Rational engineering of enzyme stability

Journal of Biotechnology

Volumn 113, Issue 1-3, 2004, Pages 105-120

  Eijsink, Vincent G H ^a   Bjørk, Alexandra ^b   Gåseidnes, Sigrid ^a   Sirevåg, Reidun ^b   Synstad, Bjørnar ^a   Burg, Bertus Van Den ^c   Vriend, Gert ^d  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c PO Box 14 9750 AA Haren N ^*  (Netherlands)

^d RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Protein engineering; Protein stability; Thermal stability; Unfolding

Indexed keywords

HYPERSTABLE PROTEINS; THERMAL INACTIVATION;

AGGLOMERATION; BIOTECHNOLOGY; ENTROPY; MUTAGENESIS; SULFUR COMPOUNDS;

ENZYMES;

AMYLASE; CHITINASE; MALATE DEHYDROGENASE; PROTEINASE; THERMOLYSIN;

BACILLUS LICHENIFORMIS; CONFERENCE PAPER; ENZYME ENGINEERING; ENZYME STABILITY; KINETICS; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; SERRATIA MARCESCENS; THERMOSTABILITY;

BIOTECHNOLOGY; ENZYMES; PROTEIN ENGINEERING;

EID: 4544244867     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2004.03.026     Document Type: Conference Paper

References (145)

1. D.E. Anderson, J.H. Hurley, H. Nicholson, W.A. Baase, and B.W. Matthews Hydrophobic core repacking and aromatic-aromatic interaction in the thermostable mutant of T4 lysozyme Ser117 → Phe. Protein Sci. 2 1993 1285 1290
2. F.H. Arnold Enzyme engineering reaches the boiling point Proc. Natl. Acad. Sci. USA 95 1998 2035 2036
3. F.H. Arnold, P.L. Wintrode, K. Miyazaki, and A. Gershenson How enzymes adapt: lessons from directed evolution Trends Biochem. Sci. 26 2001 100 106
4. M.A. Arnott, R.A. Michael, C.R. Thompson, D.W. Hough, and M.J. Danson Thermostability and thermoactivity of citrate synthases from the thermophilic and hyperthermophilic archaea Thermoplasma acidophilum and Pyrococcus furiosus J. Mol. Biol. 304 2000 657 668
5. A. Bjørk, B. Dalhus, D. Mantzilas, V.G.H. Eijsink, and R. Sirevåg Stabilization of a tetrameric malate dehydrogenase by introduction of a disulfide bridge at the dimer-dimer interface J. Mol. Biol. 334 2003 811 821
6. A. Bjørk, D. Mantzilas, R. Sirevåg, and V.G.H. Eijsink Electrostatic interactions across the dimer-dimer interface contribute to the pH-dependent stability of a tetrameric malate dehydrogenase FEBS Lett. 553 2003 423 426
7. Bjørk, A., Dalhus, B., Mantzilas, D., Sirevåg, R., Eijsink, V.G.H., 2004. Large improvement in the thermal stability of a tetrameric malate dehydrogenase by single point mutations at the dimer-dimer interface. J. Mol. Biol., in press.
