Crystal Structures of the AppA BLUF Domain Photoreceptor Provide Insights into Blue Light-mediated Signal Transduction

Journal of Molecular Biology

Volumn 362, Issue 4, 2006, Pages 717-732

  Jung, Astrid ^a   Reinstein, Jochen ^a   Domratcheva, Tatiana ^a   Shoeman, Robert L ^a   Schlichting, Ilme ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

BLUF; crystallography; photoreceptor; signal transduction

Indexed keywords

APPA PROTEIN; BACTERIAL PROTEIN; CARBONYL DERIVATIVE; DETERGENT; FLAVINE ADENINE NUCLEOTIDE; GLUTAMINE; METHIONINE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BINDING SITE; BLUE LIGHT; BLUE LIGHT USING FLAVINE ADENINE NUCLEOTIDE DOMAIN; CELL MOTILITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DARK ADAPTATION; ENZYME ACTIVE SITE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; HYDROGEN BOND; ILLUMINATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE METABOLISM; PHOTOREACTIVITY; PHOTORECEPTOR; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS);

EID: 33748300578     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.024     Document Type: Article

References (38)

1. van der Horst M.A., and Hellingwerf K.J. Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Accts. Chem. Res. 37 (2004) 13-20
2. Gomelsky M., and Kaplan S. AppA, a novel gene encoding a trans-acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 177 (1995) 4609-4618
3. Gomelsky M., and Kaplan S. Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 179 (1997) 128-134
4. Gomelsky M., and Kaplan S. 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 (1998) 35319-35325
5. Masuda S., and Bauer C.E. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110 (2002) 613-623
6. Gomelsky M., and Klug G. BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27 (2002) 497-500
7. Schmidt A.J., Ryjenkov D.A., and Gomelsky M. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187 (2005) 4774-4781
8. Masuda S., Hasegawa K., Ishii A., and Ono T.A. 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 (2004) 5304-5313
9. Han Y., Braatsch S., Osterloh L., and Klug G. A eukaryotic BLUF domain mediates light-dependent gene expression in the purple bacterium Rhodobacter sphaeroides 2.4.1. Proc. Natl Acad. Sci. USA 101 (2004) 12306-12311
10. Dragnea V., Waegele M., Balascuta S., Bauer C., and Dragnea B. Time-resolved spectroscopic studies of the AppA blue-light receptor BLUF domain from Rhodobacter sphaeroides. Biochemistry 44 (2005) 15978-15985
11. Gauden M., Yeremenko S., Laan W., van Stokkum I.H., Ihalainen J.A., van Grondelle R., et al. Photocycle of the flavin-binding photoreceptor AppA, a bacterial transcriptional antirepressor of photosynthesis genes. Biochemistry 44 (2005) 3653-3662
12. Kita A., Okajima K., Morimoto Y., Ikeuchi M., and Miki K. Structure of a cyanobacterial BLUF protein, Tll0078, containing a novel FAD-binding blue light sensor domain. J. Mol. Biol. 349 (2005) 1-9
13. Jung A., Domratcheva T., Tarutina M., Wu Q., Ko W.H., Shoeman R.L., et al. Structure of a bacterial BLUF photoreceptor: insights into blue light-mediated signal transduction. Proc. Natl Acad. Sci. USA 102 (2005) 12350-12355
14. Anderson S., Dragnea V., Masuda S., Ybe J., Moffat K., and Bauer C. Structure of a Novel Photoreceptor, the BLUF Domain of AppA from Rhodobacter sphaeroides. Biochemistry 44 (2005) 7998-8005
15. Kraft B.J., Masuda S., Kikuchi J., Dragnea V., Tollin G., Zaleski J.M., and Bauer C.E. Spectroscopic and mutational analysis of the blue-light photoreceptor AppA: a novel photocycle involving flavin stacking with an aromatic amino acid. Biochemistry 42 (2003) 6726-6734
16. Laan W., van der Horst M.A., van Stokkum I.H., and Hellingwerf K.J. 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 (2003) 290-297
