FTIR study on the hydrogen bond structure of a key tyrosine residue in the flavin-binding blue light sensor TePixD from Thermosynechococcus elongatus

Biochemistry

Volumn 46, Issue 22, 2007, Pages 6459-6467

  Takahashi, Ryouta ^a   Okajima, Koji ^b   Suzuki, Hiroyuki ^a   Nakamura, Hiro ^c,d   Ikeuchi, Masahiko ^b   Noguchi, Takumi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c RIKEN HARIMA INSTITUTE   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLUE LIGHT SENSORS; HYDROGEN BOND STRUCTURE; LIGHT RECEPTOR POSSESSING; LIGHT-INDUCED SIGNALING STATES;

BINDING SITES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; MOLECULAR STRUCTURE; OPTICAL SENSORS; PHOTOREACTIVITY;

AMINO ACIDS;

BACTERIAL PROTEIN; PROTEIN TEPIXD; QUERCETIN; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CYANOBACTERIUM; DENSITY FUNCTIONAL THEORY; HYDROGEN BOND; INFRARED SPECTROSCOPY; NONHUMAN; PHOTOREACTIVITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; THERMOSYNECHOCOCCUS ELONGATUS;

BACTERIAL PROTEINS; CARBON ISOTOPES; DARKNESS; DEUTERIUM EXCHANGE MEASUREMENT; FLAVINS; FLAVOPROTEINS; HYDROGEN BONDING; LIGHT; MODELS, CHEMICAL; MOLECULAR STRUCTURE; PHOTORECEPTORS, MICROBIAL; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SYNECHOCOCCUS; TYROSINE;

THERMOSYNECHOCOCCUS ELONGATUS;

EID: 34249887915     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7004653     Document Type: Article

References (43)

