Relative binding affinities of monolignols to horseradish peroxidase
Abstract
Monolignol binding to the peroxidase active site is the first step in lignin polymerization in plant cell walls. Using molecular dynamics, docking, and free energy perturbation calculations, we investigate the binding of monolignols to horseradish peroxidase C. Our results suggest that p-coumaryl alcohol has the strongest binding affinity followed by sinapyl and coniferyl alcohol. Stacking interactions between the monolignol aromatic rings and nearby phenylalanine residues play an important role in determining the calculated relative binding affinities. p-Coumaryl and coniferyl alcohols bind in a pose productive for reaction in which a direct H-bond is formed between the phenolic –OH group and a water molecule (W2) that may facilitate proton transfer during oxidation. In contrast, in the case of sinapyl alcohol there is no such direct interaction, the phenolic –OH group instead interacting with Pro139. Furthermore, since proton and electron transfer is the rate-limiting step in monolignol oxidation by peroxidase, the binding pose (and thus the formation of near attack conformation) appears to play a more important role than the overall binding affinity in determining the oxidation rate.
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1327712
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
- Additional Journal Information:
- Journal Volume: 120; Journal Issue: 31; Journal ID: ISSN 1520-6106
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Sangha, Amandeep K., Petridis, Loukas, Cheng, Xiaolin, and Smith, Jeremy C. Relative binding affinities of monolignols to horseradish peroxidase. United States: N. p., 2016.
Web. doi:10.1021/acs.jpcb.6b00789.
Sangha, Amandeep K., Petridis, Loukas, Cheng, Xiaolin, & Smith, Jeremy C. Relative binding affinities of monolignols to horseradish peroxidase. United States. https://doi.org/10.1021/acs.jpcb.6b00789
Sangha, Amandeep K., Petridis, Loukas, Cheng, Xiaolin, and Smith, Jeremy C. Fri .
"Relative binding affinities of monolignols to horseradish peroxidase". United States. https://doi.org/10.1021/acs.jpcb.6b00789. https://www.osti.gov/servlets/purl/1327712.
@article{osti_1327712,
title = {Relative binding affinities of monolignols to horseradish peroxidase},
author = {Sangha, Amandeep K. and Petridis, Loukas and Cheng, Xiaolin and Smith, Jeremy C.},
abstractNote = {Monolignol binding to the peroxidase active site is the first step in lignin polymerization in plant cell walls. Using molecular dynamics, docking, and free energy perturbation calculations, we investigate the binding of monolignols to horseradish peroxidase C. Our results suggest that p-coumaryl alcohol has the strongest binding affinity followed by sinapyl and coniferyl alcohol. Stacking interactions between the monolignol aromatic rings and nearby phenylalanine residues play an important role in determining the calculated relative binding affinities. p-Coumaryl and coniferyl alcohols bind in a pose productive for reaction in which a direct H-bond is formed between the phenolic –OH group and a water molecule (W2) that may facilitate proton transfer during oxidation. In contrast, in the case of sinapyl alcohol there is no such direct interaction, the phenolic –OH group instead interacting with Pro139. Furthermore, since proton and electron transfer is the rate-limiting step in monolignol oxidation by peroxidase, the binding pose (and thus the formation of near attack conformation) appears to play a more important role than the overall binding affinity in determining the oxidation rate.},
doi = {10.1021/acs.jpcb.6b00789},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 31,
volume = 120,
place = {United States},
year = {Fri Jul 22 00:00:00 EDT 2016},
month = {Fri Jul 22 00:00:00 EDT 2016}
}
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Works referenced in this record:
Biosynthesis and Constitution of Lignin
journal, April 1959
- Freudenberg, Karl
- Nature, Vol. 183, Issue 4669
The Genetics of Lignin Biosynthesis: Connecting Genotype to Phenotype
journal, December 2010
- Bonawitz, Nicholas D.; Chapple, Clint
- Annual Review of Genetics, Vol. 44, Issue 1, p. 337-363
Lignin Biosynthesis and Structure
journal, May 2010
- Vanholme, R.; Demedts, B.; Morreel, K.
