Pressure denaturation of staphylococcal nuclease studied by neutron small-angle scattering and molecular simulation

Biophysical Journal

Volumn 87, Issue 5, 2004, Pages 3479-3492

  Paliwal, Amit ^a   Asthagiri, Dilipkumar ^a,b   Bossev, Dobrin P ^a,c   Paulaitis, Michael E ^a  

^a Johns Hopkins University   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEASE; MICROCOCCAL NUCLEASE;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; HYDROPHOBICITY; MOLECULAR DYNAMICS; NEUTRON SCATTERING; PRESSURE; PROTEIN FOLDING; STAPHYLOCOCCUS; ALGORITHM; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; COMPUTER SIMULATION; EVALUATION; METHODOLOGY; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; PROTEIN DENATURATION;

ALGORITHMS; COMPUTER SIMULATION; MICROCOCCAL NUCLEASE; MODELS, CHEMICAL; MODELS, MOLECULAR; NEUTRON DIFFRACTION; PRESSURE; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING;

EID: 16344381007     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.050526     Document Type: Article

References (63)

1. Ahmad, S., M. M. Gromiha, H. Fawareh, and A. Sarai. 2004. ASA view: solvent accessibility graphics for proteins. BMC Bioinform. 5:1-12.
2. Anfinsen, C. B. 1972. The formation and stabilization of protein structure. Biochem. J. 128:737-749.
3. Bagchi, K., S. Balasubramanian, and M. L. Klein. 1997. The effects of pressure on structural and dynamical properties of associated liquids: molecular dynamics calculations for the extended simple point charge model of water. J. Chem. Phys. 107:8561-8567.
4. Baldwin, R. L. 1986. Temperature-dependence of the hydrophobic interaction in protein folding. Proc. Natl. Acad. Sci. USA. 83:8069-8072.
5. Barker, J. G., and J. S. Pedersen. 1995. Instrumental smearing effects in radially symmetrical small-angle neutron-scattering by numerical and analytical methods. J. Appl. Crystallogr. 28:105-114.
6. Bonafe, C. F., C. M. Vital, R. C. Telles, M. C. Goncalves, M. S. Matsuura, F. B. Pessine, D. R. Freitas, and J. Vega. 1998. Tobacco Mosaic virus disassembly by high hydrostatic pressure in combination with urea and low temperature. Biochemistry. 37:11097-11105.
7. Bridgman, P. W. 1935. The pressure-volume-temperature relations of the liquid, and the phase diagram of heavy water. J. Chem. Phys. 3:597-605.
8. Carra, J. H., E. A. Anderson, and P. L. Privalov. 1994. Three-state thermodynamic analysis of the denaturation of Staphylococcal nuclease mutants. Biochemistry. 33:10842-10850.
9. Carra, J. H., and P. L. Privalov. 1995. Energetics of denaturation and m-values of Staphylococcal nuclease mutants. Biochemistry. 34:2034-2041.
10. Chen, L., G. Wildegger, T. Kiefhaber, K. O. Hodgson, and S. Doniach. 1998. Kinetics of lysozyme refolding: structural characterization of a non-specifically collapsed state using time-resolved x-ray scattering. J. Mol. Biol. 276:225-237.
11. Da Poian, A. T., A. C. Oliveira, L. P. Caspar, J. L. Silva, and G. Weber. 1993. Reversible pressure dissociation of R17 bacteriophage. The physical individuality of virus particles. J. Mol. Biol 231:999-1008.
12. Da Poian, A. T., J. E. Johnson, and J. L. Silva. 1994. differences in pressure stability of the three components of Cowpea Mosaic virus: implications for virus assembly and disassembly. Biochemistry. 33:8339-8346.
13. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald-an n·log(n) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
14. Dill, K. A. 1990. Dominant forces in protein folding. Biochemistry. 29:7133-7155.
15. Ferdinand, S. 2000. Pressure-induced changes in microstructure of oil-in-water microemulsions. M.S. Thesis. Johns Hopkins University, Baltimore, MD.
16. Flanagan, J. M., M. Kataoka, D. Shortle, and D. M. Engelman. 1992. Truncated Staphylococcal nuclease is compact but disordered. Proc. Natl. Acad. Sci. USA. 89:748-752.
17. Flanagan, J. M., M. Kataoka, T. Fujisawa, and D. Engelman. 1993. Mutations can cause large changes in the conformation of a denatured protein. Biochemistry. 32:10359-10370.
