Electrostatic control of photoisomerization pathways in proteins

Romei, Matthew G.; Lin, Chi-Yun; Mathews, Irimpan I.; Boxer, Steven G.

doi:10.1126/science.aax1898

Title: Electrostatic control of photoisomerization pathways in proteins

Journal Article · 01 January 2020 · Science

DOI: https://doi.org/10.1126/science.aax1898 · OSTI ID:1604560

^[1];

^[2];

^[1]

Stanford Univ., CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Rotation around a specific bond after photoexcitation is central to vision and emerging opportunities in optogenetics, super-resolution microscopy, and photoactive molecular devices. Competing roles for steric and electrostatic effects that govern bond-specific photoisomerization have been widely discussed, the latter originating from chromophore charge transfer upon excitation. We systematically altered the electrostatic properties of the green fluorescent protein chromophore in a photoswitchable variant, Dronpa2, using amber suppression to introduce electron-donating and electron-withdrawing groups to the phenolate ring. Through analysis of the absorption (color), fluorescence quantum yield, and energy barriers to ground- and excited-state isomerization, we evaluate the contributions of sterics and electrostatics quantitatively and demonstrate how electrostatic effects bias the pathway of chromophore photoisomerization, leading to a generalized framework to guide protein design.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1604560

Journal Information:: Science, Journal Name: Science Journal Issue: 6473 Vol. 367; ISSN 0036-8075

