Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation

Tan, Tien-Chye; Kracher, Daniel; Gandini, Rosaria; Sygmund, Christoph; Kittl, Roman; Haltrich, Dietmar; Hällberg, B. Martin; Ludwig, Roland; Divne, Christina

doi:10.1038/ncomms8542

Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation

Journal Article · Tue Jul 07 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms8542· OSTI ID:1623985

Tan, Tien-Chye ^[1]; Kracher, Daniel ^[2]; Gandini, Rosaria ^[3]; Sygmund, Christoph ^[2]; Kittl, Roman ^[2]; Haltrich, Dietmar ^[2]; Hällberg, B. Martin ^[4]; Ludwig, Roland ^[2]; Divne, Christina ^[3]

KTH Royal Inst. of Technology, Stockholm (Sweden). School of Biotechnology; Karolinska Inst., Stockholm (Sweden). Dept. of Medical Biochemistry; DOE/OSTI
Univ. of Natural Resources and Life Sciences, Vienna (Austria). Food Biotechnology Lab. Dept. of Food Science and Technology
KTH Royal Inst. of Technology, Stockholm (Sweden). School of Biotechnology; Karolinska Inst., Stockholm (Sweden). Dept. of Medical Biochemistry
Karolinska Inst., Stockholm (Sweden). Dept. of Cell and Molecular Biology; European Molecular Biology Lab. (EMBL), Hamburg (Germany); Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Centre for Structural Systems Biology

A new paradigm for cellulose depolymerization by fungi focuses on an oxidative mechanism involving cellobiose dehydrogenases (CDH) and copper-dependent lytic polysaccharide monooxygenases (LPMO); however, mechanistic studies have been hampered by the lack of structural information regarding CDH. CDH contains a haem-binding cytochrome (CYT) connected via a flexible linker to a flavin-dependent dehydrogenase (DH). Electrons are generated from cellobiose oxidation catalysed by DH and shuttled via CYT to LPMO. Here we present structural analyses that provide a comprehensive picture of CDH conformers, which govern the electron transfer between redox centres. Using structure-based site-directed mutagenesis, rapid kinetics analysis and molecular docking, we demonstrate that flavin-to-haem interdomain electron transfer (IET) is enabled by a haem propionate group and that rapid IET requires a closed CDH state in which the propionate is tightly enfolded by DH. Following haem reduction, CYT reduces LPMO to initiate oxygen activation at the copper centre and subsequent cellulose depolymerization.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1623985

