The amino acids surrounding the flavin 7a-methyl group determine the UVA spectral features of a LOV protein

Biological Chemistry

Volumn 394, Issue 11, 2013, Pages 1517-1528

  Raffelberg, Sarah ^b   Gutt, Alexander ^b   Gärtner, Wolfgang ^b   Mandalari, Carmen ^a   Abbruzzetti, Stefania ^a   Viappiani, Cristiano ^a   Losi, Aba ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

Author keywords

Photobiophysics; Photochemistry; Spectral tuning; UVA blue light sensing; YtvA

Indexed keywords

DESONIDE; QUERCETIN DERIVATIVE; RIBOFLAVIN BINDING PROTEIN; THREONINE;

ABSORPTION; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DIPOLE; FLUORESCENCE ANALYSIS; GENE MUTATION; ILLUMINATION; LIGHT; NONHUMAN; PHOTOACOUSTIC SPECTROSCOPY; PRIORITY JOURNAL; QUANTUM YIELD;

AMINO ACID MOTIFS; CONSERVED SEQUENCE; FLAVIN MONONUCLEOTIDE; FLAVINS; LASERS; MICROSCOPY, FLUORESCENCE; MUTATION; NEUROSPORA CRASSA; PHOTOACOUSTIC TECHNIQUES; PHOTOCHEMISTRY; PHOTORECEPTORS, MICROBIAL; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; ULTRAVIOLET RAYS;

EID: 84888086103     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2013-0163     Document Type: Article

References (60)

