Time-resolved fourier transform infrared study on photoadduct formation and secondary structural changes within the phototropin LOV domain

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1462-1470

  Pfeifer, Anna ^a   Majerus, Teresa ^b   Zikihara, Kazunori ^c   Matsuoka, Daisuke ^d   Tokutomi, Satoru ^c   Heberle, Joachim ^a   Kottke, Tilman ^a,b  

^a BIELEFELD UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c Osaka Prefecture University   (Japan)

^d KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPROTEIN; ARABIDOPSIS PROTEIN; FLAVINE MONONUCLEOTIDE; PHOTOTROPIN; UNCLASSIFIED DRUG; CRYPTOCHROME; CYSTEINE; FLAVOPROTEIN;

ARABIDOPSIS; ARTICLE; BETA SHEET; COVALENT BOND; FOLLOW UP; GENE MUTATION; INFRARED SPECTROSCOPY; LIGHT OXYGEN VOLTAGE SENSITIVE DOMAIN; NONHUMAN; PHOTORECEPTOR; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SIGNAL TRANSDUCTION; TIME RESOLVED FOURIER TRANSFORM INFRARED SPECTROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; KINETICS; LASER; LIGHT; MUTATION; PROTEIN TERTIARY STRUCTURE;

ARABIDOPSIS;

ARABIDOPSIS; CYSTEINE; FLAVOPROTEINS; KINETICS; LASERS; LIGHT; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 62649115085     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.016     Document Type: Article

References (44)

