1932

Abstract

Genetic code reprogramming has enabled us to ribosomally incorporate various nonproteinogenic amino acids (npAAs) into peptides in vitro. The repertoire of usable npAAs has been expanded to include not only -α-amino acids with noncanonical sidechains but also those with noncanonical backbones. Despite successful single incorporation of npAAs, multiple and consecutive incorporations often suffer from low efficiency or are even unsuccessful. To overcome this stumbling block, engineering approaches have been used to modify ribosomes, EF-Tu, and tRNAs. Here, we provide an overview of these in vitro methods that are aimed at optimal expansion of the npAA repertoire and their applications for the development of de novo bioactive peptides containing various npAAs.

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2022-06-21
2024-06-24
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Literature Cited

  1. 1.
    Di Gioia ML, Leggio A, Malagrino F, Romio E, Siciliano C, Liguori A. 2016. N-Methylated α-amino acids and peptides: synthesis and biological activity. Mini-Rev. Med. Chem. 16:683–90
    [Google Scholar]
  2. 2.
    Ollivaux C, Soyez D, Toullec JY. 2014. Biogenesis of d-amino acid containing peptides/proteins: where, when and how?. J. Pept. Sci. 20:595–612
    [Google Scholar]
  3. 3.
    Kudo F, Miyanaga A, Eguchi T. 2014. Biosynthesis of natural products containing β-amino acids. Nat. Prod. Rep. 31:1056–73
    [Google Scholar]
  4. 4.
    Alonzo DA, Schmeing TM. 2020. Biosynthesis of depsipeptides, or depsi: the peptides with varied generations. Protein Sci 29:2316–47
    [Google Scholar]
  5. 5.
    Chapeville F, Lipmann F, Von Ehrenstein G, Weisblum B, Ray WJ, Benzer S. 1962. On the role of soluble ribonucleic acid in coding for amino acids. PNAS 48:1086–92
    [Google Scholar]
  6. 6.
    Fahnestock S, Rich A. 1971. Ribosome-catalyzed polyester formation. Science 173:340–43
    [Google Scholar]
  7. 7.
    Forster A, Tan Z, Nalam M, Lin H, Qu H et al. 2003. Programming peptidomimetic syntheses by translating genetic codes designed de novo. PNAS 100:6353–57
    [Google Scholar]
  8. 8.
    Ohta A, Murakami H, Higashimura E, Suga H. 2007. Synthesis of polyester by means of genetic code reprogramming. Chem. Biol. 14:1315–22
    [Google Scholar]
  9. 9.
    Noren C, Anthony-Cahill S, Griffith M, Schultz P 1989. A general method for site-specific incorporation of unnatural amino acids into proteins. Science 244:182–88
    [Google Scholar]
  10. 10.
    Hohsaka T, Ashizuka Y, Murakami H, Sisido M. 1996. Incorporation of nonnatural amino acids into streptavidin through in vitro frame-shift suppression. J. Am. Chem. Soc. 118:9778–79
    [Google Scholar]
  11. 11.
    Murakami H, Hohsaka T, Ashizuka Y, Sisido M. 1998. Site-directed incorporation of p-nitrophenylalanine into streptavidin and site-to-site photoinduced electron transfer from a pyrenyl group to a nitrophenyl group on the protein framework. J. Am. Chem. Soc. 120:7520–29
    [Google Scholar]
  12. 12.
    Hohsaka T, Ashizuka Y, Murakami H, Sisido M. 2001. Five-base codons for incorporation of nonnatural amino acids into proteins. Nucleic Acids Res 29:3646–51
    [Google Scholar]
  13. 13.
    Bain JD, Switzer C, Chamberlin R, Benner SA. 1992. Ribosome-mediated incorporation of a non-standard amino acid into a peptide through expansion of the genetic code. Nature 356:537–39
    [Google Scholar]
  14. 14.
    Hirao I, Ohtsuki T, Fujiwara T, Mitsui T, Yokogawa T et al. 2002. An unnatural base pair for incorporating amino acid analogs into proteins. Nat. Biotechnol. 20:177–82
    [Google Scholar]
  15. 15.
    Feldman AW, Dien VT, Karadeema RJ, Fischer EC, You Y et al. 2019. Optimization of replication, transcription, and translation in a semi-synthetic organism. J. Am. Chem. Soc. 141:10644–53
    [Google Scholar]
  16. 16.
