Structural basis for ligand binding and processivity in cellobiohydrolase Cel6A from Humicola insolens

Structure

Volumn 11, Issue 7, 2003, Pages 855-864

  Varrot, Annabelle ^a   Frandsen, Torben P ^b,d   Von Ossowski, Ingemar ^b   Boyer, Viviane ^c   Cottaz, Sylvain ^c   Driguez, Hugues ^c   Schülein, Martin ^b   Davies, Gideon J ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b NOVOZYMES A S   (Denmark)

^c CNRS   (France)

^d Symphogen AS   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE 1,4 BETA CELLOBIOSIDASE; MUTANT PROTEIN; TRYPTOPHAN;

ARTICLE; ENZYME STRUCTURE; HUMICOLA INSOLENS; HYDROLYSIS; LIGAND BINDING; MOLECULAR INTERACTION; MUTANT; PLANT; PRIORITY JOURNAL; WILD TYPE;

HUMICOLA; HUMICOLA INSOLENS;

EID: 0037478704     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(03)00124-2     Document Type: Article

References (52)

1. Amano Y., Shiroishi M., Nisizawa K., Hoshino E., Kanda T. Fine substrate specificities of four exo-type cellulases produced by Aspergillus niger, Trichoderma reesei, and Irpex lacteus on (1,3), (1,4)-beta-D-glucans and xyloglucan. J. Biochem. 120:1996;1123-1129.
2. Boisset C., Armand S., Drouillard H., Chanzy H., Driguez H., Henrissat B. Structure-function relationships in cellulases. the enzymatic degradation of insoluble cellulose Claeyssens M., Piens K., Nerinckx W. Carbohydrases from Trichoderma reesei and Other Microorganisms. 1998;Royal Society of Chemistry, London. 124-132.pp.
3. Boraston A.B., Nurizzo D., Notenboom V., Ducros V., Rose D.R., Kilburn D.G., Davies G.J. Differential oligosaccharide recognition by evolutionarily-related β-1,4 and β-1,3 glucan binding domains. J. Mol. Biol. 319:2002;1143-1156.
4. Boyer, V. (1999). Synthèses d'analogues de substrat pour l'étude des cellulases. PhD Thesis, University of Grenoble, France.
5. Brünger A.T. Free R value - a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475.
6. Charnock S.J., Bolam D.N., Nurizzo D., Szabo L., McKie V.A., Gilbert H.J., Davies G.J. Promiscuity in ligand binding. the three-dimensional structure of a Piromyces carbohydrate-binding module, CBM29-2, in complex with cello- and mannohexaose Proc. Natl. Acad. Sci. USA. 99:2002;14077-14082.
7. Christensen T., Wöldike H., Boel E., Mortensen S.B., Hjortshøj K., Thim L., Hansen M.T. High level expression of recombinant genes in Aspergillus oryzae. Biotechnology. 6:1988;1419-1422.
8. CCP4 The (Collaborative Computational Project, Number 4) CCP4 suite. programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50:1994;760-763.
9. Coutinho P.M., Henrissat B. Carbohydrates-active enzymes. an integrated database approach Gilbert H.J., Davies G.J., Henrissat B., Svensson B. Proceedings of the 3rd Carbohydrate Bioengineering Meeting on Recent Advances in Carbohydrate Bioengineering. 1999;Royal Society of Chemistry, Cambridge. 3-12.pp.
10. Damude H.G., Withers S.G., Kilburn D.G., Miller R.C. Jr., Warren R.A. Site-directed mutation of the putative catalytic residues of endoglucanase CenA from Cellulomonas fimi. Biochemistry. 34:1995;2220-2224.
11. Davies G.J., Henrissat B. Structures and mechanisms of glycosyl hydrolases. Structure. 3:1995;853-859.
12. Davies G., Sinnott M.L., Withers S.G. Glycosyl transfer. Sinnott M.L. Comprehensive Biological Catalysis. 1997;Academic Press, London. 119-209.pp.
13. Esnouf R.M. An extensively modified version of MolScript that includes greatly enhanced colouring capabilities. J. Mol. Graph. 15:1997;133-138.
14. Gessler K., Krauss N., Steiner T., Betzel C., Sandmann C., Saenger W. Crystal structure of beta-D-cellotetraose hemihydrate with implications for the structure of cellulose II. Science. 266:1994;1027-1029.
15. Henrissat B. Enzymatic cellulose degradation. Cellulose Commun. 5:1998;84-90.
16. Henrissat B., Bairoch A. Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316:1996;695-696.
17. Imai Y., Matsushima Y., Sugimura T., Terada M. A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res. 19:1991;2785.
18. Kelly J.M., Hynes M.J. Transformation of Aspergillus niger by the amdS gene of Aspergillus nidulans. EMBO J. 4:1985;475-479.
19. Kleywegt G.J., Jones T.A. A super position. ESF/CCP. 4(Newsletter 31):1994;9-14.
20. Kleywegt G.J., Jones T.A. Phi/psi-chology. Ramachandran revisited Structure. 4:1996;1395-1400.
21. Koivula A., Kinnari T., Harjunpaa V., Ruohonen L., Teleman A., Drakenberg T., Rouvinen J., Jones T.A., Teeri T.T. Tryptophan 272. an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A FEBS Lett. 429:1998;341-346.
22. Koivula A., Ruohonen L., Wohlfahrt G., Reinikainen T., Teeri T.T., Piens K., Claeyssens M., Weber M., Vasella A., Becker D.et al. The active site of cellobiohydrolase Cel6A from Trichoderma reesei. the roles of aspartic acids D221 and D175 J. Am. Chem. Soc. 124:2002;10015-10024.
23. Koshland D.E. Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. 28:1953;416-436.
24. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
