Structural and molecular dynamics studies of a C1‐oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition

Liu, Bing; Kognole, Abhishek A.; Wu, Miao; Westereng, Bjørge; Crowley, Michael F.; Kim, Seonah; Dimarogona, Maria; Payne, Christina M.; Sandgren, Mats

doi:10.1111/febs.14472

Title: Structural and molecular dynamics studies of a C1‐oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition

Journal Article · Tue Apr 24 00:00:00 EDT 2018 · Federation of European Biochemical Societies (FEBS) Journal

DOI:https://doi.org/10.1111/febs.14472· OSTI ID:1434537

Liu, Bing ^[1]; Kognole, Abhishek A. ^[2]; Wu, Miao ^[1]; Westereng, Bjørge ^[3]; Crowley, Michael F. ^[4]; Kim, Seonah ^[4]; Dimarogona, Maria ^[5]; Payne, Christina M. ^[6]; Sandgren, Mats ^[1]

Department of Molecular Sciences Swedish University of Agricultural Sciences Uppsala Sweden
Department of Chemical and Materials Engineering University of Kentucky Lexington KY USA
Department of Chemistry, Biotechnology, and Food Science Norwegian University of Life Sciences Ås Norway
Biosciences Center National Renewable Energy Laboratory Golden CO USA
Department of Molecular Sciences Swedish University of Agricultural Sciences Uppsala Sweden, Department of Chemical Engineering University of Patras Greece
Department of Chemical and Materials Engineering University of Kentucky Lexington KY USA, Directorate of Engineering Division of Chemical, Bioengineering, Environmental, and Transport Systems National Science Foundation Alexandria VA USA

Lytic polysaccharide monooxygenases ( LPMO s) are a group of recently discovered enzymes that play important roles in the decomposition of recalcitrant polysaccharides. Here, we report the biochemical, structural, and computational characterization of an LPMO from the white‐rot fungus Heterobasidion irregulare ( H i LPMO 9B). This enzyme oxidizes cellulose at the C1 carbon of glycosidic linkages. The crystal structure of Hi LPMO 9B was determined at 2.1 Å resolution using X‐ray crystallography. Unlike the majority of the currently available C1‐specific LPMO structures, the Hi LPMO 9B structure contains an extended L2 loop, connecting β‐strands β2 and β3 of the β‐sandwich structure. Molecular dynamics ( MD ) simulations suggest roles for both aromatic and acidic residues in the substrate binding of Hi LPMO 9B, with the main contribution from the residues located on the extended region of the L2 loop (Tyr20) and the LC loop (Asp205, Tyr207, and Glu210). Asp205 and Glu210 were found to be involved in the hydrogen bonding with the hydroxyl group of the C6 carbon of glucose moieties directly or via a water molecule. Two different binding orientations were observed over the course of the MD simulations. In each orientation, the active‐site copper of this LPMO preferentially skewed toward the pyranose C1 of the glycosidic linkage over the targeted glycosidic bond. This study provides additional insight into cellulose binding by C1‐specific LPMO s, giving a molecular‐level picture of active site substrate interactions. Database The atomic coordinates and structure factors for Hi LPMO 9B have been deposited in the Protein Data Bank with accession code 5NNS .

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1434537

Journal Information:: Federation of European Biochemical Societies (FEBS) Journal, Journal Name: Federation of European Biochemical Societies (FEBS) Journal Vol. 285 Journal Issue: 12; ISSN 1742-464X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 33 works

Citation information provided by
Web of Science

References (73)

Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases Book, Adam J.; Yennamalli, Ragothaman M.; Takasuka, Taichi E. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-109	journal	January 2014
CHAINSAW : a program for mutating pdb files used as templates in molecular replacement Stein, Norman Journal of Applied Crystallography, Vol. 41, Issue 3 https://doi.org/10.1107/S0021889808006985	journal	April 2008
Secretome data from Trichoderma reesei and Aspergillus niger cultivated in submerged and sequential fermentation methods Florencio, Camila; Cunha, Fernanda M.; Badino, Alberto C. Data in Brief, Vol. 8 https://doi.org/10.1016/j.dib.2016.05.080	journal	September 2016
Novel enzymes for the degradation of cellulose Horn, Svein; Vaaje-Kolstad, Gustav; Westereng, Bjørge Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 45 https://doi.org/10.1186/1754-6834-5-45	journal	January 2012
Interactions of a fungal lytic polysaccharide monooxygenase with β-glucan substrates and cellobiose dehydrogenase Courtade, Gaston; Wimmer, Reinhard; Røhr, Åsmund K. Proceedings of the National Academy of Sciences, Vol. 113, Issue 21 https://doi.org/10.1073/pnas.1602566113	journal	May 2016
Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism Kim, S.; Stahlberg, J.; Sandgren, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1316609111	journal	December 2013
On the catalytic mechanisms of lytic polysaccharide monooxygenases Walton, Paul H.; Davies, Gideon J. Current Opinion in Chemical Biology, Vol. 31 https://doi.org/10.1016/j.cbpa.2016.04.001	journal	April 2016
Fungal Cellulases Payne, Christina M.; Knott, Brandon C.; Mayes, Heather B. Chemical Reviews, Vol. 115, Issue 3 https://doi.org/10.1021/cr500351c	journal	January 2015
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases Frandsen, Kristian E. H.; Simmons, Thomas J.; Dupree, Paul Nature Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1038/nchembio.2029	journal	February 2016
Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-binding Module on Cellulose Nimlos, Mark R.; Beckham, Gregg T.; Matthews, James F. Journal of Biological Chemistry, Vol. 287, Issue 24 https://doi.org/10.1074/jbc.M112.358184	journal	April 2012
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
Efficient separation of oxidized cello-oligosaccharides generated by cellulose degrading lytic polysaccharide monooxygenases Westereng, Bjørge; Agger, Jane Wittrup; Horn, Svein J. Journal of Chromatography A, Vol. 1271, Issue 1 https://doi.org/10.1016/j.chroma.2012.11.048	journal	January 2013
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family Harris, Paul; Welner, Ditte; McFarland, K. Biochemistry, Vol. 49, Issue 15, p. 3305-3316 https://doi.org/10.1021/bi100009p	journal	April 2010
Crystal Structure and Computational Characterization of the Lytic Polysaccharide Monooxygenase GH61D from the Basidiomycota Fungus Phanerochaete chrysosporium Wu, Miao; Beckham, Gregg T.; Larsson, Anna M. Journal of Biological Chemistry, Vol. 288, Issue 18 https://doi.org/10.1074/jbc.M113.459396	journal	March 2013
Molecular-Level Origins of Biomass Recalcitrance: Decrystallization Free Energies for Four Common Cellulose Polymorphs Beckham, Gregg T.; Matthews, James F.; Peters, Baron The Journal of Physical Chemistry B, Vol. 115, Issue 14 https://doi.org/10.1021/jp1106394	journal	April 2011
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J. Science, Vol. 330, Issue 6001, p. 219-222 https://doi.org/10.1126/science.1192231	journal	October 2010
A Structural Overview of gh61 Proteins – Fungal Cellulose Degrading Polysaccharide Monooxygenases Leggio, Leila Lo; Welner, Ditte; De Maria, Leonardo Computational and Structural Biotechnology Journal, Vol. 2, Issue 3 https://doi.org/10.5936/csbj.201209019	journal	September 2012
Distribution and diversity of enzymes for polysaccharide degradation in fungi Berlemont, Renaud Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00258-w	journal	March 2017
Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components Quinlan, R. J.; Sweeney, M. D.; Lo Leggio, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 37, p. 15079-15084 https://doi.org/10.1073/pnas.1105776108	journal	August 2011
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Lytic polysaccharide monooxygenases disrupt the cellulose fibers structure Villares, Ana; Moreau, Céline; Bennati-Granier, Chloé Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep40262	journal	January 2017
Simultaneous analysis of C1 and C4 oxidized oligosaccharides, the products of lytic polysaccharide monooxygenases acting on cellulose Westereng, Bjørge; Arntzen, Magnus Ø.; Aachmann, Finn L. Journal of Chromatography A, Vol. 1445 https://doi.org/10.1016/j.chroma.2016.03.064	journal	May 2016
A C4-oxidizing Lytic Polysaccharide Monooxygenase Cleaving Both Cellulose and Cello-oligosaccharides Isaksen, Trine; Westereng, Bjørge; Aachmann, Finn L. Journal of Biological Chemistry, Vol. 289, Issue 5 https://doi.org/10.1074/jbc.M113.530196	journal	December 2013
Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation Tan, Tien-Chye; Kracher, Daniel; Gandini, Rosaria Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8542	journal	July 2015
Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2 Bissaro, Bastien; Røhr, Åsmund K.; Müller, Gerdt Nature Chemical Biology, Vol. 13, Issue 10 https://doi.org/10.1038/nchembio.2470	journal	August 2017
The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans Fanuel, Mathieu; Garajova, Sona; Ropartz, David Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0749-5	journal	March 2017
Transcriptome and Secretome Analyses of Phanerochaete chrysosporium Reveal Complex Patterns of Gene Expression Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M. Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/AEM.00314-09	journal	April 2009
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Additive empirical force field for hexopyranose monosaccharides Guvench, Olgun; Greene, Shannon N.; Kamath, Ganesh Journal of Computational Chemistry, Vol. 29, Issue 15 https://doi.org/10.1002/jcc.21004	journal	November 2008
Lytic polysaccharide monooxygenases from Myceliophthora thermophila C1 differ in substrate preference and reducing agent specificity Frommhagen, Matthias; Koetsier, Martijn J.; Westphal, Adrie H. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0594-y	journal	August 2016
Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation Agger, J. W.; Isaksen, T.; Varnai, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 17 https://doi.org/10.1073/pnas.1323629111	journal	April 2014
Cellulose Surface Degradation by a Lytic Polysaccharide Monooxygenase and Its Effect on Cellulase Hydrolytic Efficiency Eibinger, Manuel; Ganner, Thomas; Bubner, Patricia Journal of Biological Chemistry, Vol. 289, Issue 52 https://doi.org/10.1074/jbc.M114.602227	journal	October 2014
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
Extracellular electron transfer systems fuel cellulose oxidative degradation Kracher, D.; Scheiblbrandner, S.; Felice, A. K. G. Science, Vol. 352, Issue 6289 https://doi.org/10.1126/science.aaf3165	journal	April 2016
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Solvent-Induced Forces between Two Hydrophilic Groups Durell, Stewart R.; Brooks, Bernard R.; Ben-Naim, Arieh The Journal of Physical Chemistry, Vol. 98, Issue 8 https://doi.org/10.1021/j100059a038	journal	February 1994
Lytic polysaccharide monooxygenases: a crystallographer's view on a new class of biomass-degrading enzymes Frandsen, Kristian E. H.; Lo Leggio, Leila IUCrJ, Vol. 3, Issue 6 https://doi.org/10.1107/S2052252516014147	journal	October 2016
The Role of the Secondary Coordination Sphere in a Fungal Polysaccharide Monooxygenase Span, Elise A.; Suess, Daniel L. M.; Deller, Marc C. ACS Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1021/acschembio.7b00016	journal	March 2017
Oxidative Cleavage of Cellulose by Fungal Copper-Dependent Polysaccharide Monooxygenases Beeson, William T.; Phillips, Christopher M.; Cate, Jamie H. D. Journal of the American Chemical Society, Vol. 134, Issue 2 https://doi.org/10.1021/ja210657t	journal	December 2011
Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina Bennati-Granier, Chloé; Garajova, Sona; Champion, Charlotte Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0274-3	journal	June 2015
ExPASy: the proteomics server for in-depth protein knowledge and analysis Gasteiger, E. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg563	journal	July 2003
Structural Basis for Substrate Targeting and Catalysis by Fungal Polysaccharide Monooxygenases Li, Xin; Beeson, William T.; Phillips, Christopher M. Structure, Vol. 20, Issue 6, p. 1051-1061 https://doi.org/10.1016/j.str.2012.04.002	journal	June 2012
Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase O'Dell, William B.; Agarwal, Pratul K.; Meilleur, Flora Angewandte Chemie International Edition, Vol. 56, Issue 3 https://doi.org/10.1002/anie.201610502	journal	December 2016
The Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose Westereng, Bjørge; Ishida, Takuya; Vaaje-Kolstad, Gustav PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027807	journal	November 2011
Fungal cellulose degradation by oxidative enzymes: from dysfunctional GH61 family to powerful lytic polysaccharide monooxygenase family Morgenstern, I.; Powlowski, J.; Tsang, A. Briefings in Functional Genomics, Vol. 13, Issue 6 https://doi.org/10.1093/bfgp/elu032	journal	September 2014
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 Mackerell, Alexander D.; Feig, Michael; Brooks, Charles L. Journal of Computational Chemistry, Vol. 25, Issue 11 https://doi.org/10.1002/jcc.20065	journal	August 2004
Lytic Polysaccharide Monooxygenases: The Microbial Power Tool for Lignocellulose Degradation Johansen, Katja Salomon Trends in Plant Science, Vol. 21, Issue 11 https://doi.org/10.1016/j.tplants.2016.07.012	journal	November 2016
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Deciphering key features in protein structures with the new ENDscript server Robert, Xavier; Gouet, Patrice Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku316	journal	April 2014
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
Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61 Langston, James A.; Shaghasi, Tarana; Abbate, Eric Applied and Environmental Microbiology, Vol. 77, Issue 19, p. 7007-7015 https://doi.org/10.1128/AEM.05815-11	journal	August 2011
