A mechanistic study of Trichoderma reesei Cel7B catalyzed glycosidic bond cleavage

Journal of Physical Chemistry B

Volumn 117, Issue 29, 2013, Pages 8714-8722

  Zhang, Yu ^a   Yan, Shihai ^a   Yao, Lishan ^a  

^a QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DEGLYCOSYLATION; EXPERIMENTAL VALUES; GLYCOSIDIC BOND CLEAVAGE; HYDROGEN BOND NETWORKS; MECHANISTIC STUDIES; MOLECULAR DYNAMICS SIMULATIONS; NUCLEOPHILIC ATTACK; TRICHODERMA REESEI;

ESTERIFICATION; GLYCOSYLATION; HYDROGEN; MOLECULAR DYNAMICS;

CATALYSIS;

CELLULASE; ENDOGLUCANASE CEL5A; GLYCOSIDE;

ARTICLE; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; HYDROGEN BOND; HYDROLYSIS; MOLECULAR DYNAMICS; TRICHODERMA;

CATALYSIS; CATALYTIC DOMAIN; CELLULASE; GLYCOSIDES; HYDROGEN BONDING; HYDROLYSIS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; TRICHODERMA;

EID: 84880764785     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp403999s     Document Type: Article

References (61)

1. Boraston, A. B.; Bolam, D. N.; Gilbert, H. J.; Davies, G. J. Carbohydrate-Binding Modules: Fine-Tuning Polysaccharide Recognition Biochem. J. 2004, 382, 769-781
2. Suurnakki, A.; Tenkanen, M.; Siika-Aho, M.; Niku-Paavola, M. L.; Viikari, L.; Buchert, J. Trichoderma Reesei Cellulases And Their Core Domains In The Hydrolysis And Modification Of Chemical Pulp Cellulose 2000, 7 (2) 189-209
3. Linder, M.; Teeri, T. T. The Roles And Function Of Cellulose-Binding Domains J. Biotechnol. 1997, 57 (1-3) 15-28
4. Xiao, Z. Z.; Gao, P. J.; Qu, Y. B.; Wang, T. H. Cellulose-Binding Domain Of Endoglucanase Iii From Trichoderma Reesei Disrupting The Structure Of Cellulose Biotechnol. Lett. 2001, 23 (9) 711-715
5. Lemos, M. A.; Teixeira, J. A.; Domingues, M. R. M.; Mota, M.; Gama, F. M. The Enhancement Of The Cellulolytic Activity Of Cellobiohydrolase I And Endoglucanase By The Addition Of Cellulose Binding Domains Derived From Trichoderma Reesei Enzyme Microb. Technol. 2003, 32 (1) 35-40
6. Hall, M.; Bansal, P.; Lee, J. H.; Realff, M. J.; Bommarius, A. S. Biological Pretreatment Of Cellulose: Enhancing Enzymatic Hydrolysis Rate Using Cellulose-Binding Domains From Cellulases Bioresour. Technol. 2011, 102 (3) 2910-2915
7. Kolbe, J.; Kubicek, C. P. Quantification And Identification Of The Main Components Of The Trichoderma Cellulase Complex With Monoclonal-Antibodies Using An Enzyme-Linked-Immunosorbent-Assay (Elisa) Appl. Microbiol. Biotechnol. 1990, 34 (1) 26-30
8. Kleywegt, G. J.; Zou, J. Y.; Divne, C.; Davies, G. J.; Sinning, I.; Stahlberg, J.; Reinikainen, T.; Srisodsuk, M.; Teeri, T. T.; Jones, T. A. The Crystal Structure Of The Catalytic Core Domain Of Endoglucanase I From Trichoderma Reesei At 3.6 Angstrom Resolution, And A Comparison With Related Enzymes J. Mol. Biol. 1997, 272 (3) 383-397
9. Von Ossowski, I.; Stahlberg, J.; Koivula, A.; Piens, K.; Becker, D.; Boer, H.; Harle, R.; Harris, M.; Divne, C.; Mahdi, S. Engineering The Exo-Loop Of Trichoderma Reesei Cellobiohydrolase, Ce17a. A Comparison With Phanerochaete Chrysosporium Cel7d J. Mol. Biol. 2003, 333 (4) 817-829
