Synthesis and Protein Engineering Applications of Cyclotides
Haiou Qu A , Bronwyn J. Smithies A , Thomas Durek A and David J. Craik A B
+ Author Affiliations
- Author Affiliations
A Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld 4072, Australia.
B Corresponding author. Email: d.craik@imb.uq.edu.au
Haiou Qu is a second year Ph.D. student under the supervision of Professor D. Craik at the Institute for Molecular Bioscience, The University of Queensland. She received her B.Sc. (2012) from Northeast Forestry University and an M.Sc. in biology (2015) from Shanghai Jiao Tong University. Her research interests are in cyclotide expression in plants, and her current project is focused on the application of rice as a bioreactor to express cyclotides. |
Bronwyn Smithies received her bachelor's degree in biotechnology and medical research (Hons) from the University of Tasmania in 2013. In 2016, she commenced her Ph.D. studies at the Institute for Molecular Bioscience, The University of Queensland, in Professor David Craik's laboratory. Her research focuses on taking synthetic designer peptides and expressing them recombinantly in biological systems, especially plants. |
Thomas Durek obtained his Ph.D. degree from the Max-Planck Institute for Molecular Physiology, Dortmund, Germany. After a post-doctoral stay with Stephen Kent at the University of Chicago, he moved to The University of Queensland. His research interests are in peptide and protein chemistry, biophysics, structural biology (NMR and X-ray) as well as ion channel and GPCR pharmacology. |
David Craik is an ARC Australian Laureate Fellow at the Institute for Molecular Bioscience, The University of Queensland. He completed his Ph.D. degree in organic chemistry at La Trobe University in 1981 and after two years of post-doctoral work in the USA, he returned to Australia to a faculty position at the Victorian College of Pharmacy. He moved to UQ in 1995 to set up a new biomolecular NMR laboratory. His research focuses on the discovery and applications of peptides in drug design. |
Australian Journal of Chemistry 70(2) 152-161 https://doi.org/10.1071/CH16589
Submitted: 17 October 2016 Accepted: 1 November 2016 Published: 24 November 2016
Abstract
Cyclotides are a group of plant-derived peptides with a head-to-tail cyclized backbone that is stabilized by three knotted disulfide bonds. Their exceptional stability and tolerance for residue substitutions have led to interest in their application as drug design scaffolds. To date, chemical synthesis has been the dominant methodology for producing cyclotides and their analogues. Native chemical ligation is the most common strategy to generate the cyclic backbone and has been highly successful at producing a wide range of cyclotides for studies of structure–activity relationships. Both this and other chemical approaches require a specific linker at the C-terminus and typically involve a non-directed folding (disulfide oxidation) regimen, which can sometimes be a limiting factor in final yields. Following the recent discovery of enzymes involved in peptide cyclization in planta, site-specific and highly efficient enzymatic ligations have been used for synthetic cyclotide backbone cyclization. In this review, chemical synthesis strategies and approaches involving cyclization via enzymes for the production of cyclotides are described.
References
[1] D. J. Craik, N. L. Daly, T. Bond, C. Waine, J. Mol. Biol. 1999, 294, 1327.| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvFaqsLs%3D&md5=316c6d052fde9be5c2a8cc8bae8461e7CAS |
[2] M. L. Colgrave, D. J. Craik, Biochemistry 2004, 43, 5965.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFGgsL4%3D&md5=aa1aa9137100709fb5433ab4691f7eacCAS |
[3] S. T. Henriques, D. J. Craik, ACS Chem. Biol. 2012, 7, 626.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVOltA%3D%3D&md5=3fd2c9078b1b2ed14c2ecc624e2d0a2dCAS |
[4] 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 | 1:CAS:528:DC%2BD1cXhtlCnsLjJ&md5=402da720dc3d434c578691371473d2c4CAS |
[5] 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 | 1:CAS:528:DC%2BC3MXot1ahtg%3D%3D&md5=9fab42ab60d81420d2801d830b9d0a44CAS |
[6] 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 | 1:CAS:528:DC%2BC38XhtFaqtrrP&md5=278409382564316f1cc86ff5f66f9504CAS |
[7] L. Chiche, A. Heitz, J. C. Gelly, J. Gracy, P. T. Chau, P. T. Ha, J. F. Hernandez, D. Le-Nguyen, Curr. Protein Pept. Sci. 2004, 5, 341.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFGjtbY%3D&md5=246fcfcf4d375370e84051116650f79dCAS |
[8] J. P. Mulvenna, C. Wang, D. J. Craik, Nucleic Acids Res. 2006, 34, D192.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFOiuw%3D%3D&md5=45a22560fd80bdaf17e3db5f55c583d9CAS |
[9] J. F. Hernandez, J. Gagnon, L. Chiche, T. M. Nguyen, J. P. Andrieu, A. Heitz, T. Trinh Hong, T. T. Pham, D. Le Nguyen, Biochemistry 2000, 39, 5722.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFChsLo%3D&md5=48427f89e976e1da0689cf7d636573dbCAS |
[10] L. Gran, Medd. Nor. Farm. Selsk. 1970, 12, 173.