- Plant Physiology, Vol. 153, Issue 3, p. 895-905
Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014
- Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
- Nature, Vol. 509, Issue 7500, p. 376-380
Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks
journal, July 2014
- Poovaiah, Charleson R.; Nageswara-Rao, Madhugiri; Soneji, Jaya R.
- Plant Biotechnology Journal, Vol. 12, Issue 9
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass
journal, February 2011
- Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808
Loosening lignin's grip on biofuel production
journal, July 2007
- Chapple, Clint; Ladisch, Michael; Meilan, Rick
- Nature Biotechnology, Vol. 25, Issue 7, p. 746-748
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012
- Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
- Biotechnology for Biofuels, Vol. 5, Issue 1
Understanding Lignification: Challenges Beyond Monolignol Biosynthesis: Figure 1.
journal, October 2010
- Li, Xu; Chapple, Clint
- Plant Physiology, Vol. 154, Issue 2
Plant Cell Biology: The ABC of Monolignol Transport
journal, July 2012
- Sibout, Richard; Höfte, Herman
- Current Biology, Vol. 22, Issue 13
Differential Activity and Structure of Highly Similar Peroxidases. Spectroscopic, Crystallographic, and Enzymatic Analyses of Lignifying Arabidopsis thaliana Peroxidase A2 and Horseradish Peroxidase A2 † , ‡
journal, September 2001
- Nielsen, Kåre Lehmann; Indiani, Chiara; Henriksen, Anette
- Biochemistry, Vol. 40, Issue 37
Substituent effects of 3,5-disubstituted p-coumaryl alcohols on their oxidation using horseradish peroxidase–H2O2 as the oxidant
journal, December 2005
- Kobayashi, Takayuki; Taguchi, Hiroyasu; Shigematsu, Mikiji
- Journal of Wood Science, Vol. 51, Issue 6
Radical Coupling Reactions in Lignin Synthesis: A Density Functional Theory Study
journal, April 2012
- Sangha, Amandeep K.; Parks, Jerry M.; Standaert, Robert F.
- The Journal of Physical Chemistry B, Vol. 116, Issue 16
Cell Wall Lignin is Polymerised by Class III Secretable Plant Peroxidases in Norway Spruce
journal, February 2010
- Fagerstedt, Kurt V.; Kukkola, Eija M.; Koistinen, Ville V. T.
- Journal of Integrative Plant Biology, Vol. 52, Issue 2
Chemical Factors that Control Lignin Polymerization
journal, December 2013
- Sangha, Amandeep K.; Davison, Brian H.; Standaert, Robert F.
- The Journal of Physical Chemistry B, Vol. 118, Issue 1
Hammett ϱσ correlation for reactions of horseradish peroxidase compound II with phenols
journal, December 1986
- Dunford, H. Brian; Adeniran, Adejare Job
- Archives of Biochemistry and Biophysics, Vol. 251, Issue 2
An Efficient Proton-Coupled Electron-Transfer Process during Oxidation of Ferulic Acid by Horseradish Peroxidase: Coming Full Cycle
journal, October 2006
- Derat, Etienne; Shaik, Sason
- Journal of the American Chemical Society, Vol. 128, Issue 42
Good Practices in Free-Energy Calculations
journal, August 2010
- Pohorille, Andrew; Jarzynski, Christopher; Chipot, Christophe
- The Journal of Physical Chemistry B, Vol. 114, Issue 32
Guidelines for the analysis of free energy calculations
journal, March 2015
- Klimovich, Pavel V.; Shirts, Michael R.; Mobley, David L.
