DOI QR코드

DOI QR Code

Cyclic Peptides as Therapeutic Agents and Biochemical Tools

  • Joo, Sang-Hoon (Laboratory of Biochemistry, College of Pharmacy, Catholic University of Daegu)
  • Received : 2011.09.02
  • Accepted : 2011.10.28
  • Published : 2012.01.31

Abstract

There are many cyclic peptides with diverse biological activities, such as antibacterial activity, immunosuppressive activity, and anti-tumor activity, and so on. Encouraged by natural cyclic peptides with biological activity, efforts have been made to develop cyclic peptides with both genetic and synthetic methods. The genetic methods include phage display, intein-based cyclic peptides, and mRNA display. The synthetic methods involve individual synthesis, parallel synthesis, as well as split-and-pool synthesis. Recent development of cyclic peptide library based on split-and-pool synthesis allows on-bead screening, in-solution screening, and microarray screening of cyclic peptides for biological activity. Cyclic peptides will be useful as receptor agonist/antagonist, RNA binding molecule, enzyme inhibitor and so on, and more cyclic peptides will emerge as therapeutic agents and biochemical tools.

Keywords

References

  1. Athanassiou, Z., Dias, R. L., Moehle, K., Dobson, N., Varani, G. and Robinson, J. A. (2004) Structural mimicry of retroviral tat proteins by constrained beta-hairpin peptidomimetics: ligands with high affi nity and selectivity for viral TAR RNA regulatory elements. J. Am. Chem. Soc. 126, 6906-6913. https://doi.org/10.1021/ja0497680
  2. Athanassiou, Z., Patora, K., Dias, R. L., Moehle, K., Robinson, J. A. and Varani, G. (2007) Structure-guided peptidomimetic design leads to nanomolar beta-hairpin inhibitors of the Tat-TAR interaction of bovine immunodefi ciency virus. Biochemistry. 46, 741-751. https://doi.org/10.1021/bi0619371
  3. Bu, X., Wu, X., Xie, G. and Guo, Z. (2002) Synthesis of tyrocidine A and its analogues by spontaneous cyclization in aqueous solution. Org. Lett. 4, 2893-2895. https://doi.org/10.1021/ol0263191
  4. Colgrave, M. L., Korsinczky, M. J., Clark, R. J., Foley, F. and Craik, D. J. (2010) Sunflower trypsin inhibitor-1, proteolytic studies on a trypsin inhibitor peptide and its analogs. Biopolymers. 94, 665-672. https://doi.org/10.1002/bip.21415
  5. Dubos, R. J. and Cattaneo, C. (1939) Studies on a bactericidal agent extracted from a soil bacillus : Iii. preparation and activity of a protein-free fraction. J. Exp. Med. 70, 249-256. https://doi.org/10.1084/jem.70.3.249
  6. Eckert, K., Schwarz, H., Tomer, K. B. and Gross, M. L. (1985). Tandem mass spectrometry methodology for the sequence determination of cyclic peptides. J. Am. Chem. Soc. 107, 6765-6769. https://doi.org/10.1021/ja00310a003
  7. Edman, P. (1959) Chemistry of amino acids and peptides. Annu. Rev. Biochem. 28, 69-96. https://doi.org/10.1146/annurev.bi.28.070159.000441
  8. Furka, A., Sebestyen, F., Asgedom, M. and Dibo, G. (1991) General method for rapid synthesis of multicomponent peptide mixtures. Int. J. Pept. Protein. Res. 37, 487-493.
  9. Gehlsen, K. R., Argraves, W. S., Pierschbacher, M. D. and Ruoslahti, E. (1988) Inhibition of in vitro tumor cell invasion by Arg-Gly-Aspcontaining synthetic peptides. J. Cell. Biol. 106, 925-930. https://doi.org/10.1083/jcb.106.3.925
  10. Giroux, R. (2005) Cyclosporine. Chem. Eng. News. 83, 56. https://doi.org/10.1021/cen-v083n017.p056
  11. Gurrath, M., Müller, G., Kessler, H., Aumailley, M. and Timpl, R. (1992) Conformation/activity studies of rationally designed potent antiadhesive RGD peptides. Eur. J. Biochem. 210, 911-921. https://doi.org/10.1111/j.1432-1033.1992.tb17495.x
  12. Hayashi, R., Tanoue, K., Durell, S. R., Chatterjee, D. K., Jenkins, L. M., Appella, D. H. and Appella, E. (2011) Optimization of a cyclic peptide inhibitor of Ser/Thr phosphatase PPM1D (Wip1). Biochemistry. 50, 4537-4549. https://doi.org/10.1021/bi101949t
  13. Hayouka, Z., Hurevich, M., Levin, A., Benyamini, H., Iosub, A., Maes, M., Shalev, D. E., Loyter, A., Gilon, C. and Friedler, A. (2010) Cyclic peptide inhibitors of HIV-1 integrase derived from the LEDGF/p75 protein. Bioorg. Med. Chem. 18, 8388-8395. https://doi.org/10.1016/j.bmc.2010.09.046
  14. Hodgkin, D. C. and Oughton, B. M. (1957) Possible molecular models for gramicidin S and their relationship to present ideas of protein structure. Biochem. J. 65, 752-756.
