Thermodynamic mechanism and consequences of the polyproline II (P II) structural bias in the denatured states of proteins

Biochemistry

Volumn 43, Issue 30, 2004, Pages 9790-9799

  Hamburger, James B ^a   Ferreon, Josephine C ^a   Whitten, Steven T ^a   Hilser, Vincent J ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALORIMETRY; CONFORMATIONS; ENTHALPY; ENTROPY; PROTEINS; THERMODYNAMICS; TITRATION;

DENATURED PROTEINS; MOLECULAR LEVELS; PEPTIDES;

BIOCHEMISTRY;

POLYPROLINE II; PROLINE; UNCLASSIFIED DRUG;

ARTICLE; CALORIMETRY; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS; THERMODYNAMICS;

ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; CALORIMETRY; ENTROPY; MODELS, CHEMICAL; MODELS, MOLECULAR; OLIGOPEPTIDES; PEPTIDES; PROBABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; SON OF SEVENLESS PROTEINS; THERMODYNAMICS;

EID: 2942712684     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049352z     Document Type: Article

References (74)

1. Levinthal, C. (1969) How to fold graciously. Mossbauer spectroscopy in biological systems, Proc. Univ. Illinois Bull. 41, 22-24.
2. Kataoka, M., Nishii, I., Fujisawa, T., Ueki, T., Tokunaga, F., and Goto, Y. (1995) Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering, J. Mol. Biol. 249, 215-228.
3. Wong, K. B., Clarke, J., Bond, C. J., Neira, J. L., Freund. S. M., Fersht, A. R., and Daggett, V. (2000) Towards a complete description of the structural and dynamic properties of the denatured state of barnase and the role of residual structure in folding, J. Mol. Biol. 296, 1257-1282.
4. 13C NMR assignment and characterisation of residual structure, J. Mol. Biol. 259, 805-818.
5. Schwalbe, H., Fiebig, K. M., Buck, M., Jones, J. A., Grimshaw, S. B., Spencer, A., Glaser, S. J., Smith, L. J., and Dobson, C. M. (1997) Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea, Biochemistry 36, 8977-8991.
6. Gillespie, J. R., and Shortle, D. (1997) Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels, J. Mol. Biol. 268, 158-169.
7. Penkett, C. J., Redfield, C., Jones, J. A., Dodd, I., Hubbard, J., Smith, R. A., Smith, L. J., and Dobson, C. M. (1998) Structural and dynamical characterization of a biologically active unfolded fibronectin-binding protein from Staphylococcus aureus, Biochemistry 37, 17054-17067.
8. Bond, C. J., Wong, K. B., Clarke, J., Fersht, A. R., and Daggett, V. (1997) Characterization of residual structure in the thermally denatured state of barnase by simulation and experiment: Description of the folding pathway, Proc. Natl. Acad. Sci. U.S.A. 94, 13409-13413.
9. Zhang, O., and Forman-Kay, J. D. (1997) NMR studies of unfolded states of an SH3 domain in aqueous solution and denaturing conditions, Biochemistry 36, 3959-3970.
10. Zhang, O., Forman-Kay, J. D., Shortle, D., and Kay, L. E. (1997) Triple-resonance NOESY-based experiments with improved spectral resolution: Applications to structural characterization of unfolded, partially folded, and folded proteins, J. Biomol. NMR 9, 181-200.
11. Sreerama, N., and Woody, R. W. (1999) Molecular dynamics simulations of polypeptide conformations in water: A comparison of α, β, and poly(pro)II conformations, Proteins 36, 400-406.
12. Krimm, S., and Tiffany, M. L. (1974) The circular dichroism spectrum and structure of unordered polypeptides and proteins, lsr. J. Chem. 40, 14376-14383.
13. Woody, R. W. (1992) Circular dichroism and conformation of unordered polypeptides, Adv. Biophys. Chem. 2, 37-79.
