Structural role of tyrosine 98 in photoactive yellow protein: Effects on fluorescence, gateway, and photocycle recovery

Biochemistry

Volumn 46, Issue 1, 2007, Pages 95-105

  Kyndt, John A ^a,b   Savvides, Savvas N ^b   Memmi, Samy ^b   Koh, Moonjoo ^c   Fitch, John C ^a   Meyer, Terry E ^a   Heyn, Maarten P ^d   Van Beeumen, Jozef J ^b   Cusanovich, Michael A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b GHENT UNIVERSITY   (Belgium)

^c Chosun University   (South Korea)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; CRYSTAL STRUCTURE; ISOMERIZATION; MUTAGENESIS; PHOTOCHEMICAL REACTIONS; PROTEINS;

CONFORMATIONAL CHANGE; MUTATION; PHOTOCYCLE KINETICS; RECOVERY KINETICS;

AMINO ACIDS;

ALANINE; GLUTAMINE; METHIONINE; MUTANT PROTEIN; PHOTOACTIVE YELLOW PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; BETA CHAIN; CHROMATOPHORE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE; ISOMERIZATION; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PHOTOCHEMISTRY; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; RHODOCISTA CENTENARIA;

BACTERIAL PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HALORHODOSPIRA HALOPHILA; HYDROGEN-ION CONCENTRATION; KINETICS; MASS SPECTROMETRY; MODELS, MOLECULAR; MUTATION; PHOTORECEPTORS, MICROBIAL; SPECTROMETRY, FLUORESCENCE; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE; TYROSINE;

RHODOSPIRILLUM CENTENUM;

EID: 33846119755     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061867y     Document Type: Article

References (46)