18. Foguel, D., M. C. Suarez, A. D. Ferrão-Gonzales, T. C. R. Porto, L. Palmieri, C. M. Einsiedler, L. R. Andrade, H. A. Lashuel, P. T. Lansbury, J. W. Kelly, and J. L. Silva. 2003. Dissociation of amyloid fibrils of α-synuclein and transthyretin by pressure reveals their reversible nature and the formation of water-excluded cavities. Proc. Natl. Acad. Sci. USA. 100:9831-9836.
19. From, N. B., and B. E. Bowler. 1998. Urea denaturation of Staphylococcal nuclease monitored by Fourier transform infrared spectroscopy. Biochemistry. 37:1623-1631.
20. Frye, K. J., C. S. Perman, and C. A. Royer. 1996. Test the correlation between ΔA and ΔV of protein unfolding using m-value mutants of Staphylococcal nuclease. Biochemistry. 35:10234-10239.
21. Gast, K., H. Damaschun, R. Misselwitz, M. Müller-Frohne, D. Zirwer, and G. Damaschun. 1994. Compactness of protein molten globules: temperature-induced structural changes of apomyoglobin folding intermediates. Eur. Biophys. J. 23:297-305.
22. Glatter, O., and O. Kratky. 1982. Small Angle X-Ray Scattering. Academic Press, New York.
23. Gorovits, B. M., and P. M. Horowitz. 1998. High hydrostatic pressure can reverse aggregation of protein folding intermediates and facilitate acquisition of the native structure. Biochemistry. 37:6132-6135.
24. Griko, Y. V., P. L. Privalov, J. M. Sturtevant, and S. Venyaminov. 1988. Cold denaturation of Staphylococcal nuclease. Proc. Natl. Acad. Sci. USA. 85:3343-3347.
25. Hoover, W. G. 1985. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
26. Hummer, G., S. Garde, A. E. Garcia, M. E. Paulaitis, and L. R. Pratt. 1998. The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. Proc. Natl. Acad. Sci. USA. 95:1552-1555.
27. Hynes, T. R., and R. O. Fox. 1991. The crystal-structure of Staphylococcal nuclease refined at 1.7 Å resolution. Proteins Struct. Funct. Genet. 10:92-105.
28. Ionescu, R. M., and M. R. Eftink. 1997. Global analysis of the acid-induced and urea-induced unfolding of Staphylococcal nuclease and two of its variants. Biochemistry. 36:1129-1140.
29. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bond and geometrical features. Biopolymers. 22:2577-2637.
30. Kalé, L., R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz, J. Phillips, A. Shinozaki, K. Varadarajan, and K. Schulten. 1999. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151:283-312.
31. Kauzmann, W. 1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14:1-63.
32. Kauzmann, W. 1987. Thermodynamics of unfolding. Nature. 325:763-764.
33. 1H NMR. J. Mol. Biol. 298:293-302.
34. Lattman, E. E., K. M. Fiebig, and K. A. Dill. 1994. Modeling compact denatured states of proteins. Biochemistry. 33:6158-6166.
35. MacKerell, A. D., N. Banavali, and N. Foloppe. 2000. Development and current status of the CHARMM force field for nucleic acids. Biopolymers. 56:257-265.
36. Merzel, F., and J. C. Smith. 2002. Is the first hydration shell of lysozyme of higher density than bulk water? Proc. Natl. Acad. Sci. USA. 99:5378-5383.
37. Miller, W. G., and C. V. Goebel. 1968. Dimensions of protein random coils. Biochemistry. 7:3925-3935.
38. Neria, E., S. Fischer, and M. Karplus. 1996. Simulation of activation free energies in molecular systems. J. Chem. Phys. 105:1902-1921.
39. Oliveira, A. C., L. P. Caspar, A. T. Da Poian, and J. L. Silva. 1994. Arc repressor will not denature under pressure in the absence of water. J. Mol. Biol. 240:184-187.
40. Paci, E. 2002. High pressure simulations of biomolecules. Biochim. Biophys. Acta. 1595:185-200 (and references therein.).
41. Panick, G., R. Malessa, R. Winter, G. Rapp, K. J. Frye, and C. A. Royer. 1998. Structural characterization of the pressure-denatured state and unfolding/refolding kinetics of Staphylococcal nuclease by synchrotron small-angle x-ray scattering and Fourier-transform infrared spectroscopy. J. Mol. Biol. 275:389-402.