8. M. Blaber, X.J. Zhang, and B.W. Matthews Structural basis of amino acid alpha helix propensity Science 260 1993 1637 1640
9. O. Bogin, M. Peretz, Y. Hacham, Y. Korkhin, F. Frolow, A.J. Kalb, and Y. Burstein Enhanced thermal stability of Clostridium beijerinckii alcohol dehydrogenase after strategic substitution of amino acid residues with pralines from the homologous thermophilic Thermoanaerobacter brockii alcohol dehydrogenase Protein Sci. 7 1998 1156 1163
10. P.N. Bryan Protein engineering of subtilisin Biochim. Biophys. Acta 1543 2000 203 222
11. S.K. Burley, and G.A. Petsko Aromatic-aromatic interaction: a mechanism of protein structure stabilization Science 229 1985 23 28
12. T. Cardozo, M. Totrov, and R. Abagyan Homology modeling by the ICM method Proteins 23 1995 403 414
13. M.A. Ceruso, A. Amadei, and A. Di Nola Mechanics and dynamics of B1 domain of protein G: role of packing and surface hydrophobic residues Protein Sci. 8 1999 147 160
14. G. Chinea, G. Padron, R.W. Hooft, C. Sander, and G. Vriend The use of position-specific rotamers in model building by homology Proteins 23 1995 415 421
15. F. Chiti, M. Calamai, N. Taddei, M. Stefani, G. Ramponi, and C.M. Dobson Studies of the aggregation of mutant proteins in vitro provide insight into the genetics of amyloid diseases Proc. Natl. Acad. Sci. USA 99 2002 16419 16426
16. B. Clantin, C. Tricot, T. Lonhienne, V. Stalon, and V. Villeret Probing the role of oligomerization in the high thermal stability of Pyrococcus furiosus ornithine carbamoyltransferase by site-specific mutants Eur. J. Biochem. 268 2001 3037 3942
17. J. Clarke, and A.R. Fersht Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation Biochemistry 32 1993 4322 4329
18. J. Clarke, A.M. Hounslow, and A.R. Fersht Disulfide mutants of barnase II: changes in structure and local stability identified by hydrogen exchange J. Mol. Biol. 253 1995 505 513
19. B.A. Chrunyk, and R. Wetzel Breakdown in the relationship between thermal and thermodynamic stability in an interleukin-1β point mutant modified in a surface loop Protein Eng. 6 1993 733 738
20. B. Dahiyat, and S.L. Mayo De novo protein design: fully automated sequence selection Science 278 1997 82 87
21. B. Dalhus, M. Sarinen, U.H. Sauer, P. Eklund, K. Johansson, A. Karlsson, S. Ramaswamy, A. Bjørk, B. Synstad, K. Naterstad, R. Sirevag, and H. Eklund Structural basis for thermophilic protein stability: structures of thermophilic and mesophilic malate dehydrogenases J. Mol. Biol. 318 2002 707 721
22. S. D'Amico, C. Gerday, and G. Feller Temperature adaptation of proteins: engineering mesophilic-like activity and stability in a cold-adapted α-amylase J. Mol. Biol. 332 2003 981 988
23. S. D'Amico, J.-C. Marx, C. Gerday, and G. Feller Activity-stability relationships in extremophilic enzymes J. Biol. Chem. 278 2003 7891 7896
24. R.M. Daniel, M.J. Danson, and R. Eisenthal The temperature optima of enzymes: a new perspective on an old phenomenon Trends Biochem. Sci. 26 2001 223 225
25. M.J. Danson, D.W. Hough, R.J.M. Russell, G.L. Taylor, and L. Pearl Enzyme thermostability and thermoactivity Protein Eng. 9 1996 629 630
26. G. Dantas, B. Kuhlman, D. Callender, M. Wong, and D. Baker A large scale test of computational protein design: folding and stability of nine completely redesigned globular proteins J. Mol. Biol. 332 2003 449 460
27. S. Dao-Pin, U. Sauer, H. Nicholson, and B.W. Matthews Contributions of engineered salt bridges to the stability of T4 lysozyme determined by directed mutagenesis Biochemistry 30 1991 7142 7153
28. N. Declerck, M. Machius, G. Wiegand, R. Huber, and C. Gaillardin Probing structural determinants specifying high thermostability in Bacillus licheniformis alpha-amylase J. Mol. Biol. 301 2000 1041 1057
29. N. Declerck, M. Machius, P. Joyet, G. Wiegand, R. Huber, and C. Gaillardin Hyperstabilization of Bacillus licheniformis α-amylase and modulation of its stability over a 50°C temperature range Protein Eng. 16 2003 287 293
