Dynamics of the amino-terminal and carboxyl-terminal helices of arabidopsis phototropin 1 LOV2 studied by the transient grating

Journal of Physical Chemistry B

Volumn 117, Issue 49, 2013, Pages 15606-15613

  Takeda, Kimitoshi ^a   Nakasone, Yusuke ^a   Zikihara, Kazunori ^b   Tokutomi, Satoru ^b   Terazima, Masahide ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; CARBOXYL-TERMINAL; CONFORMATIONAL CHANGE; LIGHT OXYGEN VOLTAGES; REACTION DYNAMICS; REGULATORY FUNCTIONS; TRANSIENT GRATING; UNFOLDING PROCESS;

PHYSICAL CHEMISTRY; PHYSICS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; PHOTOTROPIN;

ARABIDOPSIS; ARTICLE; CHEMISTRY; CIRCULAR DICHROISM; GENETICS; METABOLISM; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN UNFOLDING; TIME;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CIRCULAR DICHROISM; MUTATION; PHOTOTROPINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; TIME FACTORS;

EID: 84890016804     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp406109j     Document Type: Article

References (44)

1. Christie, J. M.; Swartz, T. E.; Bogomolni, R. A.; Briggs, W. R. Phototropin LOV Domains Exhibit Distinct Roles in Regulating Photoreceptor Function Plant. J. 2002, 32 (2) 205-219
2. Huala, E.; Oeller, P. W.; Liscum, E.; Han, I. S.; Larsen, E.; Briggs, W. R. Arabidopsis NPH1: A Protein Kinase with a Putative Redox-Sensing Domain Science 1997, 278 (5346) 2120-2123
3. Briggs, W. R.; Huala, E. Blue-Light Photoreceptors in Higher Plants Annu. Rev. Cell. Dev. Biol. 1999, 15, 33-62
4. Christie, J. M.; Reymond, P.; Powell, G. K.; Bernasconi, P.; Raibekas, A. A.; Liscum, E.; Briggs, W. R. Arabidopsis NPH1: A Flavoprotein with the Properties of a Photoreceptor for Phototropism Science 1998, 282 (5394) 1698-1701
5. Jarillo, J. A.; Gabrys, H.; Capel, J.; Alonso, J. M.; Ecker, J. R.; Cashmore, A. R. Phototropin-Related NPL1 Controls Chloroplast Relocation Induced by Blue Light Nature 2001, 410 (6831) 952-954
6. Kagawa, T.; Sakai, T.; Suetsugu, N.; Oikawa, K.; Ishiguro, S.; Kato, T.; Tabata, S.; Okada, K.; Wada, M. Arabidopsis NPL1: A Phototropin Homolog Controlling the Chloroplast High-Light Avoidance Response Science 2001, 291 (5511) 2138-2141
7. Kinoshita, T.; Doi, M.; Suetsugu, N.; Kagawa, T.; Wada, M.; Shimazaki, K. phot1 and phot2 Mediate Blue Light Regulation of Stomatal Opening Nature 2001, 414 (6864) 656-660
8. Tokutomi, S.; Matsuoka, D.; Zikihara, K. Molecular Structure and Regulation of Phototropin Kinase by Blue Light Biochim. Biophys. Acta. 2008, 1784, 133-142
9. Christie, J. M.; Salomon, M.; Nozue, K.; Wada, M.; Briggs, W. R. LOV (Light, Oxygen, or Voltage) Domains of the Blue-Light Photoreceptor Phototropin (nph1): Binding Sites for the Chromophore Flavin Mononucleotide Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (15) 8779-8783
10. Matsuoka, D.; Tokutomi, S. Blue Light-Regulated Molecular Switch of Ser/Thr Kinase in Phototropin Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (37) 13337-13342
11. Salomon, M.; Lempert, U.; Rudiger, W. Dimerization of the Plant Photoreceptor Phototropin Is Probably Mediated by the LOV1 Domain FEBS Lett. 2004, 572 (1-3) 8-10
12. Nakasako, M.; Zikihara, K.; Matsuoka, D.; Katsura, H.; Tokutomi, S. Structural Basis of the LOV1 Dimerization of Arabidopsis Phototropins 1 and 2 J. Mol. Biol. 2008, 381 (3) 718-733
