Contribution of single tryptophan residues to the fluorescence and stability of ribonuclease Sa

Biophysical Journal

Volumn 87, Issue 6, 2004, Pages 4036-4047

  Alston, Roy W ^a,b   Urbanikova, Lubica ^c   Sevcik, Jozef ^c   Lasagna, Mauricio ^b   Reinhart, Gregory D ^b   Scholtz, J Martin ^a,b   Pace, C Nick ^a,b  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

AZURIN; BARNASE; ENZYME VARIANT; RIBONUCLEASE; SOLVENT; THREONINE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME STABILITY; FLUORESCENCE; PROTEIN FOLDING; PROTEIN INTERACTION; RIBONUCLEASE SA;

EID: 10044295190     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.050377     Document Type: Article

References (66)

1. Adams, P. D., Y. Chen, K. Ma, M. G. Zagorski, F. D. Sonnichsen, M. L. McLaughlin, and M. D. Barkley. 2002. Intramolecular quenching of tryptophan fluorescence by the peptide bond in cyclic hexapeptides. J. Am. Chem. Soc. 124:9278-9286.
2. Axe, D. D., N. W. Foster, and A. R. Fersht. 1999. An irregular β-bulge common to a group of bacterial RNases is an important determinant of stability and function in barnase. J. Mol. Biol. 286: 1471-1485.
3. Axelsen, P. H., and F. G. Prendergast. 1989. Molecular dynamics of tryptophan in ribonuclease-T1. II. Correlations with fluorescence. Biophys. J. 56:43-66.
4. Beechem, J. M., and L. Brand. 1985. Time-resolved fluorescence of proteins. Annu. Rev. Biochem. 54:43-71.
5. Bond, C. J., K. B. Wong, J. Clarke, A. R. Fersht, and V. Daggett. 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. USA. 94:13409-13413.
6. Brunger, A. T., and M. Nilges. 1993. Computational challenges for macromolecular structure determination by x-ray crystallography and solution NMR-spectroscopy. Q. Rev. Biophys. 26:49-125.
7. Burstein, E. A., N. S. Vedenkina, and M. N. Ivkova. 1973. Fluorescence and the location of tryptophan residues in protein molecules. Photochem. Photobiol. 18:263-279.
8. b, transitions of tryptophan: applications of theory and experimental observations to fluorescence of proteins. Methods Enzymol. 278:113-150.
9. Callis, P. R., and J. T. Vivian. 2003. Understanding the variable fluorescence quantum yield of tryptophan in proteins using QM-MM simulations. Quenching by charge transfer to the peptide backbone. Chem. Phys. Lett. 369:409-414.
10. Chen, Y., and M. D. Barkley. 1998. Toward understanding tryptophan fluorescence in proteins. Biochemistry. 37:9976-9982.
11. Creamer, T. P., R. Srinivasan, and G. D. Rose. 1995. Modeling unfolded state of peptides and proteins. Biochemistry. 34:16245-16250.
12. Creamer, T. P., R. Srinivasan, and G. D. Rose. 1997. Modeling unfolded states of proteins and peptides. II. Backbone solvent accessibility. Biochemistry. 36:2832-2835.
13. Eftink, M. R. 1991. Fluorescence techniques for studying protein structure. Methods Biochem. Anal. 35:127-205.
14. Elcock, A. H. 1999. Realistic modeling of the denatured states of proteins allows accurate calculations of the pH dependence of protein stability. J. Mol. Biol. 294:1051-1062.
15. Engelborghs, Y. 2003. Correlating protein structure and protein fluorescence. J. Fluor. 13:9-16.
16. Fauchere, J. L., and V. E. Pliska. 1983. Hydrophobic parameters of amino-acid side chains from the partitioning of N-acetyl-amino-acid amides. Eur. J. Med. Chem. 18:369-375.
17. Giletto, A., and C. N. Pace. 1999. Buried, charged, non-ion-paired aspartic acid 76 contributes favorably to the conformational stability of ribonuclease T1. Biochemistry. 38:13379-13384.
18. Grimsley, G. R., K. L. Shaw, L. R. Fee, R. W. Alston, B. M. Huyghues-Despointes, R. L. Thurlkill, J. M. Scholtz, and C. N. Pace. 1999. Increasing protein stability by altering long-range Coulombic interactions. Protein Sci. 8:1843-1849.
19. Hannemann, F., A. K. Bera, B. Fischer, M. Lisurek, K. Teuchner, and R. Bernhardt. 2002. Unfolding and conformational studies on bovine adrenodoxin probed by engineered intrinsic tryptophan fluorescence. Biochemistry. 41:11008-11016.
