Tryptophan dynamics of the FK506 binding protein: Time-resolved fluorescence and simulations

Biophysical Journal

Volumn 70, Issue 3, 1996, Pages 1122-1137

  Silva Jr , Norberto D ^a   Prendergast, Franklyn G ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG BINDING PROTEIN; RAPAMYCIN; TACROLIMUS; TRYPTOPHAN;

ABSORPTION SPECTROPHOTOMETRY; ANISOTROPY; ARTICLE; CIRCULAR DICHROISM; DRUG PROTEIN BINDING; FLUORESCENCE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE;

EID: 0030052607     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79706-0     Document Type: Article

References (67)

1. Albers, M. W., C. T. Walsh, and S. L. Schreiber. 1990. Substrate specificity for the human rotamase FKBP: a view of FK506 and rapamycin as leucine-(twisted amide)-proline mimics. J. Org. Chem. 55:4984-4986.
2. 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.
3. Bajzer, Z., and F. G. Prendergast. 1993. A model for multiexponential tryptophan fluorescence intensity decay in proteins. Biophys. J. 65: 2313-2323.
4. Bajzer, Z., A. Zelic, and F. G. Prendergast. 1995. Analytical approach to the recovery of short fluorescence lifetimes from fluorescence decay curves. Biophys. J. 69:1148-1161.
5. Becker, J. W., J Rotonda, B. M. McKeever, H. K. Chan, A. I. Marcy, G. Wiederrecht, J. D. Hermes, and J. P. Springer. 1993. FK-506-binding protein: Three-dimensional structure of the complex with the antagonist L-685,818. J. Biol. Chem. 268:11335-11339.
6. Beechem, J. M., and L. Brand. 1985. Time-resolved fluorescence of proteins. Annu. Rev. Biochem. 53:43-71.
7. Beechem, J. M., and E. Gratton. 1988. Fluorescence spectroscopy data analysis environment: a second generation global analysis program. Proc. SPIE 909:70-81.
8. Bierer, B. E., P. S. Mattila, R. F. Standaert, L. A. Herzenberg, S. J. Burakoff, G. Crabtree, and S. L. Schreiber. 1990. Two distinct signal transmission pathways in T lymphocytes are inhibited by complexes formed between an immunophilin and either FK506 or rapamycin. Proc. Natl. Acad. Sci. USA 87:9231-9235.
9. Brooks, C. L., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy. minimization and dynamics calculations. J. Comp. Chem. 4:187-217.
10. Brown, E. J , M. W. Albers, T. B. Shin, K. Ichikawa, C. T. Keith, W. S. Lane, and S. L. Schreiber. 1994. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature. 369:756-758.
11. 15N NMR relaxation studies of the FK506 binding protein: backbone dynamics of the uncomplexed receptor. Biochemistry. 32:9000-9010.
12. 15N NMR relaxation studies of the FK506 binding protein: dynamic effects of ligand binding and implications for calcineurin recognition. Biochemistry. 33: 4093-4100.
13. Clipstone, N. A., and G R. Crabtree 1992. Identification of calcineurin as a key signaling enzyme in T-lymphocyte activation. Nature. 357: 695-697.
14. Demas, J. N., and G. A. Crosby. 1971. The measurement of photoluminescence quantum yields. A review. J. Phys. Chem. 75:991-1024.
15. Egan, D A., T M. Logan, H. Liang, E. Matayoshi, S. W. Fesik, and T. F. Holzman 1993. Equilibrium denaturation of recombinant human FK binding protein in urea. Biochemistry. 32:1920-1927.
16. Fischer, S., S. Michnick, and M. Karplus. 1993. A mechanism for the rotamase catalysis by the FK506 binding protein (FKBP). Biochemistry. 32:13830-13837.
17. Frauenfelder, H., F. Parak, and R. D. Young. 1988. Conformational substates in proteins. Annu. Rev. Biophys. Biophys. Chem. 17:451-479.
18. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes 1991. The energy landscapes and motions of proteins. Science 254:1598-1603.
19. Griffith, J. P., J. L. Kim, E. E Kim, M. D. Sintchak, J. A. Thomson, M. J. Fitzgibbon, M. A. Fleming, R. R. Caron, K. Hsiao, and M. A. Navia. 1995. X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell. 82 507-522.
20. Harding, M. W., A. Galat, D. E. Uehling, and S. L. Schreiber 1989. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature. 341:758-760.