[11] M. L. Colgrave, A. C. Kotze, D. C. Ireland, C. K. Wang, D. J. Craik, ChemBioChem 2008, 9, 1939.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVegs7nI&md5=07440e251473eccf42622752692babddCAS |
[12] M. R. R. Plan, I. Saska, A. G. Cagauan, D. J. Craik, J. Agric. Food Chem. 2008, 56, 5237.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Wit7s%3D&md5=9739a7ade51f25a6383c98a0fcca2c33CAS |
[13] C. Jennings, J. West, C. Waine, D. Craik, M. Anderson, Proc. Natl. Acad. Sci. USA 2001, 98, 10614.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVGnu74%3D&md5=5657408bdc759325114742b3677f0957CAS |
[14] N. L. Daly, K. R. Gustafson, D. J. Craik, FEBS Lett. 2004, 574, 69.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFGlsr0%3D&md5=abb6fa0f7a6bf3c839628a25d886cc00CAS |
[15] C. K. Wang, M. L. Colgrave, K. R. Gustafson, D. C. Ireland, U. Göransson, D. J. Craik, J. Nat. Prod. 2008, 71, 47.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVehur7P&md5=32c6741414cf9d8f308effb7e9a57a23CAS |
[16] 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 | 1:CAS:528:DC%2BD2MXksl2htLw%3D&md5=32b971dec26b459989afdffd4a967620CAS |
[17] M. Pränting, C. Loov, R. Burman, U. Göransson, D. I. Andersson, J. Antimicrob. Chemother. 2010, 65, 1964.
| Crossref | GoogleScholarGoogle Scholar |
[18] I. C. M. Fensterseifer, O. N. Silva, U. Malik, A. S. Ravipati, N. R. F. Novaes, P. R. R. Miranda, E. A. Rodrigues, S. E. Moreno, D. J. Craik, O. L. Franco, Peptides 2015, 63, 38.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFCnsbnE&md5=f6918e26d0f397634ce67cf779852034CAS |
[19] C. Gründemann, J. Koehbach, R. Huber, C. W. Gruber, J. Nat. Prod. 2012, 75, 167.
| Crossref | GoogleScholarGoogle Scholar |
[20] R. Hellinger, J. Koehbach, H. Fedchuk, B. Sauer, R. Huber, C. W. Gruber, C. Gründemann, J. Ethnopharmacol. 2014, 151, 299.
