A base-catalyzed mechanism for dark state recovery in the Avena sativa phototropin-1 LOV2 domain

Biochemistry

Volumn 46, Issue 11, 2007, Pages 3129-3137

  Alexandre, Maxime T A ^a   Arents, Jos C ^b   Van Grondelle, Rienk ^a   Hellingwerf, Klaas J ^b   Kennis, John T M ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPLAST RELOCATION; FLAVIN MONONUCLEOTIDE (FMN); PHOTOTROPINS; PHOTOTROPISM;

BINDING SITES; CELLS; CONCENTRATION (PROCESS); LIGHT ABSORPTION; PH; PHOSPHORYLATION; RATE CONSTANTS; TITRATION;

ENZYMES;

DIETHYL PYROCARBONATE; FLAVINE MONONUCLEOTIDE; HISTIDINE; PHOTOTROPIN; PROTEIN LOV1; PROTEIN LOV2; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BLUE LIGHT; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHROMATOPHORE; CRYSTAL STRUCTURE; OAT; PHOTOTROPISM; PLANT STOMA; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; AVENA SATIVA; DARKNESS; DIETHYL PYROCARBONATE; FLAVIN MONONUCLEOTIDE; FLAVOPROTEINS; HISTIDINE; HYDROGEN-ION CONCENTRATION; IMIDAZOLES; KINETICS; MODELS, MOLECULAR; PHOTOTROPISM; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES;

AVENA SATIVA;

EID: 33947377466     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062074e     Document Type: Article

References (41)

