On the configurational and conformational changes in photoactive yellow protein that leads to signal generation in Ectothiorhodospira halophila

Journal of Biological Physics

Volumn 28, Issue 3, 2002, Pages 395-412

  Hellingwerf, K J ^a   Hendriks, J ^a   Gensch, T H ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

4 Hydroxy cinnamic acid; Contact dependence; Hysteresis; Photo isomerisation; Photoactive yellow protein; Polarization spectroscopy; Protein dynamics; Time resolved FTIR spectroscopy; Time resolved X ray diffraction; Transient intermediates

Indexed keywords

PARA COUMARIC ACID; PHOTOACTIVE YELLOW PROTEIN;

ARTICLE; CRYSTALLIZATION; FOURIER TRANSFORMATION; HALORHODOSPIRA HALOPHILA; HYDROGEN BOND; HYSTERESIS; INFRARED SPECTROSCOPY; ISOMERISM; KINETICS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; X RAY DIFFRACTION;

ECTOTHIORHODOSPIRA; HALOPHILA; HALORHODOSPIRA HALOPHILA;

EID: 0036032563     PISSN: 00920606     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020360505111     Document Type: Article

References (68)

1. Drenth, J.: Principles of Protein X-ray Crystallography, Springer-Verlag, New York, 1994.
2. Wüthrich, K.: NMR of Proteins and Nucleic Acids, John Wiley & Sons, New York, 1986.
3. Hellingwerf, K.J., Hoff, W.D. and Crielaard, W.: Photobiology of Microorganisms: How Photosensors Catch a Photon to Initialize Signaling, Mol. Microbiol. 21 (1996), 683-693.
4. Meyer, T.E.: Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium ectothiorhodospira halophila, Biochim. Biophys. Acta. 806 (1985), 175-183.
5. Kort, R., Hoff, W.D., Van West, M., Kroon, A.R., Hoffer, S.M., Vlieg, K.H., Crielaand, W. Van Beeumen, J.J. and Hellingwerf, K.J.: The xanthopsins: A new family of eubacterial bluelight photoreceptors, EMBO J 15 (1996), 3209-3218.
6. Sprenger, W.W., Hoff, W.D., Armitage, J.P. and Hellingwerf, K.J.: The eubacterium ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein, J. Bacteriol. 175 (1993), 3096-3104.
7. Jiang, Z., Swem, L.R., Rushing, B.G., Devanathan, S., Tollin, G. and Bauer, C.E.: Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes, Science 285 (1999), 406-409.
8. Hoff, W.D.: Photoactive Yellow Protein. A New Family of Eubacterial Blue-Light Photoreceptors, PhD Thesis, University of Amsterdam, Copyprint 2000, Amsterdam, 1995.
9. Imamoto, Y., Ito, T., Kataoka, M. and Tokunaga, F.: Reconstitution photoactive yellow protein from apoprotein and P-coumaric acid derivatives, FEBS Lett. 374 (1995), 157-160.
10. Genick, U.K., Devanathan, S., Meyer, T.E., Canestrelli, I.L., Williams, E., Cusanovich, M.A., Tollin, G. and Getzoff, E.D.: Active site mutants implicate key residues for control of color and light cycle kinetics of photoactive yellow protein, Biochemistry 36 (1997), 8-14.
11. Borgstahl, G.E., Williams, D.R. and Getzoff, E.D.: 1.4 A structure of photoactive yellow protein, a cytosolic photoreceptor: Unusual fold, active site and chromophore, Biochemistry 34 (1995), 6278-6287.
12. Dux, P., Rubinstenn, G., Vuister, G.W., Boelens, R., Mulder, F.A., Hard, K., Hoff, W.D., Kroon, A.R., Crielaard, W., Hellingwerf, K.J. and Kaptein, R.: Solution structure and backbone dynamics of the photoactive yellow protein, Biochemistry 37 (1998), 12689-12699.
13. McRee, D.E., Tainer, J.A., Meyer, T.E., Van Beeumen, J., Cusanovich M.A. and Getzoff, E.D.: Crystallographic structure of a photoreceptor protein at 2.4 a resolution, Proc. Natl. Acad. Sci. USA 86 (1989), 6533-6537.
14. Genick, U.K., Soltis, S.M., Kuhn, P., Canestrelli, I.L. and Getzoff, E.D.: Structure at 0.85 a resolution of an early protein photocycle intermediate, Nature 392 (1998), 206-209.
15. Scrutton, N.S. and Raine, A.R.: Cation-Pi Bonding and Amino-Aromatic Interactions in the Biomolecular Recognition of Substituted Ammonium Ligands, Biochem. J. 319 (1996), 1-8.
16. Mihara, K., Hisatomi, O., Imamoto, Y., Kataoka, M. and Tokunaga, F.: Functional expression and site-directed mutagenesis of photoactive yellow protein, J. Biochem. (Tokyo) 121 (1997), 876-880.
