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Biotechnology and Bioprocess Engineering

, Volume 24, Issue 4, pp 592–604 | Cite as

Recent Advances in Enzyme Engineering through Incorporation of Unnatural Amino Acids

  • Yumi Won
  • Amol D. Pagar
  • Mahesh D. Patil
  • Philip E. Dawson
  • Hyungdon YunEmail author
Review Paper Protein Engineering and Enzyme Biotechnology

Abstract

The development of new enzyme engineering technologies has been actively pursued as the industrial use of biocatalysts is rapidly increasing. Traditional enzyme engineering has been limited to changing the functional properties of enzymes by replacing one amino acid with the other 19 natural amino acids. However, the incorporation of unnatural amino acids (UAAs) has been exploited to manipulate efficient enzymes for biocatalysis. This has been an effective enzyme engineering technique by complementing and extending the limits of traditional enzymatic functional changes. This review paper describes the basic functions of the new functional groups of UAAs used in enzyme engineering and the utilization of UAAs in the formation of chemical bonds in the proteins. The recent developments of UAA-mediated enzymology and its applicability in industry, pharmaceutical and other research areas to overcome the limitations of existing enzymes is also emphasized.

Keywords

unnatural amino acids biocatalysis covalent and noncovalent bonds enzyme engineering 

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Notes

Acknowledgments

This manuscript was supported by Konkuk University’s ‘Research Support for faculty on Sabbatical Leave’ program-2019.