| Crossref | GoogleScholarGoogle Scholar |
[21] D. G. Barry, N. L. Daly, R. J. Clark, L. Sando, D. J. Craik, Biochemistry 2003, 42, 6688.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsleisr0%3D&md5=499518bf2072072d10edcf5e50eea7a7CAS |
[22] J. Tang, C. K. Wang, X. Pan, H. Yan, G. Zeng, W. Xu, W. He, N. L. Daly, D. J. Craik, N. Tan, Peptides 2010, 31, 1434.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVahtrY%3D&md5=c81f976863c67eb7042474d8392fe144CAS |
[23] X. M. Ding, D. S. Bai, J. J. Qian, Med. Chem. Res. 2014, 23, 1406.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlOrtrjK&md5=0b449f75a90afae105c31820d2e69479CAS |
[24] A. Herrmann, R. Burman, J. S. Mylne, G. Karlsson, J. Gullbo, D. J. Craik, R. J. Clark, U. Göransson, Phytochemistry 2008, 69, 939.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhslGrs7c%3D&md5=e7030fd3c37286d880986648efe1beaaCAS |
[25] C. W. Gruber, M. Cemazar, R. J. Clark, T. Horibe, R. F. Renda, M. A. Anderson, D. J. Craik, J. Biol. Chem. 2007, 282, 20435.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsFWnurw%3D&md5=4fd48c6e6f266ca257f50ddb346e7210CAS |
[26] S. T. Henriques, Y. H. Huang, K. J. Rosengren, H. G. Franquelim, F. A. Carvalho, A. Johnson, S. Sonza, G. Tachedjian, M. A. R. B. Castanho, N. L. Daly, D. J. Craik, J. Biol. Chem. 2011, 286, 24231.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1GltL4%3D&md5=7f13d4738f10af27eb9d8183db6b0b6aCAS |
[27] Y.-H. Huang, M. L. Colgrave, N. L. Daly, A. Keleshian, B. Martinac, D. J. Craik, J. Biol. Chem. 2009, 284, 20699.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFWrtro%3D&md5=60f995fc9b8daf4271227d8ffffac169CAS |
[28] D. J. Craik, M. Cěmažar, C. K. Wang, N. L. Daly, Biopolymers 2006, 84, 250.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1Gkt78%3D&md5=6bc56b37071f72adb8f71d8b5b007771CAS |
[29] S. T. Henriques, D. J. Craik, Drug Discovery Today 2010, 15, 57.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsV2iuw%3D%3D&md5=2a7d89bb6f34aeab0fe41f84eab4058bCAS |
[30] R. J. Clark, N. L. Daly, D. J. Craik, Biochem. J. 2006, 394, 85.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsVansA%3D%3D&md5=a9f688e1fec6782745c22b7db3d63b69CAS |
[31] X. Jia, S. Kwon, C. I. Wang, Y. H. Huang, L. Y. Chan, C. C. Tan, K. J. Rosengren, J. P. Mulvenna, C. I. Schroeder, D. J. Craik, J. Biol. Chem. 2014, 289, 6627.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjvVyltLk%3D&md5=46dfbca31458ebedc00d0c7fb4ea2429CAS |
[32] Y. Ji, S. Majumder, M. Millard, R. Borra, T. Bi, A. Y. Elnagar, N. Neamati, A. Shekhtman, J. A. Camarero, J. Am. Chem. Soc. 2013, 135, 11623.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSis7nL&md5=062d957ae169df3411c524821f1d9728CAS |
[33] B. Merrifield, Methods Enzymol. 1997, 289, 3.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXotVylurs%3D&md5=736e149cb2cdf3051d071e3b49ad43e6CAS |
[34] T. L. Aboye, J. A. Camarero, J. Biol. Chem. 2012, 287, 27026.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFaqtrrN&md5=cf4b927942487afb92db331a31519d79CAS |
[35] I. Saska, A. D. Gillon, N. Hatsugai, R. G. Dietzgen, I. Hara-Nishimura, M. A. Anderson, D. J. Craik, J. Biol. Chem. 2007, 282, 29721.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2nur7E&md5=81733250cad207f74a628517ea2965f8CAS |
[36] A. D. Gillon, I. Saska, C. V. Jennings, R. F. Guarino, D. J. Craik, M. A. Anderson, Plant J. 2008, 53, 505.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFSnu7c%3D&md5=623c965a298bfc52a47f4bee85c00feaCAS |
[37] G. K. Nguyen, S. Wang, Y. Qiu, X. Hemu, Y. Lian, J. P. Tam, Nat. Chem. Biol. 2014, 10, 732.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFygs7jL&md5=d9f36086940149292d69d8c6c6cefbdcCAS |
[38] K. S. Harris, T. Durek, Q. Kaas, A. G. Poth, E. K. Gilding, B. F. Conlan, I. Saska, N. L. Daly, N. L. van der Weerden, D. J. Craik, M. A. Anderson, Nat. Commun. 2015, 6, 10199.
