Contrasting the excited-state dynamics of the photoactive yellow protein chromophore: Protein versus solvent environments

Biophysical Journal

Volumn 87, Issue 3, 2004, Pages 1848-1857

  Vengris, Mikas ^a   Van Der Horst, Michael A ^b   Zgrablić, Goran ^c   Van Stokkum, Ivo H M ^a   Haacke, Stefan ^c   Chergui, Majed ^c   Hellingwerf, Klaas J ^b   Van Grondelle, Rienk ^a   Larsen, Delmar S ^a,d  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c EPFL   (Switzerland)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOTOACTIVE YELLOW PROTEIN; SOLVENT;

AQUEOUS SOLUTION; ARTICLE; CHROMATOPHORE; COVALENT BOND; DYNAMICS; EXCITED STATE DYNAMICS; FLUORESCENCE; HYDROGEN BOND; ISOMERISM; PHOTOCHEMICAL QUENCHING; SOLVATION; SPECTROSCOPY;

EID: 4444246946     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.043224     Document Type: Article

References (57)

1. Abramavicius, D., V. Gulbinas, L. Valkunas, Y.-J. Shiu, K. Liang, M. Hayashi, and S. Lin. 2002. Molecular twisting and relaxation in the excited state of triarylpyrylium cations. J. Phys. Chem. A. 106:8864-8869.
2. Alfano, R., R. Govindjee, B. Becher, and T. Ebrey. 1976. Picosecond kinetics of the fluorescence from the chromophore of the purple membrane protein of Halobacterium halobium. Biophys. J. 16:541-545.
3. Baca, M., G. E. Borgstahl, M. Boissinot, P. M. Burke, D. R. Williams, K. A. Slater, and E. D. Getzoff. 1994. Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochemistry. 33:14369-14377.
4. Baltuška, A., I. H. M. van Stokkum, A. Kroon, R. Monshouwer, K. J. Hellingwerf, and R. van Grondelle. 1997. The primary events in the photoactivation of yellow protein. Chem. Phys. Lett. 270:263-266.
5. Cembran, A., F. Bernardi, M. Olivucci, and M. Garavelli. 2003. Excited-state singlet manifold and oscillatory features of a nonatetraeniminium retinal chromophore model. J. Am. Chem. Soc. 125:12509-12519.
6. Changenet, P., H. Zhang, M. J. van der Meer, K. J. Hellingwerf, and M. Glasbeek. 1998. Subpicosecond fluorescence up-conversion measurements of primary events in yellow proteins. Chem. Phys. Lett. 282:276-282.
7. Changenet-Barret, P., C. Choma, E. Gooding, W. DeGrado, and R. M. Hochstrasser. 2000. Ultrafast dielectric response of proteins from dynamics Stokes shifting of coumarin in calmodulin. J. Phys. Chem. B. 104:9322-9329.
8. Changenet-Barret, P., A. Espagne, N. Katsonis, S. Charier, J.-B. Baudin, L. Jullien, P. Plaza, and M. M. Martin. 2002. Excited-state relaxation dynamics of a PYP chromophore model in solution: influence of the thioester group. Chem. Phys. Lett. 365:285-291.
9. Changenet-Barret, P., P. Plaza, and M. M. Martin. 2001. Primary events in the photoactive yellow protein chromophore in solution. Chem. Phys. Lett. 336:439-444.
10. Cusanovich, M. A., and T. E. Meyer. 2003. Photoactive yellow protein: a prototypic PAS domain sensory protein and development of a common signaling mechanism. Biochemistry. 42:4759-4770.
11. 46Gln mutant of photoactive yellow protein: femtosecond spectroscopy. Biophys. J. 79: 2132-2137.
12. Devanathan, S., A. Pacheco, L. Ujj, M. Cusanovich, G. Tollin, S. Lin, and N. Woodbury. 1999. Femtosecond spectroscopic observations of initial intermediates in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila. Biophys. J. 77:1017-1023.
13. Doig, S. J., P. J. Reid, and R. A. Mathies. 1991. Picosecond time-resolved resonance Raman spectroscopy of bacteriorhodopsin-J, bacterlorhodopsin-K, bacterlorhodopsin-K1 intermediates. J. Phys. Chem. 95:6372-6379.
