Stabilization of the cold shock protein CspB from Bacillus subtilis by evolutionary optimization of coulombic interactions

Journal of Molecular Biology

Volumn 347, Issue 5, 2005, Pages 1063-1076

  Wunderlich, Michael ^a   Martin, Andreas ^a,b   Schmid, Franz X ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Electrostatic interactions; In vitro selection; Phage display; Protein design; Protein stability

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; COLD SHOCK PROTEIN; MUTANT PROTEIN;

ARTICLE; BACILLUS SUBTILIS; CALCULATION; CODON; CONCENTRATION (PARAMETERS); CORRELATION ANALYSIS; ELECTRICITY; GENE LIBRARY; GENE MUTATION; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN VARIANT; QUANTUM THEORY; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; WILD TYPE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 15244350748     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.02.014     Document Type: Article

References (52)

1. Z.S. Hendsch, and B. Tidor Electrostatic interactions in the GCN4 leucine zipper: substantial contributions arise from intramolecular interactions enhanced on binding Protein Sci. 8 1999 1381 1392
2. 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
3. S. Dao-pin, U. Sauer, H. Nicholson, and B.W. Matthews Contributions of engineered surface salt bridges to the stability of T4 lysozyme determined by directed mutagenesis Biochemistry 30 1991 7142 7153
4. D.E. Anderson, W.J. Becktel, and F.W. Dahlquist pH-induced denaturation of proteins: a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme Biochemistry 29 1990 2403 2408
5. 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
6. K. Takano, K. Tsuchimori, Y. Yamagata, and K. Yutani Contribution of salt bridges near the surface of a protein to the conformational stability Biochemistry 39 2000 12375 12381
7. V.Z. Spassov, A.D. Karshikoff, and R. Ladenstein Optimization of the electrostatic interactions in proteins of different functional and folding type Protein Sci. 3 1994 1556 1569
8. A. Karshikoff, and R. Ladenstein Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads Trends Biochem. Sci. 26 2001 550 556
9. L. Xiao, and B. Honig Electrostatic contributions to the stability of hyperthermophilic proteins J. Mol. Biol. 289 1999 1435 1444
10. S. Spector, M. Wang, S.A. Carp, J. Robblee, Z.S. Hendsch, and R. Fairman Rational modification of protein stability by the mutation of charged surface residues Biochemistry 39 2000 872 879
11. K.L. Shaw, G.R. Grimsley, G.I. Yakovlev, A.A. Makarov, and C.N. Pace The effect of net charge on the solubility, activity, and stability of ribonuclease Sa Protein Sci. 10 2001 1206 1215
12. M. Akke, and S. Forsen Protein stability and electrostatic interactions between solvent exposed charged side chains Proteins: Struct. Funct. Genet. 8 1990 23 29
13. G.R. Grimsley, K.L. Shaw, L.R. Fee, R.W. Alston, and B.M. Huyghues-Despointes Increasing protein stability by altering long-range Coulombic interactions Protein Sci. 8 1999 1843 1849
14. P.I. de Bakker, P.H. Hunenberger, and J.A. McCammon Molecular dynamics simulations of the hyperthermophilic protein sac7d from Sulfolobus acidocaldarius: contribution of salt bridges to thermostability J. Mol. Biol. 285 1999 1811 1830
15. J.M. Sanchez-Ruiz, and G.I. Makhatadze To charge or not to charge? Trends Biotechnol. 19 2001 132 135
16. 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
17. A. Horovitz, L. Serrano, B. Avron, M. Bycroft, and A.R. Fersht Strength and cooperativity of contributions of surface salt bridges to protein stability J. Mol. Biol. 216 1990 1031 1044
18. J.H. Lebbink, S. Knapp, J. van der Oost, D. Rice, R. Ladenstein, and W.M. de Vos Engineering activity and stability of Thermotoga maritima glutamate dehydrogenase. II: construction of a 16-residue ion-pair network at the subunit interface J. Mol. Biol. 289 1999 357 369
19. H. Schindelin, M.A. Marahiel, and U. Heinemann Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein Nature 364 1993 164 168
20. D. Perl, U. Mueller, U. Heinemann, and F.X. Schmid Two exposed amino acid residues confer thermostability on a cold shock protein Nature Struct. Biol. 7 2000 380 383
21. D. Perl, and F.X. Schmid Electrostatic stabilization of a thermophilic cold shock protein J. Mol. Biol. 313 2001 343 357
22. V. Sieber, A. Plückthun, and F.X. Schmid Selecting proteins with improved stability by a phage-based method Nature Biotechnol. 16 1998 955 960
23. 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
24. A. Martin, I. Kather, and F.X. Schmid Origins of the high stability of an in vitro-selected cold-shock protein J. Mol. Biol. 318 2002 1341 1349
25. B.N. Dominy, D. Perl, F.X. Schmid, and C.L. Brooks The effects of ionic strength on protein stability: the cold shock protein family J. Mol. Biol. 319 2002 541 554
26. H.X. Zhou, and F. Dong Electrostatic contributions to the stability of a thermophilic cold shock protein Biophys. J. 84 2003 2216 2222