  15. Horswill, A. R., Savinov, S. N. and Benkovic, S. J. (2004) A systematic method for identifying small-molecule modulators of protein-protein interactions. Proc. Natl. Acad. Sci. USA. 101, 15591-15596. https://doi.org/10.1073/pnas.0406999101
  16. Horton, D. A., Bourne, G. T. and Smythe, M. L. (2002) Exploring privileged structures: the combinatorial synthesis of cyclic peptides. J. Comput. Aided. Mol. Des. 16, 415-430. https://doi.org/10.1023/A:1020863921840
  17. Hotchkiss, R. D. (1941) The chemical nature of gramicidin and tyrocidine. J. Biol. Chem. 141, 171-185.
  18. Hotchkiss, R. D. and Dubos, R. J. (1941) The isolation of bactericidal substances from cultures of Bacillus brevis. J. Biol. Chem. 141, 155-162.
  19. Houghten, R. A., Pinilla, C., Blondelle, S. E., Appel, J. R., Dooley, C. T. and Cuervo, J. H. (1991) Generation and use of synthetic peptide combinatorial libraries for basic research and drug discovery. Nature. 354, 84-86. https://doi.org/10.1038/354084a0
  20. Hull, S. E., Karlsson, R., Main, P., Woolfson, M. M. and Dodson, E. J. (1978) The crystal structure of a hydrated gramicidin S-urea complex. Nature. 275, 206-207. https://doi.org/10.1038/275206a0
  21. Hummel, G., Reineke, U. and Reimer, U. (2006) Translating peptides into small molecules. Mol. Biosyst. 2, 499-508. https://doi.org/10.1039/b611791k
  22. Humphries, M. J., Olden, K. and Yamada, K. M. (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science. 233, 467-470. https://doi.org/10.1126/science.3726541
  23. Joo, S. H., Xiao, Q., Ling, Y., Gopishetty, B. and Pei, D. (2006) Highthroughput sequence determination of cyclic peptide library members by partial Edman degradation/mass spectrometry. J. Am. Chem. Soc. 128, 13000-13009. https://doi.org/10.1021/ja063722k
  24. Kohli, R. M., Walsh, C. T. and Burkart, M. D. (2002) Biomimetic synthesis and optimization of cyclic peptide antibiotics. Nature 418, 658-661. https://doi.org/10.1038/nature00907
  25. Koivunen, E., Gay, D. A. and Ruoslahti, E. (1993) Selection of peptides binding to the alpha 5 beta 1 integrin from phage display library. J. Biol. Chem. 268, 20205-20210.
  26. Kwon, Y. U. and Kodadek, T. (2007) Quantitative comparison of the relative cell permeability of cyclic and linear peptides. Chem. Biol. 14, 671-677. https://doi.org/10.1016/j.chembiol.2007.05.006
  27. Kwon, Y. U. and Kodadek, T. (2008) Encoded combinatorial libraries for the construction of cyclic peptoid microarrays. Chem. Commun. (Camb). 44, 5704-5706.
  28. Lalonde, M. S., Lobritz, M. A., Ratcliff, A., Chamanian, M., Athanassiou, Z., Tyagi, M., Wong, J., Robinson, J. A., Karn, J., Varani, G. and Arts, E. J. (2011) Inhibition of both HIV-1 reverse transcription and gene expression by a cyclic peptide that binds the Tattransactivating response element (TAR) RNA. PLoS. Pathog. 7, e1002038. https://doi.org/10.1371/journal.ppat.1002038
  29. Lam, K. S., Salmon, S. E., Hersh, E. M., Hruby, V. J., Kazmierski, W. M. and Knapp, R. J. (1991) A new type of synthetic peptide library for identifying ligand-binding activity. Nature. 354, 82-84. https://doi.org/10.1038/354082a0
  30. Liu, T., Joo, S. H., Voorhees, J. L., Brooks, C. L. and Pei, D. (2009) Synthesis and screening of a cyclic peptide library: discovery of small-molecule ligands against human prolactin receptor. Bioorg. Med. Chem. 17, 1026-1033. https://doi.org/10.1016/j.bmc.2008.01.015
  31. Liu, T., Liu, Y., Kao, H. Y. and Pei, D. (2010) Membrane permeable cyclic peptidyl inhibitors against human Peptidylprolyl Isomerase Pin1. J. Med. Chem. 53, 2494-2501. https://doi.org/10.1021/jm901778v
  32. Loffet, A. (2002) Peptides as drugs: is there a market? J. Pept. Sci. 8, 1-7. https://doi.org/10.1002/psc.366
  33. Mas-Moruno, C., Rechenmacher, F. and Kessler, H. (2010) Cilengitide: the fi rst anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer. Agents. Med. Chem. 10, 753-768. https://doi.org/10.2174/187152010794728639
  34. Matsuzaki, K. (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta. 1462, 1-10. https://doi.org/10.1016/S0005-2736(99)00197-2
