. F. Alewood, B. M. Olivera, J. Biol. Chem. 2008, 283, 23026.
| Crossref | GoogleScholarGoogle Scholar | 18505731PubMed |
[42] E. L. Millard, S. T. Nevin, M. L. Loughnan, A. Nicke, R. J. Clark, P. F. Alewood, R. J. Lewis, D. J. Adams, D. J. Craik, N. L. Daly, J. Biol. Chem. 2009, 284, 4944.
| Crossref | GoogleScholarGoogle Scholar | 19098004PubMed |
[43] C. J. Armishaw, J. L. Dutton, D. J. Craik, P. F. Alewood, Biopolymers: Pept. Sci. 2010, 94, 307.
| Crossref | GoogleScholarGoogle Scholar |
[44] M. Muttenthaler, S. T. Nevin, A. A. Grishin, S. T. Ngo, P. T. Choy, N. L. Daly, S. H. Hu, C. J. Armishaw, C. I. Wang, R. J. Lewis, J. L. Martin, P. G. Noakes, D. J. Craik, D. J. Adams, P. F. Alewood, J. Am. Chem. Soc. 2010, 132, 3514.
| Crossref | GoogleScholarGoogle Scholar | 20163143PubMed |
[45] S. Luo, K. B. Akondi, D. Zhangsun, Y. Wu, X. Zhu, Y. Hu, S. Christensen, C. Dowell, N. L. Daly, D. J. Craik, C.-I. A. Wang, R. J. Lewis, P. F. Alewood, J. M. McIntosh, J. Biol. Chem. 2010, 285, 12355.
| Crossref | GoogleScholarGoogle Scholar | 20145249PubMed |
[46] R. A. Morales, N. L. Daly, I. Vetter, M. Mobli, I. A. Napier, D. J. Craik, R. J. Lewis, M. J. Christie, G. F. King, P. F. Alewood, T. Durek, ChemBioChem 2010, 11, 1882.
| Crossref | GoogleScholarGoogle Scholar | 20677202PubMed |
[47] A. D. de Araujo, B. Callaghan, S. T. Nevin, N. L. Daly, D. J. Craik, M. Moretta, G. Hopping, M. J. Christie, D. J. Adams, P. F. Alewood, Angew. Chem. Int. Ed. 2011, 50, 6527.
| Crossref | GoogleScholarGoogle Scholar |
[48] Z. Dekan, I. Vetter, N. L. Daly, D. J. Craik, R. J. Lewis, P. F. Alewood, J. Am. Chem. Soc. 2011, 133, 15866.
| Crossref | GoogleScholarGoogle Scholar | 21899353PubMed |
[49] A. Franco, S. N. Kompella, K. B. Akondi, C. Melaun, N. L. Daly, C. W. Luetje, P. F. Alewood, D. J. Craik, D. J. Adams, F. Mari, Biochem. Pharmacol. 2012, 83, 419.
| Crossref | GoogleScholarGoogle Scholar | 22108175PubMed |
[50] C. I. Schroeder, K. J. Nielsen, D. A. Adams, M. Loughnan, L. Thomas, P. F. Alewood, R. J. Lewis, D. J. Craik, Biopolymers: Pept. Sci. 2012, 98, 345.
| Crossref | GoogleScholarGoogle Scholar |
[51] A. A. Grishin, H. Cuny, A. Hung, R. J. Clark, A. Brust, K. Akondi, P. F. Alewood, D. J. Craik, D. J. Adams, J. Biol. Chem. 2013, 288, 34428.
| Crossref | GoogleScholarGoogle Scholar | 24100032PubMed |
[52] M. C. Inserra, S. N. Kompella, I. Vetter, A. Brust, N. L. Daly, H. Cuny, D. J. Craik, P. F. Alewood, D. J. Adams, R. J. Lewis, Biochem. Pharmacol. 2013, 86, 791.
| Crossref | GoogleScholarGoogle Scholar | 23924607PubMed |
[53] C. I. Schroeder, L. D. Rash, X. Vila-Farres, K. J. Rosengren, M. Mobli, G. F. King, P. F. Alewood, D. J. Craik, T. Durek, Angew. Chem. Int. Ed. 2014, 53, 1017.