14. Du, M., and G. R. Fleming. 1993. Femtosecond time-resolved fluorescence spectroscopy of bacteriorhodopsin-direct observation of excited-state dynamics in the primary step of the proton pump cycle. Biophys. Chem. 48:101-111.
15. Gai, F., K. C. Hasson, J. C. McDonald, and P. A. Anfinrud. 1998. Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin. Science. 279:1886-1891.
16. Gai, F., J. C. McDonald, and P. Anfinrud. 1997. Pump-dump-probe spectroscopy of bacteriorhodopsin: evidence for a near-IR excited state absorbance. J. Am. Chem. Soc. 119:6201-6202.
17. Genick, U. K., G. E. Borgstahl, K. Ng, Z. Ren, C. Pradervand, P. M. Burke, V. Srajer, T. Y. Teng, W. Schildkamp, D. E. McRee, K. Moffat, and E. D. Getzoff. 1997. Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science. 275:1471-1475.
18. Gensch, T., C. C. Gradinaru, I. H. M. van Stokkum, J. Hendriks, K. Hellingwerf, and R. van Grondelle. 2002. The primary photoreaction of photoactive yellow protein (PYP): anisotropy changes and excitation wavelength dependence. Chem. Phys. Lett. 356:347-354.
19. Gonzalez-Luque, R., M. Garavelli, F. Bernardi, M. Merchan, M. A. Robb, and M. Olivucci. 2000. Computational evidence in favor of a two-state, two-mode model of the retinal chromophore photoisomerization. Proc. Natl. Acad. Sci. USA. 97:9379-9384.
20. Groenhof, G., M. Bouxin-Cademartory, B. Hess, S. de Visser, H. Brendendsen, M. Olivucci, A. E. Mark, and M. A. Robb. 2004. Why photon absorption triggers isomerization of the chromophore in photoactive yellow protein. J. Am. Chem. Soc. 126:4228-4233.
21. Groenhof, G., M. F. Lensink, H. J. C. Berendsen, and A. E. Mark. 2002a. Signal transduction in the photoactive yellow protein. II. Proton transfer initiates conformational changes. Proteins Struct. Funct. Gen. 48:212-219.
22. Groenhof, G., M. F. Lensink, H. J. C. Berendsen, J. G. Snijders, and A. E. Mark. 2002b. Signal transduction in the photoactive yellow protein. I. Photon absorption and the isomerization of the chromophore. Proteins Struct. Funct. Gen. 48:202-211.
23. Groot, M. L., L. van Wilderen, D. S. Larsen, M. A. van der Horst, I. H. M. van Stokkum, K. J. Hellingwerf, and R. van Grondelle. 2003. Initial steps of signal generation in photoactive yellow protein revealed with femtosecond mid-infrared spectroscopy. Biochemistry. 42: 10054-10059.
24. Haacke, S., R. A. Taylor, I. Bar-Joseph, M. Brasil, M. Hartig, and B. Deveaud. 1998. Improving the signal-to-noise ratio of femtosecond luminescence up-conversion by multichannel detection. J. Optic. Soc. Am. B Optic. Phys. 15:1410-1417.
25. Hamm, P., M. Zurek, T. Röschinger, H. Patselt, D. Oesterhelt, and W. Zinth. 1996. Femtosecond spectroscopy of the photoisomerisation of the protonated Schiff base of all-trans retinal. Chem. Phys. Lett. 263:613-621.
26. Hanada, H., Y. Kanematsu, S. Kinoshita, M. Kumauchi, J. Sasaki, and F. Tokunaga. 2001. Ultrafast fluorescence spectroscopy of photoactive yellow protein. J. Luminesc. 94:593-596.
27. Hasson, K. C., F. Gai, and P. A. Anfinrud. 1996. The photoisomerization of retinal in bacteriorhodopsin: experimental evidence for a three-state model. Proc. Natl. Acad. Sci. USA. 93:15124-15129.
28. Hellingwerf, K. J., J. Hendriks, and T. Gensch. 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.
