Molecular basis for pH sensitivity and proton transfer in green fluorescent protein: Protonation and conformational substates from electrostatic calculations

Biophysical Journal

Volumn 77, Issue 4, 1999, Pages 1839-1857

  Scharnagl, Christina ^a   Raupp Kossmann, R ^a   Fischer, S F ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ACID BASE BALANCE; ARTICLE; BINDING SITE; BIOTECHNOLOGY; CHROMATOPHORE; FLUORESCENCE; HYDROGEN BOND; NONHUMAN; PH; PROTON TRANSPORT;

EID: 0032828143     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77028-1     Document Type: Article

References (63)

1. Alexov, E. G., and M. R. Gunner. 1997. Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties. Biophys. J. 74:2075-2093.
2. a's in proteins. Biochemistry. 35:7819-7833.
3. Baca, M., G. E. O. Borgstahl, M. Boissinot, P. M. Burke, R. W. DeWright, K. A. Slater, and E. D. Getzoff. 1994. Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochemistry. 33: 14369-14377.
4. Bala, P., P. Grochowski, B. Lesyng, and J. A. McCammon. 1996. Quantum-classical molecular dynamics. Models and applications. In Quantum Mechanical Simulation Methods for Studying Biological Systems. D. Bicout and M. Field, editors. Springer, Berlin. 119-156.
5. a's of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry. 34:8820-8834.
6. Balashov, S. F., E. S. Imasheva, R. Govindjee, and T. G. Ebrey. 1996. Titration of aspartate-85 in bacteriorhodopsin: what is says about chromophore isomerization and proton release. Biophys. J. 70:473-481.
7. Berendsen, H. J. C., and J. Mavri. 1996. Quantum dynamics simulation of a small quantum system embedded in a classical environment. In Quantum Mechanical Simulation Methods for Studying Biological Systems. D. Bicout and M. Field, editors. Springer, Berlin. 157-179.
8. Beroza, P., and D. A. Case. 1996. Including side chain flexibility in continuum electrostatic calculations of protein titration. J. Phys. Chem. 100:20156-20163.
9. Bokman, S. H., and W. W. Ward. 1981. Renaturation of Aequorea green-fluorescent protein. Biochem. Biophys. Res. Comm. 101:1372-1380.
10. Brejc, K., T. K. Sixma, P. A. Kitts, S. R. Kain, R. Y. Tsien, M. Ormö, and S. J. Remington. 1997. Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein. Proc. Natl. Acad. Sci. USA. 94:2306-2311.
11. Brooks, C. L., III, 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.
12. Bublitz, G., B. A. King, and S. G. Boxer. 1998. Electronic structure of the chromophore in green fluorescent protein (GFP). J. Am. Chem. Soc. 120:9370-9371.
13. Chattoraj, M., B. A. King, G. U. Bublitz, and S. G. Boxer. 1996. Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. Proc. Natl. Acad. Sci. USA. 93:8362-8367.
14. B in the photosynthetic reaction center of Rps. viridis: the role of electrostatic interactions. Int. J. Quant. Chem. Quant. Biol. Symp. 20:89-106.
15. Denisov, V. P., K. Venu, J. Petersen, H. D. Hörlein, and B. Halle. 1997. Orientational disorder and entropy of water in protein cavities. J. Phys. Chem. B. 101:9380-9389.
16. Dickson, R. M., A. B. Cubitt, R. Y. Tsien, and W. E. Moerner. 1997. On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature. 388:355-358.
17. Ehrig, T., D. J. O'Kane, and F. G. Prendergast. 1995. Green-fluorescent protein mutants with altered fluorescence excitation spectra. FEBS Lett. 367:163-166.
18. Elsliger, M.-A., R. M. Wachter, G. T. Hanson, K. Kallio, and S. J. Remington. 1999. Structural and spectral response of green fluorescent protein variants to changes in pH. Biochemistry. 38:5296-5301.
19. Gilson, M. K., K. A. Sharp, and B. Honig. 1987. Calculating the electrostatic potential of molecules in solution: method and error assessment. J. Comp. Chem. 9:327-335.
