Blue light induces global and localized conformational changes in the kinase domain of full-length phototropin

Biochemistry

Volumn 49, Issue 5, 2010, Pages 1024-1032

  Pfeifer, Anna ^a   Mathes, Tilo ^b   Lu, Yinghong ^b,d   Hegemann, Peter ^b   Kottke, Tilman ^a,c  

^a BIELEFELD UNIVERSITY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BLUE LIGHT; BLUE-LIGHT PHOTORECEPTORS; CHLAMYDOMONAS REINHARDTII; CONFORMATIONAL CHANGE; DELETION MUTANTS; FLAVIN CHROMOPHORES; FULL-LENGTH PROTEINS; GREEN ALGA; HELICITIES; IN-PLANTS; INDUCED LOSS; KINASE ACTIVATION; KINASE DOMAINS; LIGHT STIMULI; PHOTOTROPINS; SIGNALING PROCESS; STRUCTURAL CHANGE; STRUCTURAL RESPONSE; TERTIARY STRUCTURES; TURN STRUCTURE;

AMINO ACIDS; CHEMICAL ACTIVATION; CHROMOPHORES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; ORGANIC ACIDS; OXYGEN;

PROTEINS;

AMINO ACID; PHOSPHOTRANSFERASE; PHOTOTROPIN; PIGMENT; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BLUE LIGHT; CHLAMYDOMONAS REINHARDTII; CONFORMATIONAL TRANSITION; DELETION MUTANT; ENZYME STRUCTURE; INFRARED SPECTROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTON TRANSPORT;

ALGAL PROTEINS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; CHLAMYDOMONAS REINHARDTII; LIGHT; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOTOTROPINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 75749099373     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9016044     Document Type: Article

References (57)