30. DeLano, W.L., 2002. The PyMOL Molecular Graphics System. http://www.pymol.org.
31. V. De Filippis, C. Sander, and G. Vriend Predicting local structural changes that result from point mutations Protein Eng. 7 1994 1203 1208
32. S.M. Doyle, E. Anderson, D. Zhu, E.H. Braswell, and C.M. Teschke Rapid unfolding of a domain populates an aggregation-prone intermediate that can be recognized by GroEL J. Mol. Biol. 332 2003 937 951
33. P. Dürrschmidt, J. Mansfeld, and R. Ulbrich-Hofmann Differentiation between conformational and autoproteolytic stability of the neutral protease from Bacillus stearothermophilus containing an engineered disulfide bond Eur. J. Biochem. 268 2001 3612 3618
34. V.G.H. Eijsink, B. Van den Burg, G. Vriend, H.J.C. Berendsen, and G. Venema Thermostability of Bacillus subtilis neutral protease Biochem. Int. 24 1991 517 525
35. V.G.H. Eijsink, G. Vriend, B. Van der Vinne, B. Hazes, B. Van den Burg, and G. Venema Effects of changing the interaction between domains on the thermostability of Bacillus neutral proteases Proteins 14 1992 224 236
36. V.G.H. Eijsink, B.W. Dijkstra, G. Vriend, O.R. Van der Zee, O.R. Veltman, B. Van der Vinne, B. Van den Burg, S. Kempe, and G. Venema The effect of cavity-filling mutations on the thermostability of B. stearothermophilus neutral protease Protein Eng. 5 1992 421 426
37. V.G.H. Eijsink, O.R. Veltman, W. Aukema, G. Vriend, and G. Venema Structural determinants of the stability of thermolysin-like proteases Nature Struct. Biol. 2 1995 374 379
38. V.G.H. Eijsink, G. Vriend, and B. Van den Burg Engineering a hyperstable enzyme by manipulation of early steps in the unfolding process Biocatalysis Biotransformation. 19 2001 443 458
39. J.F. Espinosa, V. Munoz, and S.H. Gellman Interplay between hydrophobic cluster and loop propensity in beta-hairpin formation J. Mol. Biol. 306 2001 397 402
40. H domains with a generalizable approach Biochemistry 42 2003 1517 1528
41. A.R. Fersht Structure and mechanism in protein science 1999 W.H. Freeman New York
42. A.V. Filikov, R.J. Hayes, P. Luo, D.M. Stark, C. Chan, A. Kundu, and B.I. Dahiyat Computational stabilization of human growth hormone Protein Sci. 11 2002 1452 1461
43. A.L. Fink Protein aggregation: folding aggregates, inclusion bodies and amyloid Folding Design 3 1998 R9 R23
44. J.M. Finke, M. Roy, B.H. Zimm, and P.A. Jennings Aggregation events occur prior to stable intermediate formation during refolding of interleukin 1β Biochemistry 39 2000 575 583
45. H. Flores, and A.D. Ellington Increasing the thermal stability of an oligomeric protein, beta-glucoronidase J. Mol. Biol. 315 2002 325 337
46. S. Gåseidnes, B. Synstad, X. Jia, H. Kjellesvik, G. Vriend, and V.G.H. Eijsink Stabilization of a chitinase from Serratia marcescens by Gly → Ala and Xxx → Pro mutations Protein Eng. 16 2003 841 846
47. L. Giver, A. Gershenson, P. Freskgard, and F.H. Arnold Directed evolution of a thermostable esterase Proc. Natl. Acad. Sci. USA 95 1998 12809 12813
48. R.S. Gokhale, S. Agarwalla, V.S. Francis, D.V. Santi, and P. Balaram Thermal stabilization of thymidylate synthase by engineering two disulfide bridges across the dimer interface J. Mol. Biol. 235 1994 89 94
49. M.M. Gromiha, M. Oobatake, H. Kono, H. Uedaira, and A. Sarai Importance of mutant position in Ramachandran plot for predicting protein stability of surface mutations Biopolymers 64 2002 210 220
