Watching a signaling protein function: What has been learned over four decades of time-resolved studies of photoactive yellow protein

Schotte, Friedrich; Cho, Hyun Sun; Dyda, Fred; Anfinrud, Philip

doi:10.1063/4.0000241

Watching a signaling protein function: What has been learned over four decades of time-resolved studies of photoactive yellow protein

Journal Article · Mon Apr 08 00:00:00 EDT 2024 · Structural Dynamics

DOI:https://doi.org/10.1063/4.0000241· OSTI ID:2565040

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Photoactive yellow protein (PYP) is a signaling protein whose internal p-coumaric acid chromophore undergoes reversible, light-induced trans-to-cis isomerization, which triggers a sequence of structural changes that ultimately lead to a signaling state. Since its discovery nearly 40 years ago, PYP has attracted much interest and has become one of the most extensively studied proteins found in nature. The method of time-resolved crystallography, pioneered by Keith Moffat, has successfully characterized intermediates in the PYP photocycle at near atomic resolution over 12 decades of time down to the sub-picosecond time scale, allowing one to stitch together a movie and literally watch a protein as it functions. But how close to reality is this movie? To address this question, results from numerous complementary time-resolved techniques including x-ray crystallography, x-ray scattering, and spectroscopy are discussed. Emerging from spectroscopic studies is a general consensus that three time constants are required to model the excited state relaxation, with a highly strained ground-state cis intermediate formed in less than 2.4 ps. Persistent strain drives the sequence of structural transitions that ultimately produce the signaling state. Crystal packing forces produce a restoring force that slows somewhat the rates of interconversion between the intermediates. Moreover, the solvent composition surrounding PYP can influence the number and structures of intermediates as well as the rates at which they interconvert. When chloride is present, the PYP photocycle in a crystal closely tracks that in solution, which suggests the epic movie of the PYP photocycle is indeed based in reality.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357; AC02-06CH11357

OSTI ID:: 2565040

Alternate ID(s):: OSTI ID: 2470209

Journal Information:: Structural Dynamics, Journal Name: Structural Dynamics Journal Issue: 2 Vol. 11; ISSN 2329-7778

