Structure of the biliverdin cofactor in the Pfr state of bathy and prototypical phytochromes

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16800-16814

  Salewski, Johannes ^a   Escobar, Francisco Velazquez ^a   Kaminski, Steve ^a   Von Stetten, David ^a,b   Keidel, Anke ^a   Rippers, Yvonne ^a   Michael, Norbert ^a   Scheerer, Patrick ^c   Piwowarski, Patrick ^c   Bartl, Franz ^c   Frankenberg Dinkel, Nicole ^d   Ringsdorf, Simone ^e   Gar̈tner, Wolfgang ^e   Lamparter, Tilman ^f   Mroginski, Maria Andrea ^a   Hildebrandt, Peter ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^f KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL EQUILIBRIUM; COVALENT ATTACHMENT; CRYSTALLOGRAPHIC ANALYSIS; PSEUDOMONAS AERUGINOSA; STRUCTURAL DIFFERENCES; STRUCTURAL FLEXIBILITIES; THERMAL CONVERSION; THERMAL TRANSFORMATIONS;

CARBOXYLATION; PIGMENTS;

CHROMOPHORES;

BILIVERDIN; CARBONYL DERIVATIVE; CARBOXYLIC ACID; PHYTOCHROME; PHYTOCHROME FAR RED; PHYTOCHROME RED; TETRAPYRROLE DERIVATIVE; THIOL; UNCLASSIFIED DRUG; VINYL DERIVATIVE;

ARTICLE; CHROMATOPHORE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTALLOGRAPHY; HYDROGEN BOND; LINKAGE ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RAMAN SPECTROMETRY; REACTION ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; THERMODYNAMICS;

COMPUTER MODELING; INFRARED SPECTROSCOPY; PHOTORECEPTORS; PHYTOCHROME; QM/MM CALCULATIONS; RAMAN SPECTROSCOPY; RESONANCE RAMAN; SPECTROSCOPY;

BACTERIAL PROTEINS; BINDING SITES; PHYTOCHROME; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 84878763583     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.457531     Document Type: Article

References (71)

