OH cleavage from tyrosine: debunking a myth

Bury, Charles S.; Carmichael, Ian; Garman, Elspeth F.

doi:10.1107/S1600577516016775

OH cleavage from tyrosine: debunking a myth

Journal Article · Sat Dec 31 23:00:00 EST 2016 · Journal of Synchrotron Radiation (Online)

DOI:https://doi.org/10.1107/S1600577516016775· OSTI ID:1427170

Bury, Charles S. ^[1]; Carmichael, Ian ^[2]; Garman, Elspeth F. ^[3]

Univ. of Oxford (United Kingdom). Lab. of Molecular Biophysics; University of Oxford
Univ. of Notre Dame, IN (United States). Radiation Lab.
Univ. of Oxford (United Kingdom). Lab. of Molecular Biophysics

During macromolecular X-ray crystallography experiments, protein crystals held at 100 K have been widely reported to exhibit reproducible bond scission events at doses on the order of several MGy. With the objective to mitigate the impact of radiation damage events on valid structure determination, it is essential to correctly understand the radiation chemistry mechanisms at play. OH-cleavage from tyrosine residues is regularly cited as amongst the most available damage pathways in protein crystals at 100 K, despite a lack of widespread reports of this phenomenon in protein crystal radiation damage studies. Furthermore, no clear mechanism for phenolic C—O bond cleavage in tyrosine has been reported, with the tyrosyl radical known to be relatively robust and long-lived in both aqueous solutions and the solid state. Here, the initial findings of Tyr –OH group damage in a myrosinase protein crystal have been reviewed. Consistent with that study, at increasing doses, clear electron density loss was detectable local to Tyr –OH groups. A systematic investigation performed on a range of protein crystal damage series deposited in the Protein Data Bank has established that Tyr –OH electron density loss is not generally a dominant damage pathway in protein crystals at 100 K. Full Tyr aromatic ring displacement is here proposed to account for instances of observable Tyr –OH electron density loss, with the original myrosinase data shown to be consistent with such a damage model. Also presented are systematic analysis of the effects of other environmental factors, including solvent accessibility and proximity to disulfide bonds or hydrogen bond interactions. Residues in known active sites showed enhanced sensitivity to radiation-induced disordering, as has previously been reported.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Notre Dame, IN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); Engineering and Physical Sciences Research Council (EPSRC); Univ. of Oxford (United Kingdom)

Grant/Contract Number:: FC02-04ER15533

OSTI ID:: 1427170

Alternate ID(s):: OSTI ID: 22735824

Journal Information:: Journal of Synchrotron Radiation (Online), Journal Name: Journal of Synchrotron Radiation (Online) Journal Issue: 1 Vol. 24; ISSN 1600-5775; ISSN JSYRES