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase Martin Hallberg, B.; Henriksson, Gunnar; Pettersson, Göran Journal of Molecular Biology, Vol. 315, Issue 3 https://doi.org/10.1006/jmbi.2001.5246	journal	January 2002
Another look at the interaction between mitochondrial cytochrome c and flavocytochrome b 2 Lederer, Florence European Biophysics Journal, Vol. 40, Issue 12 https://doi.org/10.1007/s00249-011-0697-0	journal	April 2011
Heterologous production of cellobiose dehydrogenases from the basidiomycete Coprinopsis cinerea and the ascomycete Podospora anserina and their effect on saccharification of wheat straw Turbe-Doan, Annick; Arfi, Yonathan; Record, Eric Applied Microbiology and Biotechnology, Vol. 97, Issue 11 https://doi.org/10.1007/s00253-012-4355-y	journal	September 2012
WeNMR: Structural Biology on the Grid Wassenaar, Tsjerk A.; van Dijk, Marc; Loureiro-Ferreira, Nuno Journal of Grid Computing, Vol. 10, Issue 4 https://doi.org/10.1007/s10723-012-9246-z	journal	November 2012
Oxidation: An important enzyme reaction in fungal degradation of cellulose Eriksson, Karl-Erik; Pettersson, Bert; Westermark, Ulla FEBS Letters, Vol. 49, Issue 2 https://doi.org/10.1016/0014-5793(74)80531-4	journal	December 1974
Cellobiose oxidase of Phanerochaete chrysosporium enhances crystalline cellulose degradation by cellulases Bao, Wenjun; Renganathan, V. FEBS Letters, Vol. 302, Issue 1 https://doi.org/10.1016/0014-5793(92)80289-s	journal	May 1992
Biological pretreatment with a cellobiose dehydrogenase-deficient strain of Trametes versicolor enhances the biofuel potential of canola straw Canam, Thomas; Town, Jennifer R.; Tsang, Adrian Bioresource Technology, Vol. 102, Issue 21 https://doi.org/10.1016/j.biortech.2011.08.045	journal	November 2011
Cellulose oxidation and bleaching processes based on recombinant Myriococcum thermophilum cellobiose dehydrogenase Flitsch, Annemarie; Prasetyo, Endry Nugroho; Sygmund, Christoph Enzyme and Microbial Technology, Vol. 52, Issue 1 https://doi.org/10.1016/j.enzmictec.2012.10.007	journal	January 2013
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
Cellobiose dehydrogenase is essential for wood invasion and nonessential for kraft pulp delignification by Trametes versicolor Dumonceaux, Tim; Bartholomew, Kirk; Valeanu, Loredana Enzyme and Microbial Technology, Vol. 29, Issue 8-9 https://doi.org/10.1016/s0141-0229(01)00407-0	journal	November 2001
A new scaffold for binding haem in the cytochrome domain of the extracellular flavocytochrome cellobiose dehydrogenase Hallberg, B. Martin; Bergfors, Terese; Bäckbro, Kristina Structure, Vol. 8, Issue 1 https://doi.org/10.1016/s0969-2126(00)00082-4	journal	January 2000
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Putnam, Christopher D.; Hammel, Michal; Hura, Greg L. Quarterly Reviews of Biophysics, Vol. 40, Issue 3 https://doi.org/10.1017/s0033583507004635	journal	August 2007
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
Cellobiose Dehydrogenase and a Copper-Dependent Polysaccharide Monooxygenase Potentiate Cellulose Degradation by Neurospora crassa Phillips, Christopher M.; Beeson, William T.; Cate, Jamie H. ACS Chemical Biology, Vol. 6, Issue 12, p. 1399-1406 https://doi.org/10.1021/cb200351y	journal	December 2011
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
Structural Characterization of Flexible Proteins Using Small-Angle X-ray Scattering Bernadó, Pau; Mylonas, Efstratios; Petoukhov, Maxim V. Journal of the American Chemical Society, Vol. 129, Issue 17 https://doi.org/10.1021/ja069124n	journal	May 2007
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
Heme Electron Transfer in Peroxidases: The Propionate e-Pathway Guallar, Victor The Journal of Physical Chemistry B, Vol. 112, Issue 42 https://doi.org/10.1021/jp806435d	journal	October 2008
Natural engineering principles of electron tunnelling in biological oxidation–reduction Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi Nature, Vol. 402, Issue 6757 https://doi.org/10.1038/46972	journal	November 1999
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