10. Divne, C.; Stahlberg, J.; Teeri, T. T.; Jones, T. A. High-Resolution Crystal Structures Reveal How A Cellulose Chain Is Bound In The 50 Angstrom Long Tunnel Of Cellobiohydrolase I From Trichoderma Reesei J. Mol. Biol. 1998, 275 (2) 309-325
11. Stahlberg, J.; Divne, C.; Koivula, A.; Piens, K.; Claeyssens, M.; Teeri, T. T.; Jones, T. A. Activity Studies And Crystal Structures Of Catalytically Deficient Mutants Of Cellobiohydrolase I From Trichoderma Reesei J. Mol. Biol. 1996, 264 (2) 337-349
12. Divne, C.; Stahlberg, J.; Reinikainen, T.; Ruohonen, L.; Pettersson, G.; Knowles, J. K. C.; Teeri, T. T.; Jones, T. A. The 3-Dimensional Crystal-Structure Of The Catalytic Core Of Cellobiohydrolase-I From Trichoderma-Reesei Science 1994, 265 (5171) 524-528
13. Taylor, C. B.; Payne, C. M.; Himmel, M. E.; Crowley, M. F.; Mccabe, C.; Beckham, G. T. Binding Site Dynamics And Aromatic-Carbohydrate Interactions In Processive And Non-Processive Family 7 Glycoside Hydrolases J. Phys. Chem. B 2013, 117 (17) 4924-33
14. Lin, Y. C.; Silvestre-Ryan, J.; Himmel, M. E.; Crowley, M. F.; Beckham, G. T.; Chu, J. W. Protein Allostery At The Solid-Liquid Interface: Endoglucanase Attachment To Cellulose Affects Glucan Clenching In The Binding Cleft J. Am. Chem. Soc. 2011, 133 (41) 16617-16624
15. Claeyssens, M.; Tomme, P.; Brewer, C. F.; Hehre, E. J. Stereochemical Course Of Hydrolysis And Hydration Reactions Catalyzed By Cellobiohydrolase-I And Cellobiohydrolase-Ii From Trichoderma-Reesei FEBS Lett. 1990, 263 (1) 89-92
16. Knowles, J. K. C.; Lentovaara, P.; Murray, M.; Sinnott, M. L. Stereochemical Course Of The Action Of The Cellobioside Hydrolase-I And Hydrolase-Ii Of Trichoderma-Reesei J. Chem. Soc., Chem. Commun. 1988, 21, 1401-1402
17. Claeyssens, M.; Henrissat, B. Specificity Mapping Of Cellulolytic Enzymes-Classification Into Families Of Structurally Related Proteins Confirmed By Biochemical-Analysis Protein Sci. 1992, 1 (10) 1293-1297
18. Barnett, C. B.; Wilkinson, K. A.; Naidoo, K. J. Molecular Details From Computational Reaction Dynamics For The Cellobiohydrolase I Glycosylation Reaction J. Am. Chem. Soc. 2011, 133 (48) 19474-19482
19. Li, J. H.; Du, L. K.; Wang, L. S. Glycosidic-Bond Hydrolysis Mechanism Catalyzed By Cellulase Cel7a From Trichoderma Reesei: A Comprehensive Theoretical Study By Performing Md, Qm, And Qm/Mm Calculations J. Phys. Chem. B 2010, 114 (46) 15261-15268
20. Yan, S. H.; Li, T.; Yao, L. S. Mutational Effects On The Catalytic Mechanism Of Cellobiohydrolase I From Trichoderma Reesei J. Phys. Chem. B 2011, 115 (17) 4982-4989
21. Vreven, T.; Morokuma, K.; Farkas, O.; Schlegel, H. B.; Frisch, M. J. Geometry Optimization With Qm/Mm, Oniom, And Other Combined Methods. I. Microiterations And Constraints J. Comput. Chem. 2003, 24 (6) 760-769
