Product binding varies dramatically between processive and nonprocessive cellulase enzymes

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24807-24813

  Bu, Lintao ^a   Nimlos, Mark R ^a   Shirts, Michael R ^c   Ståhlberg, Jerry ^d   Himmel, Michael E ^a   Crowley, Michael F ^a   Beckham, Gregg T ^a,b  

^a NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^b Department of Metallurgical and Materials Engineering   (United States)

^c University of Virginia   (United States)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING CONSTANT; BINDING FREE ENERGY; CATALYTIC DOMAINS; CELLOBIOSE; CELLODEXTRIN; CELLULASE ENZYME; ENZYMATIC CATALYSIS; EXPERIMENTAL MEASUREMENTS; GLYCOSIDE HYDROLASES; GLYCOSIDIC LINKAGES; MOLECULAR-LEVEL INSIGHTS; PRODUCT INHIBITION;

BINDING ENERGY; CELLULOSE; ENZYME INHIBITION; HYDROGEN BONDS; LIGANDS;

BINDING SITES;

CELLOBIOSE; CELLODEXTRIN; CELLULASE; DEXTRIN; GLYCOSIDASE; NONPROCESSIVE CELLULASE; PROCESSIVE CELLULASE; UNCLASSIFIED DRUG; WATER;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME INHIBITION; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; PRIORITY JOURNAL;

BINDING SITES; CELLOBIOSE; CELLULASE; CELLULOSE; COMPUTER SIMULATION; DEXTRINS; GLYCOSIDE HYDROLASES; HYDROGEN BONDING; PROTEIN BINDING; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84863797974     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365510     Document Type: Article

References (56)