1. Christie, J. M. 2007. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58:21-45. (Pubitemid 46986316)
2. Huang, K., and C. F. Beck. 2003. Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA. 100:6269-6274. (Pubitemid 36576965)
3. Huala, E., P. W. Oeller, E. Liscum, I. S. Han, E. Larsen, et al. 1997. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science. 278:2120-2123.
4. Harper, S. M., L. C. Neil, and K. H. Gardner. 2003. Structural basis of a phototropin light switch. Science. 301:1541-1544. (Pubitemid 37128547)
5. Kennis, J. T., S. Crosson, M. Gauden, I. H. van Stokkum, K. Moffat, et al. 2003. Primary reactions of the LOV2 domain of phototropin, a plant blue-light photoreceptor. Biochemistry. 42:3385-3392.
6. Swartz, T. E., S. B. Corchnoy, J. M. Christie, J. W. Lewis, I. Szundi, et al. 2001. The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J. Biol. Chem. 276:36493-36500.
7. Crosson, S., and K. Moffat. 2001. Structure of a flavin-binding plant photoreceptor domain: insights into light-mediated signal transduction. Proc. Natl. Acad. Sci. USA. 98:2995-3000.
8. Salomon, M., J. M. Christie, E. Knieb, U. Lempert, and W. R. Briggs. 2000. Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry. 39:9401-9410.
9. Schleicher, E., R. M. Kowalczyk, C. W. Kay, P. Hegemann, A. Bacher, et al. 2004. On the reaction mechanism of adduct formation in LOV domains of the plant blue-light receptor phototropin. J. Am. Chem. Soc. 126:11067-11076.
10. Zikihara, K., T. Iwata, D. Matsuoka, H. Kandori, T. Todo, et al. 2006. Photoreaction cycle of the light, oxygen, and voltage domain in FKF1 determined by low-temperature absorption spectroscopy. Biochemistry. 45:10828-10837.
11. Christie, J. M., P. Reymond, G. K. Powell, P. Bernasconi, A. A. Raibekas, et al. 1998. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science. 282:1698-1701.
12. Harper, S. M., J. M. Christie, and K. H. Gardner. 2004. Disruption of the LOV-Jα helix interaction activates phototropin kinase activity. Biochemistry. 43:16184-16192.
13. Crosson, S., and K. Moffat. 2002. Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell. 14:1067-1075. (Pubitemid 34609217)
14. Nozaki, D., T. Iwata, T. Ishikawa, T. Todo, S. Tokutomi, et al. 2004. Role of Gln1029 in the photoactivation processes of the LOV2 domain in Adiantum phytochrome3. Biochemistry. 43:8373-8379.
15. Fedorov, R., I. Schlichting, E. Hartmann, T. Domratcheva, M. Fuhrmann, et al. 2003. Crystal structures and molecular mechanism of a light-induced signaling switch: the Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys. J. 84:2474-2482.
16. Eitoku, T., Y. Nakasone, D. Matsuoka, S. Tokutomi, and M. Terazima. 2005. Conformational dynamics of phototropin 2 LOV2 domain with the linker upon photoexcitation. J. Am. Chem. Soc. 127:13238-13244. (Pubitemid 41377616)
17. Corchnoy, S. B., T. E. Swartz, J. W. Lewis, I. Szundi, W. R. Briggs, et al. 2003. Intramolecular proton transfers and structural changes during the photocycle of the LOV2 domain of phototropin 1. J. Biol. Chem. 278:724-731.
18. Nakasako, M., T. Iwata, D. Matsuoka, and S. Tokutomi. 2004. Lightinduced structural changes of LOV domain-containing polypeptides from Arabidopsis phototropin 1 and 2 studied by small-angle x-ray scattering. Biochemistry. 43:14881-14890. (Pubitemid 39587464)
19. Chen, E., T. E. Swartz, R. A. Bogomolni, and D. S. Kliger. 2007. 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. 46:4619-4624.
20. Nakasone, Y., T. Eitoku, D. Matsuoka, S. Tokutomi, and M. Terazima. 2007. Dynamics of conformational changes of Arabidopsis phototropin 1 LOV2 with the linker domain. J. Mol. Biol. 367:432-442. (Pubitemid 46295433)
21. Iwata, T., D. Nozaki, S. Tokutomi, T. Kagawa, M. Wada, et al. 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.
22. Barth, A., and C. Zscherp. 2002. What vibrations tell us about proteins. Q. Rev. Biophys. 35:369-430. (Pubitemid 36207229)
23. Krimm, S., and J. Bandekar. 1986. Vibrational spectroscopy and conformations of peptides, polypeptides, and proteins. Adv. Protein Chem. 38:181-364.
24. Chizhov, I., D. S. Chernavskii, M. Engelhard, K. H. Mueller, B. V. Zubov, et al. 1996. Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys. J. 71:2329-2345.
25. Hendler, R. W., and R. I. Shrager. 1994. Deconvolutions based on singular value decomposition and the pseudoinverse: a guide for beginners. J. Biochem. Biophys. Methods. 28:1-33.
26. Kasahara, M., T. E. Swartz, M. A. Olney, A. Onodera, N. Mochizuki, et al. 2002. Photochemical properties of the flavin mononucleotidebinding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii. Plant Physiol. 129:762-773.
27. Losi, A., E. Polverini, B. Quest, and W. Gärtner. 2002. First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys. J. 82:2627-2634. (Pubitemid 34441300)
28. Uhmann, W., A. Becker, C. Taran, and F. Siebert. 1991. Time-resolved FTIR absorption spectroscopy using a step-scan interferometer. Appl. Spectrosc. 45:390-397.
29. Christie, J. M., S. B. Corchnoy, T. E. Swartz, M. Hokenson, I. S. Han, et al. 2007. Steric interactions stabilize the signaling state of the LOV2 domain of phototropin 1. Biochemistry. 46:9310-9319.
30. Ataka, K., P. Hegemann, and J. Heberle. 2003. Vibrational spectroscopy of an algal Phot-LOV1 domain probes the molecular changes associated with blue-light reception. Biophys. J. 84:466-474. (Pubitemid 36026414)
31. Bednarz, T., A. Losi, W. Gärtner, P. Hegemann, and J. Heberle. 2004. Functional variations among LOV domains as revealed by FTIR difference spectroscopy. Photochem. Photobiol. Sci. 3:575-579. (Pubitemid 38968070)
32. Swartz, T. E., P. J. Wenzel, S. B. Corchnoy, W. R. Briggs, and R. A. Bogomolni. 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. (Pubitemid 34602433)
33. Alexandre, M. T., J. C. Arents, R. van Grondelle, K. J. Hellingwerf, and J. T. Kennis. 2007. A base-catalyzed mechanism for dark state recovery in the Avena sativa phototropin-1 LOV2 domain. Biochemistry. 46:3129-3137. (Pubitemid 46449135)
34. Sato, Y., T. Iwata, S. Tokutomi, and H. Kandori. 2005. Reactive cysteine is protonated in the triplet excited state of the LOV2 domain in Adiantum phytochrome3. J. Am. Chem. Soc. 127:1088-1089. (Pubitemid 40228668)
35. Martin, C. B., M. L. Tsao, C. M. Hadad, and M. S. Platz. 2002. The reaction of triplet flavin with indole. A study of the cascade of reactive intermediates using density functional theory and time resolved infrared spectroscopy. J. Am. Chem. Soc. 124:7226-7234.
36. Richard, J. P., G. Williams, and J. L. Gao. 1999. Experimental and computational determination of the effect of the cyano group on carbon acidity in water. J. Am. Chem. Soc. 121:715-726. (Pubitemid 129506205)
37. Kottke, T., J. Heberle, D. Hehn, B. Dick, and P. Hegemann. 2003. Phot- LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. Biophys. J. 84:1192-1201.
38. Iwata, T., D. Nozaki, Y. Sato, K. Sato, Y. Nishina, et al. 2006. Identification of the C=O stretching vibrations of FMN and peptide backbone by (13)C-labeling of the LOV2 domain of Adiantum phytochrome3. Biochemistry. 45:15384-15391.
39. Majerus, T., T. Kottke, W. Laan, K. Hellingwerf, and J. Heberle. 2007. Time-resolved FTIR spectroscopy traces signal relay within the bluelight receptor AppA. Chem. Phys. Chem. 8:1787-1789.
40. Crosson, S., S. Rajagopal, and K. Moffat. 2003. The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry. 42:2-10.
41. Kay, C. W., E. Schleicher, A. Kuppig, H. Hofner, W. Rüdiger, et al. 2003. Blue light perception in plants. Detection and characterization of a light-induced neutral flavin radical in a C450A mutant of phototropin. J. Biol. Chem. 278:10973-10982.
42. Hienerwadel, R., A. Boussac, J. Breton, B. A. Diner, and C. Berthomieu. 1997. Fourier transform infrared difference spectroscopy of photosystem II tyrosine D using site-directed mutagenesis and specific isotope labeling. Biochemistry. 36:14712-14723. (Pubitemid 27524392)
43. Imamoto, Y., M. Kataoka, and F. Tokunaga. 1996. Photoreaction cycle of photoactive yellow protein from Ectothiorhodospira halophila studied by low-temperature spectroscopy. Biochemistry. 35:14047-14053. (Pubitemid 26384399)
44. Eitoku, T., Y. Nakasone, K. Zikihara, D. Matsuoka, S. Tokutomi, et al. 2007. Photochemical intermediates of Arabidopsis phototropin 2 LOV domains associated with conformational changes. J. Mol. Biol. 371:1290-1303.