| 1:CAS:528:DC%2BC2MXitVKrsLrK&md5=86f9821ee97c3d02ed8a59e513c1a6d9CAS |
[39] X. Hemu, Y. Qiu, G. K. T. Nguyen, J. P. Tam, J. Am. Chem. Soc. 2016, 138, 6968.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XotlaltL8%3D&md5=c3a32fbebe154f681366493a447d0907CAS |
[40] X. Hemu, Y. B. Qiu, J. P. Tam, Tetrahedron 2014, 70, 7707.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVWgsr%2FK&md5=a378bd261f10da1d00509fc1829be71dCAS |
[41] G. K. Nguyen, Y. Qiu, Y. Cao, X. Hemu, C.-F. Liu, J. P. Tam, Nat. Protoc. 2016, 11, 1977.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFGgt7jJ&md5=c36708fa105923678cb119437133438bCAS |
[42] U. C. Marx, M. L. Korsinczky, H. J. Schirra, A. Jones, B. Condie, L. Otvos, D. J. Craik, J. Biol. Chem. 2003, 278, 21782.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVemtr4%3D&md5=3787bcb91aeefd375b6550aa345900c3CAS |
[43] P. Thongyoo, A. M. Jaulent, E. W. Tate, R. J. Leatherbarrow, ChemBioChem 2007, 8, 1107.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlGhsb4%3D&md5=0c13c7d35160d9bd5862e592444ac8cbCAS |
[44] P. Thongyoo, N. Roque-Rosell, R. J. Leatherbarrow, E. W. Tate, Org. Biomol. Chem. 2008, 6, 1462.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktV2gur4%3D&md5=2cb3c6ba328604cccc3ff80036a00a18CAS |
[45] S. Tsukiji, T. Nagamune, ChemBioChem 2009, 10, 787.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVajt7o%3D&md5=aa69777274167087fa752578b7a1f4b6CAS |
[46] K. Stanger, T. Maurer, H. Kaluarachchi, M. Coons, Y. Franke, R. N. Hannoush, FEBS Lett. 2014, 588, 4487.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVartrnO&md5=4408171555eee3d76048d8eb404359f2CAS |
[47] C. P. Scott, E. Abel-Santos, M. Wall, D. C. Wahnon, S. J. Benkovic, Proc. Natl. Acad. Sci. USA 1999, 96, 13638.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1OqsLg%3D&md5=65686df2ff77a7d81f172430ed8ea245CAS |
[48] J. Austin, W. Wang, S. Puttamadappa, A. Shekhtman, J. A. Camarero, ChemBioChem 2009, 10, 2663.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlans7bO&md5=f29822944388ff7651d3bb0fe0c93639CAS |
[49] S. M. Simonsen, L. Sando, K. J. Rosengren, C. K. Wang, M. L. Colgrave, N. L. Daly, D. J. Craik, J. Biol. Chem. 2008, 283, 9805.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1aksbY%3D&md5=c3fe61393503d6bf837110972fc977d0CAS |
[50] Y. H. Huang, M. L. Colgrave, R. J. Clark, A. C. Kotze, D. J. Craik, J. Biol. Chem. 2010, 285, 10797.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFaisrY%3D&md5=09a0b98f7605dee847dea570e07f3f4dCAS |
[51] A. G. Poth, L. Y. Chan, D. J. Craik, Biopolymers 2013, 100, 480.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXls1Cqs7o%3D&md5=eb9c849f228759b3e2ab18e09fb6a38eCAS |
[52] Y. H. Huang, S. Chaousis, O. Cheneval, D. J. Craik, S. T. Henriques, Front. Pharmacol. 2015, 6, 17.
[53] C. K. Wang, C. W. Gruber, M. Cěmažar, C. Siatskas, P. Tagore, N. Payne, G. Sun, S. Wang, C. C. Bernard, D. J. Craik, ACS Chem. Biol. 2014, 9, 156.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Cktb7L&md5=5952ecab22edeecee77bfa17279899eaCAS |
[54] G. K. Oguis, M. W. Kan, D. J. Craik, in Advances in Botanical Research (Ed. D. J. Craik) 2015, Vol. 76, Ch. 7, pp. 187–226 (Academic Press: Maryland Heights, MO).
