Structure-guided engineering enhances a phytochrome-based infrared fluorescent protein

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7000-7009

  Auldridge, Michele E ^a   Satyshur, Kenneth A ^a   Anstrom, David M ^a   Forest, Katrina T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR CHANGES; CHROMOPHORE-BINDING DOMAIN; DEINOCOCCUS RADIODURANS; FAR-RED LIGHTS; FLUORESCENCE PROPERTIES; FLUORESCENT PROTEIN; IN-VIVO; MONOMERIC FORMS; MULTI DOMAINS; PHOTOCHEMICAL PROPERTIES; PHOTOCONVERSION; PHOTOCYCLES; PHYTOCHROME CHROMOPHORES; RED LIGHT; STRUCTURE-BASED; TETRAPYRROLES; WISCONSIN;

CHROMOPHORES; HYDROGEN BONDS; MONOMERS;

FLUORESCENCE;

PHYTOCHROME;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; HYDROGEN BOND; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN ENGINEERING; STRUCTURE ANALYSIS;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; FLUORESCENCE; MUTATION, MISSENSE; PHYTOCHROME; PROTEIN STRUCTURE, TERTIARY;

DEINOCOCCUS RADIODURANS;

EID: 84857715916     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.295121     Document Type: Article

References (34)

1. Rockwell, N. C., and Lagarias, J. C. (2010)Abrief history of phytochromes. ChemPhysChem 11, 1172-1180
2. Essen, L. O., Mailliet, J., and Hughes, J. (2008) The structure of a complete phytochrome sensory module in the Pr ground state. Proc. Natl. Acad. Sci. U.S.A. 105, 14709-14714
3. Yang, X., Kuk, J., and Moffat, K. (2008) Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction. Proc. Natl. Acad. Sci. U.S.A. 105, 14715-14720
4. Auldridge, M. E., and Forest, K. T. (2011) Bacterial phytochromes: more than meets the light. Crit. Rev. Biochem. Mol. Biol. 46, 67-88
5. Schumann, C., Gross, R., Michael, N., Lamparter, T., and Diller, R. (2007) Sub-picosecond mid-infrared spectroscopy of phytochrome Agp1 from Agrobacterium tumefaciens. ChemPhysChem 8, 1657-1663
6. Dasgupta, J., Frontiera, R. R., Taylor, K. C., Lagarias, J. C., and Mathies, R. A. (2009) Ultrafast excited state isomerization in phytochrome revealed by femtosecond stimulated Raman spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 106, 1784-1789
7. Wagner, J. R., Brunzelle, J. S., Forest, K. T., and Vierstra, R. D. (2005) A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438, 325-331 (Pubitemid 41643944)
8. Wagner, J. R., Zhang, J., Brunzelle, J. S., Vierstra, R. D., and Forest, K. T. (2007) High-resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution. J. Biol. Chem. 282, 12298-12309 (Pubitemid 47100678)
9. Wagner, J. R., Zhang, J., von Stetten, D., Günther, M., Murgida, D. H., Mroginski, M. A., Walker, J. M., Forest, K. T., Hildebrandt, P., and Vierstra, R. D. (2008) Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes. J. Biol. Chem. 283, 12212-12226
10. Shu, X., Royant, A., Lin, M. Z., Aguilera, T. A., Lev-Ram, V., Steinbach, P. A., and Tsien, R. Y. (2009) Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324, 804-807
11. Toh, K. C., Stojkovic, E. A., van Stokkum, I. H., Moffat, K., and Kennis, J. T. (2010) Proton transfer and hydrogen bond interactions determine fluorescence quantum yield and photochemical efficiency of bacteriophytochrome. Proc. Natl. Acad. Sci. U.S.A. 107, 9170-9175
12. Yang, X., Stojkovic, E. A., Kuk, J., and Moffat, K. (2007) Crystal structure of the chromophore-binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion. Proc. Natl. Acad. Sci. U.S.A. 104, 12571-12576 (Pubitemid 47206179)
13. Toh, K. C., Stojković, E. A., van Stokkum, I. H., Moffat, K., and Kennis, J. T. (2011) Fluorescence quantum yield and photochemistry of bacteriophytochrome constructs. Phys. Chem. Chem. Phys. 13, 11985-11997
