Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides

Biochemistry

Volumn 44, Issue 22, 2005, Pages 7998-8005

  Anderson, Spencer ^b   Dragnea, Vladimira ^a   Masuda, Shinji ^d   Ybe, Joel ^a   Moffat, Keith ^c   Bauer, Carl ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; BACTERIA; CHROMOPHORES; HYDROGEN BONDS; PROTEINS; STRUCTURE (COMPOSITION); TOPOLOGY;

BLUF DOMAINS; PHOTOACTIVATION; PHOTORECEPTORS; X RAY STRUCTURE;

BIOCHEMISTRY;

BACTERIAL PROTEIN; FERREDOXIN; FLAVINE ADENINE NUCLEOTIDE; GLUCOSAMINE; QUERCETIN;

ALPHA HELIX; ARTICLE; BETA SHEET; BLUE LIGHT; CHROMATOPHORE; HYDROGEN BOND; NONHUMAN; PHOTOACTIVATION; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RHODOBACTER SPHAEROIDES; SIGNAL TRANSDUCTION; X RAY ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DARKNESS; DIMERIZATION; FLAVIN-ADENINE DINUCLEOTIDE; FLAVOPROTEINS; GLUTAMINE; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PHOTORECEPTORS, MICROBIAL; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RHODOBACTER SPHAEROIDES;

ALGAE; BACTERIA (MICROORGANISMS); RHODOBACTER SPHAEROIDES;

EID: 20144368776     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0502691     Document Type: Article

References (45)

1. Briggs, W. R., and Kuala, E, (1999) Blue-light photoreceptors in higher plants, Annu. Rev. Cell Dev. Biol. 15, 33-62.
2. Crosson, S., Rajagopal, S., and Moffat, K. (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains, Biochemistry 42, 2-10.
3. Gomelsky, M., and Klug, G. (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms, Trends Biochein. Sci. 27, 497-500.
4. Lin, C. (2000) Plant blue-light receptors, Trends Plant Sci. 5, 337-342.
5. 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.
6. 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.
7. Han, Y., Braatsch, S., Osterloh, L., and Klug, G. (2004) A eukaryotic BLUF domain mediates light-dependent gene expression in the purple bacterium Rhodobacter sphaeroides 2.4.1, Proc. Natl. Acad. Sci. U.S.A. 101, 12306-12311.
8. Pei, J. M., and Grishin, N. V. (2001) GGDEF domain is homologous to adenylyl cyclase, Proteins 42, 210-216.
9. Galperin, M. Y., Nikolskaya, A. N., and Koonin, E. V. (2001) Novel domains of the prokaryotic two-component signal transduction systems, FEMS Microbiol. Lett. 204, 213-214.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Gauden, M., Yeremenko, S., Laan, W., van Stokkum, I. H., Ihalainen, J., van Grondelle, R., Hellingwerf, K. J., and Kennis, J. T. (2005) Photocycle of the flavin-binding photoreceptor AppA, a bacterial transcriptional antirepressor of photosynthesis genes, Biochemistry 44, 3653-3662.
16. Huala, E., Oeller, P. W., Liscum, E., Han, I. S., Larsen, E., and Briggs, W. R. (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain, Science 278, 2120-2123.
17. Christie, J. M., and Briggs, W. R. (2001) Blue light sensing in higher plants, J. Biol. Chem. 276, 11457-11460.
18. 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.
19. 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.
20. 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.
21. Lin, C., Robertson, D. E., Ahmad, M., Raibekas, A. A., Jorns, M. S., Dutton, P. L., and Cashmore, A. R. (1995) Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1, Science 269, 968-970.
22. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis, Nucleic Acids Res. 31, 3784-3788.
23. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
24. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution, Acta Crystallogr. D 55, 849-861.
25. Terwilliger, T. C. (2000) Maximum-likelihood density modification, Acta Crystallogr. D 56, 965-972.
26. McRee, D. E. (1999) XtalView Xfit-A versatile program for manipulating atomic coordinates arid electron density, J. Struct. Biol. 125, 156-165.
27. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D 53, 240-255.
28. Kort, R., Komori, H., Adachi, S., Miki, K., and Eker, A. (2004) DNA apophotolyase from Anacystis nidulans: 1.8 angstrom structure, 8-HDF reconstitution and X-ray-induced FAD reduction, Acta Crystallogr. D 60, 1205-1213.
29. Murray, J. W., Carman, E. F., and Ravelli, R. B. G. (2004) X-ray absorption by macromolecular crystals: the effects of wavelength and crystal composition on absorbed dose, J. Appl. Crystallogr. 37, 513-522.
30. 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 57, 122-133.
31. Andreeva, A., Howorth, D., Brenner, S. E., Hubbard, T. J. P., Chothia, C., and Murzin, A. G. (2004) SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res. 32, D226-D229.
32. Fraaije, M. W., van den Heuvel, R. H. H., van Berkel, W. J. H., and Mattevi, A. (2000) Structural analysis of flavinylation in vanillyl-alcohol oxidase, J. Biol. Chem. 275, 38654-38658.
33. Thunnissen, M. M., Taddei, N., Liguri, G., Ramponi, G., and Nordlund, P. (1997) Crystal structure of common type acylphosphatase from bovine testis, Structure 5, 69-79.
34. Swindells, M. B., Orengo, C. A., Jones, D. T., Pearl, L. H., and Thornton, J. M. (1993) Recurrence of a binding motif, Nature 362, 299-299.
35. Rosenzweig, A. C., and O'Halloran, T. V. (2000) Structure and chemistry of the copper chaperone proteins, Curr. Opin. Chem. Biol. 4, 140-147.
36. Lytle, B. L., Peterson, F. C., Kjer, K. L., Frederick, R. O., Zhao, Q., Thao, S., Bingman, C., Johnson, K. A., Phillips, G. N., and Volkman, B. F. (2004) Structure of the hypothetical protein At3g17210 from Arabidopsis thaliana, J. Biomol. NMR 28, 397-400.
37. Nooren, I. M. A., and Thornton, J. M. (2003) Diversity of protein-protein interactions, EMBO J. 22, 3486-3492.
38. 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.
39. Hasegawa, K., Masuda, S., and Ono, T. A. (2004) Structural intermediate in the photocycle of a BLUF (sensor of blue light using FAD) protein Slr1694 in a cyanobacteriura Synechocystis sp. PCC6803, Biochemistry 43, 14979-14986.
40. Masuda, S., Hasegawa, K., and Ono, T. A. (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.
41. Fraaije, M. W., and Mattevi, A. (2000) Flavoenzymes: diverse catalysts with recurrent features. Trends Biochem. Sci. 25, 126-132.
42. Ghisla, S., and Massey, V. (1989) Mechanisms of flavoprotein-catalyzed reactions, Eur. J. Biochem. 181, 1-17.
43. Deisenhofer, J. (2000) DNA photolyases and cryptochromes, Mutat. Res. 460, 143-149.
44. Brautigam, C. A., Smith, B. S., Ma, Z. Q., Palnitkar, M., Tomchick, D. R., Machius, M., and Deisenhofer, J. (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana, Proc. Natl. Acad. Sci. U.S.A. 101, 12142-12147.
45. Crosson, S., and Moffat, K. (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch, Plant Cell 14, 1067-1075.