Mapping Oxygen Accessibility to Ribonuclease A Using High-Resolution NMR Relaxation Spectroscopy

Biophysical Journal

Volumn 86, Issue 3, 2004, Pages 1713-1725

  Teng, Ching Ling ^a   Bryant, Robert G ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; RIBONUCLEASE A;

ARTICLE; CATTLE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

BOS TAURUS;

EID: 1542285241     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74240-X     Document Type: Article

References (61)

1. Altenbach, C., S. L. Flitsch, H. G. Khorana, and W. L. Hubbell. 1989a. Structural studies on transmembrane proteins. 2. Spin labeling of bacteriorhodopsin mutants at unique cysteines. Biochemistry. 28:7806-7812.
2. Altenbach, C., W. Froncisz, J. S. Hyde, and W. L. Hubbell. 1989b. Conformation of spin-labeled melittin at membrane surfaces investigated by pulse saturation recovery and continuous wave power saturation electron paramagnetic resonance. Biophys. J. 56:1183-1191.
3. Bloembergen, N., E. M. Purcell, and R. V. Pound. 1948. Relaxation effects in nuclear magnetic resonance absorption. Physical Review. 73:679-712.
4. Bryant, R. G. 1996. The dynamics of water-protein interactions. Annu. Rev. Biophys. Biomol. Struct. 25:29-53.
5. Calhoun, D. B., J. M. Vanderkooi, and S. W. Englander. 1983a. Penetration of small molecules into proteins studied by quenching of phosphorescence and fluorescence. Biochemistry. 22:1533-1539.
6. Calhoun, D. B., J. M. Vanderkooi, G. R. Holtom, and S. W. Englander. 1986. Protein fluorescence quenching by small molecules: protein penetration versus solvent exposure. Proteins. 1:109-115.
7. Calhoun, D. B., J. M. Vanderkooi, G. V. Woodrow III, and S. W. Englander. 1983b. Penetration of dioxygen into proteins studied by quenching of phosphorescence and fluorescence. Biochemistry. 22:1526-1532.
8. Carrero, J., D. M. Jameson, and E. Gratton. 1995. Oxygen penetration and diffusion into myoglobin revealed by quenching of zincprotoporphyrin IX fluorescence. Biophys. Chem. 54:143-154.
9. Case, D. A., and M. Karplus. 1979. Dynamics of ligand binding to heme proteins. J. Mol. Biol. 132:343-368.
10. Cocco, M. J., and J. T. Lecomte. 1994. The native state of apomyoglobin described by proton NMR spectroscopy: interaction with the paramagnetic probe hytempo and the fluorescent dye ans. Protein Sci. 3:267-281.
11. Dixon, M. E., T. K. Hitchens, and R. G. Bryant. 2000. Comparisons of pressure and temperature activation parameters for amide hydrogen exchange in t4 lysozyme. Biochemistry. 39:248-254.
12. Esposito, G., A. M. Lesk, H. Molinari, A. Motta, N. Niccolai, and A. Pastore. 1992. Probing protein structure by solvent perturbation of nuclear magnetic resonance spectra. Nuclear magnetic resonance spectral editing and topological mapping in proteins by paramagnetic relaxation filtering. J. Mol. Biol. 224:659-670.
13. Feher, V. A., E. P. Baldwin, and F. W. Dahlquist. 1996. Access of ligands to cavities within the core of a protein is rapid. Nat. Struct. Biol. 3:516-521.
14. Freed, J. H. 1978. Dynamic effects of pair correlation functions on spin relaxation by translational diffusion in liquids. II. Finite jumps and independent t1 processes. J. Chem. Phys. 68:4034-4037.
15. Gotte, G., M. Bertoldi, and M. Libonati. 1999. Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme. Eur. J. Biochem. 265:680-687.
16. Gratton, E., D. M. Jameson, G. Weber, and B. Alpert. 1984. A model of dynamic quenching of fluorescence in globular proteins. Biophys. J. 45:789-794.
17. Halle, B., and V. P. Denisov. 1995. A new view of water dynamics in immobilized proteins. Biophys. J. 69:242-249.
18. Hernandez, G., C. L. Teng, R. G. Bryant, and D. M. LeMaster. 2002. O2 penetration and proton burial depth in proteins: applicability to fold family recognition. J. Am. Chem. Soc. 124:4463-4472.
