1932

Abstract

Macrocyclic peptides are an emerging class of therapeutics that can modulate protein–protein interactions. In contrast to the heavily automated high-throughput screening systems traditionally used for the identification of chemically synthesized small-molecule drugs, peptide-based macrocycles can be synthesized by ribosomal translation and identified using in vitro selection techniques, allowing for extremely rapid (hours to days) screening of compound libraries comprising more than 1013 different species. Furthermore, chemical modification of translated peptides and engineering of the genetic code have greatly expanded the structural diversity of the available peptide libraries. In this review, we discuss the use of these technologies for the identification of bioactive macrocyclic peptides, emphasizing recent developments.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060713-035456
2014-06-02
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/biochem/83/1/annurev-biochem-060713-035456.html?itemId=/content/journals/10.1146/annurev-biochem-060713-035456&mimeType=html&fmt=ahah

Literature Cited

  1. Barnett AH, Owens DR. 1.  1997. Insulin analogues. Lancet 349:47–51 [Google Scholar]
  2. Koretz RL, Pleguezuelo M, Arvaniti V, Barrera Baena P, Ciria R. 2.  et al. 2013. Interferon for interferon nonresponding and relapsing patients with chronic hepatitis C. Cochrane Database Syst. Rev. 1:CD003617 [Google Scholar]
  3. Takeda A, Cooper K, Bird A, Baxter L, Frampton GK. 3.  et al. 2010. Recombinant human growth hormone for the treatment of growth disorders in children: a systematic review and economic evaluation. Health Technol. Assess. 14:1–209 [Google Scholar]
  4. Drucker DJ, Nauck MA. 4.  2006. The incretin system: glucagon-like peptide 1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 368:1696–705 [Google Scholar]
  5. Altschuh D, Vix O, Rees B, Thierry JC. 5.  1992. A conformation of cyclosporin A in aqueous environment revealed by the X-ray structure of a cyclosporin–Fab complex. Science 256:92–94 [Google Scholar]
  6. Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX. 6.  1989. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337:476–78 [Google Scholar]
  7. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. 7.  1984. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226:544–47 [Google Scholar]
  8. Holt DW, Mueller EA, Kovarik JM, van Bree JB, Kutz K. 8.  1994. The pharmacokinetics of Sandimmun Neoral: a new oral formulation of cyclosporine. Transplant. Proc. 26:2935–39 [Google Scholar]
  9. Takahashi N, Hayano T, Suzuki M. 9.  1989. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A–binding protein cyclophilin. Nature 337:473–75 [Google Scholar]
  10. Driggers EM, Hale SP, Lee J, Terrett NK. 10.  2008. The exploration of macrocycles for drug discovery—an underexploited structural class. Nat. Rev. Drug Discov. 7:608–24 [Google Scholar]
  11. Perlin DS.11.  2011. Current perspectives on echinocandin class drugs. Future Microbiol. 6:441–57 [Google Scholar]
  12. Berger KJ, Guss DA. 12.  2005. Mycotoxins revisited: part I. J. Emerg. Med. 28:53–62 [Google Scholar]
  13. White TR, Renzelman CM, Rand AC, Rezai T, McEwen CM. 13.  et al. 2011. On-resin N-methylation of cyclic peptides for discovery of orally bioavailable scaffolds. Nat. Chem. Biol. 7:810–17 [Google Scholar]