The HADDOCK web server for data-driven biomolecular docking de Vries, Sjoerd J.; van Dijk, Marc; Bonvin, Alexandre M. J. J. Nature Protocols, Vol. 5, Issue 5 https://doi.org/10.1038/nprot.2010.32	journal	April 2010
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
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
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
Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases Forsberg, Z.; Mackenzie, A. K.; Sorlie, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 23 https://doi.org/10.1073/pnas.1402771111	journal	May 2014
A family of starch-active polysaccharide monooxygenases Vu, V. V.; Beeson, W. T.; Span, E. A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 38 https://doi.org/10.1073/pnas.1408090111	journal	September 2014
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
Mechanism of the Reductive Half-reaction in Cellobiose Dehydrogenase Hallberg, B. Martin; Henriksson, Gunnar; Pettersson, Göran Journal of Biological Chemistry, Vol. 278, Issue 9 https://doi.org/10.1074/jbc.m210961200	journal	December 2002
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
Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants Kabsch, W. Journal of Applied Crystallography, Vol. 26, Issue 6 https://doi.org/10.1107/s0021889893005588	journal	December 1993
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/s0108767390010224	journal	March 1991
Automated main-chain model building by template matching and iterative fragment extension Terwilliger, Thomas C. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 1 https://doi.org/10.1107/s0907444902018036	journal	December 2002
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
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444909038360	journal	March 2010
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
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
Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering Tria, Giancarlo; Mertens, Haydyn D. T.; Kachala, Michael IUCrJ, Vol. 2, Issue 2 https://doi.org/10.1107/s205225251500202x	journal	February 2015
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
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
Characterization of the Two Neurospora crassa Cellobiose Dehydrogenases and Their Connection to Oxidative Cellulose Degradation Sygmund, Christoph; Kracher, Daniel; Scheiblbrandner, Stefan Applied and Environmental Microbiology, Vol. 78, Issue 17 https://doi.org/10.1128/aem.01503-12	journal	June 2012
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
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
Production of four Neurospora crassa lytic polysaccharide monooxygenases in Pichia pastoris monitored by a fluorimetric assay Kittl, Roman; Kracher, Daniel; Burgstaller, Daniel Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-79	journal	January 2012
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Automated Structure Solution With autoSHARP Vonrhein, Clemens; Blanc, Eric; Roversi, Pietro Macromolecular Crystallography Protocols, Volume 2 https://doi.org/10.1385/1-59745-266-1:215	book	January 2006
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Cellobiose Dehydrogenase – A Flavocytochrome from Wood-Degrading, Phytopathogenic and Saprotropic Fungi Zamocky, Marcel; Ludwig, R.; Peterbauer, C. Current Protein & Peptide Science, Vol. 7, Issue 3 https://doi.org/10.2174/138920306777452367	journal	June 2006
HADDOCK versus HADDOCK: New features and performance of HADDOCK2.0 on the CAPRI targets de Vries, Sjoerd J.; van Dijk, Aalt D. J.; Krzeminski, Mickaël Proteins: Structure, Function, and Bioinformatics, Vol. 69, Issue 4 https://doi.org/10.1002/prot.21723	journal	September 2007
Cellobiose dehydrogenase (cellobiose oxidase) from Phanerochaete chrysosporium as a wood-degrading enzyme. Studies on cellulose, xylan and synthetic lignin Henriksson, G.; Ander, P.; Pettersson, B. Applied Microbiology and Biotechnology, Vol. 42, Issue 5 https://doi.org/10.1007/BF00171963	journal	January 1995
Cellobiose oxidase of Phanerochaete chrysosporium enhances crystalline cellulose degradation by cellulases Bao, Wenjun; Renganathan, V. FEBS Letters, Vol. 302, Issue 1 https://doi.org/10.1016/0014-5793(92)80289-S	journal	May 1992