1. Abbruzzetti, S., Viappiani, C., Murgida, D.H., Erra-Balsells, R., and Bilmes, G.M. (1999). Non-toxic, water-soluble photocalorimetric reference compounds for UV and visible excitation. Chem. Phys. Lett. 304, 167-172. (Pubitemid 129556310)
2. Avila-Perez, M., Hellingwerf, K.J., and Kort, R. (2006). Blue light activates the sigmaB-dependent stress response of Bacillus subtilis via YtvA. J. Bacteriol. 188, 6411-6414. (Pubitemid 44448584)
3. Bauer, C., Rabl, C.R., Heberle, J., and Kottke, T. (2011). Indication for a radical intermediate preceding the signaling state in the LOV domain photocycle. Photochem. Photobiol. 87, 548-553.
4. Bonetti, C., Stierl, M., Mathes, T., van Stokkum, I.H.M., Mullen, K.M., Cohen-Stuart, T.A., van Grondelle, R., Hegemann, P., and Kennis, J.T.M. (2009). The role of key amino acids in the photoactivation pathway of the synechocystis Slr1694 BLUF domain. Biochemistry 48, 11458-11469.
5. Briggs, W.R. and Huala, E. (1999). Blue-light photoreceptors in higher plants. Annu. Rev. Cell. Dev. Biol. 15, 33-62. (Pubitemid 32250370)
6. Brosi, R., Illarionov, B., Mathes, T., Fischer, M., Joshi, M., Bacher, A., Hegemann, P., Bittl, R., Weber, S., and Schleicher, E. (2010). Hindered rotation of a cofactor methyl group as a probe for protein-cofactor interaction. J. Am. Chem. Soc. 132, 8935-8944.
7. Cao, Z., Buttani, V., Losi, A., and Gärtner, W. (2008). A blue light inducible two component signal transduction system in the plant pathogen Pseudomonas syringae pv. tomato. Biophys. J. 94, 897-905. (Pubitemid 351162456)
8. Cao, Z., Livoti, E., Losi, A., and Gärtner, W. (2010). A blue lightinducible phosphodiesterase activity in the cyanobacterium Synechococcus elongatus. Photochem. Photobiol. 86, 606-611.
9. Chan, R.H., Lewis, J.W., and Bogomolni, R.A. (2013). Photocycle of the LOV-STAS protein from the pathogen Listeria monocytogenes. Photochem. Photobiol. 89, 361-369.
10. 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. USA 96, 8779-8783. (Pubitemid 29354868)
11. Christie, J.M., Corchnoy, S.B., Swartz, T.E., Hokenson, M., Han, I.-S., Briggs, W.R., and Bogomolni, R.A. (2007). Steric interactions stabilize the signaling state of the LOV2 domain of phototropin 1. Biochemistry 46, 9310-9319. (Pubitemid 47255043)
12. Climent, T., Gonzalez-Luque, R., Merchan, M., and Serrano-Andres, L. (2006). Theoretical insight into the spectroscopy and photochemistry of isoalloxazine, the flavin core ring. J. Phys. Chem. A 110, 13584-13590. (Pubitemid 46201583)
13. Djouani-Tahri, E.B., Christie, J.M., Sanchez-Ferandin, S., Sanchez, F., Bouget, F.Y., and Corellou, F. (2011). A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus. Plant J. 65, 578-588.
14. Fedorov, R., Schlichting, I., Hartmann, E., Domratcheva, T., Fuhrmann, M., and Hegemann, P. (2003). Crystal structures and molecular mechanism of a light-induced signaling switch: the Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys. J. 84, 2492-2501.
15. Gaidenko, T.A., Kim, T.J., Weigel, A.L., Brody, M.S., and Price, C.W. (2006). The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J. Bacteriol. 188, 6387-6395. (Pubitemid 44448581)
16. Gauden, M., Crosson, S., van Stokkum, I.H.M., van Grondelle, R., Moffat, K., and Kennis, J.T.M. (2004). Low-temperature and time-resolved spectroscopic characterization of the LOV2 domain of Avena sativa phototropin. In: Femtosecond Laser Applications in Biology, S. Avrilleir and J.M. Tualle, eds. (Bellingham, WA: SPIE), 5463, pp. 97-104.
17. Hendrischk, A.K., Moldt, J., Fruhwirth, S.W., and Klug, G. (2009). Characterization of an unusual LOV domain protein in the alpha-proteobacterium Rhodobacter sphaeroides. Photochem. Photobiol. 85, 1254-1259.
18. Holzer, W., Penzkofer, A., Susdorf, T., Alvarez, M., Islam, S., and Hegemann, P. (2004). Absorption and emission spectroscopic characterisation of the LOV2-domain of phot from Chlamydomonas reinhardtii fused to a maltose binding protein. Chem. Phys. 302, 105-118.
19. Islam, S.D.M., Penzkofer, A., and Hegemann, P. (2003). Quantum yield of triplet formation of riboflavin in aqueous solution and of flavin mononucleotide bound to the LOV1 domain of Phot1 from Chlamydomonas reinhardtii. Chem. Phys. 291, 97-114.
