Non-linear effects of temperature and urea on the thermodynamics and kinetics of folding and unfolding of hisactophilin

Journal of Molecular Biology

Volumn 344, Issue 4, 2004, Pages 1089-1107

  Wong, Hannah J ^a   Stathopulos, Peter B ^a   Bonner, Julia M ^a   Sawyer, Marc ^a   Meiering, Elizabeth M ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

hisactophilin; protein folding; protein thermodynamics; two state kinetics; trefoil

Indexed keywords

AMYLOID PROTEIN; HISACTOPHILIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; UREA; WATER;

AMINO ACID COMPOSITION; ARTICLE; ENTHALPY; ENTROPY; NONLINEAR SYSTEM; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TEMPERATURE MEASUREMENT; THERMODYNAMICS;

LOTUS;

EID: 8544225716     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.091     Document Type: Article

References (98)

1. C. Liu, D. Chu, R.D. Wideman, R.S. Houliston, H.J. Wong, and E.M. Meiering Thermodynamics of denaturation of hisactophilin, a beta-trefoil protein Biochemistry 40 2001 3817 3827
2. C. Liu, J.A. Gaspar, H.J. Wong, and E.M. Meiering Conserved and nonconserved features of the folding pathway of hisactophilin, a beta-trefoil protein Protein Sci. 11 2002 669 679
3. R.S. Houliston, C. Liu, L.M. Singh, and E.M. Meiering pH and urea dependence of amide hydrogen-deuterium exchange rates in the beta-trefoil protein hisactophilin Biochemistry 41 2002 1182 1194
4. 15N NMR titration studies of hisactophilin Biochem. Cell Biol. 76 1998 294 301
5. P. Varley, A.M. Gronenborn, H. Christensen, P.T. Wingfield, R.H. Pain, and G.M. Clore Kinetics of folding of the all-beta sheet protein interleukin-1beta Science 260 1993 1110 1113
6. D.K. Heidary, L.A. Gross, M. Roy, and P.A. Jennings Evidence for an obligatory intermediate in the folding of interleukin-1 beta Nature Struct Biol. 4 1997 725 731
7. J.M. Finke, M. Roy, B.H. Zimm, and P.A. Jennings Aggregation events occur prior to stable intermediate formation during refolding of interleukin-1beta Biochemistry 39 2000 575 583
8. J.M. Finke, and P.A. Jennings Interleukin-1 beta folding between pH 5 and 7: experimental evidence for three-state folding behavior and robust transition state positions late in folding Biochemistry 41 2002 15056 15067
9. M. Roy, and P.A. Jennings Real-time NMR kinetic studies provide global and residue-specific information on the non-cooperative unfolding of the beta-trefoil protein, interleukin-1beta J. Mol. Biol. 328 2003 693 703
10. S.R. Brych, S.I. Blaber, T.M. Logan, and M. Blaber Structure and stability effects of mutations designed to increase the primary sequence symmetry within the core region of a beta-trefoil Protein Sci. 10 2001 2587 2599
11. J. Kim, S.R. Brych, J. Lee, T.M. Logan, and M. Blaber Identification of a key structural element for protein folding within beta-hairpin turns J. Mol. Biol. 328 2003 951 961
12. S.I. Blaber, J.F. Culajay, A. Khurana, and M. Blaber Reversible thermal denaturation of human FGF-1 induced by low concentrations of guanidine hydrochloride Biophys. J. 77 1999 470 477
13. D. Samuel, T.K. Kumar, K. Balamurugan, W.Y. Lin, D.H. Chin, and C. Yu Structural events during the refolding of an all beta-sheet protein J. Biol. Chem. 276 2001 4134 4141
14. Y. Chi, T.K. Kumar, H.M. Wang, M.C. Ho, I.M. Chiu, and C. Yu Thermodynamic characterization of the human acidic fibroblast growth factor: evidence for cold denaturation Biochemistry 40 2001 7746 7753
