High-throughput protein structural analysis using site-directed fluorescence labeling and the bimane derivative (2-pyridyl)dithiobimane

Biochemistry

Volumn 43, Issue 29, 2004, Pages 9426-9438

  Mansoor, Steven E ^a   Farrens, David L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; CONTAMINATION; FLUORESCENCE; PROTEINS; QUENCHING;

FLUOROPHORES; PROTEIN FOLDING;

BIOCHEMISTRY;

(2 PYRIDYL)DITHIOBIMANE; CYSTEINE; FLUORESCENT DYE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; AUTOMATION; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; FLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS;

BICYCLO COMPOUNDS, HETEROCYCLIC; DISULFIDES; FLUORESCENT DYES; MODELS, MOLECULAR; PROTEIN CONFORMATION; SOLVENTS;

EID: 3242726738     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036259m     Document Type: Article

References (61)

1. Gether, U., Lin, S., and Kobilka, B. K. (1995) Fluorescent labeling of purified beta 2 adrenergic receptor. Evidence for ligand-specific conformational changes, J. Biol. Chem. 270, 28268-28275.
2. Shepard, L. A., Heuck, A. P., Hamman, B. D., Rossjohn, J., Parker, M. W., Ryan, K. R., Johnson, A. E., and Tweten, R. K. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an alpha-helical to beta-sheet transition identified by fluorescence spectroscopy, Biochemistry 37, 14563-14574.
3. Mansoor, S. E., McHaourab, H. S., and Farrens, D. L. (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.
4. Glauner, K. S., Mannuzzu, L. M., Gandhi, C. S., and Isacoff, E. Y. (1999) Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel, Nature 402, 813-817.
5. Cha, A., Snyder, G. E., Selvin, P. R., and Bezanilla, F. (1999) Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy, Nature 402, 809-813.
6. Dunham, T. D., and Farrens, D. L. (1999) Conformational changes in rhodopsin. Movement of helix f detected by site-specific chemical labeling and fluorescence spectroscopy, J. Biol. Chem. 274, 1683-1690.
7. Imamoto, Y., Kataoka, M., Tokunaga, F., and Palczewski, K. (2000) Light-induced conformational changes of rhodopsin probed by fluorescent alexa594 immobilized on the cytoplasmic surface, Biochemistry 39, 15225-15233.
8. Ghanouni, P., Steenhuis, J. J., Farrens, D. L., and Kobilka, B. K. (2001) Agonist-induced conformational changes in the G-protein-coupling domain of the beta 2 adrenergic receptor, Proc. Natl. Acad. Sci. U.S.A. 98, 5997-6002.
9. Navon, A., Ittah, V., Landsman, P., Scheraga, H. A., and Haas, E. (2001) Distributions of intramolecular distances in the reduced and denatured states of bovine pancreatic ribonuclease A. Folding initiation structures in the C-terminal portions of the reduced protein, Biochemistry 40, 105-118.
10. Mansoor, S. E., McHaourab, H. S., and Farrens, D. L. (2002) Mapping proximity within proteins using fluorescence spectroscopy. A study of T4 lysozyme showing that tryptophan residues quench bimane fluorescence, Biochemistry 41, 2475-2484.
11. Heyduk, T. (2002) Measuring protein conformational changes by FRET/LRET, Curr. Opin. Biotechnol. 13, 292-296.
12. Mielke, T., Alexiev, U., Glasel, M., Otto, H., and Heyn, M. P. (2002) Light-induced changes in the structure and accessibility of the cytoplasmic loops of rhodopsin in the activated MII state, Biochemistry 41, 7875-7884.
13. Sathish, H. A., Stein, R. A., Yang, G., and McHaourab, H. S. (2003) Mechanism of chaperone function in small heat-shock proteins. Fluorescence studies of the conformations of T4 lysozyme bound to alphaB-crystallin, J. Biol. Chem. 278, 44214-44221.
14. Alexiev, U., Rimke, I., and Pohlmann, T. (2003) Elucidation of the nature of the conformational changes of the EF-interhelical loop in bacteriorhodopsin and of the helix VIII on the cytoplasmic surface of bovine rhodopsin: a time-resolved fluorescence depolarization study, J. Mol. Biol. 328, 705-719.
15. Kachel, K., Ren, J., Collier, R. J., and London, E. (1998) Identifying transmembrane states and defining the membrane insertion boundaries of hydrophobic helices in membrane-inserted diphtheria toxin T domain, J. Biol. Chem. 273, 22950-22956.