Publisher:: International Union of CrystallographyCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Automated electron-density sampling reveals widespread conformational polymorphism in proteins: Electron-density Sampling Detects Hidden Ensembles Lang, P. Therese; Ng, Ho-Leung; Fraser, James S. Protein Science, Vol. 19, Issue 7 https://doi.org/10.1002/pro.423	journal	May 2010
The ‘fingerprint’ that X-rays can leave on structures Ravelli, Raimond BG; McSweeney, Sean M. Structure, Vol. 8, Issue 3 https://doi.org/10.1016/S0969-2126(00)00109-X	journal	March 2000
The crystal structures of Sinapis alba myrosinase and a covalent glycosyl–enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase Burmeister, Wim P.; Cottaz, Sylvain; Driguez, Hugues Structure, Vol. 5, Issue 5 https://doi.org/10.1016/S0969-2126(97)00221-9	journal	May 1997
Prostaglandin H synthase: Resolved and unresolved mechanistic issues Tsai, Ah-Lim; Kulmacz, Richard J. Archives of Biochemistry and Biophysics, Vol. 493, Issue 1 https://doi.org/10.1016/j.abb.2009.08.019	journal	January 2010
Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease Schöneich, Christian Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1703, Issue 2 https://doi.org/10.1016/j.bbapap.2004.09.009	journal	January 2005
Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in Photosystem II Rappaport, F.; Diner, B. Coordination Chemistry Reviews, Vol. 252, Issue 3-4 https://doi.org/10.1016/j.ccr.2007.07.016	journal	February 2008
An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy Howells, M. R.; Beetz, T.; Chapman, H. N. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.10.008	journal	March 2009
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
Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range Proton-Coupled Electron Transfer? Stubbe, JoAnne; Nocera, Daniel G.; Yee, Cyril S. Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr020421u	journal	June 2003
Free Radical Catalysis by Galactose Oxidase Whittaker, James W. Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr020425z	journal	June 2003
Proton-Coupled Electron Transfer in Cytochrome Oxidase Kaila, Ville R. I.; Verkhovsky, Michael I.; Wikström, Mårten Chemical Reviews, Vol. 110, Issue 12 https://doi.org/10.1021/cr1002003	journal	December 2010
Thermochemistry and kinetics of sulfur-containing molecules and radicals Benson, Sidney W. Chemical Reviews, Vol. 78, Issue 1 https://doi.org/10.1021/cr60311a003	journal	February 1978
Reactivity of hydroxyl with tyrosine in aqueous solution studied by pulse radiolysis Solar, S.; Solar, W.; Getoff, N. The Journal of Physical Chemistry, Vol. 88, Issue 10 https://doi.org/10.1021/j150654a030	journal	May 1984
Evidence for β Scission in the Oxidation of Amino Acids Wisniowski, Pawel; Carmichael, Ian; Fessenden, Richard W. The Journal of Physical Chemistry A, Vol. 106, Issue 18 https://doi.org/10.1021/jp0139383	journal	May 2002
Soft X-ray Induced Decomposition of Phenylalanine and Tyrosine: A Comparative Study Zubavichus, Yan; Zharnikov, Michael; Shaporenko, Andrey The Journal of Physical Chemistry A, Vol. 108, Issue 20 https://doi.org/10.1021/jp049376f	journal	May 2004
Structure and mobility of electron gain and loss centres in proteins Jones, George D. D.; Lea, Jeremy S.; Symons, Martyn C. R. Nature, Vol. 330, Issue 6150 https://doi.org/10.1038/330772a0	journal	December 1987
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
Predicting the X-ray lifetime of protein crystals Zeldin, O. B.; Brockhauser, S.; Bremridge, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 51 https://doi.org/10.1073/pnas.1315879110	journal	December 2013
Electron spin Resonance of an Irradiated Single Crystal of L-Tyrosine-Hcl Fasanella, E. L.; Gordy, W. Proceedings of the National Academy of Sciences, Vol. 62, Issue 2 https://doi.org/10.1073/pnas.62.2.299	journal	February 1969
Specific chemical and structural damage to proteins produced by synchrotron radiation Weik, M.; Ravelli, R. B. G.; Kryger, G. Proceedings of the National Academy of Sciences, Vol. 97, Issue 2 https://doi.org/10.1073/pnas.97.2.623	journal	January 2000
High Resolution X-ray Crystallography Shows That Ascorbate Is a Cofactor for Myrosinase and Substitutes for the Function of the Catalytic Base Burmeister, Wilhelm Pascal; Cottaz, Sylvain; Rollin, Patrick Journal of Biological Chemistry, Vol. 275, Issue 50 https://doi.org/10.1074/jbc.M006796200	journal	September 2000
Cryo-protection of protein crystals against radiation damage in electron and X-ray diffraction Henderson, Richard Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 241, Issue 1300, p. 6-8 https://doi.org/10.1098/rspb.1990.0057	journal	July 1990
X-ray absorption by macromolecular crystals: the effects of wavelength and crystal composition on absorbed dose Murray, James W.; Garman, Elspeth F.; Ravelli, Raimond B. G. Journal of Applied Crystallography, Vol. 37, Issue 4 https://doi.org/10.1107/S0021889804010660	journal	July 2004
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
RADDOSE-3D : time- and space-resolved modelling of dose in macromolecular crystallography Zeldin, Oliver B.; Gerstel, Markus; Garman, Elspeth F. Journal of Applied Crystallography, Vol. 46, Issue 4 https://doi.org/10.1107/S0021889813011461	journal	June 2013
Crystallographic fast Fourier transforms Ten Eyck, L. F. Acta Crystallographica Section A, Vol. 29, Issue 2 https://doi.org/10.1107/S0567739473000458	journal	March 1973
Improving radiation-damage substructures for RIP Nanao, Max H.; Sheldrick, George M.; Ravelli, Raimond B. G. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 9 https://doi.org/10.1107/S0907444905019360	journal	August 2005
