Intrinsic dynamics in ECFP and cerulean control fluorescence quantum yield

Biochemistry

Volumn 48, Issue 42, 2009, Pages 10038-10046

  Lelimousin, Mickaël ^a   Noirclerc Savoye, Marjolaine ^a   Lazareno Saez, Christelle ^a   Paetzold, Bernhard ^b   Le Vot, Sophie ^a   Chazal, Richard ^a   Macheboeuf, Pauline ^a   Field, Martin J ^a   Bourgeois, Dominique ^a,b   Royant, Antoine ^a,b  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL IMAGING; COLLISIONAL QUENCHING; CYAN FLUORESCENT PROTEIN; DOUBLE PEAK; DYNAMICAL FLEXIBILITY; FLUORESCENCE PROPERTIES; FLUORESCENCE QUANTUM YIELD; FLUORESCENT PROTEIN; HIGH RESOLUTION CRYSTAL STRUCTURE; INDOLE RINGS; MOLECULAR DYNAMICS SIMULATIONS; N-TERMINALS; NONRADIATIVE DECAYS; PHYSIOLOGICAL PH; SPECTROSCOPIC SIGNATURES; TIME-SCALES; VAN DER WAALS INTERACTIONS;

AMINO ACIDS; CELL MEMBRANES; CRYSTAL STRUCTURE; FLUORESCENCE; MOLECULAR DYNAMICS; OPTICAL PROPERTIES; PH EFFECTS; PROTEINS; QUENCHING; VAN DER WAALS FORCES;

CHROMOPHORES;

CERULETIDE; ENHANCED CYAN FLUORESCENT PROTEIN; INDOLE; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATOPHORE; COLLISIONALLY ACTIVATED DISSOCIATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE SPECTROSCOPY; GENE MUTATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN STABILITY; QUANTUM YIELD; SIMULATION; SPECTROSCOPY;

COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; TRYPTOPHAN;

EID: 70350236735     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901093w     Document Type: Article

References (38)

1. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W., and Prasher, D. C. (1994) Green fluorescent protein as a marker for gene expression. Science 263, 802-805. (Pubitemid 24093206)
2. Cubitt, A. B., Woollenweber, L. A., and Heim, R. (1999) Understanding structure-function relationships in the Aequorea victoria green fluorescent protein. Methods Cell Biol. 58, 19-30.
3. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544.
4. Shaner, N. C., Steinbach, P. A., and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909.
5. Borst, J. W., Hink, M. A., van Hoek, A., and Visser, A. J. (2005) Effects of refractive index and viscosity on fluorescence and anisotropy decays of enhanced cyan and yellow fluorescent proteins. J. Fluoresc. 15, 153-160.
6. Nguyen, A. W., and Daugherty, P. S. (2005) Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 23, 355-360.
7. Hyun Bae, J., Rubini, M., Jung, G., Wiegand, G., Seifert, M. H., Azim, M. K., Kim, J. S., Zumbusch, A., Holak, T. A., Moroder, L., Huber, R., and Budisa, N. (2003) Expansion of the genetic code enables design of a novel "gold" class of green fluorescent proteins. J. Mol. Biol. 328, 1071-1081.
8. Seifert, M. H., Ksiazek, D., Azim, M. K., Smialowski, P., Budisa, N., and Holak, T.A. (2002) Slow exchange in the chromophore of a green fluorescent protein variant. J. Am. Chem. Soc. 124, 7932-7942.
9. Rizzo, M. A., Springer, G. H., Granada, B., and Piston, D. W. (2004) An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449.
10. Kremers, G. J., Goedhart, J., van Munster, E. B., and Gadella, T. W., Jr. (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 45, 6570-6580.
11. Villoing, A., Ridhoir, M., Cinquin, B., Erard, M., Alvarez, L., Vallverdu, G., Pernot, P., Grailhe, R., Merola, F., and Pasquier, H. (2008) Complex fluorescence of the cyan fluorescent protein: Comparisons with the H148D variant and consequences for quantitative cell imaging. Biochemistry 47, 12483-12492.
12. Malo, G. D., Pouwels, L. J., Wang, M., Weichsel, A., Montfort, W. R., Rizzo, M. A., Piston, D. W., and Wachter, R. M. (2007) X-ray structure of Cerulean GFP: A tryptophan-based chromophore useful for fluorescence lifetime imaging. Biochemistry 46, 9865-9873. (Pubitemid 47378577)
13. Studier, F. W., Rosenberg, A. H., Dunn, J. J., and Dubendorff, J. W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60-89.
14. Pantoliano, M. W., Petrella, E. C., Kwasnoski, J. D., Lobanov, V. S., Myslik, J., Graf, E., Carver, T., Asel, E., Springer, B. A., Lane, P., and Salemme, F. R. (2001) High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screening 6, 429-440. (Pubitemid 34052847)
15. Jain, R.K., and Ranganathan, R. (2004) Local complexity of amino acid interactions in a protein core. Proc. Natl. Acad. Sci. U.S.A. 101, 111-116.
16. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of internally unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800.
17. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
18. Ward, W. W. (1981) in Bioluminescence and Chemiluminescence: Basic Chemistry and Analytical Applications (Deluca, M., and McElroy, W., Eds.) pp 235-242, Academic Press, New York.
19. Royant, A., Carpentier, P., Ohana, J., McGeehan, J., Paetzold, B., Noirclerc-Savoye, M., Vernède, X., Adam, V., and Bourgeois, D. (2007) Advances in spectroscopic methods for biological crystals. 1. Fluorescence lifetime measurements. J. Appl. Crystallogr. 40, 1105-1112.
20. Field, M. J., Albe, M., Bret, C., Proust-De Martin, F., and Thomas, A. (2000) The Dynamo Library for Molecular Simulations using Hybrid Quantum Mechanical and Molecular Mechanical Potentials. J. Comput. Chem. 21, 1088-1100.
21. Jorgensen, W. L., Maxwell, D. S., and TiradoRives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236.
22. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
23. Demachy, I., Ridard, J., Laguitton-Pasquier, H., Durnerin, E., Vallverdu, G., Archirel, P., and Levy, B. (2005) Cyan fluorescent protein: Molecular dynamics, simulations, and electronic absorption spectrum. J. Phys. Chem. B 109, 24121-24133.
24. Antosiewicz, J., McCammon, J. A., and Gilson, M. K. (1994) Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238, 415-436.
25. Senn, H. M., and Thiel, W. (2009) QM/MM Methods for Biomolecular Systems. Angew. Chem., Int. Ed. 48, 1198-1229.
26. Repasky, M. P., Chandrasekhar, J., and Jorgensen, W. L. (2002) Improved semiempirical heats of formation through the use of bond and group equivalents. J. Comput. Chem. 23, 1601-1622.
27. Suhling, K., Siegel, J., Phillips, D., French, P. M., Leveque-Fort, S., Webb, S. E., and Davis, D. M. (2002) Imaging the environment of green fluorescent protein. Biophys. J. 83, 3589-3595. 28. Voros, J. (2004) The density and refractive index of adsorbing protein layers. Biophys. J. 87, 553-561. (Pubitemid 36041976)
28. Shu, X., Shaner, N. C., Yarbrough, C. A., Tsien, R. Y., and Remington, S. J. (2006) Novel chromophores and buried charges control color in mFruits. Biochemistry 45, 9639-9647. (Pubitemid 44257411)
29. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
30. Heim, R., and Tsien, R. Y. (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6, 178-182.
31. Andresen, M., Wahl, M. C., Stiel, A. C., Grater, F., Schafer, L. V., Trowitzsch, S., Weber, G., Eggeling, C., Grubmuller, H., Hell, S. W., and Jakobs, S. (2005) Structure and mechanism of the reversible photoswitch of a fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 102, 13070-13074.
32. Henderson, J. N., Ai, H. W., Campbell, R. E., and Remington, S. J. (2007) Structural basis for reversible photobleaching of a green fluorescent protein homologue. Proc. Natl. Acad. Sci. U.S.A. 104, 6672-6677.
33. Andresen, M., Stiel, A. C., Trowitzsch, S., Weber, G., Eggeling, C., Wahl, M. C., Hell, S. W., and Jakobs, S. (2007) Structural basis for reversible photoswitching in Dronpa. Proc. Natl. Acad. Sci. U.S.A. 104, 13005-13009.
34. Adam, V., Lelimousin, M., Boehme, S., Desfonds, G., Nienhaus, K., Field, M. J., Wiedenmann, J., McSweeney, S., Nienhaus, G. U., and Bourgeois, D. (2008) Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations. Proc. Natl. Acad. Sci. U.S.A. 105, 18343-18348.
35. Mizuno, H., Mal, T. K., Walchli, M., Kikuchi, A., Fukano, T., Ando, R., Jeyakanthan, J., Taka, J., Shiro, Y., Ikura, M., and Miyawaki, A. (2008) Light-dependent regulation of structural flexibility in a photochromic fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 105, 9227-9232.
36. Pletnev, S., Shcherbo, D., Chudakov, D. M., Pletneva, N., Merzlyak, E. M., Wlodawer, A., Dauter, Z., and Pletnev, V. (2008) A crystallographic study of bright far-red fluorescent protein mKate reveals pH-induced cis-trans isomerization of the chromophore. J. Biol. Chem. 283, 28980-28987.
37. Violot, S., Carpentier, P., Blanchoin, L., and Bourgeois, D. (2009) Reverse pH-dependence of chromophore protonation explains the large stokes shift of the red fluorescent protein mKeima. J. Am. Chem. Soc. 131, 10356-10357.
38. Megley, C. M., Dickson, L. A., Maddalo, S. L., Chandler, G. J., and Zimmer, M. (2009) Photophysics and dihedral freedom of the chromophore in yellow, blue, and green fluorescent protein. J. Phys. Chem. B 113, 302-308.