Crucial role in light signal transduction for the conserved Met93 of the BLUF protein PixD/Slr1694

Plant and Cell Physiology

Volumn 49, Issue 10, 2008, Pages 1600-1606

  Masuda, Shinji ^a   Hasegawa, Koji ^b   Ohta, Hiroyuki ^a   Ono, Taka Aki ^c  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b ADVANCESOFT CORPORATION   (Japan)

^c IBARAKI UNIVERSITY   (Japan)

Author keywords

BLUF; Cyanobacteria; Flavin; Photoreceptor; PixD

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; FLAVOPROTEIN; METHIONINE; VISUAL PROTEINS AND PIGMENTS;

ARTICLE; GENETIC COMPLEMENTATION; GENETICS; INFRARED SPECTROSCOPY; LIGHT; METABOLISM; PHOTOTRANSDUCTION; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; SYNECHOCYSTIS;

BACTERIAL PROTEINS; DNA, BACTERIAL; FLAVOPROTEINS; GENETIC COMPLEMENTATION TEST; LIGHT; METHIONINE; MUTAGENESIS, SITE-DIRECTED; PHOTORECEPTORS, MICROBIAL; PHOTOTRANSDUCTION; PROTEIN STRUCTURE, TERTIARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SYNECHOCYSTIS;

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 54149118236     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcn132     Document Type: Article

References (45)