21. Hams, D. L., and B. S. Hudson. 1990. Photophysics of tryptophan in bacteriophage T4 lysozymes. Biochemistry. 29-5276-5285.
22. Harrison, R K., and R. L. Stein 1990. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry. 29:3813-3816.
23. Haydock, C. 1993. Protein side chain rotational isomerization: a minimum perturbation mapping study J. Chem. Phys. 98:8199-8214.
24. Humik, C. M., and A. G. Szabo. 1989. Confirmation that multiexponential fluorescence decay behavior of holoazurin originates from conformational heterogeneity. Biochemistry. 28:3923-3934.
25. Janes, S. M., G. Holtom, P. Ascenzi, M. Brunori, and R. M. Hochstrasser. 1987. Fluorescence and energy transfer of tryptophans in aplysia myoglobin. Biophys. J. 51:653-660.
26. 13C NMR and fluorescence anisotropy measurements of tryptophan dynamics in wild-type and two single-tryptophan variants of Escherichia coli thioredoxin. Biophys. J. 66:2111-2126.
27. Lakowicz, J. R. 1983. Instrumentation for fluorescence spectroscopy. In Principles of fluorescence spectroscopy. Plenum Press, New York. 44.
28. Lakowicz, J. R., B. P. Maliwal, H. Cherek, and A. Balter. 1983. Rotational freedom of tryptophan residues in proteins and peptides. Biochemistry. 22:1741-1752.
29. Lepre, C. A., J. W. Cheng, and J. M. Moore. 1993. Dynamics of a receptor-bound ligand by heteronuclear NMR:FK506 bound to FKBP-12. J. Am. Chem. Soc. 115:4929-4930.
30. Liu, J., J. D. Farmer, Jr., W. S. Lane, J. Friedman, I. Weissman, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66:807-815.
31. Marquis-Omer, D., G. Sanyal, D. B. Volkin, A. I. Marcy, H. K. Chan, J. A. Ryan, and C. R. Middaugh. 1991. Stabilization of the FK506 binding protein by ligand binding. Biochem. Biophys. Res. Commun. 179: 741-748.
32. McKinnon, A. E., A. G. Szabo, and D. R. Miller. 1977. The deconvolution of photoluminiscence data. J. Phys. Chem. 81:1564-1567.
33. Michnick, S. W., M. K. Rosen, T. J. Wandless, M. Karplus, and S. L. Schreiber. 1991. Solution structure of FKBP, a rotamase enzyme and receptor for FK506 and rapamycin. Science. 252:836-839.
34. Momany, F. A., and R. Rone. 1992. Validation of the general purpose QUANTA3.2/CHARMm force field. J. Comp. Chem. 13:888-900.
35. Moore, J. M., D. A. Peattie, M. J. Fitzgibbon, and J. A. Thomson. 1991. Solution structure of the major binding protein for the immunosuppressant FK506. Nature. 351:248-250.
36. Munro, I., I. Pecht, and L. Stryer. 1979, Subnanosecond motions of tryptophan residues in proteins. Proc. Natl Acad. Sci. USA. 76:56-60.
37. O'Connor, D. V., and D. Phillips. 1984. Time-correlated Single Photon Counting. 1st ed. Academic Press. New York.
38. Orozco, M., J. Tirado-Rives, and W. L. Jorgensen. 1993. Mechanism for the rotamase activity of FK506 binding protein from molecular dynamics simulations. Biochemistry. 32:12864-12874.
39. 13C NMR spectroscopy and time-resolved fluorescence spectroscopy. J. Am. Chem. Soc. 115:6333-6345.
40. Pang. Y.-P., N. D. Silva, C. Haydock, and F. G. Prendergast. Docking studies of FKBP with its ligands: An induced-fit mechanism in the binding of FKBP. In QSAR and Molecular Modeling. In press.
41. Park. S. T., R. A. Aldape, O. Futer, M. T. DeCenzo, and D. J. Livingston. 1992 PPIase catalysis by human FK506-binding protein proceeds through a conformational twist mechanism. J. Biol. Chem. 267: 3316-3324.
42. Rasmussen, B. F., A. M. Stock, D Ringe, and G. A. Petsko. 1992 Crystalline ribonuclease A loses function below the dynamical transition at 220K. Nature. 357:423-424.
43. Rayner, D. M., and A G. Szabo. 1978. Time resolved fluorescence of aqueous tryptophan. Can. J. Chem. 56:743-745.
44. Ruggiero, A J., D. C. Todd, and G. R. Fleming 1990. Subpicosecond fluorescence anisotropy studies of tryptophan in water. J. Am. Chem. Soc. 112:1003-1014.
45. Saito, I., H Sugiyama, A. Yamamoto, S. Muramatsu, and T. Matsuura. 1984. Photochemical hydrogen-deuterium exchange reaction of tryptophan. The role in non-radiative decay of singlet tryptophan. J. Am. Chem. Soc. 106:4286-4287.