25. Lamzin V.S., Wilson K.S. Automated refinement of protein models. Acta Crystallogr. D Biol Crystallogr. 49:1993;129-147.
26. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:1993;283-291.
27. Lehtio J., Sugiyama J., Gustavsson M., Fransson L., Linder M., Teeri T.T. The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc. Natl. Acad. Sci. USA. 100:2003;484-489.
28. Mielenz J.R. Ethanol production from biomass. technology and commercialization status Curr. Opin. Microbiol. 4:2001;324-329.
29. Miettinen-Oinonen A., Suominen P. Enhanced production of Trichoderma reesei endoglucanases and use of the new cellulase preparations in producing the stonewashed effect on denim fabric. Appl. Environ. Microbiol. 68:2002;3956-3964.
30. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:1997;240-255.
31. Navaza J., Saludjian P. AMoRe. an automated molecular replacement program package Methods Enzymol. 276:1997;581-594.
32. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
33. Parsiegla G., Reverbel-Leroy C., Tardif C., Belaich J.P., Driguez H., Haser R. Crystal structures of the cellulase Cel48F in complex with inhibitors and substrates give insights into its processive action. Biochemistry. 39:2000;11238-11246.
34. Read R.J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A. 42:1986;140-149.
35. Reverbel-Leroy C., Parsiegla G., Moreau V., Juy M., Tardif C., Driguez H., Bélaich J.-P., Haser R. Crystallisation of the catalytic domain of Clostridium cellulolyticum CelF cellulase in the presence of a newly synthesized cellulase inhibitor. Acta Crystallogr. D Biol. Crystallogr. 54:1998;114-118.
36. Rouvinen J., Bergfors T., Teeri T., Knowles J.K., Jones T.A. Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science. 249:1990;380-386.
37. Ruohonen, L., Koivula, A., Reinikainen, T., Valkejärvi, A., Teleman, A., Claeyssens, M., Szardenings, M., Jones, T.A., and Teeri, T.T. (1993). Active site of T. reesei cellobiohydrolase II. In Proceedings of the Second TRICEL Symposium on Trichoderma reesei Cellulases and Other Hydrolases, P. Suominen and T. Reinikainen, eds. (Espoo, Finland: Foundation for Biotechnical and Industrial Fermentation Research), pp. 87-96.
38. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning, A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Schou C., Rasmussen G., Schülein M., Henrissat B., Driguez H. 4-thiocellooligosaccharides - their synthesis and use as inhibitors of cellulases. J. Carbohydr. Chem. 12:1993;743-752.
40. Sinnott M.L. Catalytic mechanism of enzymic glycosyl transfer. Chem. Rev. 90:1990;1171.
41. Ståhlberg J., Johansson G., Pettersson G. Trichoderma reesei has no true exo-cellulase. all intact and truncated cellulases produce new reducing end groups on cellulose Biochim. Biophys. Acta. 1157:1993;107-113.
42. Tomme P., Warren R.A., Gilkes N.R. Cellulose hydrolysis by bacteria and fungi. Adv. Microb. Physiol. 37:1995;1-81.
43. Varrot A., Hastrup S., Schülein M., Davies G.J. Crystal structure of the catalytic core domain of the family 6 cellobiohydrolase II, Cel6A, from Humicola insolens, at 1.92 Å resolution. Biochem. J. 337:1999;297-304. a.
44. Varrot A., Schülein M., Davies G.J. Structural changes of the active site tunnel of Humicola insolens cellobiohydrolase, Cel6A, upon oligosaccharide binding. Biochemistry. 38:1999;8884-8891. b.
45. Varrot A., Frandsen T., Driguez H., Davies G.J. Structure of the Humicola insolens cellobiohydrolase Cel6A D416A mutant in complex with a non-hydrolysable substrate analogue, methyl-cellobiosyl-4-thio-β-cellobioside at 1.9 Å Acta Crystallogr. D Biol. Crystallogr. 58:2002;2201-2204.
46. Varrot, A., Macdonald, J., Stick, R.V., Pell, P., Gilbert, H.J., and Davies, G.J. (2003). Distortion of a cellobio-derived isofagomine highlights the potential conformational itinerary of inverting β-glucosidases. Chem. Commun. 946-947.
47. Vyas N.K. Atomic features of protein-carbohydrate interactions. Curr. Opin. Struct. Biol. 1:1991;732-740.
48. Winn M.D., Isupov M.N., Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. D57:2001;122-133.
49. Wolfenden R., Lu X., Young G. Spontaneous hydrolysis of glycosides. J. Am. Chem. Soc. 120:1998;6814-6815.
50. Wolfgang D.E., Wilson D.B. Mechanistic studies of active site mutants of Thermomonospora fusca endocellulase E2. Biochemistry. 38:1999;9746-9751.
51. Xie H.F., Gilbert H.J., Charnock S.J., Davies G.J., Williamson M.P., Simpson P.J., Raghothama S., Fontes C., Dias F.M.V., Ferreira L.M.A.et al. Clostridium thermocellum Xyn10B carbohydrate-binding module 22-2. the role of conserved amino acids in ligand binding Biochemistry. 40:2001;9167-9176.
52. Zou J., Kleywegt G.J., Stahlberg J., Driguez H., Nerinckx W., Claeyssens M., Koivula A., Teeri T.T., Jones T.A. Crystallographic evidence for substrate ring distortion and protein conformational changes during catalysis in cellobiohydrolase Cel6A from Trichoderma reesei. Structure. 7:1999;1035-1045.