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Hydrogen Bond Fluctuations Control Photochromism in a Reversibly Photo-Switchable Fluorescent Protein Morozov, Dmitry; Groenhof, Gerrit Angewandte Chemie, Vol. 128, Issue 2 https://doi.org/10.1002/ange.201508452	journal	November 2015
Hydrogen Bond Fluctuations Control Photochromism in a Reversibly Photo-Switchable Fluorescent Protein Morozov, Dmitry; Groenhof, Gerrit Angewandte Chemie International Edition, Vol. 55, Issue 2 https://doi.org/10.1002/anie.201508452	journal	November 2015
Optogenetics: A Primer for Chemists O'Banion, Colin P.; Lawrence, David S. ChemBioChem, Vol. 19, Issue 12 https://doi.org/10.1002/cbic.201800013	journal	May 2018
Green and Red Fluorescent Proteins: Photo- and Thermally Induced Dynamics Probed by Site-Selective Spectroscopy and Hole Burning Bonsma, S.; Purchase, R.; Jezowski, S. ChemPhysChem, Vol. 6, Issue 5 https://doi.org/10.1002/cphc.200500005	journal	April 2005
The Lineshape of the Electronic Spectrum of the Green Fluorescent Protein Chromophore, Part I: Gas Phase Davari, Mehdi D.; Ferrer, Francisco J. Avila; Morozov, Dmitry ChemPhysChem, Vol. 15, Issue 15 https://doi.org/10.1002/cphc.201402355	journal	September 2014
Reversible photoswitching in fluorescent proteins: A mechanistic view Bourgeois, Dominique; Adam, Virgile IUBMB Life, Vol. 64, Issue 6 https://doi.org/10.1002/iub.1023	journal	April 2012
Room temperature crystal structure of the fast switching M159T mutant of the fluorescent protein dronpa: Structure of M159T Mutant of Dronpa Protein Kaucikas, Marius; Fitzpatrick, Ann; Bryan, Elana Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 3 https://doi.org/10.1002/prot.24742	journal	January 2015
Modern Optical Spectroscopy With Exercises and Examples from Biophysics and Biochemistry Parson, William W. https://doi.org/10.1007/978-3-540-37542-5	book	January 2007
Time-resolved FRET fluorescence spectroscopy of visible fluorescent protein pairs Visser, A. J. W. G.; Laptenok, S. P.; Visser, N. V. European Biophysics Journal, Vol. 39, Issue 2 https://doi.org/10.1007/s00249-009-0528-8	journal	August 2009
A simple procedure for selective inversion of NMR resonances for spin transfer enzyme kinetic measurements Robinson, Gae; Kuchel, Philip W.; Chapman, Bogdan E. Journal of Magnetic Resonance (1969), Vol. 63, Issue 2 https://doi.org/10.1016/0022-2364(85)90321-X	journal	June 1985
Analyzing the Distribution of Decay Constants in Pulse-Fluorimetry Using the Maximum Entropy Method Livesey, A. K.; Brochon, J. C. Biophysical Journal, Vol. 52, Issue 5 https://doi.org/10.1016/S0006-3495(87)83264-2	journal	November 1987
Unified Model for Photophysical and Electro-Optical Properties of Green Fluorescent Proteins Lin, Chi-Yun; Romei, Matthew G.; Oltrogge, Luke M. Biophysical Journal, Vol. 118, Issue 3 https://doi.org/10.1016/j.bpj.2019.11.3283	journal	February 2020
Fluorescence imaging using synthetic GFP chromophores Walker, Christopher L.; Lukyanov, Konstantin A.; Yampolsky, Ilia V. Current Opinion in Chemical Biology, Vol. 27 https://doi.org/10.1016/j.cbpa.2015.06.002	journal	August 2015
Electrostatic control of photoisomerization in the photoactive yellow protein chromophore: Ab initio multiple spawning dynamics Ko, Chaehyuk; Virshup, Aaron M.; Martínez, Todd J. Chemical Physics Letters, Vol. 460, Issue 1-3 https://doi.org/10.1016/j.cplett.2008.05.029	journal	July 2008
Mean fluorescence lifetime and its error Fišerová, Eva; Kubala, Martin Journal of Luminescence, Vol. 132, Issue 8 https://doi.org/10.1016/j.jlumin.2012.03.038	journal	August 2012
NMR studies of enzymatic rates in vitro and in vivo by magnetization transfer Alger, J. R.; Shulman, R. G. Quarterly Reviews of Biophysics, Vol. 17, Issue 1 https://doi.org/10.1017/S0033583500005266	journal	February 1984
Increasing Enzyme Stability and Activity through Hydrogen Bond-Enhanced Halogen Bonds Carlsson, Anna-Carin C.; Scholfield, Matthew R.; Rowe, Rhianon K. Biochemistry, Vol. 57, Issue 28 https://doi.org/10.1021/acs.biochem.8b00603	journal	June 2018