1. Briggs, W. R., and Spudich, J. L. (2005) Handbook of Photosensory Receptors, Wiley Verlag, Weinheim, Germany
2. Rockwell, N. C., and Lagarias, J. C. (2010) A brief history of phytochromes. Chemphyschem 11, 1172-1180
3. Kehoe, D. M., and Grossman, A. R. (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273, 1409-1412 (Pubitemid 26296533)
4. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gärtner, W., Wilde, A., and Börner, T. (1997) A prokaryotic phytochrome. Nature 386, 663
5. Wilde, A., Churin, Y., Schubert, H., and Börner, T. (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett. 406, 89-92 (Pubitemid 27156964)
6. Montgomery, B. L., and Lagarias, J. C. (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci. 7, 357-366 (Pubitemid 36726503)
7. Blumenstein, A., Vienken, K., Tasler, R., Purschwitz, J., Veith, D., Frankenberg- Dinkel, N., and Fischer, R. (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 15, 1833-1838 (Pubitemid 41501518)
8. Thümmler, F., Dufner, M., Kreisl, P., and Dittrich, P. (1992) Molecular cloning of a novel phytochrome gene of the moss ceratodon-purpureus which encodes a putative light-regulated protein kinase. Plant Mol. Biol. 20, 1003-1017
9. Yeh, K. C., Wu, S. H., Murphy, J. T., and Lagarias, J. C. (1997) A cyanobacterial phytochrome two-component light sensory system. Science 277, 1505-1508 (Pubitemid 27449238)
10. Yeh, K. C., and Lagarias, J. C. (1998) Eukaryotic phytochromes: Light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. U.S.A. 95, 13976-13981
11. Lamparter, T., Esteban, B., and Hughes, J. (2001) Phytochrome Cph1 from the cyanobacterium Synechocystis PCC6803-Purification, assembly, and quaternary structure. Eur. J. Biochem. 268, 4720-4730 (Pubitemid 34203420)
12. Hughes, J. (2010) Phytochrome three-dimensional structures and functions. Biochem. Soc. Trans. 38, 710-716
13. Essen, L. O., Mailliet, J., and Hughes, J. (2008) The structure of a complete phytochrome sensory module in the Pr ground state. Proc. Natl. Acad. Sci. U.S.A. 105, 14709-14714
14. Yang, X., Kuk, J., and Moffat, K. (2008) Crystal structure of Pseudomonas aeruginosa bacteriophyrochrome: Photoconversion and signal transduction. Proc. Natl. Acad. Sci. U.S.A. 105, 14715-14720
15. Yang, X., Kuk, J., and Moffat, K. (2009) Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome. Proc. Natl. Acad. Sci. U.S.A. 106, 15639-15644
16. Karniol, B., and Vierstra, R. D. (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc. Natl. Acad. Sci. U.S.A. 100, 2807-2812 (Pubitemid 36297580)
17. Scheerer, P., Michael, N., Park, J. H., Nagano, S., Choe, H. W., Inomata, K., Borucki, B., Krauss, N., and Lamparter, T. (2010) Light-induced conformational changes of the chromophore and the protein in phytochromes: bacterial phytochromes as model systems. Chemphyschem 11, 1090-1105
18. Wagner, J. R., Zhang, J., Brunzelle, J. S., Vierstra, R. D., and Forest, K. T. (2007) High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution. J. Biol. Chem. 282, 12298-12309 (Pubitemid 47100678)
19. Rottwinkel, G., Oberpichler, I., and Lamparter, T. (2010) Bathy phytochromes in Rhizobial soil bacteria. J. Bacteriol. 192, 5124-5133
20. Yang, X., Ren, Z., Kuk, J., and Moffat, K. (2011) Temperature-scan crystallography reveals reaction intermediates in bacteriophytochrome. Nature 479, 428-432
21. Lamparter, T., Michael, N., Mittmann, F., and Esteban, B. (2002) Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc. Natl. Acad. Sci. U.S.A. 99, 11628-11633 (Pubitemid 34994450)
22. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
23. Mroginski, M. A., von Stetten, D., Escobar, F. V., Strauss, H. M., Kaminski, S., Scheerer, P., Günther, M., Murgida, D. H., Schmieder, P., Bongards, C., Gärtner, W., Mailliet, J., Hughes, J., Essen, L. O., and Hildebrandt, P. (2009) Chromophore structure of cyanobacterial phytochrome Cph1 in the Pr state: reconciling structural and spectroscopic data by QM/MM calculations. Biophys. J. 96, 4153-4163
24. Yang, X., Stojkovic, E. A., Kuk, J., and Moffat, K. (2007) Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion. Proc. Natl. Acad. Sci. U.S.A. 104, 12571-12576 (Pubitemid 47206179)
25. von Stetten, D., Günther, M., Scheerer, P., Murgida, D. H., Mroginski, M. A., Krauss, N., Lamparter, T., Zhang, J., Anstrom, D. M., Vierstra, R. D., Forest, K. T., and Hildebrandt, P. (2008) Chromophore heterogeneity and photoconversion in phytochrome crystals and solution studied by resonance Raman spectroscopy. Angew. Chem. Int. Ed. 47, 4753-4755
