Structural and electronic snapshots during the transition from a Cu(II) to Cu(I) metal center of a lytic polysaccharide onooxygenase by x-ray photoreduction

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 18782-18792

  Gudmundsson, Mikael ^a   Kim, Seonah ^b   Wu, Miao ^a   Ishida, Takuya ^a,c   Momeni, Majid Hadadd ^a   Vaaje Kolstad, Gustav ^d   Lundberg, Daniel ^a   Royant, Antoine ^e,f   Ståhlberg, Jerry ^a,d   Eijsink, Vincent G H ^d   Beckham, Gregg T ^b   Sandgren, Mats ^a,c  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^e UNIV GRENOBLE ALPES   (France)

^f EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

CATALYTIC ACTIVATION; COPPER CENTERS; COPPER COORDINATION; ELECTRONIC CHANGES; MECHANISTIC STUDIES; MONOOXYGENASES; QUANTUM-MECHANICAL CALCULATION; X-RAY PHOTOREDUCTION;

COPPER;

COPPER; LYTIC POLYSACCHARIDE MONOOXYGENASE; OXYGEN; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; CALCULATION; CATALYSIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENTEROCOCCUS FAECALIS; ENZYME ACTIVE SITE; ENZYME STRUCTURE; GEOMETRY; METAL BINDING; NONHUMAN; OXIDATION; PRIORITY JOURNAL; X RAY ANALYSIS; X RAY DIFFRACTION; X RAY PHOTOREDUCTION;

CARBOHYDRATE-BINDING PROTEIN; CELLULASE; METALLOENZYME; POLYSACCHARIDE; X-RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; COPPER; DATABASES, PROTEIN; ELECTRONS; ENTEROCOCCUS FAECALIS; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXYGEN; PHOTOCHEMICAL PROCESSES; POLYSACCHARIDES; QUANTUM THEORY; X-RAYS;

EID: 84903852138     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.563494     Document Type: Article

References (59)