15. Y.H. Chi, T.K. Kumar, K.M. Kathir, D.H. Lin, G. Zhu, I.M. Chiu, and C. Yu Investigation of the structural stability of the human acidic fibroblast growth factor by hydrogen-deuterium exchange Biochemistry 41 2002 15350 15359
16. J.M. Sanz, M.A. Jimenez, and G. Gimenez-Gallego Hints of nonhierarchical folding of acidic fibroblast growth factor Biochemistry 41 2002 1923 1933
17. D. Estape, and U. Rinas Folding kinetics of the all-beta-sheet protein human basic fibroblast growth factor, a structural homolog of interleukin-1beta J. Biol. Chem. 274 1999 34083 34088
18. T. Schindler, and F.X. Schmid Thermodynamic properties of an extremely rapid protein folding reaction Biochemistry 35 1996 16833 16842
19. Y.J. Tan, M. Oliveberg, and A.R. Fersht Titration properties and thermodynamics of the transition state for folding: comparison of two-state and multi-state folding pathways J. Mol. Biol. 264 1996 377 389
20. M.L. Scalley, and D. Baker Protein folding kinetics exhibit an Arrhenius temperature dependence when corrected for the temperature dependence of protein stability Proc. Natl Acad. Sci. USA 94 1997 10636 10640
21. B. Kuhlman, J.A. Boice, R. Fairman, and D.P. Raleigh Structure and stability of the N-terminal domain of the ribosomal protein L9: evidence for rapid two-state folding Biochemistry 37 1998 1025 1032
22. F. Chiti, N. Taddei, N.A. van Nuland, F. Magherini, M. Stefani, G. Ramponi, and C.M. Dobson Structural characterization of the transition state for folding of muscle acylphosphatase J. Mol. Biol. 283 1998 893 903
23. D. Perl, M. Jacob, M. Bano, M. Stupak, M. Antalik, and F.X. Schmid Thermodynamics of a diffusional protein folding reaction Biophys. Chem. 96 2002 173 190
24. P.A. Dalby, J. Clarke, C.M. Johnson, and A.R. Fersht Folding intermediates of wild-type and mutants of barnase. II. Correlation of changes in equilibrium amide exchange kinetics with the population of the folding intermediate J. Mol. Biol. 276 1998 647 656
25. P.A. Dalby, M. Oliveberg, and A.R. Fersht Movement of the intermediate and rate determining transition state of barnase on the energy landscape with changing temperature Biochemistry 37 1998 4674 4679
26. M.J. Parker, M. Lorch, R.B. Sessions, and A.R. Clarke Thermodynamic properties of transient intermediates and transition states in the folding of two contrasting protein structures Biochemistry 37 1998 2538 2545
27. B. Ibarra-Molero, G.I. Makhatadze, and C.R. Matthews Mapping the energy surface for the folding reaction of the coiled-coil peptide GCN4-p1 Biochemistry 40 2001 719 731
28. L.M. Gloss, and C.R. Matthews The barriers in the bimolecular and unimolecular folding reactions of the dimeric core domain of Escherichia coli Trp repressor are dominated by enthalpic contributions Biochemistry 37 1998 16000 16010
29. J. Prieto, M. Wilmans, M.A. Jimenez, M. Rico, and L. Serrano Non-native local interactions in protein folding and stability: introducing a helical tendency in the all beta-sheet alpha-spectrin SH3 domain J. Mol. Biol. 268 1997 760 778
30. M. Silow, and M. Oliveberg High-energy channeling in protein folding Biochemistry 36 1997 7633 7637
31. M. Oliveberg, Y.J. Tan, M. Silow, and A.R. Fersht The changing nature of the protein folding transition state: implications for the shape of the free-energy profile for folding J. Mol. Biol. 277 1998 933 943
32. J.W. Schymkowitz, F. Rousseau, L.R. Irvine, and L.S. Itzhaki The folding pathway of the cell-cycle regulatory protein p13suc1: clues for the mechanism of domain swapping Struct. Fold. Des. 8 2000 89 100
