Binding and movement of individual Cel7A cellobiohydrolases on crystalline cellulose surfaces revealed by single-molecule fluorescence imaging

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 24164-24172

  Jung, Jaemyeong ^a   Sethi, Anurag ^b   Gaiotto, Tiziano ^a   Han, Jason J ^a   Jeoh, Tina ^c   Gnanakaran, Sandrasegaram ^b   Goodwin, Peter M ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLOBIOHYDROLASES; CELLULOSE HYDROLYSIS; CELLULOSE SURFACES; CRYSTALLINE CELLULOSE; MOLECULAR LEVEL MECHANISMS; SINGLE-MOLECULE FLUORESCENCES; SINGLE-MOLECULE IMAGING;

MOLECULES;

CELLULOSE;

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

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING KINETICS; BIOCATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; HYDROLYSIS KINETICS; HYPOCREA JECORINA; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; SINGLE MOLECULE FLUORESCENCE IMAGING; SURFACE PROPERTY;

BIOENERGY; BIOFUEL; CELLULASE; CELLULOSE; FLUORESCENCE; MOLECULAR IMAGING; SINGLE MOLECULE;

ADSORPTION; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME INHIBITORS; FLUORESCENCE; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; OPTICAL IMAGING; PROTEIN BINDING; PROTEIN TRANSPORT; SOLUBILITY; SUBSTRATE SPECIFICITY; SURFACE PROPERTIES; TIME FACTORS; TRICHODERMA;

EID: 84882415685     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455758     Document Type: Article

References (35)

