Structural changes of yellow cameleon domains observed by quantitative FRET analysis and polarized fluorescence correlation spectroscopy

Biophysical Journal

Volumn 95, Issue 11, 2008, Pages 5399-5411

  Borst, Jan Willem ^a   Laptenok, S P ^a   Westphal, A H ^a   Kuhnemuth R ^c   Hornen, H ^c   Visser, N V ^a   Kalinin, S ^c   Aker, J ^a   Van Hoek, A ^a   Seidel, C A M ^c   Visser, A J W G ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; UNCLASSIFIED DRUG; YELLOW CAMELEON;

ARTICLE; BLEACHING; CHEMISTRY; DRUG EFFECT; FLUORESCENCE POLARIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; METABOLISM; METHODOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; TIME;

CALCIUM; CALCIUM-BINDING PROTEINS; FLUORESCENCE POLARIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; PHOTOBLEACHING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; TIME FACTORS;

EID: 58149355793     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.114587     Document Type: Article

References (52)

1. Förster, T. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. 2:55-75.
2. Stryer, L. 1978. Fluorescence energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47:819-846.
3. Jares-Erijman, E. A., and T. M. Jovin. 2003. FRET imaging. Nat. Biotechnol. 21:1387-1395.
4. Harpur, A. G., F. S. Wouters, and P. I. Bastiaens. 2001. Imaging FRET between spectrally similar GFP molecules in single cells. Nat. Biotechnol. 19:167-169.
5. 2+ based on green fluorescent proteins and calmodulin. Nature. 388:882-887.
6. Jares-Erijman, E. A., and T.M. Jovin. 2006. Imaging molecular interactions in living cells by FRET microscopy. Curr. Opin. Chem. Biol. 10:409-416.
7. van Dongen, E.M., L.M. Dekkers, K. Spijker, E. W.Meijer, L. W. Klomp, and M. Merkx. 2006. Ratiometric fluorescent sensor proteins with subnanomolar affinity for Zn(II) based on copper chaperone domains. J. Am. Chem. Soc. 128:10754-10762.
8. Vinkenborg, J. L., T.H. Evers, S. W.Reulen, E. W. Meijer, and M. Merkx. 2007. Enhanced sensitivity of FRET-based protease sensors by redesign of the GFP dimerization interface. ChemBioChem. 8:1119-1121.
9. Suhling, K., P. M. W. French, and D. Phillips. 2005. Time-resolved fluorescence microscopy. Photochem. Photobiol. Sci. 4:13-22.
10. 2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. USA. 96:2135-2140.
11. 2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA. 101:10554-10559.
12. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 67:31-40.
13. Borst, J. W., M. A. Hink, A. van Hoek, and A. J. W. G. Visser. 2005. Effects of refractive index and viscosity on fluorescence and anisotropy decays of enhanced cyan and yellow fluorescent proteins. J. Fluoresc. 15:153-160.
14. 0 fluorescence of xanthione in different fluid solvents. Chem. Phys. Lett. 158:51-59.
15. Boens, N., N. Tamai, I. Yamazaki, and T. Yamazaki. 1990. Picosecond single photon timing measurements with a proximity type micro-channel plate photomultiplier and global analysis with reference convolution. Photochem. Photobiol. Sci. 52:911-917.
16. Karolczak, J., D. Komar, J. Kubicki, T. Wrozowa, K. Dobek, B. Ciesielska, and A. Maciejewski. 2001. The measurements of picosecond fluorescence lifetimes with high accuracy and subpicosecond precision. Chem. Phys. Lett. 344:154-164.
17. Vos, K., A. van Hoek, and A. J. W. G. Visser. 1987. Application of a reference deconvolution method to tryptophan fluorescence in proteins. A refined description of rotational dynamics. Eur. J. Biochem. 165:55-63.