  35. Millward, S. W., Fiacco, S., Austin, R. J. and Roberts, R. W. (2007) Design of cyclic peptides that bind protein surfaces with antibody-like affi nity. ACS. Chem. Biol. 2, 625-634. https://doi.org/10.1021/cb7001126
  36. Millward, S. W., Takahashi, T. T. and Roberts, R. W. (2005) A general route for post-translational cyclization of mRNA display libraries. J. Am. Chem. Soc. 127, 14142-14143. https://doi.org/10.1021/ja054373h
  37. Murphy, E. A., Majeti, B. K., Barnes, L. A., Makale, M., Weis, S. M., Lutu-Fuga, K., Wrasidlo, W. and Cheresh, D. A. (2008) Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc. Natl. Acad. Sci. USA 105, 9343-9348. https://doi.org/10.1073/pnas.0803728105
  38. Naumann, T. A., Tavassoli, A. and Benkovic, S. J. (2008) Genetic selection of cyclic peptide Dam methyltransferase inhibitors. Chembiochem. 9, 194-197. https://doi.org/10.1002/cbic.200700561
  39. Ngoka, L. C. and Gross, M. L. (1999) Multistep tandem mass spectrometry for sequencing cyclic peptides in an ion-trap mass spectrometer. J. Am. Soc. Mass. Spectrom. 10, 732-746. https://doi.org/10.1016/S1044-0305(99)00049-5
  40. Noiri, E., Gailit, J., Sheth, D., Magazine, H., Gurrath, M., Muller, G., Kessler, H. and Goligorsky, M. S. (1994) Cyclic RGD peptides ameliorate ischemic acute renal failure in rats. Kidney. Int. 46, 1050-1058. https://doi.org/10.1038/ki.1994.366
  41. O'Neil, K. T., Hoess, R. H., Jackson, S. A., Ramachandran, N. S., Mousa, S. A. and DeGrado, W. F. (1992) Identifi cation of novel peptide antagonists for GPIIb/IIIa from a conformationally constrained phage peptide library. Proteins. 14, 509-515. https://doi.org/10.1002/prot.340140411
  42. Park, B. W., Zhang, H. T., Wu, C., Berezov, A., Zhang, X., Dua, R., Wang, Q., Kao, G., O'Rourke, D. M., Greene, M. I. and Murali, R. (2000) Rationally designed anti-HER2/neu peptide mimetic disables P185HER2/neu tyrosine kinases in vitro and in vivo. Nat. Biotechnol. 18, 194-198. https://doi.org/10.1038/72651
  43. Perler, F. B. (2005) Protein splicing mechanisms and applications. IUBMB. Life. 57, 469-476. https://doi.org/10.1080/15216540500163343
  44. Perler, F. B, Davis, E. O., Dean, G. E., Gimble, F. S., Jack, W. E., Neff, N., Noren, C. J., Thorner, J. and Belfort, M. (1994) Protein splicing elements: inteins and exteins--a defi nition of terms and recommended nomenclature. Nucleic. Acids. Res. 22, 1125-1127. https://doi.org/10.1093/nar/22.7.1125
  45. Qin, C., Bu, X., Zhong, X., Ng, N. L. and Guo, Z. (2004) Optimization of antibacterial cyclic decapeptides. J. Comb. Chem. 6, 398-406. https://doi.org/10.1021/cc030117u
  46. Qin, C., Zhong, X., Bu, X., Ng, N. L. and Guo, Z. (2003) Dissociation of antibacterial and hemolytic activities of an amphipathic peptide antibiotic. J. Med. Chem. 46, 4830-4833. https://doi.org/10.1021/jm0341352
  47. Redman, J. E., Wilcoxen, K. M. and Ghadiri, M. R. (2003) Automated mass spectrometric sequence determination of cyclic peptide library members. J. Comb. Chem. 5, 33-40. https://doi.org/10.1021/cc0200639
  48. Rezai, T., Yu, B., Millhauser, G. L., Jacobson, M. P. and Lokey, R. S. (2006) Testing the conformational hypothesis of passive membrane permeability using synthetic cyclic peptide diastereomers. J. Am. Chem. Soc. 128, 2510-2511. https://doi.org/10.1021/ja0563455
  49. Roberts, R. W. and Szostak, J. W. (1997) RNA-peptide fusions for the in vitro selection of peptides and proteins. Proc. Natl. Acad. Sci. USA 94, 12297-12302. https://doi.org/10.1073/pnas.94.23.12297
  50. Schilling, B., Wang, W., McMurray, J.S. and Medzihradszky, K.F. (1999) Fragmentation and sequencing of cyclic peptides by matrixassisted laser desorption/ionization post-source decay mass spectrometry. Rapid. Commun. Mass. Spectrom. 13, 2174-2179. https://doi.org/10.1002/(SICI)1097-0231(19991115)13:21<2174::AID-RCM771>3.0.CO;2-K
  51. Scott, C. P., Abel-Santos, E., Wall, M., Wahnon, D. C. and Benkovic, S. J. (1999) Production of cyclic peptides and proteins in vivo. Proc. Natl. Acad. Sci. USA 96, 13638-13643. https://doi.org/10.1073/pnas.96.24.13638
