Tryptophan conformations associated with partial unfolding in ribonuclease T1

Biophysical Journal

Volumn 97, Issue 6, 2009, Pages 1778-1786

  Moors, Samuel L C ^a   Jonckheer, Abel ^a,b   De Maeyer, Marc ^b   Engelborghs, Yves ^a   Ceulemans, Arnout ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b IRC KUL Campus Kortrijk   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; RIBONUCLEASE T1; TRYPTOPHAN;

ARTICLE; ELECTRIC POTENTIAL; FLUORESCENCE; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTON TRANSPORT; SIMULATION;

EID: 70350025164     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.07.015     Document Type: Article

References (42)

1. Moors, S. L. C., A. Jonckheer, M. De Maeyer, Y. Engelborghs, and A. Ceulemans. 2008. How do rotameric conformations influence the time-resolved fluorescence of tryptophan in proteins? A perspective based on molecular modeling and quantum chemistry. Curr. Protein Pept. Sci. 9:427-446.
2. Donzel, B., P. Gauduchon, and P. Wahl. 1974. Study of the conformation in the excited state of two tryptophanyl diketopiperazines. J. Am. Chem. Soc. 96:801-808.
3. Gauduchon, P., and P. Wahl. 1978. Pulsefluorimetry of tyrosyl peptides. Biophys. Chem. 8:87-104.
4. Lakowicz, J. R. 2000. On spectral relaxation in proteins. Photochem. Photobiol. 72:421-437.
5. Moors, S. L. C., M. Hellings, M. De Maeyer, Y. Engelborghs, and A. Ceulemans. 2006. Tryptophan rotamers as evidenced by X-ray, fluorescence lifetimes, and molecular dynamics modeling. Biophys. J. 91:816-823.
6. Fushman, D., O. Ohlenschlager, and H. Ruterjans. 1994. Determination of the backbone mobility of ribonuclease-T1 and its 2′GMP complex using molecular-dynamics simulations and NMR relaxation data. J. Biomol. Struct. Dyn. 11:1377-1402.
7. Elofsson, A., and L. Nilsson. 1996. A 1.2 ns molecular dynamics simulation of the ribonuclease T-1-3′-guanosine monophosphate complex. J. Phys. Chem. 100:2480-2488.
8. Ababou, A., and E. Bombarda. 2001. On the involvement of electron transfer reactions in the fluorescence decay kinetics heterogeneity of proteins. Protein Sci. 10:2102-2113. (Pubitemid 32911229)
9. Mullins, L. S., C. N. Pace, and F. M. Raushel. 1997. Conformational stability of ribonuclease T1 determined by hydrogen-deuterium exchange. Protein Sci. 6:1387-1395. (Pubitemid 27299038)
10. Gohda, K., K. Oka, K. Tomita, and T. Hakoshima. 1994. Crystal-structure of RNase T1 complexed with the product 3′-GMP. Structural evidence for direct interaction of histidine 40 and glutamic acid 58 with the 2′-hydroxyl group of the ribose. J. Biol. Chem. 269:17531-17536.
11. Chen, L. X. Q., J. W. Longworth, and G. R. Fleming. 1987. Picosecond time-resolved fluorescence of ribonuclease T1. A pH and substrate analogue binding study. Biophys. J. 51:865-873.
12. Alcala, J. R., E. Gratton, and F. G. Prendergast. 1987. Interpretation of fluorescence decays in proteins using continuous lifetime distributions. Biophys. J. 51:925-936.
13. Mei, G., A. Di Venere, F. De Matteis, and N. Rosato. 2003. The recovery of dipolar relaxation times from fluorescence decays as a tool to probe local dynamics in single tryptophan proteins. Arch. Biochem. Biophys. 417:159-164.
14. Johnson, J. L., and F. M. Raushel. 1996. Influence of primary sequence transpositions on the folding pathways of ribonuclease T1. Biochemistry. 35:10223-10233.
15. Eftink, M. R., and C. A. Ghiron. 1987. Frequency-domain measurements of the fluorescence lifetime of ribonuclease-T1. Biophys. J. 52:467-473.
16. Gryczynski, I., M. Eftink, and J. R. Lakowicz. 1988. Conformation heterogeneity in proteins as an origin of heterogeneous fluorescence decays, illustrated by native and denatured ribonuclease T-1. Biochim. Biophys. Acta. 954:244-252.
17. Paschek, D., and A. E. Garcia. 2004. Reversible temperature and pressure denaturation of a protein fragment: a replica exchange molecular dynamics simulation study. Phys. Rev. Lett. 93:238105.
18. De Maeyer, M., J. Desmet, and I. Lasters. 2000. The dead-end elimination theorem: mathematical aspects, implementation, optimizations, evaluation, and performance. Methods Mol. Biol. 143:265-304.