Photoinduced Chemistry in Fluorescent Proteins: Curse or Blessing? Acharya, Atanu; Bogdanov, Alexey M.; Grigorenko, Bella L. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00238	journal	March 2016
Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores Gozem, Samer; Luk, Hoi Ling; Schapiro, Igor Chemical Reviews, Vol. 117, Issue 22 https://doi.org/10.1021/acs.chemrev.7b00177	journal	October 2017
Systematic Excited State Studies of Reversibly Switchable Fluorescent Proteins Smyrnova, Daryna; Marín, María del Carmen; Olivucci, Massimo Journal of Chemical Theory and Computation, Vol. 14, Issue 6 https://doi.org/10.1021/acs.jctc.8b00050	journal	May 2018
Electrostatic Influence on Photoisomerization in Bacteriorhodopsin and Halorhodopsin Punwong, C.; Hannongbua, S.; Martínez, T. J. The Journal of Physical Chemistry B, Vol. 123, Issue 23 https://doi.org/10.1021/acs.jpcb.9b01837	journal	May 2019
Quantifying Microsecond Transition Times Using Fluorescence Lifetime Correlation Spectroscopy Ghosh, Arindam; Isbaner, Sebastian; Veiga-Gutiérrez, Manoel The Journal of Physical Chemistry Letters, Vol. 8, Issue 24 https://doi.org/10.1021/acs.jpclett.7b02707	journal	December 2017
Ground-State Destabilization by Phe-448 and Phe-449 Contributes to Tyrosine Phenol-Lyase Catalysis Phillips, Robert S.; Vita, Andrew; Spivey, J. Blaine ACS Catalysis, Vol. 6, Issue 10 https://doi.org/10.1021/acscatal.6b01495	journal	September 2016
Short Hydrogen Bonds and Proton Delocalization in Green Fluorescent Protein (GFP) Oltrogge, Luke M.; Boxer, Steven G. ACS Central Science, Vol. 1, Issue 3 https://doi.org/10.1021/acscentsci.5b00160	journal	June 2015
Structural and Spectral Response of Aequorea victoria Green Fluorescent Proteins to Chromophore Fluorination ^† Pal, Prajna P.; Bae, Jae Hyun; Azim, M. Kamran Biochemistry, Vol. 44, Issue 10 https://doi.org/10.1021/bi0484825	journal	March 2005
A Versatile Platform for Single- and Multiple-Unnatural Amino Acid Mutagenesis in Escherichia coli Chatterjee, Abhishek; Sun, Sophie B.; Furman, Jennifer L. Biochemistry, Vol. 52, Issue 10 https://doi.org/10.1021/bi4000244	journal	February 2013
Structural Basis of Improved Second-Generation 3-Nitro-tyrosine tRNA Synthetases Cooley, Richard B.; Feldman, Jessica L.; Driggers, Camden M. Biochemistry, Vol. 53, Issue 12 https://doi.org/10.1021/bi5001239	journal	March 2014
Ground-State Proton Transfer Kinetics in Green Fluorescent Protein Oltrogge, Luke M.; Wang, Quan; Boxer, Steven G. Biochemistry, Vol. 53, Issue 37 https://doi.org/10.1021/bi500147n	journal	September 2014
Slow Exchange in the Chromophore of a Green Fluorescent Protein Variant Seifert, Markus H. J.; Ksiazek, Dorota; Azim, M. Kamran Journal of the American Chemical Society, Vol. 124, Issue 27 https://doi.org/10.1021/ja0257725	journal	July 2002
Origin, Nature, and Fate of the Fluorescent State of the Green Fluorescent Protein Chromophore at the CASPT2//CASSCF Resolution Martin, María Elena; Negri, Fabrizia; Olivucci, Massimo Journal of the American Chemical Society, Vol. 126, Issue 17 https://doi.org/10.1021/ja037278m	journal	May 2004
¹⁹ F NMR Studies of the Native and Denatured States of Green Fluorescent Protein Khan, Farid; Kuprov, Ilya; Craggs, Timothy D. Journal of the American Chemical Society, Vol. 128, Issue 33 https://doi.org/10.1021/ja060618u	journal	August 2006
A Stroboscopic Approach for Fast Photoactivation−Localization Microscopy with Dronpa Mutants Flors, Cristina; Hotta, Jun-ichi; Uji-i, Hiroshi Journal of the American Chemical Society, Vol. 129, Issue 45 https://doi.org/10.1021/ja074704l	journal	November 2007
Incorporation of Fluorotyrosines into Ribonucleotide Reductase Using an Evolved, Polyspecific Aminoacyl-tRNA Synthetase Minnihan, Ellen C.; Young, Douglas D.; Schultz, Peter G. Journal of the American Chemical Society, Vol. 133, Issue 40 https://doi.org/10.1021/ja207719f	journal	October 2011
