Effect of salt and pH on the activation of photoactive yellow protein and gateway mutants Y98Q and Y98F

Biochemistry

Volumn 44, Issue 42, 2005, Pages 13650-13663

  Borucki, Berthold ^a   Kyndt, John A ^b   Joshi, Chandra P ^a   Otto, Harald ^a   Meyer, Terry E ^b   Cusanovich, Michael A ^b   Heyn, Maarten P ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCENTRATION (PROCESS); HYDROPHOBICITY; ISOMERS; MUTAGENESIS; PH EFFECTS; SODIUM CHLORIDE;

DEPROTONATED CHROMOPHORES; PHOTOCYCLES; SALT BRIDGE; YELLOW PROTEINS;

PROTEINS;

GLUTAMINE; INORGANIC SALT; ION; PHENYLALANINE; PHOTOACTIVE YELLOW PROTEIN; POTASSIUM CHLORIDE; TYROSINE;

ACIDITY; ALKALINITY; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATOPHORE; CONFORMATIONAL TRANSITION; HALORHODOSPIRA HALOPHILA; HYDROPHOBICITY; KINETICS; NONHUMAN; PHOTOREACTIVITY; PKA; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTON TRANSPORT; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; HALORHODOSPIRA HALOPHILA; HYDROGEN-ION CONCENTRATION; MUTATION; PHOTOCHEMISTRY; PHOTORECEPTORS, MICROBIAL; SALTS;

HALORHODOSPIRA HALOPHILA;

EID: 27144534241     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050991z     Document Type: Article

References (58)