    Wang L, Brock A, Herberich B, Schultz PG. 2001. Expanding the genetic code of Escherichia coli. Science 292:498–500
    [Google Scholar]
  17. 17.
    Chin JW, Cropp TA, Anderson JC, Mukherji M, Zhang Z, Schultz PG. 2003. An expanded eukaryotic genetic code. Science 301:964–67
    [Google Scholar]
  18. 18.
    Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79:413–44
    [Google Scholar]
  19. 19.
    Ai HW. 2012. Biochemical analysis with the expanded genetic lexicon. Anal. Bioanal. Chem. 403:2089–102
    [Google Scholar]
  20. 20.
    Polycarpo CR, Herring S, Bérubé A, Wood JL, Söll D, Ambrogelly A. 2006. Pyrrolysine analogues as substrates for pyrrolysyl-tRNA synthetase. FEBS Lett 580:6695–700
    [Google Scholar]
  21. 21.
    Wang Y-S, Fang X, Wallace AL, Wu B, Liu WR. 2012. A rationally designed pyrrolysyl-tRNA synthetase mutant with a broad substrate spectrum. J. Am. Chem. Soc. 134:2950–53
    [Google Scholar]
  22. 22.
    Merryman C, Green R. 2004. Transformation of aminoacyl tRNAs for the in vitro selection of “drug-like” molecules. Chem. Biol. 11:575–82
    [Google Scholar]
  23. 23.
    Gite S, Mamaev S, Olejnik J, Rothschild K. 2000. Ultrasensitive fluorescence-based detection of nascent proteins in gels. Anal. Biochem. 279:218–25
    [Google Scholar]
  24. 24.
    Forster AC, Cornish VW, Blacklow SC. 2004. Pure translation display. Anal. Biochem. 333:358–64
    [Google Scholar]
  25. 25.
    Mamaev S, Olejnik J, Olejnik EK, Rothschild KJ. 2004. Cell-free N-terminal protein labeling using initiator suppressor tRNA. Anal. Biochem. 326:25–32
    [Google Scholar]
  26. 26.
    Hecht SM, Alford BL, Kuroda Y, Kitano S. 1978.. “ Chemical aminoacylation” of tRNA's. J. Biol. Chem. 253:4517–20
    [Google Scholar]
  27. 27.
    Heckler TG, Zama Y, Naka T, Hecht SM. 1983. Dipeptide formation with misacylated tRNAPhes. J. Biol. Chem. 258:4492–95
    [Google Scholar]
  28. 28.
    Robertson SA, Noren CJ, Anthony-Cahill SJ, Griffith MC, Schultz PG. 1989. The use of 5′-phospho-2 deoxyribocytidylylriboadenosine as a facile route to chemical aminoacylation of tRNA. Nucleic Acids Res 17:9649–60
    [Google Scholar]
  29. 29.
    Servillo L, Balestrieri C, Quagliuolo L, Iorio EL, Giovane A. 1993. tRNA fluorescent labeling at 3′ end inducing an aminoacyl-tRNA-like behavior. Eur. J. Biochem. 213:583–89
    [Google Scholar]
  30. 30.
    Ad O, Hoffman KS, Cairns AG, Featherston AL, Miller SJ et al. 2019. Translation of diverse aramid- and 1,3-dicarbonyl-peptides by wild type ribosomes in vitro. ACS Cent. Sci. 5:1289–94
    [Google Scholar]
  31. 31.
    Katoh T, Suga H. 2020. Ribosomal elongation of cyclic γ-amino acids using a reprogrammed genetic code. J. Am. Chem. Soc. 142:4965–69
    [Google Scholar]
  32. 32.
    Saito H. 2001. An in vitro evolved precursor tRNA with aminoacylation activity. EMBO J 20:1797–806
    [Google Scholar]
  33. 33.
    Saito H. 2002. Outersphere and innersphere coordinated metal ions in an aminoacyl-tRNA synthetase ribozyme. Nucleic Acids Res 30:5151–59
    [Google Scholar]
  34. 34.
    Murakami H, Bonzagni NJ, Suga H. 2002. Aminoacyl-tRNA synthesis by a resin-immobilized ribozyme. J. Am. Chem. Soc. 124:6834–35
    [Google Scholar]
  35. 35.
    Murakami H, Kourouklis D, Suga H. 2003. Using a solid-phase ribozyme aminoacylation system to reprogram the genetic code. Chem. Biol. 10:1077–84
    [Google Scholar]
  36. 36.