Photoreduction of the active site of the metalloprotein putidaredoxin by synchrotron radiation Corbett, Mary C.; Latimer, Matthew J.; Poulos, Thomas L. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 9 https://doi.org/10.1107/S0907444907035160	journal	August 2007
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
Know your dose: RADDOSE Paithankar, Karthik S.; Garman, Elspeth F. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910006724	journal	March 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Radiation damage in macromolecular crystallography: what is it and why should we care? Garman, Elspeth F. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910008656	journal	March 2010
X-ray-induced deterioration of disulfide bridges at atomic resolution Petrova, Tatiana; Ginell, Stephan; Mitschler, Andre Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 10 https://doi.org/10.1107/S0907444910033986	journal	September 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Statistical quality indicators for electron-density maps Tickle, Ian J. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444911035918	journal	March 2012
Outrunning free radicals in room-temperature macromolecular crystallography Owen, Robin L.; Axford, Danny; Nettleship, Joanne E. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7 https://doi.org/10.1107/S0907444912012553	journal	June 2012
Insights into the mechanism of X-ray-induced disulfide-bond cleavage in lysozyme crystals based on EPR, optical absorption and X-ray diffraction studies Sutton, Kristin A.; Black, Paul J.; Mercer, Kermit R. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12 https://doi.org/10.1107/S0907444913022117	journal	November 2013
Structural changes in a cryo-cooled protein crystal owing to radiation damage Burmeister, Wilhelm Pascal Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 3 https://doi.org/10.1107/S0907444999016261	journal	March 2000
Evidence for the formation of disulfide radicals in protein crystals upon X-ray irradiation Weik, Martin; Bergès, Jacqueline; Raves, Maria L. Journal of Synchrotron Radiation, Vol. 9, Issue 6 https://doi.org/10.1107/S0909049502014589	journal	November 2002
Investigation of possible free-radical scavengers and metrics for radiation damage in protein cryocrystallography Murray, James; Garman, Elspeth Journal of Synchrotron Radiation, Vol. 9, Issue 6 https://doi.org/10.1107/S0909049502014632	journal	November 2002
Specific radiation damage to acidic residues and its relation to their chemical and structural environment Fioravanti, Emanuela; Vellieux, Frédéric M. D.; Amara, Patricia Journal of Synchrotron Radiation, Vol. 14, Issue 1 https://doi.org/10.1107/S0909049506038623	journal	December 2006
Absorbed dose calculations for macromolecular crystals: improvements to RADDOSE Paithankar, Karthik S.; Owen, Robin Leslie; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 16, Issue 2 https://doi.org/10.1107/S0909049508040430	journal	February 2009
A beginner's guide to radiation damage Holton, James M. Journal of Synchrotron Radiation, Vol. 16, Issue 2 https://doi.org/10.1107/S0909049509004361	journal	February 2009
Effective scavenging at cryotemperatures: further increasing the dose tolerance of protein crystals De la Mora, Eugenio; Carmichael, Ian; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511007163	journal	April 2011
Similarities and differences in radiation damage at 100 K versus 160 K in a crystal of thermolysin Juers, Douglas H.; Weik, Martin Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511007631	journal	April 2011
Radiation damage to nucleoprotein complexes in macromolecular crystallography Bury, Charles; Garman, Elspeth F.; Ginn, Helen Mary Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577514026289	journal	January 2015
Identifying and quantifying radiation damage at the atomic level Gerstel, Markus; Deane, Charlotte M.; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577515002131	journal	February 2015
Radiation damage to macromolecules: kill or cure? Garman, Elspeth F.; Weik, Martin Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S160057751500380X	journal	February 2015
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
DIALS – a toolbox for diffraction data analysis Fuentes-Montero, Luis; Parkhurst, James; Winter, Graeme Acta Crystallographica Section A Foundations and Advances, Vol. 70, Issue a1 https://doi.org/10.1107/S2053273314085593	journal	August 2014
Radiation damage and derivatization in macromolecular crystallography: a structure factor's perspective Owen, Robin L.; Sherrell, Darren A. Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 3 https://doi.org/10.1107/S2059798315021555	journal	March 2016
RNA protects a nucleoprotein complex against radiation damage Bury, Charles S.; McGeehan, John E.; Antson, Alfred A. Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 5 https://doi.org/10.1107/S2059798316003351	journal	April 2016
Strain relief at the active site of phosphoserine aminotransferase induced by radiation damage Dubnovitsky, Anatoly P.; Ravelli, Raimond B. G.; Popov, Alexander N. Protein Science, Vol. 14, Issue 6 https://doi.org/10.1110/ps.051397905	journal	June 2005
Radiation Chemical Reactions in Aqueous Solutions of Methionine and Its Peptides Kopoldová, J.; Liebster, J.; Gross, E. Radiation Research, Vol. 30, Issue 2 https://doi.org/10.2307/3572051	journal	February 1967
Pulse Radiolysis of Phenylalanine and Tyrosine Chrysochoos, J. Radiation Research, Vol. 33, Issue 3 https://doi.org/10.2307/3572404	journal	March 1968
Exploring oxidative modifications of tyrosine: An update on mechanisms of formation, advances in analysis and biological consequences Houée-Lévin, C.; Bobrowski, K.; Horakova, L. Free Radical Research, Vol. 49, Issue 4 https://doi.org/10.3109/10715762.2015.1007968	journal	March 2015