50. N. Hakulinen, O. Turunen, J. Jänis, M. Leisola, and J. Rouvinen Three-dimensional structures of thermophilic β-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa Eur. J. Biochem. 270 2003 1399 1412
51. F. Hardy, G. Vriend, O.R. Veltman, B. Van der Vinne, G. Venema, and V.G.H. Eijsink Stabilization of Bacillus stearothermophilus neutral protease by introduction of prolines FEBS Lett. 317 1993 89 92
52. 552 J. Biol. Chem. 274 1999 37533 37537
53. B. Hazes, and B.W. Dijkstra Model building of disulfide bonds in proteins with known three-dimensional structure Protein Eng. 2 1988 119 125
54. H.W. Hellinga Computational protein engineering Nature Struct. Biol. 5 1998 525 527
55. G. Hernandez, F.E. Jenney, M.W.W. Adams, and D.M. LeMaster Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature Proc. Natl. Acad. Sci. USA 97 2000 3166 3170
56. T. Herning, K. Yutani, K. Inaka, R. Kuroki, M. Matsushima, and M. Kikuchi Role of proline residues in human lysozyme stability: a scanning calorimetric study combined with X-ray structure analysis of proline mutants Biochemistry 31 1992 7077 7085
57. B.J. Hillier, H.M. Rodriguez, and L.M. Gregoret Coupling protein stability and protein function in Escherichia coli CspA Folding Design 3 1998 87 93
58. L. Holm, and C. Sander Database algorithm for generating protein backbone and side-chain co-ordinates from a C alpha trace application to model building and detection of co-ordinate errors J. Mol. Biol. 218 1991 183 194
59. T. Hori, H. Moriyama, J. Kawaguchi, Y. Hayashi-Iwasaki, T. Oshima, and N. Tanaka The initial step of thermal unfolding of 3-isopropylmalate dehydrogenase detected by the temperature-jump Laue method Protein Eng. 13 2000 527 533
60. J. Hoseki, T. Yano, Y. Koyama, S. Kuramitsu, and H. Kagamiyama Directed evolution of thermostable kanamycin-resistance gene: a convenient selection marker for Thermus thermophilus J. Biochem. 126 1999 951 956
61. T. Imanaka, M. Shibazaki, and M. Takagi A new way of enhancing the thermostability of proteases Nature 324 1986 695 697
62. R. Jaenicke, and G. Bohm The stability of proteins in extreme environments Curr. Opin. Struct. Biol. 8 1998 738 748
63. R. Jaenicke, and H. Lilie Folding and association of oligomeric and multimeric proteins Adv. Protein Chem. 53 2000 329 401
64. R. Jaenicke Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc Natl. Acad. Sci. USA 97 2000 2962 2964
65. P. Joyet, N. Declerck, and C. Gaillardin Hyperthermostable variants of a highly thermostable alpha-amylase Biotechnology 10 1992 1579 1583
66. T. Kabashima, Y. Li, N. Kanada, K. Ito, and T. Yoshimoto Enhancement of the thermal stability of pyroglutamyl peptidase I by introduction of an intersubunit disulfide bond Biochim. Biophys. Acta 1547 2001 214 220
67. S. Kidokoro, Y. Miki, K. Endo, A. Wada, H. Nagao, T. Miyake, A. Aoyama, T. Yoneya, K. Kai, and S. Ooe Remarkable activity enhancement of thermolysin mutants FEBS Lett. 367 1995 73 76
68. Y. Khorkin, A.J. Kalb, M. Peretz, O. Bogin, Y. Burstein, and F. Frolow Oligomeric integrity - The structural key to thermal stability in bacterial alcohol dehydrogenases Protein Sci. 8 1999 1241 1249
69. E. Krieger, G. Koraimann, and G. Vriend Increasing the precision of comparative models with YASARA NOVA- a self-parameterizing force field Proteins 47 2002 393 402