14. Tiffany, M. L., and Krimm, S. (1972) Effect of temperature on the circular dichroism spectra of polypeptides in the extended state, Biopolymers 11, 2309-2316.
15. Tiffany, M. L., and Krimm, S. (1968) New chain conformations of poly(glutamic acid) and polylysine, Biopolymers 6, 1379-1382.
16. Drake, A. F., Siligardi, G., and Gibbons, W. A. (1988) Reassessment of the electronic circular dichroism criteria for random coil conformations of poly(L-lysine) and the implications for protein folding and denaturation studies, Biophys. Chem. 31, 143-146.
17. Dukor, R. K., and Keiderling, T. A. (1991) Reassessment of the random coil conformation: Vibrational CD study of proline oligopeptides and related polypeptides, Biopolymers 31, 1747-1761.
18. II conformations in the calculation of peptide fractional helix content, Protein Sci. 6, 1694-1700.
19. II conformation. J. Am. Chem. Soc 125, 8092-8093.
20. Pappu, R. V., and Rose, G. D. (2002) A simple model for polyproline II structure in unfolded states of alanine-based peptides, Protein Sci. 11, 2437-2455.
21. Wilson, G., and Hecht, L. A. B. L. D. (1996) Residual structure in unfolded proteins revealed by Raman optical activity, Biochemistry 35, 12518-12525.
22. Vila, J. A., Baldoni, H. A., Ripoll, D. R., Ghosh, A., and Scheraga, H. A. (2004) Polyproline II helix conformation in a proline-rich environment: A theoretical study, Biophys. J. 86, 731-742.
23. Shi, Z., Olson, C. A., Rose, G. D., Baldwin, R. L., and Kallenbach, N. R. (2002) Polyproline II structure in a sequence of seven alanine residues, Proc. Natl. Acad. Sci. U.S.A. 99, 9190-9195.
24. Ferreon, J. C., and Hilser, V. J. (2003) The effect of the polyproline II (PPII) conformation on the denatured state entropy, Protein Sci. 12, 447-457.
25. Rucker, A. L., and Creamer, T. P. (2002) Polyproline II helical structure in protein unfolded states: Lysine peptides revisited, Protein Sci. 11, 980-985.
26. Chellgren, B. W., and Creamer, T. P. (2004) Short sequences of non-proline residues can adopt the polyproline II helical conformation, Biochemistry 43, 5864-5869.
27. Han, W.-G., Jalkanen, K. J., Elstner, M., and Suhai, S. (1998) Theoretical study of aqueous N-acetyl-L-alanine N′-methylamide: Structures and Raman, VCD, and ROA spectra, J. Phys. Chem. B 102, 2587-2602.
28. Eker, F., Griebenow, K., and Schweitzer-Stenner, R. (2003) Stable conformations of tripeptides in aqueous solution studied by UV circular dichroism spectroscopy, J. Am. Chem. Soc. 125, 8178-8185.
29. Eker, F., Cao, X., Nafie, L., and Schweitzer-Stenner, R. (2002) Tripeptides adopt stable structures in water. A combined polarized visible Raman, FTIR, and VCD spectroscopy study, J. Am. Chem. Soc. 124, 14330-14341.
30. Weise, C. F., and Weisshaar, J. C. (2003) Conformational analysis of alanine dipeptide from dipolar couplings in a water-based liquid crystal, J. Phys. Chem. B 107, 3265-3277.
31. Hinderaker, M. P., and Raines, R. T. (2003) An electronic effect on protein structure, Protein Sci. 12, 1188-1194.
32. Creamer, T. P. (1998) Left-handed polyproline II helix formation is (very) locally driven, Proteins 33, 218-226.
33. Lim, W. A., Richards, F. M., and Fox, R. O. (1994) Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains, Nature 372, 375-379.
34. D'Aquino, J. A., Gomez, J., Hilser, V. J., Lee, K. H., Amzel, L. M., and Freire, E. (1996) The magnitude of the backbone conformational entropy change in protein folding, Proteins 25, 143-156.