  14. Rezai T, Yu B, Millhauser GL, Jacobson MP, Lokey RS. 14.  2006. Testing the conformational hypothesis of passive membrane permeability using synthetic cyclic peptide diastereomers. J. Am. Chem. Soc. 128:2510–11 [Google Scholar]
  15. Bock JE, Gavenonis J, Kritzer JA. 15.  2013. Getting in shape: controlling peptide bioactivity and bioavailability using conformational constraints. Am. Chem. Soc. Chem. Biol. 8:488–99 [Google Scholar]
  16. Beck JG, Chatterjee J, Laufer B, Kiran MU, Frank AO. 16.  et al. 2012. Intestinal permeability of cyclic peptides: common key backbone motifs identified. J. Am. Chem. Soc. 134:12125–33 [Google Scholar]
  17. Biron E, Chatterjee J, Ovadia O, Langenegger D, Brueggen J. 17.  et al. 2008. Improving oral bioavailability of peptides by multiple N-methylation: somatostatin analogues. Angew. Chem. Int. Ed. Engl. 47:2595–99 [Google Scholar]
  18. Frankel A, Millward SW, Roberts RW. 18.  2003. Encodamers: unnatural peptide oligomers encoded in RNA. Chem. Biol. 10:1043–50 [Google Scholar]
  19. Ovadia O, Greenberg S, Chatterjee J, Laufer B, Opperer F. 19.  et al. 2011. The effect of multiple N-methylation on intestinal permeability of cyclic hexapeptides. Mol. Pharmacol. 8:479–87 [Google Scholar]
  20. Geyer CR, McCafferty J, Dubel S, Bradbury AR, Sidhu SS. 20.  2012. Recombinant antibodies and in vitro selection technologies. Methods Mol. Biol. 901:11–32 [Google Scholar]
  21. Winter G, Griffiths AD, Hawkins RE, Hoogenboom HR. 21.  1994. Making antibodies by phage display technology. Annu. Rev. Immunol. 12:433–55 [Google Scholar]
  22. Scott CP, Abel-Santos E, Jones AD, Benkovic SJ. 22.  2001. Structural requirements for the biosynthesis of backbone cyclic peptide libraries. Chem. Biol. 8:801–15 [Google Scholar]
  23. Scott CP, Abel-Santos E, Wall M, Wahnon DC, Benkovic SJ. 23.  1999. Production of cyclic peptides and proteins in vivo. Proc. Natl. Acad. Sci. USA 96:13638–43 [Google Scholar]
  24. Horswill AR, Benkovic SJ. 24.  2006. Identifying small-molecule modulators of protein–protein interactions. Curr. Protoc. Protein Sci. 46:19.151–19 [Google Scholar]
  25. Tavassoli A, Benkovic SJ. 25.  2007. Split-intein mediated circular ligation used in the synthesis of cyclic peptide libraries in E. coli. Nat. Protoc. 2:1126–33 [Google Scholar]
  26. Horswill AR, Savinov SN, Benkovic SJ. 26.  2004. A systematic method for identifying small-molecule modulators of protein–protein interactions. Proc. Natl. Acad. Sci. USA 101:15591–96 [Google Scholar]
  27. Tavassoli A, Benkovic SJ. 27.  2005. Genetically selected cyclic-peptide inhibitors of AICAR transformylase homodimerization. Angew. Chem. Int. Ed. Engl. 44:2760–63 [Google Scholar]
  28. Tavassoli A, Lu Q, Gam J, Pan H, Benkovic SJ, Cohen SN. 28.  2008. Inhibition of HIV budding by a genetically selected cyclic peptide targeting the Gag–TSG101 interaction. Am. Chem. Soc. Chem. Biol. 3:757–64 [Google Scholar]
  29. Spurr IB, Birts CN, Cuda F, Benkovic SJ, Blaydes JP, Tavassoli A. 29.  2012. Targeting tumour proliferation with a small-molecule inhibitor of AICAR transformylase homodimerization. ChemBioChem 13:1628–34 [Google Scholar]
  30. Cheng L, Naumann TA, Horswill AR, Hong SJ, Venters BJ. 30.  et al. 2007. Discovery of antibacterial cyclic peptides that inhibit the ClpXP protease. Protein Sci. 16:1535–42 [Google Scholar]