References

  1. 1.
    Ravikumar, Y., S. P. Nadarajan, T. H. Yoo, C. S. Lee, and H. Yun (2015) Incorporating unnatural amino acids to engineer biocatalysts for industrial bioprocess applications. Biotechnol. J. 10: 1862–1876.CrossRefPubMedGoogle Scholar
  2. 2.
    Aissaoui, N., J. Landoulsi, L. Bergaoui, S. Boujday, and J.-F. Lambert (2013) Catalytic activity and thermostability of enzymes immobilized on silanized surface: Influence of the crosslinking agent. Enzyme Microb. Technol. 52: 336–343.CrossRefPubMedGoogle Scholar
  3. 3.
    Baslé, E., N. Joubert, and M. Pucheault (2010) Protein chemical modification on endogenous amino acids. Chem Biol. 17: 213–227.CrossRefPubMedGoogle Scholar
  4. 4.
    Drahl, C., B. F. Cravatt, and E. J. Sorensen (2005) Protein-reactive natural products. Angew. Chem. Int. Ed. Engl. 44: 5788–5809.CrossRefPubMedGoogle Scholar
  5. 5.
    Kaiser, E. T. and D. S. Lawrence (1984) Chemical mutation of enzyme active sites. Science. 226: 505–511.CrossRefPubMedGoogle Scholar
  6. 6.
    Ravikumar, Y., S. P. Nadarajan, T. H. Yoo, C. S. Lee, and H. Yun (2015) Unnatural amino acid mutagenesis-based enzyme engineering. Trends Biotechnol. 33: 462–470.CrossRefPubMedGoogle Scholar
  7. 7.
    Zheng, S. and I. Kwon (2012) Manipulation of enzyme properties by noncanonical amino acid incorporation. Biotechnol. J. 7: 47–60.Google Scholar
  8. 8.
    Link, A. J., M. K. S. Vink, N. J. Agard, J. A. Prescher, C. R. Bertozzi, and D. A. Tirrell (2006) Discovery of aminoacyl-tRNA synthetase activity through cell-surface display of noncanonical amino acids. Proc. Natl. Acad. Sci. USA. 103: 10180–10185.CrossRefPubMedGoogle Scholar
  9. 9.
    Link, A. J. and D. A. Tirrell (2005) Reassignment of sense codons in vivo. Methods. 36: 291–298.CrossRefPubMedGoogle Scholar
  10. 10.
    Minks, C., S. Alefelder, L. Moroder, R. Huber, and N. Budisa (2000) Towards new protein engineering: in vivo building and folding of protein shuttles for drug delivery and targeting by the selective pressure incorporation (SPI) method. Tetrahedron. 56: 9431–9442.CrossRefGoogle Scholar
  11. 11.
    Rajesh Mehta, K., C. Y. Yang, and J. K. Montclare (2011) Modulating substrate specificity of histone acetyltransferase with unnatural amino acids. Mol. BioSyst. 7: 3050–3055.CrossRefGoogle Scholar
  12. 12.
    Merkel, L., M. Schauer, G. Antranikian, and N. Budisa (2010) Parallel incorporation of different fluorinated amino acids: on the way to ‘teflon’ proteins. Chembiochem. 11: 1505–1507.Google Scholar
  13. 13.
    Soumillion, P. and J. Fastrez (1998) Incorporation of 1,2,4-triazole-3-alanine into a mutant of phage lambda lysozyme containing a single histidine. Protein Eng. Des. Sel. 11: 213–217.Google Scholar
  14. 14.
    Schlesinger, S. (1968) The effect of amino acid analogues on alkaline phosphatase formation in Escherichia coli K-12 II. Replacement of tryptophan by azatryptophan and by tryptazan. J. Biol. Chem. 243: 3877–3883.PubMedGoogle Scholar
  15. 15.
    Wang, L., J. Xie, and P. G. Schultz (2006) Expanding the genetic code. Ann. Rev. Biophys. Biomol. Struct. 35: 225–249.CrossRefGoogle Scholar
  16. 16.
    Noren, C. J., S. J. Anthony-Cahill, M. C. Griffith, and P. G. Schultz (1989) A general method for site-specific incorporation of unnatural amino acids into proteins. Science. 244: 182–188.CrossRefPubMedGoogle Scholar
  17. 17.
    Bain, J. D., E. S. Diala, C. G. Glabe, D. A. Wacker, M. H. Lyttle, T. A. Dix, and A. R. Chamberlin (1991) Site-specific incorporation of non-natural residues during in vitro protein biosynthesis with semi-synthetic aminoacyl-tRNAs. Biochemistry. 30: 5411–5421.CrossRefPubMedGoogle Scholar
  18. 18.
    Furter, R. (1998) Expansion of the genetic code: site-directed p-fluoro-phenylalanine incorporation in Escherichia coli. Protein Sci. 7: 419–426.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Wang, L., A. Brock, B. Herberich, and P. G. Schultz (2001) Expanding the genetic code of Escherichia coli. Science. 292: 498–500.CrossRefPubMedGoogle Scholar
