Blue light-induced conformational changes in a light-regulated transcription factor, aureochrome-1

Plant and Cell Physiology

Volumn 54, Issue 1, 2013, Pages 93-106

  Hisatomi, Osamu ^a   Takeuchi, Ken ^a   Zikihara, Kazunori ^b   Ookubo, Yuki ^b   Nakatani, Yoichi ^a   Takahashi, Fumio ^c   Tokutomi, Satoru ^b   Kataoka, Hironao ^d  

^a OSAKA UNIVERSITY   (Japan)

^b Osaka Prefecture University   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

Aureochrome; Blue light; bZIP; Conformational change; LOV; Vaucheria frigida

Indexed keywords

DNA BINDING PROTEIN; LEUCINE ZIPPER PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; GEL CHROMATOGRAPHY; GENETICS; LIGHT; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; RADIATION SCATTERING; STRAMENOPILE; ULTRAVIOLET SPECTROPHOTOMETRY;

CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; DNA-BINDING PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LEUCINE ZIPPERS; LIGHT; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SCATTERING, RADIATION; SPECTROPHOTOMETRY, ULTRAVIOLET; STRAMENOPILES;

ALGAE; VAUCHERIA FRIGIDA;

EID: 84872348427     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs160     Document Type: Article

References (55)

1. Avila-Pe'rez, M., Vreede, J., Tang, Y., Bende, O., Losi, A., Gärtner, W. et al. (2009) In vivo mutational analysis of YtvA from Bacillus subtilis: Mechanism of light activation of the general stress response. J. Biol. Chem. 284: 24958-24964
2. Christie, J.M. (2007) Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58: 21-45
3. Christie, J.M., Reymond, P., Powell, G.K., Bernasconi, P., Raibekas, A.A., Liscum, E. et al. (1998) Arabidopsis NPH1: A flavoprotein with the properties of a photoreceptor for phototropism. Science 282: 1698-1701
4. Christie, J.M., Swartz, T.E., Bogomolni, R.A. and Briggs, W.R. (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J. 32: 205-219
5. Christie, J.M., Yang, H., Richter, G.L., Sullivan, S., Thomson, C.E., Lin, J. et al. (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol. 9: E1001076
6. Ciaccio, N.A. and Laurence, J.A. (2009) Effects of disulfide bond formation and protein helicity on the aggregation of activating transcription factor 5. Mol. Pharm. 6: 1205-1215
7. 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
8. Crosson, S. and Moffat, K. (2001) Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction. Proc. Natl Acad. Sci. USA 98: 2995-3000
9. Crosson, S. and Moffat, K. (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14: 1067-1075
10. Crosson, S., Rajagopal, S. and Moffat, K. (2003) The LOV domain family: Photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42: 2-10
11. Djouani-Tahr, 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
12. Ellenberger, T.E., Brandl, C.J., Struhl, K. and Harrison, S.C. (1992) The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: Crystal structure of the protein-DNA complex. Cell 71: 1223-1237
13. 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
14. Fujii, Y., Shimizu, T., Toda, T., Yanagida, M. and Hakoshima, T. (2000) Structural basis for the diversity of DNA recognition by bZIP transcription factors. Nat. Struct. Biol. 7: 889-893
15. Goren, I., Tavor, E., Goldblum, A. and Honigman, A. (2001) Two cysteine residues in the DNA-binding domain of CREB control binding to CRE and CREB-mediated gene expression. J. Mol. Biol. 313: 695-709
16. Guo, H., Kottke, T., Hegemann, P. and Dick, B. (2005) The phot LOV2 domain and its interaction with LOV1. Biophys. J. 89: 402-412
17. Halavaty, A.S. and Moffat, K. (2007) N- and C-terminal flanking regions modulate light-induced signal transduction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry 46: 14001-14009
18. Harper, S.M., Neil, L.C., Day, I.J., Hore, P.J. and Gardner, K.H. (2004) Conformational changes in a photosensory LOV domain monitored by time-resolved NMR spectroscopy. J. Amer. Chem. Soc. 126: 3390-3391
19. Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R. and Kay, S.A. (2003) FKF1 is essential for photoperiodic-specific light signaling in Arabidopsis. Nature 426: 302-306
20. Ishikawa, M., Takahashi, F., Nozaki, H., Nagasato., C., Motomura, T. and Kataoka, H. (2009) Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes. Planta 230: 543-552
21. Iwata, T., Tokutomi, S and Kandori, H. (2002) Photoreaction of the cysteine S-H group in the LOV2 domain of Adiantum phytochrome3
22. J. Amer. Chem. Soc. 124: 11840-11841
23. Kagawa, T., Sakai, T., Suetsugu, N., Oikawa, K., Ishiguro, S., Kato, T. et al. (2001) Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141
24. Kasahara, M., Swartz, T.E., Olney, M.A., Onodera, A., Mochizuki, N., Fukuzawa, H. 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
25. Katsura, H., Zikihara, K., Okajima, K., Yoshihara, S. and Tokutomi, S. (2009) Oligomeric structure of LOV domains in Arabidopsis phototropin. FEBS Lett. 583: 526-530
26. Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M. and Shimazaki, K. (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414: 656-660
27. Kozuka, T., Kong, S.G., Doi, M., Shimazaki, K. and Nagatani, A. (2011) Tissue-autonomous promotion of palisade cell development by phototropin 2 in Arabidopsis. Plant Cell 23: 3684-3695
28. Lees, J.G., Miles, A.J., Wien, F. and Wallace, B.A. (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22: 1955-1962
29. 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
30. Losi, A., Ghiraldelli, E., Jansen, S. and Gärtner, W. (2005) Mutational effects on protein structural changes and interdomain interactions in the blue-light sensing LOV protein YtvA. Photochem. Photobiol. 81: 1145-1152
31. Malzahn, E., Ciprianidis, S., Ka'ldi, K., Schafmeier, T. and Brunner, M. (2010) Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142: 762-772
32. Mitra, D., Yang, X. and Moffat, K. (2012) Crystal structures of aureochrome1 LOV suggest new design strategies for optogenetics. Structure 20: 698-706
33. Möglich, A. and Moffat, K. (2007) Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J. Mol. Biol. 373: 112-126
34. Nakasako, M., Iwata, T., Matsuoka, D. and Tokutomi, S. (2004) Light-induced structural changes of LOV domain-containing polypeptides from Arabidopsis phototropin 1 and 2 studied by small-angle X-ray scattering. Biochemistry 43: 14881-14890
35. Nakasako, M., Zikihara, K., Matsuoka, D., Katsura, H. and Tokutomi, S. (2008) Structural basis of the LOV1 dimerization of Arabidopsis phototropins 1 and 2. J. Mol. Biol. 381: 718-733
36. Nash, A.I., McNulty, R., Shillito, M.E., Swartz, T.E., Bogomolni, R.A., Luecke, H. et al. (2011) Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein. Proc. Natl Acad. Sci. USA 108: 9449-9454
37. Okajima, K., Matsuoka, D. and Tokutomi, S. (2011) LOV2-linker-kinase phosphorylates LOV1-containing N-terminal polypeptide substrate via photoreaction of LOV2 in Arabidopsis phototropin1. FEBS Lett. 585: 3391-3395
38. Patel, T.R., Reuten, R., Xiong, S., Meier, M., Winzor, D.J., Koch, M. et al. (2012) Determination of a molecular shape for netrin-4 from hydrodynamic and small angle X-ray scattering measurements. Matrix Biol. 31: 135-140
39. Purcell, E.B., Siegal-Gaskins, D., Rawling, D.C., Fiebig, A. and Crosson, S. (2007) A photosensory two-component system regulates bacterial cell attachment. Proc. Natl Acad. Sci. USA 104: 18241-18246
40. 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. Amer. Chem. Soc. 133: 5346-5356
41. Rinaldi, J., Gallo, M., Klinke, S., Paris, G., Bonomi, H.R., Bogomolni, R.A. et al. (2012) The b-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
42. Salomon, M., Christie, J.M., Kneib, 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
43. Salomon, M., Lempert, U. and Rüdiger, W. (2004) Dimerization of the plant photoreceptor phototropin is probably mediated by the LOV1 domain. FEBS Lett. 572: 8-10
44. Sreerama, N. and Woody, R.W. (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set. Anal. Biochem. 287: 252-260
45. Swartz, T.E., Corchnoy, S.B., Christie, J.M., Lewis, J.W., Szundi, I., Briggs, W.R. et al. (2001) The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J. Biol. Chem. 276: 36493-36500
46. Swartz, T.E., Tseng, T., Frederickson, M.A., Paris, G., Comerci, D.J., Rajashekara, G. et al. (2007) Blue-light-activated histidine kinases: Two-component sensors in bacteria. Science 317: 1090-1093
47. 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
48. Takahashi, F., Yamagata, D., Ishikawa, M., Fukamatsu, Y., Ogura, Y., Kasahara, M. et al. (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc. Natl Acad. Sci. USA 104: 19625-19630
49. Toyooka, T., Hisatomi, O., Takahashi, F., Kataoka, H. and Terazima, M. (2011) Photoreactions of Aureochrome-1. Biophys. J. 100: 2801-2809
50. Wyatt, A.R., Yerbury, J.J. and Wilson, M.R. (2009) Structural characterization of clusterin-chaperone client protein complexes. J. Biol. Chem. 284: 21920-21927
51. Whitmore, L. and Wallace, B.A. (2004) DICHROWEB: An online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32: W668-W673
52. Williams, S.C., Cantwell, C.A. and Johnson, P.F. (1991) A family of C/ EBP-related proteins capable of forming covalently linked leucine zipper dimers in vitro. Genes Dev. 5: 1553-1567
53. Yang, L. and Schepartz, A. (2005) Relationship between folding and function in a sequence-specific miniature DNA-binding protein. Biochemistry 44: 7469-7478
54. Zikihara, K., Iwata, T., Matsuoka, D., Kandori, H., Todo, T. and Tokutomi, S. (2006) Photoreaction cycle of the light, oxygen, and voltage domain in FKF1 determined by low-temperature absorption spectroscopy. Biochemistry 45: 10828-10837
55. Zoltowski, B.D., Nash, A.I. and Gardner, K.H. (2011) Variations in protein- flavin hydrogen bonding in a light, oxygen, voltage domain produce non-Arrhenius kinetics of adduct decay. Biochemistry 50: 8771-8779