70. J.H. Lebbink, R.I. Eggen, A.C. Geerling, V. Consalvi, R. Chiaraluce, R. Scandurra, and W.M. De Vos Exchange of domains of glutamate dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus and the mesophilic bacterium Clostridium difficile: effects on catalysis, thermoactivity and stability Protein Eng. 8 1995 1287 1294
71. J.H.G. Lebbink, S. Knapp, J. Van der Oost, D. Rice, R. Ladenstein, and W.M. De Vos Engineering activity and stability of Thermotoga maritime glutamate dehydrogenase II: construction of a 16-residue ion-pair network at the subunit interface J. Mol. Biol. 289 1999 357 369
72. M. Lehmann, C. Loch, A. Middendorf, D. Studer, S.F. Lassen, L. Pasamontes, A.P.G.M. Van Loon, and M. Wyss The consensus concept for thermostability engineering of proteins: further proof of concept Protein Eng. 15 2002 403 411
73. M. Machius, N. Declerck, R. Huber, and G. Wiegand Kinetic stabilization of Bacillus licheniformis α-amylase through introduction of hydrophobic residues at the surface J. Biol. Chem. 278 2003 11546 11553
74. N. Maeda, T. Kanai, H. Atomik, and T. Imanaka The unique pentagonal structure of an archeal rubisco is essential for its high thermostability J. Biol. Chem. 277 2002 31656 31662
75. G.I. Makhatadze, V.V. Loladze, D.N. Ermolenko, X.F. Chen, and S.T. Thomas Contribution of surface salt bridges to protein stability: guidelines for protein engineering J. Mol. Biol. 327 2003 1135 1148
76. S.M. Malakauskas, and S.L. Mayo Design, structure and stability of a hyperthermophilic protein variant Nature Struct. Biol. 5 1998 470 475
77. J. Mansfeld, G. Vriend, B.W. Dijkstra, O.R. Veltman, B. Van den Burg, G. Venema, R. Ulbrich-Hofmann, and V.G.H. Eijsink Extreme stabilization of a thermolysin-like protease by an engineered disulfide bond J. Biol. Chem. 272 1997 11152 11156
78. S.A. Marshall, C.S. Morgan, and S.L. Mayo Electrostatics significantly affect the stability of designed homeodomain variants J. Mol. Biol. 316 2002 189 199
79. A. Martin, V. Sieber, and F.X. Schmid In vitro selection of highly stabilized protein variants with optimized surface J. Mol. Biol. 309 2001 717 726
80. A. Martin, I. Kather, and F.X. Schmid Origins of high stability of an in vitro-selected cold-shock protein J. Mol. Biol. 318 2002 1341 1349
81. M. Matsumura, G. Signor, and B.W. Matthews Substantial increase of protein stability by multiple disulfide bonds Nature 342 1989 291 293
82. B.W. Matthews, J.N. Jansonius, P.M. Colman, B.P. Schoenborn, and D. Dupourque Three-dimensional structure of thermolysin Nature 238 1972 37 42
83. B.W. Matthews, H. Nicholson, and W.J. Becktel Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding Proc. Natl. Acad. Sci. USA 84 1987 6663 6667
84. B.W. Matthews Studies on protein stability with T4 lysozyme Adv. Prot. Chem. 46 1993 249 278
85. K. Miyazaki, P.L. Wintrode, R.A. Grayling, D.N. Rubingh, and F.H. Arnold Directed evolution study of temperature adaptation in a psychrophilic enzyme J. Mol. Biol. 297 2000 1015 1026
86. B.H.M. Mooers, D. Datta, W.A. Baase, E.S. Zollars, S.L. Mayo, and B.W. Matthews Repacking the core of T4 lysozyme by automated design J. Mol. Biol. 332 2003 741 756
87. H. Nicholson, W.J. Becktel, and B.W. Matthews Enhanced protein thermostability from designed mutations that interact with alpha-helix dipoles Nature 336 1988 651 656
88. H. Nicholson, D.E. Anderson, S. Dao-pin, and B.W. Mathews Analysis of the interaction between charged side chains and the alpha-helix dipole using designed thermostable mutants of phage T4 lysozyme Biochemistry 30 1991 9816 9828
