Coupling between folding and ionization equilibria: Effects of pH on the conformational preferences of polypeptides

Journal of Molecular Biology

Volumn 264, Issue 4, 1996, Pages 770-783

  Ripoll, Daniel R ^a   Vorobjev, Yury N ^a,b,e   Liwo, Adam ^a,c   Vila, Jorge A ^d   Scheraga, Harold A ^a  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^c UNIVERSITY OF GDA SK   (Poland)

^d UNIVERSIDAD NACIONAL DE SAN LUIS   (Argentina)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Conformational search; Electrostatic; Energy functions; Polypeptide conformation; Solvation

Indexed keywords

GLUTAMIC ACID; POLYPEPTIDE;

ACCURACY; AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; IONIZATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; SOLVATION; STEREOCHEMISTRY; THERMODYNAMICS;

EID: 0030582736     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0676     Document Type: Article

References (66)

1. as of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry, 29, 10219-10225.
2. B in the reaction center. Biophys. J. 68, 2233-2250.
3. Bradley, E. K., Thomason, J. F., Cohen, F. E., Kosen P. A. & Kuntz, I. D. (1990). Studies of synthetic helical peptides using circular dichroism and nuclear magnetic resonance. J. Mol. Biol. 215, 607-622.
4. Cammers-Goodwin, A., Allen, T. J., Oslick, S. L., McClure, K. F., Lee, J. H. & Kemp, D. S. (1996). Mechanism of stabilization of helical conformations of polypeptides by water containing trifluoroethanol. J. Am. Chem. Soc. 118, 3082-3090.
5. Chothia, C. (1976). The nature of the accessible and buried surfaces in proteins. J. Mol. Biol. 105, 1-14.
6. Connolly, M. L. (1983a). Solvent-accessible surfaces of proteins and nucleic acids. Science, 221, 709-713.
7. Connolly, M. L. (1983b). Analytical molecular surface calculation. J. Appl. Crystallog. 16, 548-558.
8. Daggett, V., Kollman, P. A. & Kuntz, I. D. (1991). Molecular dynamics simulations of small peptides: dependence on dielectric model and pH. Biopolymers, 31, 285-304.
9. Dyson, H. J., Ranee, M., Houghten, R. A., Wright, P. E. & Lerner, R. A. (1988). Folding of immunogenic peptide fragments of proteins in water solution. II. The nascent helix. J. Mol. Biol. 201, 201-217.
10. Gay, D. M. (1983). Algorithm 611. Subroutines for unconstrained minimization using a model/trust-region approach. ACM Trans. Math. Software, 9, 503-524.
11. Gillilan, R. E. & Ripoll, D. R. (1995). Visualizing enzyme electrostatics with IBM visualization data explorer. In Data Visualization in Molecular Science. Bowie, J. E., ed.) pp. 61-81, Manning Publications Co. and Addison-Wesley Publishing Company Inc.
12. Gilson, M. K. (1993). Multiple-site titration and molecular modeling: two rapid methods for computing energies and forces for ionizable groups in proteins. Proteins: Struct. Funct. Genet. 15, 266-282.
13. Go, M. & Scheraga, H. A. (1984). Molecular theory of helix-coil transition in polyamino acids. V. Explanation of the different conformational behavior of valine, isoleucine, and leucine in aqueous solution. Biopolymers, 23, 1961-1977.
14. Groebke, K., Renold, P., Tsang, K. Y., Allen, T. J., McClure, K. F. & Kemp, D. S. (1966). Template-nucleated alanine-lysine helices are stabilized by position-dependent interactions between the lysine side chain and the helix barrel. Proc. Natl Acad. Sci. USA, 93, 4025-4029.
15. Gropp, W., Lusk, E. & Skjellum, A. (1994). Scientific and Engineering Computation series: Using MPI: Portable Parallel Programming with the Message-Passing Interface, MIT Press.
16. Huyghues-Despointes, B. M. P., Scholtz, J. M. & Baldwin, R. L. (1993). Helical peptides with three pairs of Asp-Arg and Glu-Arg residues in different orientations and spacings. Protein Sci. 2, 80-85.
17. Ingwall, R. T., Scheraga, H. A., Lotan, N., Berger, A. & Katchalski, E. (1968). Conformational studies of poly-(1-alanine) in water. Biopolymers, 6, 331-368.
18. Karplus, M. (1959). Contact electron-spin coupling of nuclear magnetic moments. J. Chem. Phys. 30, 11-15.
19. Karplus, M. (1963). Vicinal proton coupling in nuclear magnetic resonance. J. Am. Chem. Soc. 85, 2870-2871.
20. 1-OH). J. Org. Chem. 56, 6683-6697.
21. Kemp, D. S., Boyd, J. G. & Muendel, C. C. (1991b). The helical s constant for alanine in water derived from template-nucleated helices. Nature, 352, 451-454.
