Peptide therapeutics: Targeting the undruggable space

European Journal of Medicinal Chemistry

Volumn 94, Issue , 2015, Pages 459-470

  Tsomaia, Natia ^a  

^a IPSEN   (France)

Author keywords

Beta hairpin mimetics; Hydrogen bond surrogates; Intracellular PPI; Macrocyclization; Molecular grafting; Peptide drugs; Peptide therapeutics; Stapling; Undruggable targets

Indexed keywords

PEPTIDE; PROTEIN BINDING;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; HUMAN; SYNTHESIS;

ANIMALS; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING;

EID: 84930015010     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2015.01.014     Document Type: Article

References (163)

1. H. Ruffner A. Bauer T. Bouwmeester Human protein-protein interaction networks and the value for drug discovery Drug Discov. Today 12 2007 709 716
2. T.L. Nero C.J. Morton J.K. Holien J. Wielens M.W. Parker Oncogenic protein interfaces: small molecules, big challenges Nat. Rev. Cancer 14 2014 248 262
3. D.S. Dimitrov Therapeutic proteins Methods Mol. Biol. (N. Y., NY, U. S.) 899 2012 1 26
4. P. Kubowicz D. Zelaszczyk E. Pekala RNAi in clinical studies Curr. Med. Chem. 20 2013 1801 1816
5. A.L. Hopkins C.R. Groom The druggable genome Nat. Rev. Drug Discov. 1 2002 727 730
6. C.A. Lipinski F. Lombardo B.W. Dominy P.J. Feeney Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Deliv. Rev. 46 2001 3 26
7. J. Baell M. Congreve P. Leeson C. Abad-Zapatero Ask the Experts: past, present and future of the rule of five Future Med. Chem. 5 2013 745 752
8. D.F. Veber S.R. Johnson H.-Y. Cheng B.R. Smith K.W. Ward K.D. Kopple Molecular properties that influence the oral bioavailability of drug candidates J. Med. Chem. 45 2002 2615 2623
9. J.W. Scannell A. Blanckley H. Boldon B. Warrington Diagnosing the decline in pharmaceutical R&D efficiency Nat. Rev. Drug Discov. 11 2012 191 200
10. F. Albericio H.G. Kruger Therapeutic peptides Future Med. Chem. 4 2012 1527 1531
11. A.A. Ivanov F.R. Khuri H. Fu Targeting protein-protein interactions as an anticancer strategy Trends Pharmacol. Sci. 34 2013 393 400
12. C. Tse A.R. Shoemaker J. Adickes M.G. Anderson J. Chen S. Jin E.F. Johnson K.C. Marsh M.J. Mitten P. Nimmer L. Roberts S.K. Tahir Y. Xiao X. Yang H. Zhang S. Fesik S.H. Rosenberg S.W. Elmore ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor Cancer Res. 68 2008 3421 3428
13. L.T. Vassilev B.T. Vu B. Graves D. Carvajal F. Podlaski Z. Filipovic N. Kong U. Kammlott C. Lukacs C. Klein N. Fotouhi E.A. Liu In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848
14. Y. Zhao S. Yu W. Sun L. Liu J. Lu D. McEachern S. Shargary D. Bernard X. Li T. Zhao P. Zou D. Sun S. Wang A potent small-molecule inhibitor of the MDM2-p53 interaction (MI-888) achieved complete and durable tumor regression in mice J. Med. Chem. 56 2013 5553 5561
15. M. Leao C. Pereira A. Bisio Y. Ciribilli A.M. Paiva N. Machado A. Palmeira M.X. Fernandes E. Sousa M. Pinto A. Inga L. Saraiva Discovery of a new small-molecule inhibitor of p53-MDM2 interaction using a yeast-based approach Biochem. Pharmacol. 85 2013 1234 1245
16. C.D. Thanos W.L. DeLano J.A. Wells Hot-spot mimicry of a cytokine receptor by a small molecule Proc. Natl. Acad. Sci. U. S. A. 103 2006 15422 15427
17. M.C. Smith J.E. Gestwicki Features of protein-protein interactions that translate into potent inhibitors: topology, surface area and affinity Expert Rev. Mol. Med. 14 2012 e16/11-e16/20
18. P. Buchwald Small-molecule protein-protein interaction inhibitors: therapeutic potential in light of molecular size, chemical space, and ligand binding efficiency considerations IUBMB Life 62 2010 724 731
19. J.C. Fuller N.J. Burgoyne R.M. Jackson Predicting druggable binding sites at the protein-protein interface Drug Discov. Today 14 2009 155 161
20. T. Clackson J.A. Wells A hot spot of binding Energy in a hormone-receptor interface Science 267 1995 383 386
21. N. London, B. Raveh, and C. O, Druggable protein-protein interactions-from hot spots to hot segments. Curr. Opin. Chem. Biol., 17 952-959.
