Single-molecule imaging analysis of elementary reaction steps of trichoderma reesei cellobiohydrolase i (Cel7A) hydrolyzing crystalline cellulose Iα and IIII

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 14056-14065

  Shibafuji, Yusuke ^a   Nakamura, Akihiko ^b   Uchihashi, Takayuki ^c   Sugimoto, Naohisa ^b   Fukuda, Shingo ^c   Watanabe, Hiroki ^c   Samejima, Masahiro ^b   Ando, Toshio ^c   Noji, Hiroyuki ^a   Koivula, Anu ^d   Igarashi, Kiyohiko ^b   Iino, Ryota ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KANAZAWA UNIVERSITY   (Japan)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; CRYSTALLINE MATERIALS; DISSOCIATION; ENZYMES; HYDROLYSIS; RATE CONSTANTS; SUBSTRATES; SURFACE CHEMISTRY;

CELLOBIOHYDROLASE I; CRYSTALLINE CELLULOSE; DISSOCIATION RATE CONSTANT; ENZYME CONCENTRATIONS; HYDROPHOBIC SURFACES; SINGLE-MOLECULE FLUORESCENCE MICROSCOPY; SINGLE-MOLECULE IMAGING; SOLID/LIQUID INTERFACES;

CELLULOSE;

CELLOBIOHYDROLASE I; CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; CRYSTALLINE CELLULOSE I ALPHA; CRYSTALLINE CELLULOSE III IOTA; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVITY; ENZYME BINDING; FLUORESCENCE MICROSCOPY; HYDROPHOBICITY; HYPOCREA JECORINA; IMAGE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; CHEMICAL PHENOMENA; CHEMISTRY; ENZYMOLOGY; HYDROLYSIS; KINETICS; METABOLISM; TRICHODERMA;

CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; HYDROLYSIS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; TRICHODERMA;

EID: 84901050607     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.546085     Document Type: Article

References (40)