  20. 20.
    Cadwell, R. C. and G. F. Joyce (1992) Randomization of genes by PCR mutagenesis. Genome Res. 2: 28–33.CrossRefGoogle Scholar
  21. 21.
    Abou-Nader, M. and M. J. Benedik (2010) Rapid generation of random mutant libraries. Bioeng Bugs. 1: 337–340.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Vogel, H. J., D. J. Schibli, W. Jing, E. M. Lohmeier-Vogel, R. F. Epand, and R. M. Epand (2002) Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell Biol. 80: 49–63.CrossRefPubMedGoogle Scholar
  23. 23.
    Liu, C. C. and P. G. Schultz (2010) Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79: 413–444.CrossRefPubMedGoogle Scholar
  24. 24.
    Kirshenbaum, K., I. S. Carrico, and D. A. Tirrell (2002) Biosynthesis of proteins incorporating a versatile set of phenylalanine analogues. Chembiochem. 3: 235–237.CrossRefPubMedGoogle Scholar
  25. 25.
    Tang, Y. and D. A. Tirrell (2002) Attenuation of the editing activity of the Escherichia coli leucyl-tRNA synthetase allows incorporation of novel amino acids into proteins in vivo. Biochemistry. 41: 10635–10645.CrossRefPubMedGoogle Scholar
  26. 26.
    Wang, P., Y. Tang, and D. A. Tirrell (2003) Incorporation of trifluoroisoleucine into proteins in vivo. J. Am. Chem. Soc. 125: 6900–6906.CrossRefPubMedGoogle Scholar
  27. 27.
    Zhao, S., J. Dai, M. Z. Hu, C. Liu, R. S. Meng, X. Liu, C. Wang, and T. Luo (2016) Photo-induced coupling reactions of tetrazoles with carboxylic acids in aqueous solution: application in protein labelling. Chem. Commun. 52: 4702–4705.CrossRefGoogle Scholar
  28. 28.
    Tanaka, Y., M. R. Bond, and J. J. Kohler (2008) Photocrosslinkers illuminate interactions in living cells. Mol. BioSyst. 4: 473–480.CrossRefPubMedGoogle Scholar
  29. 29.
    Sato, S., S. Mimasu, A. Sato, N. Hino, K. Sakamoto, T. Umehara, and S. Yokoyama (2011) Crystallographic study of a site-specifically cross-linked protein complex with a genetically incorporated photoreactive amino acid. Biochemistry. 50: 250–257.CrossRefPubMedGoogle Scholar
  30. 30.
    Liu, T., Y. Wang, X. Luo, J. Li, S. A. Reed, H. Xiao, T. S. Young, and P. G. Schultz (2016) Enhancing protein stability with extended disulfide bonds. Proc. Natl. Acad. Sci. USA. 113: 5910–5915.CrossRefPubMedGoogle Scholar
  31. 31.
    Kadokura, H., F. Katzen, and J. Beckwith (2003) Protein disulfide bond formation in prokaryotes. Ann. Rev. Biochem. 72: 111–135.CrossRefPubMedGoogle Scholar
  32. 32.
    Cappadocia, L. and C. D. Lima (2018) Ubiquitin-like protein conjugation: structures, chemistry, and mechanism. Chem. Rev. 118: 889–918.CrossRefPubMedGoogle Scholar
  33. 33.
    Sevier, C. S. and C. A. Kaiser (2002) Formation and transfer of disulphide bonds in living cells. Nature Rev. Mol. Cell Biol. 3: 836–847.CrossRefGoogle Scholar
  34. 34.
    Mayer, C., D. G. Gillingham, T. R. Ward, and D. Hilvert (2011) An artificial metalloenzyme for olefin metathesis. Chem. Commun. 47: 12068–12070.CrossRefGoogle Scholar
  35. 35.
    Kuang, H. and M. D. Distefano (1998) Catalytic enantioselective reductive amination in a host—guest system based on a protein cavity. J. Am. Chem. Soc. 120: 1072–1073.CrossRefGoogle Scholar
  36. 36.
    Dombkowski, A. A., K. Z. Sultana, and D. B. Craig (2014) Protein disulfide engineering. FEBS Lett. 588: 206–212.CrossRefPubMedGoogle Scholar
  37. 37.
    Wart, H. E. V., A. Lewis, H. A. Scheraga, and F. D. Saeva (1973) Disulfide bond dihedral angles from raman spectroscopy. Proc. Natl. Acad. Sci. USA. 70: 2619–2623.CrossRefPubMedGoogle Scholar
  38. 38.
    Chin, J. W., S. W. Santoro, A. B. Martin, D. S. King, L. Wang, and P. G. Schultz (2002) Addition of p-azido-L-phenylalanine to the genetic code of Escherichia coli. J. Am. Chem. Soc. 124: 9026–9027.CrossRefPubMedGoogle Scholar
  39. 39.
