Cavity-creating mutations in Pseudomonas aeruginosa azurin: Effects on protein dynamics and stability

Biophysical Journal

Volumn 95, Issue 2, 2008, Pages 771-781

  Gabellieri, Edi ^a   Balestreri, Ettore ^a   Galli, Alvaro ^b   Cioni, Patrizia ^a  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AZURIN;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; METABOLISM; POROSITY; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

AMINO ACID SUBSTITUTION; AZURIN; COMPUTER SIMULATION; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; POROSITY; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 47749116844     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.128009     Document Type: Article

References (71)

1. Harpaz, Y., M. Gerstein, and C. Chothia. 1994. Volume changes on protein folding. Structure. 2:641-649.
2. Richards, F. M. 1974. The interpretation of protein structures: total volume, group volume distributions and packing density. J. Mol. Biol. 82:1-14.
3. Richards, F. M. 1977. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6:151-176.
4. Gavish, B., E. Gratton, and C. J. Hardy. 1983. Adiabatic compressibility of globular proteins. Proc. Natl. Acad. Sci. USA. 80:750-754.
5. Kharakoz, D. P., and A. P. Sarvazyan. 1993. Hydrational and intrinsic compressibilities of globular proteins. Biopolymers. 33:11-26.
6. Collins, M. D., M. L. Quillin, G. Hummer, B. W. Matthews, and S. M. Gruner. 2007. Structural rigidity of a large cavity-containing protein revealed by high-pressure crystallography. J. Mol. Biol. 367:752-763.
7. Kauzmann, W., K. Moore, and D. Schultz. 1974. Protein densities from x-ray crystallographic coordinates. Nature. 248:447-449.
8. Kundrot, C. E., and F. M. Richards. 1987. Crystal structure of hen egg-white lysozyme at a hydrostatic pressure of 1000 atmospheres. J. Mol. Biol. 193:157-170.
9. McCammon, J. A., and S. C. Harvey. 1987.Dynamics of Proteins and Nucleic Acids. Cambridge University Press. Cambridge, MA.
10. Collins, M. D., G. Hummer, M. L. Quillin, B. W. Matthews, and S. M. Gruner. 2005. Cooperative water filling of a nonpolar protein cavity observed by high-pressure crystallography and simulation. Proc. Natl. Acad. Sci. USA. 102:16668-16671.
11. Igumenova, T. I., K. K. Frederick, and A. J. Wand. 2006. Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution. Chem. Rev. 106:1672-1699.
12. Halle, B. 2002. Flexibility and packing in proteins. Proc. Natl. Acad. Sci. USA. 99:1274-1279.
13. Kocher, J. P., M. Prévost, S. J. Wodak, and B. Lee. 1996. Properties of the protein matrix revealed by the free energy of cavity formation. Structure. 4:1517-1529.
14. Desjarlais, J. R., and T. M. Handel. 1995. De novo design of the hydrophobic cores of proteins. Protein Sci. 4:2006-2018.
15. Eriksson, A. E., W. A. Baase, X. J. Zhang, D. W. Heinz, M. Blaber, E. P. Baldwin, and B. W. Matthews. 1992. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science. 255:178-183.
16. Jackson, S. E., M. Moracci, N. elMasry, C. M. Johnson, and A. R. Fersht. 1993. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry. 32:11259-11269.
17. Graziano, G. 2007. Cavity size distribution in the interior of globular proteins. Chem. Phys. Lett. 434:316-319.
18. Xu, J. A., W. A. Baase, E. Baldwin, and B. W. Matthews. 1998. The response of T4 lysozyme to large-to-small substitutions within the core and its relation to the hydrophobic effect. Protein Sci. 7:158-177.
19. Sibille, N., A. Favier A. I. Azuaga, G. Ganshaw, R. Bott, A. M. Bonvin, R. Boelens, and N. A. van Nuland. 2006. Comparative NMR study on the impact of point mutations on protein stability of Pseudomonas mendocina lipase. Protein Sci. 15:1915-1927.