Synthetic Control of Retinal Photochemistry and Photophysics in Solution Bassolino, Giovanni; Sovdat, Tina; Liebel, Matz Journal of the American Chemical Society, Vol. 136, Issue 6 https://doi.org/10.1021/ja4121814	journal	January 2014
Significant Expansion of Fluorescent Protein Sensing Ability through the Genetic Incorporation of Superior Photo-Induced Electron-Transfer Quenchers Liu, Xiaohong; Jiang, Li; Li, Jiasong Journal of the American Chemical Society, Vol. 136, Issue 38 https://doi.org/10.1021/ja505219r	journal	September 2014
Synthetic Control of Green Fluorescent Protein Kent, Kevin P.; Oltrogge, Luke M.; Boxer, Steven G. Journal of the American Chemical Society, Vol. 131, Issue 44 https://doi.org/10.1021/ja906303f	journal	November 2009
Protonic Gating of Excited-State Twisting and Charge Localization in GFP Chromophores: A Mechanistic Hypothesis for Reversible Photoswitching Olsen, Seth; Lamothe, Kristina; Martínez, Todd J. Journal of the American Chemical Society, Vol. 132, Issue 4 https://doi.org/10.1021/ja907447k	journal	February 2010
Mechanism of the AppA _BLUF Photocycle Probed by Site-Specific Incorporation of Fluorotyrosine Residues: Effect of the Y21 p K _a on the Forward and Reverse Ground-State Reactions Gil, Agnieszka A.; Haigney, Allison; Laptenok, Sergey P. Journal of the American Chemical Society, Vol. 138, Issue 3 https://doi.org/10.1021/jacs.5b11115	journal	January 2016
Temperature Independence of Ultrafast Photoisomerization in Thermophilic Rhodopsin: Assessment versus Other Microbial Proton Pumps Iyer, E. Siva Subramaniam; Misra, Ramprasad; Maity, Arnab Journal of the American Chemical Society, Vol. 138, Issue 38 https://doi.org/10.1021/jacs.6b05002	journal	September 2016
Electric Field Keeps Chromophore Planar and Produces High Yield Fluorescence in Green Fluorescent Protein Park, Jae Woo; Rhee, Young Min Journal of the American Chemical Society, Vol. 138, Issue 41 https://doi.org/10.1021/jacs.6b06833	journal	October 2016
A Long-Lived Triplet State Is the Entrance Gateway to Oxidative Photochemistry in Green Fluorescent Proteins Byrdin, Martin; Duan, Chenxi; Bourgeois, Dominique Journal of the American Chemical Society, Vol. 140, Issue 8 https://doi.org/10.1021/jacs.7b12755	journal	February 2018
Fluorescence Enhancement of a Microbial Rhodopsin via Electronic Reprogramming Marín, María del Carmen; Agathangelou, Damianos; Orozco-Gonzalez, Yoelvis Journal of the American Chemical Society, Vol. 141, Issue 1 https://doi.org/10.1021/jacs.8b09311	journal	November 2018
Unified Model for Photophysical and Electro-Optical Properties of Green Fluorescent Proteins Lin, Chi-Yun; Romei, Matthew G.; Oltrogge, Luke M. Journal of the American Chemical Society, Vol. 141, Issue 38 https://doi.org/10.1021/jacs.9b07152	journal	August 2019
Excited-State Dynamics in the Enhanced Green Fluorescent Protein Mutant Probed by Picosecond Time-Resolved Single Photon Counting Spectroscopy Cotlet, Mircea; Hofkens, Johan; Maus, Michael The Journal of Physical Chemistry B, Vol. 105, Issue 21 https://doi.org/10.1021/jp003813i	journal	May 2001
The Hammett Relationship and Reactions in the Excited Electronic State: Hemithioindigo Z / E -Photoisomerization Cordes, Thorben; Schadendorf, Torsten; Priewisch, Beate The Journal of Physical Chemistry A, Vol. 112, Issue 4 https://doi.org/10.1021/jp077472l	journal	January 2008
Effects of Modification of Protein Nanospace Structure and Change of Temperature on the Femtosecond to Picosecond Fluorescence Dynamics of Photoactive Yellow Protein Mataga, Noboru; Chosrowjan, Haik; Shibata, Yutaka The Journal of Physical Chemistry B, Vol. 104, Issue 21 https://doi.org/10.1021/jp994205+	journal	May 2000
Dual-Label STED Nanoscopy of Living Cells Using Photochromism Willig, Katrin I.; Stiel, Andre C.; Brakemann, Tanja Nano Letters, Vol. 11, Issue 9 https://doi.org/10.1021/nl202290w	journal	September 2011