22. J.A. Wells C.L. McClendon Reaching for high-hanging fruit in drug discovery at protein-protein interfaces Nature 450 2007 1001 1009
23. A.L. Jochim P.S. Arora Systematic analysis of helical protein interfaces reveals targets for synthetic inhibitors ACS Chem. Biol. 5 2010 919 923
24. L.N. Makley J.E. Gestwicki Expanding the number of gdruggableg™ targets: non-enzymes and protein-protein interactions Chem. Biol. Drug Des. 81 2013 22 32
25. C. Reynes H. Host A.-C. Camproux G. Laconde F. Leroux A. Mazars B. Deprez R. Fahraeus B.O. Villoutreix O. Sperandio Designing focused chemical libraries enriched in protein-protein interaction inhibitors using machine-learning methods PLoS Comput. Biol. 6 2010 No pp given
26. D.C. Fry S.-S. So Modulators of protein-protein interactions: importance of three-dimensionality Methods Princ. Med. Chem. 56 2013 55 62
27. O. Sperandio C.H. Reynes A.C. Camproux B.O. Villoutreix Rationalizing the chemical space of protein-protein interaction inhibitors Drug Discov. Today 15 2010 220 229
28. B. Leader Q.J. Baca D.E. Golan Protein therapeutics: a summary and pharmacological classification Nat. Rev. Drug Discov. 7 2008 21 39
29. V. Marx Watching peptide drugs grow up Chem. Eng. News 83 2005 17 24
30. D.J. Craik D.P. Fairlie S. Liras D. Price The future of peptide-based drugs Chem. Biol. Drug Des. 81 2013 136 147
31. V.M. Ahrens K. Bellmann-Sickert A.G. Beck-Sickinger Peptides and peptide conjugates: therapeutics on the upward path Future Med. Chem. 4 2012 1567 1586
32. J. Miller Megan C. Foy Kevin T.P. Kaumaya Pravin Cancer immunotherapy: present status, future perspective, and a new paradigm of peptide immunotherapeutics Discov. Med. 15 2013 166 176
33. I.M. Tomlinson Next-generation protein drugs Nat. Biotechnol. 22 2004 521 522
34. P. Vlieghe V. Lisowski J. Martinez M. Khrestchatisky Synthetic therapeutic peptides: science and market Drug Discov. Today 15 2010 40 56
35. A.K. Sato M. Viswanathan R.B. Kent C.R. Wood Therapeutic peptides: technological advances driving peptides into development Curr. Opin. Biotechnol. 17 2006 638 642
36. J.M. Reichert Development Trends in Peptide Therapeutics Report 2010 Peptide Therapeutic Foundation http://www.peptidetherapeutics.org/PTF-report-summary-2010.pdf
37. J.M. Reichert The Peptide Therapeutics Foundation: Mapping the Future of Peptide Therapeutics 2012 Peptide Therapeutic Foundation http://peptidereview.com/PDF/PTF-IPR12-23-7.pdf
38. A.A. Kaspar J.M. Reichert Future directions for peptide therapeutics development Drug Discov. Today 18 2013 807 817
39. L. Verdine Gregory Drugging the gundruggablegHarvey Lect. 102 2010 1 15
40. G.L. Verdine Next-generation therapeutics Abstracts of Papers, 245th ACS National Meeting & Exposition, New Orleans, LA, United States, April 7-11, 2013 2013 BIOL-118
41. F. Milletti Cell-penetrating peptides: classes, origin, and current landscape Drug Discov. Today 17 2012 850 860
42. M. Guharoy P. Chakrabarti Secondary structure based analysis and classification of biological interfaces: identification of binding motifs in protein-protein interactions Bioinformatics 23 2007 1909 1918
43. A.L. Jochim P.S. Arora Assessment of helical interfaces in protein-protein interactions Mol. Biosyst. 5 2009 924 926
44. J.E. Bock J. Gavenonis J.A. Kritzer Getting in shape: controlling peptide bioactivity and bioavailability using conformational constraints ACS Chem. Biol. 8 2012 488 499
45. A.M. Watkins, P.S. Arora, Structure-based inhibition of protein-protein interactions. Eur. J. Med. Chem. Ahead of Print.