  52. Siegel, M. M., Huang, J., Lin, B., Tsao, R. and Edmonds, C. G. (1994) Structures of bacitracin A and isolated congeners: sequencing of cyclic peptides with blocked linear side chains by electrospray ionization mass spectrometry. Biol. Mass. Spectrom. 23, 186-204. https://doi.org/10.1002/bms.1200230403
  53. Smith, G. P. (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science. 228, 1315-1317. https://doi.org/10.1126/science.4001944
  54. Stauch, B., Simon, B., Basile, T., Schneider, G., Malek, N. P., Kalesse, M. and Carlomagno, T. (2010) Elucidation of the structure and intermolecular interactions of a reversible cyclic-peptide inhibitor of the proteasome by NMR spectroscopy and molecular modeling. Angew. Chem. Int. Ed. Engl. 49, 3934-3938. https://doi.org/10.1002/anie.201000140
  55. Sweeney, M. C. and Pei, D. (2003) An improved method for rapid sequencing of support-bound peptides by partial edman degradation and mass spectrometry. J. Comb. Chem. 5, 218-222. https://doi.org/10.1021/cc020113+
  56. Synge, R. L. (1945) 'Gramicidin S': over-all chemical characteristics and amino-acid composition. Biochem. J. 39, 363-367.
  57. Tamamura, H., Tsutsumi, H., Masuno, H., Mizokami, S., Hiramatsu, K., Wang, Z., Trent, J. O., Nakashima, H., Yamamoto, N., Peiper, S. C. and Fujii, N. (2006) Development of a linear type of low molecular weight CXCR4 antagonists based on T140 analogs. Org. Biomol. Chem. 4, 2354-2357. https://doi.org/10.1039/b603818b
  58. Tamamura, H., Xu, Y., Hattori, T., Zhang, X., Arakaki, R., Kanbara, K., Omagari, A., Otaka, A., Ibuka, T., Yamamoto, N., Nakashima, H. and Fujii, N. (1998) A low-molecular-weight inhibitor against the chemokine receptor CXCR4: a strong anti-HIV peptide T140. Biochem. Biophys. Res. Commun. 253, 877-882. https://doi.org/10.1006/bbrc.1998.9871
  59. Tavassoli. A., Benkovic, S. J. (2005) Genetically selected cyclic-peptide inhibitors of AICAR transformylase homodimerization. Angew. Chem. Int. Ed. Engl. 44, 2760-2763. https://doi.org/10.1002/anie.200500417
  60. Tavassoli, A., Lu, Q., Gam, J., Pan, H., Benkovic, S. J. and Cohen, S. N. (2008) Inhibition of HIV budding by a genetically selected cyclic peptide targeting the Gag-TSG101 interaction. ACS. Chem. Biol. 3, 757-764. https://doi.org/10.1021/cb800193n
  61. Thakkar. A., Wavreille. A.S. and Pei, D. (2006) Traceless capping agent for peptide sequencing by partial edman degradation and mass spectrometry. Anal. Chem. 78, 5935-5939. https://doi.org/10.1021/ac0607414
  62. Vlieghe, P., Lisowski, V., Martinez, J. and Khrestchatisky, M. (2010) Synthetic therapeutic peptides: science and market. Drug. Discov. Today. 15, 40-56. https://doi.org/10.1016/j.drudis.2009.10.009
  63. Wenger, R. M. (1984) Synthesis of cycosporine. Total syntheses of 'cyclosporin A' and 'cyclosporin H', two fungal metabolites isolated from the species. Tolypocladium infl atum GAMS. Helvetica. Chimica. Acta. 67, 502-525. https://doi.org/10.1002/hlca.19840670220
  64. Xiao, Q. and Pei, D. (2007) High-throughput synthesis and screening of cyclic peptide antibiotics. J. Med. Chem. 50, 3132-3137. https://doi.org/10.1021/jm070282e
  65. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature. 415, 389-395. https://doi.org/10.1038/415389a

Cited by

  1. Design of Cyclic Peptide Based Glucose Receptors and Their Application in Glucose Sensing 2017, https://doi.org/10.1021/acs.analchem.7b02430
  2. Potential strategies for the eradication of multidrug-resistant Gram-negative bacterial infections vol.11, pp.7, 2016, https://doi.org/10.2217/fmb-2016-0035
  3. Cyclic peptides identified by phage display are competitive inhibitors of the tRNA-dependent amidotransferase of Helicobacter pylori vol.79, 2016, https://doi.org/10.1016/j.peptides.2016.03.001
  4. Design, synthesis and in vitro biological evaluation of a small cyclic peptide as inhibitor of vascular endothelial growth factor binding to neuropilin-1 vol.26, pp.12, 2016, https://doi.org/10.1016/j.bmcl.2016.04.059
  5. Peptides for tumor-specific drug targeting: state of the art and beyond vol.5, pp.23, 2017, https://doi.org/10.1039/C7TB00318H