33. R.L. Isaacson, A.G. Weeds, and A.R. Fersht Equilibria and kinetics of folding of gelsolin domain 2 and mutants involved in familial amyloidosis-Finnish type Proc. Natl Acad. Sci. USA 96 1999 11247 11252
34. T. Pascher Temperature and driving force dependence of the folding rate of reduced horse heart cytochrome c Biochemistry 40 2001 5812 5820
35. C. Tanford Protein denaturation. Theoretical models for the mechanism of denaturation Advan. Protein Chem. 24 1970 1 95
36. C.N. Pace Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280
37. Y. Nozaki, and C. Tanford The solubility of amino acids and related compounds in aqueous urea solutions J. Biol. Chem. 238 1963 4074 4081
38. D.R. Robinson, and W.P. Jencks The effect of compounds of the urea-guanidinium class on the activity coefficient of acetyltetraglycine ethyl ester and related compounds J. Am. Chem. Soc. 87 1965 2462 2470
39. C.M. Johnson, and A.R. Fersht Protein stability as a function of denaturant concentration: the thermal stability of barnase in the presence of urea Biochemistry 34 1995 6795 6804
40. V.V. Filimonov, A.I. Azuaga, A.R. Viguera, L. Serrano, and P.L. Mateo A thermodynamic analysis of a family of small globular proteins: SH3 domains Biophys. Chem. 77 1999 195 208
41. G.I. Makhatadze, and P.L. Privalov Protein interactions with urea and guanidinium chloride. A calorimetric study J. Mol. Biol. 226 1992 491 505
42. D.J. Felitsky, and M.T. Record Jr Thermal and urea-induced unfolding of the marginally stable lac repressor DNA-binding domain: a model system for analysis of solute effects on protein processes Biochemistry 42 2003 2202 2217
43. M.E. Zweifel, and D. Barrick Relationships between the temperature dependence of solvent denaturation and the denaturant dependence of protein stability curves Biophys. Chem. 101-102 2002 221 237
44. E.M. Nicholson, and J.M. Scholtz Conformational stability of the Escherichia coli HPr protein: test of the linear extrapolation method and a thermodynamic characterization of cold denaturation Biochemistry 35 1996 11369 11378
45. E.R. Main, K.F. Fulton, and S.E. Jackson Folding pathway of FKBP12 and characterisation of the transition state J. Mol. Biol. 291 1999 429 444
46. J.K. Myers, C.N. Pace, and J.M. Scholtz Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
47. G.T. DeKoster, and A.D. Robertson Calorimetrically-derived parameters for protein interactions with urea and guanidine-HCl are not consistent with denaturant m values Biophys. Chem. 64 1997 59 68
48. J.A. Schellman, and N.C. Gassner The enthalpy of transfer of unfolded proteins into solutions of urea and guanidinium chloride Biophys. Chem. 59 1996 259 275
49. J.A. Schellman Fifty years of solvent denaturation Biophys. Chem. 96 2002 91 101
50. I.E. Sanchez, and T. Kiefhaber Hammond behavior versus ground state effects in protein folding: evidence for narrow free energy barriers and residual structure in unfolded states J. Mol. Biol. 327 2003 867 884
51. J. Clarke, and L.S. Itzhaki Hydrogen exchange and protein folding Curr. Opin. Struct. Biol. 8 1998 112 118
52. G. Spudich, and S. Marqusee A change in the apparent m value reveals a populated intermediate under equilibrium conditions in Escherichia coli ribonuclease HI Biochemistry 39 2000 11677 11683
53. S.E. Jackson How do small single-domain proteins fold? Fold. Des. 3 1998 R81 R91
54. I.E. Sanchez, and T. Kiefhaber Non-linear rate-equilibrium free energy relationships and Hammond behavior in protein folding Biophys. Chem. 100 2003 397 407