46. M.K. Jayatunga S. Thompson A.D. Hamilton alpha-Helix mimetics: outwards and upwards Bioorg. Med. Chem. Lett. 24 2013 717 724
47. L.K. Henchey A.L. Jochim P.S. Arora Contemporary strategies for the stabilization of peptides in the alpha-helical conformation Curr. Opin. Chem. Biol. 12 2008 692 697
48. A.D. de Araujo H.N. Hoang W.M. Kok F. Diness P. Gupta T.A. Hill R.W. Driver D.A. Price S. Liras D.P. Fairlie Comparative alpha-helicity of cyclic pentapeptides in water Angew. Chem. 53 2014 6965 6969
49. T.A. Hill N.E. Shepherd F. Diness D.P. Fairlie Constraining cyclic peptides to mimic protein structure motifs Angew. Chem. 53 2014 13020 13041
50. Y.H. Lau P. de Andrade S.-T. Quah M. Rossmann L. Laraia N. Skoeld T.J. Sum P.J.E. Rowling T.L. Joseph C. Verma M. Hyvoenen L.S. Itzhaki A.R. Venkitaraman C.J. Brown D.P. Lane D.R. Spring Functionalised staple linkages for modulating the cellular activity of stapled peptides Chem. Sci. 5 2014 1804 1809
51. M. Chorev E. Roubini R.L. McKee S.W. Gibbons M.E. Goldman M.P. Caulfield M. Rosenblatt Cyclic parathyroid hormone-related protein antagonists: lysine 13 to aspartic acid 17 [i to (i + 4)] side chain to side chain lactamization Biochemistry 30 1991 5968 5974
52. N.E. Shepherd H.N. Hoang G. Abbenante D.P. Fairlie Single turn peptide alpha helices with exceptional stability in water J. Am. Chem. Soc. 127 2005 2974 2983
53. S. Cantel A. Le Chevalier Isaad M. Scrima J.J. Levy R.D. DiMarchi P. Rovero J.A. Halperin A.M. D'Ursi A.M. Papini M. Chorev Synthesis and conformational analysis of a cyclic peptide obtained via i to i + 4 intramolecular side-chain to side-chain azide-alkyne 1,3-dipolar cycloaddition J. Org. Chem. 73 2008 5663 5674
54. S.A. Kawamoto A. Coleska X. Ran H. Yi C.-Y. Yang S. Wang Design of triazole-stapled BCL9 I±-helical peptides to target the I2-Catenin/B-cell CLL/lymphoma 9 (BCL9) protein-protein interaction J. Med. Chem. 55 2012 1137 1146
55. H. Jo N. Meinhardt Y. Wu S. Kulkarni X. Hu K.E. Low P.L. Davies W.F. DeGrado D.C. Greenbaum Development of I±-helical calpain probes by mimicking a natural protein-protein interaction J. Am. Chem. Soc. 134 2012 17704 17713
56. C.E. Schafmeister J. Po G.L. Verdine An all-hydrocarbon cross-linking system for enhancing the helicity and metabolic stability of peptides J. Am. Chem. Soc. 122 2000 5891 5892
57. G.L. Verdine G.J. Hilinski Stapled peptides for intracellular drug targets Methods Enzymol. 503 2012 3 33
58. R.H. Grubbs Olefin metathesis Tetrahedron 60 2004 7117 7140
59. S.Y. Shim Y.-W. Kim G.L. Verdine A new i,i + 3 peptide stapling system for I±-Helix stabilization Chem. Biol. Drug Des. 82 2013 635 642
60. G.H. Bird W.C. Crannell L.D. Walensky Chemical synthesis of hydrocarbon-stapled peptides for protein interaction research and therapeutic targeting Curr. Protoc. Chem. Biol. 3 2011 99 117
61. L.D. Walensky A.L. Kung I. Escher T.J. Malia S. Barbuto R.D. Wright G. Wagner G.L. Verdine S.J. Korsmeyer Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix Science 305 2004 1466 1470
62. Q. Chu R.E. Moellering G.J. Hilinski Y.-W. Kim T.N. Grossmann J.T.H. Yeh G.L. Verdine Towards understanding cell penetration by stapled peptides MedChemComm 6 2015 111 119
63. G.L. Verdine G.J. Hilinski All-hydrocarbon stapled peptides as synthetic cell-accessible mini-proteins Drug Discov. Today Technol. 9 2012 e41 e47
64. R.E. Moellering M. Cornejo T.N. Davis C. Del Bianco J.C. Aster S.C. Blacklow A.L. Kung D.G. Gilliland G.L. Verdine J.E. Bradner Direct inhibition of the NOTCH transcription factor complex Nature 462 2009 182-U157