1. 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.
2. Braatsch, S., Gomelsky, M., Kuphal, S. and Klug, G. (2002) A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol. Microbiol. 45: 827-836.
3. Davison, J., Heusterspreute, M., Chevalier, N., Ha-Thi, V. and Brunel, F. (1987) Vectors with restriction site banks. V. pJRD215, a wide-host-range cosmid vector with multiple cloning sites. Gene 51: 275-280.
4. Domratcheva, T., Grigorenko, B.L., Schlichting, I. and Nemukhin, A.V. (2008) Molecular models predict light-induced glutamine tautomerization in BLUF photoreceptors. Biophys. J. 94: 3872-3879.
5. 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.
6. Fukushima, Y., Murai, Y., Okajima, K., Ikeuchi, M. and Itoh, S. (2008) Photoreactions of Tyr8- and Gln50-mutated BLUF domains of the PixD protein of Thermosynechococcus elongatus BP-1: photoconversion at low temperature without Tyr8. Biochemistry 47: 660-669.
7. Gauden, M., Grinstead, J.S., Laan, W., van Stokkum, I.H., Avila-Perez, M., Toh, K.C., Boelens, R., Kaptein, R., van Grondelle, R., Hellingwerf, K.J. and Kennis, J.T. (2007) On the role of aromatic side chains in the photoactivation of BLUF domains. Biochemistry 46: 7405-7415.
8. Gauden, M., van Stokkum, I.H., Key, J.M., Luhrs, D., van Grondelle, R., Hegemann, P. and Kennis, J.T. (2006) Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor. Proc. Natl Acad. Sci. USA 103: 10895-10900.
9. Gauden, M., Yeremenko, S., Laan, W., van Stokkum, I.H., Ihalainen, J.A., 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.
10. Gomelsky, M. and Kaplan, S. (1995) appA, a novel gene encoding a transacting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 177: 4609-4618.
11. Gomelsky, M. and Klug, G. (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27: 497-500.
12. Grinstead, J.S., Avila-Perez, M., Hellingwerf, K.J., Boelens, R. and Kaptein, R. (2006a) Light-induced flipping of a conserved glutamine sidechain and its orientation in the AppA BLUF domain. J. Am. Chem. Soc. 128: 15066-15067.
13. Grinstead, J.S., Hsu, S.T., Laan, W., Bonvin, A.M., Hellingwerf, K.J., Boelens, R. and Kaptein, R. (2006b) The solution structure of the AppA BLUF domain: insight into the mechanism of light-induced signaling. Chembiochem 7: 187-193.
14. 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 Cyanobacterium Synechocystis sp. PCC6803. Biochemistry 43: 14979-14986.
15. Hasegawa, K., Masuda, S. and Ono, T.A. (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.A. (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.
17. 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.
18. Jung, A., Domratcheva, T., Tarutina, M., Wu, Q., Ko, W.H., 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. USA 102: 12350-12355.
19. 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.
20. Kennis, J.T. and Groot, M.L. (2007) Ultrafast spectroscopy of biological photoreceptors. Curr. Opin. Struct. Biol. 17: 623-630.
21. Kita, A., Okajima, K., Morimoto, Y., Ikeuchi, M. and Miki, K. (2005) Structure of a cyanobacterial BLUF protein, Tll0078, containing a novel FAD-binding blue light sensor domain. J. Mol. Biol. 349: 1-9.
22. 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.
23. Kreps, S., Ferino, F., Mosrin, C., Gerits, J., Mergeay, M. and Thuriaux, P. (1990) Conjugative transfer and autonomous replication of a promiscuous IncQ plasmid in the cyanobacterium Synechocystis PCC 6803. Mol. Gen. Genet. 221: 129-133.
24. 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.
25. Losi, A. (2007) Flavin-based blue-light photosensors: a photobiophysics update. Photochem. Photobiol. 83: 1283-1300.
26. Majerus, T., Kottke, T., Laan, W., Hellingwerf, K. and Heberle, J. (2007) Time-resolved FT-IR spectroscopy traces signal relay within the blue-light receptor AppA. Chemphyschem 8: 1787-1789.
27. 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.
28. Masuda, S. and Bauer, C.E. (2005) The antirepressor AppA uses the novel flavin-binding BLUF domain as blue-light-absorbing photoreceptor to control photosystem synthesis. In Handbook of Photosensory Receptors. Edited by Briggs, W.R. and Spudich, J. pp. 433-445. Wiley-VCH Verlag GmbH, Weinheim.
29. Masuda, S., Hasegawa, K., Ishii, A. and Ono, T.A. (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.
30. Masuda, S., Hasegawa, K. and Ono, T.A. (2005a) Adenosine diphosphate moiety does not participate in structural changes for the signaling state in the sensor of blue-light using FAD domain of AppA. FEBS Lett. 579: 4329-4332.
31. Masuda, S., Hasegawa, K. and Ono, T.A. (2005b) 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.
32. Masuda, S., Hasegawa, K. and Ono, T.A. (2005c) 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.
33. Masuda, S. and Ono, T.A. (2004) Biochemical characterization of the major adenylyl cyclase, Cya1, in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 577: 255-258.
34. Masuda, S., Tomida, Y., Ohta, H. and Takamiya, K. (2007) The critical role of a hydrogen bond between Gln63 and Trp104 in the blue-light sensing BLUF domain that controls AppA activity. J. Mol. Biol. 368: 1223-1230.
35. Obanayama, K., Kobayashi, H., Fukushima, K. and Sakurai, M. (2008) Structures of the chromophore binding sites in BLUF domains as studied by molecular dynamics and quantum chemical calculations. Photochem. Photobiol. 84: 1003-1010.
36. Okajima, K., Yoshihara, S., Fukushima, Y., Geng, X., Katayama, M., et al. (2005) Biochemical and functional characterization of BLUF-type flavin-binding proteins of two species of cyanobacteria. J. Biochem. 137: 741-750.
37. Simon, R., Priefer, U. and Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1: 37-45.
38. Stelling, A.L., Ronayne, K.L., Nappa, J., Tonge, P.J. and Meech, S.R. (2007) Ultrafast structural dynamics in BLUF domains: transient infrared spectroscopy of AppA and its mutants. J. Am. Chem. Soc. 129: 15556-15564.
39. Takahashi, R., Okajima, K., Suzuki, H., Nakamura, H., Ikeuchi, M. and Noguchi, T. (2007) FTIR study on the hydrogen bond structure of a key tyrosine residue in the flavin-binding blue light sensor TePixD from Thermosynechococcus elongatus. Biochemistry 46: 6459-6467.
40. Toh, K.C., van Stokkum, I.H., Hendriks, J.C., Alexandre, M.T., Arents, J.C., Avila-Perez, M., van Grondelle, R., Hellingwerf, K.J. and Kennis, J.T. (2008) On the signaling mechanism and the absence of photoreversibility in the AppA BLUF domain. Biophys. J. 95: 312-321.
41. Unno, M., Masuda, S., Ono, T.A. 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.
42. Unno, M., Sano, R., Masuda, S., Ono, T.A. 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.
43. 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.
44. 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.
45. Zirak, P., Penzkofer, A., Schiereis, T., Hegemann, P. and Schlichting, I. (2005) Absorption and fluorescence spectroscopic characterization of BLUF domain of AppA from Rhodobacter sphaeroides. Chem. Phys. 315: 142-154.