19. Hellings, M., M.De Maeyer, S. Verheyden, Q. Hao, E. J. M. VanDamme, et al. 2003. The dead-end elimination method, tryptophan rotamers, and fluorescence lifetimes. Biophys. J. 85:1894-1902. (Pubitemid 37052269)
20. De Maeyer, M., J. Desmet, and I. Lasters. 1997. All in one: a highly detailed rotamer library improves both accuracy and speed in the modelling of sidechains by dead-end elimination. Fold. Des. 2:53-66.
21. Delhaise, P., M. Bardiaux, M. De Maeyer, M. Prevost, D. Vanbelle, et al. 1988. The Brugel package: toward computer-aided design of macromolecules. J. Mol. Graph. 6:219.
22. MacKerell, A. D.,D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
23. Spitzner, N., F. Lohr, S. Pfeiffer, A. Koumanov, A. Karshikoff, et al. 2001. Ionization properties of titratable groups in ribonuclease T-1-I. pK(a) values in the native state determined by two-dimensional heteronuclear NMR spectroscopy. European Biophysics Journal with Biophysics Letters. 30:186-197. (Pubitemid 32768852)
24. Leopold, P. E., M. Montal, and J. N. Onuchic. 1992. Protein folding funnels: a kinetic approach to the sequence structure relationship. Proc. Natl. Acad. Sci. USA. 89:8721-8725.
25. 25-ribonuclease T1. Biol. Chem. 384:1173-1183.
26. Pfeiffer, S., Y. Karimi-Nejad, and H. Rüterjans. 1997. Limits of NMR structure determination using variable target function calculations: ribonuclease T1, a case study. J. Mol. Biol. 266:400-423.
27. Shirley, B. A., P. Stanssens, J. Steyaert, and C. N. Pace. 1989. Conformational stability and activity of ribonuclease-T1 and mutants. Gln25-Lys, Glu58-Ala, and the double mutant. J. Biol. Chem. 264:11621-11625.
28. Kay, L. E. 1998. Protein dynamics from NMR. Nat. Struct. Biol. 5:513-517.
29. Pace, C. N., U. Heinemann, U. Hahn, and W. Saenger. 1991. Ribonuclease-T1: structure, function, and stability. Angew. Chem. Int. Ed. Engl. 30:343-360.
30. Thurlkill, R. L., G. R. Grimsley, 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.
31. Matsuura, H., S. Shimotakahara, C. Sakuma, M. Tashiro, H. Shindo, et al. 2004. Thermal unfolding of ribonuclease T1 studied by multidimensional NMR spectroscopy. Biol. Chem. 385:1157-1164.
32. Kiefhaber, T., R. Quaas, U. Hahn, and F. X. Schmid. 1990. Folding of ribonuclease-T1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry. 29:3061-3070.
33. Pace, C. N., D. V. Laurents, and J. A. Thomson. 1990. pH dependence of the urea and guanidine hydrochloride denaturation of ribonuclease A and ribonuclease T1. Biochemistry. 29:2564-2572. (Pubitemid 20100853)
34. McNutt, M., L. S. Mullins, F. M. Raushel, and C. N. Pace. 1990. Contribution of histidine residues to the conformational stability of ribonuclease T1 and mutant Glu-58-Ala. Biochemistry. 29:7572-7576. (Pubitemid 20279172)
35. Garrett, J. B., L. S. Mullins, and F. M. Raushel. 1996. Are turns required for the folding of ribonuclease T1? Protein Sci. 5:204-211.
36. James, D. R., D. R. Demmer, R. P. Steer, and R. E. Verrall. 1985. Fluorescence lifetime quenching and anisotropy studies of ribonuclease T1. Biochemistry. 24:5517-5526.
37. Meech, S. R., D. Phillips, and A. G. Lee. 1983. On the nature of the fluorescent state of methylated indole derivatives. Chem. Phys. 80:317-328.
38. Kiefhaber, T., F. X. Schmid, K. Willaert, Y. Engelborghs, and A. Chaffotte. 1992. Structure of a rapidly formed intermediate in ribonuclease T1 folding. Protein Sci. 1:1162-1172. (Pubitemid 23016430)
39. Lakowicz, J. R. 1999. Principles of Fluorescence Spectroscopy. Kluwer Academic, New York.
40. Eftink, M. R., and C. A. Ghiron. 1975. Dynamics of a protein matrix revealed by fluorescence quenching. Proc. Natl. Acad. Sci. USA. 72:3290-3294.
41. Bajzer, Z., and F. G. Prendergast. 1993. A model for multiexponential tryptophan fluorescence intensity decay in proteins. Biophys. J. 65:2313-2323. (Pubitemid 24005964)
42. Haydock, C., and F. G. Prendergast. 1993. Fluorescence intensity decay of ribonuclease T1 tryptophan-59: minimum perturbation mapping study of neighbor side-chain isomerization. 1993 Biophyical Society Meeting Abstracts. Biophys J., Supplement, 64:A54, Abstract, 180-Pos.