Pressure and Temperature Effects on the Formation of Aminoacrylate Intermediates of Tyrosine Phenol-lyase Demonstrate Reaction Dynamics

Phillips, Robert S.; Craig, Steven; Kovalevsky, Andrey; Gerlits, Oksana; Weiss, Kevin; Iorgu, Andreea I.; Heyes, Derren J.; Hay, Sam

doi:10.1021/acscatal.9b03967

Pressure and Temperature Effects on the Formation of Aminoacrylate Intermediates of Tyrosine Phenol-lyase Demonstrate Reaction Dynamics

Journal Article · Thu Dec 19 00:00:00 EST 2019 · ACS Catalysis

DOI:https://doi.org/10.1021/acscatal.9b03967· OSTI ID:1761712

^[1]; Craig, Steven ^[1]; ^[2]; Gerlits, Oksana ^[3]; ^[2]; ^[4]; Heyes, Derren J. ^[4]; ^[4]

Univ. of Georgia, Athens, GA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Tennessee Wesleyan Univ., Athens, TN (United States)
Univ. of Manchester (United Kingdom)

The structures of aminoacrylate intermediates of wild-type, F448A mutant, and perdeuterated tyrosine phenol-lyase (TPL) formed from l-tyrosine, 3-F-l-tyrosine, S-ethyl-l-cysteine, and l-serine, with bound 4-hydroxypyridine, were determined by X-ray crystallography. All the aminoacrylate Schiff’s base structures in chain A are identical regardless of the substrate used to form them. 4-Hydroxypyridine is also in an identical location, except for F448A TPL, where it is displaced about 1 Å due to the increased size of the active site. In chain B, we have found different complexes depending on the substrate. With wild-type TPL, l-tyrosine gave no density, 3-F-l-tyrosine gave a gem-diamine, and l-serine gave a gem-diamine in chain B. S-Ethyl-l-cysteine formed an aminoacrylate in chain B with both wild-type and F448A TPL, but perdeuterated TPL with S-ethyl-l-cysteine formed a gem-diamine of aminoacrylate. The kinetics of aminoacrylate intermediate formation from l-tyrosine and S-ethyl-l-cysteine were followed by stopped-flow spectrophotometry at temperatures from 281 to 320 K and hydrostatic pressures ranging from 1 bar to 1.5 kbar at 293 K. There are large negative values of ΔS^‡, ΔCp^‡, ΔV^‡, and Δβ^‡ for aminoacrylate intermediate formation for l-tyrosine but not for S-ethyl-l-cysteine. Formation of the aminoacrylate intermediates from l-tyrosine and S-ethyl-l-cysteine shows heavy enzyme deuterium kinetic isotope effects with perdeuterated TPL that are strongly temperature- and pressure-dependent and may be normal or inverse depending on conditions. Overall, these results suggest that conformational dynamics as well as vibrational coupling play a key role in the mechanism of the elimination reaction of l-tyrosine catalyzed by TPL.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-00OR22725; W-31-109-ENG-3

OSTI ID:: 1761712

Alternate ID(s):: OSTI ID: 1598026

Journal Information:: ACS Catalysis, Journal Name: ACS Catalysis Journal Issue: 3 Vol. 10; ISSN 2155-5435

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (37)