65. Y.S. Chang B. Graves V. Guerlavais C. Tovar K. Packman K.H. To K.A. Olson K. Kesavan P. Gangurde A. Mukherjee T. Baker K. Darlak C. Elkin Z. Filipovic F.Z. Qureshi H. Cai P. Berry E. Feyfant X.E. Shi J. Horstick D.A. Annis A.M. Manning N. Fotouhi H. Nash L.T. Vassilev T.K. Sawyer Stapled alpha-helical peptide drug development: a potent dual inhibitor of MDM2 and MDMX for p53-dependent cancer therapy Proc. Natl. Acad. Sci. U. S. A. 110 2013 E3445 3454
66. W. Kim G.H. Bird T. Neff G. Guo M.A. Kerenyi L.D. Walensky S.H. Orkin Targeted disruption of the EZH2-EED complex inhibits EZH2-dependent cancer Nat. Chem. Biol. 9 2013 643 650
67. G.H. Bird N. Madani A.F. Perry A.M. Princiotto J.G. Supko X. He E. Gavathiotis J.G. Sodroski L.D. Walensky Hydrocarbon double-stapling remedies the proteolytic instability of a lengthy peptide therapeutic Proc. Natl. Acad. Sci. 107 2010 14093 14098
68. G.H. Bird E. Gavathiotis J.L. LaBelle S.G. Katz L.D. Walensky Distinct BimBH3 (BimSAHB) stapled peptides for structural and cellular studies ACS Chem. Biol. 9 2014 831 837
69. T.K. Sawyer AILERON therapeutics Chem. Biol. Drug Des. 73 2009 3 6
70. Y.S. Chang B. Graves V. Guerlavais C. Tovar K. Packman K.-H. To K.A. Olson K. Kesavan P. Gangurde A. Mukherjee T. Baker K. Darlak C. Elkin Z. Filipovic F.Z. Qureshi H. Cai P. Berry E. Feyfant X.E. Shi J. Horstick D.A. Annis A.M. Manning N. Fotouhi H. Nash L.T. Vassilev T.K. Sawyer Stapled I±-helical peptide drug development: a potent dual inhibitor of MDM2 and MDMX for p53-dependent cancer therapy Proc. Natl. Acad. Sci. U. S. A. 110 2013 E3445 E3454 SE3445/3441-SE3445/3447
71. S.J. Wei T. Joseph S. Chee L. Li L. Yurlova K. Zolghadr C. Brown D. Lane C. Verma F. Ghadessy Inhibition of Nutlin-resistant HDM2 mutants by stapled peptides PLoS One 8 2013 e81068/81061-e81068/81016
72. A.M. Spokoyny Y. Zou J.J. Ling H. Yu Y.-S. Lin B.L. Pentelute A perfluoroaryl-cysteine SNAr chemistry approach to unprotected peptide stapling J. Am. Chem. Soc. 135 2013 5946 5949
73. H. Zhang Q. Zhao S. Bhattacharya A.A. Waheed X. Tong A. Hong S. Heck F. Curreli M. Goger D. Cowburn E.O. Freed A.K. Debnath A cell-penetrating helical peptide as a potential HIV-1 inhibitor J. Mol. Biol. 378 2008 565 580
74. E. Cabezas A.C. Satterthwait The hydrogen bond mimic approach: solid-phase synthesis of a peptide stabilized as an alpha-helix with a hydrazone link J. Am. Chem. Soc. 121 1999 3862 3875
75. R.N. Chapman G. Dimartino P.S. Arora A highly stable short alpha-helix constrained by a main-chain hydrogen-bond surrogate J. Am. Chem. Soc. 126 2004 12252 12253
76. A.H. Hoveyda D.G. Gillingham J.J. Van Veldhuizen O. Kataoka S.B. Garber J.S. Kingsbury J.P.A. Harrity Ru complexes bearing bidentate carbenes: from innocent curiosity to uniquely effective catalysts for olefin metathesis Org. Biomol. Chem. 2 2004 8 23
77. A.B. Mahon P.S. Arora End-capped I±-helices as modulators of protein function Drug Discov. Today: Technol. 9 2012 e57 e62
78. L.K. Henchey S. Kushal R. Dubey R.N. Chapman B.Z. Olenyuk P.S. Arora Inhibition of hypoxia inducible factor 1-Transcription coactivator interaction by a hydrogen bond surrogate I±-Helix J. Am. Chem. Soc. 132 2009 941 943
79. A. Patgiri K.K. Yadav P.S. Arora D. Bar-Sagi An orthosteric inhibitor of the Ras-Sos interaction Nat. Chem. Biol. 7 2011 585 587
80. S. Kushal B.B. Lao L.K. Henchey R. Dubey H. Mesallati N.J. Traaseth B.Z. Olenyuk P.S. Arora Protein domain mimetics as in vivo modulators of hypoxia-inducible factor signaling Proc. Natl. Acad. Sci. 110 2013 15602 15607
81. R. Kaul S. Deechongkit J.W. Kelly Synthesis of a negatively charged dibenzofuran-based beta-turn mimetic and its incorporation into the WW miniprotein-enhanced solubility without a loss of thermodynamic stability J. Am. Chem. Soc. 124 2002 11900 11907