22. 1. J. Am. Chem. Soc. 117, 6641-6657.
23. Kemp, D. S., Allen, T. J., Oslick, S. L. & Boyd, J. G. (1996a). The structure and energetics of helix formation by short templated peptides in aqueous solution. 2. Characterization of the helical structure of Ac-Hel1-Ala6-OH. J. Am. Chem. Soc. 118, 4240-4248.
24. Kemp, D. S., Oslick, S. L. & Allen, T. J. (1996b). The structure and energetics of helix formation by short templated peptides in aqueous solution. 3. Calculation of the helix propagation constant s from the template stability constant t/c for Ac-Hel1-Alan-OH, n = 1,6. AC-He1-Ala6-OH. J. Am. Chem. Soc. 118, 4249-4255.
25. Laskowski, M., Jr & Scheraga, H. A. (1954). Thermodynamic considerations of protein reactions. I. Modified reactivity of polar groups. J. Am. Chem. Soc. 76, 6305-6319.
26. Li, Z. & Scheraga, H. A. (1987). Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc. Natl Acad. Sci. USA, 84, 6611-6615.
27. Li, Z. & Scheraga, H. A. (1988). Structure and free energy of complex thermodynamic systems. J. Mol. Struct. (Theochem), 179, 333-352.
28. Marqusee, S., Robbins, V. H. & Baldwin, R. L. (1989). Unusually stable helix formation in short alanine-based peptides. Proc. Natl Acad. Sci. USA, 86, 5286-5290.
29. Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H. & Teller, E. (1953). Equation of state calculations by fast computing machines. J. Chem. Phys. 21, 1087-1092.
30. Momany, F. A., McGuire, R. F., Burgess, A. W. & Scheraga, H. A. (1975). Energy parameters in polypeptides. VII. Geometric parameters, partial atomic charges, non-bonded interactions, hydrogen bond interactions and intrinsic torsional potential for the naturally occurring amino-acids. J. Phys. Chem. 79, 2361-2381.
31. Némethy, G., Pottle, M. S. & Scheraga, H. A. (1983). Energy parameters in polypeptides. 9. Updating of geometrical parameters, nonbonded interactions and hydrogen bond interactions for the naturally occurring amino acids. J. Phys. Chem. 87, 1883-1887.
32. Nemethy, G., Gibson, K. D., Palmer, K. A., Yoon, C. N., Paterlini, G., Zagari, A., Rumsey, S. & Scheraga, H. A. (1992). Energy parameters in polypeptides. 10. Improved geometrical parameters and nonbonded interactions for use in the ECEPP/3 algorithm with application to proline-containing peptides. J. Phys. Chem. 96, 6472-6484.
33. Neurath, H., Greenstein, J. P., Putnam, F. W. & Erickson, J. O. (1944). The chemistry of protein denaturation. Chem. Revs. 34, 157-265.
34. Nicholls, A. & Honig, B. (1991). A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation. J. Comp. Chem. 12, 435-445.
35. Nicholls, A., Sharp, K. A. & Honig, B. (1991). Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11, 281-296.
36. O'Donnell, T. J., Hotovy, S. G., Pottle, M. S., Ripoll, D. R. & Scheraga, H.A. (1996). Implementation of ECEPP-based programs on the IBM SP2 and the SGI Power Challenge Computers. Lecture Notes in Computer Science; vol. 1067: High-Performance Computing and Networking (Liddell, H., Colbrook, A., Hertzberger, B. & Sloot, P., eds), pp. 365-373, Springer-Verlag, Berlin, Heidelberg, New York.
37. Perrin, D. D. (1972a). Dissociation Constants of Organic Acids in Aqueous Solution, Butterworths, London.
38. Perrin, D. D. (1972b). Dissociation Constants of Organic Bases in Aqueous Solution, Butterworths, London.
39. Perrot, G., Cheng, B., Gibson, K. D., Vila, J., Palmer, K. A., Nayeem, A., Maigret, B. & Scheraga, H. A. (1992). MSEED: A program for the rapid analytical determination of accessible surface areas and their derivatives. J. Comp. Chem. 13, 1-11.
40. Platzer, K. E. B., Ananthanarayanan, V. S., Andreatta, R. H. & Scheraga, H. A. (1972). Helix-coil stability constants for the naturally occurring amino acids in water. IV. Alanine parameters from random poly(hydroxypropylglutamine-co-L-alanine). Macromolecules, 5, 177-187.
41. Poland, D. C. & Scheraga, H. A. (1965). Statistical mechanics of non-covalent bonds in polyamino acids. Biopolymers, 3, 275-419; 593.
42. Presta, L. G. & Rose, G. D. (1988). Helix signals in proteins. Science, 240, 1632-1641.
43. Rashin, A. A. (1990). Hydration phenomena, classical electrostatics, and the boundary element method. J. Phys. Chem. 94, 1725-1733.