16. Carlsson, K., Osterlund, M., Persson, E., Freskgard, P. O., Carlsson, U., and Svensson, M. (2003) Site-directed fluorescence probing to dissect the calcium-dependent association between soluble tissue factor and factor VIIa domains, Biochim. Biophys. Acta 1648, 12-16.
17. O'Neil, K. T., Wolfe, H. R., Jr., Erickson-Viitanen, S., and DeGrado, W. F. (1987) Fluorescence properties of calmodulin-binding peptides reflect alpha-helical periodicity, Science 236, 1454-1456.
18. Malenbaum, S. E., Collier, R. J., and London, E. (1998) Membrane topography of the T domain of diphtheria toxin probed with single tryptophan mutants, Biochemistry 37, 17915-17922.
19. Chen, Y., and Barkley, M. D. (1998) Toward understanding tryptophan fluorescence in proteins, Biochemistry 37, 9976-9982.
20. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2001) Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding, Biochemistry 40, 14754-14762.
21. Voss, J., He, M. M., Hubbell, W. L., and Kaback, H. R. (1996) Site-directed spin labeling demonstrates that transmembrane domain XII in the lactose permease of Escherichia coli is an alphahelix, Biochemistry 35, 12915-12918.
22. Millhauser, G. L., Fiori, W. R., and Miick, S. M. (1995) Electron spin labels, Methods Enzymol. 246, 589-610.
23. Klug, C. S., Su, W., and Feix, J. B. (1997) Mapping of the residues involved in a proposed beta-strand located in the ferric enterobactin receptor FepA using site-directed spin-labeling, Biochemistry 36, 13027-13033.
24. Hubbell, W. L., Gross, A., Langen, R., and Lietzow, M. A. (1998) Recent advances in site-directed spin labeling of proteins, Curr. Opin. Struct. Biol. 8, 649-656.
25. Perozo, E., Cortes, D. M., and Cuello, L. G. (1998) Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy, Nat. Struct. Biol. 5, 459-469.
26. Thomas, D. D., Reddy, L. G., Karim, C. B., Li, M., Cornea, R., Autry, J. M., Jones, L. R., and Stamm, J. (1998) Direct spectroscopic detection of molecular dynamics and interactions of the calcium pump and phospholamban, Ann. N. Y. Acad. Sci. 853, 186-194.
27. Hustedt, E. J., and Beth, A. H. (1999) Nitroxide spin-spin interactions: applications to protein structure and dynamics, Annu. Rev. Biophys. Biomol. Struct. 28, 129-153.
28. Gross, A., Columbus, L., Hideg, K., Altenbach, C., and Hubbell, W. L. (1999) Structure of the KcsA potassium channel from Streptomyces lividans: a site-directed spin labeling study of the second transmembrane segment, Biochemistry 38, 10324-10335.
29. Hubbell, W. L., Cafiso, D. S., and Altenbach, C. (2000) Identifying conformational changes with site-directed spin labeling, Nat. Struct. Biol. 7, 735-739.
30. Lakshmi, K. V., and Brudvig, G. W. (2001) Pulsed electron paramagnetic resonance methods for macromolecular structure determination, Curr. Opin. Struct. Biol. 11, 523-531.
31. Fanucci, G. E., Lee, J. Y., and Cafiso, D. S. (2003) Spectroscopic Evidence that Osmolytes Used in Crystallization Buffers Inhibit a Conformation Change in a Membrane Protein, Biochemistry 42, 13106-13112.
32. McHaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics, Biochemistry 35, 7692-7704.
33. Hubbell, W. L., McHaourab, H. S., Altenbach, C., and Lietzow, M. A. (1996) Watching proteins move using site-directed spin labeling, Structure 4, 779-783.
34. McHaourab, H. S., Oh, K. J., Fang, C. J., and Hubbell, W. L. (1997) Conformation of T4 lysozyme in solution. Hinge-bending motion and the substrate-induced conformational transition studied by site-directed spin labeling, Biochemistry 36, 307-316.
35. McHaourab, H. S., Kalai, T., Hideg, K., and Hubbell, W. L. (1999) Motion of spin-labeled side chains in T4 lysozyme: effect of side chain structure, Biochemistry 38, 2947-2955.
36. Langen, R., Oh, K. J., Cascio, D., and Hubbell, W. L. (2000) Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure, Biochemistry 39, 8396-8405.
37. Borbat, P. P., McHaourab, H. S., and Freed, J. H. (2002) Protein structure determination using long-distance constraints from double-quantum coherence ESR: study of T4 lysozyme, J. Am. Chem. Soc. 124, 5304-5314.
38. Hosfield, D., Palan, J., Hilgers, M., Scheibe, D., McRee, D. E., and Stevens, R. C. (2003) A fully integrated protein crystallization platform for small-molecule drug discovery, J. Struct. Biol. 142, 207-217.