82. U. Arnold M.P. Hinderaker B.L. Nilsson B.R. Huck S.H. Gellman R.T. Raines Protein prosthesis: a semisynthetic enzyme with a beta-peptide reverse turn J. Am. Chem. Soc. 124 2002 8522 8523
83. T. Moriuchi T. Hirao Highly ordered structures of peptides by using molecular scaffolds Chem. Soc. Rev. 33 2004 294 301
84. J.S. Nowick Exploring beta-sheet structure and interactions with chemical model systems Acc. Chem. Res. 41 2008 1319 1330
85. H.E. Stanger S.H. Gellman Rules for antiparallel I2-sheet Design:g‰ d-Pro-Gly is Superior to l-Asn-Gly for I2-hairpin Nucleation1 J. Am. Chem. Soc. 120 1998 4236 4237
86. A.A. Fuller D. Du F. Liu J.E. Davoren G. Bhabha G. Kroon D.A. Case H.J. Dyson E.T. Powers P. Wipf M. Gruebele J.W. Kelly Evaluating I2-turn mimics as I2-sheet folding nucleators Proc. Natl. Acad. Sci. 106 2009 11067 11072
87. P.-N. Cheng J.D. Pham J.S. Nowick The supramolecular chemistry of I2-sheets J. Am. Chem. Soc. 135 2013 5477 5492
88. J.A. Robinson S. Demarco F. Gombert K. Moehle D. Obrecht The design, structures and therapeutic potential of protein epitope mimetics Drug Discov. Today 13 2008 944 951
89. J.A. Robinson I2-Hairpin peptidomimetics: design, structures and biological activities Acc. Chem. Res. 41 2008 1278 1288
90. R. Fasan R.L. Dias K. Moehle O. Zerbe J.W. Vrijbloed D. Obrecht J.A. Robinson Using a beta-hairpin to mimic an alpha-helix: cyclic peptidomimetic inhibitors of the p53-HDM2 protein-protein interaction Angew. Chem. 43 2004 2109 2112
91. N. Srinivas P. Jetter B.J. Ueberbacher M. Werneburg K. Zerbe J. Steinmann B. Van der Meijden F. Bernardini A. Lederer R.L.A. Dias P.E. Misson H. Henze J. Zumbrunn F.O. Gombert D. Obrecht P. Hunziker S. Schauer U. Ziegler A. Kach L. Eberl K. Riedel S.J. DeMarco J.A. Robinson Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa Science 327 2010 1010 1013
92. D. Obrecht E. Chevalier K. Moehle J.A. Robinson I2-Hairpin protein epitope mimetic technology in drug discovery Drug Discov. Today: Technol. 9 2012 e63 e69
93. J.A. Kritzer R. Zutshi M. Cheah F.A. Ran R. Webman T.M. Wongjirad A. Schepartz Miniature protein inhibitors of the p53-hDM2 interaction ChemBioChem 7 2006 29 31
94. S.E. Northfield C.K. Wang C.I. Schroeder T. Durek M.-W. Kan J.E. Swedberg D.J. Craik Disulfide-rich macrocyclic peptides as templates in drug design Eur. J. Med. Chem. 77 2014 248 257
95. D.J. Craik J.E. Swedberg J.S. Mylne M. Cemazar Cyclotides as a basis for drug design Expert Opin. Drug Discov. 7 2012 179 194
96. S.T. Henriques D.J. Craik Cyclotides as templates in drug design Drug Discov. Today 15 2010 57 64
97. S.J. Moore C.L. Leung J.R. Cochran Knottins: disulfide-bonded therapeutic and diagnostic peptides Drug Discov. Today Technol. 9 2012 e3 e11
98. C. Li M. Liu J. Monbo G.Z. Zou C.Q. Li W.R. Yuan D. Zella W.Y. Lu W.Y. Lu Turning a scorpion toxin into an antitumor miniprotein J. Am. Chem. Soc. 130 2008 13546 13548
99. D.S. Daniels A. Schepartz Intrinsically cell-permeable miniature proteins based on a minimal cationic PPII motif J. Am. Chem. Soc. 129 2007 14578 14579
100. K.P. Greenwood N.L. Daly D.L. Brown J.L. Stow D.J. Craik The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis Int. J. Biochem. Cell Biol. 39 2007 2252 2264
101. L. Cascales S.T. Henriques M.C. Kerr Y.H. Huang M.J. Sweet N.L. Daly D.J. Craik Identification and characterization of a new family of cell-penetrating peptides: cyclic cell-penetrating peptides J. Biol. Chem. 286 2011 36932 36943
102. J. Contreras A.Y.O. Elnagar S.F. Hamm-Alvarez J.A. Camarero Cellular uptake of cyclotide MCoTI-I follows multiple endocytic pathways J. Controlled Release 155 2011 134 143