1. Meyer, T. E. (1985) Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila, Biochim. Biophys. Acta 806, 175-183.
2. Meyer T. E., Yakali, E., Cusanovich, M. A., and Tollin, G. (1987) Properties of a water-soluble, yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin, Biochemistry 26, 418-423.
3. Kyndt, J. A., Meyer, T. E., and Cusanovich, M. A. (2004) Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria, Photochem. Photobiol. Sci. 3, 519-530.
4. Jiang, Z. Y., Swem, L. R., Rushing, B. G., Devanathan, S., Tollin, G., and Bauer, C. E. (1999) Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes, Science 285, 406-409.
5. Kyndt, J. A., Fitch, J. C., Meyer, T. E., and Cusanovich, M. A. (2005) Thermochromatium tepidum photoactive yellow protein/bacteriophytochrome/ diguanylate cyclase (Ppd): characterization of the PYP domain, Biochemistry 44, 4755-4764.
6. Cusanovich, M. A., and Meyer, T. E. (2003) Photoactive yellow protein: A prototypic PAS domain sensory protein and development of a common signaling mechanism, Biochemistry 42, 4759-4770.
7. Taylor, B. L., and Zhulin, I. B. (1999) PAS domains: Internal sensors of oxygen, redox potential, and light, Microbiol. Mol. Rev. 63, 479-506.
8. Hellingwerf, K. J., Hendriks, J., and Gensch, T. (2003) Photoactive yellow protein, a new type of photoreceptor protein: Will this "yellow lab" bring us where we want to go? J. Phys. Chem. A 107, 1082-1094.
9. Borgstahl, G. E. O., Williams, D. R., and Getzoff, E. D. (1995) 1.4 Angstrom structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active-site, and chromophore, Biochemistry 34, 6278-6287.
10. Genick, U. K., Borgstahl, G. E. O., Ng, K., Ren, Z., Pradervand, C., Burke, P. M., Srajer, V., Teng, T. Y., Schildkamp, W., McRee, D. E., Moffat, K., and Getzoff, E. D. (1997) Structure of a protein photocycle intermediate by millisecond time-resolved crystallography, Science 275, 1471-1475.
11. Rajagopal, S., Anderson, S., Srajer, V., Schmidt, M., Pahl, R., and Moffat, K. (2005) A structural pathway for signaling in the E46Q mutant of photoactive yellow protein, Structure 13, 55-63.
12. Unno, M., Kumauchi, M., Sasaki, J., Tokunaga, F., and Yamauchi, S. (2000) Evidence for a protonated and cis configuration chromophore in the photobleached intermediate of photoactive yellow protein, J. Am. Chem. Soc. 122, 4233-4234.
13. Ujj, L., Devanathan, S., Meyer, T. E., Cusanovich, M. A., Tollin, G., and Atkinson, G. H. (1998) New photocycle intermediate in the photoactive yellow protein from Ectorhodospira halophila: picosecond transient absorption spectroscopy, Biophys. J. 75, 406-412.
14. Xie, A. H., Kelemen, L., Hendriks, J., White, B. J., Hellingwerf, K. J., and Hoff, W. (2001) Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation, Biochemistry 40, 1510-1517.
15. Borucki, B., Devanathan, S., Otto, H., Cusanovich, M. A., Tollin, G., and Heyn, M. P. (2002) Kinetics of proton uptake and dye binding by photoactive yellow protein in wild type and in the E46Q and E46A mutants, Biochemistry 41, 10026-10037.
16. Meyer, T. E., Tollin, G., Hazzard, J. H., and Cusanovich, M. A. (1989) Photoactive yellow protein from the purple phototrophic bacterium, Ectothiorhodospira halophila-quantum yield of photobleaching and effects of temperature, alcohols, glycerol, and sucrose on kinetics of photobleaching and recovery, Biophys. J. 56, 559-564.
17. Rubinstenn, G., Vuister, G. W., Mulder, F. A. A., Dux, P. E., Boelens, R., Hellingwerf, K. J., and Kaptein, R. (1998) Structural and dynamic changes of photoactive yellow protein during its photocycle in solution, Nat. Struct. Biol. 5, 568-570.
18. Craven, C. J., Derix, N. M., Hendriks, J., Boelens, R., Hellingwerf, K. J., and Kaptein, R. (2000) Probing the nature of the blue-shifted intermediate of photoactive yellow protein in solution by NMR: hydrogen-deuterium exchange data and pH studies, Biochemistry 39, 14392-14399.
19. Brudler, R., Rammelsberg, R., Woo, T. T., Getzoff, E. D., and Gerwert, K. (2001) Structure of the II early intermediate of photoactive yellow protein by FTIR spectroscopy, Nat. Struct. Biol. 8, 265-270.