20. Finazzi-Agrò A., G. Rotilio, L. Avigliano, P. Guerrieri, V. Boffi, and B. MondovÌ. 1970. Environment of copper in Pseudomonas fluorescens azurin: fluorometric approach. Biochemistry. 9:2009-2014.
21. Guzzi, R., L. Sportelli, C. La Rosa, D. Milardi, D. Grasso, M. Ph. Verbeet, and G. W. Canters. 1999. A spectroscopic and calorimetric investigation on the thermal stability of the Cys3Ala/Cys26Ala azurin mutant. Biophys. J. 77:1052-1063.
22. Pozdnyakova, I., J. Guidry, and P. Wittung-Stafshede. 2001. Copper stabilizes azurin by decreasing the unfolding rate. Arch. Biochem. Biophys. 390:146-148.
23. Pozdnyakova, I., J. Guidry, and P. Wittung-Stafshede. 2002. Studies of Pseudomonas aeruginosa azurin mutants: cavities in beta-barrel do not affect refolding speed. Biophys. J. 82:2645-2651.
24. Pozdnyakova, I., and P.Wittung-Stafshede. 2001. Copper binding before polypeptide folding speeds up formation of active (holo) Pseudomonas aeruginosa azurin. Biochemistry. 40:13728-13733.
25. Pozdnyakova, I., and P. Wittung-Stafshede. 2001. Biological relevance of metal binding before protein folding. J. Am. Chem. Soc. 123:10135-10136.
26. Cioni, P., E. de Waal, G. W. Canters, and G. B. Strambini. 2004. Effects of cavity-forming mutations on the internal dynamics of azurin. Biophys. J. 86:1149-1159.
27. Strambini, G. B., and M. Gonnelli. 1995. Tryptophan phosphorescence in fluid solution. J. Am. Chem. Soc. 117:7646-7651.
28. Gonnelli, M., and G. B. Strambini. 1995. Phosphorescence lifetime of tryptophan in proteins. Biochemistry. 34:13847-13857.
29. Cioni, P., and G. B. Strambini. 1998. Acrylamide quenching of protein phosphorescence as a monitor of structural fluctuations in the globular fold. J. Am. Chem. Soc. 120:11749-11757.
30. Strambini, G. B., and M. Gonnelli. 2007. Protein stability in ice. Biophys. J. 92:2131-2138.
31. van de Kamp, M., M. C. Silvestrini, M. Brunori, J. Van Beeumen, F. C. Hali, and G. W. Canters. 1990. Involvement of the hydrophobic patch of azurin in the electron-transfer reactions with cytochrome c551 and nitrite reductase. Eur. J. Biochem. 194:109-118.
32. Strambini, G. B., and E. Gabellieri. 1991. Phosphorescence from Trp-48 in azurin: influence of Cu(II), Cu(I), Ag(I), and Cd(II) at the coordination site. J. Phys. Chem. 95:4352-4356.
33. Mei, G., A. Di Venere, F. Malvezzi Campeggi, G. Gilardi, N. Rosato, F. De Matteis, and A. Finazzi-Agrò . 1999. The effect of pressure and guanidine hydrochloride on azurins mutated in the hydrophobic core. Eur. J. Biochem. 265:619-626.
34. Strambini, G. B., B. A. Kerwin, B. D. Mason, M. Gonnelli. 2004. The triplet-state lifetime of indole derivatives in aqueous solution. Photochem. Photobiol. 80:462-470.
35. Wilson, C. J., and P. Wittung-Stafshede. 2005. Role of structural determinants in folding of the sandwich-like protein Pseudomonas aeruginosa azurin. Proc. Natl. Acad. Sci. USA. 102:3984-3987.
36. Leckner, J. 2001.Folding and structure of azurin - The influence of a metal. PhD thesis. Chalmers University of Technology, Göteborg, Sweden.
37. Hemmingsen, J. M., K. M. Gernert, J. S. Richardson, and D. C. Richardson. 1994. The tyrosine corner: a feature of most Greek key beta-barrel proteins. Protein Sci. 3:1927-1937.