Cellobiose dehydrogenase is essential for wood invasion and nonessential for kraft pulp delignification by Trametes versicolor Dumonceaux, Tim; Bartholomew, Kirk; Valeanu, Loredana Enzyme and Microbial Technology, Vol. 29, Issue 8-9 https://doi.org/10.1016/S0141-0229(01)00407-0	journal	November 2001
A new scaffold for binding haem in the cytochrome domain of the extracellular flavocytochrome cellobiose dehydrogenase Hallberg, B. Martin; Bergfors, Terese; Bäckbro, Kristina Structure, Vol. 8, Issue 1 https://doi.org/10.1016/S0969-2126(00)00082-4	journal	January 2000
Cloning, sequence analysis and heterologous expression in Pichia pastoris of a gene encoding a thermostable cellobiose dehydrogenase from Myriococcum thermophilum Zámocký, Marcel; Schümann, Christina; Sygmund, Christoph Protein Expression and Purification, Vol. 59, Issue 2 https://doi.org/10.1016/j.pep.2008.02.007	journal	June 2008
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Putnam, Christopher D.; Hammel, Michal; Hura, Greg L. Quarterly Reviews of Biophysics, Vol. 40, Issue 3 https://doi.org/10.1017/S0033583507004635	journal	August 2007
Sustainable bioenergy production from marginal lands in the US Midwest Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong Nature, Vol. 493, Issue 7433 https://doi.org/10.1038/nature11811	journal	January 2013
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
Studies of cellulose binding by cellobiose dehydrogenase and a comparison with cellobiohydrolase 1 Henriksson, Gunnar; Salumets, Andres; Divne, Christina Biochemical Journal, Vol. 324, Issue 3 https://doi.org/10.1042/bj3240833	journal	June 1997
Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa Tian, Chaoguang; Beeson, William T.; Iavarone, Anthony T. Proceedings of the National Academy of Sciences, Vol. 106, Issue 52 https://doi.org/10.1073/pnas.0906810106	journal	December 2009
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
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
Mechanism of the Reductive Half-reaction in Cellobiose Dehydrogenase Hallberg, B. Martin; Henriksson, Gunnar; Pettersson, Göran Journal of Biological Chemistry, Vol. 278, Issue 9 https://doi.org/10.1074/jbc.M210961200	journal	December 2002
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
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
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants Kabsch, W. Journal of Applied Crystallography, Vol. 26, Issue 6 https://doi.org/10.1107/S0021889893005588	journal	December 1993
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/S0108767390010224	journal	March 1991
Automated main-chain model building by template matching and iterative fragment extension Terwilliger, Thomas C. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 1 https://doi.org/10.1107/S0907444902018036	journal	December 2002
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
BALBES : a molecular-replacement pipeline Long, Fei; Vagin, Alexei A.; Young, Paul Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S0907444907050172	journal	December 2007
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444909038360	journal	March 2010
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
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
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
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering Tria, Giancarlo; Mertens, Haydyn D. T.; Kachala, Michael IUCrJ, Vol. 2, Issue 2 https://doi.org/10.1107/S205225251500202X	journal	February 2015
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
Characterization of the Two Neurospora crassa Cellobiose Dehydrogenases and Their Connection to Oxidative Cellulose Degradation Sygmund, Christoph; Kracher, Daniel; Scheiblbrandner, Stefan Applied and Environmental Microbiology, Vol. 78, Issue 17 https://doi.org/10.1128/AEM.01503-12	journal	June 2012
Catalytic Properties and Classification of Cellobiose Dehydrogenases from Ascomycetes Harreither, Wolfgang; Sygmund, Christoph; Augustin, Manfred Applied and Environmental Microbiology, Vol. 77, Issue 5 https://doi.org/10.1128/AEM.02052-10	journal	March 2011
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