14. Pratt, L. H. (1973) Comparative immunochemistry of phytochrome. Plant Physiol. 51, 203-209
15. Kortemme, T., Joachimiak, L. A., Bullock, A. N., Schuler, A. D., Stoddard, B. L., and Baker, D. (2004) Computational redesign of protein-protein interaction specificity. Nat. Struct. Mol. Biol. 11, 371-379 (Pubitemid 38436803)
16. Darnell, S. J., Page, D., and Mitchell, J. C. (2007) An automated decision-tree approach to predicting protein interaction hot spots. Proteins 68, 813-823 (Pubitemid 47434706)
17. 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 (Pubitemid 47080256)
18. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
19. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
20. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133 (Pubitemid 32062682)
21. Mujumdar, R. B., Ernst, L. A., Mujumdar, S. R., Lewis, C. J., and Waggoner, A. S. (1993) Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters. Bioconjug. Chem. 4, 105-111
22. von Stetten, D., Günther, M., Scheerer, P., Murgida, D. H., Mroginski, M. A., Krauss, N., Lamparter, T., Zhang, J., Anstrom, D. M., Vierstra, R. D., Forest, K. T., and Hildebrandt, P. (2008) Chromophore heterogeneity and photoconversion in phytochrome crystals and solution studied by resonance Raman spectroscopy. Angew. Chem. Int. Ed. Engl. 47, 4753-4755
23. Song, C., Psakis, G., Lang, C., Mailliet, J., Gärtner, W., Hughes, J., and Matysik, J. (2011) Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome. Proc. Natl. Acad. Sci. U.S.A. 108, 3842-3847
24. Wegele, R., Tasler, R., Zeng, Y., Rivera, M., and Frankenberg-Dinkel, N. (2004) The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. J. Biol. Chem. 279, 45791-45802 (Pubitemid 39491571)
25. Frangioni, J. V. (2003) In vivo near-infrared fluorescence imaging. Curr. Opin. Chem. Biol. 7, 626-634
26. Murphy, J. T., and Lagarias, J. C. (1997) The phytofluors: a new class of fluorescent protein probes. Curr. Biol. 7, 870-876 (Pubitemid 27493126)
27. Zienicke, B., Chen, L. Y., Khawn, H., Hammam, M. A., Kinoshita, H., Reichert, J., Ulrich, A. S., Inomata, K., and Lamparter, T. (2011) Fluorescence of phytochrome adducts with synthetic locked chromophores. J. Biol. Chem. 286, 1103-1113
28. Fischer, A. J., Rockwell, N. C., Jang, A. Y., Ernst, L. A., Waggoner, A. S., Duan, Y., Lei, H., and Lagarias, J. C. (2005) Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44, 15203-15215 (Pubitemid 41681454)
29. Fischer, A. J., and Lagarias, J. C. (2004) Harnessing phytochrome's glowing potential. Proc. Natl. Acad. Sci. U.S.A. 101, 17334-17339 (Pubitemid 39657404)
30. Su, Y. S., and Lagarias, J. C. (2007) Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 19, 2124-2139
31. Filonov, G. S., Piatkevich, K. D., Ting, L. M., Zhang, J., Kim, K., and Verkhusha, V. V. (2011) Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat. Biotechnol. 29, 757-761
32. Samma, A. A., Johnson, C. K., Song, S., Alvarez, S., and Zimmer, M. (2010) On the origin of fluorescence in bacteriophytochrome infrared fluorescent proteins. J. Phys. Chem. B 114, 15362-15369
33. Yang, X., Kuk, J., and Moffat, K. (2009) Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome. Proc. Natl. Acad. Sci. U.S.A. 106, 15639-15644
34. Rohmer, T., Lang, C., Bongards, C., Gupta, K. B., Neugebauer, J., Hughes, J., Gärtner, W., and Matysik, J. (2010) Phytochrome as molecular machine: revealing chromophore action during the Pfr 3 Pr photoconversion by magic-angle spinning NMR spectroscopy. J. Am. Chem. Soc. 132, 4431-4437