- Journal of Computer-Aided Molecular Design, Vol. 29, Issue 5
The Structures of the Horseradish Peroxidase C-Ferulic Acid Complex and the Ternary Complex with Cyanide Suggest How Peroxidases Oxidize Small Phenolic Substrates
journal, December 1999
- Henriksen, Anette; Smith, Andrew T.; Gajhede, Michael
- Journal of Biological Chemistry, Vol. 274, Issue 49
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1
Scalable molecular dynamics with NAMD
journal, January 2005
- Phillips, James C.; Braun, Rosemary; Wang, Wei
- Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins †
journal, April 1998
- MacKerell, A. D.; Bashford, D.; Bellott, M.
- The Journal of Physical Chemistry B, Vol. 102, Issue 18
Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations
journal, August 2004
- Mackerell, Alexander D.; Feig, Michael; Brooks, Charles L.
- Journal of Computational Chemistry, Vol. 25, Issue 11
Comparison of simple potential functions for simulating liquid water
journal, July 1983
- Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
- The Journal of Chemical Physics, Vol. 79, Issue 2
A molecular mechanics force field for lignin
journal, February 2009
- Petridis, Loukas; Smith, Jeremy C.
- Journal of Computational Chemistry, Vol. 30, Issue 3
CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields
journal, January 2009
- Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.
- Journal of Computational Chemistry
Constant pressure molecular dynamics simulation: The Langevin piston method
journal, September 1995
- Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W.
- The Journal of Chemical Physics, Vol. 103, Issue 11
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993
- Darden, Tom; York, Darrin; Pedersen, Lee
- The Journal of Chemical Physics, Vol. 98, Issue 12
A Toolkit for the Analysis of Free-Energy Perturbation Calculations
journal, July 2012
- Liu, Peng; Dehez, François; Cai, Wensheng
- Journal of Chemical Theory and Computation, Vol. 8, Issue 8
Efficient estimation of free energy differences from Monte Carlo data
journal, October 1976
- Bennett, Charles H.
- Journal of Computational Physics, Vol. 22, Issue 2
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
journal, December 2009
- Morris, Garrett M.; Huey, Ruth; Lindstrom, William
- Journal of Computational Chemistry, Vol. 30, Issue 16
Aromatic Substrate Specificity of Horseradish Peroxidase C Studied by a Combined Fluorescence Line Narrowing/Energy Minimization Approach: The Effect of Localized Side-Chain Reorganization
journal, July 2001
- Laberge, M.; Osvath, Sz.; Fidy, J.
- Biochemistry, Vol. 40, Issue 31
π-Stacking Interactions: ALIVE AND WELL IN PROTEINS
journal, June 1998
- McGaughey, Georgia B.; Gagné, Marc; Rappé, Anthony K.
- Journal of Biological Chemistry, Vol. 273, Issue 25
Investigation on the Effect of Key Water Molecules on Docking Performance in CSARdock Exercise
journal, May 2013
- Kumar, Ashutosh; Zhang, Kam Y. J.
- Journal of Chemical Information and Modeling, Vol. 53, Issue 8
Towards Ligand Docking Including Explicit Interface Water Molecules
journal, June 2013
- Lemmon, Gordon; Meiler, Jens
- PLoS ONE, Vol. 8, Issue 6
Works referencing / citing this record:
The role of weak interactions in lignin polymerization
journal, February 2017
- Sánchez-González, Ángel; Martín-Martínez, Francisco J.; Dobado, J. A.
- Journal of Molecular Modeling, Vol. 23, Issue 3
Acceleration of Mechanistic Investigation of Plant Secondary Metabolism Based on Computational Chemistry
journal, June 2019
- Sato, Hajime; Saito, Kazuki; Yamazaki, Mami
- Frontiers in Plant Science, Vol. 10
Acceleration of Mechanistic Investigation of Plant Secondary Metabolism Based on Computational Chemistry
journal, June 2019
- Sato, Hajime; Saito, Kazuki; Yamazaki, Mami
- Frontiers in Plant Science, Vol. 10