Cited By (52)

Biocatalytic Oxidation Reactions: A Chemist's Perspective Dong, JiaJia; Fernández-Fueyo, Elena; Hollmann, Frank Angewandte Chemie International Edition, Vol. 57, Issue 30 https://doi.org/10.1002/anie.201800343	journal	July 2018
Direct Electron Transfer of Enzymes Facilitated by Cytochromes Ma, Su; Ludwig, Roland ChemElectroChem, Vol. 6, Issue 4 https://doi.org/10.1002/celc.201801256	journal	December 2018
Multiplicity of enzymatic functions in the CAZy AA3 family Sützl, Leander; Laurent, Christophe V. F. P.; Abrera, Annabelle T. Applied Microbiology and Biotechnology, Vol. 102, Issue 6 https://doi.org/10.1007/s00253-018-8784-0	journal	February 2018
Molecular Mechanisms of Oxygen Activation and Hydrogen Peroxide Formation in Lytic Polysaccharide Monooxygenases Wang, Binju; Walton, Paul H.; Rovira, Carme ACS Catalysis, Vol. 9, Issue 6 https://doi.org/10.1021/acscatal.9b00778	journal	April 2019
Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme Cannella, D.; Möllers, K. B.; Frigaard, N. -U. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11134	journal	April 2016
Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose Garajova, Sona; Mathieu, Yann; Beccia, Maria Rosa Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28276	journal	June 2016
Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus Miyauchi, Shingo; Hage, Hayat; Drula, Elodie DNA Research, Vol. 27, Issue 2 https://doi.org/10.1093/dnares/dsaa011	journal	April 2020
The Pyrroloquinoline-Quinone-Dependent Pyranose Dehydrogenase from Coprinopsis cinerea Drives Lytic Polysaccharide Monooxygenase Action Várnai, Anikó; Umezawa, Kiwamu; Yoshida, Makoto Applied and Environmental Microbiology, Vol. 84, Issue 11 https://doi.org/10.1128/aem.00156-18	journal	June 2018
Trichoderma reesei Dehydrogenase, a Pyrroloquinoline Quinone-Dependent Member of Auxiliary Activity Family 12 of the Carbohydrate-Active Enzymes Database: Functional and Structural Characterization Turbe-Doan, Annick; Record, Eric; Lombard, Vincent Applied and Environmental Microbiology, Vol. 85, Issue 24 https://doi.org/10.1128/aem.00964-19	journal	December 2019
Molecular and catalytic properties of fungal extracellular cellobiose dehydrogenase produced in prokaryotic and eukaryotic expression systems Ma, Su; Preims, Marita; Piumi, François Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0653-5	journal	February 2017
Salt-responsive lytic polysaccharide monooxygenases from the mangrove fungus Pestalotiopsis sp. NCi6 Patel, Ilabahen; Kracher, Daniel; Ma, Su Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0520-3	journal	May 2016
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
Lytic polysaccharide monooxygenases and other oxidative enzymes are abundantly secreted by Aspergillus nidulans grown on different starches Nekiunaite, Laura; Arntzen, Magnus Ø.; Svensson, Birte Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0604-0	journal	September 2016
Polysaccharide monooxygenase-catalyzed oxidation of cellulose to glucuronic acid-containing cello-oligosaccharides Chen, Jinyin; Guo, Xiuna; Zhu, Min Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1384-0	journal	February 2019
On the functional characterization of lytic polysaccharide monooxygenases (LPMOs) Eijsink, Vincent G. H.; Petrovic, Dejan; Forsberg, Zarah Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1392-0	journal	March 2019
The H2O2-dependent activity of a fungal lytic polysaccharide monooxygenase investigated with a turbidimetric assay Filandr, Frantisek; Man, Petr; Halada, Petr Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01673-4	journal	March 2020
Myceliophthora thermophila M77 utilizes hydrolytic and oxidative mechanisms to deconstruct biomass dos Santos, Hévila Brognaro; Bezerra, Thaís Milena Souza; Pradella, José G. C. AMB Express, Vol. 6, Issue 1 https://doi.org/10.1186/s13568-016-0276-y	journal	November 2016
Biochemical studies of two lytic polysaccharide monooxygenases from the white-rot fungus Heterobasidion irregulare and their roles in lignocellulose degradation Liu, Bing; Olson, Åke; Wu, Miao PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0189479	journal	December 2017