29. Hoff, W. D., S. L. S. Kwa, R. van Grondelle, and K. J. Hellingwerf. 1992. Low temperature absorbance and fluorescence spectroscopy of the photoactive yellow protein from Ectothiorhodospira halophila. Photochem. Photobiol. 56:529-539.
30. Hoff, W. D., I. H. M. van Stokkum, H. J. van Ramesdonk, M. E. van Brederode, A. M. Brouwer, J. C. Fitch, T. E. Meyer, R. van Grondelle, and K. J. Hellingwerf. 1994. Measurement and global analysis of the absorbance changes in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila. Biophys. J. 67:1691-1705.
31. Holzwarth, A. R. 1996. Data analysis in time-resolved measurements. In Biophysical Techniques in Photosynthesis. J. Amesz and A. J. Hoff, editors. Kluwer, Dordrecht, The Netherlands.
32. Humphrey, W., H. Lu, I. Logunov, H. J. Werner, and K. Schulten. 1998. Three electronic state model of the primary phototransformation of bacteriorhodopsin. Biophys. J. 75:1689-1699.
33. Imamoto, Y., M. Kataoka, F. Tokunaga, T. Asahi, and H. Masuhara. 2001. Primary photoreaction of photoactive yellow protein studied by subpicosecond-nanosecond spectroscopy. Biochemistry. 40:6047-6052.
34. Jarzeba, W., G. C. Walker, A. E. Johnson, and B. F. Barbara. 1991. Nonexponential solvation dynamics of simple liquids and mixtures. Chem. Phys. 152:57-68.
35. Jimenez, R., G. R. Fleming, P. V. Kumar, and M. Maroncelli. 1994. Femtosecond solvation dynamics of water. Nature. 369:471-473.
36. Kholodenko, Y., M. Volk, E. Gooding, and R. M. Hochstrasser. 2000. Energy dissipation and relaxation processes in deoxy myoglobin after photoexcitation in the Soret region. Chem. Phys. 259:71-87.
37. Ko, C., B. Levine, A. Toniolo, L. Monohar, S. Olsen, H.-J. Werner, and T. J. Martínez. 2003. Ab initio excited-state dynamics of the photoactive yellow protein chromophore. J. Am. Chem. Soc. 125:12710-12711.
38. Kort, R., W. D. Hoff, M. Van West, A. R. Kroon, S. M. Hoffer, K. H. Vlieg, W. Crielaand, J. J. Van Beeumen, and K. J. Hellingwerf. 1996. The xanthopsins: a new family of eubacterial blue-light photoreceptors. EMBO J. 15:3209-3218.
39. Kort, R., M. K. Phillips-Jones, D. M. van Aalten, A. Haker, S. M. Hoffer, K. J. Hellingwerf, and W. Crielaard. 1998. Sequence, chromophore extraction and 3-D model of the photoactive yellow protein from Rhodobacter sphaeroides. Biochim. Biophys. Acta. 1385:1-6.
40. Larsen, D. S., M. Vengris, I. H. M. van Stokkum, M. van der Horst, R. Cordfunke, K. J. Hellingwerf, and R. van Grondelle. 2003. Initial photoinduced dynamics of the photoactive yellow protein chromophore in solution. Chem. Phys. Lett. 369:563-569.
41. Larsen, D. S., M. Vengris, I. H. M. van Stokkum, M. van der Horst, F. L. de Weerd, K. J. Hellingwerf, and R. van Grondelle. 2004a. Photoisomerization and photoionization of the photoactive yellow protein chromophore in solution. Biophys. J. 86:2538-2550.
42. Larsen, D., I. H. M. van Stokkum, M. Vengris, M. A. van der Horst, F. L. de Weend, K. J. Hellingwerth, and R. van Grondelle. 2004b. Incoherent manipulation of the photoactive yellow protein photocycle with dispersed pump-dump-probe spectroscopy. Biophys. J. 87:1858-1872.
43. Masciangioli, T., S. Devanathan, M. A. Cusanovich, G. Tollin, and M. A. El-Sayed. 2000. Probing the primary event in the photocycle of photoactive yellow protein using photochemical hole-burning technique. Photochem. Photobiol. 72:639-644.
