Key Role of Coulombic Interactions for the Folding Transition State of the Cold Shock Protein

Journal of Molecular Biology

Volumn 364, Issue 3, 2006, Pages 458-468

  Garcia Mira, Maria M ^a   Schmid, Franz X ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

CspB; folding kinetics; folding mechanism; protein electrostatics; protein folding

Indexed keywords

ASPARTIC ACID; COLD SHOCK PROTEIN; GUANIDINE HYDROCHLORIDE; LYSINE; UREA;

ARTICLE; COULOMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 33750833156     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.08.071     Document Type: Article

References (68)

1. Matthews C.R. Effect of point mutations on the folding of globular proteins. Methods Enzymol. 154 (1987) 498-511
2. Matouschek A., Kellis Jr. J.T., Serrano L., and Fersht A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 340 (1989) 122-126
3. Goldenberg D.P., Frieden R.W., Haack J.A., and Morrison T.B. Mutational analysis of a protein-folding pathway. Nature 338 (1989) 127-132
4. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224 (1992) 771-782
5. Fersht A. Characterizing transition states in protein folding: an essential step in the puzzle. Curr. Opin. Struct. Biol. 5 (1995) 79-84
6. Itzhaki L.S., Otzen D.E., and Fersht A. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254 (1995) 260-288
7. Milla M.E., Brown B.M., Waldburger C.D., and Sauer R.T. P22 arc repressor: transition state properties inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry 34 (1995) 13914-13919
8. Lopez-Hernandez E., and Serrano L. Structure of the transition state for folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Fold. Des. 1 (1996) 43-55
9. Villegas V., Martinez J.C., Aviles F.X., and Serrano L. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain. J. Mol. Biol. 283 (1998) 1027-1036
10. Grantcharova V.P., Alm E.J., Baker D., and Horwich A.L. Mechanisms of protein folding. Curr. Opin. Struct. Biol. 11 (2001) 70-82
11. Riddle D.S., Grantcharova V.P., Santiago J.V., Alm E., Ruczinski I., and Baker D. Experiment and theory highlight role of native state topology in SH3 folding. Nature Struct. Biol. 6 (1999) 1016-1024
12. Martinez J.C., and Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nature Struct. Biol. 6 (1999) 1010-1016
13. Burton R.E., Huang G.S., Daugherty M.A., Calderone T.L., and Oas T.G. The energy landscape of a fast-folding protein mapped by Ala-Gly substitutions. Nature Struct. Biol. 4 (1997) 305-310
14. Capaldi A.P., Kleanthous C., and Radford S.E. Im7 folding mechanism: misfolding on a path to the native state. Nature Struct. Biol. 9 (2002) 209-216
15. Friel C.T., Capaldi A.P., and Radford S.E. Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: similarities and differences in the folding of homologous proteins. J. Mol. Biol. 326 (2003) 293-305
16. Chu R.A., Pei W.H., Takei J., and Bai Y.W. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 41 (2002) 7998-8003
17. Northey J.G., Di Nardo A.A., and Davidson A.R. Hydrophobic core packing in the SH3 domain folding transition state. Nature Struct. Biol. 9 (2002) 126-130
18. Guerois R., and Serrano L. The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 304 (2000) 967-982
19. Mc Callister E.L., Alm E., and Baker D. Critical role of b-hairpin formation in protein G folding. Nature Struct. Biol. 7 (2000) 669-673
20. Kim D.E., Fisher C., and Baker D. A breakdown of symmetry in the folding transition state of protein L. J. Mol. Biol. 298 (2000) 971-984
21. Main E.R.G., Fulton K.F., Daggett V., and Jackson S.E. Folding pathway of FKBP12 and characterisation of the transition state. J. Mol. Biol. 291 (1999) 429-444
22. Fulton K.F., Main E.R.G., Daggett V., and Jackson S.E. Mapping the interactions present in the transition state for unfolding/folding of FKBP12. J. Mol. Biol. 291 (1999) 445-461