22. Lundberg, M.; Kawatsu, T.; Vreven, T.; Frisch, M. J.; Morokuma, K. Transition States In A Protein Environment-Oniom Qm:Mm Modeling Of Isopenicillin N Synthesis J. Chem. Theory Comput. 2009, 5 (1) 222-234
23. Chung, L. W.; Li, X.; Sugimoto, H.; Shiro, Y.; Morokuma, K. Oniom Study On A Missing Piece In Our Understanding Of Heme Chemistry: Bacterial Tryptophan 2,3-Dioxygenase With Dual Oxidants J. Am. Chem. Soc. 2010, 132 (34) 11993-12005
24. Ding, L. N.; Chung, L. W.; Morokuma, K. Reaction Mechanism Of Photoinduced Decarboxylation Of The Photoactivatable Green Fluorescent Protein: An Oniom(Qm:Mm) Study J. Phys. Chem. B 2013, 117 (4) 1075-1084
25. Wang, X. Q.; Hirao, H. Oniom (Dft:Mm) Study Of The Catalytic Mechanism Of Myo-Inositol Monophosphatase: Essential Role Of Water In Enzyme Catalysis In The Two-Metal Mechanism J. Phys. Chem. B 2013, 117 (3) 833-842
26. Chung, L. W.; Hirao, H.; Li, X.; Morokuma, K. The Oniom Method: Its Foundation And Applications To Metalloenzymes And Photobiology Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2012, 2 (2) 327-350
27. Ma, Y. Y.; Sun, Q.; Li, Z.; Yu, J. G.; Smith, S. C. Theoretical Studies Of Chromophore Maturation In The Wild-Type Green Fluorescent Protein: Oniom(Dft:Mm) Investigation Of The Mechanism Of Cyclization J. Phys. Chem. B 2012, 116 (4) 1426-1436
28. Hirao, H.; Morokuma, K. Oniom(Dft:Mm) Study Of 2-Hydroxyethylphosphonate Dioxygenase: What Determines The Destinies Of Different Substrates? J. Am. Chem. Soc. 2011, 133 (37) 14550-14553
29. Wang, X.; Hirao, H. Oniom (Dft:Mm) Study Of The Catalytic Mechanism Of Myo-Inositol Monophosphatase: Essential Role Of Water In Enzyme Catalysis In The Two-Metal Mechanism J. Phys. Chem. B 2013, 117 (3) 833-842
30. Hirao, H. The Effects Of Protein Environment And Dispersion On The Formation Of Ferric-Superoxide Species In Myo-Inositol Oxygenase (Miox): A Combined Oniom(Dft:Mm) And Energy Decomposition Analysis J. Phys. Chem. B 2011, 115 (38) 11278-11285
31. Zhong, L.; Matthews, J. F.; Hansen, P. I.; Crowley, M. F.; Cleary, J. M.; Walker, R. C.; Nimlos, M. R.; Brooks, C. L., III; Adney, W. S.; Himmel, M. E. Computational Simulations Of The Trichoderma Reesei Cellobiohydrolase I Acting On Microcrystalline Cellulose I Beta: The Enzyme-Substrate Complex Carbohydr. Res. 2009, 344 (15) 1984-1992
32. Payne, C. M.; Bomble, Y.; Taylor, C. B.; Mccabe, C.; Himmel, M. E.; Crowley, M. F.; Beckham, G. T. Multiple Functions Of Aromatic-Carbohydrate Interactions In A Processive Cellulase Examined With Molecular Simulation J. Biol. Chem. 2011, 286 (47) 41028-41035
33. Bu, L.; Beckham, G. T.; Shirts, M. R.; Nimlos, M. R.; Adney, W. S.; Himmel, M. E.; Crowley, M. F. Probing Carbohydrate Product Expulsion From A Processive Cellulase With Multiple Absolute Binding Free Energy Methods J. Biol. Chem. 2011, 286 (20) 18161-18169
34. Li, H.; Robertson, A. D.; Jensen, J. H. Very Fast Empirical Prediction And Rationalization Of Protein Pk(A) Values Proteins 2005, 61 (4) 704-721