Role of F225 in O-phosphoserine sulfhydrylase from Aeropyrum pernix K1 Takeda, Emi; Kunimoto, Kohei; Kawai, Yoshito Extremophiles, Vol. 20, Issue 5 https://doi.org/10.1007/s00792-016-0862-6	journal	July 2016
Synthesis of l-tyrosine from phenol and catalysed by tyrosine phenol-lyase Phillips, Robert S.; Ravichandran, Krishamurthy; Von Tersch, Robert L. Enzyme and Microbial Technology, Vol. 11, Issue 2 https://doi.org/10.1016/0141-0229(89)90064-1	journal	February 1989
The role of acidic dissociation of substrate's phenol group in the mechanism of tyrosine phenol-lyase Faleev, Nicolai G.; Axenova, Olga V.; Demidkina, Tatyana V. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1647, Issue 1-2 https://doi.org/10.1016/S1570-9639(03)00063-3	journal	April 2003
Linear and non-linear pressure dependence of enzyme catalytic parameters Masson, Patrick; Balny, Claude Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1724, Issue 3 https://doi.org/10.1016/j.bbagen.2005.05.003	journal	August 2005
Change in heat capacity accurately predicts vibrational coupling in enzyme catalyzed reactions Arcus, Vickery L.; Pudney, Christopher R. FEBS Letters, Vol. 589, Issue 17 https://doi.org/10.1016/j.febslet.2015.06.042	journal	July 2015
Two Structures of Alliinase from Alliium sativum L.: Apo Form and Ternary Complex with Aminoacrylate Reaction Intermediate Covalently Bound to the PLP Cofactor Shimon, Linda J. W.; Rabinkov, Aharon; Shin, Irina Journal of Molecular Biology, Vol. 366, Issue 2 https://doi.org/10.1016/j.jmb.2006.11.041	journal	February 2007
On the Temperature Dependence of Enzyme-Catalyzed Rates Arcus, Vickery L.; Prentice, Erica J.; Hobbs, Joanne K. Biochemistry, Vol. 55, Issue 12 https://doi.org/10.1021/acs.biochem.5b01094	journal	March 2016
Crystal Structures of Wild-Type and F448A Mutant Citrobacter freundii Tyrosine Phenol-Lyase Complexed with a Substrate and Inhibitors: Implications for the Reaction Mechanism Phillips, Robert S.; Craig, Steven Biochemistry, Vol. 57, Issue 43 https://doi.org/10.1021/acs.biochem.8b00724	journal	September 2018
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
Uncovering the Relationship between the Change in Heat Capacity for Enzyme Catalysis and Vibrational Frequency through Isotope Effect Studies Jones, Hannah B. L.; Crean, Rory M.; Matthews, Christopher ACS Catalysis, Vol. 8, Issue 6 https://doi.org/10.1021/acscatal.8b01025	journal	April 2018
Heat Capacity Changes for Transition-State Analogue Binding and Catalysis with Human 5′-Methylthioadenosine Phosphorylase Firestone, Ross S.; Cameron, Scott A.; Karp, Jerome M. ACS Chemical Biology, Vol. 12, Issue 2 https://doi.org/10.1021/acschembio.6b00885	journal	December 2016
Site-Directed Mutagenesis of Tyrosine-71 to Phenylalanine in Citrobacter freundii Tyrosine Phenol-Lyase: Evidence for Dual Roles of Tyrosine-71 as a General Acid Catalyst in the Reaction Mechanism and in Cofactor Binding Chen, Hao Yuan; Demidkina, Tatyana V.; Phillips, Robert S. Biochemistry, Vol. 34, Issue 38 https://doi.org/10.1021/bi00038a023	journal	September 1995
Characterization of the reaction of L-serine and indole with Escherichia coli tryptophan synthase via rapid-scanning ultraviolet-visible spectroscopy Drewe, William Frederick; Dunn, Michael F. Biochemistry, Vol. 25, Issue 9 https://doi.org/10.1021/bi00357a032	journal	May 1986
Mechanistic deductions from kinetic isotope effects and pH studies of pyridoxal phosphate dependent carbon-carbon lyases: Erwinia herbicola and Citrobacter freundii tyrosine phenol-lyase Kiick, Dennis M.; Phillips, Robert S. Biochemistry, Vol. 27, Issue 19 https://doi.org/10.1021/bi00419a023	journal	September 1988
Aminoacrylate Intermediates in the Reaction of Citrobacter freundii Tyrosine Phenol-Lyase ^† Phillips, Robert S.; Chen, Hao Yuan; Faleev, Nicolai G. Biochemistry, Vol. 45, Issue 31 https://doi.org/10.1021/bi060561o	journal	August 2006
Allosteric Regulation of Substrate Channeling in Tryptophan Synthase: Modulation of the l -Serine Reaction in Stage I of the β-Reaction by α-Site Ligands ^† ^, ^‡ Ngo, Huu; Kimmich, Novelle; Harris, Rodney Biochemistry, Vol. 46, Issue 26 https://doi.org/10.1021/bi7003872	journal	July 2007
LigPlot+: Multiple Ligand–Protein Interaction Diagrams for Drug Discovery Laskowski, Roman A.; Swindells, Mark B. Journal of Chemical Information and Modeling, Vol. 51, Issue 10 https://doi.org/10.1021/ci200227u	journal	October 2011
Crystallographic Snapshots of Tyrosine Phenol-lyase Show That Substrate Strain Plays a Role in C–C Bond Cleavage Milić, Dalibor; Demidkina, Tatyana V.; Faleev, Nicolai G. Journal of the American Chemical Society, Vol. 133, Issue 41 https://doi.org/10.1021/ja203361g	journal	October 2011
Heavy-Enzyme Kinetic Isotope Effects on Proton Transfer in Alanine Racemase Toney, Michael D.; Castro, Joan Nieto; Addington, Trevor A. Journal of the American Chemical Society, Vol. 135, Issue 7 https://doi.org/10.1021/ja3101243	journal	February 2013