1. Himmel, M. E., Ding, S. Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., and Foust, T. D. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807
2. Lynd, L. R., Weimer, P. J., van Zyl, W. H., and Pretorius, I. S. (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66, 506-577 (Pubitemid 35005827)
3. Andrić, P., Meyer, A. S., Jensen, P. A., and Dam-Johansen, K. (2010) Reactor design for minimizing product inhibition during enzymatic lignocellulose hydrolysis. I. Significance and mechanism of cellobiose and glucose inhibition on cellulolytic enzymes. Biotechnol. Adv. 28, 308-324
4. Bansal, P., Hall, M., Realff, M. J., Lee, J. H., and Bommarius, A. S. (2009) Modeling cellulase kinetics on lignocellulosic substrates. Biotechnol. Adv. 27, 833-848
5. Gan, Q., Allen, S. J., and Taylor, G. (2003) Kinetic dynamics in heterogeneous enzymatic hydrolysis of cellulose: an overview, an experimental study and mathematical modelling. Process Biochemistry 38, 1003-1018 (Pubitemid 36639377)
6. Gusakov, A. V., Sinitsyn, A. P., and Klyosov, A. A. (1987) Factors affecting the enzymatic hydrolysis of cellulose in batch and continuous reactors: computer simulation and experiment. Biotechnol. Bioeng. 29, 906-910
7. Bezerra, R. M., and Dias, A. A. (2004) Discrimination among eight modified Michaelis-Menten kinetics models of cellulose hydrolysis with a large range of substrate/enzyme ratios: inhibition by cellobiose. Appl. Biochem. Biotechnol. 112, 173-184 (Pubitemid 40063662)
8. Bezerra, R. M., and Dias, A. A. (2005) Enzymatic kinetic of cellulose hydrolysis: inhibition by ethanol and cellobiose. Appl. Biochem. Biotechnol. 126, 49-59 (Pubitemid 41007060)
9. Gruno, M., Väljamäe, P., Pettersson, G., and Johansson, G. (2004) Inhibition of the Trichoderma reesei cellulases by cellobiose is strongly dependent on the nature of the substrate. Biotechnol. Bioeng. 86, 503-511 (Pubitemid 38679768)
10. Oh, K. K., Kim, S. W., Jeong, Y. S., and Hong, S. I. (2000) Bioconversion of cellulose into ethanol by nonisothermal simultaneous saccharification and fermentation. Appl. Biochem. Biotechnol. 89, 15-30
11. Philippidis, G. P., Smith, T. K., and Wyman, C. E. (1993) Study of the enzymatic hydrolysis of cellulose for production of fuel ethanol by the simultaneous saccharification and fermentation process. Biotechnol. Bioeng. 41, 846-853 (Pubitemid 23089025)
12. Wald, S., Wilke, C. R., and Blanch, H. W. (1984) Kinetics of the enzymatic hydrolysis of cellulose. Biotechnol. Bioeng. 26, 221-230
13. Bommarius, A. S., Katona, A., Cheben, S. E., Patel, A. S., Ragauskas, A. J., Knudson, K., and Pu, Y. (2008) Cellulase kinetics as a function of cellulose pretreatment. Metabolic Eng. 10, 370-381
14. Beckham, G. T., Bomble, Y. J., Bayer, E. A., Himmel, M. E., and Crowley, M. F. (2011) Applications of computational science for understanding enzymatic deconstruction of cellulose. Curr. Opin. Biotechnol. 22, 231-238
15. Chundawat, S.P., Beckham, G. T., Himmel, M. E., and Dale, B. E. (2011) Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu. Rev. Chem. Biomol. Eng. 2, 121-145
16. Beckham, G. T., Bomble, Y. J., Matthews, J. F., Taylor, C. B., Resch, M. G., Yarbrough, J. M., Decker, S. R., Bu, L., Zhao, X., McCabe, C., Wohlert, J., Bergenstråhle, M., Brady, J. W., Adney, W. S., Himmel, M. E., and Crowley, M. F. (2010) The O-glycosylated linker from the Trichoderma reesei family 7 cellulase is a flexible, disordered protein. Biophys. J. 99, 3773-3781
17. Beckham, G. T., Matthews, J. F., Bomble, Y. J., Bu, L., Adney, W. S., Himmel, M. E., Nimlos, M. R., and Crowley, M. F. (2010) Identification of amino acids responsible for processivity in a family 1 carbohydrate-binding module from a fungal cellulase. J. Phys. Chem. B 114, 1447-1453
18. Payne, C. M., Bomble, Y. J., Taylor, C. B., McCabe, C., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2011) Multiple functions of aromatic-carbohydrate interactions in a processive cellulase examined with molecular simulation. J. Biol. Chem. 286, 41028-41035
19. Taylor, C. B., Talib, M. F., McCabe, C., Bu, L., Adney, W. S., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2012) Computational investigation of glycosylation effects on a family 1 carbohydrate-binding module. J. Biol. Chem. 287, 3147-3155
20. Beckham, G. T., Matthews, J. F., Peters, B., Bomble, Y. J., Himmel, M. E., and Crowley, M. F. (2011) Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. J. Phys. Chem. B 115, 4118-4127
21. Payne, C. M., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2011) Decrystallization of oligosaccharides from the cellulose Iβ surface with molecular simulation. J. Phys. Chem. Lett. 2, 1546-1550
22. Bu, L., Beckham, G. T., Shirts, M. R., Nimlos, M. R., Adney, W. S., Himmel, M. E., and Crowley, M. F. (2011) Probing carbohydrate product expulsion from a processive cellulase with multiple absolute binding free energy methods. J. Biol. Chem. 286, 18161-18169
23. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-238
24. Rosgaard, L., Pedersen, S., Langston, J., Akerhielm, D., Cherry, J. R., and Meyer, A. S. (2007) Evaluation of minimal Trichoderma reesei cellulase mixtures on differently pretreated Barley straw substrates. Biotechnol. Prog. 23, 1270-1276 (Pubitemid 350261860)
25. Boisset, C., Fraschini, C., Schülein, M., Henrissat, B., and Chanzy, H. (2000) Imaging the enzymatic digestion of bacterial cellulose ribbons reveals the endo character of the cellobiohydrolase Cel6A from Humicola insolens and its mode of synergy with cellobiohydrolase Cel7A. Appl. Environ. Microbiol. 66, 1444-1452 (Pubitemid 30185615)