35. Bas, D. C.; Rogers, D. M.; Jensen, J. H. Very Fast Prediction And Rationalization Of Pk(A) Values For Protein-Ligand Complexes Proteins 2008, 73 (3) 765-783
36. Olsson, M. H. M.; Sondergaard, C. R.; Rostkowski, M.; Jensen, J. H. Propka3: Consistent Treatment Of Internal And Surface Residues In Empirical Pk(A) Predictions J. Chem. Theory Comput. 2011, 7 (2) 525-537
37. Sondergaard, C. R.; Olsson, M. H. M.; Rostkowski, M.; Jensen, J. H. Improved Treatment Of Ligands And Coupling Effects In Empirical Calculation And Rationalization Of Pk(A) Values J. Chem. Theory Comput. 2011, 7 (7) 2284-2295
38. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Amber 11, 2010.
39. Hornak, V.; Simmerling, C. Generation Of Accurate Protein Loop Conformations Through Low-Barrier Molecular Dynamics Proteins: Struct. Funct. Genet. 2003, 51 (4) 577-590
40. Wang, J. M.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development And Testing Of A General Amber Force Field J. Comput. Chem. 2004, 25 (9) 1157-1174
41. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, Efficient Generation Of High-Quality Atomic Charges. Am1-Bcc Model: I. Method J. Comput. Chem. 2000, 21 (2) 132-146
42. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, Efficient Generation Of High-Quality Atomic Charges. Am1-Bcc Model: Ii. Parameterization And Validation J. Comput. Chem. 2002, 23 (16) 1623-1641
43. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison Of Simple Potential Functions For Simulating Liquid Water J. Chem. Phys. 1983, 79 (2) 926-935
44. Perdew, J. P.; Chevary, J. A.; Vosko, S. H.; Jackson, K. A.; Pederson, M. R.; Singh, D. J.; Fiolhais, C. Atoms, Molecules, Solids, And Surfaces-Applications Of The Generalized Gradient Approximation For Exchange And Correlation Phys. Rev. B 1992, 46 (11) 6671-6687
45. Perdew, J. P.; Wang, Y. Accurate And Simple Analytic Representation Of The Electron-Gas Correlation-Energy Phys. Rev. B 1992, 45 (23) 13244-13249
46. Becke, A. D. A New Mixing Of Hartree-Fock And Local Density-Functional Theories J. Chem. Phys. 1993, 98 (2) 1372-1377
47. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. The Development And Use Of Quantum-Mechanical Molecular-Models 0.76. Am1-A New General-Purpose Quantum-Mechanical Molecular-Model J. Am. Chem. Soc. 1985, 107 (13) 3902-3909
48. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Gaussian 09, Revision B.01; Gaussian, Inc.: Wallingford, CT, 2010.
49. Svensson, M.; Humbel, S.; Froese, R. D. J.; Matsubara, T.; Sieber, S.; Morokuma, K. Oniom: A Multilayered Integrated Mo+Mm Method For Geometry Optimizations And Single Point Energy Predictions. A Test For Diels-Alder Reactions And Pt(P(T-Bu)(3))(2)+H-2 Oxidative Addition J. Phys. Chem. 1996, 100 (50) 19357-19363
50. Tomasi, J.; Mennucci, B.; Cammi, R. Quantum Mechanical Continuum Solvation Models Chem. Rev. 2005, 105 (8) 2999-3093
51. Mennucci, B. Time Dependent Solvation: A New Frontier For Quantum Mechanical Continuum Models Theor. Chem. Acc. 2006, 116 (1-3) 31-42