18. Digris, A. V., V. V. Skakoun, E. G. Novikov, A. van Hoek, A. Claiborne, and A. J. W. G. Visser. 1999. Thermal stability of a flavoprotein assessed from associative analysis of polarized time-resolved fluorescence spectroscopy. Eur. Biophys. J. 28:526-531.
19. van den Berg, P. A. W., K. A. Feenstra, A. E. Mark, H. J. C. Berendsen, and A. J. W. G. Visser. 2002. Dynamic conformations of flavin adenine dinucleotide: simulated molecular dynamics of the flavin cofactor related to time-resolved fluorescence characteristics. J. Phys. Chem. B. 106: 8858-8869.
20. van den Berg, P. A. W., A. van Hoek, and A. J. W. G. Visser. 2004. Evidence for a novel mechanism of time-resolved flavin fluorescence depolarization in glutathione reductase. Biophys. J. 87:2577-2586.
21. Visser, N. V., J. W. Borst, M. A. Hink, A. vanHoek, and A. J. W. G. Visser. 2005. Direct observation of resonance tryptophan-to-chromophore energy transfer in visible fluorescent proteins. Biophys. Chem. 116:207-212.
22. Patterson, G. H., S. M. Knobel, W. D. Sharif, S. R. Kain, and D. W. Piston. 1997. Use of green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys. J. 73:2782-2790.
23. Bastiaens, P. I., I. V. Majoul, P. J. Verveer, H. D. Söling, and T. M. Jovin. 1996. Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15:4246-4253.
24. Felekyan, S., R. Kühnemuth, V. Kudryavtsev, C. Sandhagen, W. Becker, and C. A. M. Seidel. 2005. Full correlation from picoseconds to seconds by time-resolved and time-correlated single photon detection. Rev. Sci. Instrum. 76:83104-83118.
25. Widengren, J., V. Kudryavtsev, M. Antonik, S. Berger, M. Gerken, and C. A. M. Seidel. 2006. Single-molecule detection and identification of multiple species by multiparameter fluorescence detection. Anal. Chem. 78:2039-2050.
26. Kühnemuth, R., and C. A. M. Seidel. 2001. Principles of single molecule multiparameter fluorescence spectroscopy. Single Molecules. 2:251-254.
27. Schaffer, J., A. Volkmer, C. Eggeling, V. Subramaniam, G. Striker, and C. A. M. Seidel. 1999. Identification of single molecules in aqueous solution by time-resolved fluorescence anisotropy. J. Phys. Chem. A. 103:331-336.
28. Enderlein, J., I. Gregor, D. Patra, T. Dertinger, and U. B. Kaupp. 2005. Performance of fluorescence correlation spectroscopy for measuring diffusion and concentration. ChemPhysChem. 6:2324-2336.
29. Rosell, F. I., and S. G. Boxer. 2003. Polarized absorption spectra of green fluorescent protein single crystals: Transition dipole moment directions. Biochemistry. 42:177-183.
30. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
31. Kulinski, T., A. J. W. G. Visser, D. J. O'Kane, and J. Lee. 1987. Spectroscopic investigations of the single tryptophan residue and of riboflavin and 7-oxolumazine bound to lumazine apoprotein from Photobacterium leiognathi. Biochemistry. 26:540-549.
32. Aragón, S. R., and R. Pecora. 1975. Fluorescence correlation spectroscopy and brownian rotational diffusion. Biopolymers. 14:119-138.
33. Ehrenberg, M., and R. Rigler. 1974. Rotational brownian motion and fluorescence intensity fluctuations. Chem. Phys. 4:390-401.
34. Kask, P., P. Piksarv, M. Pooga, Ü. Mets, and E. Lippmaa. 1989. Separation of the rotational contribution in fluorescence correlation experiments. Biophys. J. 55:213-220.
35. Mets, Ü. 2001. Antibunching and rotational diffusion in FCS. In Fluorescence Correlation Spectroscopy. R. Rigler and E. S. Elson, editors. Springer-Verlag, Berlin, Heidelberg, New York.
