Structural tuning of the fluorescent protein iLOV for improved photostability

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22295-22304

  Christie, John M ^a,b   Hitomi, Kenichi ^a,c,d   Arvai, Andrew S ^a   Hartfield, Kimberly A ^a   Mettlen, Marcel ^a   Pratt, Ashley J ^a   Tainer, John A ^a,c   Getzoff, Elizabeth D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC CONDITIONS; AROMATIC RESIDUES; BLUE LIGHT; CRYSTALLOGRAPHIC STRUCTURE; DIRECTED EVOLUTION; FLAVIN MONONUCLEOTIDES; FLUORESCENT PROPERTY; FLUORESCENT PROTEIN; FLUORESCENT REPORTER; GREEN FLUORESCENT PROTEIN; MAMMALIAN CELLS; METHYL GROUP; MOLECULAR BASIS; PHOTO-STABILITY; PHOTOCHEMICAL PROPERTIES; PHOTOSTABLE; PHOTOTROPINS; SCAFFOLD PROTEIN; SIDE-CHAINS; STRUCTURAL TUNING; STRUCTURE DETERMINATION; VIRAL INFECTIONS;

CHROMOPHORES; FLUORESCENCE; FUNCTIONAL GROUPS; OXYGEN;

PROTEINS;

FLAVINE MONONUCLEOTIDE; FLUORESCENT DYE; PROTEIN ILOV; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CHROMATOPHORE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTALLOGRAPHY; DIRECTED MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTODYNAMICS; PHOTOSTABILITY; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ANIMALS; ARABIDOPSIS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; FLAVOPROTEINS; FLUORESCENCE; GENES, REPORTER; HAPLORHINI; LIGHT; LUMINESCENT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS; OXYGEN; PHOTOCHEMISTRY; PHOTOTROPINS; PROTEIN CONFORMATION; SPECTROPHOTOMETRY;

EID: 84862644823     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.318881     Document Type: Article

References (39)