1. Van der Horst, M. A., and Hellingwerf, K. J. (2004) Photoreceptor proteins, "star actors of modern times": A review of the functional dynamics in the structure of representative members of six different photoreceptor families, Acc. Chem. Res. 37, 13-20.
2. Gomelsky, M., and Klug, G. (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms, Trends Biochem. Sci. 27, 497-500.
3. Gomelsky, M., and Kaplan, S. (1998) AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel fad binding domain, J. Biol. Chem. 273, 35319-35325.
4. Masuda, S., and Bauer, C. E. (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides, Cell 110, 613-623.
5. Jung, A., Domratcheva, T., Tarutina, M., Wu, Q., Ko, W., Shoeman, R. L., Gomelsky, M., Gardner, K. H., and Schlichting, I. (2005) Structure of a bacterial BLUF photoreceptor: Insights into blue light-mediated signal transduction, Proc. Natl. Acad. Sci. U.S.A. 102, 12350-12355.
6. Okajima, K., Yoshihara, S., Fukushima, Y., Geng, X., Katayama, M., Higashi, S., Watanabe, M., Sato, S., Tabata, S., Shibata, Y., Itoh, S., and Ikeuchi, M. (2005) Biochemical and functional characterization of BLUF-type flavin-binding proteins of two species of cyanobacteria, J. Biochem. 137, 741-750.
7. Okajima, K., Fukushima, Y., Suzuki, H., Kita, A., Ochiai, Y., Katayama, M., Shibata, Y., Miki, K., Noguchi, T., Itoh, S., and Ikeuchi, M. (2006) Fate determination of the flavin photoreceptions in the cyanobacterial blue light receptor TePixD (T110078), J. Mol. Biol. 363, 10-18.
8. Iseki, M., Matsunaga, S., Murakami, A., Ohno, K., Shiga, K., Yoshida, K., Sugai, M., Takahashi, T., Hori, T., and Watanabe, M. (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis, Nature 415, 1047-1051.
9. Rajagopal, S., Key, J. M., Purcell, E. B., Boerema, D. J., and Moffat, K. (2004) Purification and initial characterization of a putative blue light-regulated phosphodiesterase from Escherichia coli, Photochem. Photobiol. 80, 542-547.
10. Laan, W., van der Horst, M. A., van Stokkum, I. H., and Hellingwerf, K. J. (2003) Initial characterization of the primary photochemistry of AppA, a blue-light-using flavin adenine dinucleotide-domain containing transcriptional antirepressor protein from Rhodobacter sphaeroides: A key role for reversible intramolecular proton transfer from the flavin adenine dinucleotide chromophore to a conserved tyrosine?, Photochem. Photobiol. 78, 290-297.
11. Fukushima, Y., Okajima, K., Shibata, Y., Ikeuchi, M., and Itoh, S. (2005) Primary intermediate in the photocycle of a blue-light sensory BLUF FAD-protein, T110078, of Thermosynechococcus elongatus BP-1, Biochemistry 44, 5149-5158.
12. Ito, S., Murakami, A., Sato, K., Nishina, Y., Shiga, K., Takahashi, T., Higashi, S., Iseki, M., and Watanabe, M. (2005) Photocycle features of heterologously expressed and assembled eukaryotic flavin-binding BLUF domains of photoactivated adenylyl cyclase (PAC), a blue-light receptor in Euglena gracilis, Photochem. Photobiol. Sci. 4, 762-769.
13. Zirak, P., Penzkofer, A., Schiereis, T., Hegemann, P., Jung, A., and Schlichting, I. (2006) Photodynamics of the small BLUF protein BIrB from Rhodobacter sphaeroides, J. Photochem. Photobiol. B 83, 180-194.
14. Unno, M., Masuda, S., Ono, T., and Yamauchi, S. (2006) Orientation of a key glutamine residue in the BLUF Domain from AppA revealed by mutagenesis, spectroscopy, and quantum chemical calculations, J. Am. Chem. Soc. 128, 5638-5639.
15. Hasegawa, K., Masuda, S., and Ono, T. (2005) Spectroscopic analysis of the dark relaxation process of a photocycle in a sensor of blue light using FAD (BLUF) protein Slr1694 of the cyanobacterium Synechocystis sp. PCC6803, Plant Cell Physiol. 46, 136-146.
16. Hasegawa, K., Masuda, S., and Ono, T. (2004) Structural intermediate in the photocycle of a BLUF (Sensor of Blue Light Using FAD) protein Slr1694 in a cyanobacterium Synechocystis sp. PCC6803, Biochemistry 43, 14979-14986.
17. Hasegawa, K., Masuda, S., and Ono, T. (2006) Light induced structural changes of a full-length protein and its BLUF domain in YcgF(Blrp), a blue-light sensing protein that uses FAD (BLUF), Biochemistry 45, 3785-3793.
18. Masuda, S., Hasegawa, K., Ishii, A., and Ono, T. (2004) Light-induced structural changes in a putative blue-light receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of Synechocystis sp. PCC6803, Biochemistry 43, 5304-5313.
19. Masuda, S., Hasegawa, K., and Ono, T. (2005) Light-induced structural changes of apoprotein and chromophore in the sensor of blue light using FAD (BLUF) domain of AppA for a signaling state, Biochemistry 44, 1215-1224.
