Ultrafast light-induced response of photoactive yellow protein chromophore analogues

Photochemical & Photobiological Sciences - Tập 6 - Trang 780-787 - 2007
Agathe Espagne1,2,3, Daniel H. Paik2,4, Pascale Changenet-Barret1, Pascal Plaza1, Monique M. Martin1, Ahmed H. Zewail2
1UMR CNRS-ENS 8640 P.A.S.T.E.U.R., Département de Chimie, Ecole Normale Supérieure, Paris, France
2Laboratory for Molecular Sciences, Arthur Amos Noyes Laboratory of Chemical Physics, California Institute of Technology, Pasadena, USA
3Service de Bioénergétique, CEA-Saclay, Gif-sur-Yvette Cedex, France
4JILA, University of Colorado, Boulder, USA

Tóm tắt

The fluorescence decays of several analogues of the photoactive yellow protein (PYP) chromophore in aqueous solution have been measured by femtosecond fluorescence up-conversion and the corresponding time-resolved fluorescence spectra have been reconstructed. The native chromophore of PYP is a thioester derivative of p-coumaric acid in its trans deprotonated form. Fluorescence kinetics are reported for a thioester phenyl analogue and for two analogues where the thioester group has been changed to amide and carboxylate groups. The kinetics are compared to those we previously reported for the analogues bearing ketone and ester groups. The fluorescence decays of the full series are found to lie in the 1–10 ps range depending on the electron-acceptor character of the substituent, in good agreement with the excited-state relaxation kinetics extracted from transient absorption measurements. Steady-state photolysis is also examined and found to depend strongly on the nature of the substituent. While it has been shown that the ultrafast light-induced response of the chromophore in PYP is controlled by the properties of the protein nanospace, the present results demonstrate that, in solution, the relaxation dynamics and pathway of the chromophore is controlled by its electron donor—acceptor structure: structures of stronger electron donor—acceptor character lead to faster decays and less photoisomerisation.

Tài liệu tham khảo

K. J. Hellingwerf, J. Hendriks and T. Gensch, Photoactive yellow protein, a new type of photoreceptor protein: Will this “yellow lab” bring us where we want to go?, J. Phys. Chem. A, 2003, 107, 1082–1094.

M. A. Cusanovich and T. E. Meyer, Photoactive yellow protein: a prototypic PAS domain sensory protein and development of a common signaling mechanism, Biochemistry, 2003, 42, 4759–4770.

N. Mataga, H. Chosrowjan and S. Taniguchi, Investigations into the dynamics and mechanisms of ultrafast photoinduced reactions taking place in photoresponsive protein nanospaces (PNS), J. Photochem. Photobiol., C, 2004, 5, 155–168.

P. Changenet-Barret, A. Espagne, P. Plaza, K. J. Hellingwerf and M. M. Martin, Investigations of the primary events in a bacterial photoreceptor for photomotility: photoactive yellow protein (PYP), New J. Chem., 2005, 4, 527–534.

D. S. Larsen, R. van Grondelle, Initial photoinduced dynamics of the photoactive yellow protein, ChemPhysChem, 2005, 6, 828–837.

L. J. G. W. van Wilderen, M. A. van der Horst, I. H. M. van Stokkum, K. J. Hellingwerf, R. van Grondelle and M. L. Groot, Ultrafast infrared spectroscopy reveals a key step for successful entry into the photocycle for photoactive yellow protein, Proc. Natl. Acad. Sci. USA, 2006, 103, 15050–15055.

W. W. Sprenger, W. D. Hoff, J. P. Armitage and K. J. Hellingwerf, The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein, J. Bacteriol., 1993, 175, 3096–3104.

D.-P. Häder and M. Lebert, Photomovement, in Comprehensive series in photosciences, Elsevier, Amsterdam, 2001

P. Changenet-Barret, P. Plaza and M. M. Martin, Primary events in the photoactive yellow protein chromophore in solution, Chem. Phys. Lett., 2001, 336, 439–444.

P. Changenet-Barret, A. Espagne, N. Katsonis, S. Charier, J.-B. Baudin, L. Jullien, P. Plaza and M. M. Martin, Excited-state relaxation dynamics of a PYP chromophore model in solution: Influence of the thioester group, Chem. Phys. Lett., 2002, 365, 285–291.

D. S. Larsen, M. Vengris, I. H. M. Van Stokkum, M. A. van der Horst, R. A. Cordfunke, K. J. Hellingwerf, R. van Grondelle, Initial photo-induced dynamics of the photoactive yellow protein chromophore in solution, Chem. Phys. Lett., 2003, 369, 563–569.

