Conferring Thermostability to Mesophilic Proteins through Optimized Electrostatic Surfaces

Biophysical Journal

Volumn 85, Issue 5, 2003, Pages 2845-2853

  Torrez, Michael ^a   Schultehenrich, Michael ^a   Livesay, Dennis R ^a  

^a CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DISULFIDE BOND; HYDROGEN BOND; MUTAGENESIS; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SURFACE PROPERTY; TARGET CELL; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

BACTERIA (MICROORGANISMS);

EID: 0242385395     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74707-9     Document Type: Article

References (53)

1. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1994. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:415-436.
2. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1996. The determinants of pKas in proteins. Biochemistry. 35:7819-7833.
3. Baldwin, R. L., and G. D. Rose. 1999a. Is protein folding hierarchic? I. Local structure and peptide folding. Trends Biochem. Sci. 24:26-33.
4. Baldwin, R. L., and G. D. Rose. 1999b. Is protein folding hierarchic? II. Folding intermediates and transition states. Trends Biochem. Sci. 24:77-83.
5. Boschitsch, A. H., M. O. Fenley, and H.-X. Zhou. 2002. Fast boundary element method for the linear Poisson-Boltzmann equation. J. Phys. Chem. B. 106:2741-2754.
6. Bower, M. J., F. E. Cohen, and R. L. Dunbrack, Jr. 1997. Prediction of protein side-chain rotamers from a backbone-dependent rotamer library: a new homology modeling tool. J. Mol. Biol. 267:1268-1282.
7. Brooks, B. R., R. E. Ruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM, A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
8. Brooks, III, C. L. 2002. Protein and peptide folding explored with molecular simulations. Acc. Chem. Res. 35:447-454.
9. Bryson, J. W., S. F. Betz, H. S. Lu, D. J. Suich, H. X. Zhou, K. T. O'Neil, and W. F. DeGrado. 1995. Protein design: a hierarchic approach. Science. 270:935-941.
10. Cordes, M. H., A. R. Davidson, and R. T. Sauer. 1996. Sequence space, folding and protein design. Curr. Opin. Struct. Biol. 6:3-10.
11. Daggett, V. 2002. Molecular dynamics simulations of the protein unfolding/folding reaction. Acc. Chem. Res. 35:422-429.
12. Dao-pin, S., D. E. Anderson, W. A. Baase, F. W. Dahlquist, and B. W. Matthews. 1991. Structural and thermodynamic consequences of burying a charged residue within the hydrophobic core of T4 lysozyme. Biochemistry. 30:11521-11529.
13. Dominy, B. N., D. Perl, F. X. Schmid, and C. L. Brooks, III. 2002. The effects of ionic strength on protein stability: the cold shock protein family. J. Mol. Biol. 319:541-554.
14. Elcock, A. H. 1999. Realistic modeling of the denatured states of proteins allows accurate calculations of the pH dependence of protein stability. J. Mol. Biol. 294:1051-1062.
15. Gibas, C. J., and S. Subramaniam. 1996. Explicit solvent models in protein pKa calculations. Biophys. J. 71:138-147.
16. Gibas, C. J., S. Subramaniam, J. A. McCammon, B. C. Braden, and R. J. Poljak. 1997. pH dependence of antibody/lysozyme complexation. Biochemistry. 36:15599-15614.
17. Gillespie, J. R., and D. Shortle. 1997. Characterization of long-range structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. J. Mol. Biol. 268:170-184.
18. Gilson, M. K. 1993. Multiple-site titration and molecular modeling: two rapid methods for computing energies and forces for ionizable groups in proteins. Proteins. 15:266-282.
19. Grimsley, G. R., K. L. Shaw, L. R. Fee, R. W. Alston, B. M. Huyghues-Despointes, R. L. Thurlkill, J. M. Scholtz, and C. N. Pace. 1999. Increasing protein stability by altering long-range coulombic interactions. Protein Sci. 8:1843-1849.
20. Houry, W. A., D. M. Rothwarf, and H. A. Scheraga. 1996. Circular dichroism evidence for the presence of burst-phase intermediates on the conformational folding pathway of ribonuclease A. Biochemistry. 35:10125-10133.
21. Houry, W. A., and H. A. Scheraga. 1996. Structure of a hydrophobically collapsed intermediate on the conformational folding pathway of ribonuclease A probed by hydrogen-deuterium exchange. Biochemistry. 35:11734-11746.
22. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential function for proteins, energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
23. Kumar, S., C. J. Tsai, and R. Nussinov. 2000. Factors enhancing protein thermostability. Protein Eng. 13:179-191.
24. Livesay, D., S. Linthicum, and S. Subramaniam. 1999. pH dependence of antibody: hapten association. Mol. Immunol. 36:397-410.
25. Livesay, D. R., P. Jambeck, A. Rojnuckarin, and S. Subramaniam. 2003. Conservation of electrostatic properties within enzyme families and superfamilies. Biochemistry. 42:3464-3473.
26. Loladze, V. V., B. Ibarra-Molero, J. M. Sanchez-Ruiz, and G. I. Makhatadze. 1999. Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry. 38:16419-16423.