  6. Anticancer compounds from cyanobacterium Lyngbya species: a review vol.108, pp.2, 2015, https://doi.org/10.1007/s10482-015-0487-2
  7. Peptide Macrocycles Featuring a Backbone Secondary Amine: A Convenient Strategy for the Synthesis of Lipidated Cyclic and Bicyclic Peptides on Solid Support vol.17, pp.10, 2015, https://doi.org/10.1021/acs.orglett.5b01026
  8. Chemical Platform for the Preparation of Synthetic Orally Active Peptidomimetics with Hemoregulating Activity vol.11, pp.18, 2016, https://doi.org/10.1002/cmdc.201600157
  9. Pyrrolysine-Inspired Protein Cyclization vol.15, pp.12, 2014, https://doi.org/10.1002/cbic.201402129
  10. Enzymatic Macrocyclization of 1,2,3-Triazole Peptide Mimetics vol.55, pp.19, 2016, https://doi.org/10.1002/anie.201601564
  11. Screening of commercial cyclic peptide conjugated to HIV-1 Tat peptide as inhibitor of N-terminal heptad repeat glycoprotein-2 ectodomain Ebola virus through in silico analysis vol.74, 2017, https://doi.org/10.1016/j.jmgm.2017.04.001
  12. Solid-phase synthesis, cyclization, and site-specific functionalization of aziridine-containing tetrapeptides vol.12, pp.6, 2017, https://doi.org/10.1038/nprot.2017.035
  13. Total Synthesis and Pharmacological Investigation of Cordyheptapeptide A vol.22, pp.6, 2017, https://doi.org/10.3390/molecules22060682
  14. Review cyclic peptides on a merry-go-round; towards drug design vol.104, pp.5, 2015, https://doi.org/10.1002/bip.22669
  15. Increase of Positive Net Charge and Conformational Rigidity Enhances the Efficacy ofd-Enantiomeric Peptides Designed to Eliminate Cytotoxic Aβ Species vol.7, pp.8, 2016, https://doi.org/10.1021/acschemneuro.6b00047
  16. Structure and Antibacterial Activity of Ambobactin, a New Telomycin-Like Cyclic Depsipeptide Antibiotic Produced by Streptomyces ambofaciens F3 vol.20, pp.9, 2015, https://doi.org/10.3390/molecules200916278
  17. Characterization of the Free State Ensemble of the CoRNR Box Motif by Molecular Dynamics Simulations vol.120, pp.6, 2016, https://doi.org/10.1021/acs.jpcb.5b11565
  18. Fine-Tuning the Balance between Peptide Thioester Cyclization and Racemization vol.2016, pp.3, 2016, https://doi.org/10.1002/ejoc.201501366
  19. “Freeze, Don’t Move”: How to Arrest a Suspect in Heart Failure – A Review on Available GRK2 Inhibitors vol.3, 2016, https://doi.org/10.3389/fcvm.2016.00048
  20. Structural analyses of isolated cyclic tetrapeptides with varying amino acid residues vol.19, pp.17, 2017, https://doi.org/10.1039/C6CP08696A
  21. Triazene as a Powerful Tool for Solid-Phase Derivatization of Phenylalanine Containing Peptides: Zygosporamide Analogues as a Proof of Concept vol.79, pp.23, 2014, https://doi.org/10.1021/jo501830w
  22. Investigation of the structural requirements of K-Ras(G12D) selective inhibitory peptide KRpep-2d using alanine scans and cysteine bridging vol.27, pp.12, 2017, https://doi.org/10.1016/j.bmcl.2017.04.063
  23. Antifungal activityin vitroandin vivoof a salmon protamine peptide and its derived cyclic peptide againstCandida albicans vol.17, pp.1, 2017, https://doi.org/10.1093/femsyr/fow099
  24. Synthetic strategy for bicyclic tetrapeptides HDAC inhibitors using ring closing metathesis vol.127, pp.9, 2015, https://doi.org/10.1007/s12039-015-0922-y
  25. Re-evaluation of the N-terminal substitution and the D-residues of teixobactin vol.6, pp.77, 2016, https://doi.org/10.1039/C6RA17720D
  26. Controlling Cyclopeptide Backbone Conformation with β/α-Hybrid Peptide-Heterocycle Scaffolds vol.2016, pp.19, 2016, https://doi.org/10.1002/ejoc.201600448
  27. Phage Selection of Cyclic Peptides for Application in Research and Drug Development vol.50, pp.8, 2017, https://doi.org/10.1021/acs.accounts.7b00184
  28. Improving the passive permeability of macrocyclic peptides: Balancing permeability with other physicochemical properties vol.23, pp.2, 2015, https://doi.org/10.1016/j.bmc.2014.11.034
  29. Scalable synthesis of the unusual amino acid segment (ADMOA unit) of marine anti-inflammatory peptide: solomonamide A vol.13, pp.22, 2015, https://doi.org/10.1039/C5OB00481K
