A short history of structure based research on the photocycle of photoactive yellow protein

Schmidt, Marius

doi:10.1063/1.4974172

Title: A short history of structure based research on the photocycle of photoactive yellow protein

Journal Article · Tue Jan 31 00:00:00 EST 2017 · Structural Dynamics

DOI:https://doi.org/10.1063/1.4974172· OSTI ID:1414462

Schmidt, Marius ^[1]

Univ. of Wisconsin, Milwaukee, WI (United States)

The goals of time-resolved macromolecular crystallography are to extract the molecular structures of the reaction intermediates and the reaction dynamics from time-resolved X-ray data alone. To develop the techniques of time-resolved crystallography, biomolecules with special properties are required. The Photoactive Yellow Protein is the most sparkling of these.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Science Foundation (NSF)

Grant/Contract Number:: STC-1231306

OSTI ID:: 1414462

Journal Information:: Structural Dynamics, Vol. 4, Issue 3; ISSN 2329-7778

Publisher:: American Crystallographic Association/AIPCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 19 works

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References (67)

Crystallographic structure of a photoreceptor protein at 2.4 A resolution McRee, D. E.; Tainer, J. A.; Meyer, T. E. Proceedings of the National Academy of Sciences, Vol. 86, Issue 17 https://doi.org/10.1073/pnas.86.17.6533	journal	September 1989
Thiol ester-linked p-coumaric acid as a new photoactive prosthetic group in a protein with rhodopsin-like photochemistry Hoff, W. D.; Dux, P.; Hard, K. Biochemistry, Vol. 33, Issue 47 https://doi.org/10.1021/bi00251a001	journal	November 1994
Protein Conformational Relaxation and Ligand Migration in Myoglobin: A Nanosecond to Millisecond Molecular Movie from Time-Resolved Laue X-ray Diffraction ^† Šrajer, Vukica; Ren, Zhong; Teng, Tsu-Yi Biochemistry, Vol. 40, Issue 46 https://doi.org/10.1021/bi010715u	journal	November 2001
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
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
BioCARS: a synchrotron resource for time-resolved X-ray science Graber, T.; Anderson, S.; Brewer, H. Journal of Synchrotron Radiation, Vol. 18, Issue 4 https://doi.org/10.1107/S0909049511009423	journal	May 2011
Influence of the Crystalline State on Photoinduced Dynamics of Photoactive Yellow Protein Studied by Ultraviolet-Visible Transient Absorption Spectroscopy Yeremenko, Sergey; van Stokkum, Ivo H. M.; Moffat, Keith Biophysical Journal, Vol. 90, Issue 11 https://doi.org/10.1529/biophysj.105.074765	journal	June 2006
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
Room temperature structures beyond 1.5 Å by serial femtosecond crystallography Schmidt, Marius; Pande, Kanupriya; Basu, Shibom Structural Dynamics, Vol. 2, Issue 4 https://doi.org/10.1063/1.4919903	journal	May 2015
Spectroscopic Studies of Model Photo-Receptors: Validation of a Nanosecond Time-Resolved Micro-Spectrophotometer Design Using Photoactive Yellow Protein and α-Phycoerythrocyanin Purwar, Namrta; Tenboer, Jason; Tripathi, Shailesh International Journal of Molecular Sciences, Vol. 14, Issue 9 https://doi.org/10.3390/ijms140918881	journal	September 2013
Chromophore Conformation and the Evolution of Tertiary Structural Changes in Photoactive Yellow Protein Anderson, Spencer; Srajer, Vukica; Pahl, Reinhard Structure, Vol. 12, Issue 6 https://doi.org/10.1016/j.str.2004.04.008	journal	June 2004
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography Boutet, S.; Lomb, L.; Williams, G. J. Science, Vol. 337, Issue 6092 https://doi.org/10.1126/science.1217737	journal	May 2012
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
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
[8] Singular value decomposition: Application to analysis of experimental data Henry, E. R.; Hofrichter, J. Methods in Enzymology https://doi.org/10.1016/0076-6879(92)10010-B	book	January 1992
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
The Solution Structure of a Transient Photoreceptor Intermediate: Δ25 Photoactive Yellow Protein Bernard, Cédric; Houben, Klaartje; Derix, Nocky M. Structure, Vol. 13, Issue 7 https://doi.org/10.1016/j.str.2005.04.017	journal	July 2005
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
Femtosecond Spectroscopic Observations of Initial Intermediates in the Photocycle of the Photoactive Yellow Protein from Ectothiorhodospira halophila Devanathan, Savitha; Pacheco, Andrew; Ujj, Laszlo Biophysical Journal, Vol. 77, Issue 2 https://doi.org/10.1016/S0006-3495(99)76952-3	journal	August 1999
