Reconciling observations of sequence-specific conformational propensities with the generic polymeric behavior of denatured proteins

Biochemistry

Volumn 44, Issue 34, 2005, Pages 11369-11380

  Tran, Hoang T ^a   Wang, Xiaoling ^a   Pappu, Rohit V ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COMPUTER SIMULATION; CONFORMATIONS; POLYMERS; POLYPEPTIDES; SET THEORY; SPECTROSCOPIC ANALYSIS;

CHAIN LENGTH; DENATURED PROTEINS; GYRATION; STERIC OVERLAP;

PROTEINS;

AMINO ACID; PEPTIDE; POLYMER; SOLVENT;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CALCULATION; ENTROPY; OBSERVATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; SIMULATION; STEREOCHEMISTRY;

AMINO ACID SEQUENCE; DIPEPTIDES; MODELS, THEORETICAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEINS; REPRODUCIBILITY OF RESULTS;

EID: 23944453852     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050196l     Document Type: Article

References (100)

1. Kauzmann, W. (1959) Some factors in the interpretation of protein denaturation, Adv. Protein Chem. 14, 1-63.
2. Tanford, C. (1968) Protein denaturation, Adv. Protein Chem. 23, 121-282.
3. Tanford, C. (1970) Protein denaturation: Part C. Theoretical models for the mechanism of denaturation, Adv. Protein Chem. 24, 1-95.
4. Dill, K. A., and Shortle, D. (1991) Denatured states of proteins, Annu. Rev. Biochem. 60, 795-825.
5. Shortle, D., and Ackerman, M. S. (2001) Persistence of native-like topology in a denatured protein in 8M urea, Science 293, 487-489.
6. Hodsdon, M. E., and Frieden, C. (2001) Intestinal fatty acid binding protein: The folding mechanism as determined by NMR studies, Biochemistry 40, 732-742.
7. van Gunsteren, W. F., Burgi, R., Peter, C., and Daura, X. (2001) The key to solving the protein-folding problem lies in an accurate description of the denatured state, Angew. Chem., Int. Ed. Engl. 40, 351-355.
8. Klein-Seetharaman, J., Oikawa, M., Grimshaw, S. B., Wirmer, J., Duchardt, E., Ueda, T., Imoto, T., Smith, L. J., Dobson, C. M., and Schwalbe, H. (2002) Long-range interactions within a nonnative protein, Science 295, 1719-1722.
9. Shortle, D. (2002) The expanded denatured state: An ensemble of conformations trapped in a locally encoded topological space, Adv. Protein Chem. 62, 1-23.
10. Dyson, H. J., and Wright, P. E. (2002) Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance, Adv. Protein Chem. 62, 311-340.
11. Myers, J. M., and Oas, T. G. (2002) Mechanism of fast protein folding, Annu. Rev. Biochem. 71, 783-815.
12. Zagrovic, B., and Pande, V. S. (2003) Structural correspondence between the α-helix and the random-flight chain resolves how unfolded proteins can have nativelike properties, Nat. Struct. Biol. 10, 955-961.
13. Mohana-Borges, R., Goto, N. K., Kroon, G. J. A., Dyson, H. J., and Wright, P. E. (2004) Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings, J. Mol. Biol. 340, 1131-1142.
14. Uversky, V. N., and Fink, A. L. (2004) Conformational constraints for amyloid formation: the importance of being unfolded, Biochim. Biophys. Acta 1698, 131-153.
15. Minton, A. P. (2000) Implications of macromolecular crowding for protein assembly, Curr. Opin. Struct. Biol. 10, 13-15.
16. Ghaemmaghami, S., and Oas, T. G. (2001) Quantitative protein stability measurement in vivo, Nat. Struct. Biol. 8, 879-882.
17. Dedmon, M. M., Patel, C. N., Young, G. B., and Pielak, G. J. (2002) FlgM gains structure in living cells, Proc. Natl. Acad. Sci. U.S.A. 99, 12681-12684.
18. Plaxco, K. W., and Gross, M. (1997) The importance of being unfolded, Nature 386, 657.
19. Wright, P. E., and Dyson, H. J. (1999) Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm, J. Mol. Biol. 293, 321-331.
20. Dunker, A. K., Brown, C. J., and Obradovic, Z. (2002) Identification and functions of usefully disordered proteins, Adv. Protein Chem. 62, 25-49.
21. Uversky, V. N. (2002) Natively unfolded proteins: A point where biology waits for physics, Protein Sci. 11, 739-756.
22. Rose, G. D. (2002) Getting to know U, Adv. Protein Chem. 62, xv-xxi.