13. Moglich, A.; Yang, X. J.; Ayers, R. A.; Moffat, K. Structure and Function of Plant Photoreceptors Ann. Rev. Plant. Biol. 2010, 61) 21-47
14. Herrou, J.; Crosson, S. Function, Structure and Mechanism of Bacterial Photosensory LOV Proteins Nat. Rev. Microbiol. 2011, 9 (10) 713-723
15. Harper, S. M.; Neil, L. C.; Gardner, K. H. Structural Basis of a Phototropin Light Switch Science 2003, 301 (5639) 1541-1544
16. Schuttrigkeit, T. A.; Kompa, C. K.; Salomon, M.; Rudiger, W.; Michel-Beyerle, M. E. Primary Photophysics of the FMN Binding LOV2 Domain of the Plant Blue Light Receptor Phototropin of Avena Sativa Chem. Phys. 2003, 294 (3) 501-508
17. Kennis, J. T. M.; Crosson, S.; Gauden, M.; van Stokkum, I. H. M.; Moffat, K.; van Grondelle, R. Primary Reactions of the LOV2 Domain of Phototropin, A Plant Blue-Light Photoreceptor Biochemistry 2003, 42 (12) 3385-3392
18. Schleicher, E.; Kowalczyk, R. M.; Kay, C. W. M.; Hegemann, P.; Bacher, A.; Fischer, M.; Bittl, R.; Richter, G.; Weber, S. On the Reaction Mechanism of Adduct Formation in LOV Domains of the Plant Blue-Light Receptor Phototropin J. Am. Chem. Soc. 2004, 126 (35) 11067-11076
19. Nakasone, Y.; Eitoku, T.; Matsuoka, D.; Tokutomi, S.; Terazima, M. Kinetic Measurement of Transient Dimerization and Dissociation Reactions of Arabidopsis Phototropin 1 LOV2 Domain Biophys. J. 2006, 91 (2) 645-653
20. Nakasone, Y.; Eitoku, T.; Matsuoka, D.; Tokutomi, S.; Terazima, M. Dynamics of Conformational Changes of Arabidopsis Phototropin 1 LOV2 with the Linker Domain J. Mol. Biol. 2007, 367 (2) 432-442
21. Eitoku, T.; Nakasone, Y.; Zikihara, K.; Matsuoka, D.; Tokutomi, S.; Terazima, M. Photochemical intermediates of Arabidopsis Phototropin 2 LOV Domains Associated with Conformational Changes J. Mol. Biol. 2007, 371 (5) 1290-1303
22. Alexandre, M. T. A.; van Grondelle, R.; Hellingwerf, K. J.; Kennis, J. T. M. Conformational Heterogeneity and Propagation of Structural Changes in the LOV2/J alpha Domain from Avena sativa Phototropin 1 as Recorded by Temperature-Dependent FTIR Spectroscopy Biophys. J. 2009, 97 (1) 238-247
23. Yamamoto, A.; Iwata, T.; Sato, Y.; Matsuoka, D.; Tokutomi, S.; Kandori, H. Light Signal Transduction Pathway from Flavin Chromophore to the J alpha Helix of Arabidopsis Phototropin1 Biophys. J. 2009, 96 (7) 2771-2778
24. Koyama, T.; Iwata, T.; Yamamoto, A.; Sato, Y.; Matsuoka, D.; Tokutomi, S.; Kandori, H. Different Role of the J alpha Helix in the Light-Induced Activation of the LOV2 Domains in Various Phototropins Biochemistry 2009, 48 (32) 7621-7628
25. Chen, E. F.; Swartz, T. E.; Bogomolni, R. A.; Kliger, D. S. A LOV Story: The Signaling State of the Phot1 LOV2 Photocycle Involves Chromophore-Triggered Protein Structure Relaxation, As Probed by Far-UV Time-Resolved Optical Rotatory Dispersion Spectroscopy Biochemistry 2007, 46 (15) 4619-4624
26. Zayner, J. P.; Antoniou, C.; Sosnick, T. R. The Amino-Terminal Helix Modulates Light-Activated Conformational Changes in AsLOV2 J. Mol. Biol. 2012, 419 (1-2) 61-74
27. Nash, A. I.; Ko, W. H.; Harper, S. M.; Gardner, K. H. A Conserved Glutamine Plays a Central Role in LOV Domain Signal Transmission and Its Duration Biochemistry 2008, 47 (52) 13842-13849