20. Iwata, T., Nozaki, D., Tokutomi, S., and Kandori, H. (2005). Comparative investigation of the LOV1 and LOV2 domains in Adiantum phytochrome 3. Biochemistry 44, 7427-7434. (Pubitemid 40695996)
21. Jentzsch, K., Wirtz, A., Circolone, F., Drepper, T., Losi, A., Gärtner, W., Jaeger, K.-E., and Krauss, U. (2009). Mutual exchange of kinetic properties by extended mutagenesis in two short LOV domain proteins from Pseudomonas putida. Biochemistry 48, 10321-10333.
22. Johansson, L.B., Davidsson, A., Lindblom, G., and Naqvi, K.R. (1979). Electronic transitions in the isoalloxazine ring and orientation of flavins in model membranes studied by polarized light spectroscopy. Biochemistry 18, 4249-4253.
23. Kasahara, M., Swartz, T.E., Olney, M.A., Onodera, A., Mochizuki, N., Fukuzawa, H., Asamizu, E., Tabata, S., Kanegae, H., Takano, M., et al. (2002). Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii. Plant Physiol. 129, 762-773. (Pubitemid 34689160)
24. Kennis, J.T.M., van Stokkum, I.H.M., Crosson, S., Gauden, M., Moffat, K., and van Grondelle, R. (2004). The LOV2 domain of phototropin: a reversible photochromic switch. J. Am. Chem. Soc. 126, 4512-4513. (Pubitemid 38469088)
25. Kottke, T., Heberle, J., Dominic H., Dick, B., and Hegemann, P. (2003). Phot-LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. Biophys. J. 84, 1192-1201. (Pubitemid 36133440)
26. Krauss, U., Losi, A., Gärtner, W., Jaeger, K.-E., and Eggert, T. (2005). Initial characterization of a blue-light sensing, phototropinrelated protein from Pseudomonas putida: a paradigm for an extended LOV construct. Phys. Chem. Chem. Phys. 7, 2229-2236.
27. Losi, A. (2007). Flavin-based blue-light photosensors: a photobiophysics update. Photochem. Photobiol. 83, 1283-1300. (Pubitemid 350132622)
28. Losi, A. and Braslavsky, S.E. (2003). The time-resolved thermodynamics of the chromophore-protein interactions in biological photosensors. Learning from photothermal measurements. Phys. Chem. Chem. Phys. 5, 2739-2750.
29. Losi, A. and Gärtner, W. (2011). Old chromophores, new photoactivation paradigms, trendy applications: flavins in blue light-sensing photoreceptors. Photochem. Photobiol. 87, 491-510.
30. Losi, A. and Gärtner, W. (2012). The evolution of flavin-binding photoreceptors: an ancient chromophore serving trendy blue-light sensors. Annu. Rev. Plant Biol. 63, 49-72.
31. Losi, A., Wegener, A.A., Engelhardt, M., and Braslavsky, S.E. (2001). Enthalpy-entropy compensation in a photocycle: the K to L transition in sensory rhodopsin II from Natronobacterium pharaonis. J. Am. Chem. Soc. 123, 1766-1767. (Pubitemid 32179430)
32. Losi, A., Polverini, E., Quest, B., and Gärtner, W. (2002). First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys. J. 82, 2627-2634. (Pubitemid 34441300)
33. Losi, A., Quest, B., and Gärtner, W. (2003). Listening to the blue: the time-resolved thermodynamics of the bacterial blue-light receptor YtvA and its isolated LOV domain. Photochem. Photobiol. Sci. 2, 759-766. (Pubitemid 41662962)
34. Losi, A., Kottke, T., and Hegemann, P. (2004). Recording of blue light-induced energy and volume changes within the wild-type and mutated Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys. J. 86, 1051-1060. (Pubitemid 38209549)
35. Losi, A., Gärtner, W., Raffelberg, S., Cella Zanacchi, F., Bianchini, P., Diaspro, A., Mandalari, C., Abbruzzetti, S., and Viappiani, C. (2013). A photochromic bacterial photoreceptor with potential for super-resolution microscopy. Photochem. Photobiol. Sci. 12, 231-235.
36. Mandalari, C., Losi, A., and Gärtner, W. (2013). Distance-tree analysis, distribution and co-presence of bilin- and flavinbinding prokaryotic photoreceptors for visible light. Photochem. Photobiol. Sci. 18, 1144-1157.
37. Möglich, A., Ayers, R.A., and Moffat, K. (2009). Structure and signaling mechanism of per-ARNT-Sim domains. Structure 17, 1282-1294.
38. Narikawa, R., Zikihara, K., Okajima, K., Ochiai, Y., Katayama, M., Shichida, Y., Tokutomi, S., and Ikeuchi, M. (2006). Three putative photosensory light, oxygen or voltage (LOV) domains with distinct biochemical properties from the filamentous cyanobacterium Anabaena sp. PCC 7120. Photochem. Photobiol. 82, 1627-1633. (Pubitemid 46158855)
39. Nash, A.I., McNulty, R., Shillito, M.E., Swartz, T.E., Bogomolni, R.A., Luecke, H., and Gardner, K.H. (2011). Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turnhelix (LOV-HTH) DNA-binding protein. Proc. Natl. Acad Sci. USA 108, 9449-9454.