39. Carlsson, J., Drevin, H., and Axen, R. (1978) Protein thiolation and reversible protein-protein conjugation. N-Succinimidyl 3-(2-pyridyldithio) propionate, a new heterobifunctional reagent, Biochem. J. 173, 723-737.
40. Becktel, W. J., and Schellman, J. A. (1987) Protein stability curves, Biopolymers 26, 1859-1877.
41. James, D. R., Siemiarczuk, A., and Ware, W. R. (1992) Stroboscopic optical boxcar technique for the determination of fluorescence lifetimes, Rev. Sci. Instrum. 63, 1710-1716.
42. D'Auria, S., Gryczynski, Z., Gryczynski, I., Rossi, M., and Lakowicz, J. R. (2000) A protein biosensor for lactate, Anal. Biochem. 283, 83-88.
43. Hawkins, M. E., Pfleiderer, W., Balis, F. M., Porter, D., and Knutson, J. R. (1997) Fluorescence properties of pteridine nucleoside analogues as monomers and incorporated into oligonucleotides, Anal. Biochem. 244, 86-95.
44. Lakowicz, J. R. (1983) Principles of Fluorescence Spectroscopy, Plenum Press, New York.
45. Maliwal, B. P., Malicka, J., Gryczynski, I., Gryczynski, Z., and Lakowicz, J. R. (2003) Fluorescence properties of labeled proteins near silver colloid surfaces, Biopolymers 70, 585-594.
46. Webber, S. E. (1997) The Role of Time-Dependent Measurements in Elucidating Static Versus Dynamic Quenching Processes, Photochem. Photobiol. 65, 33-38.
47. Lakowicz, J. R., and Weber, G. (1973) Quenching of fluorescence by oxygen. A probe for structural fluctuations in macromolecules, Biochemistry 12, 4161-4170.
48. Abagyan, R., Totrov, M., and Kuznetsov, D. N. (1994) ICM - a new method for protein modelling and design. Applications to docking and structure prediction from the distorted native conformation, J. Comput. Chem. 15, 488-506.
49. Nicholson, H., Anderson, D. E., Dao-pin, S., and Matthews, B. W. (1991) Analysis of the interaction between charged side chains and the alpha-helix dipole using designed thermostable mutants of phage T4 lysozyme, Biochemistry 30, 9816-9828.
50. Han, J. C., and Han, G. Y. (1994) A procedure for quantitative determination of tris(2-carboxyethyl)phosphine, an odorless reducing agent more stable and effective than dithiothreitol, Anal. Biochem. 220, 5-10.
51. Hu, L., and Colman, R. F. (1995) Monobromobimane as an affinity label of the xenobiotic binding site of rat glutathione S-transferase 3-3, J. Biol. Chem. 270, 21875-21883.
52. Kosower, E. M., Giniger, R., Radkowsky, A., Hebel, D., and Shusterman, A. (1986) Bimanes 22. Flexible fluorescent molecules. Solvent effects on the photophysical properties of synbimanes (1,5-diazabicyclo[3.3.0]octa-3,6-diene-2, 8-diones), J. Phys. Chem. 90, 5552-5557.
53. Kosower, E. M., Kanety, H., Dodluk, H., and Hermolin, J. (1982) Bimanes. 9. Solvent and substituent effects on intramolecular charge-transfer quenching of the fluorescence of syn-1,5-diazabicyclo[3.3.0]octadienediones (syn-9,10-dioxabimanes), J. Phys. Chem. 86, 1270-1277.
54. Lockhart, D. J., and Kim, P. S. (1992) Internal stark effect measurement of the electric field at the amino terminus of an alpha helix, Science 257, 947-951.
55. Closs, G. L., and Miller, J. R. (1988) Intramolecular Long-Distance Electron Transfer in Organic Molecules, Science 240, 440-447.
56. Siders, P., Cave, R. J., and Marcus, R. A. (1984) A model for orientation effects in electron-transfer reactions, J. Chem. Phys. 81, 5613-5624.
57. Zelent, B., Kusba, J., Gryczynski, I., Johnson, M. L., and Lakowicz, J. R. (1998) Time-resolved and steady-state fluorescence quenching of N-acetyl-L-tryptophanamide by acrylamide and iodide, Biophys. Chem. 73, 53-75.
58. Sato, E., Sakashita, M., Kanaoka, Y., and Kosower, E. M. (1988) Bioorg. Chem. 16, 298-306.
59. Heyduk, T., and Heyduk, E. (2002) Molecular beacons for detecting DNA binding proteins, Nat. Biotechnol. 20, 171-176.
60. Farrens, D. L., Altenbach, C., Yang, K., Hubbell, W. L., and Khorana, H. G. (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin, Science 274, 768-770.
61. Liu, Y. S., Sompornpisut, P., and Perozo, E. (2001) Structure of the KcsA channel intracellular gate in the open state, Nat. Struct. Biol. 8, 883-887.