19. Hitchens, T. K., and R. G. Bryant. 1998. Pressure dependence of amide hydrogen-deuterium exchange rates for individual sites in t4 lysozyme. Biochemistry. 37:5878-5887.
20. Hwang, L., and J. H. Freed. 1975. Dynamic effects of pair correlation functions on spin relaxation by translational diffusion in liquids. J. Chem. Phys. 63:4017-4025.
21. Kim, K. S., J. A. Fuchs, and C. K. Woodward. 1993. Hydrogen exchange identifies native-state motional domains important in protein folding. Biochemistry. 32:9600-9608.
22. Lakowicz, J. R., and G. Weber. 1973a. Quenching of fluorescence by oxygen. A probe for structural fluctuations in macromolecules. Biochemistry. 12:4161-4170.
23. Lakowicz, J. R., and G. Weber. 1973b. Quenching of protein fluorescence by oxygen. Detection of structural fluctuations in proteins on the nanosecond time scale. Biochemistry. 12:4171-4179.
24. Lee, B., and F. M. Richards. 1971. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:379-400.
25. Li, R., and C. Woodward. 1999. The hydrogen exchange core and protein folding. Protein Sci. 8:1571-1590.
26. Liu, Y., G. Gotte, M. Libonati, and D. Eisenberg. 2002. Structures of the two 3d domain swapped mase a trimers. Protein Sci. 11:371-380.
27. Liu, Y., P. J. Hart, M. P. Schlunegger, and D. Eisenberg. 1998. The crystal structure of a 3d domain-swapped dimer of mase a at a 2.1 a resolutioin. Proc. Natl. Acad. Sci. USA. 95:3437-3442.
28. Mansoor, S. E., H. S. McHaourab, and D. L. Farrens. 1999. Determination of protein secondary structure and solvent accessibility using site-directed fluorescence labeling. Studies of t4 lysozyme using the fluorescent probe monobromobimane. Biochemistry. 38:16383-16393.
29. 2+-protoporphyrin ix deoxymyoglobin mimic: application to oxygen migration pathway analysis. J. Am. Chem. Soc. 125:3813-3820.
30. Merlino, A., L. Vitagliano, M. A. Ceruso, A. Di Nola, and L. Mazzarella. 2002. Global and local motions in ribonuclease A: a molecular dynamics study. Biopolymers. 65:274-283.
31. Merlino, A., L. Vitagliano, M. A. Ceruso, and L. Mazzarella. 2003. Subtle functional collective motions in pancreatic-like ribonucleases: from ribonuclease A to angiogenin. Proteins. 53:101-110.
32. Molinari, H., G. Esposito, L. Ragona, M. Pegna, N. Niccolai, R. M. Brunne, A. M. Lesk, and L. Zetta. 1997. Probing protein structure by solvent perturbation of NMR spectra: the surface accessibility of bovine pancreatic trypsin inhibitor. Biophys. J. 73:382-396.
33. Niccolai, N., A. Ciutti, O. Spiga, M. Scarselli, A. Bernini, L. Bracci, D. Di Maro, C. Dalvit, H. Molinari, G. Esposito, and P. A. Temussi. 2001a. NMR studies of protein surface accessibility. J. Biol. Chem. 276:42455-42461.
34. Niccolai, N., G. Valensin, C. Rossi, and W. Gibbons. 1982. The stereochemistry and dynamics of natural products and biopolymers from proton relaxation spectroscopy: spin label delineation of inner and outer protons of gramicidin s including hydrogen bonds. J. Amer. Chem. Soc. 104:1534-1537.
35. Niccolai, N., C. Rossi, G. Valensin, P. Mascagni, and W. A. Gibbons. 1984. An investigation of the mechanisms of nitroxide-induced proton relaxation enhancements in biopolymers. J. Phys. Chem. 88:5689-5692.
36. Niccolai, N., R. Spadaccini, M. Scarselli, A. Bernini, O. Crescenzi, O. Spiga, A. Ciutti, D. Di Maro, L. Bracci, C. Dalvit, and P. A. Temussi. 2001b. Probing the surface of a sweet protein: NMR study of MNEI with a paramagnetic probe. Protein Sci. 10:1498-1507.
37. Otting, G., E. Liepinsh, B. Halle, and U. Frey. 1997. NMR identification of hydrophobic cavities with low water occupancies in protein structures using small gas molecules. Nat. Struct. Biol. 4:396-404.
38. 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.
39. Piantini, U., O. W. Sorensen, and R. R. Ernst. 1982. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104:6800-6801.
