Pre-steady-state kinetics for hydrolysis of insoluble cellulose by cellobiohydrolase Cel7A

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18451-18458

  Cruys Bagger, Nicolaj ^a   Elmerdahl, Jens ^a   Praestgaard, Eigil ^a   Tatsumi, Hirosuke ^b   Spodsberg, Nikolaj ^c   Borch, Kim ^c   Westh, Peter ^a  

^a ROSKILDE UNIVERSITY   (Denmark)

^b SHINSHU UNIVERSITY   (Japan)

^c NOVOZYMES A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMPEROMETRIC BIOSENSORS; CELLOBIOHYDROLASE CEL7A; ENZYME COMPLEXES; ENZYME REACTION; ENZYME-SUBSTRATE COMPLEXES; EXPLICIT MODELS; GLYCOSIDIC BOND; HYDROLYTIC ACTIVITIES; NATURAL SUBSTRATES; PROCESSIVITY; PSEUDO STEADY STATE; RATE LIMITING; SPECIFIC ACTIVITY; STEADY STATE; TRANSIENT KINETICS;

BIOSENSORS; CELLULOSE; DISSOCIATION; ENZYMES; KINETICS; RATE CONSTANTS;

HYDROLYSIS;

CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; CELLULOSE 1,4 BETA CELLOBIOSIDASE CEL7A; UNCLASSIFIED DRUG;

AMPEROMETRIC BIOSENSOR; ARTICLE; CATALYSIS; CHEMICAL BINDING; CONTROLLED STUDY; DESORPTION; DISSOCIATION; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; GLYCOSIDIC BONDING; HALF LIFE TIME; HYDROLYSIS; HYPOCREA JECORINA; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FOLDING; QUANTITATIVE STUDY; STEADY STATE;

ADSORPTION; BIOSENSING TECHNIQUES; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; HYDROLYSIS; KINETICS;

EID: 84861552894     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.334946     Document Type: Article

References (40)