17. Pellequer, J.L., Wager-Smith, K.A., Kay, S.A. and Getzoff, E.D.: Photoactive yellow protein: A structural prototype for the three-dimensional fold of the pas domain superfamily, Proc. Natl. Acad. Sci. USA 95 (1998), 5884-5890.
18. Weaver, T.M.: The pi-helix translates structure into function, Protein Sci. 9 (2000), 201-206.
19. Van Aalten, D.M.F., Crielaard, W., Hellingwerf, K.J. and Joshua-Tor, L.: Conformational substates in different crystal forms of the photoactive yellow protein - Correlation with theoretical and experimental flexibility, Protein Science 9 (2000), 64-72.
20. Van Beeumen, J.J., Devreese, B.V., Van Bun, S.M., Hoff, W.D., Hellingwerf, K.J., Meyer, T.E., McRee, D.E. and Cusanovich, M.A.: Primary structure of a photoactive yellow protein from the phototrophic bacterium ectothiorhodospira halophila, with evidence for the mass and the binding site of the chromophore, Protein Sci. 2 (1993), 1114-1125.
21. Hoff, W.D., Dux, P., Hard, K., Devreese, B., Nugteren-Roodzant, I.M., Crielaard, W., Boelens, R., Kaptein, R., van Beeumen, J. and Hellingwerf, K.J.: Thiol ester-linked p-coumaric acid as a new photoactive prosthetic group in a protein with rhodopsin-like photochemistry, Biochemistry 33 (1994), 13959-13962.
22. Baca, M., Borgstahl, G.E., Boissinot, M., Burke, P.M., Williams, D.R., Slater, K.A. and Getzoff, E.D.: Complete chemical structure of photoactive yellow protein: Novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry, Biochemistry 33 (1994), 14369-14377.
23. Kim, M., Mathies, R.A., Hoff, W.D. and Hellingwerf, K.J.: Resonance raman evidence that the thioester-linked 4-hydroxycinnamyl chromophore of photoactive yellow protein is deprotonated, Biochemistry 34 (1995), 12669-12672.
24. Hoff, W.D., Van Stokkum, I.H.M., Gural, J. and Hellingwerf, K.J.: Comparison of acid denaturation and light activation in the eubacterial blue-light receptor photoactive yellow protein, Biochim. Biophys. Acta 1322 (1997), 151-162.
25. Kroon, A.R., Hoff, W.D., Fennema, H.P., Gijzen, J., Koomen, J.G., Verhoeven, J.W., Crielaard, W. and Hellingwerf, K.J.: Spectral tuning, fluorescence and photoactivity in hybrids of photoactive yellow protein, reconstituted with native or modified chromophores, J. Biol. Chem. 271 (1996), 31949-31956.
26. van Aalten, D.M., Hoff, W.D., Findlay, J.B., Crielaard, W. and Hellingwerf, K.J.: Concerted motions in the photoactive yellow protein, Protein Eng 11 (1998), 873-879.
27. Hoff, W.D., van Stokkum, I.H.M., van Ramesdonk, H.J., van Brederode, M.E., Brouwer, A.M., Fitch, J.C., Meyer, T.E., van Grondelle, R. and Hellingwerf, K.J.: Measurement and Global Analysis of the Absorbance Changes in the Photocycle of the Photoactive Yellow Protein from Ectothiorhodospira halophila, Biophys. J. 67 (1994), 1691-705.
28. Baltuška, A., van Stokkum, I.H.M., Kroon, A., Monshouwer, R., Hellingwerf, K.J. and van Grondelle, R.: The primary events in the photoactivation of yellow protein, Chem. Phys. Lett. 270 (1997), 263-266.
29. Ujj, L., Devanathan, S., Meyer, T.E., Cusanovich, M.A., Tollin, G. and Atkinson, G.H.: New photocycle intermediates in the photoactive yellow protein from ectothiorhodospira halophila: Picosecond transient absorption spectroscopy, Biophys. J. 75 (1998), 406-412.
30. Devanathan, S., Pacheco, A., Ujj, L., Cusanovich, M., Tollin, G., Lin, S. and Woodbury, N.: Femtosecond spectroscopic observations of initial intermediates in the photocycle of the photoactive yellow protein from ectothiorhodospira halophila, Biophys. J. 77 (1999), 1017-1023.
31. Zhou, Y., Ujj, L., Meyer, T.E., Cussanovich, M.A. and Atkinson, G.H.: Photocycle dynamics and vibrational spectroscopy of the e46q mutant of photoactive yellow protein, J. Phys. Chem. A 105 (2001), 5719-5726.