1. (2006) Breaking the biological barriers to cellulosic ethanol. A joint research agenda. Report from the December 2005 workshop, DOE/SC-0095. U.S. Department of Energy Office of Science
2. Zhang, Y.-H. P., and Lynd, L. R. (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose. Noncomplexed cellulase systems. Biotechnol. Bioeng. 88, 797-824
3. 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
4. Henrissat, B., Teeri, T. T., and Warren, R. A. (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett. 425, 352-354
5. Jeoh, T., Ishizawa, C. I., Davis, M. F., Himmel, M. E., Adney, W. S., and Johnson, D. K. (2007) Cellulase digestibility of pretreated biomass is limited by cellulose accessibility. Biotechnol. Bioeng. 98, 112-122
6. Medve, J., Lee, D., and Tjerneld, F. (1998) Ion-exchange chromatographic purification and quantitative analysis of Trichoderma reesei cellulases cellobiohydrolase I, II and endoglucanase II by fast protein liquid chromatography. J. Chromatogr. A 808, 153-165
7. Sangseethong, K., and Penner, M. H. (1998) p-Aminophenyl-cellobioside as an affinity ligand for exo-type cellulases. Carbohydr. Res. 314, 245-250
8. Jeoh, T., Wilson, D. B., and Walker, L. P. (2002) Cooperative and competitive binding in synergistic mixtures of Thermobifida fusca cellulases Cel5A, Cel6B, and Cel9A. Biotechnol. Prog. 18, 760-769
9. Moran-Mirabal, J. M., Bolewski, J. C., and Walker, L. P. (2011) Reversibility and binding kinetics of Thermobifida fusca cellulases studied through fluorescence recovery after photobleaching microscopy. Biophys. Chem. 155, 20-28
10. Doner, L. W., and Irwin, P. L. (1992) Assay of reducing end-groups in oligosaccharide homologs with 2,2-bicinchoninate. Anal. Biochem. 202, 50-53
11. Chernoglazov, V. M., Jafarova, A. N., and Klyosov, A. A. (1989) Continuous photometric determination of endo-1,4-D-glucanase (cellulase) activity using 4-methylumbelliferyl-D-cellobioside as a substrate. Anal. Biochem. 179, 186-189
12. 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
13. Helbert, W., Chanzy, H., Husum, T. L., Schülein, M., and Ernst, S. (2003) Fluorescent cellulose microfibrils as substrate for the detection of cellulase activity. Biomacromolecules 4, 481-487
14. Santa-Maria, M., and Jeoh, T. (2010) Molecular-scale investigations of cellulose microstructure during enzymatic hydrolysis. Biomacromolecules 11, 2000-2007
15. Lavenson, D. M., Tozzi, E. J., McCarthy, M. J., Powell, R. L., and Jeoh, T. (2011) Investigating adsorption of bovine serum albumin on cellulosic substrates using magnetic resonance imaging. Cellulose 18, 1543-1554
16. Yang, B., and Wyman, C. E. (2006) BSA treatment to enhance enzymatic hydrolysis of cellulose in lignin containing substrates. Biotechnol. Bioeng. 94, 611-617
17. Zhang, Y., Sivasankar, S., Nelson, W. J., and Chu, S. (2009) Resolving cadherin interactions and binding cooperativity at the single-molecule level. Proc. Natl. Acad. Sci. U.S.A. 106, 109-114
18. Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifacino, J. S., Davidson, M. W., Lippincott-Schwartz, J., and Hess, H. F. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645
19. Sharonov, A., and Hochstrasser, R. M. (2006) Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc. Natl. Acad. Sci. U.S.A. 103, 18911-18916
20. Thompson, R. E., Larson, D. R., and Webb, W. W. (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82, 2775-2783
21. Chanzy, H., Henrissat, B., and Vuong, R. (1984) Colloidal gold labelling of l,4-D-glucan cellobiohydrolase adsorbed on cellulose substrates. FEBS Lett. 172, 193-197
22. Chanzy, H., Henrissat, B., Vuong, R., and Schülein, M. (1983) The action of 1,4-D-glucan cellobiohydrolase on Valonia cellulose microcrystals. An electron microscopic study. FEBS Lett. 153, 113-118
23. 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
24. Boer, H., and Koivula, A. (2003) The relationship between thermal stability and pH optimum studied with wild-type and mutant Trichoderma reesei cellobiohydrolase Cel7A. Eur. J. Biochem. 270, 841-848
25. Lehtiö, J., Sugiyama, J., Gustavsson, M., Fransson, L., Linder, M., and Teeri, T. T. (2003) The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc. Natl. Acad. Sci. U.S.A. 100, 484-489
26. 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
27. 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
28. Kurasin, M., and Väljamäe, P. (2011) Processivity of cellobiohydrolases is limited by the substrate. J. Biol. Chem. 286, 169-177
29. Cruys-Bagger, N., Elmerdahl, J., Praestgaard, E., Tatsumi, H., Spodsberg, N., Borch, K., and Westh, P. (2012) Pre-steady-state kinetics for hydrolysis of insoluble cellulose by cellobiohydrolase Cel7A. J. Biol. Chem. 287, 18451-18458
30. 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
31. Sugimoto, N., Igarashi, K., Wada, M., and Samejima, M. (2012) Adsorption characteristics of fungal family 1 cellulose-binding domain from Trichoderma reesei cellobiohydrolase I on crystalline cellulose. Negative cooperative adsorption via a steric exclusion effect. Langmuir 28, 14323-14329
32. 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. Eur. J. Biochem. 170, 575-581
33. Van Tilbeurgh, H., Tomme, P., Claeyssens, M., Bhikhabhai, R., and Pettersson, G. (1986) Limited proteolysis of the cellobiohydrolase I from Trichoderma reesei. Separation of functional domains. FEBS Lett. 204, 223-227
34. Linder, M., and Teeri, T. T. (1996) The cellulose-binding domain of the major cellobiohydrolase of Trichoderma reesei exhibits true reversibility and a high exchange rate on crystalline cellulose. Proc. Natl. Acad. Sci. U.S.A. 93, 12251-12255
35. Bu, L., Nimlos, M. R., Shirts, M. R., StAhlberg, J., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2012) Product binding baries dramatically between processive and nonprocessive cellulase enzymes. J. Biol. Chem. 287, 24807-24813