  31. Naumann TA, Tavassoli A, Benkovic SJ. 31.  2008. Genetic selection of cyclic peptide Dam methyltransferase inhibitors. ChemBioChem 9:194–97 [Google Scholar]
  32. Kinsella TM, Ohashi CT, Harder AG, Yam GC, Li W. 32.  et al. 2002. Retrovirally delivered random cyclic peptide libraries yield inhibitors of interleukin-4 signaling in human B cells. J. Biol. Chem. 277:37512–18 [Google Scholar]
  33. Kritzer JA, Hamamichi S, McCaffery JM, Santagata S, Naumann TA. 33.  et al. 2009. Rapid selection of cyclic peptides that reduce α-synuclein toxicity in yeast and animal models. Nat. Chem. Biol. 5:655–63 [Google Scholar]
  34. Frost JR, Smith JM, Fasan R. 34.  2013. Design, synthesis, and diversification of ribosomally derived peptide macrocycles. Curr. Opin. Struct. Biol. 23:571–80 [Google Scholar]
  35. Frost JR, Vitali F, Jacob NT, Brown MD, Fasan R. 35.  2013. Macrocyclization of organo-peptide hybrids through a dual bio-orthogonal ligation: insights from structure-reactivity studies. ChemBioChem 14:147–60 [Google Scholar]
  36. Satyanarayana M, Vitali F, Frost JR, Fasan R. 36.  2012. Diverse organo-peptide macrocycles via a fast and catalyst-free oxime/intein-mediated dual ligation. Chem. Commun. 48:1461–63 [Google Scholar]
  37. Smith JM, Frost JR, Fasan R. 37.  2013. Emerging strategies to access peptide macrocycles from genetically encoded polypeptides. J. Org. Chem. 78:3525–31 [Google Scholar]
  38. Smith JM, Vitali F, Archer SA, Fasan R. 38.  2011. Modular assembly of macrocyclic organo-peptide hybrids using synthetic and genetically encoded precursors. Angew. Chem. Int. Ed. Engl. 50:5075–80 [Google Scholar]
  39. Smith GP.39.  1985. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–17 [Google Scholar]
  40. Vaughan TJ, Williams AJ, Pritchard K, Osbourn JK, Pope AR. 40.  et al. 1996. Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library. Nat. Biotechnol. 14:309–14 [Google Scholar]
  41. Clackson T, Wells JA. 41.  1994. In vitro selection from protein and peptide libraries. Trends Biotechnol. 12:173–84 [Google Scholar]
  42. Chen S, Rentero Rebollo I, Buth SA, Morales-Sanfrutos J, Touati J. 42.  et al. 2013. Bicyclic peptide ligands pulled out of cysteine-rich peptide libraries. J. Am. Chem. Soc. 135:6562–69 [Google Scholar]
  43. McLafferty MA, Kent RB, Ladner RC, Markland W. 43.  1993. M13 bacteriophage displaying disulfide-constrained microproteins. Gene 128:29–36 [Google Scholar]
  44. Giebel LB, Cass RT, Milligan DL, Young DC, Arze R, Johnson CR. 44.  1995. Screening of cyclic peptide phage libraries identifies ligands that bind streptavidin with high affinities. Biochemistry 34:15430–35 [Google Scholar]
  45. Katz BA.45.  1995. Binding to protein targets of peptidic leads discovered by phage display: crystal structures of streptavidin-bound linear and cyclic peptide ligands containing the HPQ sequence. Biochemistry 34:15421–29 [Google Scholar]
  46. O'Neil KT, Hoess RH, Jackson SA, Ramachandran NS, Mousa SA, DeGrado WF. 46.  1992. Identification of novel peptide antagonists for GPIIb/IIIa from a conformationally constrained phage peptide library. Proteins 14:509–15 [Google Scholar]
  47. Daly NL, Clark RJ, Craik DJ. 47.  2003. Disulfide folding pathways of cystine knot proteins. Tying the knot within the circular backbone of the cyclotides. J. Biol. Chem. 278:6314–22 [Google Scholar]