46. Schevitz, R. W., N. J. Bach, D. G. Carlson, N. Y. Chirgadze, D. K. Clawson, R D. Dillard, S. E. Drahmeim, L. W. Hartley, N. D. Jones, E. D. Mihelich, J. L. Olkowski, D W. Snyder, C. Sommers, and J.-P. Wery. 1995. Structure-base design of the first potent and selective inhibitor of human non-pancreatic secretory phospholipase A,. Nature Struct Biol. 2:458-465.
47. Schreiber, S. L. 1992. Immunophilin-sensitive protein phosphatase action in cell signaling pathways. Cell. 70:365-368.
48. Schreiber, S. L., and G. R. Crabtree. 1992. The mechanism of action of cyclosporin A and FK506. Immunol. Today. 13:136-142.
49. Sharp, K. A. 1993. Inclusion of solvent effects in molecular mechanics force fields. In Computer Simulation of Biomolecular Systems. Theoretical and Experimental Applications. Vol. 2. W. F. Gunsteren, P. K. Weiner, and A. J. Wilkinson, editors. ESCOM, Leiden. 147-160.
50. Shizuka, H., M. Serizawa, T. Shimo, I. Saito, and T Matsuura. 1988. Fluorescence-quenching mechanism of tryptophan. Remarkably efficient internal proton-induced quenching and charge-transfer quenching. J. Am. Chem. Soc. 110:1930-1934.
51. Siekierka, J. J., S. H. Y. Hung, M. Poe, C. S. Lin, and N. H. Sigal. 1989. A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature. 341:755-757.
52. Sigal, N. H., and F. J. Dumont. 1992. Cyclosporin A. FK-506 and rapamycin: pharmacologic probes of lymphocyte signal transduction. Annu. Rev. Immunol. 10:519-560.
53. Starzl, T. E. 1993. FK506 versus cyclosporine. Transplant. Proc. 25: 511-512.
54. Starzl, T. E., J. Fung, M. Jordan, R. Shapiro, A. Tzakis, J. McCauley, J. Johnston, Y. Iwaki, A. Jain, M. Alessiani, and S. Todo. 1990. Kidney transplantation under FK506. JAMA. 264:63-67.
55. Steiner, R. F., and E. P. Kirby. 1969. The interaction of the ground and excited states of indole derivatives with electron scavengers. J. Phys. Chem. 73:4130-4135.
56. Szabo, A. G., and C. Faerman. 1992. Dilemma of correlating fluorescence quantum yields and intensity decay times in single tryptophan mutant proteins SPIE. Time-Resolve Laser Spectroscopy in Biochemistry III. 1640:70-80.
57. Thomson, A. W. 1989. FK-506 - how much potential? Immunol. Today. 10:6-9.
58. b, excitation bands. Photochem. Photobiol. 25:441-444.
59. Van Duyne, G. D., R. F. Standaert, P. A. Karplus, S. L. Schreiber, and J. Clardy. 1991a. Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science. 252:839-842.
60. Van Duyne, G. D., R. F. Standaert, S. L. Schreiber, and J. Clardy. 1991b. Atomic structure of the rapamycin human immunophilin FKBP-12 complex J. Am. Chem. Soc. 113.7433-7434.
61. van Gunsteren, W. F., and M. Karplus. 1980. A method for constrained energy minimization of macro molecules. J Comp. Chem. 1:266-274.
62. Verlinde, C. L. M. J., and B. W. Dijkstra. 1995. Drug or tool, design or serendipity? Nature Struct. Biol. 2:429-432.
63. Wetlaufer, D. B. 1962. Ultraviolet absorption spectra of proteins and amino acids. Adv. Protein Chem. 17:303-390.
64. Wiederrecht, G., S. Hung, H. K. Chan, A. Marcy, M. Martin, J. Calaycay, D. Boulton, N. Sigal, R. L. Kincaid, and J. J. Siekierka. 1992. Characterization of high molecular weight FK-506 binding activities reveals a novel FK-506-binding protein as well as a protein complex. J. Biol. Chem. 267:21753-21760.
65. Wilson, K. P., M. M. Yamashita, M. D. Sintchak, S. H. Rotstein, M. A. Murcko, J Boger, J. A. Thomson, M. J. Fitzgibbon, J. R Black, and M. A. Navia. 1995. Comparative x-ray structures of the major binding protein for the immunosuppressant FK506 (tacrolimus) in unliganded form and in complex with FK506 and rapamycin. Acta Crystallogr. D51:511-521.
66. Yamamoto, Y., and J. Tanaka. 1972. Polarized absorption of spectra of crystals of indole and its related compounds. Bull. Chem. Soc. Jpn. 45:1362-1366.
67. Yu, N. T. 1977. Raman spectroscopy: a conformational probe in biochemistry. CRC Crit. Rev. Biochem. 4:229-280.