P. Changenet-Barret, A. Espagne, S. Charier, J.-B. Baudin, L. Jullien, P. Plaza, K. J. Hellingwerf and M. M. Martin, Early molecular events in the photoactive yellow protein: Role of the chromophore photophysics, Photochem. Photobiol. Sci., 2004, 3, 823–829.

D. S. Larsen, M. Vengris, I. H. M. van Stokkum, M. A. van der Horst, F. L. de Weerd, K. J. Hellingwerf, R. van Grondelle, Photoisomerization and photoionization of the photoactive yellow protein chromophore in solution, Biophys. J., 2004, 86, 2538–2550.

M. Vengris, M. A. van der Horst, G. Zgrablic, I. H. M. van Stokkum, S. Haacke, M. Chergui, K. J. Hellingwerf, R. van Grondelle and D. S. Larsen, Contrasting the excited-state dynamics of the photoactive yellow protein chromophore: Protein vs. solvent environments, Biophys. J., 2004, 87, 1848–1857.

M. Vengris, D. S. Larsen, M. A. van der Horst, O. F. A. Larsen, K. J. Hellingwerf, R. van Grondelle, Ultrafast dynamics of isolated model photoactive yellow protein chromophores: “Chemical perturbation theory” in the laboratory, J. Phys. Chem. B, 2005, 109, 4197–4208.

H. El-Gezawy, W. Rettig, A. Danel and G. Jonusauskas, Probing the photochemical mechanism in photoactive yellow protein, J. Phys. Chem. B, 2005, 109, 18699–18705.

A. Usman, O. F. Mohammed, K. Heyne, J. Dreyer and E. T. J. Nibbering, Excited state dynamics of a PYP chromophore model system explored with ultrafast infrared spectroscopy, Chem. Phys. Lett., 2005, 401, 157–163.

A. Espagne, P. Changenet-Barret, P. Plaza and M. M. Martin, Solvent effect on the excited-state dynamics of analogues of the photoactive yellow protein chromophore, J. Phys. Chem. A, 2006, 110, 3393–3404.

A. Espagne, D. H. Paik, P. Changenet-Barret, M. M. Martin and A. H. Zewail, Ultrafast photoisomerization of photoactive yellow protein chromophore analogues in solution: Influence of the protonation state, ChemPhysChem, 2006, 7, 1717–1726.

A. Espagne, P. Changenet-Barret, P. Plaza, J.-B. Baudin and M. M. Martin, Photoinduced charge shift as the driving force for the excited-state relaxation of analogues of the photoactive yellow protein chromophore in solution, J. Photochem. Photobiol., A, 2007, 185, 245–252.

I. B. Nielsen, S. Boye-Peronne, M. O. A. El Ghazaly, M. B. Kristensen, S. B. Nielsen and L. H. Andersen, Absorption spectra of photoactive yellow protein chromophores in vacuum, Biophys. J., 2005, 89, 2597–2604.

I.-R. Lee, W. Lee and A. H. Zewail, Primary steps of the photoactive yellow protein: Isolated chromophore dynamics and protein directed function, Proc. Natl. Acad. Sci. USA, 2006, 103, 258–262.

T. Fiebig, C. Z. Wan and A. H. Zewail, Femtosecond charge transfer dynamics of a modified DNA base: 2-aminopurine in complexes with nucleotides, ChemPhysChem, 2002, 3, 781–788.

M. Maroncelli and G. R. Fleming, Picosecond solvation dynamics of coumarin 153: The importance of molecular aspects of solvation, J. Chem. Phys., 1987, 86, 6221–6239.

B. Borucki, H. Otto, T. E. Meyer, M. A. Cusanovich and M. P. Heyn, Sensitive circular dichroism marker for the chromophore environment of photoactive yellow protein: assignment of the 307 and 318 nm bands to the np* transition of the carbonyl, J. Phys. Chem. B, 2005, 109, 629–633.

G. Aulin-Erdtman, R. Sandèn, Spectrographic contributions to lignin Chemistry, Acta Chem. Scand., 1968, 22, 1187–1209.

Y. Maeda, T. Okada and N. Mataga, Photoinduced trans→cis isomerization and intramolecular-charge-transfer interaction. Photochemistry and picosecond laser spectroscopy of 4-substituted β-(1-pyrenyl)styrenes, J. Phys. Chem., 1984, 88, 2714–2718.

F. D. Lewis, J. E. Elbert, A. L. Upthagrove and P. D. Hale, Lewis-acid catalysis of photochemical reactions. 9. Structure and photoisomerization of (E)- and (Z)-cinnamamides and their Lewis acid complexes, J. Org. Chem., 1991, 56, 553–561.