    Murakami H, Saito H, Suga H. 2003. A versatile tRNA aminoacylation catalyst based on RNA. Chem. Biol. 10:655–62
    [Google Scholar]
  37. 37.
    Murakami H, Ohta A, Ashigai H, Suga H. 2006. A highly flexible tRNA acylation method for non-natural polypeptide synthesis. Nat. Methods 3:357–59
    [Google Scholar]
  38. 38.
    Goto Y, Katoh T, Suga H. 2011. Flexizymes for genetic code reprogramming. Nat. Protoc. 6:779–90
    [Google Scholar]
  39. 39.
    Niwa N, Yamagishi Y, Murakami H, Suga H. 2009. A flexizyme that selectively charges amino acids activated by a water-friendly leaving group. Bioorg. Med. Chem. Lett. 19:3892–94
    [Google Scholar]
  40. 40.
    Goto Y, Murakami H, Suga H. 2008. Initiating translation with d-amino acids. RNA 14:1390–98
    [Google Scholar]
  41. 41.
    Goto Y, Suga H. 2009. Translation initiation with initiator tRNA charged with exotic peptides. J. Am. Chem. Soc. 131:5040–41
    [Google Scholar]
  42. 42.
    Kawakami T, Murakami H, Suga H. 2008. Messenger RNA-programmed incorporation of multiple N-methyl-amino acids into linear and cyclic peptides. Chem. Biol. 15:32–42
    [Google Scholar]
  43. 43.
    Kawakami T, Murakami H, Suga H. 2008. Ribosomal synthesis of polypeptoids and peptoid-peptide hybrids. J. Am. Chem. Soc. 130:16861–63
    [Google Scholar]
  44. 44.
    Yamagishi Y, Shoji I, Miyagawa S, Kawakami T, Katoh T 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]
  45. 45.
    Fujino T, Goto Y, Suga H, Murakami H. 2013. Reevaluation of the d-amino acid compatibility with the elongation event in translation. J. Am. Chem. Soc. 135:1830–37
    [Google Scholar]
  46. 46.
    Fujino T, Goto Y, Suga H, Murakami H. 2016. Ribosomal synthesis of peptides with multiple β-amino acids. J. Am. Chem. Soc. 138:1962–69
    [Google Scholar]
  47. 47.
    Takatsuji R, Shinbara K, Katoh T, Goto Y, Passioura T et al. 2019. Ribosomal synthesis of backbone-cyclic peptides compatible with in vitro display. J. Am. Chem. Soc. 141:2279–87
    [Google Scholar]
  48. 48.
    Maini R, Kimura H, Takatsuji R, Katoh T, Goto Y, Suga H. 2019. Ribosomal formation of thioamide bonds in polypeptide synthesis. J. Am. Chem. Soc. 141:20004–8
    [Google Scholar]
  49. 49.
    Katoh T, Sengoku T, Hirata K, Ogata K, Suga H. 2020. Ribosomal synthesis and de novo discovery of bioactive foldamer peptides containing cyclic β-amino acids. Nat. Chem. 12:1081–88
    [Google Scholar]
  50. 50.
    Katoh T, Suga H. 2020. Ribosomal elongation of aminobenzoic acid derivatives. J. Am. Chem. Soc. 142:16518–22
    [Google Scholar]
  51. 51.
    Tan Z, Forster A, Blacklow S, Cornish V. 2004. Amino acid backbone specificity of the Escherichia coli translation machinery. J. Am. Chem. Soc. 126:12752–53
    [Google Scholar]
  52. 52.
    Dedkova LM, Fahmi NE, Golovine SY, Hecht SM. 2003. Enhanced d-amino acid incorporation into protein by modified ribosomes. J. Am. Chem. Soc. 125:6616–17
    [Google Scholar]
  53. 53.
    Achenbach J, Jahnz M, Bethge L, Paal K, Jung M et al. 2015. Outwitting EF-Tu and the ribosome: translation with d-amino acids. Nucleic Acids Res 43:5687–98
    [Google Scholar]
  54. 54.
    Katoh T, Tajima K, Suga H. 2017. Consecutive elongation of D-amino acids in translation. Cell Chem. Biol. 24:46–54
    [Google Scholar]
  55. 55.
    Katoh T, Iwane Y, Suga H. 2017. Logical engineering of D-arm and T-stem of tRNA that enhances d-amino acid incorporation. Nucleic Acids Res 45:12601–10
    [Google Scholar]
  56. 56.