    Tippmann, E. M., W. Liu, D. Summerer, A. V. Mack, and P. G. Schultz (2007) A genetically encoded diazirine photocrosslinker in Escherichia coli. Chembiochem. 8: 2210–2214.CrossRefPubMedGoogle Scholar
  40. 40.
    Ai, H. W., W. Shen, A. Sagi, P. R. Chen, and P. G. Schultz (2011) Probing Protein—protein interactions with a genetically encoded photo-crosslinking amino acid. Chembiochem. 12: 1854–1857.CrossRefPubMedGoogle Scholar
  41. 41.
    Chou, C., R. Uprety, L. Davis, J. W. Chin, and A. Deiters (2011) Genetically encoding an aliphatic diazirine for protein photocrosslinking. Chem. Sci. 2: 480–483.CrossRefGoogle Scholar
  42. 42.
    Zhang, M., S. Lin, X. Song, J. Liu, Y. Q. Fu, X. Ge, X. Fu, Z. Chang, and P. R. Chen (2011) A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat. Chem. Biol. 7: 671–677.CrossRefPubMedGoogle Scholar
  43. 43.
    Lin, S., Z. J. Zhang, H. Xu, L. Li, S. Chen, J. Li, Z. Hao, and P. R. Chen (2011) Site-specific incorporation of photo-cross-linker and bio-orthogonal amino acids into enteric bacterial pathogens. J. Am. Chem. Soc. 133: 20581–20587.CrossRefPubMedGoogle Scholar
  44. 44.
    Chin, J. W., A. B. Martin, D. S. King, L. Wang, and P. G. Schultz (2002) Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. USA. 99: 11020–11024.CrossRefPubMedGoogle Scholar
  45. 45.
    Hino, N., M. Oyama, A. Sato, T. Mukai, F. Iraha, A. Hayashi, H. Kozuka-Hata, T. Yamamoto, S. Yokoyama and K. Sakamoto (2011) Genetic incorporation of a photocrosslinkable amino acid reveals novel protein complexes with GRB2 in mammalian cells. J. Mol. Biol. 406: 343–353.CrossRefPubMedGoogle Scholar
  46. 46.
    Coin, I., V. Katritch, T. Sun, Z. Xiang, F. Y. Siu, M. Beyermann, R. C. Stevens, and L. Wang (2013) Genetically encoded chemical probes in cells reveal the binding path of urocortin-I to CRF class B GPCR. Cell. 155: 1258–1269.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Ray-Saha, S., T. Huber, and T. P. Sakmar (2014) Antibody epitopes on g protein-coupled receptors mapped with genetically encoded photoactivatable cross-linkers. Biochemistry. 53: 1302–1310.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Dugan, A., C. Y. Majmudar, R. Pricer, S. Niessen, J. K. Lancia, H. Y. Fung, B. F. Cravatt, and A. K. Mapp (2016) Discovery of enzymatic targets of transcriptional activators via in vivo covalent chemical capture. J. Am. Chem. Soc. 138: 12629–12635.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Wilkins, B. J., N. A. Rall, Y. Ostwal, T. Kruitwagen, K. Hiragami-Hamada, M. Winkler, Y. Barral, W. Fischle, and H. Neumann (2014) A cascade of histone modifications induces chromatin condensation in mitosis. Science. 343: 77–80.CrossRefPubMedGoogle Scholar
  50. 50.
    Li, J. C., T. Liu, Y. Wang, A. P. Mehta, and P. G. Schultz (2018) Enhancing protein stability with genetically encoded noncanonical amino acids. J. Am. Chem. Soc. 140: 15997–16000.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Banerjee, D., A. P. Liu, N. R. Voss, S. L. Schmid, and M. G. Finn (2010) Multivalent display and receptor-mediated endocytosis of transferrin on virus-like particles. ChemBioChem. 11: 1273–1279.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Rostovtsev, V. V., L. G. Green, V. V. Fokin, and K. B. Sharpless (2002) A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective ‘ligation’ of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41: 2596–2599.CrossRefPubMedGoogle Scholar
  53. 53.
