Protein engineering 20 years on

Nature Reviews Molecular Cell Biology

Volumn 3, Issue 12, 2002, Pages 964-970

  Brannigan, James A ^a   Wilkinson, Anthony J ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; LYSOZYME; TYROSINE TRANSFER RNA LIGASE;

CATALYSIS; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; HISTORY OF MEDICINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN STABILITY; REVIEW; SITE DIRECTED MUTAGENESIS;

ANTIBODIES; BINDING SITES; HEMOGLOBINS; HUMANS; INSULIN; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN ENGINEERING; TYROSINE-TRNA LIGASE;

EID: 0036906253     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm975     Document Type: Review

References (88)

1. Knowles, J. R. & Albery, W. J. Perfection in enzyme catalysis: The energetics of triose phosphate isomerase. Acc. Chem. Res. 10, 105-111 (1977).
2. Fersht, A. R. Enzyme Structure and Mechanism (W. H. Freeman & Co., San Francisco, 1977).
3. Campbell, I. D. The march of structural biology. Nature Rev. Mol. Cell Biol. 3, 377-381 (2002).
4. Winter, G., Fersht, A. R., Wilkinson, A. J., Zoller, M. & Smith, M. Redesigning enzyme structure by site-directed mutagenesis: Tyrosyl tRNA synthetase and ATP binding. Nature 299, 756-758 (1982).
5. Dalbadie-MacFarland, G. et al. Oligonucleotide-directed mutagenesis as a powerful method for studies of protein function. Proc. Natl. Acad. Sci. USA 79, 6409-6413 (1982).
6. Sigal, I. S., Harwood, B. G. & Arentzen, R. Thiol β-lactamase: Replacement of the active site serine of RTEM β-lactamase by a cysteine residue. Proc. Natl. Acad. Sci. USA 79, 7157-7160 (1982).
7. Jones, P. T., Dear, P. H., Foote, J., Neuberger, M. S. & Winter, G Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321, 522-525 (1986).
8. Neuberger, M. S., Williams, G. T. & Fox, R. O. Recombinant antibodies possessing novel effector functions. Nature 312, 604-608 (1984).
9. Wilkinson, A. J., Fersht, A. R, Blow, D. M. & Winter, G. Site-directed mutagenesis as a probe of enzyme structure and catalysis: Tyrosyl-tRNA synthetase cysteine-35 to glyclne-35 mutation. Biochemistry 22, 3581-3586 (1983).
10. Leatherbarrow, R. J., Fersht, A. R. & Winter, G. Transition-state stabilisation in the mechanism of tyrosyl-tRNA synthetase revealed by protein engineering. Proc. Natl. Acad. Sci. USA 82, 7840-7844 (1985).
11. Wilkinson, A. J., Fersht, A. R., Blow, D. M., Carter, P. & Winter, G. A large increase in enzyme-substrate affinity by protein engineering. Nature 307, 187-188 (1984).
12. Fersht, A. R. et al. Hydrogen bonding and biological specificity analysed by protein engineering. Nature 314, 235-238 (1985).
13. Smith, M. In vitro mutagenesis. Annu. Rev. Genet. 19, 423-462 (1985).
14. Carter, P. & Wells, J. A. Dissecting the catalytic triad of a serine protease. Nature 332, 564-568 (1988).
15. Wells, J. A., Cunningham, B. C., Graycar, T. P. & Estell, D. A. Importance of hydrogen-bond formation in stabilizing the transition state of subtilisin. Phil. Trans. R. Soc. Lond. A 317, 415-423 (1986).
16. Bryan, P., Pantoliano, M. W., Quill, S. G., Hsiao, H.-Y. & Poulos, T. Site-directed mutagenesis and the role of the oxyanion hole in subtilisin. Proc. Natl. Acad. Sci. USA 83, 3743-3745 (1986).
17. Springer, B. A. et al. Discrimination between oxygen and carbon monoxide and inhibition of autooxidation by myoglobin. J. Biol. Chem. 264, 3057-3060 (1989).
18. Gardell, S. J., Craik, C. S., Hilvert, D., Urdea, M. S. & Rutter, W. J. Site-directed mutagenesis shows that tyrosine 248 of carboxypeptidase A does not play a crucial role in catalysis. Nature 317, 551-555 (1985).