103. Y. Ji S. Majumder M. Millard R. Borra T. Bi A.Y. Elnagar N. Neamati A. Shekhtman J.A. Camarero In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide J. Am. Chem. Soc. 135 2013 11623 11633
104. M. Pazgier M. Liu G. Zou W. Yuan C. Li C. Li J. Li J. Monbo D. Zella S.G. Tarasov W. Lu Structural basis for high-affinity peptide inhibition of p53 interactions with MDM2 and MDMX Proc. Natl. Acad. Sci. U. S. A. 106 2009 4665 4670
105. C. Li M. Pazgier M. Liu W.Y. Lu W. Lu Apamin as a template for structure-based rational design of potent peptide activators of p53 Angew. Chem. 48 2009 8712 8715
106. E.M. Driggers S.P. Hale J. Lee N.K. Terrett The exploration of macrocycles for drug discovery-an underexploited structural class Nat. Rev. Drug Discov. 7 2008 608 624
107. A.T. Bockus C.M. McEwen R.S. Lokey Form and function in cyclic peptide natural products: a pharmacokinetic perspective Curr. Top. Med. Chem. 13 2013 821 836
108. L. Gentilucci R. De Marco L. Cerisoli Chemical modifications designed to improve peptide Stability: Incorporation of non-natural amino acids, pseudo-peptide bonds, and cyclization Curr. Pharm. Des. 16 2010 3185 3203
109. K. Josephson A. Ricardo J.W. Szostak mRNA display: from basic principles to macrocycle drug discovery Drug Discov. Today 19 2013 388 399
110. H.R. Loosli H. Kessler H. Oschkinat H.P. Weber T.J. Petcher A. Widmer Peptide conformations. 31. The conformation of cyclosporin-A in the crystal and in solution Helv. Chim. Acta 68 1985 682 704
111. H. Kessler M. Kock T. Wein M. Gehrke Reinvestigation of the conformation of cyclosporine-A in chloroform Helv. Chim. Acta 73 1990 1818 1832
112. L. Jin S.C. Harrison Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin Proc. Natl. Acad. Sci. U. S. A. 99 2002 13522 13526
113. S.Y. Ko C. Dalvit Conformation of cyclosporin a in polar solvents Int. J. Pept. Protein Res. 40 1992 380 382
114. T. Rezai B. Yu G.L. Millhauser M.P. Jacobson R.S. Lokey Testing the conformational hypothesis of passive membrane permeability using synthetic cyclic peptide diastereomers J. Am. Chem. Soc. 128 2006 2510 2511
115. T. Rezai J.E. Bock M.V. Zhou C. Kalyanaraman R.S. Lokey M.P. Jacobson Conformational flexibility, internal hydrogen bonding, and passive membrane permeability: successful in silico prediction of the relative permeabilities of cyclic peptides J. Am. Chem. Soc. 128 2006 14073 14080
116. T.R. White C.M. Renzelman A.C. Rand T. Rezai C.M. McEwen V.M. Gelev R.A. Turner R.G. Linington S.S. Leung A.S. Kalgutkar J.N. Bauman Y. Zhang S. Liras D.A. Price A.M. Mathiowetz M.P. Jacobson R.S. Lokey On-resin N-methylation of cyclic peptides for discovery of orally bioavailable scaffolds Nat. Chem. Biol. 7 2011 810 817
117. J. Chatterjee D. Mierke H. Kessler N-methylated cyclic pentaalanine peptides as template structures J. Am. Chem. Soc. 128 2006 15164 15172
118. J.G. Beck J. Chatterjee B. Laufer M.U. Kiran A.O. Frank S. Neubauer O. Ovadia S. Greenberg C. Gilon A. Hoffman H. Kessler Intestinal permeability of cyclic peptides: common key backbone motifs identified J. Am. Chem. Soc. 134 2012 12125 12133
119. J. Chatterjee C. Gilon A. Hoffman H. Kessler N-Methylation of peptides: a new perspective in medicinal chemistry Acc. Chem. Res. 41 2008 1331 1342
120. O. Ovadia S. Greenberg B. Laufer C. Gilon A. Hoffman Improvement of drug-like properties of peptides: the somatostatin paradigm Expert Opin. Drug Discov. 5 2010 655 671
121. F. Giordanetto J. Kihlberg Macrocyclic drugs and clinical candidates: what can medicinal chemists learn from their properties? J. Med. Chem. 57 2013 278 295
122. K.V. Lawson T.E. Rose P.G. Harran Template-constrained macrocyclic peptides prepared from native, unprotected precursors Proc. Natl. Acad. Sci. U. S. A. 110 2013 E3753 3760