20. Masuda, S., Hasegawa, K., and Ono, T. (2005) Tryptophan at position 104 is involved in transforming light signal into changes of β-sheet structure for the signaling state in the BLUF domain of AppA, Plant Cell Physiol. 46, 1894-1901.
21. Unno, M., Sano, R., Masuda, S., Ono, T., and Yamauchi, S. (2005) Light-induced structural changes in the active site of the BLUF domain in AppA by Raman spectroscopy, J. Phys. Chem. B 109, 12620-12626.
22. Kita, A., Okajima, K., Morimoto, Y., Ikeuchi, M., and Miki, K. (2005) Structure of a cyanobacterial BLUF protein, T1I0078, containing a novel FAD-binding blue light sensor domain, J. Mol. Biol. 349, 1-9.
23. Yuan, H., Anderson, S., Masuda, S., Dragnea, V., Moffat, K., and Bauer, C. (2006) Crystal structures of the Synechocystis photoreceptor Slr1694 reveal distinct structural states related to signaling, Biochemistry 45, 12687-12694.
24. Anderson, S., Dragnea, V., Masuda, S., Ybe, J., Moffat, K., and Bauer, C. (2005) Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides, Biochemistry 44, 7998-8005.
25. Jung, A., Reinstein, J., Domratcheva, T., Shoeman, R. L., and Schlichting, I. (2006) Crystal structures of the AppA BLUF domain photoreceptor provide insights into blue light-mediated signal transduction, J. Mol. Biol. 362, 717-732.
26. Kraft, B. J., Masuda, S., Kikuchi, J., Dragnea, V., Tollin, G., Zaleski, J. M., and Bauer, C. E. (2003) Spectroscopic and mutational analysis of the blue-light photoreceptor AppA: A novel photocycle involving flavin stacking with an aromatic amino acid, Biochemistry 42, 6726-6734.
27. Dragnea, V., Waegele, M., Balascuta, S., Bauer, C., and Dragnea, B. (2005) Time-resolved spectroscopic studies of the AppA blue-light receptor BLUF domain from Rhodobacter sphaeroides, Biochemistry 44, 15978-15985.
28. Gauden, M., van Stokkum, I. H. M., Key, J. M., Luhrs, D. C., van Grondelle, R., Hegemann, P., and Kennis, J. T. M. (2006) Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor, Proc. Natl. Acad. Sci. U.S.A. 103, 10895-10900.
29. Grinstead, J. S., Avila-Perez, M., Hellingwerf, K. J., Boelens, R., and Kaptein, R. (2006) Light-induced flipping of a conserved glutamine sidechain and its orientation in the AppA BLUF domain, J. Am. Chem. Soc. 128, 15066-15067.
30. Uchida, T., Mogi, T., Nakamura, H., and Kitagawa, T. (2004) Role of Tyr-288 at the dioxygen reduction site of cytochrome bo studied by stable isotope labeling and resonance Raman spectroscopy, J. Biol. Chem. 279, 53613-53620.
31. Noguchi, T., and Sugiura, M. (2002) Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated photosystem II core films: Effect of hydration extent on S-state transitions, Biochemistry 41, 2322-2330.
32. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tornasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, Revision C.02, Gaussian, Inc., Wallingford, CT.
33. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
34. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
35. Jakobsen, R. J. (1965) The vibrational spectra of p-cresol, Spectrochim. Acta 21, 433-442.
36. Takeuchi, H., Watanabe, N., and Harada, I. (1988) Vibrational spectra and normal coordinate analysis of p-cresol and its deuterated analogs, Spectrochim. Acta, Part A 44, 749-761.
37. -1 region, J. Raman Spectrosc. 20, 233-237.
38. 17O NMR approach, J. Am. Chem. Soc. 114, 9043-9047.
39. Noguchi, T., Inoue, Y., and Tang, X.-S. (1997) Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in photosystem II as revealed by Fourier transform infrared spectroscopy, Biochemistry 36, 14705-14711.
40. Hienerwadel, R., Boussac, A., Breton, J., Diner, B. A., and Berthomieu, C. (1997) Fourier transform infrared difference spectroscopy of photosystem II tyrosine D using site-directed mutagenesis and specific isotope labeling, Biochemistry 36, 14712-14723.
41. Iwata, T., Nozaki, D., Tokutomi, S., Kagawa, T., Wada, M., and Kandori, H. (2003) Light-induced structural changes in the LOV2 domain of Adiantum phytochrome3 studied by low-temperature FTIR and UV-visible spectroscopy, Biochemistry 42, 8183-8191.
42. Swartz, T. E., Wenzel, P. J., Corchnoy, S. B., Briggs, W. R., and Bogomolni, R. A. (2002) Vibration spectroscopy reveals light-induced chromophore and protein structural changes in the LOV2 domain of the plant blue-light receptor phototropin 1, Biochemistry 41, 7183-7189.
43. Kottke, T., Batschauer, A., Ahmad, M., and Heberle, J. (2006) Blue-light-induced changes in Arabidopsis cryptochrome 1 probed by FTIR difference spectroscopy, Biochemistry 45, 2472-2479.