  30. Synthesis of Hybrid Cyclopeptides through Enzymatic Macrocyclization vol.6, pp.1, 2017, https://doi.org/10.1002/open.201600134
  31. Enzymatic Macrocyclization of 1,2,3-Triazole Peptide Mimetics vol.128, pp.19, 2016, https://doi.org/10.1002/ange.201601564
  32. Peptide 2-formylthiophenol esters do not proceed through a Ser/Thr ligation pathway, but participate in a peptide aminolysis to enable peptide condensation and cyclization vol.13, pp.25, 2015, https://doi.org/10.1039/C5OB00825E
  33. Emerging biopharmaceuticals from bioactive peptides derived from marine organisms vol.90, pp.1, 2017, https://doi.org/10.1111/cbdd.12925
  34. Oral Administration of Peptide-Based Drugs: Beyond Lipinski's Rule vol.11, pp.20, 2016, https://doi.org/10.1002/cmdc.201600288
  35. Virtual screening of commercial cyclic peptides as NS2B-NS3 protease inhibitor of dengue virus serotype 2 through molecular docking simulation vol.188, 2017, https://doi.org/10.1088/1757-899X/188/1/012017
  36. A Threshold-Minimization Scheme for Exploring the Energy Landscape of Biomolecules: Application to a Cyclic Peptide and a Disaccharide vol.12, pp.5, 2016, https://doi.org/10.1021/acs.jctc.6b00118
  37. Antimicrobial Cyclic Peptides for Plant Disease Control vol.31, pp.1, 2015, https://doi.org/10.5423/PPJ.RW.08.2014.0074
  38. Characterization of bacterial antimicrobial peptides active againstCampylobacter jejuni vol.93, pp.4, 2015, https://doi.org/10.1139/cjc-2014-0411
  39. Incrementally increasing the length of a peptide backbone: effect on macrocyclisation efficiency vol.12, pp.26, 2014, https://doi.org/10.1039/c4ob00492b
  40. Ring Closing and Macrocyclization of β-Dipeptides by Olefin Metathesis vol.2013, pp.28, 2013, https://doi.org/10.1002/ejoc.201300608
  41. Selective Phosphorylation Inhibitor of Delta Protein Kinase C–Pyruvate Dehydrogenase Kinase Protein–Protein Interactions: Application for Myocardial Injuryin Vivo vol.138, pp.24, 2016, https://doi.org/10.1021/jacs.6b02724
  42. Aziridine-Mediated Ligation at Phenylalanine and Tryptophan Sites vol.12, pp.15, 2017, https://doi.org/10.1002/asia.201700538
  43. Accurate Structure Prediction and Conformational Analysis of Cyclic Peptides with Residue-Specific Force Fields vol.7, pp.10, 2016, https://doi.org/10.1021/acs.jpclett.6b00452
  44. Sirtuin Inhibition: Strategies, Inhibitors, and Therapeutic Potential vol.38, pp.5, 2017, https://doi.org/10.1016/j.tips.2017.01.009
  45. Peptide Synthesis Utilizing Micro-flow Technology pp.18614728, 2018, https://doi.org/10.1002/asia.201801488
  46. -methylation in amino acids and peptides: Scope and limitations vol.109, pp.10, 2018, https://doi.org/10.1002/bip.23110
  47. Application of HPCCC Combined with Polymeric Resins and HPLC for the Separation of Cyclic Lipopeptides Muscotoxins A–C and Their Antimicrobial Activity vol.23, pp.10, 2018, https://doi.org/10.3390/molecules23102653
  48. A Tetra-Orthogonal Strategy for the Efficient Synthesis of Scaffolds Based on Cyclic Peptides vol.24, pp.4, 2018, https://doi.org/10.1007/s10989-017-9642-0
  49. to novel approaches for overcoming antibiotic resistance pp.02724391, 2019, https://doi.org/10.1002/ddr.21456
  50. Natural Cyclic Peptides as an Attractive Modality for Therapeutics: A Mini Review vol.23, pp.8, 2018, https://doi.org/10.3390/molecules23082080
  51. Quantification of intramolecular click chemistry modified synthetic peptide isomers in mixtures using tandem mass spectrometry and the survival yield technique vol.410, pp.23, 2018, https://doi.org/10.1007/s00216-018-1258-5
  52. Recent Reports of Solid-Phase Cyclohexapeptide Synthesis and Applications vol.23, pp.6, 2018, https://doi.org/10.3390/molecules23061475
  53. Development of a Novel Backbone Cyclic Peptide Inhibitor of the Innate Immune TLR/IL1R Signaling Protein MyD88 vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-27773-8
  54. Chemical Synthesis and Functional Analysis of VarvA Cyclotide vol.23, pp.4, 2018, https://doi.org/10.3390/molecules23040952
  55. Synthesis and anticancer activities of proline-containing cyclic peptides and their linear analogs and congeners vol.49, pp.2, 2019, https://doi.org/10.1080/00397911.2018.1550201