27. Loladze, V. V., and G. I. Makhatadze. 2002. Removal of surface charge-charge interactions from ubiquitin leaves the protein folded and very stable. Protein Sci. 11:174-177.
28. Madura, J. D., J. M. Briggs, R. C. Wade, M. E. Davis, B. A. Lutty, A. Ilin, J. Antosiewicz, M. K. Gilson, B. Gagheri, L. R. Scott, and J. A. McCammon. 1995. Electrostatics and diffusion of molecules in solution, simulations with the University of Houston Brownian dynamics program. Comput. Phys. Comm. 91:57-95.
29. Maier, C. S., M. I. Schimerlik, and M. L. Deinzer. 1999. Thermal denaturation of Escherichia coli thioredoxin studied by hydrogen/deuterium exchange and electrospray ionization mass spectrometry: monitoring a two-state protein unfolding transition. Biochemistry. 38:1136-1143.
30. Martin, A., V. Sieber, and F. X. Schmid. 2001. In-vitro selection of highly stabilized protein variants with optimized surface. J. Mol. Biol. 309:717-726.
31. Martinez-Oyanedel, J., H. W. Choe, U. Heinemann, and W. Saenger. 1991. Ribonuclease T1 with free recognition and catalytic site: crystal structure analysis at 1.5 Å resolution. J. Mol. Biol. 222:335-352.
32. Matsumura, P., J. J. Rydel, R. Linzmeier, and D. Vacante. 1984. Overexpression and sequence of the Escherichia coli cheY gene and biochemical activities of the CheY protein. J. Bacteriol. 160:36-41.
33. Matthews, B. W. 1995. Studies on protein stability with T4 lysozyme. Adv. Protein Chem. 46:249-278.
34. Mueller, U., D. Perl, F. X. Schmid, and U. Heinemann. 2000. Thermal stability and atomic-resolution crystal structure of the Bacillus caldolyticus cold shock protein. J. Mol. Biol. 297:975-988.
35. Pace, C. N. 1995. Evaluating contribution of hydrogen bonding and hydrophobic bonding to protein folding. Methods Enzymol. 259:538-554.
36. Pace, C. N., R. W. Alston, and K. L. Shaw. 2000. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9:1395-1398.
37. Pedone, E., M. Saviano, M. Rossi, and S. Bartolucci. 2001. A single point mutation (Glu85Arg) increases the stability of the thioredoxin from Escherichia coli. Protein Eng. 14:255-260.
38. Perl, D., U. Mueller, U. Heinemann, and F. X. Schmid. 2000. Two exposed amino acid residues confer thermostability on a cold shock protein. Nat. Struct. Biol. 7:380-383.
39. Perl, D., and F. X. Schmid. 2001. Electrostatic stabilization of a thermophilic cold shock protein. J. Mol. Biol. 313:343-357.
40. Perry, K. M., J. J. Onuffer, M. S. Gittelman, L. Barmat, and C. R. Matthews. 1989. Long-range electrostatic interactions can influence the folding, stability, and cooperativity of dihydrofolate reductase. Biochemistry. 28:7961-7968.
41. Schindelin, H., M. A. Marahiel, and U. Heinemann. 1993. Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature. 364:164-168.
42. Scholtz, J. M., and R. L. Baldwin. 1992. The mechanism of alpha-helix formation by peptides. Annu. Rev. Biophys. Biomol. Struct. 21:95-118.
43. Sehorn, M. G., S. V. Slepenkov, and S. N. Witt. 2002. Characterization of two partially unfolded intermediates of the molecular chaperone DnaK at low pH. Biochemistry. 41:8499-8507.
44. Serrano, L., J. T. Kellis, Jr., P. Cann, A. Matouschek, and A. R. Fersht. 1992. The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability. J. Mol. Biol. 224:783-804.
45. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301-332.
46. Spector, S., M. Wang, S. A. Carp, J. Robblee, Z. S. Hendsch, R. Fairman, B. Tidor, and D. P. Raleigh. 2000. Rational modification of protein stability by the mutation of charged surface residues. Biochemistry. 39:872-879.
47. Strop, P., and S. L. Mayo. 2000. Contribution of surface salt bridges to protein stability. Biochemistry. 39:1251-1255.
48. Usher, K. C., A. F. de la Cruz, F. W. Dahlquist, R. V. Swanson, M. I. Simon, and S. J. Remington. 1998. Crystal structures of CheY from Thermotoga maritima do not support conventional explanations for the structural basis of enhanced thermostability. Protein Sci. 7:403-412.
49. Volz, K., and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution. J. Biol. Chem. 266:15511-15519.
50. Xiao, L., and B. Honig. 1999. Electrostatic contributions to the stability of hyperthermophilic proteins. J. Mol. Biol. 289:1435-1444.
51. Zhou, H. X. 2002a. A Gaussian-chain model for treating residual charge-charge interactions in the unfolded state of proteins. Proc. Natl. Acad. Sci. USA. 99:3569-3574.
52. Zhou, H. X. 2002b. Residual electrostatic effects in the unfolded state of the N-terminal domain of L9 can be attributed to nonspecific nonlocal charge-charge interactions. Biochemistry. 41:6533-6538.
53. Zhou, H. X., and F. Dong. 2003. Electrostatic contributions to the stability of a thermophilic cold shock protein. Biophys. J. 84:2216-2222.