19. Blake, C. C. F. et al. Structure of hen egg white lysozyme. A three-dimensional fourier synthesis at 2Å resolution. Nature 206, 757-763 (1965).
20. Vocadlo, D. J., Davies, G. J., Laine, R. & Withers, S. G. Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature 412, 835-838 (2001).
21. Kantrowitz, E. R. & Lipscomb, W. N. Escherichia coli aspartate transcarbamylase: The relation between structure and function. Science 241, 669-674 (1988).
22. Matouschek, A., Kellis J. T. Jr, Serrano, L. & Fersht, A. R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 340, 122-126, (1989).
23. Fersht, A. R. & Daggett, V. Protein folding and unfolding at atomic resolution. Cell 108, 573-582 (2002).
24. Matthews, B. W. Genetic and structural analysis of the protein stability problem. Biochemistry 26, 6855-6888 (1987).
25. Shortle, D. Probing the determinants of protein folding and stability with amino acid substitutions. J. Biol. Chem. 264, 5315-5318 (1989).
26. Arnold, F. H. Engineering enzymes for non-aqueous solvents. Trends Biotechnol. 8, 244-249 (1990).
27. Perry, L. J. & Wetzel, R. Disulfide bond engineering into T4 lysozyme: Stabilization of the protein toward thermal inactivation. Science 226, 555-557 (1984).
28. Van den Burg, B., Vriend, G., Veltman, O. R., Venema, G. & Eijsink, V. G. H. Engineering an enzyme to resist boiling. Proc. Natl. Acad. Sci. USA 95, 2056-2060 (1998).
29. Russell, A. J. & Fersht, A. R. Rational modification of enzyme catalysis by engineering surface charge. Nature 326, 496-500 (1987).
30. Fersht, A. R., Leatherbarrow, R. J. & Wells, T. N. C. Structure-activity relationships in engineered proteins: Analysis of use of binding energy by linear free energy relationships. Biochemistry 26, 6030-6038 (1987).
31. Wells, J. A. Activity of mutational effects in proteins. Biochemistry 29, 8509-8517 (1990).
32. Wilks, H. M. et al. A specific, highly active malate dehydrogenase by redesign of a lactate dehydrogenase framework. Science 242, 1541-1544 (1988).
33. Wilks, H. M. et al. Designs for a broad substrate specificity keto acid dehydrogenase. Biochemistry 29, 8587-8591 (1990).
34. Wilks, H. M. et al. Design of a specific phenyllactate dehydrogenase by peptide loop exchange on the Bacillus stearothermophilus lactate dehydrogenase framework. Biochemistry 31, 7802-7806 (1992).
35. Graf, L. et al. Selective alteration of substrate specificity by replacement of aspartic acid-189 with lysine in the binding pocket of trypsin. Biochemistry 26, 2616-2623 (1987).
36. Perona, J. J. et al. Structural origins of substrate discrimination in trypsin and chymotrypsin. Biochemistry 34, 1489-1499 (1995).
37. Venekei, I., Szilagy L, Graf, L. & Rutter, W. J. Attempts to convert chymotrypsin to trypsin. FEBS Lett. 379, 143-147 (1996).
38. Bedouelle, H. & Winter, G. A model of synthetase/transfer RNA interaction as deduced by protein engineering. Nature 320, 371-373 (1986).
39. Cunningham, B. C. & Wells, J. A. High-resolution epitope mapping of HGH-receptor interactions by alanine-scanning mutagenesis. Science 244, 1081-1085 (1989).
40. Wells, J. A. & Estell, D. A. Subtilisin - An enzyme designed to be engineered. Trends Biochem. Sci. 13, 291-297 (1988).
41. Duncan, A. R. & Winter, G. The binding site for C1q on IgG. Nature 332, 738-740 (1988).
42. Oliphant, A. R. & Struhl, K. An efficient method for generating proteins with altered enzymatic properties: Application to β-lactamase. Proc. Natl. Acad. Sci, USA 86, 9094-9098 (1989).