89. C.N. Pace Measuring and increasing protein stability Trends Biochem. Sci. 8 1990 93 98
90. C.N. Pace, R.W. Alston, and K.L. Shaw Charge-charge interactions influence the denatured state ensemble and contribute to protein stability Protein Sci. 9 2000 1395 1398
91. D. Perl, U. Mueller, U. Heinemann, and F.X. Schmid Two exposed amino acid residues confer thermostability on a cold shock protein Nature Struc. Biol. 7 2000 380 383
92. D. Perl, and F.X. Schmid Electrostatic stabilization of a thermophilic cold shock protein J. Mol. Biol. 313 2001 343 357
93. N. Pokala, and T.M. Handel Review: protein design - where we were, where we are, where we're going J. Struct. Biol. 134 2001 269 281
94. J.W. Ponder, and F.M. Richards Tertiary templates for proteins use of packing criteria in the enumeration of allowed sequences for different structural classes J. Mol. Biol. 193 1987 775 791
95. A.V. Puchkaev, L.S. Koo, and P.R. Ortiz de Montellano Aromatic stacking as a determinant of the thermal stability of CYP119 from Sulfolobus solfataricus Arch. Biochem. Biophys. 409 2003 52 58
96. R.N. Rahman, S. Fujiwara, H. Nakamura, M. Takagi, and T. Imanaka Ion pairs involved in maintaining a thermostable structure of glutamate dehydrogenase from a hyperthermophilic archaeon Biochem. Biophys. Res. Commun. 248 1998 920 926
97. R.J. Russell, D.W. Hough, M.J. Danson, and G.L. Taylor The crystal structure of citrate synthase from the thermophilic archaeon Thermoplasma acidophilum Structure 2 1994 1157 1167
98. D. Sali, M. Bycroft, and A.R. Fersht Stabilization of protein structure by interaction of alpha-helix dipole with a charged side chain Nature 335 1988 740 743
99. M. Sandgren, P.J. Gualfetti, A. Shaw, L.S. Gross, M. Saldajeno, A.G. Day, T.A. Jones, and C. Mitchinson Comparison of family 12 glycosyl hydrolases and recruited substitutions important for stability Protein Sci. 12 2003 848 860
100. R.T. Sauer, K. Hehir, R.S. Stearman, M.A. Weiss, A. Jeitler-Nilsson, E.G. Suchanek, and C.O. Pabo An engineered intersubunit disulfide enhances the stability and DNA binding of the N-terminal domain of lambda repressor Biochemistry 25 1986 5992 5998
101. T. Schindler, D. Perl, P. Graumann, V. Sieber, M.A. Marahiel, and F.X. Schmid Surface-exposed phenylalanines in the RNP1/RNP2 motif stabilize the cold-shock protein CspB from Bacillus subtilis Proteins 30 1998 401 406
102. J.M. Schwehm, E.S. Kristyanne, C.C. Biggers, and W.E. Stites Stability effects of increasing the hydrophobicity of solvent-exposed side chains in staphylococcal nuclease Biochemistry 37 1998 6939 6948
103. J.M. Schwehm, C.A. Fitch, B.N. Dang, B. Garcia-Moreno, and W.E. Stites Changes in stability upon charge reversal and neutralization substitution in staphylococcal nuclease are dominated by favourable electrostatic effects Biochemistry 42 2003 1118 1128
104. L. Serrano, and A.R. Fersht Capping and alpha-helix stability Nature 342 1989 296 299
105. L. Serrano, A. Horovitz, B. Avron, M. Bycroft, and A.R. Fersht Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles Biochemistry 29 1990 9343 9352
106. L. Serrano, M. Bycroft, and A.R. Fersht Aromatic-aromatic interactions and protein stability investigation by double-mutant circles J. Mol. Biol. 218 1991 465 475
107. L. Serrano, J.L. Neira, J. Sancho, and A.R. Fersht Effect of alanine versus glycine in alpha-helices on protein stability Nature 356 1992 453 455