20. Gutman, M., and E. Nachliel. 1990. The dynamic aspects of proton transfer processes. Biochim. Biophys. Acta. 1015:391-414.
21. Haupts, U., S. Maiti, P. Schwille, and W. W. Webb. 1998. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA. 95: 13573-13578.
22. Heim, R., A. B. Cubitt, and R. Y. Tsien. 1995. Improved green fluorescence. Nature. 373:663-664.
23. Heim, R., and R. Y. Tsien. 1996. Engineering green fluorescent protein for improved brightness, longer wavelength and fluorescence resonance energy transfer. Curr. Biol. 6:178-182.
24. Honig, B., and A. Nicholls. 1995. Classical electrostatic in biology and chemistry. Science. 268:1144-1149.
25. Jung, G., J. Wiehler, W. Göhde, J. Tittel, T. Basché, B. Steipe, and C. Bräuchle. 1998. Confocal microscopy of single molecules of the green fluorescent protein. Bioimaging 6:54-61.
26. Karplus, M., and G. A. Petsko. 1990. Molecular dynamics simulations in biology. Nature. 347:631-639.
27. Kneen, M., J. Farinas, Y. Li, and A. S. Verkman. 1998. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J. 74: 1591-1599.
28. Lanyi, J. 1997. Mechanism of ion transport across membranes: bacteriorhodopsin as a prototype for proton pumps. J. Biol. Chem. 272: 31209-31212.
29. Laria, D., G. Ciccotti, M. Ferrario, and R. Kapral. 1992. Molecular-dynamics study of adiabatic proton-transfer reactions in solution. J. Chem. Phys. 97:378-388.
30. Lossau, H., A. Kummer, R. Heinecke, F. Pöllinger-Dammer, C. Kompa, G. Bieser, T. Jonsson, C. M. Silva, M. M. Yang, D. C. Youvan, M. E. Michel-Beyerle. 1996. Time-resolved spectroscopy of wild-type and mutant green fluorescent proteins revealed excited state deprotonation consistent with fluorophore-protein interactions. Chem. Phys. 213:1-16.
31. Marrink, S. J., F. Jähnig, and H. J. C. Berendsen. 1996. Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations. Biophys. J. 71:632-647.
32. Misteli, T., and D. L. Spector. 1997. Applications of the green fluorescent protein in cell biology and biotechnology. Nature Biotechnol. 15: 961-964.
33. Nagle, J. F., M. Mille, and J. J. Moritz. 1980. Theory of hydrogen bonded chains in bioenergetics. J. Phys. Chem. 72:3959-3971.
34. Niwa, H., S. Inouye, T. Hirano, T. Matsuno, S. Kojima, M. Kubota, M. Ohashi, and T. I. Tsuji. 1996. Chemical nature of the light emitter of the Aequorea green fluorescent protein. Proc. Natl. Acad. USA. 93: 13617-13622.
35. Ormö, M., A. B. Cubitt, K. Kallio, L. A. Gross, R. Y. Tsien, S. J. Remington. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science. 273:1392-1395.
36. Palm, G. J., A. Zdanov, G. A. Gaitanaris, R. Stauber, G. N. Pavlakis, and A. Wlodawer. 1997. The structural basis for spectral variations in green fluorescent protein. Nature Struct. Biol. 4:361-365.
37. Patterson, G. H., S. M. Knobel, W. D. Sharif, S. R. Kain, and D. W. Piston. 1997. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys. J. 73:2782-2790.
38. + conduction along hydrogen-bonded chains of water molecules. Biophys. J. 75: 33-40.
39. Ripoll, D. R., Y. N. Vorobjev, A. Liwo, J. A. Vila, and H. A. Scheraga. 1996. Coupling between folding and ionization equilibria: effects of pH on the conformational preferences of polypeptides. J. Mol. Biol. 264: 770-778.
40. Robey, R. B., O. Ruiz, A. V. P. Santoz, J. Ma, F. Kear, L.-L. Wang, C.-J. Li, A. A. Bernardo, and J. A. L. Arruda. 1998. pH-dependent fluorescence of a heterologously expressed Aequorea green fluorescent protein mutant: in situ spectral characteristics and application to intracellular pH estimation. Biochemistry. 37:9894-9901.
41. Scharnagl, C., and S. F. Fischer. 1996. Conformational flexibility of arginine-82 as source for the heterogeneous and pH-dependent kinetics of the primary proton transfer step in the bacteriorhodopsin photocycle: an electrostatic model. Chem. Phys. 212:231-246.
42. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Ann. Rev. Biophys. Biophys. Chem. 19:301-332.
43. Sigfridsson, E., and U. Ryde. 1998. Comparison of methods for deriving atomic partial charges from the electrostatic potential and moments. J. Comp. Chem. 19:377-395.
44. Sitkoff, D., K. A. Sharp, and B. Honig. 1994. Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
45. Stewart, R. 1985. The Proton: Application to Organic Chemistry. Academic Press, New York.
46. Stryer, L. 1988. Biochemistry. W. H. Freeman and Company, New York.
47. Terry, B. R., E. K. Matthews, and J. Haseloof. 1995. Molecular characterisation of recombinant green fluorescent protein by fluorescence correlation microscopy. Biochem. Biophys. Res. Comm. 217:21-27.
48. Thompson, M. A., and M. Zerner. 1991. A theoretical examination of the electronic structure and spectroscopy of the photosynthetic reaction center from Rhodopseudomonas viridis. J. Am. Chem. Soc. 113: 8210-8215.
49. Tsien, R. Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544.
50. Van Thor, J. J., A. J. Pierik, I. Nugteren-Roodzant, A. Xie, and K. J. Hellingwerf. 1998. Characterization of the photoconversion of green fluorescent protein with FTIR spectroscopy. Biochemistry. 37: 16915-16921.
51. a calculations: conformational averaging versus the average structure. Proteins: Struct. Funct. Genet. 33:145-158.
52. Voityuk, A. A., M.-E. Michel-Beyerle, and N. Rösch. 1998. Quantum chemical modeling of structure and absorption spectra of the chromophore in green fluorescent proteins. Chem. Phys. 231:13-27.
53. Wachter, R. M., B. A. King, R. Heim, K. Kallio, R. Y. Tsien, S. G. Boxer, and S. J. Remington. 1997. Crystal structure and photodynamic behavior of the blue emission variant Y66H/Y145F of green fluorescent protein. Biochemistry. 36:9759-9765.
54. Wachter, R. M., M.-A. Elsliger, K. Kallio, G. T. Hanson, and S. J. Remington. 1998. Structural basis of spectral shifts in the yellow-emission variant of green fluorescent protein. Structure. 6:1267-1277.
55. Ward, W. W. 1981. Properties of the coelenterate green-fluorescent protein. In Bioluminescence and Chemiluminescence. M. A. DeLuca and W. D. McElroy. Academic Press, New York. 235-242.
56. Ward, W. W., H. J. Prentice, A. F. Roth, C. W. Cody, and S. C. Reeves. 1982. Spectral perturbation of the Aequorea green-fluorescent protein. Photochem. Photobiol. 35:803-808.
57. Ward, W. W., and S. H. Bokman. 1982. Reversible denaturation of Aequorea green-fluorescent protein: physical separation and characterization of the renatured protein. Biochemistry. 21:4535-4540.
58. Warshel, A. 1982. Dynamics of reactions in polar solvent. Semiclassical trajectory studies of electron-transfer and proton-transfer reactions. J. Phys. Chem. 86:2218-2224.
59. Warshel, A. 1986. Correlation between the structure and efficiency of light-induced proton pumps. Methods Enzymol. 127:578-587.
60. Warshel, A. 1991. Computer Modeling of Chemical Reactions in Enzymes and Solutions. Wiley-Interscience, New York.
61. Yang, F., L. G. Moss, and G. N. Phillips, Jr. 1996. The molecular structure of green fluorescent protein. Nature Biotechnol. 14:1246-1251.
62. Yang, T. T., P. Sinai, G. Green, P. A. Kitts, Y. T. Cheng, L. Lybarger, R. Chervenak, G. H. Patterson, D. W. Piston, and S. R. Kain. 1998. Improved fluorescence and dual color detection with enhanced blue and green variants of the green fluorescing protein. J. Biol. Chem. 273:8212-8216.
63. You, T. J., and D. Bashford. 1995. Conformation and hydrogen ion titration of proteins: a continuum electrostatic model with conformational flexibility. Biophys. J. 69:1721-1733.