1. Liscum, E., and Briggs, W. R. (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell 7, 473-485.
2. Sakai, T., Kagawa, T., Kasahara, M., Swartz, T. E., Christie, J. M., Briggs, W. R., Wada, M., and Okada, K. (2001) Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl. Acad. Sci. U.S.A. 98, 6969-6974.
3. Kagawa, T., Sakai, T., Suetsugu, N., Oikawa, K., Ishiguro, S., Kato, T., Tabata, S., Okada, K., and Wada, M. (2001) Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138-2141.
4. Jarillo, J. A., Gabrys, H., Capel, J., Alonso, J. M., Ecker, J. R., and Cashmore, A. R. (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410, 952-954.
5. 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.
6. Folta, K. M., and Spalding, E. P. (2001) Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J. 26, 471-478.
7. Ohgishi, M., Saji, K., Okada, K., and Sakai, T. (2004) Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 2223-2228.
8. Huang, K., and Beck, C. F. (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. U.S.A. 100, 6269-6274.
9. Ermilova, E. V., Zalutskaya, Z. M., Huang, K. Y., and Beck, C. F. (2004) Phototropin plays a crucial role in controlling changes in chemotaxis during the initial phase of the sexual life cycle in Chlamydomonas. Planta 219, 420-427.
10. Onodera, A., Kong, S. G., Doi, M., Shimazaki, K., Christie, J., Mochizuki, N., and Nagatani, A. (2005) Phototropin from Chlamydomonas reinhardtii is functional in Arabidopsis thaliana. Plant Cell Physiol. 46, 367-374.
11. Tokutomi, S., Matsuoka, D., and Zikihara, K. (2008) Molecular structure and regulation of phototropin kinase by blue light. Biochim. Biophys. Acta 1784, 133-142.
12. Zegzouti, H., Li, W., Lorenz, T. C., Xie, M., Payne, C. T., Smith, K., Glenny, S., Payne, G. S., and Christensen, S. K. (2006) Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J. Biol. Chem. 281, 35520-35530.
13. Christie, J. M. (2007) Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21-45.
14. Hanks, S. K., and Hunter, T. (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596.
15. Bichsel, S. J., Tamaskovic, R., Stegert, M. R., and Hemmings, B. A. (2004) Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J. Biol. Chem. 279, 35228-35235.
16. 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.
17. 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.
18. 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.
19. Harper, S. M., Neil, L. C., and Gardner, K. H. (2003) Structural basis of a phototropin light switch. Science 301, 1541-1544.
20. Nakasone, Y., Eitoku, T., Matsuoka, D., Tokutomi, S., and Terazima, M. (2007) Dynamics of conformational changes of Arabidopsis phototropin 1 LOV2 with the linker domain. J. Mol. Biol. 367, 432-442.
21. Alexandre, M. T., van Grondelle, R., Hellingwerf, K. J., and Kennis, J. T. (2009) Conformational heterogeneity and propagation of structural changes in the LOV2/Jα domain from Avena sativa phototropin 1 as recorded by temperature-dependent FTIR spectroscopy. Biophys. J. 97, 238-247.
22. Yamamoto, A., Iwata, T., Sato, Y., Matsuoka, D., Tokutomi, S., and Kandori, H. (2009) Light signal transduction pathway from flavin chromophore to the Jα helix of Arabidopsis phototropin1. Biophys. J. 96, 2771-2778.
23. Koyama, T., Iwata, T., Yamamoto, A., Sato, Y., Matsuoka, D., Tokutomi, S., and Kandori, H. (2009) Different role of the Jα helix in the light-induced activation of the LOV2 domains in various phototropins. Biochemistry 48, 7621-7628.
24. 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.
25. 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.
26. Harper, S. M., Christie, J. M., and Gardner, K. H. (2004) Disruption of the LOV-Jα helix interaction activates phototropin kinase activity. Biochemistry 43, 16184-16192.
27. Matsuoka, D., and Tokutomi, S. (2005) Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc. Natl. Acad. Sci. U.S.A. 102, 13337-13342.
28. Kong, S. G., Kinoshita, T., Shimazaki, K., Mochizuki, N., Suzuki, T., and Nagatani, A. (2007) The C-terminal kinase fragment of Arabidopsis phototropin 2 triggers constitutive phototropin responses. Plant J. 51, 862-873.
29. Im, C. S., Eberhard, S., Huang, K., Beck, C. F., and Grossman, A. R. (2006) Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J. 48, 1-16.
30. Inoue, S., Kinoshita, T., Matsumoto, M., Nakayama, K. I., Doi, M., and Shimazaki, K. (2008) Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 5626-5631.
31. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430.
32. Krimm, S., and Bandekar, J. (1986) Vibrational spectroscopy and conformations of peptides, polypeptides, and proteins. Adv. Protein Chem. 38, 181-364.
33. Ataka, K., Hegemann, P., and Heberle, J. (2003) Vibrational Spectroscopy of an Algal Phot-LOV1 Domain Probes the Molecular Changes Associated with Blue-Light Reception. Biophys. J. 84, 466-474.
34. 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.
35. 13C-Labeling of the LOV2 Domain of Adiantum Phytochrome3. Biochemistry 45, 15384-15391.
36. Pfeifer, A., Majerus, T., Zikihara, K., Matsuoka, D., Tokutomi, S., Heberle, J., and Kottke, T. (2009) Time-resolved Fourier transform infrared study on photoadduct formation and secondary structural changes within the phototropin LOV domain. Biophys. J. 96, 1462-1470.
37. 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.
38. 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.
39. Bednarz, T., Losi, A., Gärtner, W., Hegemann, P., and Heberle, J. (2004) Functional variations among LOV domains as revealed by FT-IR difference spectroscopy. Photochem. Photobiol. Sci. 3, 575-579.
40. 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.
41. Guo, H., Kottke, T., Hegemann, P., and Dick, B. (2005) The phot LOV2 domain and its interaction with LOV1. Biophys. J. 89, 402-412.
42. Macheroux, P. (1999) UV-visible spectroscopy as a tool to study flavoproteins. Methods Mol. Biol. 131, 1-7.
43. Iwata, T., Yamamoto, A., Tokutomi, S., and Kandori, H. (2007) Hydration and temperature similarly affect light-induced protein structural changes in the chromophoric domain of phototropin. Biochemistry 46, 7016-7021.
44. 2O) solutions. III. Estimation of the protein secondary structure. Biopolymers 30, 1273-1280.
45. de Jongh, H. H., Goormaghtigh, E., and Ruysschaert, J. M. (1996) The different molar absorptivities of the secondary structure types in the amide I region: An attenuated total reflection infrared study on globular proteins. Anal. Biochem. 242, 95-103.
46. Akamine, P., Madhusudan,Wu, J., Xuong, N.H., Ten Eyck, L. F., and Taylor, S. S. (2003)Dynamic features of cAMP-dependent protein kinase revealed by apoenzyme crystal structure. J. Mol. Biol. 327, 159-171.
47. Zheng, J., Trafny, E. A., Knighton, D. R., Xuong, N. H., Taylor, S. S., Ten Eyck, L. F., and Sowadski, J. M. (1993) 2.2 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallogr. D49, 362-365.
48. Masterson, L. R., Mascioni, A., Traaseth, N. J., Taylor, S. S., and Veglia, G. (2008) Allosteric cooperativity in protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 105, 506-511.
49. Amezcua, C. A., Harper, S. M., Rutter, J., and Gardner, K. H. (2002) Structure and interactions of PAS kinase N-terminal PAS domain: Model for intramolecular kinase regulation. Structure 10, 1349-1361.
50. 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.
51. 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.
52. Johnson, D. A., Akamine, P., Radzio-Andzelm, E., Madhusudan, M., and Taylor, S. S. (2001) Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101, 2243-2270.
53. Subramaniam, S. (1998) The Biology Workbench: A seamless database and analysis environment for the biologist. Proteins 32, 1-2.
54. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases: Controlling activity through activation segment conformation. Mol. Cell 15, 661-675.
55. Jauch, R., Jakel, S., Netter, C., Schreiter, K., Aicher, B., Jackle, H., and Wahl, M. C. (2005) Crystal structures of the Mnk2 kinase domain reveal an inhibitory conformation and a zinc binding site. Structure 13, 1559-1568.
56. Söding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248.
57. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.