  48. Daly NL, Craik DJ. 48.  2011. Bioactive cystine knot proteins. Curr. Opin. Chem. Biol. 15:362–68 [Google Scholar]
  49. Daly NL, Koltay A, Gustafson KR, Boyd MR, Casas-Finet JR, Craik DJ. 49.  1999. Solution structure by NMR of circulin A: a macrocyclic knotted peptide having anti-HIV activity. J. Mol. Biol. 285:333–45 [Google Scholar]
  50. Gilbert HF.50.  1995. Thiol/disulfide exchange equilibria and disulfide bond stability. Methods Enzymol. 251:8–28 [Google Scholar]
  51. Heinis C, Rutherford T, Freund S, Winter G. 51.  2009. Phage-encoded combinatorial chemical libraries based on bicyclic peptides. Nat. Chem. Biol. 5:502–7 [Google Scholar]
  52. Angelini A, Cendron L, Chen S, Touati J, Winter G. 52.  et al. 2012. Bicyclic peptide inhibitor reveals large contact interface with a protease target. Am. Chem. Soc. Chem. Biol. 7:817–21 [Google Scholar]
  53. Baeriswyl V, Calzavarini S, Gerschheimer C, Diderich P, Angelillo-Scherrer A, Heinis C. 53.  2013. Development of a selective peptide macrocycle inhibitor of coagulation factor XII toward the generation of a safe antithrombotic therapy. J. Med. Chem. 56:3742–46 [Google Scholar]
  54. Frankel A, Li S, Starck SR, Roberts RW. 54.  2003. Unnatural RNA display libraries. Curr. Opin. Struct. Biol. 13:506–12 [Google Scholar]
  55. Pluckthun A.55.  2012. Ribosome display: a perspective. Methods Mol. Biol. 805:3–28 [Google Scholar]
  56. Roberts RW.56.  1999. Totally in vitro protein selection using mRNA–protein fusions and ribosome display. Curr. Opin. Chem. Biol. 3:268–73 [Google Scholar]
  57. Roberts RW, Szostak JW. 57.  1997. RNA–peptide fusions for the in vitro selection of peptides and proteins. Proc. Natl. Acad. Sci. USA 94:12297–302 [Google Scholar]
  58. Nemoto N, Miyamoto-Sato E, Husimi Y, Yanagawa H. 58.  1997. In vitro virus: bonding of mRNA bearing puromycin at the 3′-terminal end to the C-terminal end of its encoded protein on the ribosome in vitro. FEBS Lett. 414:405–8 [Google Scholar]
  59. Takahashi TT, Austin RJ, Roberts RW. 59.  2003. mRNA display: ligand discovery, interaction analysis and beyond. Trends Biochem. Sci. 28:159–65 [Google Scholar]
  60. Barrick JE, Takahashi TT, Balakin A, Roberts RW. 60.  2001. Selection of RNA-binding peptides using mRNA–peptide fusions. Methods 23:287–93 [Google Scholar]
  61. Ja WW, Roberts RW. 61.  2004. In vitro selection of state-specific peptide modulators of G protein signaling using mRNA display. Biochemistry 43:9265–75 [Google Scholar]
  62. Wilson DS, Keefe AD, Szostak JW. 62.  2001. The use of mRNA display to select high-affinity protein-binding peptides. Proc. Natl. Acad. Sci. USA 98:3750–55 [Google Scholar]
  63. Ja WW, Adhikari A, Austin RJ, Sprang SR, Roberts RW. 63.  2005. A peptide core motif for binding to heterotrimeric G protein α subunits. J. Biol. Chem. 280:32057–60 [Google Scholar]
  64. Ja WW, Wiser O, Austin RJ, Jan LY, Roberts RW. 64.  2006. Turning G proteins on and off using peptide ligands. Am. Chem. Soc. Chem. Biol. 1:570–74 [Google Scholar]
  65. Keefe AD, Szostak JW. 65.  2001. Functional proteins from a random-sequence library. Nature 410:715–18 [Google Scholar]
  66. Ja WW, West AP Jr, Delker SL, Bjorkman PJ, Benzer S, Roberts RW. 66.  2007. Extension of Drosophila melanogaster life span with a GPCR peptide inhibitor. Nat. Chem. Biol. 3:415–19 [Google Scholar]