20. Sasaki, J., Kumauchi, M., Hamada, N., Oka, T., and Tokunaga, F. (2002) Light-induced unfolding of photoactive yellow protein mutant M100L, Biochemistry 41, 1915-1922.
21. Lee, B.-C., Croonquist, P. A., Sosnick, T. R., and Hoff, W. D. (2001) PAS domain receptor photoactive yellow protein is converted to a molten globule state upon activation, J. Biol. Chem. 276, 20821-20823.
22. Imamoto, Y., Kamikubo, H., Harigai, M., Shimizu, N., and Kataoka, M. (2002) Light-induced global conformational change of photoactive yellow protein in solution, Biochemistry 41, 13595-13601.
23. Hendriks, J., Gensch, T., Hviid, L., van der Horst, M. A., Hellingwerf, K. J., and van Thor, J. J. (2002) Transient exposure of hydrophobic surface in the photoactive yellow protein monitored with Nile red, Biophys. J. 82, 1632-1643.
24. Kelemen, L., Nie, B., Phillip, A., Hoff, W., and Xie, A. (2005) Impact of crystallization on protein structural dynamics, Biophys. J. 88, 208a.
25. Vogel, R., Ruprecht, J., Villa, C., Mielke, T., Schertier, G. F. X., and Siebert, F. (2004) Rhodopsin photoproducts in 2D crystals, J. Mol. Biol. 338, 597-609.
26. Hoff, W. D., Xie, A., Van Stokkum, I. H. M., Tang, X., Gural, J., Kroon, A. R., and Hellingwerf, K. J. (1999) Global conformational changes upon receptor stimulation in photoactive yellow protein, Biochemistry 38, 1009-1017.
27. Harigai, M., Imamoto, Y., Kamikubo, H., Yamazaki, Y., and Kataoka, M. (2003) Role of an N-terminal loop in the secondary structural change of photoactive yellow protein, Biochemistry 42, 13893-13900.
28. 2 intermediates, chromophore deprotonation by hydroxyl uptake, and protonation relaxation of the dark state, Biochemistry 42, 8780-8790.
29. Hendriks, J., van Stokkum, I. H. M., and Hellingwerf, K. J. (2003) Deuterium isotope effects in the photocycle transitions of the photoactive yellow protein, Biophys. J. 84, 1180-1191.
30. Imamoto, Y., Harigai, M., and Kataoka, M. (2004) Direct observation of the pH-dependent equilibrium between L-like and M intermediates of photoactive yellow protein, FEBS Lett. 577, 75-80.
31. 2 intermediates in the photocycle of photoactive yellow protein by double flash experiments with variable time delay, Biochemistry 44, 656-665.
32. Dux, P., Rubinstenn, G., Vuister, G. W., Boelens, R., Mulder, F. A. A., Hard, K., Hoff, W. D., Kroon, A. R., Crielaard, W, Hellingwerf, K. J., and Kaptein, R. (1998) Solution structure and backbone dynamics of the photoactive yellow protein, Biochemistry 37, 12689-12699.
33. Devanathan, S., Genick, U. K., Canestrelli, I. L., Meyer, T. E., Cusanovich, M. A., Getzoff, E. D., and Tollin, G. (1998) New insights into the photocycle of Ectothiorhodospira halophila photoactive yellow protein: Photorecovery of the long-lived photobleached intermediate in the Met100Ala mutant, Biochemistry 37, 11563-11568.
34. Getzoff, E. D., Gutwin, K. N., and Genick, U. K. (2003) Anticipatory active-site motions and chromophore distortion prime photoreceptor PYP for light activation, Nat. Struct. Biol. 10, 663-668.
35. Kyndt, J. A., Vanrobaeys, F., Fitch, J. C., Devreese, B. V., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (2003) Heterologous production of Halorhodospira halophila holophotoactive yellow protein through tandem expression of the postulated biosynthetic genes, Biochemistry 42, 965-970.
36. Kyndt, J. A., Hurley, J. K., Devreese, B., Meyer, T. E., Cusanovich, M. A., Tollin, G., and Van Beeumen, J. J. (2004) Rhodobacter capsulatus photoactive yellow protein: Genetic context, spectral and kinetics characterization, and mutagenesis, Biochemistry 43, 1809-1820.
37. Borucki, B., Otto, H., and Heyn, M. P. (1999) Reorientation of the retinylidene chromophore in the K, L, and M intermediates of bacteriorhodopsin from time-resolved linear dichroism: resolving kinetically and spectrally overlapping intermediates of chromoproteins, J. Phys. Chem B 103, 6371-6383.
38. Borucki, B., Otto, H., Rottwinkel, G., Hughes, J., Heyn, M. P., and Lamparter, T. (2003) Mechanism of Cph1 phytochrome assembly from stopped-flow kinetics and circular dichroism, Biochemistry 42, 13684-13697.