26. Chanzy, H., and Henrissat, B. (1985) Unidirectional degradation of Valonia cellulose microcrystals subjected to cellulase action. FEBS Lett. 184, 285-288
27. Chanzy, H., Henrissat, B., Vuong, R., and Schulein, M. (1983) The action of 1,4-β-D-glucan cellobiohydrolase on Valonia cellulose microcrystals: an electron microscopic study. FEBS Lett. 153, 113-118
28. Schülein, M. (1997) Enzymatic properties of cellulases from Humicola insolens. J. Biotechnol. 57, 71-81
29. Davies, G. J., Brzozowski, A. M., Dauter, M., Varrot, A., and Schülein, M. (2000) Structure and function of Humicola insolens family 6 cellulases: structure of the endoglucanase, Cel6B, at 1.6Aresolution. Biochem. J. 348, 201-207 (Pubitemid 30312149)
30. Brooks, B. R., Brooks, C. L., 3rd, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: the biomolecular simulation program. J. Comput. Chem. 30, 1545-1614
31. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (Pubitemid 128576688)
32. Feig, M., MacKerell, A. D., and Brooks, C. L. (2003) Force field influence on the observation of π-helical protein structures in molecular dynamics simulations. J. Phys. Chem. B 107, 2831-2836
33. Mackerell, A. D., Jr., Feig, M., and Brooks, C. L., 3rd. (2004) 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. J. Comput. Chem. 25, 1400-1415
34. MacKerell, A. D., Jr., Feig, M., and Brooks, C. L., 3rd. (2004) Improved treatment of the protein backbone in empirical force fields. J. Am. Chem. Soc. 126, 698-699 (Pubitemid 38114337)
35. Guvench, O., Greene, S. N., Kamath, G., Brady, J. W., Venable, R. M., Pastor, R. W., and Mackerell, A. D. (2008) Additive empirical force field for hexopyranose monosaccharides. J. Comput. Chem. 29, 2543-2564
36. Guvench, O., Hatcher, E. R., Venable, R. M., Pastor, R. W., and Mackerell, A. D. (2009) CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses. J. Chem. Theory Comput. 5, 2353-2370
37. Jo, S., Kim, T., Iyer, V. G., and Im, W. (2008) CHARMM-GUI: a web-based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859 -1865
38. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593
39. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341
40. Hoover, W. G. (1985) Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A 31, 1695-1697
41. Nose, S. (1984) A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81, 511-519
42. Crowley, M. F., Williamson, M. J., and Walker, R. C. (2009) CHAMBER: comprehensive support for CHARMM force fields within the AMBER software. Int. J. Quantum. Chem. 109, 3767-3772
43. Case, D. A., Cheatham, T. E., 3rd., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The AMBER biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688 (Pubitemid 43076180)
44. Hummer, G. (2001) Fast-growth thermodynamic integration: error and efficiency analysis. J. Chem. Phys. 114, 7330-7337
45. Hummer, G., and Szabo, A. (2001) Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc. Natl. Acad. Sci. U.S.A. 98, 3658-3661 (Pubitemid 32249826)
46. Jarzynski, C. (1997) Nonequilibrium equality for free energy differences. Phys. Rev. Lett. 78, 2690-2693
47. Efron, B., and Tibshirani, R. (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statistical Sci. 1, 54-75
48. Varrot, A., Frandsen, T. P., von Ossowski, I., Boyer, V., Cottaz, S., Driguez, H., Schülein, M., and Davies, G. J. (2003) Structural basis for ligand binding and processivity in cellobiohydrolase Cel6A from Humicola insolens. Structure 11, 855-864 (Pubitemid 36833271)
49. Varrot, A., Macdonald, J., Stick, R. V., Pell, G., Gilbert, H. J., and Davies, G. J. (2003) Distortion of a cellobio-derived isofagomine highlights the potential conformational itinerary of inverting β-glucosidase. Chem. Commun. 946-947 (Pubitemid 36469642)
50. Varrot, A., Schülein, M., and Davies, G. J. (1999) Structural changes of the active site tunnel of Humicola insolens cellobiohydrolase, Cel6A, upon oligosaccharide binding. Biochemistry 38, 8884-8891
51. Du, F., Wolger, E., Wallace, L., Liu, A., Kaper, T., and Kelemen, B. Determination of product inhibition of CBH1, CBH2, and EG1 using a novel cellulase activity assay. Appl. Biochem. Biotechnol. 161, 313-317
52. Van Tilbeurgh, H., Loontiens, F. G., Engelborgs, Y., and Claeyssens, M. (1989) Studies of the cellulolytic system of Trichoderma reesei QM 9414: binding of small ligands to the 1,4-β-glucan cellobiohydrolase II and influence of glucose on their affinity. Eur. J. Biochem. 184, 553-559 (Pubitemid 19260687)
53. Claeyssens, M., Van Tilbeurgh, H., Tomme, P., Wood, T. M., and McRae, S. I. (1989) Fungal cellulase systems: comparison of the specificities of the cellobiohydrolases isolated from Penicillium pinophilum and Trichoderma reesei. Biochem. J. 261, 819-825 (Pubitemid 19209521)
54. Ubhayasekera, W., Muñoz, I. G., Vasella, A., Ståhlberg, J., and Mowbray, S. L. (2005) Structures of Phanerochaete chrysosporium Cel7D in complex with product and inhibitors. FEBS J. 272, 1952-1964 (Pubitemid 40547251)
55. Igarashi, K., Uchihashi, T., Koivula, A., Wada, M., Kimura, S., Okamoto, T., Penttilä, M., Ando, T., and Samejima, M. (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333, 1279-1282
56. Jalak, J., and Väljamäe, P. (2010) Mechanism of initial rapid rate retardation in cellobiohydrolase catalyzed cellulose hydrolysis. Biotechnol. Bioeng. 106, 871-883