    Katoh T, Suga H. 2018. Ribosomal incorporation of consecutive β-amino acids. J. Am. Chem. Soc. 140:12159–67
    [Google Scholar]
  57. 57.
    Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Reshetnikova L et al. 1995. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270:1464–72
    [Google Scholar]
  58. 58.
    Asahara H, Uhlenbeck OC. 2002. The tRNA specificity of Thermus thermophilus EF-Tu. PNAS 99:3499–504
    [Google Scholar]
  59. 59.
    Sanderson LE, Uhlenbeck OC. 2007. Directed mutagenesis identifies amino acid residues involved in elongation factor Tu binding to yeast Phe-tRNAPhe. J. Mol. Biol. 368:119–30
    [Google Scholar]
  60. 60.
    Schrader JM, Chapman SJ, Uhlenbeck OC. 2009. Understanding the sequence specificity of tRNA binding to elongation factor Tu using tRNA mutagenesis. J. Mol. Biol. 386:1255–64
    [Google Scholar]
  61. 61.
    LaRiviere FJ, Wolfson AD, Uhlenbeck OC. 2001. Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294:165–68
    [Google Scholar]
  62. 62.
    Iwane Y, Kimura H, Katoh T, Suga H. 2021. Uniform affinity-tuning of N-methyl-aminoacyl-tRNAs to EF-Tu enhances their multiple incorporation. Nucleic Acids Res 49:10807–17
    [Google Scholar]
  63. 63.
    Schrader JM, Chapman SJ, Uhlenbeck OC. 2011. Tuning the affinity of aminoacyl-tRNA to elongation factor Tu for optimal decoding. PNAS 108:5215–20
    [Google Scholar]
  64. 64.
    Terasaka N, Hayashi G, Katoh T, Suga H. 2014. An orthogonal ribosome-tRNA pair via engineering of the peptidyl transferase center. Nat. Chem. Biol. 10:555–57
    [Google Scholar]
  65. 65.
    Doi Y, Ohtsuki T, Shimizu Y, Ueda T, Sisido M. 2007. Elongation factor Tu mutants expand amino acid tolerance of protein biosynthesis system. J. Am. Chem. Soc. 129:14458–62
    [Google Scholar]
  66. 66.
    Park HS, Hohn MJ, Umehara T, Guo LT, Osborne EM et al. 2011. Expanding the genetic code of Escherichia coli with phosphoserine. Science 333:1151–54
    [Google Scholar]
  67. 67.
    Fan C, Ip K, Soll D. 2016. Expanding the genetic code of Escherichia coli with phosphotyrosine. FEBS Lett 590:3040–47
    [Google Scholar]
  68. 68.
    Haruna K, Alkazemi MH, Liu Y, Soll D, Englert M. 2014. Engineering the elongation factor Tu for efficient selenoprotein synthesis. Nucleic Acids Res 42:9976–83
    [Google Scholar]
  69. 69.
    Melnikov SV, Khabibullina NF, Mairhofer E, Vargas-Rodriguez O, Reynolds NM et al. 2019. Mechanistic insights into the slow peptide bond formation with D-amino acids in the ribosomal active site. Nucleic Acids Res 47:2089–100
    [Google Scholar]
  70. 70.
    Englander MT, Avins JL, Fleisher RC, Liu B, Effraim PR et al. 2015. The ribosome can discriminate the chirality of amino acids within its peptidyl-transferase center. PNAS 112:6038–43
    [Google Scholar]
  71. 71.
    Fleisher RC, Cornish VW, Gonzalez RL. 2018. d-Amino acid-mediated translation arrest is modulated by the identity of the incoming aminoacyl-tRNA. Biochemistry 57:4241–46
    [Google Scholar]
  72. 72.
    Liljeruhm J, Wang J, Kwiatkowski M, Sabari S, Forster AC. 2019. Kinetics of d-amino acid incorporation in translation. ACS Chem. Biol. 14:204–13
    [Google Scholar]
  73. 73.
    Dedkova LM, Fahmi NE, Golovine SY, Hecht SM. 2006. Construction of modified ribosomes for incorporation of d-amino acids into proteins. Biochemistry 45:15541–51
    [Google Scholar]
  74. 74.
    Dedkova LM, Fahmi NE, Paul R, del Rosario M, Zhang L et al. 2011. β-Puromycin selection of modified ribosomes for in vitro incorporation of β-amino acids. Biochemistry 51:401–15
    [Google Scholar]
  75. 75.