108. L. Serrano, A.G. Day, and A.R. Fersht Step-wise mutation of barnase to binase: a procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability J. Mol. Biol. 233 1993 305 312
109. B. Spiller, A. Gershenson, F.H. Arnold, and R.C. Stevens A structural view of evolutionary divergence Proc. Natl. Acad. Sci. USA 96 1999 12305 12310
110. R. Sterner, and W. Liebl Thermophilic adaptation of proteins Crit. Rev. Biochem. Mol. Biol. 36 2001 39 106
111. P. Strop, and S.L. Mayo Contribution of surface salt bridges to protein stability Biochemistry 39 2000 1251 1255
112. M. Takagi, T. Imanaka, and S. Aiba Nucleotide sequence and promoter region for the neutral protease gene from Bacillus stearothermophilus J. Bacteriol. 163 1985 824 831
113. D. Thirumilai, D.K. Klimov, and R.I. Dima Emerging ideas on the molecular basis of protein and peptide aggregation Curr. Opin. Struct. Biol. 13 2003 146 159
114. R. Thoma, M. Hennig, R. Sterner, and K. Kirschner Structure and function of mutationally generated monomers of dimeric phosphoribosylanthranilate isomerase from Thermotoga maritima Structure 8 2000 265 276
115. T.M. Thomas, and R.K. Scopes The effects of temperature on the kinetics and stability of mesophilic and thermophilic 3-phosphoglycerate kinases Biochem. J. 330 1998 1087 1095
116. L.C. Tisi, and P.A. Evans Conserved structural features on protein surfaces: small exterior hydrophobic clusters J. Mol. Biol. 249 1995 251 258
117. M. Tollinger, K.A. Crowhurst, L.E. Kay, and J.D. Forman-Kay Site-specific contributions to the pH-dependence of protein stability Proc. Natl. Acad. Sci. USA 100 2003 4545 4550
118. B. Van den Burg, H.G. Enequist, M.E. Van der Haar, V.G.H. Eijsink, B.K. Stulp, and G. Venema A highly thermostable neutral protease from Bacillus caldoèlyticus: cloning and expression of the gene in Bacillus subtilis and characterization of the gene product J. Bacteriol. 173 1991 4107 4115
119. B. Van den Burg, B.W. Dijkstra, G. Vriend, B. Van der Vinne, G. Venema, and V.G.H. Eijsink Protein stabilization by hydrophobic interactions at the surface Eur. J. Biochem. 220 1994 981 985
120. B. Van den Burg, G. Vriend, O.R. Veltman, G. Venema, and V.G.H. Eijsink Engineering an enzyme to resist boiling Proc. Natl. Acad. Sci. USA 95 1998 2056 2060
121. B. Van den Burg, A. De Kreij, P. Van der Veek, J. Mansfeld, and G. Venema Characterization of a novel stable biocatalyst obtained by protein engineering Biotechnol. Appl. Biochem. 30 1999 35 40
122. B. Van den Burg, and V.G.H. Eijsink Selection of mutations for increased protein stability Curr. Opin. Biotechnol. 13 2002 333 337
123. O.R. Veltman, G. Vriend, P.J. Middelhoven, B. Van den Burg, G. Venema, and V.G.H. Eijsink Analysis of the structural determinants of the stability of thermolysin-like proteases by molecular modelling and site-directed mutagenesis Protein Eng. 9 1996 1181 1189
124. O.R. Veltman, G. Vriend, F. Hardy, J. Mansfeld, B. Van den Burg, G. Venema, and V.G.H. Eijsink Mutational analysis of a surface area that is critical for the thermal stability of thermolysin-like proteases Eur. J. Biochem. 248 1997 433 440
125. O.R. Veltman, G. Vriend, B. Van den Burg, F. Hardy, G. Venema, and V.G.H. Eijsink Engineering thermolysin-like proteases whose stability is largely independent of calcium FEBS Lett. 405 1997 241 244
126. O.R. Veltman, G. Vriend, H.J.C. Berendsen, B. Van den Burg, G. Venema, and V.G.H. Eijsink A single calcium binding site is crucial for the calcium-dependent thermal stability of thermolysin-like proteases Biochemistry 37 1998 5312 5319