A. M. Brouwer, S. M. Fazio, N. Haraszkiewicz, D. A. Leigh, C. M. Lennon (neé Keaveney), Coumaric amide rotaxanes: effects of hydrogen bonding and mechanical interlocking on the photochemistry and photophysics, Photochem. Photobiol. Sci., 2007, 4, 480–486.

J. Berna, A. M. Brouwer, S. M. Fazio, N. Haraszkiewicz, D. A. Leigh and C. M. Lennon, A rotaxane mimic of the photoactive yellow protein chromophore environment: effects of hydrogen bonding and mechanical interlocking on a coumaric amide derivative, Chem. Commun., 2007, DOI: 10.1039/b618781a.

R. Jimenez, G. R. Fleming, P. V. Kumar and M. Maroncelli, Femtosecond solvation dynamics of water, Nature, 1994, 369, 471–473.

L. L. Premvardhan, F. Buda, M. A. van der Horst, D. C. Lührs, K. J. Hellingwerf, R. van Grondelle, Impact of photon absorption on the electronic properties of p-coumaric acid derivatives of the photoactive yellow protein chromophore, J. Phys. Chem. B, 2004, 108, 5138–5148.

C. Hansch, A. Leo and R. W. Taft, A survey of Hammett substituent constants and resonance and field parameters, Chem. Rev., 1991, 91, 165–195.

R. F. Grote and J. T. Hynes, The stable states picture of chemical reactions. II. Rate, constants for condensed and gas phase reaction models, J. Chem. Phys., 1980, 73, 2715–2732.

R. S. H. Liu and A. E. Asato, The primary process of vision and the structure of bathorhodopsin: A mechanism for photoisomerization of polyenes, Proc. Natl. Acad. Sci. USA, 1985, 82, 259–263.

A. Warshel, Bicycle-pedal model for the first step in the vision process, Nature, 1976, 260, 679–683.

A. Usman, H. Masuhara and T. Asahi, Trans–cis photoisomerization of a photoactive yellow protein model chromophore in crystalline phase, J. Phys. Chem. B, 2006, 110, 20085–20088.

H. Chosrowjan, N. Mataga, N. Nakashima, Y. Imamoto and F. Tokunaga, Femtosecond-picosecond fluorescence studies on excited state dynamics of photoactive yellow protein from Ectothiorhodospira Halophila, Chem. Phys. Lett., 1997, 270, 267–272.

H. Chosrowjan, N. Mataga, Y. Shibata, Y. Imamoto and F. Tokunaga, 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, 1998, 102, 7695–7698.

H. Chosrowjan, S. Taniguchi, N. Mataga, M. Unno, S. Yamauchi, N. Hamada, M. Kumauchi and F. Tokunaga, Low-frequency vibrations and their role in ultrafast photoisomerization reaction dynamics of photoactive yellow protein, J. Phys. Chem. B, 2004, 108, 2686–2698.

N. Mataga, H. Chosrowjan, Y. Shibata, Y. Imamoto and F. Tokunaga, 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, 2000, 104, 5191–5199.

N. Mataga, H. Chosrowjan, Y. Shibata, Y. Imamoto, M. Kataoka and F. Tokunaga, Ultrafast photoinduced reaction dynamics of photoactive yellow protein (PYP): Observation of coherent oscillations in the femtosecond fluorescence decay dynamics, Chem. Phys. Lett., 2002, 352, 220–225.

N. Mataga, H. Chosrowjan, S. Taniguchi, N. Hamada, F. Tokunaga, Y. Imamoto and M. Kataoka, Ultrafast photoreactions in protein nanospaces as revealed by fs fluorescence dynamics measurements on photoactive yellow protein and related systems, Phys. Chem. Chem. Phys., 2003, 5, 2454–2460.

S. Devanathan, S. Lin, M. A. Cusanovich, N. Woodbury and G. Tollin, Early intermediates in the photocycle of the Glu46Gln mutant of photoactive yellow protein: femtosecond spectroscopy, Biophys. J., 2000, 79, 2132–2137.

S. Devanathan, S. Lin, M. A. Cusanovich, N. Woodbury and G. Tollin, Early photocycle kinetic behavior of the E46A and Y42F mutants of photoactive yellow protein: Femtosecond spectroscopy, Biophys. J., 2001, 81, 2314–2319.

P. Changenet-Barret, P. Plaza, M. M. Martin, H. Chosrowjan, S. Taniguchi, N. Mataga, Y. Imamoto and M. Kataoka, Role of arginine 52 on the primary photoinduced events in the PYP photocycle, Chem. Phys. Lett., 2007, 434, 220–225.

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Photochemical & Photobiological Sciences

Tập 6

780-787

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