    Maini R, Nguyen DT, Chen S, Dedkova LM, Chowdhury SR et al. 2013. Incorporation of β-amino acids into dihydrofolate reductase by ribosomes having modifications in the peptidyltransferase center. Bioorg. Med. Chem. 21:1088–96
    [Google Scholar]
  76. 76.
    Maini R, Chowdhury SR, Dedkova LM, Roy B, Daskalova SM et al. 2015. Protein synthesis with ribosomes selected for the incorporation of β-amino acids. Biochemistry 54:3694–706
    [Google Scholar]
  77. 77.
    Czekster CM, Robertson WE, Walker AS, Soll D, Schepartz A. 2016. In vivo biosynthesis of a β-amino acid-containing protein. J. Am. Chem. Soc. 138:5194–97
    [Google Scholar]
  78. 78.
    Doerfel LK, Wohlgemuth I, Kubyshkin V, Starosta AL, Wilson DN et al. 2015. Entropic contribution of elongation factor P to proline positioning at the catalytic center of the ribosome. J. Am. Chem. Soc. 137:12997–3006
    [Google Scholar]
  79. 79.
    Ude S, Lassak J, Starosta A, Kraxenberger T, Wilson D, Jung K 2013. Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339:82–85
    [Google Scholar]
  80. 80.
    Katoh T, Wohlgemuth I, Nagano M, Rodnina MV, Suga H. 2016. Essential structural elements in tRNAPro for EF-P-mediated alleviation of translation stalling. Nat. Commun. 7:11657
    [Google Scholar]
  81. 81.
    Huter P, Arenz S, Bock LV, Graf M, Frister JO et al. 2017. Structural basis for polyproline-mediated ribosome stalling and rescue by the translation elongation factor EF-P. Mol. Cell 68:515–27.e6
    [Google Scholar]
  82. 82.
    Tajima K, Katoh T, Suga H. 2022. Drop-off-reinitiation triggered by EF-G-driven mistranslocation and its alleviation by EF-P. Nucleic Acids Res. 50:273653
    [Google Scholar]
  83. 83.
    Kang TJ, Suga H. 2011. Translation of a histone H3 tail as a model system for studying peptidyl-tRNA drop-off. FEBS Lett 585:2269–74
    [Google Scholar]
  84. 84.
    Rao AR. 2001. Specific interaction between the ribosome recycling factor and the elongation factor G from Mycobacterium tuberculosis mediates peptidyl-tRNA release and ribosome recycling in Escherichia coli. EMBO J 20:2977–86
    [Google Scholar]
  85. 85.
    Iwane Y, Hitomi A, Murakami H, Katoh T, Goto Y, Suga H. 2016. Expanding the amino acid repertoire of ribosomal polypeptide synthesis via the artificial division of codon boxes. Nat. Chem. 8:317–25
    [Google Scholar]
  86. 86.
    Dunkelmann DL, Willis JCW, Beattie AT, Chin JW. 2020. Engineered triply orthogonal pyrrolysyl–tRNA synthetase/tRNA pairs enable the genetic encoding of three distinct non-canonical amino acids. Nat. Chem. 12:535–44
    [Google Scholar]
  87. 87.
    Switzer C, Moroney SE, Benner SA. 1989. Enzymatic incorporation of a new base pair into DNA and RNA. J. Am. Chem. Soc. 111:8322–23
    [Google Scholar]
  88. 88.
    Nemoto N, Miyamoto-Sato E, Husimi Y, Yanagawa H. 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]
  89. 89.
    Roberts RW, Szostak JW. 1997. RNA-peptide fusions for the in vitro selection of peptides and proteins. PNAS 94:12297–302
    [Google Scholar]
  90. 90.
    Mattheakis LC, Bhatt RR, Dower WJ. 1994. An in vitro polysome display system for identifying ligands from very large peptide libraries. PNAS 91:9022–26
    [Google Scholar]
  91. 91.
    Smith G. 1985. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–17
    [Google Scholar]
  92. 92.
    Mathur D, Prakash S, Anand P, Kaur H, Agrawal P et al. 2016. PEPlife: a repository of the half-life of peptides. Sci. Rep. 6:36617
    [Google Scholar]
  93. 93.
    Miller SM, Simon RJ, Ng S, Zuckermann RN, Kerr JM, Moos WH. 1995. Comparison of the proteolytic susceptibilities of homologous L-amino acid, D-amino acid, and N-substituted glycine peptide and peptoid oligomers. Drug Dev. Res. 35:20–32
    [Google Scholar]
  94. 94.