40. Onodera, A., Christie, J.M., Kasahara, M., Mochizuki, N., Asamizu, E., Tabata, S., Fukuzawa, H., Briggs, W.R., and Nagatani, A. (2002). Analysis of phototropin-like gene of Chlamydomonas reinhardtii. Plant Cell Physiol. 43, S230.
41. Penzkofer, A., Endres, L., Schiereis, T., and Hegemann, P. (2005). Yield of photo-adduct formation of LOV domains from Chlamydomonas reinhardtii by picosecond laser excitation. Chem. Phys. 316, 185-194. (Pubitemid 41253584)
42. Penzkofer, A., Bansal, A.K., Song, S.H., and Dick, B. (2007). Fluorescence quenching of flavins by reductive agents. Chem. Phys. 336, 14-21.
43. Purcell, E.B., McDonald, C.A., Palfey, B.A., and Crosson, S. (2010). An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry 49, 6761-6770.
44. Raffelberg, S., Mansurova, M., Gärtner, W., and Losi, A. (2011). Modulation of the photocycle of a LOV domain photoreceptor by the hydrogen bonding network. J. Am. Chem. Soc. 133, 5346-5356.
45. Rinaldi, J., Gallo, M., Klinke, S., Paris, G., Bonomi, H.R., Bogomolni, R.A., Cicero, D.O., and Goldbaum, F.A. (2012). The β-scaffold of the LOV domain of the Brucella light-activated histidine kinase is a key element for signal transduction. J. Mol. Biol. 420, 112-127.
46. Rudzki, J.E., Goodman, J.L., and Peters, K.S. (1985). Simultaneous determination of photoreaction dynamics and energetics using pulsed, time resolved photoacoustic calorimetry. J. Am. Chem. Soc. 107, 7849-7854.
47. 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. (Pubitemid 30626330)
48. Salzmann, S., Tatchen, J., and Marian, C.M. (2008). The photophysics of flavins: what makes the difference between gas phase and aqueous solution? J. Photochem. Photobiol. A Chem. 198, 221-231.
49. Sato, Y., Nabeno, M., Iwata, T., Tokutomi, S., Sakurai, M., and Kandori, H. (2007). Heterogeneous environment of the S-H group of Cys966 near the flavin chromophore in the LOV2 domain of Adiantum neochrome1. Biochemistry 46, 10258-10265. (Pubitemid 350067619)
50. Schwerdtfeger, C. and Linden, H. (2003). VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J. 22, 4846-4855. (Pubitemid 37162920)
51. Song, S.H., Freddolino, P.L., Nash, A.I., Carroll, E.C., Schulten, K., Gardner, K.H., and Larsen, D.S. (2011). Modulating LOV domain photodynamics with a residue alteration outside the chromophore binding site. Biochemistry 50, 2411-2423.
52. 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.
53. Swartz, T.E., Tseng, T.S., Frederickson, M.A., Paris, G., Comerci, D.J., Rajashekara, G., Kim, J.G., Mudgett, M.B., Splitter, G.A., Ugalde, R.A., et al. (2007). Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317, 1090-1093. (Pubitemid 47330194)
54. Takahashi, F., Yamagata, D., Ishikawa, M., Fukamatsu, Y.,Ogura, Y., Kasahara, M., Kiyosue, T., Kikuyama, M., Wada, M., and Kataoka, H. (2007). AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc. Natl. Acad. Sci. USA 104, 19625-19630.
55. Tang, Y., Cao, Z., Livoti, E., Krauss, U., Jaeger, K.-E., Gärtner, W., and Losi, A. (2010). Interdomain signalling in the blue-light sensing and GTP-binding protein YtvA: a mutagenesis study uncovering the importance of specific protein sites. Photochem. Photobiol. Sci. 9, 47-56.
56. Tsentalovich, Y.P., Lopez, J.J., Hore, P.J., and Sagdeev, R.Z. (2002). Mechanisms of reactions of flavin mononucleotide triplet with aromatic amino acids. Spectrochim. Acta A 58, 2043-2050. (Pubitemid 34624049)
57. van den Berg, P.W., Widengren, J., Hink, M.A., Rigler, R., and Visser, A.G. (2001). Fluorescence correlation spectroscopy of flavins and flavoenzymes: photochemical and photophysical aspects. Spectrochim. Acta A 57, 2135-2144. (Pubitemid 32867021)
58. Walter, J., Hausmann, S., Drepper, T., Puls, M., Eggert, T., and Dihné, M. (2012). Flavin mononucleotide-based fluorescent proteins function in mammalian cells without oxygen requirement. Plos One 7, e43921.
59. Zoltowski, B.D., Schwerdtfeger, C., Widom, J., Loros, J.J., Bilwes, A.M., Dunlap, J.C., and Crane, B.R. (2007). Conformational switching in the fungal light sensor Vivid. Science 316, 1054-1057. (Pubitemid 46799496)
60. Zoltowski, B.D., Vaccaro, B., and Crane, B.R. (2009). Mechanismbased tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5, 827-834.