17. van der Horst M.A., Laan W., Yeremenko S., Wende A., Palm P., Oesterhelt D., and Hellingwerf K.J. From primary photochemistry to biological function in the blue-light photoreceptors PYP and AppA. Photochem. Photobiol. Sci. 4 (2005) 688-693
18. Grinstead J.S., Hsu S.T., Laan W., Bonvin A.M., Hellingwerf K.J., Boelens R., and Kaptein R. The solution structure of the AppA BLUF domain: insight into the mechanism of light-induced signaling. ChemBiochem. 7 (2006) 187-193
19. Pal D., and Chakrabarti P. Non-hydrogen bond interactions involving the methionine sulfur atom. J. Biomol. Struct. Dynam. 19 (2001) 115-128
20. Rosenfield R.E., Parthasarathy R., and Dunitz J.D. Directional preferences of nonbonded atomic contacts with divalent sulfur. 1. Electrophiles and nucleophiles. J. Am. Chem. Soc. 99 (1977) 4860-4862
21. Gauden, M., van Stokkum, I. H., Key, J. M., Luhrs, D. C., van Grondelle, Hegemann, R. P., & Kennis, J. T., (2006). Hydrogen bond switching via a radical pair mechanism in a flavin-binding photoreceptor. Proc. Natl Acad. Sci. USA (in press).
22. Unno M., Masuda S., Ono T.A., and Yamauchi S. 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 (2006) 5638-5639
23. Masuda S., Hasegawa K., and Ono T.A. Tryptophan at position 104 is involved in transforming light signal into changes of beta-sheet structure for the signaling state in the BLUF domain of AppA. Plant Cell Physiol. 46 (2005) 1894-1901
24. Laan W., Gauden M., Yeremenko S., van Grondelle R., Kennis J.T., and Hellingwerf K.J. On the mechanism of activation of the BLUF domain of AppA. Biochemistry 45 (2006) 51-60
25. Fukushima Y., Okajima K., Shibata Y., Ikeuchi M., and Itoh S. Primary intermediate in the photocycle of a blue-light sensory BLUF FAD-protein, Tll0078, of Thermosynechococcus elongatus BP-1. Biochemistry 44 (2005) 5149-5158
26. Hasegawa K., Masuda S., and Ono T.A. Structural intermediate in the photocycle of a BLUF (sensor of blue light using FAD) protein Slr1694 in a Cyanobacterium Synechocystis sp. PCC6803. Biochemistry 43 (2004) 14979-14986
27. Vetter I.R., and Wittinghofer A. Nucleoside triphosphate-binding proteins: different scaffolds to achieve phosphoryl transfer. Quart. Rev. Biophys. 32 (1999) 1-56
28. Laan W., Bednarz T., Heberle J., and Hellingwerf K.J. Chromophore composition of a heterologously expressed BLUF-domain. Photochem. Photobiol. Sci. 3 (2004) 1011-1016
29. Zirak P., Penzkofer A., Schiereis T., Hegemann P., Jung A., and Schlichting I. Absorption and fluorescence spectroscopic characterization of BLUF domain of AppA from Rhodobacter sphaeroides. Chem. Phys. 315 (2005) 142-154
30. Zirak P., Penzkofer A., Schiereis T., Hegemann P., Jung A., and Schlichting I. Photodynamics of the small BLUF protein BlrB from Rhodobacter sphaeroides. J. Photochem. Photobiol. B. 83 (2006) 180-194
31. Masuda S., Hasegawa K., and Ono T.A. 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 (2005) 1215-1224
32. Ma J.C., and Dougherty D.A. The Cationminus signpi interaction. Chem. Rev. 97 (1997) 1303-1324
33. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., and Clardy J. Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 252 (1991) 839-842
34. Kabsch W. Automatic processing of rotation diffraction dadta from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 26 (1993) 795-806
35. Sheldrick G., and Schneider T. SHELXL: high resolution refinement. Methods Enzymol. 277 (1997) 319-343
36. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
37. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
38. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., and Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallog. sect. D 55 (1999) 247-255