35. Smith, C. K., Bu, Z., Anderson, K. S., Sturtevant, J. M., Engelman, D. M., and Regan, L. (1996) Surface point mutations that significantly alter the structure and stability of a protein's denatured state, Protein Sci. 5, 2009-2019.
36. Drozdov, A. N., Grossfield, A., and Pappu, R. V. (2004) Role of solvent in determining conformational preferences of alanine dipeptide in water, J. Am. Chem. Soc. 126, 2574-2581.
37. 15N backbone dynamics of the S-peptide from ribonuclease A in its free and S-protein bound forms: Toward a site-specific analysis of entropy changes upon folding, Protein Sci. 7, 389-402.
38. Kelly, M. A., Chellgren, B. W., Rucker, A. L., Troutman, J. M., Fried, M. G., Miller, A. F., and Creamer, T. P. (2001) Host-guest study of left-handed polyproline II helix formation, Biochemistry 40, 14376-14383.
39. Myers, J. K., Pace. C. N., and Scholtz, J. M. (1995) Denaturant in values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
40. Freire, E. (1995) Differential scanning calorimetry, Methods Mol. Biol. 40, 191-218.
41. Gomez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins, Proteins 22, 404-412.
42. Freire, E. (1995) Thermal denaturation methods in the study of protein folding, Methods Enaymol. 259, 144-168.
43. Biltonen, R. L., and Freire, E. (1978) Thermodynamic characterization of conformational states of biological macromolecules using differential scanning calorimetry, CRC Crit. Rev. Biochem. 5, 85-124.
44. Murphy, K. P., and Freire, E. (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins, Adv. Protein Chem. 43, 313-361.
45. Makhatadze, G. I. (1998) Heat capacities of amino acids, peptides, and proteins, Biophys. Chem. 71, 133-156.
46. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA, Science 263, 777-784.
47. Dill, K. A., and Chan, H. S. (1997) From Levinthal to pathways to funnels, Nat. Struct. Biol. 4, 10-19.
48. Freire, E. (1995) Thermodynamics of partly folded intermediates in proteins, Annu. Rev. Biophys. Biomol. Struct. 24, 141-165.
49. Ferguson, N., and Fersht, A. R. (2003) Early events in protein folding, Curr. Opin. Struct. Biol. 13, 75-81.
50. Sreerama, N., and Woody, R. W. (1994) Poly(pro)II helices in globular proteins: Identification and circular dichroic analysis, Biochemistry 33, 10022-10025.
51. Swint, L., and Robertson, A. D. (1993) Thermodynamics of unfolding for turkey ovomucoid third domain: Thermal and chemical denaturation, Protein Sci. 2, 2037-2049.
52. O'Neil, K. T., Hoess, R. H., Raleigh, D. P., and DeGrado, W. F. (1995) Thermodynamic genetics of the folding of the B1 immunoglobulin-binding domain from streptococcal protein G, Proteins 21, 11-21.
53. Viguera, A. R., Martinez, J. C., Filimonov, V. V., Mateo, P. L., and Serrano, L. (1994) Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition, Biochemistry 33, 2142-2150.
54. Jackson, S. E., Moracci, M., elMasry, N., Johnson, C. M., and Fersht, A. R. (1993) Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2, Biochemistry 32. 11259-11269.
55. Knapp, S., Mattson, P. T., Christova, P., Berndt, K. D., Karshikoff, A., Vihinen, M., Smith, C. I., and Ladenstein, R. (1998) Thermal unfolding of small proteins with SH3 domain folding pattern, Proteins 31, 309-319.
56. Huang, G. S., and Oas, T. G. (1996) Heat and cold denatured states of monomeric λ repressor are thermodynamically and conformationally equivalent, Biochemistry 35, 6173-6180.