26. Tasler, R., Moises, T., and Frankenberg-Dinkel, N. (2005) Biochemical and spectroscopic characterization of the bacterial phytochrome of Pseudomonas aeruginosa. FEBS J. 272, 1927-1936 (Pubitemid 40547249)
27. Inomata, K., Noack, S., Hammam, M. A., Khawn, H., Kinoshita, H., Murata, Y., Michael, N., Scheerer, P., Krauss, N., and Lamparter, T. (2006) Assembly of synthetic locked chromophores with Agrobacterium phytochromes Agp1 and Agp2. J. Biol. Chem. 281, 28162-28173 (Pubitemid 44414530)
28. Quest, B., Hübschmann, T., Sharda, S., Tandeau de Marsac, N., and Gärtner, W. (2007) Homologous expression of a bacterial phytochrome-The cyanobacterium Fremyella diplosiphon incorporates biliverdin as a genuine, functional chromophore. FEBS J. 274, 2088-2098 (Pubitemid 46588006)
29. Borucki, B., Seibeck, S., Heyn, M. P., and Lamparter, T. (2009) Characterization of the covalent and noncovalent adducts of Agp1 phytochrome assembled with biliverdin and phycocyanobilin by circular dichroism and flash photolysis. Biochemistry 48, 6305-6317
30. Sharda, S., Shah, R., and Gärtner, W. (2007) Domain interaction in cyanobacterial phytochromes as a prerequisite for spectral integrity. Eur. Biophys. J. 36, 815-821 (Pubitemid 350092522)
31. Borucki, B., von Stetten, D., Seibeck, S., Lamparter, T., Michael, N., Mroginski, M. A., Otto, H., Murgida, D. H., Heyn, M. P., and Hildebrandt, P. (2005) Light-induced proton release of phytochrome is coupled to the transient deprotonation of the tetrapyrrole chromophore. J. Biol. Chem. 280, 34358-34364 (Pubitemid 41443162)
32. von Stetten, D., Seibeck, S., Michael, N., Scheerer, P., Mroginski, M. A., Murgida, D. H., Krauss, N., Heyn, M. P., Hildebrandt, P., Borucki, B., and Lamparter, T. (2007) Highly conserved residues Asp-197 and His-250 in Agp1 phytochrome control the proton affinity of the chromophore and Pfr formation. J. Biol. Chem. 282, 2116-2123 (Pubitemid 47076728)
33. Manitto, P., and Monti, D. (1980) Reaction of biliverdins with thiobarbituric acid-novel fragmentation reaction of bilin-1,19(21H,24H)-diones. J. Chem. Soc. Chem. Comm. 178-180
34. Lindner, I., Knipp, B., Braslavsky, S. E., Gärtner, W., and Schaffner, K. (1998) A novel chromophore selectively modifies the spectral properties of one of the two stable states of the plant photoreceptor phytochrome. Angew. Chem. Int. Ed. 37, 1843-1846 (Pubitemid 28397782)
35. Murgida, D. H., von Stetten, D., Hildebrandt, P., Schwinté, P., Siebert, F., Sharda, S., Gärtner, W., and Mroginski, M. A. (2007) The chromophore structures of the Pr states in plant and bacterial phytochromes. Biophys. J. 93, 2410-2417 (Pubitemid 47511141)
36. Buchan, D. W., Ward, S. M., Lobley, A. E., Nugent, T. C., Bryson, K., and Jones, D. T. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res. 38, W563-W568
37. Jones, D. T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195-202
38. Brooks, B. R., Brooks, C. L., MacKerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: the biomolecular simulation program. J. Comp. Chem. 30, 1545-1614
39. Feller, S. E., Zhang, Y. H., Pastor, R. W., and Brooks, B. R. (1995) Constant-pressure molecular-dynamics simulation-the Langevin piston method. J. Chem. Phys. 103, 4613-4621
40. Martyna, G. J., Tobias, D. J., and Klein, M. L. (1994) Constant-pressure molecular dynamics algorithms. J. Chem. Phys. 101, 4177-4189
41. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comp. Chem. 26, 1781-1802 (Pubitemid 43078511)
42. MacKerell, A. D. Jr., Bashford, D., Bellott, M., Dunbrack, R. L. Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E. I., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz- Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (Pubitemid 128576688)
43. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald-an N. log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
44. Senn, H. M., and Thiel, W. (2007)QM/MMstudies of enzymes. Curr. Op. Chem. Biol. 11, 182-187
45. Becke, A. D. (1993) Density-functional thermochemistry. 3. The role of exact exchange. J. Chem. Phys. 98, 5648-5652
46. Sherwood, P., de Vries, A. H., Guest, M. F., Schreckenbach, G., Catlow, C. R. A., French, S. A., Sokol, A. A., Bromley, S. T., Thiel, W., Turner, A. J., Billeter, S., Terstegen, F., Thiel, S., Kendrick, J., Rogers, S. C., Casci, J., Watson, M., King, F., Karlsen, E., Sjøvoll, M., Fahmi, A., Schäfer, A., and Lennartz, Ch. (2003) QUASI: A general purpose implementation of the QM/MM approach and its application to problems in catalysis. J. Mol. Struct. (Theochem.) 632, 1-28
47. Mroginski, M. A., Mark, F., Thiel, W., and Hildebrandt, P. (2007) Quantum mechanics/molecular mechanics calculation of the Raman spectra of the phycocyanobilin chromophore in α-c-phycocyanin. Biophys. J. 93, 1885-1894 (Pubitemid 47437573)