    Steinmetz, N. F., V. Hong, E. D. Spoerke, P. Lu, K. Breitenkamp, M. G. Finn, and M. Manchester (2009) Buckyballs meet viral nanoparticles: candidates for biomedicine. J. Am. Chem. Soc. 131: 17093–17095.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Xuan, W., D. Collins, M. Koh, S. Shao, A. Yao, H. Xiao, P. Garner, and P. G. Schultz (2018) Site-specific incorporation of a thioester containing amino acid into proteins. ACS Chem. Biol. 13: 578–581.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Xiang, Z., V. K. Lacey, H. Ren, J. Xu, D. J. Burban, P. A. Jennings, and L. Wang (2014) Proximity-enabled protein crosslinking through genetically encoding haloalkane unnatural amino acids. Angew. Chem. Int. Ed. Engl. 53: 2190–2193.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Chen, X. H., Z. Xiang, Y. S. Hu, V. K. Lacey, H. Cang, and L. Wang (2014) Genetically encoding an electrophilic amino acid for protein stapling and covalent binding to native receptors. ACS Chem. Biol. 9: 1956–1961.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Xuan, W., S. Shao, and P. G. Schultz (2017) Protein crosslinking by genetically encoded nncanonical amino acids with reactive aryl carbamate side chains. Angew. Chem. Int. Ed. Engl. 56: 5096–5100.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Wang, N., B. Yang, C. Fu, H. Zhu, F. Zheng, T. Kobayashi, J. Liu, S. Li, C. Ma, P. G. Wang, Q. Wang, and L. Wang (2018) Genetically encoding fluorosulfate-l-tyrosine to react with lysine, histidine, and tyrosine via SuFEx in proteins in vivo. J. Am. Chem. Soc. 140: 4995–4999.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Xuan, W., J. Li, X. Luo, and P. G. Schultz (2016) Genetic incorporation of a reactive isothiocyanate group into proteins. Angew. Chem. Int. Ed. Engl. 55: 10065–10068.CrossRefPubMedGoogle Scholar
  60. 60.
    Kim, S., W. Ko, B. H. Sung, S. C. Kim, and H. S. Lee (2016) Direct protein—protein conjugation by genetically introducing bioorthogonal functional groups into proteins. Bioorg. Med. Chem. 24: 5816–5822.CrossRefPubMedGoogle Scholar
  61. 61.
    Chen, X., J. L. Zaro, and W. C. Shen (2013) Fusion protein linkers: Property, design and functionality. Adv. Drug Deliv. Rev. 65: 1357–1369.CrossRefPubMedGoogle Scholar
  62. 62.
    Bai, Y. and W. C. Shen (2006) Improving the oral efficacy of recombinant granulocyte colony-stimulating factor and transferrin fusion protein by spacer optimization. Pharm. Res. 23: 2116–2121.CrossRefPubMedGoogle Scholar
  63. 63.
    McCormick, A. L., M. S. Thomas, and A. W. Heath (2001) Immunization with an interferon-gamma-gp120 fusion protein induces enhanced immune responses to human immunodeficiency virus gp120. J. Infect. Dis. 184: 1423–1430CrossRefPubMedGoogle Scholar
  64. 64.
    Bergeron, L. M., L. Gomez, T. A. Whitehead, and D. S. Clark (2009) Self-renaturing enzymes: design of an enzyme-chaperone chimera as a new approach to enzyme stabilization. Biotechnol. Bioeng. 102: 1316–1322.CrossRefPubMedGoogle Scholar
  65. 65.
    Bartlett, G. J., C. T. Porter, N. Borkakoti, and J. M. Thornton (2002) Analysis of catalytic residues in enzyme active sites. J. Mol. Biol. 324: 105–121.CrossRefPubMedGoogle Scholar
  66. 66.
    McCall, K. A., C. Huang, and C. A. Fierke (2000) Function and mechanism of zinc metalloenzymes. J. Nutr. 130: 1437S–1446S.CrossRefPubMedGoogle Scholar
  67. 67.
    Vallee, B. L. and D. S. Auld (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry. 29: 5647–5659.CrossRefPubMedGoogle Scholar
  68. 68.
    Oikawa, A. (1959) The role of calcium in Taka-amylase A: II. The exchange reaction of calcium. J. Biochem. 46: 463–473.CrossRefGoogle Scholar
  69. 69.
    Toda, H., I. Kato, and K. Narita (1968) Correlation of the masked sulfhydryl group with the essential calcium in Takaamylase A. J. Biochem. 63: 295–301.PubMedGoogle Scholar
  70. 70.
    Lu, Y., N. Yeung, N. Sieracki, and N. M. Marshall (2009) Design of functional metalloproteins. Nature. 460: 855–862.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Waldron, K. J., J. C. Rutherford, D. Ford, and N. J. Robinson (2009) Metalloproteins and metal sensing. Nature. 460: 823–830CrossRefPubMedGoogle Scholar
  72. 72.
    Rosati, F. and G. Roelfes (2010) Artificial metalloenzymes. ChemCatChem. 2: 916–927.CrossRefGoogle Scholar
  73. 73.
    Reetz, M. T., M. Rentzsch, A. Pletsch, A. Taglieber, F. Hollmann, R. J. Mondière, N. Dickmann, B. Höcker, S. Cerrone, M. C. Haeger, and R. Sterner (2008) A robust protein host for anchoring chelating ligands and organocatalysts. ChemBioChem. 9: 552–564.CrossRefPubMedGoogle Scholar