  67. Millward SW, Takahashi TT, Roberts RW. 67.  2005. A general route for post-translational cyclization of mRNA display libraries. J. Am. Chem. Soc. 127:14142–43 [Google Scholar]
  68. Millward SW, Fiacco S, Austin RJ, Roberts RW. 68.  2007. Design of cyclic peptides that bind protein surfaces with antibody-like affinity. Am. Chem. Soc. Chem. Biol. 2:625–34 [Google Scholar]
  69. Hallen HE, Luo H, Scott-Craig JS, Walton JD. 69.  2007. Gene family encoding the major toxins of lethal Amanita mushrooms. Proc. Natl. Acad. Sci. USA 104:19097–101 [Google Scholar]
  70. Koehnke J, Bent A, Houssen WE, Zollman D, Morawitz F. 70.  et al. 2012. The mechanism of patellamide macrocyclization revealed by the characterization of the PatG macrocyclase domain. Nat. Struct. Mol. Biol. 19:767–72 [Google Scholar]
  71. Strieker M, Tanovic A, Marahiel MA. 71.  2010. Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 20:234–40 [Google Scholar]
  72. Siewers V, San-Bento R, Nielsen J. 72.  2010. Implementation of communication-mediating domains for non-ribosomal peptide production in Saccharomyces cerevisiae. Biotechnol. Bioeng. 106:841–44 [Google Scholar]
  73. Wilkinson B, Micklefield J. 73.  2007. Mining and engineering natural-product biosynthetic pathways. Nat. Chem. Biol. 3:379–86 [Google Scholar]
  74. Yin J, Liu F, Schinke M, Daly C, Walsh CT. 74.  2004. Phagemid encoded small molecules for high throughput screening of chemical libraries. J. Am. Chem. Soc. 126:13570–71 [Google Scholar]
  75. Ellman JA, Mendel D, Schultz PG. 75.  1992. Site-specific incorporation of novel backbone structures into proteins. Science 255:197–200 [Google Scholar]
  76. Noren CJ, Anthony-Cahill SJ, Griffith MC, Schultz PG. 76.  1989. A general method for site-specific incorporation of unnatural amino acids into proteins. Science 244:182–88 [Google Scholar]
  77. Davis L, Chin JW. 77.  2012. Designer proteins: applications of genetic code expansion in cell biology. Nat. Rev. Mol. Cell Biol. 13:168–82 [Google Scholar]
  78. Hoesl MG, Budisa N. 78.  2012. Recent advances in genetic code engineering in Escherichia coli. Curr. Opin. Biotechnol. 23:751–57 [Google Scholar]
  79. Liu CC, Schultz PG. 79.  2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79:413–44 [Google Scholar]
  80. Neumann H.80.  2012. Rewiring translation—genetic code expansion and its applications. FEBS Lett. 586:2057–64 [Google Scholar]
  81. Hohsaka T, Fukushima M, Sisido M. 81.  2002. Nonnatural mutagenesis in E. coli and rabbit reticulocyte lysates by using four-base codons. Nucleic Acids Res. Suppl. 2:201–2 [Google Scholar]
  82. Hohsaka T, Muranaka N, Komiyama C, Matsui K, Takaura S. 82.  et al. 2004. Position-specific incorporation of dansylated non-natural amino acids into streptavidin by using a four-base codon. FEBS Lett. 560:173–77 [Google Scholar]
  83. Neumann H, Wang K, Davis L, Garcia-Alai M, Chin JW. 83.  2010. Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 464:441–44 [Google Scholar]
  84. Taira H, Fukushima M, Hohsaka T, Sisido M. 84.  2005. Four-base codon–mediated incorporation of non-natural amino acids into proteins in a eukaryotic cell–free translation system. J. Biosci. Bioeng. 99:473–76 [Google Scholar]