23. Baldwin, R. L. (2002) A new perspective on unfolded proteins, Adv. Protein Chem. 62, 361-366.
24. Doniach, S. (2001) Changes in biomolecular conformation seen by small-angle X-ray scattering, Chem. Rev. 101, 1763-1778.
25. Millett, I. S., Doniach, S., and Plaxco, K. W. (2002) Toward a taxonomy of the denatured state: Small angle scattering studies of unfolded proteins, Adv. Protein Chem. 62, 241-262.
26. Kohn, J. E., Millett, I. S., Jacob, J., Zagrovic, B., Dillon, T. M., Cingel, N., Dothager, R. S., Seifert, S., Thiyagarajan, P., Sosnick, T. R., Hasan, M. Z., Pande, V. S., Ruczinski, I., Doniach, S., and Plaxco, K. W. (2004) Random-coil behavior and the dimensions of chemically unfolded proteins, Proc. Natl. Acad. Sci. U.S.A. 101, 12491-12496.
27. Woody, R. W. (1992) Circular dichroism of unordered polypeptides, Adv. Biophys. Chem. 2, 37-79.
28. Spector, S., Rosconi, M., and Raleigh, D. P. (1999) Conformational analysis of peptide fragments derived from the peripheral subunit binding domain from the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophillus: Evidence for nonrandom structure in the unfolded state, Biopolymers 49, 29-40.
29. Woutersen, S., and Hamm, P. (2000) Structure determination of trialanine in water using polarization sensitive two-dimensional vibrational spectroscopy, J. Phys. Chem. B 104, 11316-11320.
30. Poon, C.-D., Samulski, E. T., Weise, C. F., and Weishaar, J. C. (2000) Do bridging water molecules dictate the structure of a model dipeptide in aqueous solution?, J. Am. Chem. Soc. 122, 5642-5643.
31. 2O determined by combining FTIR and polarized visible Raman spectroscopy, J. Am. Chem. Soc. 123, 9628-9633.
32. 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.
33. Shi, Z., Woody, R. W., and Kallenbach, N. R. (2002) Is polyproline II a major backbone conformation in unfolded proteins?, Adv. Protein Chem. 62, 163-240.
34. Barron, L. D., Blanch, E. W., and Hecht, L. (2002) Unfolded proteins studied by Raman optical activity, Adv. Protein Chem. 62, 51-90.
35. Keiderling, T. A., and Xu, Q. (2002) Unfolded peptides and proteins studied with infrared absorption and vibrational circular dichroism spectra, Adv. Protein Chem. 62, 111-161.
36. Eker, F., Griebenow, K., and Schweitzer-Stenner, R. (2003) Stable conformations of peptides in solution studied using UV circular dichroism spectroscopy, J. Am. Chem. Soc. 125, 8178-8185.
37. II conformation, J. Am. Chem. Soc. 125, 8092-8093.
38. Ferreon, J. C., and Hilser, V. J. (2003) The effect of polyproline II structure on denatured state entropy, Protein Sci. 12, 447-457.
39. Rucker, A. L., and Creamer, T. P. (2002) Polyproline II helical structure in protein unfolded states: Lysine peptides revisited, Protein Sci. 11, 980-985.
40. Rucker, A. L., Pager, C. T., Campbell, M. N., Qualls, J. E., and Creamer, T. P. (2003) Host-guest scale of left-handed polyproline II helix formation, Proteins: Struct., Funct., Genet. 53, 68-75.
41. Chen, K., Liu, Z. G., and Kallenbach, N. R. (2004) The polyproline II conformation in short alanine peptides is noncooperative, Proc. Natl. Acad. Sci. U.S.A. 101, 15352-15357.
42. 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.
43. Eker, F., Griebenow, K., Cao, X. L., Nafie L. A., and Schweitzer-Stenner, R. (2004) Preferred peptide backbone conformations in the unfolded state revealed by the structure analysis of alanine-based AXA tripeptides in aqueous solution, Proc. Natl. Acad. Sci. U.S.A. 101, 10054-10059.
44. II) helix formation, Biochemistry 43, 7787-7797.
45. Shortle, D. (1996) Structural analysis of non-native states of proteins by NMR, Curr. Opin. Struct. Biol. 6, 24-30.
46. Fieber, W., Kragelund, B. B., Meldal, M., and Poulsen, F. M. (2005) Reversible denaturation of acid-denatured ACBP controlled by helix A4, Biochemistry 44, 1375-1384.
47. Tiffany, M. L., and Krimm, S. (1968) Circular dichroism of poly-L-proline in an unordered conformation, Biopolymers 6, 1767-1770.
48. Tiffany, M. L., and Krimm, S. (1969) Circular dichroism of the "random" polypeptide chain, Biopolymers 8, 347-359.