  74. 74.
    Matsuo, T. and S. Hirota (2014) Artificial enzymes with protein scaffolds: structural design and modification. Bioorg. Med. Chem. 22: 5638–5656.CrossRefPubMedGoogle Scholar
  75. 75.
    Drienovska, I., A. Rioz-Martínez, A. Draksharapu, and G. Roelfes (2015) Novel artificial metalloenzymes by in vivo incorporation of metal-binding unnatural amino acids. Chem. Sci. 6: 770–776.CrossRefPubMedGoogle Scholar
  76. 76.
    Lee, H. S. and P. G. Schultz (2008) Biosynthesis of a site-specific DNA cleaving protein. J. Am. Chem. Soc. 130: 13194–13195.CrossRefPubMedGoogle Scholar
  77. 77.
    Yang, H., P. Srivastava, C. Zhang, and J. C. Lewis (2014) A general method for artificial metalloenzyme formation through strain-promoted azide.alkyne cycloaddition. ChemBioChem. 15: 223–227.CrossRefPubMedGoogle Scholar
  78. 78.
    Glazer, A. N. (1970) Specific chemical modification of proteins. Annu. Rev. Biochem. 39: 101–130.CrossRefPubMedGoogle Scholar
  79. 79.
    Wong, L. S., F. Khan, and J. Micklefield (2009) Selective covalent protein immobilization: strategies and applications. Chem. Rev. 109: 4025–4053.CrossRefPubMedGoogle Scholar
  80. 80.
    Umeda, A., G. N. Thibodeaux, J. Zhu, Y. A. Lee, and Z. J. Zhang (2009) Site-specific protein cross-linking with genetically incorporated 3,4-dihydroxy-L-phenylalanine. ChemBioChem. 10: 1302–1304.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Yang, B., N. Ayyadurai, H. Yun, Y. S. Choi, B. H. Hwang, J. Huang, Q. Lu, H. Zeng, and H. J. Cha (2014) In vivo residuespecific dopa-incorporated engineered mussel bioglue with enhanced adhesion and water resistance. Angew. Chem. Int. Ed. Engl. 53: 13360–13364.CrossRefPubMedGoogle Scholar
  82. 82.
    Ayyadurai, N., N. S. Prabhu, K. Deepankumar, Y. J. Jang, N. Chitrapriya, E. Song, N. Lee, S. K. Kim, B. G. Kim, N. Soundrarajan, S. Lee, H. J. Cha, N. Budisa, and H. Yun (2011) Bioconjugation of L-3,4-dihydroxyphenylalanine containing protein with a polysaccharide. Bioconjug Chem. 22: 551–555.CrossRefPubMedGoogle Scholar
  83. 83.
    Deepankumar, K., S. P. Nadarajan, S. Mathew, S. G. Lee, T. H. Yoo, E. Y. Hong, B. G. Kim, and H. Yun (2015) Engineering transaminase for stability enhancement and site-specific immobilization through multiple noncanonical amino acids incorporation. ChemCatChem. 7: 417–421.CrossRefGoogle Scholar
  84. 84.
    Lim, S. I., Y. Mizuta, A. Takasu, Y. H. Kim, and I. Kwon (2014) Site-specific bioconjugation of a murine dihydrofolate reductase enzyme by copper(I)-catalyzed azide-alkyne cycloaddition with retained activity. PLoS One 9: e9840CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Bornscheuer, U. T. and M. Pohl (2001) Improved biocatalysts by directed evolution and rational protein design. Curr. Opin. Chem. Biol. 5: 137–143.CrossRefPubMedGoogle Scholar
  86. 86.
    Steinrauf, L. K., J. A. Hamilton, B. C. Braden, J. R. Murrell, and M. D. Benson (1993) X-ray crystal structure of the Ala-109→Thr variant of human transthyretin which produces euthyroid hyperthyroxinemia. J. Biol. Chem. 268: 2425–2430.PubMedGoogle Scholar
  87. 87.
    Howard, E. I., R. Sanishvili, R. E. Cachau, A. Mitschler, B. Chevrier, P. Barth, V. Lamour, M. Van Zandt, E. Sibley, C. Bon, D. Moras, T. R. Schneider, A. Joachimiak, and A. Podjarny (2004) Ultrahigh resolution drug design I: details of interactions in human aldose reductase.inhibitor complex at 0.66 A. Proteins. 55: 792–804.CrossRefPubMedGoogle Scholar
  88. 88.
    Yabe-Nishimura, C. (1998) Aldose reductase in glucose toxicity: a potential target for the prevention of diabetic complications. Pharmacol. Rev. 50: 21–33.PubMedGoogle Scholar
  89. 89.
    Holliday, G. L., J. B. O. Mitchell, and J. M. Thornton (2009) Understanding the functional roles of amino acid residues in enzyme catalysis. J. Mol. Biol. 390: 560–577.CrossRefPubMedGoogle Scholar
  90. 90.