23. Kragelund B.B., Osmark P., Neergaard T.B., Schiodt J., Kristiansen K., Knudsen J., and Poulsen F.M. The formation of a native-like structure containing eight conserved hydrophobic residues is rate limiting in two-state protein folding of ACBP. Nature Struct. Biol. 6 (1999) 594-601
24. Jemth P., Day R., Gianni S., Khan F., Allen M., Daggett V., and Fersht A. The structure of the major transition state for the folding of an FF domain from experiment and simulation. J. Mol. Biol. 350 (2005) 363-378
25. Sato S., Reluga T.L., Daggett V., and Fersht A. Testing protein-folding simulations by experiment: B domain of protein A. Proc. Natl Acad. Sci. USA 101 (2004) 6952-6956
26. Scott K.A., Randles L.G., and Clarke J. The folding of spectrin domains II: phi-value analysis of R16. J. Mol. Biol. 344 (2004) 207-221
27. Went H.M., and Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng. Des. Sel. 18 (2005) 229-237
28. Merlo C., Dill K.A., and Weikl T.R. Phi values in protein-folding kinetics have energetic and structural components. Proc. Natl Acad. Sci. USA 102 (2005) 10171-10175
29. Schindelin H., Marahiel M.A., and Heinemann U. Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364 (1993) 164-168
30. Schnuchel A., Wiltscheck R., Czisch M., Herrler M., Willimsky G., Graumann P., et al. Structure in solution of the major cold-shock protein from Bacillus subtilis. Nature 364 (1993) 169-171
31. Schindler T., Herrler M., Marahiel M.A., and Schmid F.X. Extremely rapid protein folding in the absence of intermediates: the cold-shock protein from Bacillus subtilis. Nature Struct. Biol. 2 (1995) 663-673
32. Schindler T., and Schmid F.X. Thermodynamic properties of an extremely rapid protein folding reaction. Biochemistry 35 (1996) 16833-16842
33. Garcia-Mira M.M., Boheringer D., and Schmid F.X. The folding transition state of the cold shock protein is strongly polarized. J. Mol. Biol. 339 (2004) 555-569
34. Ibarra-Molero B., Loladze V.V., Makhatadze G.I., and Sanchez-Ruiz J.M. Thermal versus guanidine-induced unfolding of ubiquitin. An analysis in terms of the contributions from charge-charge interactions to protein stability. Biochemistry 38 (1999) 8138-8149
35. Perez-Jimenez R., Godoy-Ruiz R., Ibarra-Molero B., and Sanchez-Ruiz J.M. The efficiency of different salts to screen charge interactions in proteins: a Hofmeister effect?. Biophys. J. 86 (2004) 2414-2429
36. Luisi D.L., Snow C.D., Lin J.-J., Hendsch Z.S., Tidor B., and Raleigh D. 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
37. Kao Y.H., Fitch C.A., Bhattacharya S., Sarkisian C.J., Lecomte J.T., and Garcia-Moreno E.B. Salt effects on ionization equilibria of histidines in myoglobin. Biophys. J. 79 (2000) 1637-1654
38. Dominy B.N., Perl D., Schmid F.X., and Brooks III C.L. The effects of ionic strength on protein stability: the cold shock protein family. J. Mol. Biol. 319 (2002) 541-554
39. Fersht A., and Sato S. Phi-value analysis and the nature of protein-folding transition states. Proc. Natl Acad. Sci. USA 101 (2004) 7976-7981
40. Perl D., Holtermann G., and Schmid F.X. Role of the chain termini for the folding transition state of the cold shock protein. Biochemistry 40 (2001) 15501-15511
41. Makhatadze G.I., Loladze V.V., Ermolenko D.N., Chen X., and Thomas S.T. Contribution of surface salt bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327 (2003) 1135-1148
42. Horovitz A., and Fersht A. Co-operative interactions during protein folding. J. Mol. Biol. 224 (1992) 733-740
43. Cota E., Steward A., Fowler S.B., and Clarke J. The folding nucleus of a fibronectin type III domain is composed of core residues of the immunoglobulin-like fold. J. Mol. Biol. 305 (2001) 1185-1194
44. Hamill S.J., Steward A., and Clarke J. The folding of an immunoglobulin-like Greek key protein is defined by a common-core nucleus and regions constrained by topology. J. Mol. Biol. 297 (2000) 165-178
45. Jäger M., Nguyen H., Crane J.C., Kelly J.W., and Gruebele M. The folding mechanism of a b-sheet: the WW domain. J. Mol. Biol. 311 (2001) 373-393
46. Tissot A.C., Vuilleumier S., and Fersht A.R. Importance of two buried salt bridges in the stability and folding pathway of Barnase. Biochemistry 35 (1996) 6786-6794