    Elmquist A, Langel Ü. 2003. In vitro uptake and stability study of pVEC and its all-D analog. Biol. Chem. 384:387–93
    [Google Scholar]
  95. 95.
    Zhao YY, Zhang M, Qiu S, Wang JY, Peng JX et al. 2016. Antimicrobial activity and stability of the d-amino acid substituted derivatives of antimicrobial peptide polybia-MPI. AMB Express 6:122
    [Google Scholar]
  96. 96.
    Elfgen A, Hupert M, Bochinsky K, Tusche M, González de San Román Martin E et al. 2019. Metabolic resistance of the D-peptide RD2 developed for direct elimination of amyloid-β oligomers. Sci. Rep. 9:5715
    [Google Scholar]
  97. 97.
    Imanishi S, Katoh T, Yin Y, Yamada M, Kawai M, Suga H. 2021. In vitro selection of macrocyclic d/l-hybrid peptides against human EGFR. J. Am. Chem. Soc. 143:5680–84
    [Google Scholar]
  98. 98.
    Goto Y, Ohta A, Sako Y, Yamagishi Y, Murakami H, Suga H. 2008. Reprogramming the translation initiation for the synthesis of physiologically stable cyclic peptides. ACS Chem. Biol. 3:120–29
    [Google Scholar]
  99. 99.
    Appella DH, Christianson LA, Karle IL, Powell DR, Gellman SH. 1996. β-Peptide foldamers: robust helix formation in a new family of β-amino acid oligomers. J. Am. Chem. Soc. 118:13071–72
    [Google Scholar]
  100. 100.
    Gellman SH. 1998. Foldamers: a manifesto. Acc. Chem. Res. 31:173–80
    [Google Scholar]
  101. 101.
    Schumann F, Müller A, Koksch M, Müller G, Sewald N. 2000. Are β-amino acids γ-turn mimetics? Exploring a new design principle for bioactive cyclopeptides. J. Am. Chem. Soc. 122:12009–10
    [Google Scholar]
  102. 102.
    Strijowski U, Sewald N. 2004. Structural properties of cyclic peptides containing cis- or trans-2-aminocyclohexane carboxylic acid. Org. Biomol. Chem. 2:1105–9
    [Google Scholar]
  103. 103.
    Malešević M, Majer Z, Vass E, Huber T, Strijowski U et al. 2006. Spectroscopic detection of pseudo-turns in homodetic cyclic penta- and hexapeptides comprising β-homoproline. Int. J. Pept. Res. Ther. 12:165–77
    [Google Scholar]
  104. 104.
    Guthohrlein EW, Malesevic M, Majer Z, Sewald N. 2007. Secondary structure inducing potential of β-amino acids: Torsion angle clustering facilitates comparison and analysis of the conformation during MD trajectories. Biopolymers 88:829–39
    [Google Scholar]
  105. 105.
    Appella DH, Christianson LA, Klein DA, Powell DR, Huang X et al. 1997. Residue-based control of helix shape in β-peptide oligomers. Nature 387:381–84
    [Google Scholar]
  106. 106.
    Langer O, Kahlig H, Zierler-Gould K, Bats JW, Mulzer J. 2002. A bicyclic cispentacin derivative as a novel reverse turn inducer in a GnRH mimetic. J. Org. Chem. 67:6878–83
    [Google Scholar]
  107. 107.
    Checco JW, Lee EF, Evangelista M, Sleebs NJ, Rogers K et al. 2015. α/β-peptide foldamers targeting intracellular protein–protein interactions with activity in living cells. J. Am. Chem. Soc. 137:11365–75
    [Google Scholar]
  108. 108.
    Katoh T, Sengoku T, Hirata K, Ogata K, Suga H. 2020. Ribosomal synthesis and de novo discovery of bioactive foldamer peptides containing cyclic β-amino acids. Nat. Chem. 12:1081–88
    [Google Scholar]
  109. 109.
    Katoh T, Suga H. 2022. In vitro selection of foldamer-like macrocyclic peptides containing 2-aminobenzoic acid and 3-aminothiophene-2-carboxylic acid. J. Am. Chem. Soc. 144:2069–72
    [Google Scholar]
  110. 110.
    Passioura T, Liu W, Dunkelmann D, Higuchi T, Suga H. 2018. Display selection of exotic macrocyclic peptides expressed under a radically reprogrammed 23 amino acid genetic code. J. Am. Chem. Soc. 140:11551–55
    [Google Scholar]
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