20. Harpaz, Y., M. Gerstein, and C. Chothia. 1994. Volume changes in protein folding. Structure. 2:641-649.
21. Hebert, E. J. 1997. Conformational stability of ribonuclease Sa from Streptomyces aureofaciens. Ph.D. dissertation. Texas A&M University, College Station, TX.
22. Hebert, E. J., G. R. Grimsley, R. W. Hartley, G. Horn, D. Schell, S. Garcia, V. Both, J. Sevcik, and C. N. Pace. 1997. Purification of ribonucleases Sa, Sa2, and Sa3 after expression in Escherichia coli. Protein Expr. Purif. 11:162-168.
23. Huyghues-Despointes, B. M., R. L. Thurlkill, M. D. Daily, D. Schell, J. M. Briggs, J. M. Antosiewicz, C. N. Pace, and J. M. Scholtz. 2003. pK values of histidine residues in ribonuclease Sa: effect of salt and net charge. J. Mol. Biol. 325:1093-1105.
24. Kabsch, W. 1976. Solution for best rotation to relate two sets of vectors. Acta Crystallogr. A. 32:922-923.
25. Killick, T. R., S. M. Freund, and A. R. Fersht. 1998. Real-time NMR studies on folding of mutants of barnase and chymotrypsin inhibitor 2. FEBS Lett. 423:110-112.
26. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
27. Lakowicz, J. R. 1999. Principles of Fluorescence Spectroscopy. Kluwer Academic/Plenum Publishers, New York.
28. Laurents, D., J. M. Perez-Canadillas, J. Santoro, M. Rico, D. Schell, C. N. Pace, and M. Bruix. 2001. Solution structure and dynamics of ribonuclease Sa. Proteins. 44:200-211.
29. Laurents, D. V., B. M. Huyghues-Despointes, M. Bruix, R. L. Thurlkill, D. Schell, S. Newsom, G. R. Grimsley, K. L. Shaw, S. Trevino, M. Rico, J. M. Briggs, J. M. Antosiewicz, J. M. Scholtz, and C. N. Pace. 2003. Charge-charge interactions are key determinants of the pK values of ionizable groups in ribonuclease Sa (pI = 3.5) and a basic variant (pI = 10.2). J. Mol. Biol. 325:1077-1092.
30. Lee, B., and F. M. Richards. 1971. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:379-400.
31. Lesser, G. J., and G. D. Rose. 1990. Hydrophobicity of amino acid subgroups in proteins. Proteins. 8:6-13.
32. Loewenthal, R., J. Sancho, and A. R. Fersht. 1991. Fluorescence spectrum of barnase: contributions of three tryptophan residues and a histidine-related pH dependence. Biochemistry. 30:6775-6779.
33. Longworth, J. W. 1971. The luminescence of the aromatic amino acids. In Excited States of Proteins and Nucleic Acids. R.F. Steiner and I. Weinryb, editors. Plenum Press, New York. 319-484.
34. Loris, R., U. Langhorst, S. De Vos, K. Decanniere, J. Bouckaert, D. Maes, T. R. Transue, and J. Steyaert. 1999. Conserved water molecules in a large family of microbial ribonucleases. Proteins. 36:117-134.
35. Martinez-Oyanedel, J., H.-W. Choe, U. Heinemann, and W. Saenger. 1991. Ribonuclease T1 with free recognition and catalytic site: crystal structure analysis at 1.5 Å resolution. J. Mol. Biol. 222:335-352.
36. Mascotti, D. P., and T. M. Lohman. 1997. Thermodynamics of oligoarginines binding to RNA and DNA. Biochemistry. 36:7272-7279.
37. Matthews, B. W. 1968. Solvent content of protein crystals. J. Mol. Biol. 33:491-497.
38. McRee, B. 1993. 1993 Founders Award. Presented to Elizabeth Katsikas. Health Phys. 65:465-466.
39. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
40. Pace, C. N., E. J. Hebert, K. L. Shaw, D. Schell, V. Both, D. Krajcikova, J. Sevcik, K. S. Wilson, Z. Dauter, R. W. Hartley, and G. R. Grimsley. 1998. Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2 and Sa3. J. Mol. Biol. 279:271-286.
41. Pace, C. N., G. Horn, E. J. Hebert, J. Bechert, K. Shaw, L. Urbanikova, J. M. Scholtz, and J. Sevcik. 2001. Tyrosine hydrogen bonds make a large contribution to protein stability. J. Mol. Biol. 312:393-404.
42. Pace, C. N., D. V. Laurents, and R. E. Erickson. 1992. Urea denaturation of barnase: pH dependence and characterization of the unfolded state. Biochemistry. 31:2728-2734.