44. Renold, P., Tsang, K. Y., Shimizu, L. A. & Kemp, D. S. (1996). Large temperature dependencies of the helical propensities of lysine residues within short helical alanine-lysine peptides. J. Am. Chem. Soc. In the press.
45. Richardson, J. S. & Richardson, D. C. (1988). Amino acid preferences for specific locations at the ends of α helices. Science, 240, 1648-1652.
46. Ripoll, D. R. & Scheraga, H. A. (1988). On the multiple problem in the conformational analysis of polypeptides. II. An electrostatically driven Monte Carlo method: tests on poly (L-alanine). Biopolymers, 27, 1283-1303.
47. Ripoll, D. R. & Scheraga, H. A. (1989). On the multiple-minima problem in the conformational analysis of polypeptides. III. An electrostatically driven Monte Carlo method: tests on enkephalin. J. Protein Chem. 8, 263-287.
48. Shoemaker, K. R., Kim, P. S., York, E. J., Stewart, J. M. & Baldwin, R. L. (1987). Tests of the helix dipole model for stabilization of α-helices. Nature, 326, 563-567.
49. Simonson, T. & Brünger, A. T. (1994). Solvation free energies estimated from macroscopic continuum theory: an accuracy assessment. J. Phys. Chem. 98, 4683-4694.
50. Sippl, M. J., Némethy, G. & Scheraga, H. A. (1984). Intermolecular potentials from crystal data. 6. Determination of empirical potentials for O-H . . . O-C hydrogen bonds from packing configurations. J. Phys. Chem. 88, 6231-6233.
51. Sitkoff, D., Sharp, K. A. & Honig, B. (1994). Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98, 1978-1988.
52. Sung, S. (1995). Folding simulations of alanine-based peptides with lysine residues. Biophys. J. 68, 826-834.
53. Vásquez, M. & Scheraga, H. A. (1988). Effect of sequence-specific interactions on the stability of helical conformations in polypeptides. Biopolymers, 27, 41-58.
54. Vila, J., Williams, R. L., Vásquez, M. & Scheraga, H. A. (1991). Empirical solvation models can be used to differentiate native from near-native conformations of bovine pancreatic trypsin inhibitor. Proteins: Struct. Funct. Genet. 10, 199-218.
55. Vila, J., Williams, R. L., Grant, J. A., Wojcik, J. & Scheraga, H. A. (1992). The intrinsic helix-forming tendency of 1-alanine. Proc. Natl Acad. Sci. USA, 89, 7821-7825.
56. Vorobjev, Y. N. & Scheraga, H. A. (1993). Interaction of a biomolecule with mobile ions in aqueous solution. Comparison of three fast approximate methods with the direct solution of the nonlinear Poisson-Boltzmann equation. J. Phys. Chem. 97, 4855-4864.
57. Vorobjev, Y. N. & Scheraga, H. A. (1996). A fast multigrid boundary element method for macromolecular electrostatic computations in a solvent. J. Comput. Chem. In the press.
58. Vorobjev, Y. N., Grant, J. A. & Scheraga, H. A. (1992). A combined iterative and boundary element approach for solution of the nonlinear Poisson-Boltzmann equation. J. Am. Chem. Soc. 114, 3189-3196.
59. Vorobjev, Y. N., Scheraga, H. A., Hitz, B. & Honig, B. (1994). Theoretical modeling of electrostatic effects of titratable side-chain groups on protein conformation in a polar ionic solution. 1. Potential of mean force between charged lysine residues and titration of poly(L-lysine) in 95% methanol solution. J. Phys. Chem. 98, 10940-10948.
60. Wojcik, J., Altman, K. H. & Scheraga, H. A. (1990). Helix-coil stability constants for the naturally occurring amino acids in water. XXIV. Half-cysteine parameters from random poly (hydroxybutylglutamine-co-S-methylthio-L-cysteine). Biopolymers, 30, 121-134.
61. Yang, A.-S. & Honig, B. (1993). On the pH dependence of protein stability. J. Mol. Biol. 231, 459-474.
62. as in proteins. Proteins: Struct. Funct. Genet. 15, 252-265.
63. You, T. J. & Bashford, D. (1995). Conformation and hydrogen ion titration of proteins: A continuum electrostatic model with conformational flexibility. Biophys. J. 69, 1721-1733.
64. Zauhar, R. J. & Morgan, R. S. (1988). The rigorous computation of the molecular electric potential. J. Comp. Chem. 9, 171-187.
65. Zimm, B. H. & Bragg, J. K. (1959). Theory of the phase transition between helix and random coil in polypeptide chains. J. Chem. Phys. 31, 526-535.
66. Zimmerman, S. S., Pottle, M. S., Némethy, G. & Scheraga, H. A. (1977). Conformational analysis of the 20 naturally occurring amino acid residues using ECEPP. Macromolecules, 10, 1-9.