1. 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
2. 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
3. Eijsink, V. G., Vaaje-Kolstad, G., Vårum, K. M., and Horn, S. J. (2008) Towards new enzymes for biofuels: lessons from chitinase research. Trends Biotechnol. 26, 228-235
4. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37, D233-D238
5. Levasseur, A., Drula, E., Lombard, V., Coutinho, P. M., and Henrissat, B. (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels 6, 41
6. Vaaje-Kolstad, G., Westereng, B., Horn, S. J., Liu, Z., Zhai, H., Sørlie, M., and Eijsink, V. G. (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330, 219-222
7. 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
8. Forsberg, Z., Vaaje-Kolstad, G., Westereng, B., Bunaes, A. C., Stenstrøm, Y., MacKenzie, A., Sørlie, M., Horn, S. J., and Eijsink, V. G. (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci. 20, 1479-1483
9. Westereng, B., Ishida, T., Vaaje-Kolstad, G., Wu, M., Eijsink, V. G., Igarashi, K., Samejima, M., Ståhlberg, J., Horn, S. J., and Sandgren, M. (2011) The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS One 6, e27807
10. Phillips, C. M., Beeson, W. T., Cate, J. H., and Marletta, M. A. (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem. Biol. 6, 1399-1406
11. Kim, S., Ståhlberg, J., Sandgren, M., Paton, R. S., and Beckham, G. T. (2014) Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism. Proc. Natl. Acad. Sci. U. S. A. 111, 149-154
12. Hemsworth, G. R., Henrissat, B., Davies, G. J., and Walton, P. H. (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat. Chem. Biol. 10, 122-126
13. Harris, P. V., Welner, D., McFarland, K. C., Re, E., NavarroPoulsen, J. C., Brown, K., Salbo, R., Ding, H., Vlasenko, E., Merino, S., Xu, F., Cherry, J., Larsen, S., and Lo Leggio, L. (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49, 3305-3316
14. Horn, S. J., Vaaje-Kolstad, G., Westereng, B., and Eijsink, V. G. (2012) Novel enzymes for the degradation of cellulose. Biotechnol. Biofuels 5, 45
15. Merino, S., and Cherry, J. (2007) Progress and challenges in enzyme development for biomass utilization. In Biofuels (Olsson, L., ed) pp. 95-120, Springer, Berlin
16. Beckham, G. T., and Crowley, M. F. (2011) Examination of the -chitin structure and decrystallization thermodynamics at the nanoscale. J. Phys. Chem. B 115, 4516-4522
17. 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
18. Payne, C. M., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2011) Decrystallization of oligosaccharides from the cellulose I- surface with molecular simulation. J. Phys. Chem. Lett. 2, 1546-1550
19. Aachmann, F. L., Sørlie, M., Skjåk-Braek, G., Eijsink, V. G., and Vaaje- Kolstad, G. (2012) NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc. Natl. Acad. Sci. U. S. A. 109, 18779-18784
20. Isaksen, T., Westereng, B., Aachmann, F. L., Agger, J. W., Kracher, D., Kittl, R., Ludwig, R., Haltrich, D., Eijsink, V. G., and Horn, S. J. (2014) A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J. Biol. Chem. 289, 2632-2642
21. Vaaje-Kolstad, G., Horn, S. J., van Aalten, D. M., Synstad, B., and Eijsink, V. G. (2005) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J. Biol. Chem. 280, 28492-28497
22. Vaaje-Kolstad, G., Houston, D. R., Riemen, A. H., Eijsink, V. G., and van Aalten, D. M. (2005) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J. Biol. Chem. 280, 11313-11319
23. Bøhle, L. A., Mathiesen, G., Vaaje-Kolstad, G., and Eijsink, V. G. (2011) An endo-ss- N -acetylglucosaminidase from Enterococcus faecalis V583 responsible for the hydrolysis of high-mannose and hybrid-type N-linked glycans. FEMS Microbiol. Lett. 325, 123-129
24. Vaaje-Kolstad, G., Bøhle, L. A., Gåseidnes, S., Dalhus, B., Bjørås, M., Mathiesen, G., and Eijsink, V. G. (2012) Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J. Mol. Biol. 416, 239-254
25. Vebø, H. C., Snipen, L., Nes, I. F., and Brede, D. A. (2009) The transcriptome of the nosocomial pathogen Enterococcus faecalis V583 reveals adaptive responses to growth in blood. PLoS One 4, e7660
26. Vebø, H. C., Solheim, M., Snipen, L., Nes, I. F., and Brede, D. A. (2010) Comparative genomic analysis of pathogenic and probiotic Enterococcus faecalis isolates, and their transcriptional responses to growth in human urine. PLoS One 5, e12489
27. Hemsworth, G. R., Taylor, E. J., Kim, R. Q., Gregory, R. C., Lewis, S. J., Turkenburg, J. P., Parkin, A., Davies, G. J., and Walton, P. H. (2013) The copper active site of CBM33 polysaccharide oxygenases. J. Am. Chem. Soc. 135, 6069-6077
28. Wu, M., Beckham, G. T., Larsson, A. M., Ishida, T., Kim, S., Payne, C. M., Himmel, M. E., Crowley, M. F., Horn, S. J., Westereng, B., Igarashi, K., Samejima, M., Ståhlberg, J., Eijsink, V. G., and Sandgren, M. (2013) Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the basidiomycota fungus Phanerochaete chrysosporium. J. Biol. Chem. 288, 12828-12839