  56. Combinatorial Library Screening Coupled to Mass Spectrometry to Identify Valuable Cyclic Peptides vol.8, pp.2, 2012, https://doi.org/10.1002/cpch.2
  57. A DFT study on the kinetics and mechanism of cyclodiglycine thermal decomposition in the gas phase vol.41, pp.2, 2012, https://doi.org/10.3184/146867816x14651390195612
  58. Tyrocidine A Analogues Bearing the Planar d-Phe-2-Abz Turn Motif: How Conformation Impacts Bioactivity vol.60, pp.23, 2012, https://doi.org/10.1021/acs.jmedchem.7b00953
  59. Designing Well-Structured Cyclic Pentapeptides Based on Sequence-Structure Relationships vol.122, pp.14, 2018, https://doi.org/10.1021/acs.jpcb.8b01747
  60. Oxazolidinone-Mediated Sequence Determination of One-Bead One-Compound Cyclic Peptide Libraries vol.20, pp.8, 2012, https://doi.org/10.1021/acs.orglett.8b00717
  61. Development of aspartic acid ligation for peptide cyclization derived from serine/threonine ligation vol.29, pp.7, 2012, https://doi.org/10.1016/j.cclet.2018.03.012
  62. Methods for engineering therapeutic peptides vol.29, pp.7, 2012, https://doi.org/10.1016/j.cclet.2018.05.027
  63. Design of Linear and Cyclic Mutant Analogues of Dirucotide Peptide (MBP 82–98 ) against Multiple Sclerosis: Conformational and Binding Studies to MHC Class II vol.8, pp.12, 2012, https://doi.org/10.3390/brainsci8120213
  64. Seongsanamides A-D: Antiallergic Bicyclic Peptides from Bacillus safensis KCTC 12796BP vol.20, pp.23, 2012, https://doi.org/10.1021/acs.orglett.8b03293
  65. Photocyclization of Tetra- and Pentapeptides Containing Adamantylphthalimide and Phenylalanines: Reaction Efficiency and Diastereoselectivity vol.83, pp.24, 2018, https://doi.org/10.1021/acs.joc.8b01785
  66. Cyclopeptides design as blockers against HCV p7 channel in silico vol.45, pp.17, 2012, https://doi.org/10.1080/08927022.2019.1641604
  67. Engineering the Biointerface of Electrospun 3D Scaffolds with Functionalized Polymer Brushes for Enhanced Cell Binding vol.20, pp.2, 2019, https://doi.org/10.1021/acs.biomac.8b01427
  68. Ribosomal Synthesis of Backbone-Cyclic Peptides Compatible with In Vitro Display vol.141, pp.6, 2012, https://doi.org/10.1021/jacs.8b05327
  69. Synthesis of chiral nine and twelve-membered cyclic polyamines from natural building blocks vol.55, pp.32, 2019, https://doi.org/10.1039/c9cc00720b
  70. Peptide-based vaccine successfully induces protective immunity against canine visceral leishmaniasis vol.4, pp.None, 2012, https://doi.org/10.1038/s41541-019-0144-2
  71. Predicting the bioactive conformations of macrocycles: a molecular dynamics-based docking procedure with DynaDock vol.25, pp.7, 2019, https://doi.org/10.1007/s00894-019-4077-5
  72. Cyclic peptide: a safe and effective alternative to synthetic aflatoxin B1-competitive antigens vol.411, pp.17, 2012, https://doi.org/10.1007/s00216-019-01862-7
  73. Ligation Technologies for the Synthesis of Cyclic Peptides vol.119, pp.17, 2019, https://doi.org/10.1021/acs.chemrev.8b00657
  74. Stability of Cu(II) complexes with FomA protein fragments containing two His residues in the peptide chain vol.11, pp.9, 2012, https://doi.org/10.1039/c9mt00131j
  75. Molecular Docking Studies of a Cyclic Octapeptide-Cyclosaplin from Sandalwood vol.9, pp.11, 2012, https://doi.org/10.3390/biom9110740
  76. Improving In Vivo Brain Delivery of Monoclonal Antibody Using Novel Cyclic Peptides vol.11, pp.11, 2012, https://doi.org/10.3390/pharmaceutics11110568
  77. Structure-Activity Study of an All- D Antimicrobial Octapeptide D2D vol.24, pp.24, 2019, https://doi.org/10.3390/molecules24244571
  78. Recent Trends in Cyclic Peptides as Therapeutic Agents and Biochemical Tools vol.28, pp.1, 2012, https://doi.org/10.4062/biomolther.2019.082
  79. Designing Short Peptides: A Sisyphean Task? vol.24, pp.None, 2020, https://doi.org/10.2174/1385272824999200910094034
  80. Utilizing Copper-Mediated Deprotection of Selenazolidine for Cyclic Peptide Synthesis vol.85, pp.3, 2012, https://doi.org/10.1021/acs.joc.9b02644
