Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: Structural characterization and applications in fluorescence imaging

Biochemical Journal

Volumn 400, Issue 3, 2006, Pages 531-540

  Ai, Hui Wang ^a   Henderson, J Nathan ^b   Remington, S James ^b   Campbell, Robert E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

Clavularia; Fluorescence imaging; Fluorescence resonance energy transfer (FRET); Genetic fusion; Teal fluorescent protein

Indexed keywords

BIOCHEMISTRY; CHROMOPHORES; CRYSTAL STRUCTURE; FLUORESCENCE; MONOMERS; PH EFFECTS;

CLAVULARIA; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER (FRET); GENETIC FUSION; TEAL FLUORESCENT PROTEINS;

PROTEINS;

CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; MONOMERIC TEAL FLUORESCENT PROTEIN 1;

ARTICLE; CLAVULARIA; CORAL; CRYSTAL STRUCTURE; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE FUSION; GENE LIBRARY; GENE SEQUENCE; GENE STRUCTURE; GENETIC IDENTIFICATION; GENETIC VARIABILITY; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

ANIMALS; ANTHOZOA; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; FLUORESCENCE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION;

AEQUOREA; ANTHOZOA; CLAVULARIA; MAMMALIA; SCYPHOZOA;

EID: 33845751079     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060874     Document Type: Article

References (55)

1. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544
2. Matz, M. V., Fradkov, A. F., Labas, Y. A., Savitsky, A. P., Zaraisky, A. G., Markelov, M. L. and Lukyanov, S. A. (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17, 969-973
3. Verkhusha, V. V. and Lukyanov, K. A. (2004) The molecular properties and applications of Anthozoa fluorescent proteins and chromoproteins. Nat. Biotechnol. 22, 289-296
4. Zhang, J., Campbell, R. E., Ting, A. Y. and Tsien, R. Y. (2002) Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3, 906-918
5. Chudakov, D. M., Lukyanov, S. and Lukyanov, K. A. (2005) Fluorescent proteins as a toolkit for in vivo imaging. Trends Biotechnol. 23, 605-613
6. Yang, F., Moss, L. G. and Phillips, Jr, G. N. (1996) The molecular structure of green fluorescent protein. Nat. Biotechnol. 14, 1246-1251
7. Ormo, M., Cubitt, A. B., Kallio, K., Gross, L. A., Tsien, R. Y. and Remington, S. J. (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392-1395
8. Cody, C. W., Prasher, D. C., Westler, W. M., Prendergast, F. G. and Ward, W. W. (1993) Chemical structure of the hexapeptide chromophore of the Aequorea green-fluorescent protein. Biochemistry 32, 1212-1218
9. Chattoraj, M., King, B. A., Bublitz, G. U. and Boxer, S. G. (1996) Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. Proc. Natl. Acad. Sci. U.S.A. 93, 8362-8367
10. Cormack, B. P., Valdivia, R. H. and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38
11. Heim, R., Prasher, D. C. and Tsien, R. Y. (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 91, 12501-12504
12. 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
13. 2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887
14. 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
15. Nguyen, A. W. and Daugherty, P. S. (2005) Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 23, 355-360
16. Shaner, N. C., Steinbach, P. A. and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909
17. Carter, R. W., Schmale, M. C. and Gibbs, P. D. (2004) Cloning of anthozoan fluorescent protein genes. Comp. Biochem. Physiol. C 138, 259-270
18. Sun, Y., Castner, Jr, E. W., Lawson, C. L. and Falkowski, P. G. (2004) Biophysical characterization of natural and mutant fluorescent proteins cloned from zooxanthellate corals. FEBS Lett. 570, 175-183
19. Kelmanson, I. V. and Matz, M. V. (2003) Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol. Biol. Evol. 20, 1125-1133
20. Shagin, D. A., Barsova, E. V., Yanushevich, Y. G., Fradkov, A. F., Lukyanov, K. A., Labas, Y. A., Semenova, T. N., Ugalde, J. A., Meyers, A., Nunez, J. M. et al. (2004) GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. Mol. Biol. Evol. 21, 841-850
21. Karasawa, S., Araki, T., Nagai, T., Mizuno, H. and Miyawaki, A. (2004) Cyan-emitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem. J. 381, 307-312
22. Lauf, U., Lopez, P. and Falk, M. M. (2001) Expression of fluorescently tagged connexins: a novel approach to rescue function of oligomeric DsRed-tagged proteins. FEBS Lett. 498, 11-15
23. Gavin, P., Devenish, R. J. and Prescott, M. (2002) An approach for reducing unwanted oligomerisation of DsRed fusion proteins. Biochem. Biophys. Res. Commun. 298, 707-713
24. Soling, A., Simm, A. and Rainov, N. (2002) Intracellular localization of Herpes simplex virus type 1 thymidine kinase fused to different fluorescent proteins depends on choice of fluorescent tag. FEBS Lett. 527, 153-158
25. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2002) A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 99, 7877-7882
26. Karasawa, S., Araki, T., Yamamoto-Hino, M. and Miyawaki, A. (2003) A green-emitting fluorescent protein from Galaxeidae coral and its monomeric version for use in fluorescent labeling. J. Biol. Chem. 278, 34167-34171
27. Wiedenmann, J., Ivanchenko, S., Oswald, F., Schmitt, F., Rocker, C., Salih, A., Spindler, K. D. and Nienhaus, G. U. (2004) EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc. Natl. Acad. Sci. U.S.A. 101, 15905-15910
28. Gurskaya, N. G., Verkhusha, V. V., Shcheglov, A. S., Staroverov, D. B., Chepurnykh, T. V., Fradkov, A. F., Lukyanov, S. and Lukyanov, K. A. (2006) Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465
29. Ando, R., Mizuno, H. and Miyawaki, A. (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306, 1370-1373
30. Kogure, T., Karasawa, S., Araki, T., Saito, K., Kinjo, M. and Miyawaki, A. (2006) A fluorescent variant of a protein from the stony coral Montipora facilitates dual-color single-laser fluorescence cross-correlation spectroscopy. Nat. Biotechnol. 24, 577-581
31. Zacharias, D. A., Violin, J. D., Newton, A. C. and Tsien, R. Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916
32. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. and Tsien, R. Y. (2001) Reducing the environmental sensitivity of yellow fluorescent protein: mechanism and applications. J. Biol. Chem. 276, 29188-29194
33. 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
34. Rizzo, M. A. and Piston, D. W. (2005) High-contrast imaging of fluorescent protein FRET by fluorescence polarization microscopy. Biophys. J. 88, L14-L16
35. Fromant, M., Blanquet, S. and Plateau, P. (1995) Direct random mutagenesis of gene-sized DNA fragments using polymerase chain reaction. Anal. Biochem. 224, 347-353
36. Cheng, Z. and Campbell, R. E. (2006) Assessing the structural stability of designed β-hairpin peptides in the cytoplasm of live cells. ChemBioChem 7, 1147-1150
37. Brannon, J. H. and Magde, D. (1978) Absolute quantum yield determination by thermal blooming-fluorescein. J. Phys. Chem. 82, 705-709
38. Ward, W. W. (1998) Biochemical and physical properties of GFP. In Green Fluorescent Protein: Properties, Applications and Protocols (Chalfie, M. K. S., ed.), pp. 45-75, Wiley, New York
39. 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
40. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
41. Kissinger, C. R., Gehlhaar, D. K. and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. Sect. D Biol. Crystallogr. 55, 484-491
42. Nienhaus, K., Nienhaus, G. U., Wiedenmann, J. and Nar, H. (2005) Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP. Proc. Natl. Acad. Sci. U.S.A. 102, 9156-9159
43. Sheldrick, G. M. and Schneider, T. R. (1997) SHELXL: high-resolution refinement. Methods Enzymol. 277, 319-343
44. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132
45. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
46. Kraulis, P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950
47. Merritt, E. A. and Bacon, D. J. (1997) Raster3D: photorealistic molecular graphics. Methods Enzymol. 277, 505-524
48. Henderson, J. N. and Remington, S. J. (2005) Crystal structures and mutational analysis of amFP486, a cyan fluorescent protein from Anemonia majano. Proc. Natl. Acad. Sci. U.S.A. 102, 12712-12717
49. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K. and Miyawaki, A. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90
50. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138
51. Holm, L. and Park, J. (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16, 566-567
52. Yarbrough, D., Wachter, R. M., Kallio, K., Matz, M. V. and Remington, S. J. (2001) Refined crystal structure of DsRed, a red fluorescent protein from coral, at 2.0-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 98, 462-167
53. Wall, M. A., Socolich, M. and Ranganathan, R. (2000) The structural basis for red fluorescence in the tetrameric GFP homolog DsRed. Nat. Struct. Biol. 7, 1133-1138
54. Henderson, J. N. and Remington, S. J. (2006) The kindling fluorescent protein: a transient photoswitchable marker. Physiology 21, 162-170
55. Miyawaki, A. and Tsien, R. Y. (2000) Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327, 472-500