44. Mataga, N., H. Chosrowjan, Y. Shibata, Y. Imamoto, M. Kataoka, and F. Tokunaga. 2002. Ultrafast photoinduced reaction dynamics of photoactive yellow protein (PYP): observation of coherent oscillations in the femtosecond fluorescence decay dynamics. Chem. Phys. Lett. 352:220-225.
45. Mataga, N., H. Chosrowjan, Y. Shibata, Y. Imamoto, and F. Tokunaga. 2000a. Effects of modification of protein nanospace structure and change of temperature on the femtosecond to picosecond fluorescence dynamics of photoactive yellow protein. J. Phys. Chem. B. 104:5191-5199.
46. Mataga, N., H. Chosrowjan, Y. Shibata, Y. Imamoto, F. Tokunaga, and F. Tanaka. 2000b. Femtosecond fluorescence studies on ultrafast reaction dynamics of photoactive proteins. J. Luminesc. 98-89:821-823.
47. Mataga, N., H. Chosrowjan, S. Taniguchi, N. Hamada, F. Tokunaga, Y. Imamoto, and M. Kataoka. 2003. Ultrafast photoreactions in protein nanospaces as revealed by femtosecond fluorescence dynamics measurements on photoactive yellow protein and related systems. Phys. Chem. Chem. Phys. 5:2454-2460.
48. Perman, B., V. Srajer, Z. Ren, T. Teng, C. Pradervand, T. Ursby, D. Bourgeois, F. Schotte, M. Wulff, R. Kort, K. Hellingwerf, and K. Moffat. 1998. Energy transduction on the nanosecond time scale: early structural events in a xanthopsin photocycle. Science. 279:1946-1950.
49. Premvardhan, L. L., F. Buda, M. A. van der Horst, D. Luehrs, K. J. Hellingwerf, and R. van Grondelle. 2004. The impact of photon absorption on the electronic properties of p-coumaric acid derivatives of the photoactive yellow protein chromophore. J. Phys. Chem. B. 108: 5138-5148.
50. Ren, Z., B. Perman, V. Srajer, T.-V. Teng, C. Pradervand, D. Bourgeois, F. Schotte, T. Ursby, R. Kort, M. Wulff, and K. Moffat. 2001. A molecular movie at 1.8Å resolution displays the photocycle of photoactive yellow protein, a eubacterial blue-light receptor, from nanoseconds to seconds. Biochemistry. 40:13788-13801.
51. Rubinstenn, G., G. W. Vuister, F. A. Mulder, P. E. Dux, R. Boelens, K. J. Hellingwerf, and R. Kaptein. 1998. Structural and dynamic changes of photoactive yellow protein during its photocycle in solution. Nat. Struct. Biol. 5:568-570.
52. Ruhman, S., B. Hou, N. Freidman, M. Ottolenghi, and M. Sheves. 2002. Following evolution of bacteriorhodopsin in its reactive excited state via stimulated emission pumping. J. Am. Chem. Soc. 124:8854-8858.
53. Sprenger, W. W., W. D. Hoff, J. P. Armitage, and K. J. Hellingwerf. 1993. The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. J. Bacteriol. 175:3096-3104.
54. van Beeumen, J. J., B. V. Devreese, S. M. van Bun, W. D. Hoff, K. J. Hellingwerf, T. E. Meyer, D. E. McRee, and M. A. Cusanovich. 1993. 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. 2:1114-1125.
55. van Brederode, M. E., W. D. Hoff, I. H. Van Stokkum, M. L. Groot, and K. J. Hellingwerf. 1996. Protein folding thermodynamics applied to the photocycle of the photoactive yellow protein. Biophys. J. 71:365-380.
56. Xie, A., L. Kelemen, J. Hendriks, B. J. White, K. J. Hellingwerf, and W. D. Hoff. 2001. Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation. Biochemistry. 40: 1510-1517.
57. Zgrablić, G., K. Votchovsky, M. Kindermann, M. Chergui, and S. Haacke. 2003. Ultrafast photophysics of the protonated Schiff base of retinal in alcohols studied by femtosecond fluorescence up-conversion. In Femtochemistry and Femtobiology: Ultrafast Events in Molecular Science. M. M. Martin and J. T. Hynes, editors. Elsevier, Paris, France.