| Crossref | GoogleScholarGoogle Scholar |
[54] K. B. Akondi, M. Muttenthaler, S. Dutertre, Q. Kaas, D. J. Craik, R. J. Lewis, P. F. Alewood, Chem. Rev. 2014, 114, 5815.
| Crossref | GoogleScholarGoogle Scholar | 24720541PubMed |
[55] G. Berecki, N. L. Daly, Y. H. Huang, S. Vink, D. J. Craik, P. F. Alewood, D. J. Adams, Br. J. Pharmacol. 2014, 171, 3313.
| Crossref | GoogleScholarGoogle Scholar | 24628243PubMed |
[56] S. Vink, N. L. Daly, N. Steen, D. J. Craik, P. F. Alewood, Toxicon 2014, 90, 308.
| Crossref | GoogleScholarGoogle Scholar | 25172536PubMed |
[57] J. R. Deuis, Z. Dekan, M. C. Inserra, T.-H. Lee, M.-I. Aguilar, D. J. Craik, R. J. Lewis, P. F. Alewood, M. Mobli, C. I. Schroeder, S. T. Henriques, I. Vetter, J. Biol. Chem. 2016, 291, 11829.
| Crossref | GoogleScholarGoogle Scholar | 27026701PubMed |
[58] A.-H. Jin, M. Muttenthaler, S. Dutertre, S. W. A. Himaya, Q. Kaas, D. J. Craik, R. J. Lewis, P. F. Alewood, Chem. Rev. 2019, 119, 11510.
| Crossref | GoogleScholarGoogle Scholar | 31633928PubMed |
[59] A. L. Harvey, Toxicon 2014, 92, 193.
| Crossref | GoogleScholarGoogle Scholar | 25448391PubMed |
[60] M. W. Pennington, A. Czerwinski, R. S. Norton, Bioorg. Med. Chem. 2018, 26, 2738.
| Crossref | GoogleScholarGoogle Scholar | 28988749PubMed |
[61] D. J. Craik, N. L. Daly, T. Bond, C. Waine, J. Mol. Biol. 1999, 294, 1327.
| Crossref | GoogleScholarGoogle Scholar | 10600388PubMed |
[62] D. J. Craik, D. P. Fairlie, S. Liras, D. Price, Chem. Biol. Drug Des. 2013, 81, 136.
| Crossref | GoogleScholarGoogle Scholar | 23253135PubMed |
[63] A. G. Poth, L. Y. Chan, D. J. Craik, Biopolymers: Pept. Sci. 2013, 100, 480.
| Crossref | GoogleScholarGoogle Scholar |
[64] S. E. Northfield, C. K. Wang, C. I. Schroeder, T. Durek, M.-W. Kan, J. E. Swedberg, D. J. Craik, Eur. J. Med. Chem. 2014, 77, 248.
| Crossref | GoogleScholarGoogle Scholar | 24650712PubMed |
[65] D. J. Craik, J. Du, Curr. Opin. Chem. Biol. 2017, 38, 8.
| Crossref | GoogleScholarGoogle Scholar | 28249194PubMed |
[66] J. A. Camarero, Bioorg. Med. Chem. Lett. 2017, 27, 5089.
| Crossref | GoogleScholarGoogle Scholar | 29110985PubMed |
[67] C. K. Wang, D. J. Craik, Nat. Chem. Biol. 2018, 14, 417.
| Crossref | GoogleScholarGoogle Scholar | 29662187PubMed |
[68] J. A. Camarero, M. J. Campbell, Biomedicines 2019, 7, 31.
| Crossref | GoogleScholarGoogle Scholar |
[69] D. Chaudhuri, T. Aboye, J. A. Camarero, Biochem. J. 2019, 476, 67.
| Crossref | GoogleScholarGoogle Scholar | 30635453PubMed |
[70] C. Jennings, J. West, C. Waine, D. Craik, M. Anderson, Proc. Natl. Acad. Sci. USA 2001, 98, 10614.
| Crossref | GoogleScholarGoogle Scholar | 11535828PubMed |
[71] D. J. Craik, D. G. Barry, R. J. Clark, N. L. Daly, L. Sando, Toxin Rev. 2003, 22, 555.