Site-specific incorporation of fluorotyrosines into the R2 subunit of E. coli ribonucleotide reductase by expressed protein ligation Seyedsayamdost, Mohammad R.; Yee, Cyril S.; Stubbe, JoAnne Nature Protocols, Vol. 2, Issue 5 https://doi.org/10.1038/nprot.2007.159	journal	May 2007
Relative and absolute determination of fluorescence quantum yields of transparent samples Würth, Christian; Grabolle, Markus; Pauli, Jutta Nature Protocols, Vol. 8, Issue 8 https://doi.org/10.1038/nprot.2013.087	journal	July 2013
Designing logical codon reassignment – Expanding the chemistry in biology Dumas, Anaëlle; Lercher, Lukas; Spicer, Christopher D. Chemical Science, Vol. 6, Issue 1 https://doi.org/10.1039/C4SC01534G	journal	January 2015
Improved maximum entropy method for the analysis of fluorescence spectroscopy data: evaluating zero-time shift and assessing its effect on the determination of fluorescence lifetimes Esposito, Rosario; Mensitieri, Giuseppe; de Nicola, Sergio The Analyst, Vol. 140, Issue 24 https://doi.org/10.1039/C5AN01811K	journal	January 2015
Significant improvement of oxidase activity through the genetic incorporation of a redox-active unnatural amino acid Yu, Yang; Zhou, Qing; Wang, Li Chemical Science, Vol. 6, Issue 7 https://doi.org/10.1039/C5SC01126D	journal	January 2015
Low-temperature switching by photoinduced protonation in photochromic fluorescent proteins Faro, Aline Regis; Adam, Virgile; Carpentier, Philippe Photochemical & Photobiological Sciences, Vol. 9, Issue 2 https://doi.org/10.1039/b9pp00121b	journal	January 2010
Photoswitching of E222Q GFP mutants: “concerted” mechanism of chromophore isomerization and protonation Abbruzzetti, Stefania; Bizzarri, Ranieri; Luin, Stefano Photochemical & Photobiological Sciences, Vol. 9, Issue 10 https://doi.org/10.1039/c0pp00189a	journal	January 2010
Estimation of kinetic parameters from time-resolved fluorescence data: A compressed sensing approach Groma, Géza I.; Heiner, Zsuzsanna; Makai, András RSC Advances, Vol. 2, Issue 30 https://doi.org/10.1039/c2ra21773b	journal	January 2012
Ultrafast dual photoresponse of isolated biological chromophores: link to the photoinduced mode-specific non-adiabatic dynamics in proteins Bochenkova, Anastasia V.; Andersen, Lars H. Faraday Discussions, Vol. 163 https://doi.org/10.1039/c3fd20150c	journal	January 2013
Molecular mechanics and molecular shape. Part 4. Size, shape, and steric parameters Meyer, Amatzya Y. Journal of the Chemical Society, Perkin Transactions 2, Issue 10 https://doi.org/10.1039/p29860001567	journal	January 1986
1.8 Å bright-state structure of the reversibly switchable fluorescent protein Dronpa guides the generation of fast switching variants Stiel, Andre C.; Trowitzsch, Simon; Weber, Gert Biochemical Journal, Vol. 402, Issue 1 https://doi.org/10.1042/BJ20061401	journal	January 2007
Reaction Rates by Nuclear Magnetic Resonance McConnell, Harden M. The Journal of Chemical Physics, Vol. 28, Issue 3 https://doi.org/10.1063/1.1744152	journal	March 1958
A diabatic three-state representation of photoisomerization in the green fluorescent protein chromophore Olsen, Seth; McKenzie, Ross H. The Journal of Chemical Physics, Vol. 130, Issue 18 https://doi.org/10.1063/1.3121324	journal	January 2009
Structural basis for reversible photoswitching in Dronpa Andresen, M.; Stiel, A. C.; Trowitzsch, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 32 https://doi.org/10.1073/pnas.0700629104	journal	July 2007
Spectral tuning in photoactive yellow protein by modulation of the shape of the excited state energy surface Philip, A. F.; Nome, R. A.; Papadantonakis, G. A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 13 https://doi.org/10.1073/pnas.0903092107	journal	March 2010
Protein-induced photophysical changes to the amyloid indicator dye thioflavin T Wolfe, L. S.; Calabrese, M. F.; Nath, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 39 https://doi.org/10.1073/pnas.1002867107	journal	September 2010