38. Engeseth, H. R., and D. R. McMillin. 1986. Studies of thermally induced denaturation of azurin and azurin derivatives by differential scanning calorimetry: evidence for copper selectivity. Biochemistry. 25:2448-2455.
39. Gilardi, G., G. Mei, N. Rosato, G. W. Canters, and A. Finazzi-Agrò. 1994. Unique environment of Trp48 in Pseudomonas aeruginosa azurin as probed by site-directed mutagenesis and dynamic fluorescence spectroscopy. Biochemistry. 33:1425-1432.
40. Galley, W. C., and G. B. Strambini. 1976. Kinetics of triplet-triplet energy transfer and intramolecular distances in enzyme-inhibitor complexes. Nature. 261:521-522.
41. Broos, J., E. Gabellieri, G. I. van Boxel, J. B. Jackson, and G. B. Strambini. 2003. Tryptophan phosphorescence spectroscopy reveals that a domain in the NAD(H)-binding component (dI) of transhydrogenase from Rhodospirillum rubrum has an extremely rigid and conformationally homogeneous protein core. J. Biol. Chem. 278:47578-47584.
42. Kerwin, B. A. B. S. C., C. V. Gegg, M. Gonnelli, T. Li, and G. B. Strambini. 2002. Interaction between PEG and type I soluble tumor necrosis receptor: modulation by pH and by PEGylationat the N-terminus. Protein Sci. 11:1825-1833.
43. Punyiczki, M., and A. Rosenberg. 1992. The effect of viscosity on the accessibility of the single tryptophan in human serum albumin. Biophys. Chem. 42:93-100.
44. Eftink, M. R., and C. A. Ghiron. 1976. Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry. 15:672-680.
45. Miner, C. S., and N. N. Dalton. 1953. Glycerol. Reinhold Publishers, New York.
46. Myers, J. K., C. N. Pace, and J. M. Scholtz. 1995. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:2138-2148.
47. Courtenay, E. S., M. W. Capp, R. M. Saecker, and M. T. Record Jr. 2000.Thermodynamic analysis of interactions between denaturants and protein surface exposed on unfolding: interpretation of urea and guanidinium chloride m-values and their correlation with changes in accessible surface area (ASA) using preferential interaction coefficients and the local-bulk domain model. Proteins. 41 (Suppl. S4):72-85.
48. Jones, S., J. S. Reader, M. Healy, A. P. Capaldi, A. E. Capaldi, A. E. Ashcroft, A. P. Kalverda, D. A. Smith, and S. E. Radford. 2000. Partially unfolded species populated during equilibrium denaturation of the beta-sheet protein Y74W apo-pseudoazurin. Biochemistry. 39:5672-5682.
49. Nicaise, M., M. Valerio-Lepiniec, N. Izadi-Pruneyre, E. Adjadj, P. Minard, and M. Desmadril. 2003. Role of the tyrosine corner motif in the stability of neocarzinostatin. Protein Eng. 16:733-738.
50. Hammann, C., A. Messerschmidt, R. Huber, H. Nar, G. Gilardi, and G. W. Canters. 1996. X-ray crystal structure of the two site-specific mutants Ile7Ser and Phe110Ser of azurin from Pseudomonas aeruginosa. J. Mol. Biol. 255:362-366.
51. Nar, H., A. Messerschmidt, R. Huber, M. van de Kamp, and G. W. Canters. 1991. Crystal structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0. A pH-induced conformational transition involves a peptide bond flip. J. Mol. Biol. 221:765-772.
52. Mei, G., M. Venanzi, N. Rosato, G. W. Canters, and A. F. Agro. 1996. Probing the structure and mobility of Pseudomonas aeruginosa azurin by circular dichroism and dynamic fluorescence anisotropy. Protein Sci. 5:2248-2254.
53. Arcangeli, C., A. R. Bizzarri, and S. Cannistraro. 1999. Long-term molecular dynamics simulation of copper azurin: structure, dynamics and functionality. Biophys. Chem. 78:247-257.