[55] J. Weidmann, D. J. Craik, J. Exp. Bot. 2016, 67, 4801.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVejs7fN&md5=1631eb05ef713a14b331d55459b09858CAS |
[56] J. A. Camarero, R. H. Kimura, Y. H. Woo, A. Shekhtman, J. Cantor, ChemBioChem 2007, 8, 1363.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXps1alt7k%3D&md5=3969e10c5540315f61bfb38834dad7baCAS |
[57] K. Jagadish, A. Gould, R. Borra, S. Majumder, Z. Mushtaq, A. Shekhtman, J. A. Camarero, Angew. Chem., Int. Ed. 2015, 54, 8390.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVensLrE&md5=51b2922f94cf326aee655bddf7048cf6CAS |
[58] J. P. Tam, Y.-A. Lu, Q. Yu, J. Am. Chem. Soc. 1999, 121, 4316.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFOmsLw%3D&md5=6294eb34b8a0a645030752fb8f191b70CAS |
[59] O. Cheneval, C. I. Schroeder, T. Durek, P. Walsh, Y.-H. Huang, S. Liras, D. A. Price, D. J. Craik, J. Org. Chem. 2014, 79, 5538.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXos1Wksrw%3D&md5=ae16587b814ba640279275f990dcdd2dCAS |
[60] J. B. Blanco-Canosa, P. E. Dawson, Angew. Chem., Int. Ed. 2008, 47, 6851.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2iurjK&md5=6fb2d10cb31e79fc15a4d18094d2f9caCAS |
[61] J. B. Blanco-Canosa, B. Nardone, F. Albericio, P. E. Dawson, J. Am. Chem. Soc. 2015, 137, 7197.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosVChsbw%3D&md5=8b589617df861292fc76f507adb96686CAS |
[62] S. Gunasekera, T. Aboye, W. Madian, H. El-Seedi, U. Göransson, Int. J. Pept. Res. Ther. 2013, 19, 43.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2qtbbF&md5=e2dc749cd432efe7606aa3b4c5122202CAS |
[63] G. M. Fang, Y. M. Li, F. Shen, Y. C. Huang, J. B. Li, Y. Lin, H. K. Cui, L. Liu, Angew. Chem., Int. Ed. 2011, 50, 7645.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntV2rsr8%3D&md5=684cc6a193e96fefab162f3f66c0deb9CAS |
[64] J. S. Zheng, S. Tang, Y. Guo, H. N. Chang, L. Liu, ChemBioChem 2012, 13, 542.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsF2qtr0%3D&md5=662b536d5b9667e972c3df5480171a04CAS |
[65] L. Raibaut, H. Adihou, R. Desmet, A. F. Delmas, V. Aucagne, O. Melnyk, Chem. Sci. 2013, 4, 4061.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlentrbN&md5=cee0ce3517c8c0a0a3fe4c2ac3d50170CAS |
[66] T. Aboye, C. Meeks, S. Majumder, A. Shekhtman, K. Rodgers, J. Camarero, Molecules 2016, 21, 152.