123. C.J. White A.K. Yudin Contemporary strategies for peptide macrocyclization Nat. Chem. 3 2011 509 524
124. G.K.T. Nguyen S. Wang Y. Qiu X. Hemu Y. Lian J.P. Tam Butelase 1 is an Asx-specific ligase enabling peptide macrocyclization and synthesis Nat. Chem. Biol. 10 2014 732 738
125. A. Bhat L.R. Roberts J.J. Dwyer Lead discovery and optimization strategies for peptide macrocycles Eur. J. Med. Chem. 2014 http://dx.doi.org/10.1016/j.ejmech.2014.07.083
126. E.A. Villar D. Beglov S. Chennamadhavuni J.A. Porco Jr. D. Kozakov S. Vajda A. Whitty How proteins bind macrocycles Nat. Chem. Biol. 10 2014 723 731
127. J. Gavenonis B.A. Sheneman T.R. Siegert M.R. Eshelman J.A. Kritzer Comprehensive analysis of loops at protein-protein interfaces for macrocycle design Nat. Chem. Biol. 10 2014 716 722
128. N.K. Terrett Methods for the synthesis of macrocycle libraries for drug discovery Drug Discov. Today: Technol. 7 2010 e97 e104
129. J. Mallinson I. Collins Macrocycles in new drug discovery Future Med. Chem. 4 2012 1409 1438
130. R. Hili V. Rai A.K. Yudin Macrocyclization of linear peptides enabled by amphoteric molecules J. Am. Chem. Soc. 132 2010 2889 2891
131. A. Roxin J. Chen C.C. Scully B.H. Rotstein A.K. Yudin G. Zheng Conformational modulation of in vitro activity of cyclic RGD peptides via aziridine aldehyde-driven macrocyclization chemistry Bioconjugate Chem. 23 2012 1387 1395
132. E. Marsault H.R. Hoveyda R. Gagnon M.L. Peterson M. Vezina C. Saint-Louis A. Landry J.F. Pinault L. Ouellet S. Beauchemin S. Beaubien A. Mathieu K. Benakli Z. Wang M. Brassard D. Lonergan F. Bilodeau M. Ramaseshan N. Fortin R. Lan S. Li F. Galaud V. Plourde M. Champagne A. Doucet P. Bherer M. Gauthier G. Olsen G. Villeneuve S. Bhat L. Foucher D. Fortin X. Peng S. Bernard A. Drouin R. Deziel G. Berthiaume Y.L. Dory G.L. Fraser P. Deslongchamps Efficient parallel synthesis of macrocyclic peptidomimetics Bioorg. Med. Chem. Lett. 18 2008 4731 4735
133. P. Timmerman J. Beld W.C. Puijk R.H. Meloen Rapid and quantitative cyclization of multiple peptide loops onto synthetic scaffolds for structural mimicry of protein surfaces ChemBioChem 6 2005 821 824
134. Z.J. Gartner B.N. Tse R. Grubina J.B. Doyon T.M. Snyder D.R. Liu DNA-templated organic synthesis and selection of a library of macrocycles Science 305 2004 1601 1605
135. Y. Zou A.M. Spokoyny C. Zhang M.D. Simon H. Yu Y.-S. Lin B.L. Pentelute Convergent diversity-oriented side-chain macrocyclization scan for unprotected polypeptides Org. Biomol. Chem. 12 2014 566 573
136. W. Lian P. Upadhyaya C.A. Rhodes Y. Liu D. Pei Screening bicyclic peptide libraries for Protein-Protein interaction inhibitors: discovery of a tumor necrosis factor-I± antagonist J. Am. Chem. Soc. 135 2013 11990 11995
137. S.H. Joo Q. Xiao Y. Ling B. Gopishetty D. Pei High-throughput sequence determination of cyclic peptide library members by partial Edman degradation/mass spectrometry J. Am. Chem. Soc. 128 2006 13000 13009
138. R.W. Roberts J.W. Szostak RNA-peptide fusions for the in vitro selection of peptides and proteins Proc. Natl. Acad. Sci. U. S. A. 94 1997 12297 12302
139. K. Josephson M.C.T. Hartman J.W. Szostak Ribosomal synthesis of unnatural peptides J. Am. Chem. Soc. 127 2005 11727 11735
140. M.C.T. Hartman K. Josephson C.W. Lin J.W. Szostak An expanded set of amino acid analogs for the ribosomal translation of unnatural peptides PLos One 2 2007
141. Y. Shimizu A. Inoue Y. Tomari T. Suzuki T. Yokogawa K. Nishikawa T. Ueda Cell-free translation reconstituted with purified components Nat. Biotechnol. 19 2001 751 755
142. Y.V.G. Schlippe M.C.T. Hartman K. Josephson J.W. Szostak In vitro selection of highly modified cyclic peptides that act as tight binding inhibitors J. Am. Chem. Soc. 134 2012 10469 10477