42. Panick, G., G. J. A. Vidugiris, R. Malessa, G. Rapp, R. Winter, and C. A. Royer. 1999. Exploring the temperature-pressure phase diagram of Staphylococcal nuclease. Biochemistry. 38:4157-4164.
43. Perez, J., P. Vachette, D. Russo, M. Desmadril, and D. Durand. 2001. Heat-induced unfolding of neocarzinostatin, a small all-β protein investigated by small-angle x-ray scattering. J. Mol. Biol. 308:721-743.
44. Royer, C. A. 2002. Revisiting volume changes in pressure-induced protein unfolding. Biochim. Biophys. Acta. 1595:201-209.
45. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
46. Seemann, H., R. Winter, and C. A. Royer. 2001. Volume, expansivity, and isothermal compressibility changes associated with temperature and pressure unfolding of Staphylococcal nuclease. J. Mol. Biol. 307:1091-1102.
47. Segel, D., A. L. Fink, K. O. Hodgson, and S. Doniach. 1998. Protein denaturation: a small-angle x-ray scattering study of the ensemble of unfolded states of cytochrome c. Biochemistry. 37:12443-12451.
48. Segel, D. J., A. Bachmann, J. Hofrichter, K. O. Hodgson, S. Doniach, and T. Kiefhaber. 1999. Characterization of transient intermediates in lysozyme folding with time-resolved small-angle x-ray scattering. J. Mol. Biol. 288:489-499.
49. Segel, D. J., D. Eliezer, V. Uversky, A. L. Fink, K. O. Hodgson, and S. Doniach. 1999. Transient dimer in the refolding kinetics of cytochrome c characterized by small-angle x-ray scattering. Biochemistry. 38:15352-15359.
50. Semisotnov, G. V., H. Kihara, N. V. Kotova, K. Kimura, Y. Amemiya, K. Wakabayashi, I. N. Serdyuk, A. A. Timchenko, K. Chiba, K. Nikaido, T. Ikura, and K. Kuwajima. 1996. Protein globularization during folding. A study by synchrotron small angle x-ray scattering. J. Mol. Biol. 262:559-574.
51. Shortle, D. 1986. Guanidinium hydrochloride denaturation studies of mutant forms of Staphylococcal nuclease. J. Cell. Biochem. 30:281-289.
52. Shortle, D., and A. K. Meeker. 1986. Mutant forms of Staphylococcal nuclease with altered patterns of guanidine hydrochloride and urea denaturation. Proteins Struct. Funct. Genet. 1:81-89.
53. Shortle, D., W. E. Stites, and A. K. Meeker. 1990. Contributions of the large hydrophobic amino acids to the stability of Staphylococcal nuclease. Biochemistry. 29:8033-8041.
54. Shortle, D., and C. Abeygunawardana. 1993. NMR analysis of the residual structure in the denatured state of an unusual mutant of Staphylococcal nuclease. Structure. 1:121-134.
55. Shortle, D. 1995. Staphylococcal nuclease: a showcase of m-value effects. Adv. Protein Chem. 46:217-247.
56. Silva, J. L., and G. Weber. 1993. Pressure stability of proteins. Ann. Rev. Phys. Chem. 44:89-113.
57. Sosnick, T. R., and J. Trewhella. 1992. Denatured states of ribonuclease A have compact dimensions and residual secondary structure. Biochemistry. 31:8329-8335.
58. Svergun, D. I. 1991. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Cryst. 24:495-503.
59. Svergun, D. I., C. Barberato, and M. H. J. Koch. 1995. CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Cryst. 28:768-773.
60. Svergun, D. I., S. Richard, M. H. J. Koch, Z. Sayers, S. Kuprin, and G. Zaccai. 1998. Protein hydration in solution: experimental observation by x-ray and neutron scattering. Proc. Natl. Acad. Sci. USA. 95:2267-2272.
61. Vidugiris, G. J. A, J. L. Markley, and C. A. Royer. 1995. Evidence of a molten globule-like transition state in protein folding from determination of activation volumes. Biochemistry. 34:4909-4912.
62. Wang, Y., and D. Shortle. 1995. The equilibrium folding pathway of Staphylococcal nuclease: identification of the most stable chain-chain interactions by NMR and CD spectroscopy. Biochemistry. 34:15895-15905.
63. Woenckhaus, J., R. Köhling, P. Thiyagarajan, K. C. Littrell, S. Seifert, C. A. Royer, and R. Winter. 2001. Pressure-jump small angle x-ray scattering detected kinetics of Staphylococcal nuclease folding. Biophys. J. 80:1518-1523.