49. Tiffany, M. L., and Krimm, S. (1973) Extended conformations of polypeptides and proteins in urea and guanidine hydrochloride, Biopolymers 12, 575-587.
50. Krimm, S., and Tiffany, M. L. (1974) The circular dichroism spectrum and structure of unordered polypeptides and proteins, Isr. J. Chem. 12, 189-200.
51. Miller, W. G., and Goebel, C. V. (1968) Dimensions of protein random coils, Biochemistry 7, 3925-3935.
52. II conformation in model alanine peptides, J. Am. Chem. Soc. 126, 15141-15150.
53. Whittington, S. J., Chellgren, B. W., Hermann, V. M., and Creamer, T. P. (2005) Urea promotes polyproline II helix formation: Implications for protein denatured states, Biochemistry 44, 6269-6275.
54. Fleming, P. J., and Rose, G. D. (2005) Conformational properties of unfolded proteins, in Protein folding handbook (Buchner, J., and Kiefhaber, T., Eds.) Vol. 2, Part 1, Chapter 20, pp 710-736, Wiley-VCH, Weinheim.
55. Flory, P. J. (1953) Principles of polymer chemistry, Cornell University Press, Ithaca, NY.
56. Chan, H. S., and Dill, K. A. (1991) Polymer principles in protein structure and stability, Annu. Rev. Biophys. Biophys. Chem. 20, 447-490.
57. Grosberg, A. Y., and Khokhlov, A. R. (1994) Statistical physics of macromolecules, AIP series in polymers and complex materials, AIP Press, New York.
58. Rubenstein, M., and Colby, R. H. (2003) Polymer Physics, Oxford University Press, Oxford.
59. Le Guillou, J. C., and Zinn-Justin, J. (1980) Critical exponents from field theory, Phys. Rev. B 21, 3976-3998.
60. Schäfer, L. (1984) Unified description of temperature and concentration crossover in the excluded volume problem. 1. Osmotic pressure and correlation lengths, Macromolecules 17, 1357-1370.
61. Li, B., Madras, N., and Sokal, A. D. (1995) Critical exponents, hyperscaling and universal amplitude ratios for two- and three-dimensional self-avoiding walks, J. Stat. Phys. 80, 661-754.
62. Schäfer, L. (1999) Excluded volume effects in polymer solutions as explained by the renormalization group, Springer, Berlin.
63. deGennes, P.-G. (1979) Scaling concepts in polymer physics, Cornell University Press, Ithaca and London.
64. Flory, P. J. (1969) Statistical mechanics of chain molecules, Chapter 7, Hanser Publishers, Munich.
65. Richards, F. M. (1977) Areas, volumes, packing and protein structure, Annu. Rev. Biophys. Bioeng. 6, 151-176.
66. 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.
67. Hoover, W. G., Gray, S. G., and Johnson, K. W. (1971) Thermodynamic properties of the fluid and solid phases for inverse power potentials, J. Chem. Phys. 55, 1128-1136.
68. Hopfinger, A. J. (1973) Conformational properties of macromolecules, Academic Press, New York.
69. Pauling, L. (1970) Chapter 11, in General Chemistry, 3rd ed., W. H. Freeman Press, San Francisco, CA.
70. Slater, J. C., and Kirkwood, J. G. (1931) The van der Waals forces in gases, Phys. Rev. 37, 682-696.
71. Venkatachalam, C. M., Price, B. J., and Krimm, S. (1974) Theoretical analysis of pyrrolidine ring puckering and the conformational energies of proline and 5-methylproline dimers, Macromolecules 7, 212-220.
72. Vitagliano, L., Berisio, R., Mastrangelo, A., Mazzarella, L., and Zagari A. (2001) Preferred proline puckerings in cis and trans peptide groups: implications for collagen stability, Protein Sci. 10, 2627-2632.
73. Benzi, C., Improta, R., Scalmani, G., and Barone, V. (2002) Quantum mechanical study of the conformational behavior of proline and 4R-hydroxyproline dipeptide analogues in a vacuum and in aqueous solution, J. Comput. Chem. 23, 341-350.
74. Allen, W. D., Czinki, E., and Csaszar, A. G. (2004) Molecular structure of proline, Chem. Eur. J. 10, 4512-4517.
75. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation, Proteins: Struct., Funct., Genet. 50, 437-450.
76. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure refinement, Acta Crystallogr. 47, 392-400.
77. Frenkel, D., and Smit, B. (2002) Chapter 3, in Understanding molecular simulation, Academic Press, London, U.K.
78. Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H., and Teller, E. (1953) Equation of state calculations by fast computing machines, J. Chem. Phys. 21, 1087-1092.