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. 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
3. Wilson, D. B. (2009) Cellulases and biofuels. Curr. Opin. Biotechnol. 20, 295-299
4. Wilson, D. B. (2012) Processive and nonprocessive cellulases for biofuel production: lessons from bacterial genomes and structural analysis. Appl. Microbiol. Biotechnol. 93, 497-502
5. Tomme, P., Van Tilbeurgh, H., Pettersson, G., Van Damme, J., Vandekerckhove, J., Knowles, J., Teeri, T., and Claeyssens, M. (1988) Studies of the cellulolytic system of Trichoderma reesei QM 9414: analysis of domain function in two cellobiohydrolases by limited proteolysis. Eur. J. Biochem. 170, 575-581
6. Reinikainen, T., Teleman, O., and Teeri, T. T. (1995) Effects of pH and high ionic strength on the adsorption and activity of native and mutated cellobiohydrolase I from Trichoderma reesei. Proteins 22, 392-403
7. 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
8. 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
9. Igarashi, K., Wada, M., and Samejima, M. (2007) Activation of crystalline cellulose to cellulose IIII results in efficient hydrolysis by cellobiohydrolase. FEBS J. 274, 1785-1792
10. Wada, M., Heux, L., Isogai, A., Nishiyama, Y., Chanzy, H., and Sugiyama, J. (2001) Improved structural data of cellulose IIII prepared in supercritical ammonia. Macromolecules 34, 1237-1243
11. Nishiyama, Y., Sugiyama, J., Chanzy, H., and Langan, P. (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron x-ray and neutron fiber diffraction. J. Am. Chem. Soc. 125, 14300-14306
12. Wada, M., Chanzy, H., Nishiyama, Y., and Langan, P. (2004) Cellulose IIII crystal structure and hydrogen bonding by synchrotron x-ray and neutron fiber diffraction. Macromolecules 37, 8548-8555
13. Wada, M., Nishiyama, Y., and Langan, P. (2006) X-ray structure of ammonia- cellulose I: new insights into the conversion of cellulose I to cellulose IIII. Macromolecules 39, 2947-2952
14. Chundawat, S. P., Bellesia, G., Uppugundla, N., da Costa Sousa, L., Gao, D., Cheh, A. M., Agarwal, U. P., Bianchetti, C. M., Phillips, G. N., Jr., Langan, P., Balan, V., Gnanakaran, S., and Dale, B. E. (2011) Restructuring the crystalline cellulose hydrogen bond network enhances its depolymerization rate. J. Am. Chem. Soc. 133, 11163-11174
15. 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
16. Gao, D., Chundawat, S. P., Sethi, A., Balan, V., Gnanakaran, S., and Dale, B. E. (2013) Increased enzyme binding to substrate is not necessary for more efficient cellulose hydrolysis. Proc Natl. Acad. Sci. U.S.A. 110, 10922-10927
17. Payne, C. M., Jiang, W., Shirts, M. R., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2013) Glycoside hydrolase processivity is directly related to oligosaccharide binding free energy. J. Am. Chem. Soc. 135, 18831-18839
18. Divne, C., Sinning, I., Stahlberg, J., Pettersson, G., Bailey, M., Siika-aho, M., Margolles-Clark, E., Teeri, T., and Jones, T. A. (1993) Crystallization and preliminary x-ray studies on the core proteins of cellobiohydrolase I and endoglucanase I from Trichoderma reesei. J. Mol. Biol. 234, 905-907
19. Srisodsuk, M., Reinikainen, T., Penttilä, M., and Teeri, T. T. (1993) Role of the interdomain linker peptide of Trichoderma reesei cellobiohydrolase I in its interaction with crystalline cellulose. J. Biol. Chem. 268, 20756-20761
20. Kremer, S. M., and Wood, P. M. (1992) Evidence that cellobiose oxidase from Phanerochaete chrysosporium is primarily an Fe(III) reductase: kinetic comparison with neutrophil NADPH oxidase and yeast flavocytochrome b2. Eur. J. Biochem. 205, 133-138
21. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
22. Igarashi, K., Wada, M., Hori, R., and Samejima, M. (2006) Surface density of cellobiohydrolase on crystalline celluloses: a critical parameter to evaluate enzymatic kinetics at a solid-liquid interface. FEBS J. 273, 2869-2878
23. Wada, M., Okano, T., and Sugiyama, J. (2001) Allomorphs of native crystalline cellulose I evaluated by two equatorial d-spacings. J. Wood Sci. 47, 124-128
24. Tenkanen, M., Makkonen, M., Perttula, M., Viikari, L., and Teleman, A. (1997) Action of Trichoderma reesei mannanase on galactoglucomannan in pine kraft pulp. J. Biotechnol. 57, 191-204
25. Nishizaka, T., Hasimoto, Y., and Masaike, T. (2011) Simultaneous observation of chemomechanical coupling of a molecular motor. Methods Mol. Biol. 778, 259-271
26. Adachi, K., Oiwa, K., Nishizaka, T., Furuike, S., Noji, H., Itoh, H., Yoshida, M., and Kinosita, K. (2007) Coupling of rotation and catalysis in F1- ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321
27. Fukuda, S., Uchihashi, T., Iino, R., Okazaki, Y., Yoshida, M., Igarashi, K., and Ando, T. (2013) High-speed atomic force microscope combined with single-molecule fluorescence microscope. Rev. Sci. Instrum. 84, 073706
28. Kurasin, M., and Väljamäe, P. (2011) Processivity of cellobiohydrolases is limited by the substrate. J. Biol. Chem. 286, 169-177
29. Jalak, J., and Väljamäe, P. (2010) Mechanism of initial rapid rate retardation in cellobiohydrolase-catalyzed cellulose hydrolysis. Biotechnol. Bioeng. 106, 871-883
30. Cruys-Bagger, N., Tatsumi, H., Ren, G. R., Borch, K., and Westh, P. (2013) Transient kinetics and rate-limiting steps for the processive cellobiohydrolase Cel7A: effects of substrate structure and carbohydrate binding domain. Biochemistry 52, 8938-8948
31. 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
32. Yanagisawa, M., Shibata, I., and Isogai, A. (2005) SEC-MALLS analysis of softwood kraft pulp using LiCl/1,3-dimethyl-2-imidazolidinone as an eluent. Cellulose 12, 151-158
33. Nakamura, A., Watanabe, H., Ishida, T., Uchihashi, T., Wada, M., Ando, T., Igarashi, K., and Samejima, M. (2014) Trade-off between processivity and hydrolytic velocity of cellobiohydrolases at the surface of crystalline cellulose. J. Am. Chem. Soc. 136, 4584-4592
34. Jalak, J., Kurašin, M., Teugjas, H., and Väljamäe, P. (2012) Endo-exo synergism in cellulose hydrolysis revisited. J. Biol. Chem. 287, 28802-28815
35. Bustamante, C., Chemla, Y. R., Forde, N. R., and Izhaky, D. (2004) Mechanical processes in biochemistry. Annu. Rev. Biochem. 73, 705-748
36. Greenleaf, W. J., Woodside, M. T., and Block, S. M. (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36, 171-190
37. Uchihashi, T., Iino, R., Ando, T., and Noji, H. (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755-758
38. Ando, T., Uchihashi, T., and Kodera, N. (2013) High-speed AFM and applications to biomolecular systems. Annu. Rev. Biophys. 42, 393-414
39. Ueno, H., Nishikawa, S., Iino, R., Tabata, K. V., Sakakihara, S., Yanagida, T., and Noji, H. (2010) Simple dark-field microscopy with nanometer spatial precision and microsecond temporal resolution. Biophys. J. 98, 2014-2023
40. Minagawa, Y., Ueno, H., Hara, M., Ishizuka-Katsura, Y., Ohsawa, N., Terada, T., Shirouzu, M., Yokoyama, S., Yamato, I., Muneyuki, E., Noji, H., Murata, T., and Iino, R. (2013) Basic properties of rotary dynamics of the molecular motor Enterococcus hirae V1-ATPase. J. Biol. Chem. 288, 32700-32707 Technology Technology Technology Technology Technology Technology