Ligand migration pathway and protein dynamics in myoglobin: A time-resolved crystallographic study on L29W MbCO Schmidt, M.; Nienhaus, K.; Pahl, R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 33 https://doi.org/10.1073/pnas.0504932102	journal	August 2005
Five-dimensional crystallography Schmidt, Marius; Graber, Tim; Henning, Robert Acta Crystallographica Section A Foundations of Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0108767309054166	journal	February 2010
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia Science, Vol. 346, Issue 6214 https://doi.org/10.1126/science.1259357	journal	December 2014
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
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
Protein Structural Dynamics of Photoactive Yellow Protein in Solution Revealed by Pump–Probe X-ray Solution Scattering Kim, Tae Wu; Lee, Jae Hyuk; Choi, Jungkweon Journal of the American Chemical Society, Vol. 134, Issue 6 https://doi.org/10.1021/ja210435n	journal	February 2012
X-ray Laue Diffraction from Protein Crystals Moffat, K.; Szebenyi, D.; Bilderback, D. Science, Vol. 223, Issue 4643 https://doi.org/10.1126/science.223.4643.1423	journal	March 1984
Formation of a New Buried Charge Drives a Large-Amplitude Protein Quake in Photoreceptor Activation ^† Xie, Aihua; Kelemen, Lorand; Hendriks, Johnny Biochemistry, Vol. 40, Issue 6 https://doi.org/10.1021/bi002449a	journal	February 2001
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
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
Observation of Decreased Radiation Damage at Higher Dose Rates in Room Temperature Protein Crystallography Southworth-Davies, Robert J.; Medina, Melissa A.; Carmichael, Ian Structure, Vol. 15, Issue 12 https://doi.org/10.1016/j.str.2007.10.013	journal	December 2007
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
Application of Singular Value Decomposition to the Analysis of Time-Resolved Macromolecular X-Ray Data Schmidt, Marius; Rajagopal, Sudarshan; Ren, Zhong Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/S0006-3495(03)75018-8	journal	March 2003
Photoactivation of the Photoactive Yellow Protein: Why Photon Absorption Triggers a Trans-to-Cis Isomerization of the Chromophore in the Protein Groenhof, Gerrit; Bouxin-Cademartory, Mathieu; Hess, Berk Journal of the American Chemical Society, Vol. 126, Issue 13 https://doi.org/10.1021/ja039557f	journal	April 2004
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
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
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
New software for the singular value decomposition of time-resolved crystallographic data Zhao, Yi; Schmidt, Marius Journal of Applied Crystallography, Vol. 42, Issue 4 https://doi.org/10.1107/S0021889809019050	journal	June 2009
Reply to 'Contradictions in X-ray structures of intermediates in the photocycle of photoactive yellow protein' Jung, Yang Ouk; Lee, Jae Hyuk; Kim, Joonghan Nature Chemistry, Vol. 6, Issue 4 https://doi.org/10.1038/nchem.1897	journal	March 2014
Structural Heterogeneity of Cryotrapped Intermediates in the Bacterial Blue Light Photoreceptor, Photoactive Yellow Protein¶ Anderson, Spencer; Šrajer, Vukica; Moffat, Keith Photochemistry and Photobiology, Vol. 80, Issue 1 https://doi.org/10.1562/2004-03-15-RA-115.1	journal	January 2004
Extended subnanosecond structural dynamics of myoglobin revealed by Laue crystallography Bourgeois, D.; Vallone, B.; Arcovito, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 13 https://doi.org/10.1073/pnas.0508880103	journal	March 2006
Structural and dynamic changes of photoactive yellow protein during its photocycle in solution Rubinstenn, Gilles; Vuister, Geerten W.; Mulder, Frans A. A. Nature Structural Biology, Vol. 5, Issue 7 https://doi.org/10.1038/823	journal	July 1998
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
Short hydrogen bonds in photoactive yellow protein Anderson, Spencer; Crosson, Sean; Moffat, Keith Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 6 https://doi.org/10.1107/S090744490400616X	journal	May 2004
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 Short-Lived Signaling State of the Photoactive Yellow Protein Photoreceptor Revealed by Combined Structural Probes Ramachandran, Pradeep L.; Lovett, Janet E.; Carl, Patrick J. Journal of the American Chemical Society, Vol. 133, Issue 24 https://doi.org/10.1021/ja200617t	journal	June 2011