54. Arcangeli, C., A. R. Bizzarri, and S. Cannistraro. 2001. Concerted motions in copper plastocyanin and azurin: an essential dynamics study. Biophys. Chem. 90:45-56.
55. Mulder, F. A., B. Hon, D. R. Muhandiram, F. W. Dahlquist, and L. E. Kay. 2000. Flexibility and ligand exchange in a buried cavity mutant of T4 lysozyme studied by multinuclear NMR. Biochemistry. 39:12614-12622.
56. Mulder, F. A., N. R. Skrynnikov, B. Hon, F. W. Dahlquist, and L. E. Kay. 2001. Measurement of slow (micros-ms) time scale dynamics in protein side chains by (15)N relaxation dispersion NMR spectroscopy: application to Asn and Gln residues in a cavity mutant of T4 lysozyme. J. Am. Chem. Soc. 123:967-975.
57. Mulder, F. A., B. Hon, A. Mittermaier, F. W. Dahlquist, and L. E. Kay. 2002. Slow internal dynamics in proteins: application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme. J. Am. Chem. Soc. 124:1443-1451.
58. Quillin, M. L., W. A. Breyer, I. J. Griswold, and B. W. Matthews. 2000. Size versus polarizability in protein-ligand interactions: binding of noble gases within engineered cavities in phage T4 lysozyme. J. Mol. Biol. 302:955-977.
59. Vlassi, M., G. Cesareni, and M. Kokkinidis. 1999. A correlation between the loss of hydrophobic core packing interactions and protein stability. J. Mol. Biol. 285:817-827.
60. Buckle, A. M., P. Cramer, and A. R. Fersht. 1996. Structural and energetic responses to cavity-creating mutations in hydrophobic cores: observation of a buried water molecule and the hydrophilic nature of such hydrophobic cavities. Biochemistry. 35:4298-4305.
61. Hamill, S. J., E. Cota, C. Chothia, and J. Clarke. 2000. Conservation of folding and stability within a protein family: the tyrosine corner as an evolutionary cul-de-sac. J. Mol. Biol. 295:641-649.
62. Collins, T., M. A. Meuwis, C. Gerday, and G. Feller. 2003. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 328:419-428.
63. Tsai, A. M., T. J. Udovic, and D. A. Neumann. 2001. The inverse relationship between protein dynamics and thermal stability. Biophys. J. 81:2339-2343.
64. Zavodszky, P., J. Kardos, A. Svingor, and G. A. Petsko. 1998. Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc. Natl. Acad. Sci. USA. 95:7406-7411.
65. Tang, K. E., and K. A. Dill. 1998. Native protein fluctuations: the conformational-motion temperature and the inverse correlation of protein flexibility with protein stability. J. Biomol. Struct. Dyn. 16:397-411.
66. Hernandez, G., F. E. Jenney Jr., M. W. Adams, and D. M. LeMaster. 2000. Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc. Natl. Acad. Sci. USA. 97:3166-3170.
67. Fitter, J., R. Herrmann, N. A. Dencher, A. Blume, and T. Hauss. 2001. Activity and stability of a thermostable alpha-amylase compared to its mesophilic homologue: mechanisms of thermal adaptation. Biochemistry. 40:10723-10731.
68. Grottesi, A., M. A. Ceruso, A. Colosimo, and A. Di Nola. 2002. Molecular dynamics study of a hyperthermophilic and a mesophilic rubredoxin. Proteins. 46:287-294.
69. Amadei, A., A. B. Linssen, and H. J. Berendsen. 1993. Essential dynamics of proteins. Proteins. 17:412-425.
70. de Groot, B. L., S. Hayward, D. M. F. van Aalten, A. Amadei, and H. J. C. Berendsen. 1998. Domain motions in bacteriophage T4 lysozyme: a comparison between molecular dynamics and crystallographic data. Proteins. 31:116-127.
71. Bahar, I., A. R. Atilgan, M. C. Demirel, and B. Erman. 1998. Vibrational dynamics of folded proteins: significance of slow and fast motions in relation to function and stability. Phys. Rev. Lett. 80:2733-2736.