Initial recognition of a cellodextrin chain in the cellulose-binding tunnel may affect cellobiohydrolase directional specificity

Biophysical Journal

Volumn 104, Issue 4, 2013, Pages 904-912

  Ghattyvenkatakrishna, Pavan K ^a,b   Alekozai, Emal M ^b,c   Beckham, Gregg T ^d,e   Schulz, Roland ^b,f   Crowley, Michael F ^b,d   Uberbacher, Edward C ^a,b   Cheng, Xiaolin ^b,f  

^a Computational Biology and Bioinformatics Group ^*  (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^e Department of Geology and Geological Engineering   (United States)

^f UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLODEXTRIN; CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; DEXTRIN; DRUG DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; HYPOCREA; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN BINDING;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; DEXTRINS; HYPOCREA; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 84874159970     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.12.052     Document Type: Article

References (57)

1. A. Vasella, G.J. Davies, and M. Böhm Glycosidase mechanisms Curr. Opin. Chem. Biol. 6 2002 619 629
2. E.A. Bayer, and H. Chanzy Y. Shoham Cellulose, cellulases and cellulosomes Curr. Opin. Struct. Biol. 8 1998 548 557
3. K. Igarashi, and A. Koivula M. Samejima High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose J. Biol. Chem. 284 2009 36186 36190
4. K. Igarashi, and T. Uchihashi M. Samejima Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface Science 333 2011 1279 1282
5. J. Jalak, and P. Väljamäe Mechanism of initial rapid rate retardation in cellobiohydrolase catalyzed cellulose hydrolysis Biotechnol. Bioeng. 106 2010 871 883
6. M. Kurašin, and P. Väljamäe Processivity of cellobiohydrolases is limited by the substrate J. Biol. Chem. 286 2011 169 177
7. J. Jalak, and M. Kurašin P. Väljamäe Endo-exo synergism in cellulose hydrolysis revisited J. Biol. Chem. 287 2012 28802 28815
8. J. Stahlberg, G. Johansson, and G. Pettersson A new model for enzymatic-hydrolysis of cellulose based on the 2-domain structure of cellobiohydrolase-I Nat. Biotechnol. 9 1991 286 290
9. H. Chanzy, and B. Henrissat M. Schulein The action of 1,4-beta-D-glucan cellobiohydrolase on valonia cellulose micro-crystals - an electron-microscopic study FEBS Lett. 153 1983 113 118
10. B.K. Barr, and Y.-L. Hsieh D.B. Wilson Identification of two functionally different classes of exocellulases Biochemistry 35 1996 586 592
11. C.S. Rye, and S.G. Withers Glycosidase mechanisms Curr. Opin. Chem. Biol. 4 2000 573 580
12. C. Divne, and J. Ståhlberg T.A. Jones High-resolution crystal structures reveal how a cellulose chain is bound in the 50 A long tunnel of cellobiohydrolase I from Trichoderma reesei J. Mol. Biol. 275 1998 309 325
13. W. Ubhayasekera, and I.G. Muñoz S.L. Mowbray Structures of Phanerochaete chrysosporium Cel7D in complex with product and inhibitors FEBS J. 272 2005 1952 1964
14. J. Ståhlberg, and C. Divne T.A. Jones Activity studies and crystal structures of catalytically deficient mutants of cellobiohydrolase I from Trichoderma reesei J. Mol. Biol. 264 1996 337 349
15. J. Rouvinen, and T. Bergfors T.A. Jones Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei Science 249 1990 380 386
16. C. Divne, and J. Ståhlberg T.A. Jones The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei Science 265 1994 524 528
17. B.G. Guimarães, and H. Souchon P.M. Alzari The crystal structure and catalytic mechanism of cellobiohydrolase CelS, the major enzymatic component of the Clostridium thermocellum Cellulosome J. Mol. Biol. 320 2002 587 596
18. A. Koivula, and T. Kinnari T.T. Teeri Tryptophan 272: an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A FEBS Lett. 429 1998 341 346
19. I. von Ossowski, and J. Ståhlberg T.T. Teeri Engineering the exo-loop of Trichoderma reesei cellobiohydrolase, Cel7A. A comparison with Phanerochaete chrysosporium Cel7D J. Mol. Biol. 333 2003 817 829
20. J.M. Fox, and S.E. Levine H.W. Blanch Initial- and processive-cut products reveal cellobiohydrolase rate limitations and the role of companion enzymes Biochemistry 51 2012 442 452
21. D. Martinez, and R.M. Berka T.S. Brettin Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina) Nat. Biotechnol. 26 5 2008 553 560
22. J. Kraulis, and G.M. Clore A.M. Gronenborn Determination of the three-dimensional solution structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing Biochemistry 28 1989 7241 7257
23. G.T. Beckham, and Y.J. Bomble M.F. Crowley The O-glycosylated linker from the Trichoderma reesei Family 7 cellulase is a flexible, disordered protein Biophys. J. 99 2010 3773 3781
24. M.J. Harrison, and A.S. Nouwens N.H. Packer Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei Eur. J. Biochem. 256 1998 119 127
25. H. Henriksson, and J. Stahlberg R. Isaksson The catalytic amino-acid residues in the active site of cellobiohydrolase 1 are involved in chiral recognition J. Biotechnol. 57 1997 115 125
26. G.J. Kleywegt, and J.Y. Zou T.A. Jones The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 A resolution, and a comparison with related enzymes J. Mol. Biol. 272 1997 383 397