40. Pintacuda, G., and G. Otting. 2002. Identification of protein surfaces by NMR measurements of a paramagnetic gd(III) chelate. J. Am. Chem. Soc. 124:372-373.
41. Polnaszek, C. F., and R. G. Bryant. 1984. Nitroxide radical induced solvent proton relaxation: measurement of localized translational diffusion. J. Chem. Phys. 81:4038-4045.
42. Prosser, R. S., P. A. Luchette, and P. W. Westerman. 2000. Using O2 to probe membrane immersion depth by 19F NMR. Proc. Natl. Acad. Sci. USA. 97:9967-9971.
43. Prosser, R. S., P. A. Luchette, P. W. Westerman, A. Rozek, and R. E. Hancock. 2001. Determination of membrane immersion depth with O(2): a high-pressure (19)F NMR study. Biophys. J. 80:1406-1416.
44. Rance, M., O. W. Sorensen, G. Bodenhausen, G. Wagner, R. R. Ernst, and K. Wuthrich. 1983. Improved spectral resolution in cosy 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:479-485.
45. Rasmssen, B. F., A. M. Stock, D. Ringe, and G. A. Petsko. 1992. Crystalline ribonuclease A loses function below the dynamical transition at 220 k. Nature. 357:423-424.
46. Rico, M., M. Bruix, J. Santoro, C. Gonzalez, J. L. Neira, J. L. Nieto, and J. Herranz. 1989. Sequential 1H-NMR assignment and solution structure of bovine pancreatic ribonuclease A. Eur. J. Biochem. 183:623-638.
47. Robertson, A. D., E. O. Purisima, M. A. Eastman, and H. A. Scheraga. 1989. Proton NMR assignments and regular backbone structure of bovine pancreatic ribonuclease A in aqueous solution. Biochemistry. 28:5930-5938.
48. Sadasivan, C., H. G. Nagendra, and M. Vijayan. 1998. Plasticity, hydration and accessibility in ribonuclease A. The structure of a new crystal form and its low-humidity variant. Acta Crystallogr. D Biol. Crystallogr. 54:1343-1352.
49. Santoro, J., C. Gonzalez, M. Bruix, J. L. Neira, J. L. Nieto, J. Herranz, and M. Rico. 1993. High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 229:722-734.
50. Savage, H., and A. Wlodawer. 1986. Determination of water structure around biomolecules using x-ray and neutron diffraction methods. Methods Enzymol. 127:162-183.
51. Scheraga, H. A., W. J. Wedemeyer, and E. Welker. 2001. Bovine pancreatic ribonuclease A: oxidative and conformational folding studies. Methods Enzymol. 341:189-221.
52. Solomon, I. 1955. Relaxation processes in a system of two spins. Physcial Review. 99:559-565.
53. Teng, C. L., and R. G. Bryant. 2000. Experimental measurement of nonuniform dioxygen accessibility to ribonuclease A surface and interior. J. Am. Chem. Soc. 122:2667-2668.
54. Teng, C. L., H. Hong, S. Kiihne, and R. G. Bryant. 2001. Molecular oxygen spin-lattice relaxation in solutions measured by proton magnetic relaxation dispersion. J. Magn. Reson. 148:31-34.
55. Victor, K., and D. S. Cafiso. 1998. Structure and position of the n-terminal membrane-binding domain of pp60src at the membrane interface. Biochemistry. 37:3402-3410.
56. Wang, A., A. D. Robertson, and D. W. Bolen. 1995. Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry. 34:15096-15104.
57. Wilhelm, E., R. Battino, and R. J. Wilcock. 1977. Low-pressure solubility of gasses in liquid water. Chem. Rev. 77:219-262.
58. Wlodawer, A., L. A. Svensson, L. Sjolin, and G. L. Gilliland. 1988. Structure of phosphate-free ribonuclease A refined at 1.26 A. Biochemistry. 27:2705-2717.
59. Woodward, C., I. Simon, and E. Tuchsen. 1982. Hydrogen exchange and the dynamic structure of proteins. Mol. Cell. Biochem. 48:135-160.
60. Woodward, C. K., and A. Rosenberg. 1971. Studies of hydrogen exchange in proteins. V. The correlation of ribonuclease exchange kinetics with the temperature-induced transition. J. Biol. Chem. 246:4105-4113.
61. Zhou, N., P. Mascagni, W. Gibbons, N. Niccolai, C. Rossi, and H. Wyssbrod. 1985. Confirmation of the solution structure of tyrocidine a using perturbation of proton relaxation rates by nitroxide spin labels. J. Chem. Soc. Perkin Trans. 2:581-587.