Untangling Heavy Protein and Cofactor Isotope Effects on Enzyme-Catalyzed Hydride Transfer Longbotham, James E.; Hardman, Samantha J. O.; Görlich, Stefan Journal of the American Chemical Society, Vol. 138, Issue 41 https://doi.org/10.1021/jacs.6b07852	journal	October 2016
Dynamical origins of heat capacity changes in enzyme-catalysed reactions van der Kamp, Marc W.; Prentice, Erica J.; Kraakman, Kirsty L. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03597-y	journal	March 2018
Mechanism of catalysis by tyrosine phenol lyase from Erwinia herbicola. Multiple kinetic isotope effects for the reactions with adequate substrates Faleev, Nikolai G.; Spirina, Svetlana N.; Demidkina, Tatyana V. Journal of the Chemical Society, Perkin Transactions 2, Issue 9 https://doi.org/10.1039/P29960002001	journal	January 1996
Threonine-124 and phenylalanine-448 in Citrobacter freundii tyrosine phenol-lyase are necessary for activity with l-tyrosine Demidkina, Tatyana V.; Barbolina, Maria V.; Faleev, Nicolai G. Biochemical Journal, Vol. 363, Issue 3 https://doi.org/10.1042/bj3630745	journal	April 2002
Structural basis for substrate activation and regulation by cystathionine beta-synthase (CBS) domains in cystathionine -synthase Koutmos, M.; Kabil, O.; Smith, J. L. Proceedings of the National Academy of Sciences, Vol. 107, Issue 49 https://doi.org/10.1073/pnas.1011448107	journal	November 2010
Inverse enzyme isotope effects in human purine nucleoside phosphorylase with heavy asparagine labels Harijan, Rajesh K.; Zoi, Ioanna; Antoniou, Dimitri Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1805416115	journal	June 2018
Crystal Structure of Escherichia coli Diaminopropionate Ammonia-lyase Reveals Mechanism of Enzyme Activation and Catalysis Bisht, Shveta; Rajaram, Venkatesan; Bharath, Sakshibeedu R. Journal of Biological Chemistry, Vol. 287, Issue 24 https://doi.org/10.1074/jbc.M112.351809	journal	June 2012
Structural Insights into Catalysis and Inhibition of O-Acetylserine Sulfhydrylase from Mycobacterium tuberculosis Schnell, Robert; Oehlmann, Wulf; Singh, Mahavir Journal of Biological Chemistry, Vol. 282, Issue 32 https://doi.org/10.1074/jbc.M703518200	journal	August 2007
Insights into the Catalytic Mechanism of Tyrosine Phenol-lyase from X-ray Structures of Quinonoid Intermediates Milić, Dalibor; Demidkina, Tatyana V.; Faleev, Nicolai G. Journal of Biological Chemistry, Vol. 283, Issue 43 https://doi.org/10.1074/jbc.M802061200	journal	August 2008
The Method of Successive Integration: a General Technique for Recasting Kinetic Equations in a Readily Soluble Form Which Is Linear in the Coefficients and Sufficiently Rapid for Real Time Instrumental Use. Matheson, I. B. C. Instrumentation Science & Technology, Vol. 16, Issue 3 https://doi.org/10.1080/10739148708543650	journal	January 1987
Elementary Processes in the Interaction of Tyrosine Phenol Lyase with Inhibitors and Substrate Muro, Tetsuo; Nakatani, Hiroshi; Hiromi, Keitaro The Journal of Biochemistry, Vol. 84, Issue 3 https://doi.org/10.1093/oxfordjournals.jbchem.a132168	journal	September 1978
Citrobacter freundii tyrosine phenol-lyase: the role of asparagine 185 in modulating enzyme function through stabilization of a quinonoid intermediate Barbolina, M. V.; Phillips, R. S.; Gollnick, P. D. Protein Engineering, Design and Selection, Vol. 13, Issue 3 https://doi.org/10.1093/protein/13.3.207	journal	March 2000
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
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
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
A complete thermodynamic analysis of enzyme turnover links the free energy landscape to enzyme catalysis Jones, Hannah B. L.; Wells, Stephen A.; Prentice, Erica J. The FEBS Journal, Vol. 284, Issue 17 https://doi.org/10.1111/febs.14152	journal	July 2017
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012

Similar Records

Crystal Structures of Wild-Type and F448A Mutant Citrobacter freundii Tyrosine Phenol-Lyase Complexed with a Substrate and Inhibitors: Implications for the Reaction Mechanism

Journal Article · Wed Sep 26 20:00:00 EDT 2018 · Biochemistry · OSTI ID:1483076

Structural Snapshots of Proteus vulgaris Tryptophan Indole-Lyase Reveal Insights into the Catalytic Mechanism

Journal Article · Wed Jul 17 20:00:00 EDT 2024 · ACS Catalysis · OSTI ID:2470137

Imaging active site chemistry and protonation states: NMR crystallography of the tryptophan synthase α-aminoacrylate intermediate

Journal Article · Thu Jan 06 19:00:00 EST 2022 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1845011

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
enzyme mechanism
heat capacity
pressure dependence
pyridoxal-5'-phosphate
stopped-flow kinetics
temperature dependence

Pressure and Temperature Effects on the Formation of Aminoacrylate Intermediates of Tyrosine Phenol-lyase Demonstrate Reaction Dynamics

Citation Formats

References (37)

Similar Records

Related Subjects