1. Christie, J. M., and Briggs, W. R. (2005) in Handbook of Photosensory Receptors (Briggs, W. R., and Spudich, J. L., Eds.) pp 277-304, Wiley-VCH Verlag GmbH & Co., Weinheim, Germany.
2. Christie, J. M., Reymond, P., Powell, G. K., Bernasconi, P., Raibekas, A. A., Liscum, E., and Briggs, W. R. (1998) Arabidopsis NPH1: A flavoprotein with the properties of a photoreceptor for phototropism, Science 282, 1698-1701.
3. Losi, A. (2004) The bacterial counterparts of plant phototropins, Photochem. Photobiol. Sci. 3, 566-574.
4. Crosson, S., Rajagopal, S., and Moffat, K. (2003) The LOV domain family: Photoresponsive signaling modules coupled to diverse output domains, Biochemistry 42, 2-10.
5. Ballario, P., Talora, C., Galli, D., Linden, H., and Macino, G. (1998) Roles in dimerization and blue light photoresponse of the PAS and LOV domains of Neurospora crassa white collar proteins, Mol. Microbiol. 29, 719-729.
6. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R., and Kay, S. A. (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis, Nature 426, 302-306.
7. He, Q. Y., Cheng, P., Yang, Y. H., Wang, L. X., Gardner, K. H., and Liu, Y. (2002) White collar-1, a DNA binding transcription factor and a light sensor, Science 297, 840-843.
8. 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.
9. 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.
10. 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, 2474-2482.
11. Kennis, J. T. M., Crosson, S., Gauden, M., van Stokkum, I. H. M., Moffat, K., and van Grondelle, R. (2003) Primary reactions of the LOV2 domain of phototropin, a plant blue-light photoreceptor, Biochemistry 42, 3385-3392.
12. Kottke, T., Heberle, J., Hehn, D., 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.
13. Crosson, S., and Moffat, K. (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch, Plant Cell 14, 1067-1075.
14. Salomon, M., Eisenreich, W., Durr, H., Schleicher, E., Knieb, E., Massey, V., Rudiger, W., Muller, F., Bacher, A., and Richter, G. (2001) An optomechanical transducer in the blue light receptor phototropin from Avena sativa, Proc. Natl. Acad. Sci. U.S.A. 98, 12357-12361.
15. 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.
16. 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.
17. Kasahara, M., Swartz, T. E., Olney, M. A., Onodera, A., Mochizuki, N., Fukuzawa, H., Asamizu, E., Tabata, S., Kanegae, H., Takano, M., Christie, J. M., Nagatani, A., and Briggs, W. R. (2002) Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii, Plant Physiol. 129, 762-773.
18. 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.
19. Guo, H. M., Kottke, T., Hegemann, P., and Dick, B. (2005) The Phot LOV2 domain and its interaction with LOV1, Biophys. J. 89, 402-412.
20. Losi, A., Polverini, E., Quest, B., and Gartner, W. (2002) First evidence for phototropin-related blue-light receptors in prokaryotes, Biophys. J. 82, 2627-2634.
21. 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.
22. Iwata, T., Nozaki, D., Tokutomi, S., and Kandori, H. (2005) Comparative investigation of the LOV1 and LOV2 domains in Adiantum phytochrome3, Biochemistry 44, 7427-7434.
23. Nozaki, D., Iwata, T., Ishikawa, T., Todo, T., Tokutomi, S., and Kandori, H. (2004) Role of Gln1029 in the photoactivation processes of the LOV2 domain in Adiantum phytochrome3, Biochemistry 43, 8373-8379.
24. Harper, S. M., Neil, L. C., and Gardner, K. H. (2003) Structural basis of a phototropin light switch, Science 301, 1541-1544.
25. Laan, W., Gauden, M., Yeremenko, S., van Grondelle, R., Kennis, J. T. M., and Hellingwerf, K. J. (2006) On the mechanism of activation of the BLUF domain of AppA, Biochemistry 45, 51-60.
26. Newmyer, S. L., Sun, J., Loehr, T. M., and deMontellano, P. R. O. (1996) Rescue of the horseradish peroxidase His-170 → Ala mutant activity by imidazole: Importance of proximal ligand tethering, Biochemistry 35, 12788-12795.
27. Newmyer, S. L., and deMontellano, P. R. O. (1996) Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles, J. Biol. Chem. 271, 14891-14896.
28. a of the retinal Schiff base during the photocycle of bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 93, 1731-1734.
29. Ghanem, M., and Gadda, G. (2005) On the catalytic role of the conserved active site residue His(466) of choline oxidase, Biochemistry 44, 893-904.
30. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF chimera: A visualization system for exploratory research and analysis, J. Comput. Chem. 25, 1605-1612.
31. DeLano, W. L. (2002) PyMOL, DeLano Scientific, San Carlos, CA.
32. Petrek, M., Otyepka, M., Banas, P., Kosinova, P., Koca, J., and Damborsky, J. (2006) CAVER: A new tool to explore routes from protein clefts, pockets and cavities, BMC Bioinf. 7, 316.
33. Rudiger, W., and Briggs, W. R. (1995) Involvement of Thiol-Groups in Blue-Light-Induced Phosphorylation of a Plasma Membrane-Associated Protein from Coleoptile Tips of Zea-Mays L, Z. Naturforsch., C: J. Biosci. 50, 231-234.
34. 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.
35. Xie, A., Kelemen, L., Hendriks, J., White, B. J., Hellingwerf, K. J., and Hoff, W. D. (2001) Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation, Biochemistry 40, 1510-1517.
36. Genick, U. K., Soltis, S. M., Kuhn, P., Canestrelli, I. L., and Getzoff, E. D. (1998) Structure at 0.85 Å resolution of an early protein photocycle intermediate [see comments], Nature 392, 206-209.
37. Key, J., Hefti, M., Purcell, E. B., Moffat, K. (2007) Structure of the redox sensor domain of Azotobacter vinelandii NifL at atomic resolution: Signaling, dimerization and mechanism, Biochemistry, in press.
38. Corchnoy, S. B., Swartz, T. E., Lewis, J. W., Szundi, I., Briggs, W. R., and Bogomolni, R. A. (2003) Intramolecular proton transfers and structural changes during the photocycle of the LOV2 domain of phototropin 1, J. Biol. Chem. 278, 724-731.
39. Drossler, P., Holzer, W., Penzkofer, A., and Hegemann, P. (2002) pH dependence of the absorption and emission behaviour of riboflavin in aqueous solution, Chem. Phys. 282, 429-439.
40. Godavarti, R., Cooney, C. L., Langer, R., and Sasisekharan, R. (1996) Heparinase I from Flavobacterium heparinum. Identification of a critical histidine residue essential for catalysis as probed by chemical modification and site-directed mutagenesis, Biochemistry 35, 6846-6852.
41. Perrotta, A. T., Shih, I. H., and Been, M. D. (1999) Imidazole rescue of a cytosine mutation in a self-cleaving ribozyme, Science 286, 123-126.