Sequence and Structural Analysis of AA9 and AA10 LPMOs: An Insight into the Basis of Substrate Specificity and Regioselectivity Zhou, Xiaoli; Qi, Xiaohua; Huang, Hongxia International Journal of Molecular Sciences, Vol. 20, Issue 18 https://doi.org/10.3390/ijms20184594	journal	September 2019
Influence of Lytic Polysaccharide Monooxygenase Active Site Segments on Activity and Affinity Laurent, Christophe V. F. P.; Sun, Peicheng; Scheiblbrandner, Stefan International Journal of Molecular Sciences, Vol. 20, Issue 24 https://doi.org/10.3390/ijms20246219	journal	December 2019
Direct Electron Transfer of Dehydrogenases for Development of 3rd Generation Biosensors and Enzymatic Fuel Cells Bollella, Paolo; Gorton, Lo; Antiochia, Riccarda Sensors, Vol. 18, Issue 5 https://doi.org/10.3390/s18051319	journal	April 2018
Additional file 2 of Low-abundance populations distinguish microbiome performance in plant cell wall deconstruction Tom, Lauren M.; Aulitto, Martina; Wu, Yu-Wei figshare https://doi.org/10.6084/m9.figshare.21391677	dataset	January 2022
Additional file 1 of Characterization of a novel AA3_1 xylooligosaccharide dehydrogenase from Thermothelomyces myriococcoides CBS 398.93 Zhao, Hongbo; Karppi, Johanna; Nguyen, Thi Truc Minh figshare https://doi.org/10.6084/m9.figshare.22609450.v1	dataset	January 2023
Additional file 3 of Characterization of a novel AA3_1 xylooligosaccharide dehydrogenase from Thermothelomyces myriococcoides CBS 398.93 Zhao, Hongbo; Karppi, Johanna; Nguyen, Thi Truc Minh figshare https://doi.org/10.6084/m9.figshare.22609456.v1	dataset	January 2023
Biokatalytische Oxidationsreaktionen - aus der Sicht eines Chemikers Dong, JiaJia; Fernández-Fueyo, Elena; Hollmann, Frank Angewandte Chemie, Vol. 130, Issue 30 https://doi.org/10.1002/ange.201800343	journal	July 2018
Studying Direct Electron Transfer by Site‐Directed Immobilization of Cellobiose Dehydrogenase Meneghello, Marta; Al‐Lolage, Firas A.; Ma, Su ChemElectroChem, Vol. 6, Issue 3 https://doi.org/10.1002/celc.201801503	journal	September 2018
Direct Electron Transfer of Enzymes Facilitated by Cytochromes Ma, Su; Ludwig, Roland ChemElectroChem, Vol. 6, Issue 4 https://doi.org/10.1002/celc.201900058	journal	January 2019
Activation of bacterial lytic polysaccharide monooxygenases with cellobiose dehydrogenase: Activation of Bacterial LPMOs with CDH Loose, Jennifer S. M.; Forsberg, Zarah; Kracher, Daniel Protein Science, Vol. 25, Issue 12 https://doi.org/10.1002/pro.3043	journal	September 2016
Chitin-Active Lytic Polysaccharide Monooxygenases Courtade, Gaston; Aachmann, Finn L. Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-981-13-7318-3_6	book	January 2019
Insights into the mechanism(s) of digestion of crystalline cellulose by plant class C GH9 endoglucanases Kundu, Siddhartha Journal of Molecular Modeling, Vol. 25, Issue 8 https://doi.org/10.1007/s00894-019-4133-1	journal	July 2019
A fungal family of lytic polysaccharide monooxygenase-like copper proteins Labourel, Aurore; Frandsen, Kristian E. H.; Zhang, Feng Nature Chemical Biology, Vol. 16, Issue 3 https://doi.org/10.1038/s41589-019-0438-8	journal	January 2020
Activity, stability and 3-D structure of the Cu( ii ) form of a chitin-active lytic polysaccharide monooxygenase from Bacillus amyloliquefaciens Gregory, Rebecca C.; Hemsworth, Glyn R.; Turkenburg, Johan P. Dalton Transactions, Vol. 45, Issue 42, p. 16904-16912 https://doi.org/10.1039/c6dt02793h	journal	January 2016
Molecular mechanism of lytic polysaccharide monooxygenases Hedegård, Erik Donovan; Ryde, Ulf Chemical Science, Vol. 9, Issue 15 https://doi.org/10.1039/c8sc00426a	journal	January 2018
Learning from microbial strategies for polysaccharide degradation Hemsworth, Glyn R.; Déjean, Guillaume; Davies, Gideon J. Biochemical Society Transactions, Vol. 44, Issue 1 https://doi.org/10.1042/bst20150180	journal	February 2016
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
Reactivity of O 2 versus H 2 O 2 with polysaccharide monooxygenases Hangasky, John A.; Iavarone, Anthony T.; Marletta, Michael A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 19 https://doi.org/10.1073/pnas.1801153115	journal	April 2018
Heterogeneity in the Histidine-brace Copper Coordination Sphere in Auxiliary Activity Family 10 (AA10) Lytic Polysaccharide Monooxygenases Chaplin, Amanda K.; Wilson, Michael T.; Hough, Michael A. Journal of Biological Chemistry, Vol. 291, Issue 24, p. 12838-12850 https://doi.org/10.1074/jbc.m116.722447	journal	April 2016