Publisher:: American Institute of PhysicsCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila Meyer, T. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 806, Issue 1 https://doi.org/10.1016/0005-2728(85)90094-5	journal	January 1985
Evidence for trans-cis isomerization of the p -coumaric acid chromophore as the photochemical basis of the photocycle of photoactive yellow protein Kort, R.; Vonk, H.; Xu, X. FEBS Letters, Vol. 382, Issue 1-2 https://doi.org/10.1016/0014-5793(96)00149-4	journal	March 1996
Measurement and global analysis of the absorbance changes in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila Hoff, W. D.; van Stokkum, I. H.; van Ramesdonk, H. J. Biophysical Journal, Vol. 67, Issue 4 https://doi.org/10.1016/S0006-3495(94)80643-5	journal	October 1994
New Photocycle Intermediates in the Photoactive Yellow Protein from Ectothiorhodospira halophila: Picosecond Transient Absorption Spectroscopy Ujj, L.; Devanathan, S.; Meyer, T. E. Biophysical Journal, Vol. 75, Issue 1 https://doi.org/10.1016/S0006-3495(98)77525-3	journal	July 1998
Global and target analysis of time-resolved spectra van Stokkum, Ivo H. M.; Larsen, Delmar S.; van Grondelle, Rienk Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1657, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.04.011	journal	July 2004
pH Dependence of the Photoactive Yellow Protein Photocycle Investigated by Time-Resolved Crystallography Tripathi, Shailesh; Šrajer, Vukica; Purwar, Namrta Biophysical Journal, Vol. 102, Issue 2 https://doi.org/10.1016/j.bpj.2011.11.4021	journal	January 2012
Photocycle populations with femtosecond excitation of crystalline photoactive yellow protein Hutchison, Christopher D. M.; Kaucikas, Marius; Tenboer, Jason Chemical Physics Letters, Vol. 654 https://doi.org/10.1016/j.cplett.2016.04.087	journal	June 2016
A Structural Pathway for Signaling in the E46Q Mutant of Photoactive Yellow Protein Rajagopal, Sudarshan; Anderson, Spencer; Srajer, Vukica Structure, Vol. 13, Issue 1 https://doi.org/10.1016/j.str.2004.10.016	journal	January 2005
Excitation-Wavelength-Dependent Photocycle Initiation Dynamics Resolve Heterogeneity in the Photoactive Yellow Protein from Halorhodospira halophila Mix, L. Tyler; Carroll, Elizabeth C.; Morozov, Dmitry Biochemistry, Vol. 57, Issue 11 https://doi.org/10.1021/acs.biochem.7b01114	journal	February 2018
Optical Studies of a Bacterial Photoreceptor Protein, Photoactive Yellow Protein, in Single Crystals Ng, Kingman; Getzoff, Elizabeth D.; Moffat, Keith Biochemistry, Vol. 34, Issue 3 https://doi.org/10.1021/bi00003a022	journal	January 1995
1.4 .ANG. Structure of Photoactive Yellow Protein, a Cytosolic Photoreceptor: Unusual Fold, Active Site, and Chromophore Borgstahl, Gloria E. O.; Williams, DeWight R.; Getzoff, Elizabeth D. Biochemistry, Vol. 34, Issue 19 https://doi.org/10.1021/bi00019a004	journal	May 1995
Complete Chemical Structure of Photoactive Yellow Protein: Novel Thioester-Linked 4-Hydroxycinnamyl Chromophore and Photocycle Chemistry Baca, Manuel; Borgstahl, Gloria E. O.; Boissinot, Maurice Biochemistry, Vol. 33, Issue 48 https://doi.org/10.1021/bi00252a001	journal	December 1994
Properties of a water-soluble, yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin Meyer, T. E.; Yakali, E.; Cusanovich, M. A. Biochemistry, Vol. 26, Issue 2 https://doi.org/10.1021/bi00376a012	journal	January 1987
A Molecular Movie at 1.8 Å Resolution Displays the Photocycle of Photoactive Yellow Protein, a Eubacterial Blue-Light Receptor, from Nanoseconds to Seconds ^† Ren, Zhong; Perman, Benjamin; Šrajer, Vukica Biochemistry, Vol. 40, Issue 46 https://doi.org/10.1021/bi0107142	journal	November 2001
Pump−Dump−Probe Spectroscopy of Bacteriorhodosin: Evidence for a Near-IR Excited State Absorbance Gai, Feng; McDonald, J. Cooper; Anfinrud, Philip A. Journal of the American Chemical Society, Vol. 119, Issue 26 https://doi.org/10.1021/ja9703685	journal	July 1997
Picosecond Photobiology: Watching a Signaling Protein Function in Real Time via Time-Resolved Small- and Wide-Angle X-ray Scattering Cho, Hyun Sun; Schotte, Friedrich; Dashdorj, Naranbaatar Journal of the American Chemical Society, Vol. 138, Issue 28 https://doi.org/10.1021/jacs.6b03565	journal	July 2016
Probing Anisotropic Structure Changes in Proteins with Picosecond Time-Resolved Small-Angle X-ray Scattering Cho, Hyun Sun; Schotte, Friedrich; Dashdorj, Naranbaatar The Journal of Physical Chemistry B, Vol. 117, Issue 49 https://doi.org/10.1021/jp407593j	journal	October 2013