The Activated Complex in Chemical Reactions Eyring, Henry The Journal of Chemical Physics, Vol. 3, Issue 2 https://doi.org/10.1063/1.1749604	journal	February 1935
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
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
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
Photoactive yellow protein: A structural prototype for the three-dimensional fold of the PAS domain superfamily Pellequer, J. -L.; Wager-Smith, K. A.; Kay, S. A. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.5884	journal	May 1998
Perspective: On the relevance of slower-than-femtosecond time scales in chemical structural-dynamics studies Coppens, Philip Structural Dynamics, Vol. 2, Issue 2 https://doi.org/10.1063/1.4913362	journal	February 2015
A micro-patterned silicon chip as sample holder for macromolecular crystallography experiments with minimal background scattering Roedig, P.; Vartiainen, I.; Duman, R. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep10451	journal	May 2015
Protein kinetics: Structures of intermediates and reaction mechanism from time-resolved x-ray data Schmidt, M.; Pahl, R.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 101, Issue 14 https://doi.org/10.1073/pnas.0305983101	journal	March 2004
Experimental determination of the radiation dose limit for cryocooled protein crystals Owen, R. L.; Rudino-Pinera, E.; Garman, E. F. Proceedings of the National Academy of Sciences, Vol. 103, Issue 13 https://doi.org/10.1073/pnas.0600973103	journal	March 2006
Spectral encoding of x-ray/optical relative delay Bionta, Mina R.; Lemke, H. T.; Cryan, J. P. Optics Express, Vol. 19, Issue 22 https://doi.org/10.1364/OE.19.021855	journal	January 2011
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
Microcrystallization techniques for serial femtosecond crystallography using photosystem II from Thermosynechococcus elongatus as a model system Kupitz, Christopher; Grotjohann, Ingo; Conrad, Chelsie E. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0316	journal	July 2014
The xanthopsins: a new family of eubacterial blue-light photoreceptors. Kort, R.; Hoff, W. D.; Van West, M. The EMBO Journal, Vol. 15, Issue 13 https://doi.org/10.1002/j.1460-2075.1996.tb00685.x	journal	July 1996
Laue crystallography: coming of age Ren, Zhong; Bourgeois, Dominique; Helliwell, John R. Journal of Synchrotron Radiation, Vol. 6, Issue 4 https://doi.org/10.1107/S0909049599006366	journal	July 1999
Photolysis of the Carbon Monoxide Complex of Myoglobin: Nanosecond Time-Resolved Crystallography Srajer, V.; Teng, T. -y.; Ursby, T. Science, Vol. 274, Issue 5293 https://doi.org/10.1126/science.274.5293.1726	journal	December 1996
Chromophore Dynamics in the PYP Photocycle from Femtosecond Stimulated Raman Spectroscopy Creelman, Mark; Kumauchi, Masato; Hoff, Wouter D. The Journal of Physical Chemistry B, Vol. 118, Issue 3 https://doi.org/10.1021/jp408584v	journal	January 2014
Analysis of experimental time-resolved crystallographic data by singular value decomposition Rajagopal, Sudarshan; Schmidt, Marius; Anderson, Spencer Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 5 https://doi.org/10.1107/S0907444904004160	journal	April 2004
PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light Taylor, Barry L.; Zhulin, Igor B. Microbiology and Molecular Biology Reviews, Vol. 63, Issue 2 https://doi.org/10.1128/MMBR.63.2.479-506.1999	journal	June 1999
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
Protein folding thermodynamics applied to the photocycle of the photoactive yellow protein Van Brederode, M. E.; Hoff, W. D.; Van Stokkum, I. H. Biophysical Journal, Vol. 71, Issue 1 https://doi.org/10.1016/s0006-3495(96)79234-2	journal	July 1996
The kinetic dose limit in room-temperature time-resolved macromolecular crystallography Schmidt, M.; Šrajer, V.; Purwar, N. Journal of Synchrotron Radiation, Vol. 19, Issue 2 https://doi.org/10.1107/s090904951105549x	journal	January 2012
Structural Heterogeneity of Cryotrapped Intermediates in the Bacterial Blue Light Photoreceptor, Photoactive Yellow Protein¶ Anderson, Spencer; Šrajer, Vukica; Moffat, Keith Photochemistry and Photobiology, Vol. 80, Issue 1 https://doi.org/10.1111/j.1751-1097.2004.tb00042.x	journal	April 2007

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Title: A short history of structure based research on the photocycle of photoactive yellow protein

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