X-ray structure of the direct electron transfer-type FAD glucose dehydrogenase catalytic subunit complexed with a hitchhiker protein Yoshida, Hiromi; Kojima, Katsuhiro; Shiota, Masaki Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 9 https://doi.org/10.1107/s2059798319010878	journal	August 2019
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 The FEBS Journal, Vol. 285, Issue 12 https://doi.org/10.1111/febs.14472	journal	April 2018
Polysaccharide oxidation by lytic polysaccharide monooxygenase is enhanced by engineered cellobiose dehydrogenase Kracher, Daniel; Forsberg, Zarah; Bissaro, Bastien The FEBS Journal, Vol. 287, Issue 5 https://doi.org/10.1111/febs.15067	journal	October 2019
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
How to break down crystalline cellulose Martínez, Angel T. Science, Vol. 352, Issue 6289 https://doi.org/10.1126/science.aaf8920	journal	May 2016
Crystal Structure of the Catalytic and Cytochrome b Domains in a Eukaryotic Pyrroloquinoline Quinone-Dependent Dehydrogenase Takeda, Kouta; Ishida, Takuya; Yoshida, Makoto Applied and Environmental Microbiology, Vol. 85, Issue 24 https://doi.org/10.1128/aem.01692-19	journal	October 2019
Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass Bissaro, Bastien; Várnai, Anikó; Røhr, Åsmund K. Microbiology and Molecular Biology Reviews, Vol. 82, Issue 4 https://doi.org/10.1128/mmbr.00029-18	journal	September 2018
Isolation of homogeneous polysaccharide monooxygenases from fungal sources and investigation of their synergism with cellulases when acting on cellulose Bulakhov, A. G.; Gusakov, A. V.; Chekushina, A. V. Biochemistry (Moscow), Vol. 81, Issue 5 https://doi.org/10.1134/s0006297916050102	journal	May 2016
Regioselectivity of oxidation by a polysaccharide monooxygenase from Chaetomium thermophilum Chen, Chen; Chen, Jinyin; Geng, Zhigang Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1156-2	journal	June 2018
The GMC superfamily of oxidoreductases revisited: analysis and evolution of fungal GMC oxidoreductases Sützl, Leander; Foley, Gabriel; Gillam, Elizabeth M. J. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1457-0	journal	May 2019
Discovery, activity and characterisation of an AA10 lytic polysaccharide oxygenase from the shipworm symbiont Teredinibacter turnerae Fowler, Claire. A.; Sabbadin, Federico; Ciano, Luisa Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1573-x	journal	September 2019
Cellobiose dehydrogenase: An essential enzyme for lignocellulose degradation in nature – A review / Cellobiosedehydrogenase: Ein essentielles Enzym für den Lignozelluloseabbau in der Natur – Eine Übersicht Kracher, Daniel; Ludwig, Roland Die Bodenkultur: Journal of Land Management, Food and Environment, Vol. 67, Issue 3 https://doi.org/10.1515/boku-2016-0013	journal	September 2016
Distinct Substrate Specificities and Electron-Donating Systems of Fungal Lytic Polysaccharide Monooxygenases Frommhagen, Matthias; Westphal, Adrie H.; van Berkel, Willem J. H. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01080	journal	May 2018
Molecular mechanism of lytic polysaccharide monooxygenases Hedegård, Erik D.; Ryde, Ulf arXiv https://doi.org/10.48550/arxiv.1801.07696	text	January 2018
Plant–necrotroph co-transcriptome networks illuminate a metabolic battlefield Zhang, Wei; Corwin, Jason A.; Copeland, Daniel Harrison eLife, Vol. 8 https://doi.org/10.7554/elife.44279	journal	May 2019

Similar Records

Amino Acid Residues Controlling Domain Interaction and Interdomain Electron Transfer in Cellobiose Dehydrogenase

Journal Article · Wed Sep 27 20:00:00 EDT 2023 · ChemBioChem: a European journal of chemical biology · OSTI ID:2280921

Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms

Journal Article · Tue Jan 30 19:00:00 EST 2018 · Biochimica et Biophysica Acta - General Subjects · OSTI ID:1424446

Resolving domain positions of cellobiose dehydrogenase by small angle X–ray scattering

Journal Article · Wed Jun 07 20:00:00 EDT 2023 · Federation of European Biochemical Societies (FEBS) Journal · OSTI ID:2473029

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics

Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation

Citation Formats

References (79)

Cited By (52)

Similar Records

Related Subjects