55. I.E. Sanchez, and T. Kiefhaber Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding J. Mol. Biol. 325 2003 367 376
56. A.R. Fersht Structure and Mechanism in Protein Science 1999 W.H. Freeman and Company New York
57. R. Day, B.J. Bennion, S. Ham, and V. Daggett Increasing temperature accelerates protein unfolding without changing the pathway of unfolding J. Mol. Biol. 322 2002 189 203
58. V. Daggett Molecular dynamics simulations of the protein unfolding/folding reaction Accts. Chem. Res. 35 2002 422 429
59. A. Bachmann, and T. Kiefhaber Apparent two-state tendamistat folding is a sequential process along a defined route J. Mol. Biol. 306 2001 375 386
60. S.S. Plotkin, and J.N. Onuchic Understanding protein folding with energy landscape theory. Part I: Basic concepts Quart. Rev. Biophys. 35 2002 111 167
61. S.S. Plotkin, and J.N. Onuchic Understanding protein folding with energy landscape theory. Part II: Quantitative aspects Quart. Rev. Biophys. 35 2002 205 286
62. M. Jacob, and F.X. Schmid Protein folding as a diffusional process Biochemistry 38 1999 13773 13779
63. D. Samuel, T.K. Kumar, T. Srimathi, H. Hsieh, and C. Yu Identification and characterization of an equilibrium intermediate in the unfolding pathway of an all beta-barrel protein J. Biol. Chem. 275 2000 34968 34975
64. J.A. Schellman The thermodynamic stability of proteins Annu. Rev. Biophys. Biophys. Chem. 16 1987 115 137
65. B.L. Chen, W.A. Baase, and J.A. Schellman Low-temperature unfolding of a mutant of phage T4 lysozyme. 2. Kinetic investigations Biochemistry 28 1989 691 699
66. D. Perrin, and B. Dempsey Buffers for pH and Metal Ion Control 1974 Chapman and Hall London
67. O.V. Tsodikov, M.T. Record Jr, and Y.V. Sergeev Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature J. Comput. Chem. 23 2002 600 609
68. T.P. Creamer, R. Srinivasan, and G.D. Rose Modeling unfolded states of proteins and peptides. II. Backbone solvent accessibility Biochemistry 36 1997 2832 2835
69. J. Taylor An Introduction to Error Analysis: The Study of Uncertainties in Physical Measurements 2nd edit. 1997 University Science Books Sausalito
70. J.C. Martinez, and L. Serrano The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved Nature Struct. Biol. 6 1999 1010 1016
71. E.S. Cobos, V.V. Filimonov, M.C. Vega, P.L. Mateo, L. Serrano, and J.C. Martinez A thermodynamic and kinetic analysis of the folding pathway of an SH3 domain entropically stabilised by a redesigned hydrophobic core J. Mol. Biol. 328 2003 221 233
72. H.M. Rodriguez, D.M. Vu, and L.M. Gregoret Role of a solvent-exposed aromatic cluster in the folding of Escherichia coli CspA Protein Sci. 9 2000 1993 2000
73. C.T. Friel, A.P. Capaldi, and S.E. Radford 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
74. E.M. Nicholson, R.W. Peterson, and J.M. Scholtz A partially buried site in homologous HPr proteins is not optimized for stability J. Mol. Biol. 321 2002 355 362
75. E. Cota, S.J. Hamill, S.B. Fowler, and J. Clarke Two proteins with the same structure respond very differently to mutation: the role of plasticity in protein stability J. Mol. Biol. 302 2000 713 725
76. S.J. Hamill, A.E. Meekhof, and J. Clarke The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin Biochemistry 37 1998 8071 8079
77. F. Chiti, N. Taddei, P.M. White, M. Bucciantini, F. Magherini, M. Stefani, and C.M. Dobson Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding Nature Struct. Biol. 6 1999 1005 1009