| Crossref | GoogleScholarGoogle Scholar |
[67] T. L. Aboye, H. Ha, S. Majumder, F. Christ, Z. Debyser, A. Shekhtman, N. Neamati, J. A. Camarero, J. Med. Chem. 2012, 55, 10729.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Ohs7vM&md5=341ae3edb0c841b3be98a8f6fb21abecCAS |
[68] T. Aboye, Y. Kuang, N. Neamati, J. A. Camarero, ChemBioChem 2015, 16, 827.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXksF2htrk%3D&md5=a96d6190416e85a5f280b1d14d45e87dCAS |
[69] T. L. Aboye, R. J. Clark, D. J. Craik, U. Göransson, ChemBioChem 2008, 9, 103.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1Wiu7w%3D&md5=60e401dee41e758350311cfb081ddfceCAS |
[70] S. Gunasekera, N. Daly, R. Clark, D. J. Craik, Antioxid. Redox Signaling 2009, 11, 971.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkt1Chsbw%3D&md5=9f1a0b60bc5f8730bf9b2cd8fa44fbf4CAS |
[71] N. L. Daly, S. Love, P. F. Alewood, D. J. Craik, Biochemistry 1999, 38, 10606.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVOltLo%3D&md5=0b29ed360b40d72c609fcf09004fe484CAS |
[72] J. S. Mylne, M. L. Colgrave, N. L. Daly, A. H. Chanson, A. G. Elliott, E. J. McCallum, A. Jones, D. J. Craik, Nat. Chem. Biol. 2011, 7, 257.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKrsrs%3D&md5=19946192392464bac807235894bfaa65CAS |
[73] G. K. Nguyen, X. Hemu, J. P. Quek, J. P. Tam, Angew. Chem., Int. Ed. 2016, 55, 12802.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFWntbvK&md5=86ac412aa2436299bdf18916f900c90fCAS |
[74] G. K. Nguyen, A. Kam, S. Loo, A. E. Jansson, L. X. Pan, J. P. Tam, J. Am. Chem. Soc. 2015, 137, 15398.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFGns7zK&md5=fe3a58efa81b8c880965dc1c42944d28CAS |
[75] C. J. Barber, P. T. Pujara, D. W. Reed, S. Chiwocha, H. Zhang, P. S. Covello, J. Biol. Chem. 2013, 288, 12500.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvF2hsbw%3D&md5=652180d7d8abfd147b7bdd190535f3caCAS |
[76] J. Haase, E. Lanka, J. Bacteriol. 1997, 179, 5728.
| 1:CAS:528:DyaK2sXmt1Ggsbw%3D&md5=dd868715ec05cd975b123ce84cdaba50CAS |
[77] J. Lee, J. McIntosh, B. J. Hathaway, E. W. Schmidt, J. Am. Chem. Soc. 2009, 131, 2122.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVaqtrw%3D&md5=53816ffa427e4c85b12e828e15080644CAS |
[78] L. Cascales, S. T. Henriques, M. C. Kerr, Y. H. Huang, M. J. Sweet, N. L. Daly, D. J. Craik, J. Biol. Chem. 2011, 286, 36932.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlSqtLvM&md5=a60b0c77136b3c8e233d939e78a2b10dCAS |
[79] S. K. Mazmanian, G. Liu, H. Ton-That, O. Schneewind, Science 1999, 285, 760.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVehu7Y%3D&md5=dfff58b0953c3a501deb2f6ab09aa9b2CAS |
[80] M. W. L. Popp, H. L. Ploegh, Angew. Chem., Int. Ed. 2011, 50, 5024.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFymu7g%3D&md5=bdfa77daeb410d824604746589c0cc83CAS |
[81] J. G. Bolscher, M. J. Oudhoff, K. Nazmi, J. M. Antos, C. P. Guimaraes, E. Spooner, E. F. Haney, J. J. G. Vallejo, H. J. Vogel, W. van’t Hof, FASEB J. 2011, 25, 2650.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFers7o%3D&md5=df0f2964be136a01eb3d7e2a88523691CAS |
[82] T. Matsumoto, S. Sawamoto, T. Sakamoto, T. Tanaka, H. Fukuda, A. Kondo, J. Biotechnol. 2011, 152, 37.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisF2isbo%3D&md5=6ecfc69cebb3c8602c24a53e8119b97cCAS |
[83] R. J. Clark, J. Jensen, S. T. Nevin, B. P. Callaghan, D. J. Adams, D. J. Craik, Angew. Chem., Int. Ed. 2010, 49, 6545.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFamur3N&md5=3e4ea972da500de5b7c228a0c56ceca9CAS |
[84] I. Chen, B. M. Dorr, D. R. Liu, Proc. Natl. Acad. Sci. USA 2011, 108, 11399.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlartb4%3D&md5=f0eccef39fadf39f13b28aca88392931CAS |
[85] S. Gunasekera, F. M. Foley, R. J. Clark, L. Sando, L. J. Fabri, D. J. Craik, N. L. Daly, J. Med. Chem. 2008, 51, 7697.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOjsL3F&md5=34ca03042081083cb262963537369c0eCAS |
[86] C. T. T. Wong, D. K. Rowlands, C. H. Wong, T. W. C. Lo, G. K. T. Nguyen, H. Y. Li, J. P. Tam, Angew. Chem., Int. Ed. 2012, 51, 5620.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFersrg%3D&md5=4e3753486827f98a98a63931f44caf88CAS |
[87] V. R. Pattabiraman, J. W. Bode, Nature 2011, 480, 471.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1GksL3L&md5=4a4d07562b970ae49a315f72166f4b44CAS |
[88] Y. Li, T. Bi, J. A. Camarero, in Advances in Botanical Research (Ed. D. J. Craik) 2015, Vol. 76, Ch. 9, pp. 271–303 (Academic Press: Maryland Heights, MO).