[72] C. W. Gruber, A. G. Elliott, D. C. Ireland, P. G. Delprete, S. Dessein, U. Göransson, M. Trabi, C. K. Wang, A. B. Kinghorn, E. Robbrecht, D. J. Craik, Plant Cell 2008, 20, 2471.
| Crossref | GoogleScholarGoogle Scholar | 18827180PubMed |
[73] L. Gran, Medd. Nor. Farm. Selsk. 1970, 12, 173.
[74] L. Gran, Medd. Nor. Farm. Selsk. 1972, 34, 125.
[75] L. Gran, Lloydia 1973, 36, 174.
| 4744554PubMed |
[76] L. Gran, Lloydia 1973, 36, 207.
[77] L. Gran, Acta Pharmacol. Toxicol. 1973, 33, 400.
| Crossref | GoogleScholarGoogle Scholar |
[78] J. P. Mulvenna, C. Wang, D. J. Craik, Nucleic Acids Res. 2006, 34, D192.
| Crossref | GoogleScholarGoogle Scholar | 16381843PubMed |
[79] C. K. Wang, Q. Kaas, L. Chiche, D. J. Craik, Nucleic Acids Res. 2008, 36, D206.
| Crossref | GoogleScholarGoogle Scholar | 17986451PubMed |
[80] Q. Kaas, D. J. Craik, Biopolymers: Pept. Sci. 2010, 94, 584.
| Crossref | GoogleScholarGoogle Scholar |
[81] J. C. Gelly, J. Gracy, Q. Kaas, D. Le‐Nguyen, A. Heitz, L. Chiche, Nucleic Acids Res. 2004, 32, D156.
| Crossref | GoogleScholarGoogle Scholar | 14681383PubMed |
[82] U. Göransson, R. Burman, S. Gunasekera, A. A. Strömstedt, K. J. Rosengren, J. Biol. Chem. 2012, 287, 27001.
| Crossref | GoogleScholarGoogle Scholar | 22700984PubMed |
[83] S. L. Gerlach, U. Göransson, Q. Kaas, D. J. Craik, D. Mondal, C. W. Gruber, Biopolymers: Pept. Sci. 2013, 100, 433.
| Crossref | GoogleScholarGoogle Scholar |
[84] R. Burman, S. Gunasekera, A. A. Strömstedt, U. Göransson, J. Nat. Prod. 2014, 77, 724.
| Crossref | GoogleScholarGoogle Scholar | 24527877PubMed |
[85] U. Göransson, S. Malik, B. Slazak, in Advances in Botanical Research: Plant Cyclotides (Ed. D. J. Craik) 2015, Vol. 76, Ch. 2, pp. 15–49 (Academic Press: London).
[86] S. J. de Veer, J. Weidmann, D. J. Craik, Acc. Chem. Res. 2017, 50, 1557.
| Crossref | GoogleScholarGoogle Scholar | 28644007PubMed |
[87] H. Qu, B. J. Smithies, T. Durek, D. J. Craik, Aust. J. Chem. 2017, 70, 152.
| Crossref | GoogleScholarGoogle Scholar |
[88] A. Gould, J. A. Camarero, ChemBioChem 2017, 18, 1350.
| Crossref | GoogleScholarGoogle Scholar | 28544675PubMed |
[89] M.-W. Kan, D. J. Craik, in Cyclic Peptides: From Bioorganic Synthesis to Applications (Eds J. Koehnke, J. Naismith, W. A. van der Donk) 2018, Ch. 14, pp. 302–339 (The Royal Society of Chemistry: London).
[90] S. J. de Veer, M.-W. Kan, D. J. Craik, Chem. Rev. 2019, 119, 12375.
| Crossref | GoogleScholarGoogle Scholar | 31829013PubMed |
[91] Y.-H. Huang, Q. Du, D. J. Craik, Toxicon 2019, 172, 33.
| Crossref | GoogleScholarGoogle Scholar | 31682883PubMed |
[92] D. J. Craik (Ed.), Advances in Botanical Research: Plant Cyclotides Vol. 76 2015 (Academic Press: London).