47. Oliveberg M., and Fersht A.R. A new approach to the study of transient protein conformations: the formation of a semiburied salt link in the folding pathway of barnase. Biochemistry 35 (1996) 6795-6805
48. Ibarra-Molero B., Zitzewitz J.A., and Matthews C.R. Salt-bridges can stabilize but do not accelerate the folding of the homodimeric coiled-coil peptide GCN4-p1. J. Mol. Biol. 336 (2004) 989-996
49. Laurents D.V., Corrales S., Elías-Arnanz M., Sevilla P., Rico M., and Padmanabhan S. Folding kinetics of phage 434 Cro protein. Biochemistry 39 (2000) 13963-13973
50. Travaglini-Allocatelli C., Cutruzzolà F., Bigotti M.G., Staniforth R.A., and Brunori M. Folding mechanism of Pseudomonas aeruginosa cytochrome c551: role of electrostatic interactions on the hydrophobic collapse and transition state properties. J. Mol. Biol. 289 (1999) 1459-1467
51. Gianni S., Brunori M., and Travaglini-Allocatelli C. Refolding kinetics of cytochrome c551 reveals a mechanistic difference between urea and guanidine. Protein Sci. 10 (2001) 1685-1688
52. Luisi D.L., and Raleigh D.P. pH-dependent interactions and the stability and folding kinetics of the N-terminal domain of L9. Electrostatic interactions are only weakly formed in the transition state for folding. J. Mol. Biol. 299 (2000) 1091-1100
53. Cho J.-H., Sato S., and Raleigh D.P. Thermodynamics and kinetics of non-native interactions in protein folding: a single point mutant significantly stabilizes the N-terminal domain of L9 by modulating non-native interactions in the denatured state. J. Mol. Biol. 338 (2004) 827-837
54. Vaughan C.K., Harryson P., Buckle A.M., and Fersht A. A structural double-mutant cycle: estimating the strength of a buried salt bridge in barnase. Acta Crystallog. sect. D 58 (2002) 591-600
55. Serrano L., Horovitz A., Avron B., Bycroft M., and Fersht A. Estimating the contribution of engineered surface electrostatic interactions to protein by using double-mutant cycles. Biochemistry 29 (1990) 9343-9352
56. Willimsky G., Bang H., Fischer G., and Marahiel M.A. Characterization of CspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures. J. Bacteriol. 174 (1992) 6326-6335
57. Schindelin H., Herrler M., Willimsky G., Marahiel M.A., and Heinemann U. 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
58. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Annal. Biochem. 182 (1989) 319-326
59. Shrake A., and Rupley J.A. Environment and exposure to solvent of protein atoms. Lysozyme and insulin. J. Mol. Biol. 79 (1973) 351-371
60. Chothia C. The nature of the accessible and buried surfaces in proteins. J. Mol. Biol. 105 (1976) 1-12
61. Tanford C., and Kirkwood J.G. Theory of protein titration curves. I. General equations for impenetrable spheres. J. Am. Chem. Soc. 79 (1957) 5333-5339
62. Mattew J.B., and Gurd F.R. Calculation of electrostatic interactions in proteins. Methods Enzymol. 130 (1986) 413-436
63. Garcia-Mira M.M., and Sanchez-Ruiz J.M. pH corrections and protein ionization in water/guanidinium chloride. Biophys. J. 81 (2001) 3489-3502
64. Acevedo O., Guzman-Casado M., Garcia-Mira M.M., Ibarra-Molero B., and Sanchez-Ruiz J.M. pH corrections in chemical denaturant solutions. Anal. Biochem. 306 (2002) 158-161
65. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131 (1986) 266-280
66. Georgescu R.E., Garcia-Mira M.M., Tasayco M.L., and Sanchez-Ruiz J.M. Heat capacity analysis of oxidized Escherichia coli thioredoxin fragments (1-73, 74-108) and their noncovalent complex. Evidence for the burial of apolar surface in protein unfolded states. Eur. J. Biochem. 268 (2001) 1477-1485
67. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl a-chymotrypsin using different denaturants. Biochemistry 27 (1988) 8063-8068
68. Perl D., Mueller U., Heinemann U., and Schmid F.X. Two exposed amino acid residues confer thermostability on a cold shock protein. Nature Struct. Biol. 7 (2000) 380-383