Carbohydrate-binding modules: fine-tuning polysaccharide recognition Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J. Biochemical Journal, Vol. 382, Issue 3 https://doi.org/10.1042/BJ20040892	journal	September 2004
Fg LPMO9A from Fusarium graminearum cleaves xyloglucan independently of the backbone substitution pattern Nekiunaite, Laura; Petrović, Dejan M.; Westereng, Bjørge FEBS Letters, Vol. 590, Issue 19 https://doi.org/10.1002/1873-3468.12385	journal	September 2016
Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase Lo Leggio, Leila; Simmons, Thomas J.; Poulsen, Jens-Christian N. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6961	journal	January 2015
Structural and Functional Characterization of a Lytic Polysaccharide Monooxygenase with Broad Substrate Specificity Borisova, Anna S.; Isaksen, Trine; Dimarogona, Maria Journal of Biological Chemistry, Vol. 290, Issue 38 https://doi.org/10.1074/jbc.M115.660183	journal	July 2015
Lytic Polysaccharide Monooxygenases in Biomass Conversion Hemsworth, Glyn R.; Johnston, Esther M.; Davies, Gideon J. Trends in Biotechnology, Vol. 33, Issue 12 https://doi.org/10.1016/j.tibtech.2015.09.006	journal	December 2015
Using a model filamentous fungus to unravel mechanisms of lignocellulose deconstruction Znameroski, Elizabeth A.; Glass, N. Louise Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-6	journal	January 2013
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
An introduction to data reduction: space-group determination, scaling and intensity statistics Evans, Philip R. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S090744491003982X	journal	March 2011
A quantitative indicator diagram for lytic polysaccharide monooxygenases reveals the role of aromatic surface residues in HjLPMO9A regioselectivity Danneels, Barbara; Tanghe, Magali; Joosten, Henk-Jan PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0178446	journal	May 2017
CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses Guvench, Olgun; Hatcher, Elizabeth; Venable, Richard M. Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct900242e	journal	August 2009
Type-dependent action modes of TtAA9E and TaAA9A acting on cellulose and differently pretreated lignocellulosic substrates Kim, In Jung; Seo, Nari; An, Hyun Joo Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0721-4	journal	February 2017
Phi/Psi-chology: Ramachandran revisited Kleywegt, Gerard J.; Jones, T. Alwyn Structure, Vol. 4, Issue 12 https://doi.org/10.1016/S0969-2126(96)00147-5	journal	December 1996
Free R value: a novel statistical quantity for assessing the accuracy of crystal structures Brünger, Axel T. Nature, Vol. 355, Issue 6359 https://doi.org/10.1038/355472a0	journal	January 1992
CHARMM Additive All-Atom Force Field for Carbohydrate Derivatives and Its Utility in Polysaccharide and Carbohydrate–Protein Modeling Guvench, Olgun; Mallajosyula, Sairam S.; Raman, E. Prabhu Journal of Chemical Theory and Computation, Vol. 7, Issue 10 https://doi.org/10.1021/ct200328p	journal	August 2011
The First Structure of a Glycoside Hydrolase Family 61 Member, Cel61B from Hypocrea jecorina, at 1.6 Å Resolution Karkehabadi, Saeid; Hansson, Henrik; Kim, Steve Journal of Molecular Biology, Vol. 383, Issue 1, p. 144-154 https://doi.org/10.1016/j.jmb.2008.08.016	journal	October 2008
Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates Simmons, T. J.; Frandsen, K. E. H.; Ciano, L. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01247-3	journal	October 2017
Determinants of Regioselective Hydroxylation in the Fungal Polysaccharide Monooxygenases Vu, Van V.; Beeson, William T.; Phillips, Christopher M. Journal of the American Chemical Society, Vol. 136, Issue 2 https://doi.org/10.1021/ja409384b	journal	December 2013
Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction Nishiyama, Yoshiharu; Langan, Paul; Chanzy, Henri Journal of the American Chemical Society, Vol. 124, Issue 31 https://doi.org/10.1021/ja0257319	journal	August 2002
Classification of fungal and bacterial lytic polysaccharide monooxygenases Busk, Peter K.; Lange, Lene BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1601-6	journal	May 2015
Cellulose Degradation by Polysaccharide Monooxygenases Beeson, William T.; Vu, Van V.; Span, Elise A. Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034439	journal	June 2015
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

Similar Records

Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition

Journal Article · Tue Apr 24 00:00:00 EDT 2018 · Federation of European Biochemical Societies (FEBS) Journal · OSTI ID:1434537

Liu, Bing; Kognole, Abhishek A.; Wu, Miao; +6 more

O‐glycosylation effects on family 1 carbohydrate‐binding module solution structures

Journal Article · Mon Sep 21 00:00:00 EDT 2015 · Federation of European Biochemical Societies (FEBS) Journal · OSTI ID:1434537

Happs, Renee M.; Guan, Xiaoyang; Resch, Michael G.; +4 more

Systems biology defines the biological significance of redox‐active proteins during cellulose degradation in an aerobic bacterium

Journal Article · Mon Nov 03 00:00:00 EST 2014 · Molecular Microbiology · OSTI ID:1434537

Gardner, Jeffrey G.; Crouch, Lucy; Labourel, Aurore; +5 more

Title: Structural and molecular dynamics studies of a C1‐oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition

Citation Formats

References (73)

Similar Records

Related Subjects