Mechanism and bottlenecks in strand photodissociation of split green fluorescent proteins (GFPs) Lin, Chi-Yun; Both, Johan; Do, Keunbong Proceedings of the National Academy of Sciences, Vol. 114, Issue 11 https://doi.org/10.1073/pnas.1618087114	journal	February 2017
The invasin D protein from Yersinia pseudotuberculosis selectively binds the Fab region of host antibodies and affects colonization of the intestine Sadana, Pooja; Geyer, Rebecca; Pezoldt, Joern Journal of Biological Chemistry, Vol. 293, Issue 22 https://doi.org/10.1074/jbc.RA117.001068	journal	March 2018
The energy gap law for radiationless transitions in large molecules Englman, Robert; Jortner, Joshua Molecular Physics, Vol. 18, Issue 2 https://doi.org/10.1080/00268977000100171	journal	February 1970
Analysis of time-correlated single photon counting data: a comparative evaluation of deterministic and probabilistic approaches Smith, Darren A.; McKenzie, Grant; Jones, Anita C. Methods and Applications in Fluorescence, Vol. 5, Issue 4 https://doi.org/10.1088/2050-6120/aa8055	journal	October 2017
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Solvent Dependence of the Fluorescence Lifetimes of Xanthene Dyes Magde, Douglas; Rojas, Gail E.; Seybold, Paul G. Photochemistry and Photobiology, Vol. 70, Issue 5 https://doi.org/10.1111/j.1751-1097.1999.tb08277.x	journal	November 1999
Probing the Ultrafast Charge Translocation of Photoexcited Retinal in Bacteriorhodopsin Schenkl, S. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1111482	journal	August 2005
The Molecular Mechanism of Thermal Noise in Rod Photoreceptors Gozem, S.; Schapiro, I.; Ferre, N. Science, Vol. 337, Issue 6099 https://doi.org/10.1126/science.1220461	journal	September 2012
A Unified Description of Linear and Nonlinear Polarization in Organic Polymethine Dyes Marder, S. R.; Gorman, C. B.; Meyers, F. Science, Vol. 265, Issue 5172 https://doi.org/10.1126/science.265.5172.632	journal	July 1994
Use of 19F NMR to Probe Protein Structure and Conformational Changes Danielson, M. A.; Falke, J. J. Annual Review of Biophysics and Biomolecular Structure, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.bb.25.060196.001115	journal	June 1996
The Green Fluorescent Protein Tsien, Roger Y. Annual Review of Biochemistry, Vol. 67, Issue 1, p. 509-544 https://doi.org/10.1146/annurev.biochem.67.1.509	journal	June 1998
The Photophysics of Green Fluorescent Protein: Influence of the Key Amino Acids at Positions 65, 203, and 222 Jung, Gregor; Wiehler, Jens; Zumbusch, Andreas Biophysical Journal, Vol. 88, Issue 3 https://doi.org/10.1529/biophysj.104.044412	journal	March 2005
The Role of the Protein Matrix in Green Fluorescent Protein Fluorescence Maddalo, Scott L.; Zimmer, Marc Photochemistry and Photobiology, Vol. 82, Issue 2 https://doi.org/10.1562/2005-04-11-RA-485	journal	January 2006
Measurement of the fluorescence quantum yield using a spectrometer with an integrating sphere detector Gaigalas, Adolfas K.; Wang, Lili Journal of Research of the National Institute of Standards and Technology, Vol. 113, Issue 1 https://doi.org/10.6028/jres.113.004	journal	January 2008

Similar Records

Retinal Photoisomerization in Rhodopsin: Electrostatic and Steric Catalysis

Journal Article · 2007 · AIP Conference Proceedings · OSTI ID:21043544

Tomasello, Gaia; Altoe, Piero; Stenta, Marco; +3 more

Mimicking Microbial Rhodopsin Isomerization in a Single Crystal

Journal Article · 2018 · Journal of the American Chemical Society · OSTI ID:1544875

Ghanbarpour, Alireza; Nairat, Muath; Nosrati, Meisam; +5 more

Electrostatic Influence on Photoisomerization in Bacteriorhodopsin and Halorhodopsin

Journal Article · 2019 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1547066

Punwong, Chutintorn; Hannongbua, Supot; Martínez, Todd J.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Electrostatic control of photoisomerization pathways in proteins

Citation Formats

References (79)

Similar Records

Related Subjects