36. Habuchi, S., M. Cotlet, J. Hofkens, G. Dirix, J. Michiels, J. Vanderleyden, V. Subramaniam, and F. C. De Schryver. 2002. Resonance energy transfer in a calcium concentration-dependent cameleon protein. Biophys. J. 83:3499-3506.
37. Tramier, M., I. Gautier, T. Piolot, S. Ravalet, K. Kemnitz, J. Coppey, C. Durieux, V. Mignotte, and M. Coppey-Moisan. 2002. Picosecond-hetero-FRET microscopy to probe protein-protein interactions in live cells. Biophys. J. 83:3570-3577.
38. Grailhe, R., F. Merola, J. Ridard, S. Couvignou, C. Le Pouponon, J. P. Changeux, and H. Laguitton-Pasquier. 2006. Monitoring protein interactions in the living cell through the fluorescence decays of the cyan fluorescent protein. ChemPhysChem. 7:1442-1454.
39. Camuzeaux, B., C. Spriet, L. Heliot, J. Coll, and M. Duterque-Coquillaud. 2005. Imaging Erg and Jun transcription factor interaction in living cells using fluorescence resonance energy transfer analyses. Biochem. Biophys. Res. Commun. 332:1107-1114.
40. Millington, M., G. J. Grindlay, K. Altenbach, R. K. Neely, W. Kolch, M. Bencina, N. D. Read, A. C. Jones, D. T. Dryden, and S. W. Magennis. 2007. High-precision FLIM-FRET in fixed and living cells reveals heterogeneity in a simple CFP-YFP fusion protein. Biophys. Chem. 127:155-164.
41. Jose, M., D. K. Nair, C. Reissner, R. Hartig, and W. Zuschratter. 2007. Photophysics of Clomeleon by FLIM: discriminating excited state reactions along neuronal development. Biophys. J. 92:2237-2254.
42. Hyun Bae, J., M. Rubini, G. Jung, G. Wiegand, M. H. J. Seifert, M. K. Azim, J.-S. Kim, A. Zumbusch, T. A. Holak, L. Moroder, R. Huber, and N. Budisa. 2003. Expansion of the genetic code enables design of a novel "gold" class of green fluorescent proteins. J. Mol. Biol. 328:1071-1081.
43. Seifert, M. H., D. Ksiazek, M. K. Azim, P. Smialowski, N. Budisa, and T. A. Holak. 2002. Slow exchange in the chromophore of a green fluorescent protein variant. J. Am. Chem. Soc. 124:7932-7942.
44. Demachy, I., J. Ridard, H. Laguitton-Pasquier, E. Durnerin, G. Vallverdu, P. Archirel, and B. Levy. 2005. Cyan fluorescent protein: molecular dynamics, simulations, and electronic absorption spectrum. J. Phys. Chem. B. 109:24121-24133.
45. Nagai, T., K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20:87-90.
46. Hink, M.A., N. V. Visser, J. W.Borst, A. vanHoek, and A. J. W. G. Visser. 2003. Practical use of corrected fluorescence excitation and emission spectra of fluorescent proteins in Förster resonance energy transfer (FRET) studies. J. Fluoresc. 13:185-188.
47. Tanaka, F., and N. Mataga. 1979. Theory of time-dependent photoselection in interacting fixed systems. Photochem. Photobiol. 29:1091-1097.
48. Hink, M. A., R. A. Griep, J. W. Borst, A. van Hoek, M. H. M. Eppink, A. Schots, and A. J. W. G. Visser. 2000. Structural dynamics of green fluorescent protein alone and fused with a single chain Fv protein. J. Biol. Chem. 275:17556-17560.
49. Harvey, S. C. 1979. Transport properties of particles with segmental flexibility. I. Hydrodynamic resistance and diffusion coefficients of a freely hinged particle. Biopolymers. 18:1081-1104.
50. Harvey, S. C., and H. C. Cheung. 1980. Transport properties of particles with segmental flexibility. II. Decay of fluorescence polarization anisotropy from hinged macromolecules. Biopolymers. 19:913-930.
51. Garcia de la Torre, J., M. L. Huertas, and B. Carrasco. 2000. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78:719-730.
52. Dale, R. E., J. Eisinger, and W. E. Blumberg. 1979. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys. J. 26:161-193.