1. Meyer, T. E., Yakali, E., Cusanovich, M. A., and Tollin, G. (1987) Properties of a water-soluble, yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin, Biochemistry 26, 418-423.
2. Cusanovich, M. A., and Meyer, T. E. (2003) Photoactive yellow protein: A prototypic PAS domain sensory protein and development of a common signaling mechanism, Biochemistry 42, 4759-4770.
3. Meyer, T. E. (1985) Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila, Biochim. Biophys. Acta 806, 175-183.
4. Kyndt, J. A., Meyer, T. E., and Cusanovich, M. A. (2004) Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria, Photochem. Photobiol. Sci. 3, 519-530.
5. Jiang, Z. Y., Swem, L. R., Rushing, B. G., Devanathan, S., Tollin, G., and Bauer, C. E. (1999) Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285, 406-409.
6. Kyndt, J. A., Fitch, J. C., Meyer, T. E., and Cusanovich, M. A. (2005) Thermochromatium tepidum photoactive yellow protein/ bacteriophytochrome/ diguanulate cyclase: Characterization of the PYP domain, Biochemistry 44, 4755-4764.
7. Haker, A., Hendriks, J., Gensch, T., Hellingwerf, K., and Crielaard, W. (2000) Isolation, reconstitution and functional characterization of the Rhodobacter sphaeroides photoactive yellow protein, FEBS Lett. 486, 52-56.
8. Kyndt, J. A., Hurley, J. K., Devreese, B., Meyer, T. E., Cusanovich, M. A., Tollin, G., and Van Beeumen, J. J. (2004) Rhodobacter capsulatus photoactive yellow protein: Genetic context, spectral and kinetics characterization, and mutagenesis, Biochemistry 43, 1808-1820.
9. Wise, K. J., Gillespie, N. B., Stuart, J. A., Krebs, M. P., and Birge, R. R. (2002) Optimization of bacteriorhodopsin for bioelectronic devices, Trends Biotechnol. 20, 387-394.
10. Getzoff, E. D., Gutwin, K. N., and Genick, U. K. (2003) Anticipatory active-site motions and chromophore distortion prime photoreceptor PYP for light activation, Nat. Struct. Biol. 10, 663-668.
11. Ujj, L., Devanathan, S., Meyer, T. E., Cusanovich, M. A., Tollin, G., and Atkinson, G. H. (1998) New photocycle intermediates in the photoactive yellow protein from Ectothiorhodospira halophila: Picosecond transient absorption spectroscopy, Biophys. J. 75, 406-412.
12. Devanathan, S., Pacheco, A., Ujj, L., Cusanovich, M., Tollin, G., Lin, S., and Woodbury, N. (1999) Femtosecond spectroscopic observations of initial intermediates in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila, Biophys. J. 77, 1017-1023.
13. Borucki, B., Devanathan, S., Otto, H., Cusanovich, M. A., Tollin, G., and Heyn, M. P. (2002) Kinetics of proton uptake and dye binding by photoactive yellow protein in WT and in the E46Q and E46A mutants, Biochemistry 41, 10026-10037.
14. 2 intermediates, chromophore deprotonation by hydroxyl uptake, and protonation relaxation of the dark state, Biochemistry 42, 8780-8790.
15. Xie, A., Kelemen, L., Hendriks, J., White, B. J., Hellingwerf, K. J., and Hoff, W. D. (2001) Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation, Biochemistry 40, 1510-1517.
16. 2 intermediates in the photocycle of photoactive yellow protein by double flash experiments with variable time delay, Biochemistry 44, 656-665.
17. Otto, H., Hoersch, D., Meyer, T. E., Cusanovich, M. A., and Heyn, M. P. (2005) Time-resolved single tryptophan fluorescence in photoactive yellow protein monitors changes in the chromophore structure during the photocycle via energy transfer, Biochemistry 44, 16804-16816.
18. Shimizu, N., Imamoto, Y., Harigai, M., Kamikubo, H., Yamazaki, Y., and Kataoka, M. (2006) pH-dependent equilibrium between long lived near-UV intermediates of photoactive yellow protein, J. Biol. Chem. 281, 4318-4325.
19. Borgstahl, G. E. O., Williams, D. R., and Getzoff, E. D. (1995) 1.4 Å structure of photoactive yellow protein, a cytosolic photoreceptor: Unusual fold, active site, and chromophore, Biochemistry 34, 6278-6287.
20. 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.
21. Genick, U. K., Borgstahl, G. E. O., Ng, K., Ren, Z., Pradervand, C., Burke, P. M., Srajer, V., Teng, T.-Y., Schildkamp, W., McRee, D. E., Moffat, K., and Getzoff, E. D. (1997) Structure of a protein photocycle intermediate by millisecond time-resolved crystallography, Science 275, 1471 -1475.
22. Düx, P., Rubinstenn, G., Vuister, G. W., Boelens, R., Mulder, F. A. A., Hård, K., Hoff, W. D., Kroon, A. R., Crielaard, W., Hellingwerf, K. J., and Kaptein, R. (1998) Solution structure and backbone dynamics of the photoactive yellow protein, Biochemistry 37, 12689-12699.
23. Genick, U. K., Devanathan, S., Meyer, T. E., Canestrelli, I. L., Williams, E., Cusanovich, M. A., Tollin, G., and Getzoff, E. D. (1997) Active site mutants implicate key residues for control of color and light cycle kinetics of photoactive yellow protein, Biochemistry 36, 8-14.