1. Johnson, K. A. (1992) in The Enzymes (Sigman, D. S., ed) pp. 1-61, Academic Press, San Diego, CA
2. Abel, M., Planas, A., and Christensen, U. (2001) Pre-steady-state kinetics of Bacillus 1,3-1,4-β-glucanase: binding and hydrolysis of a 4-methylumbelliferyl trisaccharide substrate. Biochem. J. 357, 195-202 (Pubitemid 32642916)
3. Barr, B. K., and Holewinski, R. J. (2002) 4-Methyl-7-thioumbelliferyl- β-D-cellobioside: a fluorescent, non-hydrolyzable substrate analog for cellulases. Biochemistry 41, 4447-4452
4. Kim, Y. S., Kanayama, S., Kawabe, S., and Usami, S. (1983) Enzymatic hydrolysis of cellotetraose by Trichoderma viride cellulase. Experimental study of enzymatic analysis on initial reaction. Waseda Daigaku Rikogaku Kenkyusho Hokoku 104, 29-32
5. Tull, D., and Withers, S. G. (1994) Mechanisms of cellulases and xylanases: a detailed kinetic study of the exo-β-1,4-glycanase from Cellulomonas fimi. Biochemistry 33, 6363-6370 (Pubitemid 24190793)
6. Väljamäe, P., Sild, V., Pettersson, G., and Johansson, G. (1998) The initial kinetics of hydrolysis by cellobiohydrolases I and II is consistent with a cellulose surface erosion model. Eur. J. Biochem. 253, 469-475 (Pubitemid 28191849)
7. Baker, J. O., King, M. R., Adney, W. S., Decker, S. R., Vinzant, T. B., Lantz, S. E., Nieves, R. E., Thomas, S. R., Li, L. C., Cosgrove, D. J., and Himmel, M. E. (2000) Investigation of the cell wall-loosening protein expansin as a possible additive in the enzymatic saccharification of lignocellulosic biomass. Appl. Biochem. Biotechnol. 84, 217-223 (Pubitemid 30349462)
8. 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
9. Hildén, L., Eng, L., Johansson, G., Lindqvist, S. E., and Pettersson, G. (2001) An amperometric cellobiose dehydrogenase-based biosensor can be used for measurement of cellulase activity. Anal. Biochem. 290, 245-250 (Pubitemid 32217535)
10. Ludwig, R., Harreither, W., Tasca, F., and Gorton, L. (2010) Cellobiose dehydrogenase: a versatile catalyst for electrochemical applications. ChemPhysChem 11, 2674-2697
11. Tatsumi, H., Katano, H., and Ikeda, T. (2006) Kinetic analysis of enzymatic hydrolysis of crystalline cellulose by cellobiohydrolase using an amperometric biosensor. Anal. Biochem. 357, 257-261 (Pubitemid 44415696)
12. Praestgaard, E., Elmerdahl, J., Murphy, L., Nymand, S., McFarland, K. C., Borch, K., and Westh, P. (2011) A kinetic model for the burst phase of processive cellulases. FEBS J. 278, 1547-1560
13. Zhang, Y. H., and Lynd, L. R. (2005) Determination of the number-average degree of polymerization of cellodextrins and cellulose with application to enzymatic hydrolysis. Biomacromolecules 6, 1510-1515
14. Murphy, L., Baumann, M. J., Borch, K., Sweeney, M., and Westh, P. (2010) An enzymatic signal amplification system for calorimetric studies of cellobiohydrolases. Anal. Biochem. 404, 140-148
15. Matulova, M., Nouaille, R., Capek, P., Péan, M., Delort, A. M., and Forano, E. (2008) NMR study of cellulose and wheat straw degradation by Ruminococcus albus 20. FEBS J. 275, 3503-3511 (Pubitemid 351813560)
16. Henriksson, G., Sild, V., Szabó, I. J., Pettersson, G., and Johansson, G. (1998) Substrate specificity of cellobiose dehydrogenase from Phanerochaete chrysosporium. Biochim. Biophys. Acta 1383, 48-54 (Pubitemid 28130423)
17. 1H NMR evidence for conversion of β-D-cellobiose to cellobionolactone by cellobiose dehydrogenase from Phanerochaete chrysosporium. FEBS Lett. 351, 128-132
18. Kabayama, M. A., Patterson, D., and Piche, L. (1958) The thermodynamics of mutarotation of some sugars: 1. Measurement of the heat of mutarotation by microcalorimetry. Can. J. Chem. 36, 557-562
19. Karim, N., Okada, H., and Kidokoro, S. (2005) Calorimetric evaluation of the activity and the mechanism of cellulases for the hydrolysis of cellooligosaccharides accompanied by the mutarotation reaction of the hydrolyzed products. Thermochim. Acta 431, 9-20 (Pubitemid 40773883)
20. Jalak, J., and Väljamäe, P. (2010) Mechanism of initial rapid rate retardation in cellobiohydrolase-catalyzed cellulose hydrolysis. Biotechnol. Bioeng. 106, 871-883
21. Bohlin, C., Olsen, S. N., Morant, M. D., Patkar, S., Borch, K., and Westh, P. (2010) A comparative study of activity and apparent inhibition of fungal β-glucosidases. Biotechnol. Bioeng. 107, 943-952
22. 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)
23. Kostylev, M., Moran-Mirabal, J. M., Walker, L. P., and Wilson, D. B. (2012) Determination of the molecular states of the processive endocellulase Thermobifida fusca Cel9A during crystalline cellulose depolymerization. Biotechnol. Bioeng. 109, 295-299
24. 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
25. Kurasin, M., and Väljamäe, P. (2011) Processivity of cellobiohydrolases is limited by the substrate. J. Biol. Chem. 286, 169-177
26. Ma, A., Hu, Q., Qu, Y., Bai, Z., Liu, W., and Zhuang, G. (2008) The enzymatic hydrolysis rate of cellulose decreases with irreversible adsorption of cellobiohydrolase I. Enzyme Microb. Technol. 42, 543-547
27. Harjunpää, V., Teleman, A., Koivula, A., Ruohonen, L., Teeri, T. T., Teleman, O., and Drakenberg, T. (1996) Cello-oligosaccharide hydrolysis by cellobiohydrolase II from Trichoderma reesei. Association and rate constants derived from an analysis of progress curves. Eur. J. Biochem. 240, 584-591 (Pubitemid 26321159)
28. Medve, J., Karlsson, J., Lee, D., and Tjerneld, F. (1998) Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol. Bioeng. 59, 621-634 (Pubitemid 28350464)
29. Medve, J., Ståhlberg, J., and Tjerneld, F. (1994) Adsorption and synergism of cellobiohydrolases I and II of Trichoderma reesei during hydrolysis of microcrystalline cellulose. Biotechnol. Bioeng. 44, 1064-1073 (Pubitemid 24331656)
30. Nidetzky, B., Steiner, W., and Claeyssens, M. (1994) Cellulose hydrolysis by the cellulases from Trichoderma reesei: adsorptions of two cellobiohydrolases, two endocellulases, and their core proteins on filter paper and their relation to hydrolysis. Biochem. J. 303, 817-823 (Pubitemid 24326016)
31. Tomme, P., Heriban, V., and Claeyssens, M. (1990) Adsorption of two cellobiohydrolases from Trichoderma reesei to Avicel: Evidence for "exoexo"synergism and possible "loose complex" formation. Biotechnol. Lett. 12, 525-530 (Pubitemid 20245599)
32. Igarashi, K., Koivula, A., Wada, M., Kimura, S., Penttilä, M., and Samejima, M. (2009) High-speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J. Biol. Chem. 284, 36186-36190
33. 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
34. Wilson, D. B. (2009) Cellulases and biofuels. Curr. Opin. Biotechnol. 20, 295-299
35. Quinlan, R. J., Sweeney, M. D., Lo Leggio, L., Otten, H., Poulsen, J. C., Johansen, K. S., Krogh, K. B., Jørgensen, C. I., Tovborg, M., Anthonsen, A., Tryfona, T., Walter, C. P., Dupree, P., Xu, F., Davies, G. J., and Walton, P. H. (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc. Natl. Acad. Sci. U.S.A. 108, 15079-15084
36. Zhang, Y. H., and Lynd, L. R. (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol. Bioeng. 88, 797-824
37. Eriksson, T., Karlsson, J., and Tjerneld, F. (2002) A model explaining declining rate in hydrolysis of lignocellulose substrates with cellobiohydrolase I (Cel7A) and endoglucanase I (Cel7B) of Trichoderma reesei. Appl. Biochem. Biotechnol. 101, 41-60 (Pubitemid 34460685)
38. Fox, J. M., Levine, S. E., Clark, D. S., and Blanch, H. W. (2012) Initial- and processive-cut products reveal cellobiohydrolase rate limitations and the role of companion enzymes. Biochemistry 51, 442-452
39. Yang, B., Willies, D. M., and Wyman, C. E. (2006) Changes in the enzymatic hydrolysis rate of Avicel cellulose with conversion. Biotechnol. Bioeng. 94, 1122-1128 (Pubitemid 44221057)
40. Murphy, L., Cruys-Bagger, N., Damgaard, H. D., Baumann, M. J., Olsen, S. N., Borch, K., Lassen, S. F., Sweeney, M., Tatsumi, H., and Westh, P. (2012) Origin of initial burst in activity for Trichoderma reesei endoglucanases hydrolyzing insoluble cellulose. J. Biol. Chem. 287, 1252-1260