Tryptophan fluorescence reveals the presence of long-range interactions in the denatured state of Ribonuclease Sa

Biophysical Journal

Volumn 94, Issue 6, 2008, Pages 2288-2296

  Alston, Roy W ^a,b   Lasagna, Mauricio ^a   Grimsley, Gerald R ^a   Scholtz, J Martin ^a   Reinhart, Gregory D ^a   Pace, C Nick ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLAMIDE; ACRYLAMIDE DERIVATIVE; DISULFIDE; IODIDE; PEPTIDE; PROTEIN; RIBONUCLEASE; RIBONUCLEASE SA3; TRYPTOPHAN; UREA;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CONFORMATION; FLUORESCENCE; METHODOLOGY; MOLECULAR GENETICS; SPECTROFLUOROMETRY; TIME;

ACRYLAMIDE; ACRYLAMIDES; AMINO ACID SEQUENCE; DISULFIDES; FLUORESCENCE; IODIDES; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEINS; RIBONUCLEASES; SPECTROMETRY, FLUORESCENCE; TIME FACTORS; TRYPTOPHAN; UREA;

EID: 44049105914     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.116954     Document Type: Article

References (74)

1. Radivojac, P., L. M. Iakoucheva, C. J. Oldfield, Z. Obradovic, V. N. Uversky, and A. K. Dunker. 2007. Intrinsic disorder and functional proteomics. Biophys. J. 92:1439-1456.
2. Sanchez-Puig, N., D. B. Veprintsev, and A. R. Fersht. 2005. Human full-length Securin is a natively unfolded protein. Protein Sci. 14: 1410-1418.
3. Pace, C. N., R. W. Alston, and K. L. Shaw. 2000. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9:1395-1398.
4. Strickler, S. S., A. V. Gribenko, T. R. Keiffer, J. Tomlinson, T. Reihle, V. V. Loladze, and G. I. Makhatadze. 2006. Protein stability and surface electrostatics: a charged relationship. Biochemistry. 45:2761-2766.
5. Cho, J. H., and D. P. Raleigh. 2005. Mutational analysis demonstrates that specific electrostatic interactions can play a key role in the denatured state ensemble of proteins. J. Mol. Biol. 353:174-185.
6. Trefethen, J. M., C. N. Pace, J. M. Scholtz, and D. N. Brems. 2005. Charge-charge interactions in the denatured state influence the folding kinetics of ribonuclease Sa. Protein Sci. 14:1934-1938.
7. Cho, J. H., and D. P. Raleigh. 2006. Denatured state effects and the origin of nonclassical phi values in protein folding. J. Am. Chem. Soc. 128:16492-16493.
8. Arai, M., M. Kataoka, K. Kuwajima, C. R. Matthews, and M. Iwakura. 2003. Effects of the difference in the unfolded-state ensemble on the folding of Escherichia coli dihydrofolate reductase. J. Mol. Biol. 329:779-791.
9. Teale, F. W. 1960. The ultraviolet fluorescence of proteins in neutral solution. Biochem. J. 76:381-388.
10. Kronman, M. J., and L. G. Holmes. 1971. The fluorescence of native, denatured and reduced-denatured proteins. Photochem. Photobiol. 14:113-134.
11. Pajot, P. 1976. Fluorescence of proteins in 6-M guanidine hydrochloride. A method for the quantitative determination of tryptophan. Eur. J. Biochem. 63:263-269.
12. Garcia, P., M. Desmadril, P. Minard, and J. M. Yon. 1995. Evidence for residual structures in an unfolded form of yeast phosphoglycerate kinase. Biochemistry. 34:397-404.
13. Scalley, M. L., S. Nauli, S. T. Gladwin, and D. Baker. 1999. Structural transitions in the protein L denatured state ensemble. Biochemistry. 38:15927-15935.
14. Tcherkasskaya, O., V. E. Bychkova, V. N. Uversky, and A. M. Gronenborn. 2000. Multisite fluorescence in proteins with multiple tryptophan residues. APO myoglobin natural variants and site-directed mutants. J. Bio. Chem. 275:36285-36294.
15. Chattopadhyay, A., S. S. Rawat, D. A. Kelkar, S. Ray, and A. Chakrabarti. 2003. Organization and dynamics of tryptophan residues in erythroid spectrin: novel structural features of denatured spectrin revealed by the wavelength-selective fluorescence approach. Protein Sci. 12:2389-2403.
16. Dubey, V. K., and M. V. Jagannadham. 2003. Differences in the unfolding of procerain induced by pH, guanidine hydrochloride, urea, and temperature. Biochemistry. 42:12287-12297.
17. Tew, D. J., and S. P. Bottomley. 2001. Probing the equilibrium denaturation of the serpin alpha(1)-antitrypsin with single tryptophan mutants; evidence for structure in the urea unfolded state. J. Mol. Biol. 313:1161-1169.
18. Saxena, A. M., J. B. Udgaonkar, and G. Krishnamoorthy. 2006. Characterization of intra-molecular distances and site-specific dynamics in chemically unfolded Barstar: evidence for denaturant-dependent non-random structure. J. Mol. Biol. 359:174-189.