[89] J. A. Getz, J. J. Rice, P. S. Daugherty, ACS Chem. Biol. 2011, 6, 837.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWhsb8%3D&md5=0e480f551af5b67bd844bb1ba32b326eCAS |
[90] R. Eliasen, N. L. Daly, B. S. Wulff, T. L. Andresen, K. W. Conde-Frieboes, D. J. Craik, J. Biol. Chem. 2012, 287, 40493.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslansbbF&md5=4d2bd097b24d857839b4eca7c4ee9e1dCAS |
[91] J. A. Getz, O. Cheneval, D. J. Craik, P. S. Daugherty, ACS Chem. Biol. 2013, 8, 1147.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkslWgu7w%3D&md5=0a2ed394dc216fb1786de8569fa55c5cCAS |
[92] P. Thongyoo, C. Bonomelli, R. J. Leatherbarrow, E. W. Tate, J. Med. Chem. 2009, 52, 6197.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKns7jN&md5=4ef5450c084c2b290dfd5a9358e1148dCAS |
[93] C. P. Sommerhoff, O. Avrutina, H. U. Schmoldt, D. Gabrijelcic-Geiger, U. Diederichsen, H. Kolmar, J. Mol. Biol. 2010, 395, 167.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2msr7M&md5=e19ee8896f4fc7db3c65fa0d4df8ad6bCAS |
[94] L. Y. Chan, S. Gunasekera, S. T. Henriques, N. F. Worth, S. J. Le, R. J. Clark, J. H. Campbell, D. J. Craik, N. L. Daly, Blood 2011, 118, 6709.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVCntw%3D%3D&md5=a5d67248efef778eab16a97bd50ae80dCAS |
[95] B. Glotzbach, M. Reinwarth, N. Weber, S. Fabritz, M. Tomaszowski, H. Fittler, A. Christmann, O. Avrutina, H. Kolmar, PLoS One 2013, 8, e76956.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Gjsr7M&md5=75d962b3584536e15aa05f7f77b1bcaaCAS |
[96] F. Maaß, J. Wustehube-Lausch, S. Dickgiessr, B. Valldorf, M. Reinwarth, H. U. Schmoldt, M. Daneschdar, O. Avrutina, U. Sahin, H. Kolmar, J. Pept. Sci. 2015, 21, 651.
| Crossref | GoogleScholarGoogle Scholar |
[97] L. Y. Chan, D. J. Craik, N. L. Daly, Sci. Rep. 2016, 6, 35347.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslSitLfP&md5=f5112e5239ebe5316ab863d72c124ac5CAS |
[98] P. Thongyoo, E. W. Tate, R. J. Leatherbarrow, Chem. Commun. 2006, 2848.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsFKku78%3D&md5=20b42f73ed8bcfdb121db6ff3e1fdd97CAS |
[99] H. Abdul Ghani, S. T. Henriques, Y. H. Huang, J. E. Swedberg, C. I. Schroeder, D. J. Craik, Pept. Sci. 2016, in press.
| Crossref | GoogleScholarGoogle Scholar |
[100] T. M. Hackeng, J. H. Griffin, P. E. Dawson, Proc. Natl. Acad. Sci. USA 1999, 96, 10068.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFegsLw%3D&md5=a0792e9b56bcc5137fc200505190522aCAS |