32. Devanathan, S., Lin, S., Cusanovich, M.A., Woodbury, N. and Tollin, G.: Early intermediates in the photocycle of the glu46gln mutant of photoactive yellow protein: Femtosecond spectroscopy, Biophys. J. 79 (2000), 2132-2137.
33. Chosrowjan, H., Mataga, N., Shibata, Y., Imamoto, Y. and Tokunaga, F.: Environmental effects on the femtosecond-picosecond fluorescence dynamics of photoactive yellow protein: Chromophores in aqueous solutions and in protein nanospaces modified by site-directed mutagenesis, J. Phys. Chem. B 102 (1998), 7695-7698.
34. Xie, A., Hoff, W.D., Kroon, A.R. and Hellingwerf, K.J.: Glu46 donates a proton to the 4-hydroxycinnamate anion chromophore during the photocycle of photoactive yellow protein, Biochemistry 35 (1996), 14671-1468.
35. Imamoto, Y., Shirahige, Y., Tokunaga, F., Kinoshita, T., Yoshihara, K., Kataoka, M.: Low-temperature fourier transform infrared spectroscopy of photoactive yellow protein, Biochemistry 40 (2001), 8997-9004.
36. Imamoto, Y. Kataoka, M. and Tokunaga, F.: Photoreaction cycle of photoactive yellow protein from ectothiorhodospira halophila studied by low temperature spectroscopy, Biochem. 35 (1996), 14047-14053.
37. Imamoto, Y. Kataoka, M. and Tokunaga, F., Asahi, T. and Masuhara, H.: Primary photoreaction of photoactive yellow protein studied by subpicosecond-nanosecond spectroscopy, Biochemistry 40 (2001), 6047-6052.
38. Meyer, T.E., Yakali, E., Cusanovich, M.A. and Tollin, G.: Properties of a water-soluble, yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin, Biochemistry 26 (1987), 418-423.
39. Miller, A. Leigeber, H., Hoff, W.D. and Hellingwerf, K.J.: A light-dependent branchingreaction in the photocycle of the yellow protein from ectothiorhodospira halophila, Biochim. Biophys. Acta 1141 (1993), 190-196.
40. Hendriks, J., van Stokkum, I.H., Crielaard, W. and Hellingwerf, K.J.: Kinetics of and intermediates in a photocycle branching reaction of the photoactive yellow protein from ectothiorhodospira halophila, FEBS Lett. 458 (1999), 252-256.
41. Van Brederode, M.E., Hoff, W.D., Van Stokkum, I.H., Groot, M.L. and Hellingwerf, K.J.: Protein folding thermodynamics applied to the photocycle of the photoactive yellow protein, Biophys. J. 71 (1996), 365-380.
42. Frauenfelder, H., Sligar, S.G. and Wolynes, P.G.: The energy landscapes and motions of proteins, Science 254 (1991), 1598-1603.
43. Hendriks, J., Hoff, W.D., Crielaard, W. and Hellingwerf, K.J.: Protonation/deprotonation reactions triggered by photoactivation of photoactive yellow protein from ectothiorhodospira halophila, J. Biol. Chem 274 (1999), 17655-17660.
44. Kort, R., Vonk, H., Xu, X., Hoff, W.D., Crielaard, W. and Hellingwerf, K.J.: Evidence for trans-cis isomerization of the p-coumaric acid chromophore as the photochemical basis of the photocycle of photoactive yellow protein, FEBS Lett. 382 (1996), 73-78.
45. Rubinstenn, G., Vuister, G.W., Mulder, F.A., Dux, P.E., Boelens, R., Hellingwerf, K.J. and Kaptein, R.: Structural and dynamic changes of photoactive yellow protein during its photocycle in solution, Nat. Struct. Biol. 5 (1998), 568-570.
46. Devanathan, S., Genick, U.K., Canestrelli, I.L., Meyer, T.E., Cusanovich, M.A., Getzoff, E.D. and Tollin, G.: New insights into the photocycle of ectothiorhodospira halophila photoactive yellow protein: photorecovery of the long-lived photobleached intermediate in the met100ala mutant, Biochemistry 37 (1998), 11563-11568.
47. Devanathan, S., Genick, U.K., Getzoff, E.D., Meyer, T.E., Cusanovich, M.A. and Tollin, G.: Preparation and properties of a 3,4-dihydroxycinnamic acid chromophore variant of the photoactive yellow protein, arch. Biochem. Biophys. 340 (1997), 83-89.
48. Amadei, A., Linssen, A.B. and Berendsen, H.J.: Essential dynamics of proteins, Proteins 17 (1993), 412-25.
49. van Aalten, D.M., Findlay, J.B., Amadei, A. and Berendsen, H.J.: Essential dynamics of the cellular retinol-binding protein - Evidence for ligand-induced conformational changes, Protein Eng. 8 (1995), 1129-35.