  85. Hayashi G, Goto Y, Suga H. 85.  2010. Ribosome evolution for two artificial amino acids in E. coli. Chem. Biol. 17:320–21 [Google Scholar]
  86. Bain JD, Diala ES, Glabe CG, Wacker DA, Lyttle MH. 86.  et al. 1991. Site-specific incorporation of nonnatural residues during in vitro protein biosynthesis with semisynthetic aminoacyl-tRNAs. Biochemistry 30:5411–21 [Google Scholar]
  87. Bain JD, Wacker DA, Kuo EE, Chamberlin AR. 87.  1991. Site-specific incorporation of non-natural residues into peptides: effect of residue structure on suppression and translation efficiencies. Tetrahedron 47:2389–400 [Google Scholar]
  88. Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T. 88.  et al. 2001. Cell-free translation reconstituted with purified components. Nat. Biotechnol. 19:751–55 [Google Scholar]
  89. Forster AC, Tan Z, Nalam MN, Lin H, Qu H. 89.  et al. 2003. Programming peptidomimetic syntheses by translating genetic codes designed de novo. Proc. Natl. Acad. Sci. USA 100:6353–57 [Google Scholar]
  90. Pavlov MY, Watts RE, Tan Z, Cornish VW, Ehrenberg M, Forster AC. 90.  2009. Slow peptide bond formation by proline and other N-alkylamino acids in translation. Proc. Natl. Acad. Sci. USA 106:50–54 [Google Scholar]
  91. Tan Z, Blacklow SC, Cornish VW, Forster AC. 91.  2005. De novo genetic codes and PURE translation display. Methods 36:279–90 [Google Scholar]
  92. Zhang B, Tan Z, Dickson LG, Nalam MN, Cornish VW, Forster AC. 92.  2007. Specificity of translation for N-alkyl amino acids. J. Am. Chem. Soc. 129:11316–17 [Google Scholar]
  93. Josephson K, Hartman MC, Szostak JW. 93.  2005. Ribosomal synthesis of unnatural peptides. J. Am. Chem. Soc. 127:11727–35 [Google Scholar]
  94. Hartman MC, Josephson K, Szostak JW. 94.  2006. Enzymatic aminoacylation of tRNA with unnatural amino acids. Proc. Natl. Acad. Sci. USA 103:4356–61 [Google Scholar]
  95. Hartman MC, Josephson K, Lin CW, Szostak JW. 95.  2007. An expanded set of amino acid analogs for the ribosomal translation of unnatural peptides. PLoS ONE 2:e972 [Google Scholar]
  96. Schlippe YV, Hartman MC, Josephson K, Szostak JW. 96.  2012. In vitro selection of highly modified cyclic peptides that act as tight binding inhibitors. J. Am. Chem. Soc. 134:10469–77 [Google Scholar]
  97. Seebeck FP, Ricardo A, Szostak JW. 97.  2011. Artificial lantipeptides from in vitro translations. Chem. Commun. 47:6141–43 [Google Scholar]
  98. Seebeck FP, Szostak JW. 98.  2006. Ribosomal synthesis of dehydroalanine-containing peptides. J. Am. Chem. Soc. 128:7150–51 [Google Scholar]
  99. Merryman C, Green R. 99.  2004. Transformation of aminoacyl tRNAs for the in vitro selection of “drug-like” molecules. Chem. Biol. 11:575–82 [Google Scholar]
  100. Subtelny AO, Hartman MC, Szostak JW. 100.  2008. Ribosomal synthesis of N-methyl peptides. J. Am. Chem. Soc. 130:6131–36 [Google Scholar]
  101. Subtelny AO, Hartman MC, Szostak JW. 101.  2011. Optimal codon choice can improve the efficiency and fidelity of N-methyl amino acid incorporation into peptides by in-vitro translation. Angew. Chem. Int. Ed. Engl. 50:3164–67 [Google Scholar]
  102. Morimoto J, Hayashi Y, Iwasaki K, Suga H. 102.  2011. Flexizymes: their evolutionary history and the origin of catalytic function. Acc. Chem. Res. 44:1359–68 [Google Scholar]
  103. Passioura T, Suga H. 103.  2013. Flexizyme-mediated genetic reprogramming as a tool for noncanonical peptide synthesis and drug discovery. Chemistry 19:6530–36 [Google Scholar]