48. Mroginski, M. A., Kaminski, S., von Stetten, D., Ringsdorf, S., Gärtner, W., Essen, L. O., and Hildebrandt, P. (2011) Structure of the chromophore binding pocket in the Pr state of plant phytochrome phyA. J. Phys. Chem. B 115, 1220-1231
49. Mroginski, M. A., Kaminski, S., and Hildebrandt, P. (2010) Raman spectra of the phycoviolobilin cofactor in phycoerythrocyanin calculated by QM/ MM. Chemphyschem 11, 1265-1274
50. Hildebrandt, P., Hoffmann, A., Lindemann, P., Heibel, G., Braslavsky, S. E., Schaffner, K., and Schrader, B. (1992) Fourier-transform resonance Raman-spectroscopy of phytochrome. Biochem. 31, 7957-7962
51. Fodor, S. P. A., Lagarias, J. C., and Mathies, R. A. (1990) Resonance Raman analysis of the Pr and Pfr forms of phytochrome. Biochem. 29, 11141-11146
52. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385 (Pubitemid 37442164)
53. Buckler, D. R., Zhou, Y., and Stock, A. M. (2002) Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermotoga maritima. Structure 10, 153-164 (Pubitemid 34164594)
54. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse- Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Cryst. D 54, 905-921
55. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
56. Hooft, R. W., Vriend, G., Sander, C., and Abola, E. E. (1996) Errors in protein structures. Nature 381, 272
57. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 486-501
58. Kneip, C., Hildebrandt, P., Schlamann, W., Braslavsky, S. E., Mark, F., and Schaffner, K. (1999) Protonation state and structural changes of the tetrapyrrole chromophore during the Pr → Pfr phototransformation of phytochrome. A resonance Raman spectroscopic study. Biochemistry 38, 15185-15192 (Pubitemid 129520349)
59. Mroginski, M. A., von Stetten, D., Kaminski, S., Velazquez Escobar, F., Michael, N., Daminelli-Widany, G., Hildebrandt, P. (2011) Elucidating photoinduced structural changes in phytochromes by the combined application of resonance Raman spectroscopy and theoretical methods. J. Mol. Struct. 993, 15-25
60. Rice, J. A. (2007) Mathematical Statistics and Data Analysis, 3 Ed., Thomson Books/Cole, Duxbury Press, Pacific Grove, CA
61. Schwinté, P., Foerstendorf, H., Hussain, Z., Gärtner, W., Mroginski, M. A., Hildebrandt, P., and Siebert, F. (2008) FTIR study of the photoinduced processes of plant phytochrome phyA using isotope-labeled bilins and density functional theory calculations. Biophys. J. 95, 1256-1267
62. Wagner, J. R., Zhang, J., von Stetten, D., Günther, M., Murgida, D. H., Mroginski, M. A., Walker, J. M., Forest, K. T., Hildebrandt, P., and Vierstra, R. D. (2008) Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes. J. Biol. Chem. 283, 12212-12226
63. Brandt, S., von Stetten, D., Günther, M., Hildebrandt, P., and Frankenberg- Dinkel, N. (2008) The fungal phytochrome FphA from Aspergillus nidulans. J. Biol. Chem. 283, 34605-34614
64. Song, C., Essen, L. O., Gärtner, W., Hughes, J., and Matysik, J. (2012) Solid-state NMR spectroscopic study of chromophore-protein interactions in the Pr ground state of plant phytochrome A. Mol. Plant 5, 698-715
65. Song, C., Rohmer, T., Tiersch, M., Zaanen, J., Hughes, J., Matysik, J. (2013) Solid state NMR spectroscopy to probe photoactivation in canonical phytochromes. Photochem. Photobiol. 89, 259-273
66. Freer, L., Kim, P. W., Corley, S. C., Rockwell, N. C., Zhao, L., Thibert, A. J., Lagarias, J. C., Larsen, D. S. (2012) Chemical inhomogeneity in the ultrafast dynamics of the DXCF cyanobacteriochrome Tlr0924. J. Phys. B, 116, 10571-10581
67. Chen, Y., Zhang, J., Luo, J., Tu, J. M., Zeng, X. L., Xie, J., Zhou, M., Zhao, J. Q., Scheer, H., Zhao, K. H. (2012) Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics. FEBS J. 279, 40-54
68. Schmidt, P., Gensch, T., Remberg, A., Gärtner, W., Braslavsky, S. E., Schaffner, K. (1998) The complexity of the Pr to Pfr phototransformation kinetics is an intrinsic property of native phytochrome. Photochem. Photobiol. 68, 754-761 (Pubitemid 128472307)
69. Kim, P. W., Freer, L. H., Rockwell, N. C., Martin, S. S., Lagarias, J. C., Larsen, D. S. (2012) Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 2. reverse dynamics. Biochemistry 51, 619-630
70. Rockwell, N. C., Shang, L., Martin, S. S., Lagarias, J. C (2009) Distinct classes of red/far-red photochemistry within the phytochrome superfamily. Proc. Natl. Acad. Sci. U.S.A. 106, 6123-6127
71. Song, C., Psakis, G., Lang, C., Mailliet, J., Gärtner, W., Hughes, J., Matysik, J. (2011) Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome. Proc. Natl. Acad. Sci. U.S.A. 108, 3842-3847