127. S. Ventura, M.C. Vega, E. Lacroix, I. Angrand, L. Spagnolo, and L. Serrano Conformational strain in the hydrophobic core and its implications for protein folding and design Nature Struct. Biol. 9 2002 485 493
128. C. Vetriani, D.L. Maeder, N. Tolliday, K.S.P. Yip, T.J. Stillman, K.L. Britton, D.W. Rice, H.H. Klump, and F.T. Robb Protein thermostability above 100°C: a key role for ionic interactions Proc. Natl. Acad. Sci. USA 95 1998 12300 12305
129. C. Vieille, and G.J. Zeikus Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol. Mol. Biol. Rev. 65 2001 1 43
130. G. Vriend WHAT IF, a molecular modeling and drug design program J. Mol. Graph 8 1990 52 56
131. G. Vriend, and V.G.H. Eijsink Prediction and analysis of structure, stability and unfolding of Bacillus neutral proteases J. Comp. Aided Mol. Design 7 1993 367 396
132. G. Vriend, and C. Sander Quality control of protein models: Directional atomic contact analysis J. Appl. Cryst. 26 1993 47 60
133. G. Vriend, H.J.C. Berendsen, B. Van den Burg, G. Venema, and V.G.H. Eijsink Early steps in the unfolding of thermolysin-like proteases J. Biol. Chem. 273 1998 35074 35077
134. C.D. Waldburger, J.F. Schildbach, and R.T. Sauer Are buried salt bridges important for protein stability and conformational specificity? Nature Struct. Biol. 2 1995 122 128
135. H. Walden, G.S. Bell, R.J.M. Russell, B. Siebersm, R. Hensel, and G.L. Taylor Tiny TIM: a small tetrameric, hyperthermostable triosephosphate isomerase J. Mol. Biol. 306 2001 745 757
136. K. Watanabe, T. Masud, H. Ohashi, H. Mihara, and Y. Suzuki Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase - irrefragable proof supporting the proline rule. Eur. J. Biochem. 226 1994 277 283
137. J.A. Wells Additivity of mutational effects in proteins Biochemistry 29 1990 8509 8517
138. J.C. Williams, J.P. Zeelen, G. Neubauer, G. Vriend, J. Backmann, P.A.M. Michels, A.M. Lambeir, and R.K. Wierenga Structural and mutagenesis studies of leishmania triophosphate isomerase: a point mutation can convert a mesophilic enzyme into a superstable enzyme without losing catalytic power Protein Eng. 12 1999 243 250
139. P.L. Wintrode, and F.H. Arnold Temperature adaptation of enzymes: lessons from laboratory evolution Adv. Prot. Chem. 55 2000 161 225
140. P.L. Wintrode, D. Zhang, N. Vaidehi, F.H. Arnold, and W.A. Goddard III Protein dynamics in a family of laboratory evolved thermophilic enzymes J. Mol. Biol. 327 2003 745 757
141. L. Xiao, and B. Honig Electrostatic contributions to the stability of hyperthermophilic proteins J. Mol. Biol. 289 1999 1435 1444
142. K.S.P. Yip, T.J. Stillman, K.L. Britton, P.J. Artymiuk, P.J. Baker, S.E. Sedelnikova, P.C. Engel, A. Pasquo, R. Chiaraluce, V. Consalvi, R. Scandurra, and D.W. Rice The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures Structure 3 1995 1147 1158
143. P. Zavodszky, J. Kardos, A. Svingor, and G.A. Petsko Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins Proc. Natl. Acad. Sci. USA 95 1998 7406 7411
144. X. Zhang, W.A. Baase, B.K. Shoichet, K.P. Wilson, and B.W. Matthes Enhancement of protein stability by the combination of point mutations in T4 lysozyme is additive Protein Eng. 8 1995 1017 1022
145. H. Zhao, and F.H. Arnold Directed evolution converts subtilisin E into a functional equivalent of thermitase Protein Eng. 12 1999 47 53