Structure at 0.85 Å resolution of an early protein photocycle intermediate Genick, Ulrich K.; Soltis, S. Michael; Kuhn, Peter Nature, Vol. 392, Issue 6672 https://doi.org/10.1038/32462	journal	March 1998
Volume-conserving trans–cis isomerization pathways in photoactive yellow protein visualized by picosecond X-ray crystallography Jung, Yang Ouk; Lee, Jae Hyuk; Kim, Joonghan Nature Chemistry, Vol. 5, Issue 3 https://doi.org/10.1038/nchem.1565	journal	February 2013
Contradictions in X-ray structures of intermediates in the photocycle of photoactive yellow protein Kaila, Ville R. I.; Schotte, Friedrich; Cho, Hyun Sun Nature Chemistry, Vol. 6, Issue 4 https://doi.org/10.1038/nchem.1898	journal	March 2014
Probing the early stages of photoreception in photoactive yellow protein with ultrafast time-domain Raman spectroscopy Kuramochi, Hikaru; Takeuchi, Satoshi; Yonezawa, Kento Nature Chemistry, Vol. 9, Issue 7 https://doi.org/10.1038/nchem.2717	journal	February 2017
Confinement in crystal lattice alters entire photocycle pathway of the Photoactive Yellow Protein Konold, Patrick E.; Arik, Enis; Weißenborn, Jörn Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18065-9	journal	August 2020
Photoisomerisation quantum yield and non-linear cross-sections with femtosecond excitation of the photoactive yellow protein Lincoln, Craig N.; Fitzpatrick, Ann E.; Thor, Jasper J. van Physical Chemistry Chemical Physics, Vol. 14, Issue 45 https://doi.org/10.1039/c2cp41718a	journal	January 2012
Coherent oscillations in ultrafast fluorescence of photoactive yellow protein Nakamura, Ryosuke; Hamada, Norio; Ichida, Hideki The Journal of Chemical Physics, Vol. 127, Issue 21 https://doi.org/10.1063/1.2802297	journal	December 2007
From The Cover: Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds Ihee, H.; Rajagopal, S.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 102, Issue 20 https://doi.org/10.1073/pnas.0409035102	journal	May 2005
Low-barrier hydrogen bond in photoactive yellow protein Yamaguchi, S.; Kamikubo, H.; Kurihara, K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 2 https://doi.org/10.1073/pnas.0811882106	journal	January 2009
Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography Schotte, F.; Cho, H. S.; Kaila, V. R. I. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1210938109	journal	November 2012
Protein energy landscapes determined by five-dimensional crystallography Schmidt, Marius; Srajer, Vukica; Henning, Robert Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12 https://doi.org/10.1107/S0907444913025997	journal	November 2013
Ultrafast fluorescence upconversion technique and its applications to proteins Chosrowjan, Haik; Taniguchi, Seiji; Tanaka, Fumio The FEBS Journal, Vol. 282, Issue 16 https://doi.org/10.1111/febs.13180	journal	January 2015
Structure of a Protein Photocycle Intermediate by Millisecond Time-Resolved Crystallography Genick, U. K. Science, Vol. 275, Issue 5305 https://doi.org/10.1126/science.275.5305.1471	journal	March 1997
Energy Transduction on the Nanosecond Time Scale: Early Structural Events in a Xanthopsin Photocycle Perman, B. Science, Vol. 279, Issue 5358 https://doi.org/10.1126/science.279.5358.1946	journal	March 1998
Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein Pande, K.; Hutchison, C. D. M.; Groenhof, G. Science, Vol. 352, Issue 6286 https://doi.org/10.1126/science.aad5081	journal	May 2016
The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. Sprenger, W. W.; Hoff, W. D.; Armitage, J. P. Journal of Bacteriology, Vol. 175, Issue 10 https://doi.org/10.1128/jb.175.10.3096-3104.1993	journal	January 1993
Conformational Substates in Proteins Frauenfelder, H.; Parak, F.; Young, R. D. Annual Review of Biophysics and Biophysical Chemistry, Vol. 17, Issue 1 https://doi.org/10.1146/annurev.bb.17.060188.002315	journal	June 1988
Incoherent Manipulation of the Photoactive Yellow Protein Photocycle with Dispersed Pump-Dump-Probe Spectroscopy Larsen, Delmar S.; van Stokkum, Ivo H. M.; Vengris, Mikas Biophysical Journal, Vol. 87, Issue 3 https://doi.org/10.1529/biophysj.104.043794	journal	September 2004
Preparation of Large Crystals of Photoactive Yellow Protein for Neutron Diffraction and High Resolution Crystal Structure Analysis†: Photochemistry and Photobiology, 2007, 83 Yamaguchi, Shigeo; Kamikubo, Hironari; Shimizu, Nobutaka Photochemistry and Photobiology, Vol. 83, Issue 2 https://doi.org/10.1562/2006-07-23-RA-977	journal	February 2007

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