  104. Goto Y, Suga H. 104.  2012. Flexizymes as a tRNA acylation tool facilitating genetic code reprogramming. Methods Mol. Biol. 848:465–78 [Google Scholar]
  105. Goto Y, Katoh T, Suga H. 105.  2011. Flexizymes for genetic code reprogramming. Nat. Protoc. 6:779–90 [Google Scholar]
  106. Murakami H, Ohta A, Ashigai H, Suga H. 106.  2006. A highly flexible tRNA acylation method for non-natural polypeptide synthesis. Nat. Methods 3:357–59 [Google Scholar]
  107. Niwa N, Yamagishi Y, Murakami H, Suga H. 107.  2009. A flexizyme that selectively charges amino acids activated by a water-friendly leaving group. Bioorg. Med. Chem. Lett. 19:3892–94 [Google Scholar]
  108. Kawakami T, Murakami H, Suga H. 108.  2008. Ribosomal synthesis of polypeptoids and peptoid–peptide hybrids. J. Am. Chem. Soc. 130:16861–63 [Google Scholar]
  109. Kawakami T, Murakami H, Suga H. 109.  2008. Messenger RNA–programmed incorporation of multiple N-methyl-amino acids into linear and cyclic peptides. Chem. Biol. 15:32–42 [Google Scholar]
  110. Yamagishi Y, Shoji I, Miyagawa S, Kawakami T, Katoh T. 110.  et al. 2011. Natural product–like macrocyclic N-methyl-peptide inhibitors against a ubiquitin ligase uncovered from a ribosome-expressed de novo library. Chem. Biol. 18:1562–70 [Google Scholar]
  111. Goto Y, Ashigai H, Sako Y, Murakami H, Suga H. 111.  2006. Translation initiation by using various N-acylaminoacyl tRNAs. Nucleic Acids Symp. Ser. 50293–94
  112. Goto Y, Suga H. 112.  2009. Translation initiation with initiator tRNA charged with exotic peptides. J. Am. Chem. Soc. 131:5040–41 [Google Scholar]
  113. Goto Y, Murakami H, Suga H. 113.  2008. Initiating translation with D-amino acids. RNA 14:1390–98 [Google Scholar]
  114. Fujino T, Goto Y, Suga H, Murakami H. 114.  2013. Reevaluation of the D-amino acid compatibility with the elongation event in translation. J. Am. Chem. Soc. 135:1830–37 [Google Scholar]
  115. Murakami H, Ohta A, Goto Y, Sako Y, Suga H. 115.  2006. Flexizyme as a versatile tRNA acylation catalyst and the application for translation. Nucleic Acids Symp. Ser. 5035–36
  116. Ohta A, Murakami H, Higashimura E, Suga H. 116.  2007. Synthesis of polyester by means of genetic code reprogramming. Chem. Biol. 14:1315–22 [Google Scholar]
  117. Goto Y, Ohta A, Sako Y, Yamagishi Y, Murakami H, Suga H. 117.  2008. Reprogramming the translation initiation for the synthesis of physiologically stable cyclic peptides. Am. Chem. Soc. Chem. Biol. 3:120–29 [Google Scholar]
  118. Ohta A, Murakami H, Suga H. 118.  2008. Polymerization of α-hydroxy acids by ribosomes. ChemBioChem 9:2773–78 [Google Scholar]
  119. Sako Y, Goto Y, Murakami H, Suga H. 119.  2008. Ribosomal synthesis of peptidase-resistant peptides closed by a nonreducible inter-side-chain bond. Am. Chem. Soc. Chem. Biol. 3:241–49 [Google Scholar]
  120. Sako Y, Morimoto J, Murakami H, Suga H. 120.  2008. Ribosomal synthesis of bicyclic peptides via two orthogonal inter-side-chain reactions. J. Am. Chem. Soc. 130:7232–34 [Google Scholar]
  121. Goto Y, Iwasaki K, Torikai K, Murakami H, Suga H. 121.  2009. Ribosomal synthesis of dehydrobutyrine- and methyllanthionine-containing peptides. Chem. Commun. 23:3419–21 [Google Scholar]