78. A. Giletto, and C.N. Pace Buried, charged, non-ion-paired aspartic acid 76 contributes favorably to the conformational stability of ribonuclease T1 Biochemistry 38 1999 13379 13384
79. G.R. Grimsley, K.L. Shaw, L.R. Fee, R.W. Alston, B.M. Huyghues-Despointes, and R.L. Thurlkill Increasing protein stability by altering long-range Coulombic interactions Protein Sci. 8 1999 1843 1849
80. 1 Biochemistry 37 1998 16192 16200
81. J.K. Myers, C.N. Pace, and J.M. Scholtz Helix propensities are identical in proteins and peptides Biochemistry 36 1997 10923 10929
82. 1 Biochemistry 31 1992 725 732
83. A.K. Srivastava, and R.T. Sauer Mutational studies of protein stability and folding of the hyperstable MYL Arc repressor variant Biophys. Chem. 101-102 2002 35 42
84. A.K. Srivastava, and R.T. Sauer Evidence for partial secondary structure formation in the transition state for arc repressor refolding and dimerization Biochemistry 39 2000 8308 8314
85. E.R. Main, K.F. Fulton, and S.E. Jackson Context-dependent nature of destabilizing mutations on the stability of FKBP12 Biochemistry 37 1998 6145 6153
86. S.E. Choe, L. Li, P.T. Matsudaira, G. Wagner, and E.I. Shakhnovich Differential stabilization of two hydrophobic cores in the transition state of the villin 14T folding reaction J. Mol. Biol. 304 2000 99 115
87. K. Julenius, E. Thulin, S. Linse, and B.E. Finn Hydrophobic core substitutions in calbindin D9k: effects on stability and structure Biochemistry 37 1998 8915 8925
88. G.I. Makhatadze, V.V. Loladze, D.N. Ermolenko, X. Chen, and S.T. Thomas Contribution of surface salt bridges to protein stability: guidelines for protein engineering J. Mol. Biol. 327 2003 1135 1148
89. V.V. Loladze, B. Ibarra-Molero, J.M. Sanchez-Ruiz, and G.I. Makhatadze Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface Biochemistry 38 1999 16419 16423
90. V. Villegas, J.C. Martinez, F.X. Aviles, and L. Serrano Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain J. Mol. Biol. 283 1998 1027 1036
91. D.P. Smith, S. Jones, L.C. Serpell, M. Sunde, and S.E. Radford A systematic investigation into the effect of protein destabilisation on beta 2-microglobulin amyloid formation J. Mol. Biol. 330 2003 943 954
92. J.M. Matthews, and A.R. Fersht Exploring the energy surface of protein folding by structure-reactivity relationships and engineered proteins: observation of Hammond behavior for the gross structure of the transition state and anti-Hammond behavior for structural elements for unfolding/folding of barnase Biochemistry 34 1995 6805 6814
93. J.M. Sanz, and A.R. Fersht Rationally designing the accumulation of a folding intermediate of barnase by protein engineering Biochemistry 32 1993 13584 13592
94. 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
95. L. Serrano, J.T. Kellis Jr, P. Cann, A. Matouschek, and A.R. Fersht The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability J. Mol. Biol. 224 1992 783 804
96. M. Tanaka, Y. Machida, Y. Nishikawa, T. Akagi, I. Morishima, and T. Hashikawa The effects of aggregation-inducing motifs on amyloid formation of model proteins related to neurodegenerative diseases Biochemistry 41 2002 10277 10286
97. M.P. Irun, S. Maldonado, and J. Sancho Stabilization of apoflavodoxin by replacing hydrogen-bonded charged Asp or Glu residues by the neutral isosteric Asn or Gln Protein Eng. 14 2001 173 181
98. K.S. Tang, A.R. Fersht, and L.S. Itzhaki Sequential unfolding of ankyrin repeats in tumor suppressor p16 Structure (Camb) 11 2003 67 73