1. Shaner, N. C., Patterson, G. H., and Davidson, M. W. (2007) Advances in fluorescent protein technology. J. Cell Sci. 120, 4247-4260
2. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544
3. Chapman, S., Faulkner, C., Kaiserli, E., Garcia-Mata, C., Savenkov, E. I., Roberts, A. G., Oparka, K. J., and Christie, J. M. (2008) The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc. Natl. Acad. Sci. U.S.A. 105, 20038-20043
4. Drepper, T., Eggert, T., Circolone, F., Heck, A., Krauss, U., Guterl, J. K., Wendorff, M., Losi, A., Gärtner, W., and Jaeger, K. E. (2007) Reporter proteins for in vivo fluorescence without oxygen. Nat. Biotechnol. 25, 443-445
5. Shu, X., Lev-Ram, V., Deerinck, T. J., Qi, Y., Ramko, E. B., Davidson, M. W., Jin, Y., Ellisman, M. H., and Tsien, R. Y. (2011) A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS. Biol. 9, e1001041
6. Pellequer, J. L., Wager-Smith, K. A., Kay, S. A., and Getzoff, E. D. (1998) Photoactive yellow protein: a structural prototype for the three-dimensional fold of the PAS domain superfamily. Proc. Natl. Acad. Sci. U.S.A. 95, 5884-5890
7. Taylor, B. L., and Zhulin, I. B. (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev 63, 479-506
8. Genick, U. K., Soltis, S. M., Kuhn, P., Canestrelli, I. L., and Getzoff, E. D. (1998) Structure at 0.85 Å resolution of an early protein photocycle intermediate. Nature 392, 206-209
9. 2 intermediate formation, probed with enhanced hydrogen/deuterium exchange mass spectrometry. J. Mol. Biol. 363, 148-160
10. Christie, J. M. (2007) Phototropin blue light receptors. Annu. Rev. Plant Biol. 58, 21-45
11. Salomon, M., Christie, J. M., Knieb, E., Lempert, U., and Briggs, W. R. (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39, 9401-9410
12. Baca, M., Borgstahl, G. E., Boissinot, M., Burke, P. M., Williams, D. R., Slater, K. A., and Getzoff, E. D. (1994) Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochemistry 33, 14369-14377
13. Möglich, A., Yang, X., Ayers, R. A., and Moffat, K. (2010) Structure and function of plant photoreceptors. Annu. Rev. Plant Biol. 61, 21-47
14. Christie, J. M., Reymond, P., Powell, G. K., Bernasconi, P., Raibekas, A. A., Liscum, E., and Briggs, W. R. (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698-1701
15. Christie, J. M., Salomon, M., Nozue, K., Wada, M., and Briggs, W. R. (1999) LOV (light, oxygen, or voltage) domains of the blue light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc. Natl. Acad. Sci. U.S.A. 96, 8779-8783
16. Swartz, T. E., Corchnoy, S. B., Christie, J. M., Lewis, J. W., Szundi, I., Briggs, W. R., and Bogomolni, R. A. (2001) The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J. Biol. Chem. 276, 36493-36500
17. Drepper, T., Huber, R., Heck, A., Circolone, F., Hillmer, A. K., Büchs, J., and Jaeger, K. E. (2010) Flavin mononucleotide-based fluorescent reporter proteins outperform green fluorescent protein-like proteins as quantitative in vivo real-time reporters. Appl. Environ. Microbiol. 76, 5990-5994
18. Tielker, D., Eichhof, I., Jaeger, K. E., and Ernst, J. F. (2009) Flavin mononucleotide- based fluorescent protein as an oxygen-independent reporter in Candida albicans and Saccharomyces cerevisiae. Eukaryot. Cell 8, 913-915
19. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307-326
20. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
21. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132
22. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213-221
23. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D. 67, 235-242
24. Christie, J. M., Corchnoy, S. B., Swartz, T. E., Hokenson, M., Han, I. S., Briggs, W. R., and Bogomolni, R. A. (2007) Steric interactions stabilize the signaling state of the LOV2 domain of phototropin 1. Biochemistry 46, 9310-9319
25. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., and Stuurman, N. (2010) Computer control of microscopes using μManager. Curr. Protoc. Mol. Biol. Chapter 14, Unit 14.20
26. Tainer, J. A., Getzoff, E. D., Alexander, H., Houghten, R. A., Olson, A. J., Lerner, R. A., and Hendrickson, W. A. (1984) The reactivity of anti-peptide antibodies is a function of the atomic mobility of sites in a protein. Nature 312, 127-134
27. Crosson, S., and Moffat, K. (2001) Structure of a flavin-binding plant photoreceptor domain: insights into light-mediated signal transduction. Proc. Natl. Acad. Sci. U.S.A. 98, 2995-3000
28. Christie, J. M., Swartz, T. E., Bogomolni, R. A., and Briggs, W. R. (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J. 32, 205-219
29. Iwata, T., Nozaki, D., Tokutomi, S., and Kandori, H. (2005) Comparative investigation of the LOV1 and LOV2 domains in Adiantum phytochrome3. Biochemistry 44, 7427-7434
30. Nozaki, D., Iwata, T., Ishikawa, T., Todo, T., Tokutomi, S., and Kandori, H. (2004) Role of Gln-1029 in the photoactivation processes of the LOV2 domain in Adiantum phytochrome3. Biochemistry 43, 8373-8379
31. Nakasako, M., Zikihara, K., Matsuoka, D., Katsura, H., and Tokutomi, S. (2008) Structural basis of the LOV1 dimerization of Arabidopsis phototropins 1 and 2. J. Mol. Biol. 381, 718-733
32. Salomon, M., Lempert, U., and Rüdiger, W. (2004) Dimerization of the plant photoreceptor phototropin is probably mediated by the LOV1 domain. FEBS Lett. 572, 8-10
33. Yamamoto, A., Iwata, T., Tokutomi, S., and Kandori, H. (2008) Role of Phe-1010 in light-induced structural changes of the neo1-LOV2 domain of Adiantum. Biochemistry 47, 922-928
34. Jones, M. A., Feeney, K. A., Kelly, S. M., and Christie, J. M. (2007) Mutational analysis of phototropin 1 provides insights into the mechanism underlying LOV2 signal transmission. J. Biol. Chem. 282, 6405-6414
35. Eisenreich, W., Fischer, M., Römisch-Margl, W., Joshi, M., Richter, G., Bacher, A., and Weber, S. (2009) Tryptophan 13C nuclear-spin polarization generated by intraprotein electron transfer in a LOV2 domain of the blue light receptor phototropin. Biochem. Soc. Trans. 37, 382-386
36. Kay, C. W., Schleicher, E., Kuppig, A., Hofner, H., Rüdiger, W., Schleicher, M., Fischer, M., Bacher, A., Weber, S., and Richter, G. (2003) Blue light perception in plants: detection and characterization of a light-induced neutral flavin radical in a C450A mutant of phototropin. J. Biol. Chem. 278, 10973-10982
37. Shaner, N. C., Lin, M. Z., McKeown, M. R., Steinbach, P. A., Hazelwood, K. L., Davidson, M. W., and Tsien, R. Y. (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551
38. Nash, A. I., Ko, W. H., Harper, S. M., and Gardner, K. H. (2008) A conserved glutamine plays a central role in LOV domain signal transmission and its duration. Biochemistry 47, 13842-13849
39. Pathak, G. P., Ehrenreich, A., Losi, A., Streit, W. R., and Gärtner, W. (2009) Novel blue light-sensitive proteins from a metagenomic approach. Environ. Microbiol. 11, 2388-2399