52. Claeyssens, M.; Vantilbeurgh, H.; Kamerling, J. P.; Berg, J.; Vrsanska, M.; Biely, P. Studies Of The Cellulolytic System Of The Filamentous Fungus Trichoderma-Reesei Qm-9414-Substrate-Specificity And Transfer Activity Of Endoglucanase-I Biochem. J. 1990, 270 (1) 251-256
53. Textor, L. C.; Colussi, F.; Silveira, R. L.; Serpa, V.; De Mello, B. L.; Muniz, J. R. C.; Squina, F. M.; Pereira, N., Jr.; Skaf, M. S.; Polikarpov, I. Joint X-Ray Crystallographic And Molecular Dynamics Study Of Cellobiohydrolase I From Trichoderma Harzianum: Deciphering The Structural Features Of Cellobiohydrolase Catalytic Activity FEBS J. 2013, 280 (1) 56-69
54. Grassick, A.; Murray, P. G.; Thompson, R.; Collins, C. M.; Byrnes, L.; Birrane, G.; Higgins, T. M.; Tuohy, M. G. Three-Dimensional Structure Of A Thermostable Native Cellobiohydrolase, Cbhib, And Molecular Characterization Of The Cel7 Gene From The Filamentous Fungus, Talaromyces Emersonii Eur. J. Biochem. 2004, 271 (22) 4495-4506
55. Momeni, M. H.; Payne, C. M.; Hansson, H.; Mikkelsen, N. E.; Svedberg, J.; Engstrom, A.; Sandgren, M.; Beckham, G. T.; Stahlberg, J. Structural, Biochemical, And Computational Characterization Of The Glycoside Hydrolase Family 7 Cellobiohydrolase Of The Tree-Killing Fungus Heterobasidion Irregulare J. Biol. Chem. 2013, 288 (8) 5861-5872
56. Parkkinen, T.; Koivula, A.; Vehmaanpera, J.; Rouvinen, J. Crystal Structures Of Melanocarpus Albomyces Cellobiohydrolase Ce17b In Complex With Cello-Oligomers Show High Flexibility In The Substrate Binding Protein Sci. 2008, 17 (8) 1383-1394
57. Sulzenbacher, G.; Driguez, H.; Henrissat, B.; Schulein, M.; Davies, G. J. Structure Of The Fusarium Oxysporum Endoglucanase I With A Nonhydrolyzable Substrate Analogue: Substrate Distortion Gives Rise To The Preferred Axial Orientation For The Leaving Group Biochemistry 1996, 35 (48) 15280-15287
58. Davies, G. J.; Ducros, V.; Lewis, R. J.; Borchert, T. V.; Schulein, M. Oligosaccharide Specificity Of A Family 7 Endoglucanase: Insertion Of Potential Sugar-Binding Subsites J. Biotechnol. 1997, 57 (1-3) 91-100
59. Munoz, I. G.; Ubhayasekera, W.; Henriksson, H.; Szabo, I.; Pettersson, G.; Johansson, G.; Mowbray, S. L.; Stahlberg, J. Family 7 Cellobiohydrolases From Phanerochaete Chrysosporium: Crystal Structure Of The Catalytic Module Of Cel7d (Cbh58) At 1.32 Angstrom Resolution And Homology Models Of The Isozymes J. Mol. Biol. 2001, 314 (5) 1097-1111
60. Larkin, M. A.; Blackshields, G.; Brown, N. P.; Chenna, R.; Mcgettigan, P. A.; Mcwilliam, H.; Valentin, F.; Wallace, I. M.; Wilm, A.; Lopez, R., Et Al.; Clustal, W.; Clustal, X. Version 2.0. Bioinformatics 2007, 23 (21), 2947-2948.
61. Claeyssens, M.; Van Tilbeurgh, H.; Tomme, P.; Wood, T. M.; Mcrae, S. I. Fungal Cellulase Systems. Comparison Of The Specificities Of The Cellobiohydrolases Isolated From Penicillium Pinophilum And Trichoderma Reesei Biochem. J. 1989, 261 (3) 819-25