50. Genick, U.K., Borgstahl, G.E., 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.: Structure of a protein photocycle intermediate by millisecond time-resolved crystallography, Science 275 (1997), 1471-1475.
51. Perman, B., Srajer, V., Ren, Z., Teng, T., Pradervand, C., Ursby, T., Bourgeois, D., Schotte, F., Wulff, M., Kort, R., Hellingwerf, K. and Moffat, K.: Energy transduction on the nanosecond time scale: Early structural events in a xanthopsin photocycle, Science 279 (1998), 1946-1950.
52. Ren, Z.: Nanosecond Time-Resolved Crystallography Signal Transduction By Photoreceptor Proteins, Academy Colloqium, Royal Dutch Academy of Sciences, Amsterdam, 2000.
53. Brudler, R., Rammelsberg, R., Woo, T.T., Getzoff, E.D. and Gerwert, K.: Structure of the II early intermediate of photoactive yellow protein by ftir spectroscopy, Nat. Struct. Biol. 8 (2001), 265-270.
54. Xie, A., Kelemen, L., Hendriks, J., White, B.J., Hellingwerf, K.J. and Hoff, W.D.: Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation, Biochemistry 40 (2001), 1510-1517.
55. Imamoto, Y., Mihara, K., Hisatomi, O., Kataoka, M., Tokunaga, F., Bojkova, N. and Yoshihara, K.: Evidence for proton transfer from glu-46 to the chromophore during the photocycle of photoactive yellow protein, J. Biol. Chem. 272 (1997), 12905-12908.
56. McCain, D.A., Amici, L.A. and Spudich, J.L.: Kinetically Resolved States of the Halobacterium Halobium Flagellar Motor Switch and Modulation of the Switch by Sensory Rhodopsin 1, J. Bacteriol. 169 (1987), 4750-4758.
57. Craven, C.J., Derix, N.M., Hendriks, J., Boelens, R., Hellingwerf, K.J. and Kaptein, R.: Probing the nature of the blue-shifted intermediate of photoactive yellow protein in solation by nmr: Hydrogen-deuterium exchange data and ph studies, Biochemistry 39 (2000), 14392-14399.
58. Privalov, P.L. and Makhatadze, G.I.: Heat capacity of proteins. II. Partial molar heat capacity of the unfolded polypeptide chain of proteins: Protein unfolding effects, J. Mol. Biol. 213 (1990), 385-391.
59. Oliveberg, M., Tan, Y.J. and Fersht, A.R.: Negative Activation Enthalpies in the Kinetics of Protein Folding, Proc. Natl. Acad. Sci. USA 92 (1995), 8926-8929.
60. Karplus, M.: Aspects of protein reaction dynamics: Deviations from simple behavior, J. Phys. Chem. B 104 (2000), 11-27.
61. Hoff, W.D., Xie, A., Van Stokkum. I.H., Tang, X.J., Gural, J., Kroon, A.R. and Hellingwerf, K.J.: Global conformational changes upon receptor stimulation in photoactive yellow protein, Biochemistry 38 (1999), 1009-1017.
62. Meyer, T.E., Tollin, G., Hazzard, J.H. and Cusanovich, M.A.: 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 (1989), 559-564.
63. van der Horst, M., van Stokkum, I.H., Crielaard, W. and Hellingwerf, K.J.: The role of the n-terminal domain of photoactive yellow protein in the transient partial unfolding during signalling state formation, FEBS Lett. 497 (2001), 26-30.
64. Sergi, A., Grüning, M., Ferrario, M. and Buda, F.: Density functional study of the photoactive yellow protein's chromophore, J. Phys. Chem. B 105 (2001), 4386-4391.
65. Mayor, U., Johnson, C.M., Daggett, V. and Fersht, A.R.: Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation, Proc. Natl. Acad. Sci. USA 97 (2000), 13518-13522.
66. Shiozawa, M., Yoda, M., Kamiya, N., Asakawa, N., Higo, J., Inoue, Y. and Sakurai, M.: Evidence for large structural fluctuations of the photobleached intermediate of photoactive yellow protein in solution, J. Am. Chem. Soc. 123 (2001), 7445-7446.
67. Liu, R.S. and Hammond, G.S.: The case of medium-dependent dual mechanisms for photolsomerization: One-bond-flip and hula-twist, Proc. Natl. Acad. Sci. USA 97 (2000), 11153-11158.
68. Takeshita, K., Hirota, N., Imamoto, Y., Kataoka, M., Tokunaga, F. and Terazima, M.: Temperature-dependent volume change of the initial step of the photoreaction of photoactive yellow protein (pyp) studied by transient grating, J. Am. Chem. Soc. 122 (2000), 8524-8528.