[93] D. J. Craik, J. Pept. Sci. 2013, 19, 393.
| Crossref | GoogleScholarGoogle Scholar | 23737440PubMed |
[94] S. L. Gerlach, D. Mondal, Chron. Young Sci. 2012, 3, 169.
| Crossref | GoogleScholarGoogle Scholar |
[95] M. Trabi, E. Svangård, A. Herrmann, U. Göransson, P. Claeson, D. J. Craik, L. Bohlin, J. Nat. Prod. 2004, 67, 806.
| Crossref | GoogleScholarGoogle Scholar | 15165141PubMed |
[96] M. Trabi, D. J. Craik, Plant Cell 2004, 16, 2204.
| Crossref | GoogleScholarGoogle Scholar | 15295104PubMed |
[97] E. K. Gilding, M. A. Jackson, A. G. Poth, S. T. Henriques, P. J. Prentis, T. Mahatmanto, D. J. Craik, New Phytol. 2016, 210, 717.
| Crossref | GoogleScholarGoogle Scholar | 26668107PubMed |
[98] T. Mahatmanto, A. G. Poth, J. S. Mylne, D. J. Craik, Fitoterapia 2014, 95, 22.
| Crossref | GoogleScholarGoogle Scholar | 24613804PubMed |
[99] T. Mahatmanto, J. S. Mylne, A. G. Poth, J. E. Swedberg, Q. Kaas, H. Schaefer, D. J. Craik, Mol. Biol. Evol. 2015, 32, 392.
| Crossref | GoogleScholarGoogle Scholar | 25376175PubMed |
[100] A. M. Broussalis, U. Göransson, J. D. Coussio, G. Ferraro, V. Martino, P. Claeson, Phytochemistry 2001, 58, 47.
| Crossref | GoogleScholarGoogle Scholar | 11524112PubMed |
[101] R. Burman, M. Y. Yeshak, S. Larsson, D. J. Craik, K. J. Rosengren, U. Göransson, Front. Plant Sci. 2015, 6, 855.
| Crossref | GoogleScholarGoogle Scholar | 26579135PubMed |
[102] P. Niyomploy, L. Y. Chan, A. G. Poth, M. L. Colgrave, P. Sangvanich, D. J. Craik, Biopolymers: Pept. Sci. 2016, 106, 796.
| Crossref | GoogleScholarGoogle Scholar |
[103] P. Niyomploy, L. Y. Chan, P. J. Harvey, A. G. Poth, M. L. Colgrave, D. J. Craik, J. Nat. Prod. 2018, 81, 2512.
| Crossref | GoogleScholarGoogle Scholar | 30387611PubMed |
[104] J. Zhang, Z. S. Hua, Z. B. Huang, Q. Z. Chen, Q. Y. Long, D. J. Craik, A. J. M. Baker, W. S. Shu, B. Liao, Planta 2015, 241, 929.
| Crossref | GoogleScholarGoogle Scholar | 25528148PubMed |
[105] A.-H. Jin, I. Vetter, S. W. A. Himaya, P. F. Alewood, R. J. Lewis, S. Dutertre, Proteomics 2015, 15, 4030.
| Crossref | GoogleScholarGoogle Scholar | 26506909PubMed |
[106] D. C. Ireland, M. L. Colgrave, P. Nguyencong, N. L. Daly, D. J. Craik, J. Mol. Biol. 2006, 357, 1522.
| Crossref | GoogleScholarGoogle Scholar | 16488428PubMed |
[107] G. K. T. Nguyen, S. Zhang, W. Wang, C. T. T. Wong, T. K. N. Ngan, J. P. Tam, J. Biol. Chem. 2011, 286, 44833.
| Crossref | GoogleScholarGoogle Scholar |
[108] G. K. T. Nguyen, W. H. Lim, P. Q. T. Nguyen, J. P. Tam, J. Biol. Chem. 2012, 287, 17598.
| Crossref | GoogleScholarGoogle Scholar |
[109] A. G. Poth, J. S. Mylne, J. Grassl, R. E. Lyons, A. H. Millar, M. L. Colgrave, D. J. Craik, J. Biol. Chem. 2012, 287, 27033.
| Crossref | GoogleScholarGoogle Scholar | 22700981PubMed |
[110] J. L. Dutton, R. F. Renda, C. Waine, R. J. Clark, N. L. Daly, C. V. Jennings, M. A. Anderson, D. J. Craik, J. Biol. Chem. 2004, 279, 46858.