24. Devanathan, S., Genick, U. K., Canestrelli, I. L., Meyer, T. E., Cusanovich, M. A., Getzoff, E. D., and Tollin, G. (1998) New insights into the photocycle of Ectothiorhodospira halophila photoactive yellow protein: Photorecovery of the long-lived photobleached intermediate in the Met100Ala mutant, Biochemistry 37, 11563-11568.
25. M decay process in the photocycle of photoactive yellow protein, J. Biochem. 132, 205-210.
26. Rajagopal, S., and Moffat, K. (2003) Crystal structure of a photoactive yellow protein from a sensor histidine kinase: Conformational variability and signal transduction, Proc. Natl. Acad. Sci. U.S.A. 100, 1649-1654.
27. Borucki, B., Kyndt, J. A., Joshi, C. P., Otto, H., Meyer, T. E., Cusanovich, M. A., and Heyn, M. P. (2005) Effect of salt and pH on the activation of photoactive yellow protein and gateway mutants Y98Q and Y98F, Biochemistry 44, 13650-13663.
28. Kyndt, J. A., Vanrobaeys, F., Fitch, J. C., Devreese, B. V., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (2003) Heterologous production of Halorhodospira halophila holophotoactive yellow protein through tandem expression of the postulated biosynthetic genes, Biochemistry 42, 965-970.
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
30. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likelihood-enhanced fast rotation functions, Acta Crystallogr. D60, 432-438.
31. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
32. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I. W., Word, J. M., Prisant, M. J., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: φ, ψ, and Cβ deviation, Proteins: Struct., Funct., Genet. 50, 437-450.
33. Simondsen, R. P., and Tollin, G. (1983) Transient kinetics of redox reactions of flavodoxin: Effects of chemical modification of the flavin mononucleotide prosthetic group on the dynamics of intermediate complex formation and electron transfer, Biochemistry 22, 3008-3016.
34. Anderson, S., Crosson, S., and Moffat, K. (2004) Short hydrogen bonds in photoactive yellow protein, Acta Crystallogr. D60, 1008-1016.
35. Meyer, T. E., Tollin, G., Causgrove, T. P., Cheng, P., and Blankenship, R. E. (1991) Picosecond decay kinetics and quantum yield of fluorescence of the photoactive yellow protein from the halophilic purple phototrophic bacterium, Ectothiorhodospira halophila, Biophys. J. 59, 988-991.
36. Lackowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd ed., Springer Publishing, New York.
37. Morishita, T., Harigai, M., Yamazaki, Y., Kamikubo, H., Kataoka, M., and Imamoto, Y. (2006) Array of aromatic amino acid side chains located near the chromophore of photoactive yellow protein, Photochem. Photobiol. (Epub 6/1/06).
38. Brudler, R., Meyer, T. E., Genick, U. K., Devanathan, S., Woo, T. T., Millar, D. P., Gerwert, K., Cusanovich, M. A., Tollin, G., and Getzoff, E. D. (2000) Coupling of hydrogen bonding to chromophore conformation and function in photoactive yellow protein, Biochemistry 39, 13478-13486.
39. Quillin, M. L., Anstrom, D. M., Shu, X., O'Leary, S., Kallio, K., Chudakov, D. M., and Remington, S. J. (2005) Kindling fluorescent protein from Anemonia sulcata: Dark-state structure at 1.38 Å resolution, Biochemistry 44, 5774-5787.
40. Harigai, M., Kataoka, M., and Imamoto, Y. (2006) A single CH/π weak hydrogen bond governs stability and the photocycle of the photoactive yellow protein, J. Am. Chem. Soc. 128, 10646-10647.
41. Premvardhan, L. L., van der Horst, M. A., Hellingwerf, K. J., and van Grondelle, R. (2003) Stark spectroscopy on photoactive yellow protein, E46Q, and a nonisomerizing derivative, probes photoinduced charge motion, Biophys. J. 84, 3226-3239.
42. Meyer, T. E., Devanathan, S., Woo, T., Getzoff, E. D., Tollin, G., and Cusanovich, M. A. (2003) Site specific mutations provide new insights into the origin of pH effects and alternative spectral forms in the photoactive yellow protein from Ectothiorhodospira halophila, Biochemistry 42, 3319-3325.
43. Meyer, T. E., Tollin, G., Hazzard, J. H., and Cusanovich, M. A. (1989) Photoactive yellow protein from the purple phototrophic bacterium, Ectothiorhodospira halophila, Biophys. J. 56, 559-564.
44. Van Brederode, M. E., Gensch, T., Hoff, W. D., Hellingwerf, K. J., and Braslavsky, S. E. (1995) Photoinduced volume change and energy storage associated with the early transformations of the photoactive yellow protein from Ectothiorhodospira halophila, Biophys. J. 68, 1101-1109.
45. Takeshita, K., Imamoto, Y., Kataoka, M., Mihara, K., Tokunaga, P., and Terazima, M. (2002) Structural change of site-directed mutants of PYP: New dynamics during pR state, Biophys. J. 83, 1567-1577.
46. Bruns, C. M., Hubatsch, I., Ridderström, M., Mannervik, B., and Tainer, J. A. (1999) Human glutathione transferase A4-4. Crystal structures and mutagenesis reveal the basis of high catalytic efficiency with toxic lipid peroxidation products, J. Mol. Biol. 288, 427-439.