19. Vangala, S., G. Vidugiris, and C. Royer. 1998. Probing the relation between protein structure and intrinsic tryptophan fluorescence using super repressor mutants of the Trp repressor. J. Fluoresc. 8:1-11.
20. Nath, U., and J. B. Udgaonkar. 1997. Folding of tryptophan mutants of Barstar: evidence for an initial hydrophobic collapse on the folding pathway. Biochemistry. 36:8602-8610.
21. Nanda, V., S. M. Liang, and L. Brand. 2000. Hydrophobic clustering in acid-denatured IL-2 and fluorescence of a Trp NH-pi H-bond. Biochem. Biophys. Res. Commun. 279:770-778.
22. Chattopadhyay, K., E. L. Elson, and C. Frieden. 2005. The kinetics of conformational fluctuations in an unfolded protein measured by fluorescence methods. Proc. Natl. Acad. Sci. USA. 102:2385-2389.
23. Merchant, K. A., R. B. Best, J. M. Louis, I. V. Gopich, and W. A. Eaton. 2007. Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. Proc. Natl. Acad. Sci. USA. 104:1528-1533.
24. Sinha, K. K., and J. B. Udgaonkar. 2007. Dissecting the non-specific and specific components of the initial folding reaction of Barstar by multi-site FRET measurements. J. Mol. Biol. 370:385-405.
25. Shehu, A., L. E. Kavraki, and C. Clementi. 2007. On the characterization of protein native state ensembles. Biophys. J. 92:1503-1511.
26. Tanford, C., K. Kawahara, S. Lapanje, T. M. Hooker, Jr., M. H. Zarlengo, A. Salahuddin, K. C. Aune, and T. Takagi. 1967. Proteins as random coils. 3. Optical rotatory dispersion in 6 M guanidine hydrochloride. J. Am. Chem. Soc. 89:5023-5029.
27. Rose, G. D. (editor). 2002. Advances in Protein Chemistry, Vol. 62. Elsevier, New York.
28. Matsuo, K., Y. Sakurada, R. Yonehara, M. Kataoka, and K. Gekko. 2007. Secondary-structure analysis of denatured proteins by vacuum ultraviolet circular dichroism spectroscopy. Biophys. J. 92:4088-4096.
29. Tanford, C. 1968. Protein denaturation. Adv. Protein Chem. 23:121-282.
30. Miller, W. G., and C. V. Goebel. 1968. Dimensions of protein random coils. Biochemistry. 7:3925-3935.
31. Kohn, J. E., I. S. Millett, J. Jacob, B. Zagrovic, T. M. Dillon, N. Cingel, R. S. Dothager, S. Seifert, P. Thiyagarajan, T. R. Sosnick, M. Z. Hasan, V. S. Pande, I. Ruczinski, S. Doniach, and K. W. Plaxco. 2004. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl. Acad. Sci. USA. 101:12491-12496.
32. Shortle, D. 2002. The expanded denatured state: an ensemble of conformations trapped in a locally encoded topological space. Adv. Protein Chem. 62:1-23.
33. Dill, K. A., and D. Shortle. 1991. Denatured states of proteins. Annu. Rev. Biochem. 60:795-825.
34. Denisov, V. P., B. H. Jonsson, and B. Halle. 1999. Hydration of denatured and molten globule proteins. Nat. Struct. Biol. 6:253-260.
35. Shortle, D., and M. S. Ackerman. 2001. Persistence of native-like topology in a denatured protein in 8 M urea. Science. 293:487-489.
36. Klein-Seetharaman, J., M. Oikawa, S. B. Grimshaw, J. Wirmer, E. Duchardt, T. Ueda, T. Imoto, L. J. Smith, C. M. Dobson, and H. Schwalbe. 2002. Long-range interactions within a nonnative protein. Science. 295:1719-1722.
37. Ferreon, A. C., and D. W. Bolen. 2004. Thermodynamics of denaturant-induced unfolding of a protein that exhibits variable two-state denaturation. Biochemistry. 43:13357-13369.
38. Mok, Y. K., C. M. Kay, L. E. Kay, and J. Forman-Kay. 1999. NOE data demonstrating a compact unfolded state for an SH3 domain under non-denaturing conditions. J. Mol. Biol. 289:619-638.
39. Dyson, H. J., and P. E. Wright. 2002. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv. Protein Chem. 62:311-340.
40. Anil, B., Y. Li, J. H. Cho, and D. P. Raleigh. 2006. The unfolded state of NTL9 is compact in the absence of denaturant. Biochemistry. 45:10110-10116.
41. Choy, W. Y., F. A. Mulder, K. A. Crowhurst, D. R. Muhandiram, I. S. Millett, S. Doniach, J. D. Forman-Kay, and L. E. Kay. 2002. Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques. J. Mol. Biol. 316:101-112.
42. Mayor, U., J. G. Grossmann, N. W. Foster, S. M. Freund, and A. R. Fersht. 2003. The denatured state of Engrailed Homeodomain under denaturing and native conditions. J. Mol. Biol. 333:977-991.
43. Goldenberg, D. P. 2003. Computational simulation of the statistical properties of unfolded proteins. J. Mol. Biol. 326:1615-1633.
44. 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.
45. Fitzkee, N. C., and G. D. Rose. 2005. Sterics and solvation window accessible conformational space for unfolded proteins. J. Mol. Biol. 353:873-887.