57. Nicholson, E. M., and Scholtz, J. M. (1996) Conformational stability of the Escherichia coli HPr protein: Test of the linear extrapolation method and a thermodynamic characterization of cold denaturation, Biochemistry 35, 11369-11378.
58. Scholtz, J. M. (1995) Conformational stability of HPr: The histidine-containing phosphocarrier protein from Bacillus subtilis, Protein Sci. 4, 35-43.
59. Agashe, V. R., and Udgaonkar, J. B. (1995) Thermodynamics of denaturation of barstar: Evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride, Biochemistry 34, 3286-3299.
60. Pace, C. N., Hebert, E. J., Shaw, K. L., Schell, D., Both, V., Krajcikova, D., Sevcik, J., Wilson, K. S., Dauter, Z., Hartley, R. W., and Grimsley, G. R. (1998) Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2, and Sa3, J. Mol. Biol. 279, 271-286.
61. Privalov, P. L., and Gill, S. J. (1988) Stability of protein structure and hydrophobic interaction, Adv. Protein Chem. 39, 191-234.
62. Yu, Y., Makhatadze, G. I., Pace, C. N., and Privalov, P. L. (1994) Energetics of ribonuclease T1 structure, Biochemistry 33, 3312-3319.
63. Bowie, J. U., and Sauer, R. T. (1989) Equilibrium dissociation and unfolding of the Arc repressor dimer, Biochemistry 28, 7139-7143.
64. Cohen, D. S., and Pielak, G. J. (1994) Stability of yeast iso-1-ferricytochrome c as a function of pH and temperature, Protein Sci. 3, 1253-1260.
65. Santoro, M. M., and Bolen, D. W. (1992) A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range, Biochemistry 31, 4901-4907.
66. Protasevich, I. I., Platonov, A. L., Pavlovsky, A. G., and Esipova, N. G. (1987) Distribution of charges in Bacillus intermedius 7P ribonuclease determines the number of cooperatively melting regions of the globule, J. Biomol. Struct. Dyn. 4, 885-893.
67. Griko, Y. V., Makhatadze, G. I., Privalov, P. L., and Hartley, R. W. (1994) Thermodynamics of barnase unfolding, Protein Sci. 3, 669-676.
68. Munson, M., O'Brien, R., Sturtevant, J. M., and Regan, L. (1994) Redesigning the hydrophobic core of a four-helix-bundle protein, Protein Sci. 3, 2015-2022.
69. Herning, T., Yutani, K., Inaka, K., Kuroki, R., Matsushima, M., and Kikuchi, M. (1992) Role of proline residues in human lysozyme stability: A scanning calorimetric study combined with X-ray structure analysis of proline mutants, Biochemistry 31, 7077-7085.
70. Carra, J. H., Anderson, E. A., and Privalov, P. L. (1994) Thermodynamics of staphylococcal nuclease denaturation. I. The acid-denatured state, Protein Sci. 3, 944-951.
71. Makhatadze, G. I., Clore, G. M., Gronenborn, A. M., and Privalov, P. L. (1994) Thermodynamics of unfolding of the all β-sheet protein interleukin-1 β, Biochemistry 33, 9327-9332.
72. Kelly, L., and Holladay, L. A. (1990) A comparative study of the unfolding thermodynamics of vertebrate metmyoglobins, Biochemistry 29, 5062-5069.
73. Hu, C. Q., Kitamura, S., Tanaka, A., and Sturtevant, J. M. (1992) Differential scanning calorimetric study of the thermal unfolding of mutant forms of phage T4 lysozyme, Biochemistry 31, 1643-1647.
74. Stackhouse, T. M., Onuffer, J. J., Matthews, C. R., Ahmed, S. A., and Miles, E. W. (1988) Folding of homologous proteins: Conservation of the folding mechanism of the α subunit of tryptophan synthase from Escherichia coli, Salmonella typhimurium, and five interspecies hybrids, Biochemistry 27, 824-832.