Cited By (15)

Direct Radiation Effects on the Structure and Stability of Collagen and Other Proteins Lalande, Mathieu; Schwob, Lucas; Vizcaino, Violaine ChemBioChem, Vol. 20, Issue 24 https://doi.org/10.1002/cbic.201900202	journal	August 2019
Atomic displacement parameters in structural biology Carugo, Oliviero Amino Acids, Vol. 50, Issue 7 https://doi.org/10.1007/s00726-018-2574-y	journal	May 2018
RIDL : a tool to investigate radiation-induced density loss Bury, Charles Simon; Garman, Elspeth Frances Journal of Applied Crystallography, Vol. 51, Issue 3 https://doi.org/10.1107/s1600576718005241	journal	May 2018
Real-space analysis of radiation-induced specific changes with independent component analysis Borek, Dominika; Bromberg, Raquel; Hattne, Johan Journal of Synchrotron Radiation, Vol. 25, Issue 2 https://doi.org/10.1107/s1600577517018148	journal	February 2018
Real-space analysis of radiation-induced specific changes with independent component analysis Borek, Dominika; Bromberg, Raquel; Hattne, Johan International Union of Crystallography (IUCr) https://doi.org/10.1107/s1600577517018148/gm5051sup4.zip	text	January 2018
Real-space analysis of radiation-induced specific changes with independent component analysis Borek, Dominika; Bromberg, Raquel; Hattne, Johan International Union of Crystallography (IUCr) https://doi.org/10.1107/s1600577517018148/gm5051sup5.zip	text	January 2018
Comprehensive model for X-ray-induced damage in protein crystallography Close, David M.; Bernhard, William A.; Close, David M. Journal of Synchrotron Radiation, Vol. 26, Issue 4 https://doi.org/10.1107/s1600577519005083	journal	May 2019
Comprehensive model for X-ray-induced damage in protein crystallography Close, David M.; Bernhard, William A. International Union of Crystallography (IUCr) https://doi.org/10.1107/s1600577519005083/xh5052sup1.pdf	text	January 2019
Structural knowledge or X-ray damage? A case study on xylose isomerase illustrating both Taberman, Helena; Bury, Charles S.; van der Woerd, Mark J. Journal of Synchrotron Radiation, Vol. 26, Issue 4 https://doi.org/10.1107/s1600577519005599	journal	June 2019
The potential benefits of using higher X-ray energies for macromolecular crystallography Dickerson, Joshua L.; Garman, Elspeth F.; Dickerson, Joshua L. Journal of Synchrotron Radiation, Vol. 26, Issue 4 https://doi.org/10.1107/s160057751900612x	journal	June 2019
The potential benefits of using higher X-ray energies for macromolecular crystallography Dickerson, Joshua L.; Garman, Elspeth F. International Union of Crystallography (IUCr) https://doi.org/10.1107/s160057751900612x/xh5054sup1.pdf	text	January 2019
Radiation-damage investigation of a DNA 16-mer Bugris, Valéria; Harmat, Veronika; Ferenc, Györgyi Journal of Synchrotron Radiation, Vol. 26, Issue 4 https://doi.org/10.1107/s160057751900763x	journal	June 2019
Radiation-damage investigation of a DNA 16-mer Bugris, Valéria; Harmat, Veronika; Ferenc, Györgyi International Union of Crystallography (IUCr) https://doi.org/10.1107/s160057751900763x/xh5055sup1.pdf	text	January 2019
The potential benefits of using higher X-ray energies for macromolecular crystallography Dickerson, Joshua; Garman, Elspeth Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue a2 https://doi.org/10.1107/s2053273319089307	journal	August 2019
Direct Radiation Effects on the Structure and Stability of Collagen and Other Proteins Lalande, Mathieu; Schwob, Lucas; Vizcaino, Violaine Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2020-00285	text	January 2019

Similar Records

gamma. irradiation of Bowman--Birk soybean proteinase inhibitor

Journal Article · Wed Nov 30 23:00:00 EST 1977 · Radiat. Res.; (United States) · OSTI ID:7090760

Radiation-damage investigation of a DNA 16-mer

Journal Article · Fri Jun 21 00:00:00 EDT 2019 · Journal of Synchrotron Radiation (Online) · OSTI ID:1609177

Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts regenerated with deuterated tyrosine

Journal Article · Tue Oct 21 00:00:00 EDT 1986 · Biochemistry; (United States) · OSTI ID:7035559

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
74 ATOMIC AND MOLECULAR PHYSICS
Fourier difference maps
electron density loss
radiation chemistry
specific damage
tyrosine

OH cleavage from tyrosine: debunking a myth

Citation Formats

References (57)

Cited By (15)

Similar Records

Related Subjects