  122. Kawakami T, Ohta A, Ohuchi M, Ashigai H, Murakami H, Suga H. 122.  2009. Diverse backbone-cyclized peptides via codon reprogramming. Nat. Chem. Biol. 5:888–90 [Google Scholar]
  123. Nakajima E, Goto Y, Sako Y, Murakami H, Suga H. 123.  2009. Ribosomal synthesis of peptides with C-terminal lactams, thiolactones, and alkylamides. ChemBioChem 10:1186–92 [Google Scholar]
  124. Yamagishi Y, Ashigai H, Goto Y, Murakami H, Suga H. 124.  2009. Ribosomal synthesis of cyclic peptides with a fluorogenic oxidative coupling reaction. ChemBioChem 10:1469–72 [Google Scholar]
  125. Ohshiro Y, Nakajima E, Goto Y, Fuse S, Takahashi T. 125.  et al. 2011. Ribosomal synthesis of backbone-macrocyclic peptides containing γ-amino acids. ChemBioChem 12:1183–87 [Google Scholar]
  126. Hayashi Y, Morimoto J, Suga H. 126.  2012. In vitro selection of anti-Akt2 thioether-macrocyclic peptides leading to isoform-selective inhibitors. Am. Chem. Soc. Chem. Biol. 7:607–13 [Google Scholar]
  127. Morimoto J, Hayashi Y, Suga H. 127.  2012. Discovery of macrocyclic peptides armed with a mechanism-based warhead: isoform-selective inhibition of human deacetylase SIRT2. Angew. Chem. Int. Ed. Engl. 51:3423–27 [Google Scholar]
  128. Frankel A, Roberts RW. 128.  2003. In vitro selection for sense codon suppression. RNA 9:780–86 [Google Scholar]
  129. Li S, Millward S, Roberts R. 129.  2002. In vitro selection of mRNA display libraries containing an unnatural amino acid. J. Am. Chem. Soc. 124:9972–73 [Google Scholar]
  130. Liu CC, Mack AV, Brustad EM, Mills JH, Groff D. 130.  et al. 2009. Evolution of proteins with genetically encoded “chemical warheads”. J. Am. Chem. Soc. 131:9616–17 [Google Scholar]
  131. Liu CC, Mack AV, Tsao ML, Mills JH, Lee HS. 131.  et al. 2008. Protein evolution with an expanded genetic code. Proc. Natl. Acad. Sci. USA 105:17688–93 [Google Scholar]
  132. Liu M, Tada S, Ito M, Abe H, Ito Y. 132.  2012. In vitro selection of a photo-responsive peptide aptamer using ribosome display. Chem. Commun. 48:11871–73 [Google Scholar]
  133. Muranaka N, Hohsaka T, Sisido M. 133.  2006. Four-base codon mediated mRNA display to construct peptide libraries that contain multiple nonnatural amino acids. Nucleic Acids Res. 34:e7 [Google Scholar]
  134. Young TS, Young DD, Ahmad I, Louis JM, Benkovic SJ, Schultz PG. 134.  2011. Evolution of cyclic peptide protease inhibitors. Proc. Natl. Acad. Sci. USA 108:11052–56 [Google Scholar]
  135. Forster AC, Cornish VW, Blacklow SC. 135.  2004. PURE translation display. Anal. Biochem. 333:358–64 [Google Scholar]
  136. Hofmann FT, Szostak JW, Seebeck FP. 136.  2012. In vitro selection of functional lantipeptides. J. Am. Chem. Soc. 134:8038–41 [Google Scholar]
  137. Tanaka Y, Hipolito CJ, Maturana AD, Ito K, Kuroda T. 137.  et al. 2013. Structural basis for the drug extrusion mechanism by a MATE multidrug transporter. Nature 496:247–51 [Google Scholar]
  138. Kawakami T, Ishizawa T, Fujino T, Reid PC, Suga H, Murakami H. 138.  2013. In vitro selection of multiple libraries created by genetic code reprogramming to discover macrocyclic peptides that antagonize VEGFR2 activity in living cells. ACS Chem. Biol. 8:1205–14 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060713-035456
Loading
/content/journals/10.1146/annurev-biochem-060713-035456
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error