43. Pace, C. N., and J. M. Scholtz. 1997. Measuring the conformational stability of a protein. In Protein Structure: A Practical Approach. T.E. Creighton, editor. Oxford University Press, New York, NY. 299-321.
44. Pace, C. N., and K. L. Shaw. 2000. Linear extrapolation method of analyzing solvent denaturation curves. Proteins. Suppl 4:1-7.
45. Pace, C. N., F. Vajdos, L. Fee, G. Grimsley, and T. Gray. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4:2411-2423.
46. Pan, C. P., and M. D. Barkley. 2004. Conformational effects on tryptophan fluorescence in cyclic hexapeptides. Biophys. J. 86:3828-3835.
47. Perrakis, A., R. Morris, and V. S. Lamzin. 1999. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6:458-463.
48. Pierce, D. W., and S. G. Boxer. 1995. Stark-effect spectroscopy of tryptophan. Biophys. J. 68:1583-1591.
49. Ross, J. B., A. G. Szabo, and C. W. Hogue. 1997. Enhancement of protein spectra with tryptophan analogs: fluorescence spectroscopy of protein-protein and protein-nucleic acid interactions. Methods Enzymol. 278: 151-190.
50. Santoro, M. M., and D. W. Bolen. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry. 27:8063-8068.
51. Schmid, F. X. 1997. Optical spectroscopy to characterize protein conformation and conformational changes. In Protein Structure: A Practical Approach. T.E. Creighton, editor. Oxford University Press, New York. 261-297.
52. Sendak, R. A., D. M. Rothwarf, W. J. Wedemeyer, W. A. Houry, and H. A. Scheraga. 1996. Kinetic and thermodynamic studies of the folding/ unfolding of a tryptophan-containing mutant of ribonuclease A. Biochemistry. 35:12978-12992.
53. Sevcik, J., Z. Dauter, V. S. Lamzin, and K. S. Wilson. 1996. Ribonuclease from Streptomyces aureofaciens at atomic resolution. Acta Crystallogr. D Crys. Struct. Comm. 52:327-344.
54. Sevcik, J., V. S. Lamzin, Z. Dauter, and K. S. Wilson. 2002a. Atomic resolution data reveal flexibility in the structure of RNase Sa. Acta Crystallogr. D Biol. Crystallogr. 58:1307-1313.
55. Sevcik, J., L. Urbanikova, P. A. Leland, and R. T. Raines. 2002b. X-ray structure of two crystalline forms of a streptomycete ribonuclease with cytotoxic activity. J. Biol. Chem. 277:47325-47330.
56. Shortle, D. 2002. The expanded denatured state: an ensemble of conformations trapped in a locally encoded topological space. Adv. Protein Chem. 62:1-23.
57. Sillen, A., J. F. Diaz, and Y. Engelborghs. 2000. A step toward the prediction of the fluorescence lifetimes of tryptophan residues in proteins based on structural and spectral data. Protein Sci. 9:158-169.
58. Soler-Gonzalez, A. S., and A. R. Fersht. 1997. Helix stability in barstar peptides. Eur. J. Biochem. 249:724-732.
59. Swaminathan, R., G. Krishnamoorthy, and N. Periasamy. 1994. Similarity of fluorescence lifetime distributions for single tryptophan proteins in the random coil state. Biophys. J. 67:2013-2023.
60. 1-antitrypsin with single tryptophan mutants; evidence for structure in the urea unfolded state. J. Mol. Biol. 313:1161-1169.
61. Vivian, J. T., and P. R. Callis. 2001. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80:2093-2109.
62. Volotovskii, I. D., and S. V. Konev. 1967. [Relation between the conformation and UV luminescence of proteins.] Biofizika. 12: 200-205.
63. Weinryb, I., and R. F. Steiner. 1971. The luminescence of the aromatic amino acids. In Excited States of Proteins and Nucleic Acids. Plenum Press, New York. 277-318.
64. Willaert, K., R. Loewenthal, J. Sancho, M. Froeyen, A. Fersht, and Y. Engelborghs. 1992. Determination of the excited-state lifetimes of the tryptophan residues in barnase, via multifrequency phase fluorometry of tryptophan mutants. Biochemistry. 31:711-716.
65. Wong, K. B., J. Clarke, C. J. Bond, J. L. Neira, S. M. Freund, A. R. Fersht, and V. Daggett. 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.
66. Woody, R. W. 1994. Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins. Eur. Biophys. J. 23:253-262.