27. S. Garofoli, M. Falconi, and A. Desideri Thermophilicity of wild type and mutant cold shock proteins by molecular dynamics simulation J. Biomol. Struct. Dynam. 21 2004 771 779
28. M. Torrez, M. Schultehenrich, and D.R. Livesay Conferring thermostability to mesophilic proteins through optimized electrostatic surfaces Biophys. J. 85 2003 2845 2853
29. B.N. Dominy, H. Minoux, and C.L. Brooks An electrostatic basis for the stability of thermophilic proteins Proteins Struct. Funct. Genet. 57 2004 128 141
30. D. Wassenberg, C. Welker, and R. Jaenicke Thermodynamics of the unfolding of the cold-shock protein from Thermotoga maritima J. Mol. Biol. 289 1999 187 193
31. K.K. Lee, C.A. Fitch, and B. Garcia-Moreno Distance dependence and salt sensitivity of pairwise, coulombic interactions in a protein Protein Sci. 11 2002 1004 1016
32. K.K. Lee, C.A. Fitch, J.T.J. Lecomte, and B. Garcia-Moreno Electrostatic effects in highly charged proteins: salt sensitivity of pK(a) values of histidines in staphylococcal nuclease Biochemistry 41 2002 5656 5667
33. D.L. Luisi, C.D. Snow, J.J. Lin, Z.S. Hendsch, B. Tidor, and D.P. Raleigh Surface salt bridges, double-mutant cycles, and protein stability: an experimental and computational analysis of the interaction of the Asp 23 side chain with the N-terminus of the N-terminal domain of the ribosomal protein L9 Biochemistry 42 2003 7050 7060
34. A. Koide, M.R. Jordan, S.R. Horner, V. Batori, and S. Koide Stabilization of a fibronectin type III domain by the removal of unfavorable electrostatic interactions on the protein surface Biochemistry 40 2001 10326 10333
35. R. Perez-Jimenez, R. Godoy-Ruiz, B. Ibarra-Molero, and J.M. Sanchez-Ruiz The efficiency of different salts to screen charge interactions in proteins: a Hofmeister effect? Biophys. J. 86 2004 2414 2429
36. D. Perl, C. Welker, T. Schindler, K. Schröder, M.A. Marahiel, R. Jaenicke, and F.X. Schmid Conservation of rapid two-state folding in mesophilic, thermophilic, and hyperthermophilic cold shock proteins Nature Struct. Biol. 5 1998 229 235
37. M.F. Perutz, A.M. Gronenborn, G.M. Clore, J.H. Fogg, and D.T.-B. Shih The pKa values of two histidine residues in human haemoglobin, the Bohr effect, and the dipole moments of α-helices J. Mol. Biol. 183 1985 491 498
38. Y.H. Kao, C.A. Fitch, S. Bhattacharya, C.J. Sarkisian, J.T.J. Lecomte, and B. Garcia-Moreno Salt effects on ionization equilibria of histidines in myoglobin Biophys. J. 79 2000 1637 1654
39. M.M. Garcia-Mira, D. Boehringer, and F.X. Schmid The folding transition state of the cold shock protein is strongly polarized J. Mol. Biol. 339 2004 555 569
40. A. Mozo-Villarias, J. Cedano, and E. Querol A simple electrostatic criterion for predicting the thermal stability of proteins Protein Engng. 16 2003 279 286
41. G.I. Makhatadze, V.V. Loladze, A.V. Gribenko, and M.M. Lopez Mechanism of thermostabilization in a designed cold shock protein with optimized surface electrostatic interactions J. Mol. Biol. 336 2004 929 942
42. W.R. Forsyth, M.K. Gilson, J. Antosiewicz, O.R. Jaren, and A.D. Robertson Theoretical and experimental analysis of ionization equilibria in ovomucoid third domain Biochemistry 37 1998 8643 8652
43. M. Sundd, and A.D. Robertson Rearrangement of charge-charge interactions in variant ubiquitins as detected by double-mutant cycles and NMR J. Mol. Biol. 332 2003 927 936
44. D.N. Marti, and H.R. Bosshard Inverse electrostatic effect: electrostatic repulsion in the unfolded state stabilizes a leucine zipper Biochemistry 43 2004 12436 12447
45. B. Kuhlman, D.L. Luisi, P. Young, and D.P. Raleigh pK(a) values and the pH dependent stability of the N-terminal domain of L9 as probes of electrostatic interactions in the denatured state. Differentiation between local and non-local interactions Biochemistry 38 1999 4896 4903
46. 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
47. A. Martin, F.X. Schmid, and V. Sieber Proside: a phage based method for selecting thermostable proteins Methods Mol. Biol. 230 2003 57 70
48. U. Mueller, D. Perl, F.X. Schmid, and U. Heinemann Thermal stability and atomic-resolution crystal structure of the Bacillus caldolyticus cold shock protein J. Mol. Biol. 297 2000 975 988
49. H. Schindelin, M. Herrler, G. Willimsky, M.A. Marahiel, and U. Heinemann Overproduction, crystallization, and preliminary X-ray diffraction studies of the major cold shock protein from Bacillus subtilis, CspB Proteins: Struct. Funct. Genet. 14 1992 120 124
50. T.L. Calderone, R.D. Stevens, and T.G. Oas High-level misincorporation of lysine for arginine at AGA codons in a fusion protein expressed in Escherichia coli J. Mol. Biol. 262 1996 407 412
51. C. Magg, and F.X. Schmid Rapid collapse precedes the fast two-state folding of the cold shock protein J. Mol. Biol. 335 2004 1309 1323
52. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55