27. A. Koivula, and T. Reinikainen T.T. Teeri The active site of Trichoderma reesei cellobiohydrolase II: the role of tyrosine 169 Protein Eng. 9 1996 691 699
28. S.P. Chundawat, and G.T. Beckham B.E. Dale Deconstruction of lignocellulosic biomass to fuels and chemicals Annu. Rev. Chem. Biomol. Eng. 2 2011 121 145
29. G.T. Beckham, and Y.J. Bomble M.F. Crowley Applications of computational science for understanding enzymatic deconstruction of cellulose Curr. Opin. Biotechnol. 22 2011 231 238
30. G.T. Beckham, and J.F. Matthews M.F. Crowley Identification of amino acids responsible for processivity in a Family 1 carbohydrate-binding module from a fungal cellulase J. Phys. Chem. B 114 2010 1447 1453
31. L. Bu, and G.T. Beckham M.R. Nimlos The energy landscape for the interaction of the family 1 carbohydrate-binding module and the cellulose surface is altered by hydrolyzed glycosidic bonds J. Phys. Chem. B 113 2009 10994 11002
32. C.B. Taylor, and M.F. Talib G.T. Beckham Computational investigation of glycosylation effects on a family 1 carbohydrate-binding module J. Biol. Chem. 287 2012 3147 3155
33. M.R. Nimlos, and G.T. Beckham M.F. Crowley Binding preferences, surface attachment, diffusivity, and orientation of a family 1 carbohydrate-binding module on cellulose J. Biol. Chem. 287 2012 20603 20612
34. C.B. Barnett, K.A. Wilkinson, and K.J. Naidoo Molecular details from computational reaction dynamics for the cellobiohydrolase I glycosylation reaction J. Am. Chem. Soc. 133 2011 19474 19482
35. C.B. Barnett, K.A. Wilkinson, and K.J. Naidoo Pyranose ring transition state is derived from cellobiohydrolase I induced conformational stability and glycosidic bond polarization J. Am. Chem. Soc. 132 2010 12800 12803
36. C.L. Ting, D.E. Makarov, and Z.-G. Wang A kinetic model for the enzymatic action of cellulase J. Phys. Chem. B 113 2009 4970 4977
37. Y. Lin, and J. Silvestre-Ryan J.W. Chu Protein allostery at the solid-liquid interface: endoglucanase attachment to cellulose affects glucan clenching in the binding cleft J. Am. Chem. Soc. 133 2011 16617 16624
38. L. Bu, and G.T. Beckham M.F. Crowley Probing carbohydrate product expulsion from a processive cellulase with multiple absolute binding free energy methods J. Biol. Chem. 286 2011 18161 18169
39. L.T. Bu, and M.R. Nimlos G.T. Beckham Product binding varies dramatically between processive and nonprocessive cellulase enzymes J. Biol. Chem. 287 2012 24807 24813
40. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
41. A.D. MacKerell, and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
42. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd 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 2004 1400 1415
43. O. Guvench, and E.R. Hatcher A.D. Mackerell CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses J. Chem. Theory Comput. 5 2009 2353 2370
44. T. Darden, D. York, and L. Pedersen Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
45. M. Tuckerman, B. Berne, and G. Martyna Reversible multiple time scale molecular dynamics J. Chem. Phys. 97 1992 1990 2001
46. J.P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
47. S. Kumar, and D. Bouzida J.M. Rosenberg The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method J. Comput. Chem. 13 1992 1011 1021
48. H.S. Ashbaugh, and L.R. Pratt T.L. Beck Deblurred observation of the molecular structure of an oil-water interface J. Am. Chem. Soc. 127 2005 2808 2809
49. S.T. Lin, M. Blanco, and W.A. Goddard The two-phase model for calculating thermodynamic properties of liquids from molecular dynamics: validation for the phase diagram of Lennard-Jones fluids J. Chem. Phys. 119 2003 11792 11805
50. S.T. Lin, P.K. Maiti, and W.A. Goddard 3rd Two-phase thermodynamic model for efficient and accurate absolute entropy of water from molecular dynamics simulations J. Phys. Chem. B 114 2010 8191 8198
51. L. Petridis, R. Schulz, and J.C. Smith Simulation analysis of the temperature dependence of lignin structure and dynamics J. Am. Chem. Soc. 133 2011 20277 20287
52. G.M. Torrie, and J.P. Valleau Non-physical sampling distributions in Monte-Carlo free-energy estimation: umbrella sampling J. Comput. Phys. 23 1977 187 199
53. G.T. Beckham, and J.F. Matthews M.F. Crowley Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs J. Phys. Chem. B 115 2011 4118 4127
54. D.F. Gauto, and S. Di Lella M.A. Martí Carbohydrate-binding proteins: dissecting ligand structures through solvent environment occupancy J. Phys. Chem. B 113 2009 8717 8724
55. K. Saraboji, and M. Håkansson D.T. Logan The carbohydrate-binding site in galectin-3 is preorganized to recognize a sugarlike framework of oxygens: ultra-high-resolution structures and water dynamics Biochemistry 51 2012 296 306
56. R. Kadirvelraj, and B.L. Foley R.J. Woods Involvement of water in carbohydrate-protein binding: concanavalin A revisited J. Am. Chem. Soc. 130 2008 16933 16942
57. C.M. Payne, and Y.J. Bomble G.T. Beckham Multiple functions of aromatic-carbohydrate interactions in a processive cellulase examined with molecular simulation J. Biol. Chem. 286 2011 41028 41035