43. Loeb, D. D. et al. Complete mutagenesis of the HIV-1 protease. Nature 340, 397-400 (1989).
44. Merino, E., Osuna, J., Bolivar, F. & Soberon, X. A general, PCR-based method for single or combinatorial oligonucleotide-directed mutagenesis on pUC/M13 vectors. Biotechniques 12, 508-510 (1992).
45. Dawkins, R. The Blind Watchmaker: Why the Evidence of Evolution Reveals A Universe Without Design (Longman, London, 1986).
46. Chen, K. & Arnold, F. H. Tuning the activity of an enzyme for unusual environments: Sequential random mutagenesis of subtilisin E for catalysis in dimethytformamide. Proc. Natl. Acad. Sci. USA 90, 5618-5622 (1993).
47. Winter, G. & Milstein, C. Man-made antibodies. Nature 349, 293-299 (1991).
48. Stemmer, W. P. Rapid evolution of a protein in vitro by A shuffling. Nature 370, 389-391 (1994).
49. Crameri, A., Raillard, S. A., Bermudez, E & Stemmer W. P. DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 391, 288-291 (1998).
50. Arnold, F. H. Design by directed evolution, Acc. Chem. Res. 31, 125-131 (1998).
51. Stemmer, W. P. C. DNA shuffling by random fragmentation and reassembly: In vitro recombination for molecular evolution. Proc. Natl. Acad. Sci. USA 91, 10747-10751 (1994).
52. Miyazaki, K. & Arnold, F. H. Exploring nonnatural evolutionary pathways by saturation mutagenesis: Rapid improvement of protein function. J. Mol. Evol. 49, 716-720 (1999).
53. Gaytan, P., Osuna, J. & Soberon, X. Novel ceftazidime-resistance β-lactamases generated by a codon-based mutagenesis method and selection. Nucleic Acids Res. 30, e84 (2002),
54. Murakami, H., Hohsaka, T. & Sisido, M. Random insertion and deletion of arbitrary number of bases for codon-based random mutation of DNAs. Nature Biotechnol. 20, 76-81 (2002).
55. Xia, G., Chen, L., Sera, T., Fa, M., Schultz, P. G. & Romesberg, F. E. Directed evolution of novel polymerase activities: Mutation of a DNA polymerase into an efficient RNA polymerase. Proc. Natl. Acad. Sci. USA 99, 6597-6602 (2002).
56. Griffiths, A. D. & Tawfik, D. S. Man-made enzymes - From design to in vitro compartmentalisation. Curr. Opin. Biotechnol. 11, 338-353 (2000).
57. Ghadessy, F. J., Ong, J. L. & Holliger, P. Directed evolution of polymerase function by compartmentalised self-replication. Proc. Natl. Acad. Sci. USA 98, 4552-4557 (2001).
58. Facciotti, M. T., Bertain, P. B. & Yuan, L. Improved stearate phenotype in transgenic canola expressing a modified acyl-acyl carrier protein thioesterase. Nature Biotechnol. 17, 593-597 (1999).
59. Lehmann, M. et al. The consensus concept for thermostability engineering of proteins: Further proof of concept. Protein Eng. 15, 403-411 (2002).
60. Burton, S. G. The search for the ideal biocatalyst. Nature Biotechnol. 20, 37-45 (2002).
61. Kumamaru, T., Suenaga, H., Mitsuoka, M., Watanabe, T & Furukawa, K. Enhanced degradation of polychlorinated biphenyls by directed evolution of biphenyl oxygenase. Nature Biotechnol. 16, 663-666 (1998).
62. Bayley, H. & Cremer, P. S. Stochastic sensors inspired by biology. Nature 413, 226-230 (2001).
63. Holliger P & Bohlen, H. Engineering antibodies for the clinic. Cancer Metastasis Rev. 18, 411-419 (1999).
64. McCafferty, J. & Glover, D. R. Engineering therapeutic proteins. Curr. Opin. Struct. Biol. 10, 417-420 (2000).
65. Winslow, R. M. Blood substitutes: Refocusing an elusive goal. Br. J. Haematol. 111, 387-396 (2000).
66. Perutz, M. F. Stereochemistry of the cooperative effects in haemoglobin. Nature 228, 726-734 (1970).