28. Harper, S. M.; Christie, J. M.; Gardner, K. H. Disruption of the LOV-J Alpha Helix Interaction Activates Phototropin Kinase Activity Biochemistry 2004, 43 (51) 16184-16192
29. Halavaty, A. S.; Moffat, K. 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 2007, 46 (49) 14001-14009
30. Aihara, Y.; Yamamoto, T.; Okajima, K.; Yamamoto, K.; Suzuki, T.; Tokutomi, S.; Tanaka, K.; Nagatani, A. Mutations in N-terminal Flanking Region of Blue Light-Sensing Light-Oxygen and Voltage 2 (LOV2) Domain Disrupt Its Repressive Activity on Kinase Domain in the Chlamydomonas Phototropin J. Biol. Chem. 2012, 287 (13) 9901-9909
31. Pfeifer, A.; Majerus, T.; Zikihara, K.; Matsuoka, D.; Tokutomi, S.; Heberle, J.; Kottke, T. Time-Resolved Fourier Transform Infrared Study on Photoadduct Formation and Secondary Structural Changes within the Phototropin LOV Domain Biophys. J. 2009, 96 (4) 1462-1470
32. Freddolino, P. L.; Gardner, K. H.; Schulten, K. Signaling mechanisms of LOV domains: new insights from molecular dynamics studies Photochem. Photobiol. Sci. 2013, 10.1039/c3pp25400c
33. Nada, T.; Terazima, M. A Novel Method for Study of Protein Folding Kinetics by Monitoring Diffusion Coefficient in Time Domain Biophys. J. 2003, 85 (3) 1876-1881
34. Nishida, S.; Nada, T.; Terazima, M. Kinetics of Intermolecular Interaction during Protein Folding of Reduced Cytochrome c Biophys. J. 2004, 87 (4) 2663-2675
35. Kelly, S. M.; Jess, T. J.; Price, N. C. How to Study Proteins by Circular Dichroism BBA Proteins Protein 2005, 1751 (2) 119-139
36. Buttani, V.; Losi, A.; Eggert, T.; Krauss, U.; Jaeger, K. E.; Cao, Z.; Gartner, W. Conformational Analysis of the Blue-Light Sensing Protein YtvA Reveals a Competitive Interface for LOV-LOV Dimerization and Interdomain Interactions Photochem. Photobiol. Sci. 2007, 6 (1) 41-49
37. Terazima, M. Photothermal Studies of Photophysical and Photochemical Processes by the Transient Grating Method Adv. Photochem. 1998, 24, 255-338
38. Terazima, M. Molecular volume and Enthalpy Changes Associated with Irreversible Photo-Reaction J. Photochem. Photobiol. C 2002, 3, 81-108
39. Terazima, M. Studies of Photo-Induced Protein Reactions by Spectrally Silent Reaction Dynamics Detection Methods: Applications to the Photoreaction of the LOV2 Domain of Phototropin from Arabidopsis Thaliana BBA Proteins Protein 2011, 1814 (8) 1093-1105
40. Hazra, P.; Inoue, K.; Laan, W.; Hellingwerf, K. J.; Terazima, M. Tetramer Formation Kinetics in the Signaling State of AppA Monitored by Time-Resolved Diffusion Biophys. J. 2006, 91 (2) 654-661
41. Terazima, M. Time-Dependent Intermolecular Interaction during Protein Reactions Phys. Chem. Chem. Phys. 2011, 13 (38) 16928-16940
42. Nakasako, M.; Iwata, T.; Matsuoka, D.; Tokutomi, S. Light-Induced Structural Changes of LOV Domain-Containing Polypeptides from Arabidopsis Phototropin 1 and 2 Studied by Small-Angle X-ray Scattering Biochemistry 2004, 43 (47) 14881-14890
43. Takayama, Y.; Nakasako, M.; Okajima, K.; Iwata, A.; Kashojiya, S.; Matsui, Y.; Tokutomi, S. Light-Induced Movement of the LOV2 Domain in an Asp720Asn Mutant LOV2-Kinase Fragment of Arabidopsis Phototropin 2 Biochemistry 2011, 50 (7) 1174-1183
44. Freddolino, P. L.; Dittrich, M.; Schulten, K. Dynamic Switching Mechanisms in LOV1 and LOV2 Domains of Plant Phototropins Biophys. J. 2006, 91 (10) 3630-3639