143. H. Murakami A. Ohta H. Ashigai H. Suga A highly flexible tRNA acylation method for non-natural potypeptide synthesis Nat. Methods 3 2006 357 359
144. Y. Goto T. Katoh H. Suga Flexizymes for genetic code reprogramming Nat. Protoc. 6 2011 779 790
145. J. Morimoto Y. Hayashi K. Iwasaki H. Suga Flexizymes: their evolutionary history and the origin of catalytic function Acc. Chem. Res. 44 2011 1359 1368
146. C.J. Hipolito H. Suga Ribosomal production and in vitro selection of natural product-like peptidomimetics: the FIT and RaPID systems Curr. Opin. Chem. Biol. 16 2012 196 203
147. F.P. Seebeck J.W. Szostak Ribosomal synthesis of dehydroalanine-containing peptides J. Am. Chem. Soc. 128 2006 7150 7151
148. Y. Sako Y. Goto H. Murakami H. Suga Ribosomal synthesis of peptidase-resistant peptides closed by a nonreducible inter-side-chain bond ACS Chem. Biol. 3 2008 241 249
149. T. Kawakami A. Ohta M. Ohuchi H. Ashigai H. Murakami H. Suga Diverse backbone-cyclized peptides via codon reprogramming Nat. Chem. Biol. 5 2009 888 890
150. T. Passioura H. Suga Flexizyme-mediated genetic reprogramming as a tool for noncanonical peptide synthesis and drug discovery Chem. Eur. J. 19 2013 6530 6536
151. Y. Goto A. Ohta Y. Sako Y. Yamagishi H. Murakami H. Suga Reprogramming the translation initiation for the synthesis of physiologically stable cyclic peptides ACS Chem. Biol. 3 2008 120 129
152. Y. Yamagishi I. Shoji S. Miyagawa T. Kawakami T. Katoh Y. Goto H. Suga Natural product-like macrocyclic n-methyl-peptide inhibitors against a ubiquitin ligase uncovered from a ribosome-expressed De Novo library Chem. Biol. 18 2011 1562 1570
153. Y. Hayashi J. Morimoto H. Suga In vitro selection of anti-Akt2 thioether-macrocyclic peptides leading to isoform-selective inhibitors ACS Chem. Biol. 7 2012 607 613
154. Jumpei Morimoto Yuuki Hayashi Hiroaki Suga Discovery of macrocyclic peptides armed with a mechanism-based warhead: isoform-selective inhibition of human deacetylase SIRT2 Angew. Chem. Int. Ed. 51 2012 3423 3427
155. N. London B. Raveh D. Movshovitz-Attias O. Schueler-Furman Can self-inhibitory peptides be derived from the interfaces of globular protein-protein interactions? Proteins 78 2010 3140 3149
156. C. Heinis T. Rutherford S. Freund G. Winter Phage-encoded combinatorial chemical libraries based on bicyclic peptides Nat. Chem. Biol. 5 2009 502 507
157. P. Diderich C. Heinis Directed evolution of bicyclic peptides for therapeutic application Chimia 67 2013 910 915
158. A. Angelini J. Morales-Sanfrutos P. Diderich S.Y. Chen C. Heinis Bicyclization and tethering to albumin yields long-acting peptide antagonists J. Med. Chem. 55 2012 10187 10197
159. A. Angelini L. Cendron S.Y. Chen J. Touati G. Winter G. Zanotti C. Heinis Bicyclic peptide inhibitor reveals large contact interface with a protease target ACS Chem. Biol. 7 2012 817 821
160. S. Chen I. Rentero Rebollo S.A. Buth J. Morales-Sanfrutos J. Touati P.G. Leiman C. Heinis Bicyclic peptide ligands pulled out of cysteine-rich peptide libraries J. Am. Chem. Soc. 135 2013 6562 6569
161. S. Chen D. Bertoldo A. Angelini F. Pojer C. Heinis Peptide ligands stabilized by small molecules Angew. Chem. Int. Ed. 53 2014 1602 1606
162. S. Chen D. Gfeller S.A. Buth O. Michielin P.G. Leiman C. Heinis Improving binding affinity and stability of peptide ligands by substituting glycines with d-amino acids ChemBioChem 14 2013 1316 1322
163. R. Wallbrecher L. Depre W.P. Verdurmen P.H. Bovee-Geurts R.H. van Duinkerken M.J. Zekveld P. Timmerman R. Brock Exploration of the design principles of a cell-penetrating bicylic peptide scaffold Bioconjugate Chem. 5 2014 955 964