29. Beeson, W. T., Phillips, C. M., Cate, J. H., and Marletta, M. A. (2012) Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J. Am. Chem. Soc. 134, 890-892
30. Vu, V. V., Beeson, W. T., Phillips, C. M., Cate, J. H., and Marletta, M. A. (2014) Determinants of regioselective hydroxylation in the fungal polysaccharide monooxygenases. J. Am. Chem. Soc. 136, 562-565
31. Allen, F. H. (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr. B 58, 380-388
32. McGeehan, J., Ravelli, R. B., Murray, J. W., Owen, R. L., Cipriani, F., McSweeney, S., Weik, M., and Garman, E. F. (2009) Colouring cryocooled crystals: online microspectrophotometry. J. Synchrotron Radiat. 16, 163-172
33. Flot, D., Mairs, T., Giraud, T., Guijarro, M., Lesourd, M., Rey, V., van Brussel, D., Morawe, C., Borel, C., Hignette, O., Chavanne, J., Nurizzo, D., McSweeney, S., and Mitchell, E. (2010) The ID23-2 structural biology microfocus beamline at the ESRF. J. Synchrotron Radiat. 17, 107-118
34. Adam, V., Royant, A., Nivière, V., Molina-Heredia, F. P., and Bourgeois, D. (2004) Structure of superoxide reductase bound to ferrocyanide and active site expansion upon x-ray-induced photo-reduction. Structure 12, 1729-1740
35. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
36. Bailey, S. (1994) The Ccp4 Suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763
37. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132
38. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255
39. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA
40. Kleywegt, G. J. (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D Biol. Crystallogr. 52, 842-857
41. Kleywegt, G. J., and Jones, T. A. (1996) Phi/psi-chology: Ramachandran revisited. Structure 4, 1395-1400
42. Echols, N., Grosse-Kunstleve, R. W., Afonine, P. V., Bunkóczi, G., Chen, V. B., Headd, J. J., McCoy, A. J., Moriarty, N. W., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Adams, P. D. (2012) Graphical tools for macromolecular crystallography in PHENIX. J. Appl. Crystallogr. 45, 581-586
43. Murray, J. W., Garman, E. F., and Ravelli, R. B. (2004) X-ray absorption by macromolecular crystals: the effects of wavelength and crystal composition on absorbed dose. J. Appl. Crystallogr. 37, 513-522
44. Paithankar, K. S., Owen, R. L., and Garman, E. F. (2009) Absorbed dose calculations for macromolecular crystals: improvements to RADDOSE. J. Synchrotron Radiat. 16, 152-162
45. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., and Petersson, G. A. (2010) Gaussian 09, revision B. 01. Gaussian, Inc., Wallingford, CT
46. Dechancie, J., Clemente, F. R., Smith, A. J., Gunaydin, H., Zhao, Y.-L., Zhang, X., and Houk, K. N. (2007) How similar are enzyme active site geometries derived from quantum mechanical theozymes to crystal structures of enzyme-inhibitor complexes? Implications for enzyme design. Protein Sci. 16, 1851-1866
47. Zhao, Y., and Truhlar, D. (2008) The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor. Chem. Account 120, 215-241
48. Zhao, Y., and Truhlar, D. G. (2008) Density functionals with broad applicability in chemistry. Acc. Chem. Res. 41, 157-167
49. Barone, V., and Cossi, M. (1998) Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model. J. Phys. Chem. A 102, 1995-2001
50. Cossi, M., Rega, N., Scalmani, G., and Barone, V. (2003) Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J. Comput. Chem. 24, 669-681
51. Liao, R.-Z., and Thiel, W. (2013) On the effect of varying constraints in the quantum mechanics only modeling of enzymatic reactions: the case of acetylene hydratase. J. Phys. Chem. B 117, 3954-3961
52. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Adams, P. D., Read, R. J., Zwart, P. H., and Hung, L. W. (2008) Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias. Acta Crystallogr. D Biol. Crystallogr. 64, 515-524
53. Matthews, B. W. (1968) Solvent content of protein crystals. J. Mol. Biol. 33, 491-497
54. Hemsworth, G. R., Davies, G. J., and Walton, P. H. (2013) Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr. Opin. Struct. Biol. 23, 660-668
55. Karkehabadi, S., Hansson, H., Kim, S., Piens, K., Mitchinson, C., and Sandgren, M. (2008) The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1. 6 angstrom resolution. J. Mol. Biol. 383, 144-154
56. Li, X., Beeson, W. T., 4th, Phillips, C. M., Marletta, M. A., and Cate, J. H. (2012) Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure 20, 1051-1061
57. Casella, L., Carugo, O., Gullotti, M., Doldi, S., and Frassoni, M. (1996) Synthesis, structure, and reactivity of model complexes of copper nitrite reductase. Inorg. Chem. 35, 1101-1113
58. Sorrell, T. N., Garrity, M. L., Richards, J. L., and White, P. S. (1994) Synthesis, structural characterization and dioxygen reactivity of imidazoleligated Cu (I) complexes. Inorg. Chim. Acta 218, 103-108
59. Que, L., Jr., and Tolman, W. B. (2008) Biologically inspired oxidation catalysis. Nature 455, 333-340