79. Binder, K. (1995) In Monte Carlo and Molecular Dynamics Simulations in Polymer Science (Binder, K., Ed.) Chapter 1, Oxford University Press, Oxford.
80. Stillinger, F. H., and Weber, T. A. (1984) Packing structures and transitions in liquids and solids, Science 225, 983-989.
81. Stillinger, F. H., and Weber, T. A. (1985) Inherent structure theory of liquids in the hard-sphere limit, J. Chem. Phys. 83, 4767-4775.
82. Luenberger, D. G. (1984) Chapter 9, in Linear and nonlinear programming, 2nd ed., Addison-Wesley, Reading, MA.
83. Hu, H., Elstner, M., and Hermans, J. (2003) Comparison of a QM/MM force field and molecular mechanics force fields in simulations of alanine and glycine "dipeptides" (Ace-Ala-Nme and Ace-Gly-Nme) in water in relation to the problem of modeling the unfolded peptide backbone in solution, Proteins: Struct., Funct., Genet. 50, 451-463.
84. Drozdov, A. N., Grossfield, A., and Pappu, R. V. (2004) The role of solvent in determining conformational preferences of alanine dipeptide in water, J. Am. Chem. Soc. 126, 2574-2581.
85. Brahmachari, S. K., Bansal, M., Ananthanarayanan, V. S., and Sasisekharan, V. (1979) Structural investigation on poly(4-hydroxyl-L-proline). 2. Physicochemical studies, Macromolecules, 12, 23-28.
86. Pappu, R. V., Srinivasan, R., and Rose, G. D. (2000) The Flory isolated pair hypothesis is not valid for polypeptide chains: Implications for protein folding, Proc. Natl. Acad. Sci. U.S.A. 97, 12565-12570.
87. Penkett, C. J., Redfield, C., Dodd, I., Hubbard, J., McBay, D. L., Mossakowska, D. E., Smith, R. A., Dobson, C. M., and Smith, L. J. (1997) NMR analysis of main-chain conformational preferences in an unfolded fibronectin-binding protein, J. Mol. Biol. 274, 152-159.
88. Petrescu, A.-J., Calmettes, P., Durand, D., Receveur, V., and Smith, J. C. (2000) Change in backbone torsion angle distributions on protein folding, Protein Sci. 9, 1129-1136.
89. Yang, W. Y., Larios, E., and Gruebele, M. (2003) On the extended β-conformation propensity of polypeptides at high temperature, J. Am. Chem. Soc. 125, 16220-16227.
90. Ohkubo, Y. Z., and Brooks, C. L. (2003) Exploring Flory's isolated-pair hypothesis: statistical mechanics of helix-coil transitions in polyalanine and the C-peptide from RNase A, Proc. Natl. Acad. Sci. U.S.A. 100, 13916-13921.
91. Kentsis, A., Mezei, M., Gindin, T., and Osman, R. (2004) Unfolded state of polyalanine is a segmented polyproline II helix, Proteins 55, 493-501.
92. MacArthur, M. W., and Thornton, J. M. (1991) Influence of proline residues on protein conformation, J. Mol. Biol. 218, 397-412.
93. Pedersen, J. S., and Schurtenberger, P. (2004) Scattering functions of semidilute solutions of polymers in a good solvent, J. Polym. Sci., Part B: Polym. Phys. 42, 3081-3094.
94. Timasheff, S. N. (2002) Protein hydration, thermodynamic binding, and preferential hydration, Biochemistry 41, 13473-13482.
95. Yang, M., Ferreon, A. C. M., and Bolen, D. W. (2000) Structural thermodynamics of a random coil protein in guanidine hydrochloride, Proteins: Struct., Funct., Genet., Suppl. 4, 44-49.
96. Pace, C. N., Grimsley, G. R., and Scholtz, J. M. (2005) Protein folding handbook (Buchner, J., and Kiefhaber, T., Eds.) Vol. 1, Part 1, Chapter 3, pp 45-69, Wiley-VCH, Winheim.
97. Felitsky, D. J., and Record, M. T. (2004) Application of the local-bulk partitioning and competitive binding models to interpret preferential interactions of glycine betaine and urea with protein surface, Biochemistry 43, 9276-9288.
98. Kröger, M., Ramírez, J., and Öttinger, H. C. (2002) Projection from an atomistic chain contour to its primitive path, Polymer 43, 477-487.
99. Thompson, J. B., Hansma, H. G., Hansma, P. K., and Plaxco, K. W. (2002) The backbone conformational entropy of protein folding: Experimental measures from atomic force microscopy, J. Mol. Biol. 322, 645-652.
100. Fitzkee, N. C., and Rose, G. D. (2004) Reassessing random-coil statistics in unfolded proteins, Proc. Natl. Acad. Sci. U.S.A. 101, 12497-12502.