67. Dickerson, R. E. & Geis, I. Haemoglobin: Structure, Function, Evolution and Pathology (Benjamin/Cummings Publishing Co., Inc., Menlo Park, California, 1983).
68. Looker, D. et al. A human recombinant haemoglobin designed for use as a blood substitute. Nature 356, 258-260 (1992).
69. Olson, J, S., Eich, R., Smith, L.P., Warren, J. J. & Knowles, B. C. Protein engineering strategies for designing more stable hemoglobin-based blood substitutes. Artif. Cells Blood Substit. Immobil. Biotechnol. 25, 227-241 (1997).
70. Doherty, D. H. et al. Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin. Nature Biotechnol. 16, 672-676 (1998).
71. Brange, J, & Vølund, A. Insulin analogs with improved pharmacokinetic profiles. Adv. Drug Deliv. Rev. 35, 307-335 (1999).
72. Vajo, Z. & Duckworth, W. C. Genetically engineered insulin analogues: Diabetes in the new millennium. Pharmacol. Rev. 52, 1-10 (2000).
73. Blundell, T., Dodson, G., Hodgkin, D. & Mercola, D. Insulin: The structure in the crystal and its reflection in chemistry and biology. Adv. Protein Chem. 26, 279-402 (1972).
74. Brange, J. et al. Monomeric insulins obtained by protein engineering and their medical implications. Nature 333, 679-682 (1988).
75. Knowles, J. R. Tinkering with enzymes: What are we learning? Science 236, 1252-1259 (1987).
76. Yano, T. & Kagamiyama, H. Directed evolution of ampicillin-resistant activity from a functionally unrelated DNA fragment: A laboratory model of molecular evolution. Proc. Natl. Acad. Sci. USA 98, 903-907 (2001).
77. Mendel, D., Cornish, V. W. & Schultz, P. G. Site-directed mutagenesis with an expanded code. Annu. Rev. Biophys. Biomol. Struct. 24, 435-462 (1995).
78. Wang, L., Brock, A., Herberich, B. & Schultz, P. G. Expanding the genetic code of Escherichia coli. Science 292, 498-504 (2001).
79. Kiga, D. et al. An engineered Escherichia coli tyrosyl-tRNA synthetase for site-specific incorporation of an unnatural amino acid into proteins in eukaryotic translation and its application in a wheat germ cell-free system. Proc. Natl. Acad. Sci. USA 99, 9715-9720 (2002).
80. Hutchison, C. A. et al. Mutagenesis at a specific position in a DNA sequence. J. Biol. Chem. 253, 6551-6560 (1978).
81. Chang, C. C. et al. Evolution of a cytokine using DNA family shuffling. Nature Biotechnol. 17, 793-797 (1999).
82. Sieber, V., Martinez, C. A. & Arnold, F. H. Libraries of hybrid proteins from distantly related sequences. Nature Biotechnol. 19, 456-460 (2001).
83. Lutz, S., Ostermeier, M. & Benkovic, S. J. Rapid generation of incremental truncation libraries for protein engineering using α-phosphothioate nucleotides. Nucleic Acids Res. 29, 16e (2001).
84. Lutz, S., Ostermeier, M., Moore, G. L., Maranas, C. D. & Benkovic, S. J. Creating multiple-crossover DNA libraries independent of sequence identity. Proc. Natl. Acad. Sci. USA 98, 11248-11253 (2001).
85. O'Maille, P. E., Bakhtina, M. & Tsai, M.-D. Structure-based combinatorial protein engineering (SCOPE). J. Mol. Biol. 321, 677-691 (2002).
86. Kilmartin, J. V. & Rossi-Bernardi, L. Interaction of haemaglobin with hydrogen ions, carbon dioxide and organic phosphates Physiol. Rev. 53, 836-890 (1973).
87. Whittingham, J. L., Havelund, S. & Jonassen, I. Crystal structure of a prolonged-acting insulin with albumin-binding properties. Biochemistry 36, 2826-2831 (1997).
88. McCafferty, J., Griffiths, A. D., Winter, G. & Chiswell, D. J. Phage antibodies: Filamentous phage displaying antibody variable domains. Nature 348, 552-554 (1990).