39. Vogel, R., and Siebert, F. (2002) Conformation and stability of α-helical membrane proteins. 1. Influence of salts on conformational equilibria between active and inactive states of rhodopsin, Biochemistry 41, 3529-3535.
40. Genick, U. K., Devanathan, S., Meyer, T. E., Canestrelli, I. L., Williams, E., Cusanovich, M. A., Tollin, G., and Getzoff, E. D. (1997) Active site mutants implicate key residues for control of color and light cycle kinetics of photoactive yellow protein, Biochemistry 36, 8-14.
41. Scrutton, N. S., and Raine, A. R. C. (1996) Cation-π bonding and amino-aromatic interactions in the biomolecular recognition of substituted ammonium ligands, Biochem. J. 319, 1-8.
42. Rajagopal, S., and Moffat, K. (2003) Crystal structure of a photoactive yellow protein from a sensor histidine kinase: Conformational variability and signal transduction, Proc. Natl. Acad. Sci. U.S.A. 100, 1649-1654.
43. Kraft, B. J., Masuda, S., Kikuchi, J., Dragnea, V., Tollin, G., Zaleski, J. M., and Bauer, C. E. (2003) Spectroscopic and mutational analysis of the blue-light photoreceptor AppA: A novel photocycle involving flavin stacking with an aromatic amino acid, Biochemistry 42, 6726-6734.
44. Hendriks, J., Hoff, W. D., Crielaard, W., and Hellingwerf, K. J. (1999) Protonation deprotonation reactions triggered by photoactivation of photoactive yellow protein from Ectothiorhodospira halophila, J. Biol. Chem. 274, 17655-17660.
45. Brudler, R., Meyer, T. E., Genick, U. K., Devanathan, S., Woo, T. T., Millar, D. P., Gerwert, K., Cusanovich, M. A., Tollin, G., and Getzoff, E. D. (2000) Coupling of hydrogen bonding to chromophore conformation and function in photoactive yellow protein, Biochemistry 39, 13478-13486.
46. Meyer, T. E., Devanathan, S., Woo, T., Getzoff, E. D., Tollin, G., and Cusanovich, M. A. (2003) Site-specific mutations provide new insights into the origin of pH effects and alternative spectral forms in the photoactive yellow protein from Halorhodospira halophila, Biochemistry 42, 3319-3325.
47. Baldwin, R. L. (1996) How Hofmeister ion interactions affect protein stability, Biophys. J. 71, 2056-2063.
48. Harper, S. M., Neil, L. C., and Gardner, K. H. (2003) Structural basis of a phototropin light switch, Science 301, 1541-1544.
49. α helix interaction activates phototropin kinase activity, Biochemistry 43, 16184-16192.
50. Shimizu, N., Kamikubo, H., Mihara, K., Imamoto, Y., and Kataoka, M. (2002) Effect of organic anions on the photoreaction of photoactive yellow protein, J. Biochem. (Tokyo) 132, 257-263.
51. Vogel, R., Fan, G.-B., Siebert, F., and Sheves, M. (2001) Anions stabilize a metarhodopsin II-like photoproduct with a protonated Schiff base, Biochemistry 40, 13342-13352.
52. Dickopf, S., Mielke, T., and Heyn, M. P. (1998) Kinetics of the light-induced proton translocation associated with the pH-dependent formation of the metarhodopsin I/II equilibrium of bovine rhodopsin, Biochemistry 37, 16888-16897.
53. Vogel, R. (2004) Influence of salts on rhodopsin photoproduct equilibria and protein stability, Curr. Opin. Colloid Interface Sci. 9, 133-138.
54. Farrens, D. L., Altenbach, C., Yang, K., Hubbell, W. L., and Khorana, H. G. (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin, Science 274, 768-770.
55. Sheikh, S. P., Zvyaga, T. A., Lichtarge, O., Sakmar, T. P., and Bourne, H. R. (1996) Rhodopsin activation blocked by metalion-binding sites linking transmembrane helices C and F, Nature 383, 347-350.
56. Ghadouni, P., Steenhuis, J. J., Farrens, D. L., and Kobilka, B. K. (2001) Agonist-induced conformational changes in the G-protein-coupling domain of the β2 adrenergic receptor, Proc. Natl. Acad. Sci. U.S.A. 98, 5997-6002.
57. Ballesteros, J. A., Jensen, A. D., Liapakis, G., Rasmussen, S. G., Shi, L., Gether, U., and Javitch, J. A. (2001) Activation of the β2 adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6, J. Biol. Chem. 276, 27171-27177.
58. Shapiro, D. A., Kristiansen, K., Weiner, D. M., Kroeze, W. K., and Roth, B. L. (2002) Evidence for a model of agonist-induced activation of 5-hydroxytryptamine 2A serotonin receptors that involves the disruption of a strong ionic interaction between helices 3 and 6, J. Biol. Chem. 277, 11441-11449.