| Crossref | GoogleScholarGoogle Scholar | 15328347PubMed |
[111] D. C. Ireland, M. L. Colgrave, D. J. Craik, Biochem. J. 2006, 400, 1.
| Crossref | GoogleScholarGoogle Scholar | 16872274PubMed |
[112] M. L. Colgrave, A. G. Poth, Q. Kaas, D. J. Craik, Biopolymers: Pept. Sci. 2010, 94, 592.
| Crossref | GoogleScholarGoogle Scholar |
[113] B. Chen, M. L. Colgrave, N. L. Daly, K. J. Rosengren, K. R. Gustafson, D. J. Craik, J. Biol. Chem. 2005, 280, 22395.
| Crossref | GoogleScholarGoogle Scholar | 15824119PubMed |
[114] B. Chen, M. L. Colgrave, C. Wang, D. J. Craik, J. Nat. Prod. 2006, 69, 23.
| Crossref | GoogleScholarGoogle Scholar | 16441062PubMed |
[115] N. L. Daly, B. Chen, P. Nguyencong, D. J. Craik, Aust. J. Chem. 2010, 63, 771.
| Crossref | GoogleScholarGoogle Scholar |
[116] A. S. Ravipati, A. G. Poth, S. T. Henriques, M. Bhandari, Y. H. Huang, J. Nino, M. L. Colgrave, D. J. Craik, J. Nat. Prod. 2017, 80, 1522.
| Crossref | GoogleScholarGoogle Scholar | 28471681PubMed |
[117] P. Claeson, U. Göransson, S. Johansson, T. Luijendijk, L. Bohlin, J. Nat. Prod. 1998, 61, 77.
| Crossref | GoogleScholarGoogle Scholar | 9548831PubMed |
[118] A. S. Ravipati, S. T. Henriques, A. G. Poth, Q. Kaas, C. K. Wang, M. L. Colgrave, D. J. Craik, ACS Chem. Biol. 2015, 10, 2491.
| Crossref | GoogleScholarGoogle Scholar | 26322745PubMed |
[119] M. Trabi, J. S. Mylne, L. Sando, D. J. Craik, Org. Biomol. Chem. 2009, 7, 2378.
| Crossref | GoogleScholarGoogle Scholar | 19462049PubMed |
[120] S. M. Simonsen, L. Sando, D. C. Ireland, M. L. Colgrave, R. Bharathi, U. Göransson, D. J. Craik, Plant Cell 2005, 17, 3176.
| Crossref | GoogleScholarGoogle Scholar | 16199617PubMed |
[121] C. T. Wong, M. Taichi, H. Nishio, Y. Nishiuchi, J. P. Tam, Biochemistry 2011, 50, 7275.
| Crossref | GoogleScholarGoogle Scholar | 21776968PubMed |
[122] A. G. Poth, M. L. Colgrave, R. Philip, B. Kerenga, N. L. Daly, M. A. Anderson, D. J. Craik, ACS Chem. Biol. 2011, 6, 345.
| Crossref | GoogleScholarGoogle Scholar | 21194241PubMed |
[123] A. G. Poth, M. L. Colgrave, R. E. Lyons, N. L. Daly, D. J. Craik, Proc. Natl. Acad. Sci. USA 2011, 108, 10127.
| Crossref | GoogleScholarGoogle Scholar | 21593408PubMed |
[124] M. E. Felizmenio-Quimio, N. L. Daly, D. J. Craik, J. Biol. Chem. 2001, 276, 22875.
| Crossref | GoogleScholarGoogle Scholar | 11292835PubMed |
[125] J. S. Mylne, L. Y. Chan, A. H. Chanson, N. L. Daly, H. Schaefer, T. L. Bailey, P. Nguyencong, L. Cascales, D. J. Craik, Plant Cell 2012, 24, 2765.
| Crossref | GoogleScholarGoogle Scholar | 22822203PubMed |
[126] U. Göransson, T. Luijendijk, S. Johansson, L. Bohlin, P. Claeson, J. Nat. Prod. 1999, 62, 283.
| Crossref | GoogleScholarGoogle Scholar | 10075760PubMed |