    O’Hagan, D. (2008) Understanding organofluorine chemistry. An introduction to the C–F bond. Chem. Soc. Rev. 37: 308–319.CrossRefPubMedGoogle Scholar
  91. 91.
    Purser, S., P. R. Moore, S. Swallow, and V. Gouverneur (2008) Fluorine in medicinal chemistry. Chem. Soc. Rev. 37: 320–330.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Bondi, A. (1964) van der Waals volumes and radii. J. Phys. Chem. 68: 441–451.CrossRefGoogle Scholar
  93. 93.
    Budisa, N., W. Wenger, and B. Wiltschi (2010) Residue-specific global fluorination of Candida antarctica lipase B in Pichia pastoris. Mol. Biosyst. 6: 1630–1639.CrossRefPubMedGoogle Scholar
  94. 94.
    Mathew, S., S. P. Nadarajan, T. Chung, H. H. Park, and H. Yun (2016) Biochemical characterization of thermostable ω-transaminase from Sphaerobacter thermophilus and its application for producing aromatic β- and γ-amino acids. Enzyme Microb. Technol. 87-88: 52–60.CrossRefPubMedGoogle Scholar
  95. 95.
    Mathew, S., K. Deepankumar, G. Shin, E. Y. Hong, B. G. Kim, T. Chung, H. Yun (2016) Identification of novel thermostable ω-transaminase and its application for enzymatic synthesis of chiral amines at high temperature. RSC Adv. 6: 69257–69260.CrossRefGoogle Scholar
  96. 96.
    Deepankumar, K., M. Shon, S. P. Nadarajan, G. Shin, S. Mathew, N. Ayyadurai, B. G. Kim, S. H. Choi, S. H. Lee, H. Yun (2014) Enhancing thermostability and organic solvent tolerance of ω-transaminase through global incorporation of fluorotyrosine. Adv. Synth. Catal. 356: 993–998.CrossRefGoogle Scholar
  97. 97.
    Ohtake, K., A. Yamaguchi, T. Mukai, H. Kashimura, N. Hirano, M. Haruki, S. Kohashi, K. Yamagishi, K. Murayama, Y. Tomabechi, T. Itagaki, R. Akasaka, M. Kawazoe, C. Takemoto, M. Shirouzu, S. Yokoyama, and K. Sakamoto (2015) Protein stabilization utilizing a redefined codon. Sci. Rep. 5: 9762.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Hoesl, M. G., C. G. Acevedo-Rocha, S. Nehring, M. Royter, C. Wolschner, B. Wiltschi, and N. Budisa (2011) Lipase congeners designed by genetic code engineering. ChemCatChem. 3: 213–221.CrossRefGoogle Scholar
  99. 99.
    Ugwumba, I. N., K. Ozawa, Z. Q. Xu, F. Ely, J. L. Foo, A. J. Herlt, C. Coppin, S. Brown, M. C. Taylor, D. L. Ollis, L. N. Mander, G. Schenk, N. E. Dixon, G. Otting, J. G. Oakeshott, and C. J. Jackson (2011) Improving a natural enzyme activity through incorporation of unnatural amino acids. J. Am. Chem. Soc. 133: 326–333.CrossRefPubMedGoogle Scholar
  100. 100.
    Windle, C. L., K. J. Simmons, J. R. Ault, C. H. Trinh, A. Nelson, A. R. Pearson, and A. Berry (2017) Extending enzyme molecular recognition with an expanded amino acid alphabet. Proc. Natl. Acad. Sci. USA. 114: 2610–2615.CrossRefPubMedGoogle Scholar
  101. 101.
    Kim, S., B. H. Sung, S. C. Kim, and H. S. Lee (2018) Genetic incorporation of l-dihydroxyphenylalanine (DOPA) biosynthesized by a tyrosine phenol-lyase. Chem. Commun. 54: 3002–3005.CrossRefGoogle Scholar
  102. 102.
    Chen, Y., A. Loredo, A. Gordon, J. Tang, C. Yu, J. Ordonez, and H. Xiao (2018) A noncanonical amino acid-based relay system for site-specific protein labeling. Chem. Commun. 54: 7187–7190.CrossRefGoogle Scholar
  103. 103.
    Ma, Y., H. Biava, R. Contestabile, N. Budisa, and M. L. Di Salvo (2014) Coupling bioorthogonal chemistries with artificial metabolism: intracellular biosynthesis of azidohomoalanine and its incorporation into recombinant proteins. Molecules. 19: 1004–1022.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Korean Society for Biotechnology and Bioengineering and Springer 2019

Authors and Affiliations

  • Yumi Won
    • 1
  • Amol D. Pagar
    • 1
  • Mahesh D. Patil
    • 1
  • Philip E. Dawson
    • 2
  • Hyungdon Yun
    • 1
    Email author
  1. 1.Department of Systems BiotechnologyKonkuk UniversitySeoulKorea
  2. 2.Department of ChemistryThe Scripps Research InstituteLa JollaUSA

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