  81. Cell-penetrating peptides containing 2,5-diketopiperazine (DKP) scaffolds as shuttles for anti-cancer drugs: conformational studies and biological activity vol.56, pp.42, 2020, https://doi.org/10.1039/d0cc01490g
  82. Involvement of the gabaergic, serotonergic and glucocorticoid mechanism in the anxiolytic-like effect of mastoparan-L vol.81, pp.None, 2012, https://doi.org/10.1016/j.npep.2020.102027
  83. Natural Bioactive Thiazole-Based Peptides from Marine Resources: Structural and Pharmacological Aspects vol.18, pp.6, 2012, https://doi.org/10.3390/md18060329
  84. Synthesis of peptide homo‐ and heterodimers as potential mimics of platelet‐derived growth factor BB vol.112, pp.4, 2012, https://doi.org/10.1002/pep2.24150
  85. Inhibiting Matrix Metalloproteinase-2 Activation by Perturbing Protein-Protein Interactions Using a Cyclic Peptide vol.63, pp.13, 2012, https://doi.org/10.1021/acs.jmedchem.0c00180
  86. Marine Bioactive Peptides—An Overview of Generation, Structure and Application with a Focus on Food Sources vol.18, pp.8, 2012, https://doi.org/10.3390/md18080424
  87. Therapeutic peptides for the treatment of systemic lupus erythematosus: a place in therapy vol.29, pp.8, 2012, https://doi.org/10.1080/13543784.2020.1777983
  88. Click-Free Synthesis of a Multivalent Tricyclic Peptide as a Molecular Transporter vol.12, pp.9, 2020, https://doi.org/10.3390/pharmaceutics12090842
  89. Phage display-based vaccine with cathepsin L and excretory-secretory products mimotopes of Fasciola hepatica induces protective cellular and humoral immune responses in sheep vol.289, pp.None, 2012, https://doi.org/10.1016/j.vetpar.2020.109340
  90. Presence of short and cyclic peptides in Acacia and Ziziphus honeys may potentiate their medicinal values vol.19, pp.1, 2012, https://doi.org/10.1515/chem-2021-0106
  91. Antibacterial and antibiofilm efficacy of synthetic polymyxin‐mimetic lipopeptides vol.113, pp.1, 2012, https://doi.org/10.1002/pep2.24188
  92. Specific Inhibition of HIF Activity: Can Peptides Lead the Way? vol.13, pp.3, 2012, https://doi.org/10.3390/cancers13030410
  93. Depsipeptide synthesis using a late-stage Ag(I)-promoted macrolactonisation of peptide thioamides vol.57, pp.16, 2012, https://doi.org/10.1039/d0cc07747j
  94. MCH-R1 Antagonist GPS18169, a Pseudopeptide, Is a Peripheral Anti-Obesity Agent in Mice vol.26, pp.5, 2012, https://doi.org/10.3390/molecules26051291
  95. Conformational Strain of Macrocyclic Peptides in Ligand-Receptor Complexes Based on Advanced Refinement of Bound-State Conformers vol.64, pp.6, 2012, https://doi.org/10.1021/acs.jmedchem.0c02159
  96. Natural Cyclopeptides as Anticancer Agents in the Last 20 Years vol.22, pp.8, 2012, https://doi.org/10.3390/ijms22083973
  97. Tuning the Anti-Angiogenic Effect of the P15 Peptide Using Cyclic Trypsin Inhibitor Scaffolds vol.16, pp.5, 2012, https://doi.org/10.1021/acschembio.0c00907
  98. Oral delivery of peptide therapeutics in infants: Challenges and opportunities vol.173, pp.None, 2012, https://doi.org/10.1016/j.addr.2021.03.011
  99. Cyclic Peptides as Protein Kinase Inhibitors: Structure-Activity Relationship and Molecular Modeling vol.61, pp.6, 2021, https://doi.org/10.1021/acs.jcim.1c00320
  100. Argyrin F Treatment‐Induced Vulnerabilities Lead to a Novel Combination Therapy in Experimental Glioma vol.4, pp.9, 2012, https://doi.org/10.1002/adtp.202100078
  101. Design and Synthesis of Novel Peptides to Protect Ferulic Acid against Ultraviolet Radiation Based on Domain Site IIA of Bovine Serum Albumin vol.11, pp.9, 2012, https://doi.org/10.3390/biom11091285
  102. Blockade of GRTH/DDX25 Phosphorylation by Cyclic Peptides Provides an Avenue for Developing a Nonhormonal Male Contraceptive vol.64, pp.19, 2012, https://doi.org/10.1021/acs.jmedchem.1c01201
  103. Synthetic Glycomacromolecules of Defined Valency, Absolute Configuration, and Topology Distinguish between Human Lectins vol.1, pp.10, 2012, https://doi.org/10.1021/jacsau.1c00255
  104. Protease-Resistant Peptides for Targeting and Intracellular Delivery of Therapeutics vol.13, pp.12, 2012, https://doi.org/10.3390/pharmaceutics13122065