46. Jha, A. K., A. Colubri, K. F. Freed, and T. R. Sosnick. 2005. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc. Natl. Acad. Sci. USA. 102:13099-13104.
47. Tran, H. T., and R. V. Pappu. 2006. Toward an accurate theoretical framework for describing ensembles for proteins under strongly denaturing conditions. Biophys. J. 91:1868-1886.
48. Thurlkill, R. L., G. R. Grimsley, J. M. Scholtz, and C. N. Pace. 2006. Hydrogen bonding markedly reduces the pK of buried carboxyl groups in proteins. J. Mol. Biol. 362:594-604.
49. Trevino, S. R., K. Gokulan, S. Newsom, R. L. Thurlkill, K. L. Shaw, V. A. Mitkevich, A. A. Makarov, J. C. Sacchettini, J. M. Scholtz, and C. N. Pace. 2005. Asp79 makes a large, unfavorable contribution to the stability of RNase Sa. J. Mol. Biol. 354:967-978.
50. Trevino, S. R., J. M. Scholtz, and C. N. Pace. 2007. Amino acid contribution to protein solubility: Asp, Glu, and Ser contribute more favorably than the other hydrophilic amino acids in RNase Sa. J. Mol. Biol. 366:449-460.
51. Sevcik, J., V. S. Lamzin, Z. Dauter, and K. S. Wilson. 2002. Atomic resolution data reveal flexibility in the structure of RNase Sa. Acta Crystallogr. D Biol. Crystallogr. 58:1307-1313.
52. 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.
53. 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.
54. 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.
55. Alston, R. W., L. Urbanikova, J. Sevcik, M. Lasagna, G. D. Reinhart, J. M. Scholtz, and C. N. Pace. 2004. Contribution of single tryptophan residues to the fluorescence and stability of ribonuclease Sa. Biophys. J. 87:4036-4047.
56. 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. IRL Press, Oxford. 299-321.
57. 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.
58. Hebert, E. J., A. Giletto, J. Sevcik, L. Urbanikova, K. S. Wilson, Z. Dauter, and C. N. Pace. 1998. Contribution of a conserved asparagine to the conformational stability of ribonucleases Sa, Ba, and T1. Biochemistry. 37:16192-16200.
59. 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.
60. Alston, R. W., M. Lasagna, J. M. Scholtz, G. D. Reinhart, and C. N. Pace. 2008. Peptide sequence and conformation strongly influence tryptophan fluorescence. Biophys. J. 94:2280-2287.
61. 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.
62. Eftink, M. R. 1991. Fluorescence Techniques for Studying Protein- Structure. Methods Biochem. Anal. 35:127-205.
63. Vivian, J. T., and P. R. Callis. 2001. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80:2093-2109.
64. Callis, P. R. 1997. 1La and 1Lb transitions of tryptophan: applications of theory and experimental observations to fluorescence of proteins. Methods Enzymol. 278:113-150.
65. Chakraborty, S., V. Ittah, P. Bai, L. Luo, E. Haas, and Z. Peng. 2001. Structure and dynamics of the alpha-lactalbumin molten globule: fluorescence studies using proteins containing a single tryptophan residue. Biochemistry. 40:7228-7238.
66. Cowgill, R. W. 1967. Fluorescence and protein structure. X. Reappraisal of solvent and structural effects. Biochim. Biophys. Acta. 133:6-18.
67. Eftink, M. R., Y. Jia, D. Hu, and C. A. Ghiron. 1995. Fluorescence studies with tryptophan analogues: excited state interactions involving the side chain amino group. J. Phys. Chem. 99:5713-5723.
68. Hellings, M., M. De Maeyer, S. Verheyden, Q. Hao, E. J. Van Damme, W. J. Peumans, and Y. Engelborghs. 2003. The dead-end elimination method, tryptophan rotamers, and fluorescence lifetimes. Biophys. J. 85:1894-1902.
69. Pan, C. P., and M. D. Barkley. 2004. Conformational effects on tryptophan fluorescence in cyclic hexapeptides. Biophys. J. 86:3828-3835.
70. Callis, P. R., and T. Q. Liu. 2004. Quantitative prediction of fluorescence quantum yields for tryptophan in proteins. J. Phys. Chem. B. 108:4248-4259.
71. Chen, J., S. L. Flaugh, P. R. Callis, and J. King. 2006. Mechanism of the highly efficient quenching of tryptophan fluorescence in human gammaD-crystallin. Biochemistry. 45:11552-11563.
72. Bowler, B. E. 2007. Thermodynamics of protein denatured states. Mol. Biosyst. 3:88-99.
73. Baldwin, R. L. 2002. Making a network of hydrophobic clusters. Science. 295:1657-1658.
74. Eftink, M. R., and K. A. Hagaman. 1986. Viscosity dependence of the solute quenching of the tryptophanyl fluorescence of proteins. Biophys.Chem. 25:277-282.