Harnessing glycosylation to improve cellulase activity

Current Opinion in Biotechnology

Volumn 23, Issue 3, 2012, Pages 338-345

  Beckham, Gregg T ^a,b   Dai, Ziyu ^c   Matthews, James F ^a   Momany, Michelle ^d   Payne, Christina M ^a   Adney, William S ^a   Baker, Scott E ^c   Himmel, Michael E ^a  

^a NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

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

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULASE ACTIVITY; ENZYME ENGINEERING; ENZYME FUNCTIONS; ENZYME STRUCTURES; FILAMENTOUS FUNGI; GLYCOSIDE HYDROLASES; GROWTH CONDITIONS; HEMICELLULASES; MOLECULAR LEVELS; N-LINKED; O-LINKED; PLANT CELL WALL; SECRETOME;

CARBOHYDRATES; ESTERIFICATION; GLYCOSYLATION; PLANT CELL CULTURE;

ENZYME ACTIVITY;

CARBOHYDRATE BINDING PROTEIN; CELLULASE; GLYCOSIDASE;

BIOMASS; CATALYSIS; CELL WALL; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME GLYCOSYLATION; ENZYME RELEASE; ENZYME STRUCTURE; FUNGUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; REVIEW; SPECIES DIFFERENTIATION;

BIOFUELS; BIOMASS; CELL WALL; CELLULASES; FUNGI; GLYCOSIDE HYDROLASES; GLYCOSYLATION; POLYSACCHARIDES; PROTEIN ENGINEERING;

FUNGI;

EID: 84861981519     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2011.11.030     Document Type: Review

References (52)

1. Chundawat S.P.S., Beckham G.T., Himmel M.E., Dale BE Deconstruction of lignocellulosic biomass to fuels and chemicals. Annual Review of Chemical and Biomolecular Engineering 2011, vol. 2:121-145. (annual reviews).
2. Himmel M.E., Ding S.Y., Johnson D.K., Adney W.S., Nimlos M.R., Brady J.W., Foust T.D. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 2007, 315:804-807.
3. Heinzelman P., Snow C.D., Wu I., Nguyen C., Villalobos A., Govindarajan S., Minshull J., Arnold F.H. A family of thermostable fungal cellulases created by structure-guided recombination. Proc Natl Acad Sci U S A 2009, 106:5610-5615.
4. Lantz S.E., Goedegebuur F., Hommes R., Kaper T., Kelemen B.R., Mitchinson C., Wallace L., Stahlberg J., Larenas E.A. Hypocrea jecorina Cel6A protein engineering. Biotechnol Biofuels 2010, 3:20.
5. Wilson D.B. Cellulases and biofuels. Curr Opin Biotechnol 2009, 20:295-299.
6. Sandgren M., Gualfetti P.J., Shaw A., Gross L.S., Saldajeno M., Day A.G., Jones T.A., Mitchinson C. Comparison of family 12 glycoside hydrolases and recruited substitutions important for thermal stability. Protein Sci 2003, 12:848-860.
7. Bu L.T., Beckham G.T., Shirts M.R., Nimlos M.R., Adney W.S., Himmel M.E., Crowley M.F. Probing carbohydrate product expulsion from a processive cellulase with multiple absolute binding free energy methods. J Biol Chem 2011, 286:18161-18169.
8. Martinez D., Berka R.M., Henrissat B., Saloheimo M., Arvas M., Baker S.E., Chapman J., Chertkov O., Coutinho P.M., Cullen D., et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn Hypocrea jecorina). Nat Biotechnol 2008, 26:553-560.
9. Reese E.T. History of cellulose program at US Army Natick Development Center. Biotechnol Bioeng 1976, 9-20.
10. Hart G.W., Copeland R.J. Glycomics hits the big time. Cell 2010, 143:672-676.
11. Varki A. Biological roles of oligosaccharides-all of the theories are correct. Glycobiology 1993, 3:97-130.
12. Adney W.S., Jeoh T., Beckham G.T., Chou Y.C., Baker J.O., Michener W., Brunecky R., Himmel M.E. Probing the role of N-linked glycans in the stability and activity of fungal cellobiohydrolases by mutational analysis. Cellulose 2009, 16:699-709.
13. Jeoh T., Michener W., Himmel M.E., Decker S.R., Adney W.S. Implications of cellobiohydrolase glycosylation for use in biomass conversion. Biotechnol Biofuels 2008, 1:10.
14. Boraston A.B., Sandercock L.E., Warren R.A.J., Kilburn D.G. O-glycosylation of a recombinant carbohydrate-binding module mutant secreted by Pichia pastoris. J Mol Microbiol Biotechnol 2003, 5:29-36.
15. Boraston A.B., Warren R.A.J., Kilburn D.G. Glycosylation by Pichia pastoris decreases the affinity of a family 2a carbohydrate-binding module from Cellulomonas fimi: a functional and mutational analysis. Biochem J 2001, 358:423-430.
16. Stals I., Sandra K., Geysens S., Contreras R., Van Beeumen J., Claeyssens M. Factors influencing glycosylation of Trichoderma reesei cellulases I: postsecretorial changes of the O- and N-glycosylation pattern of Cel7A. Glycobiology 2004, 14:713-724.
17. Prescher J.A., Bertozzi C.R. Chemical technologies for probing glycans. Cell 2006, 126:851-854.
18. Beckham G.T., Bomble Y.J., Bayer E.A., Himmel M.E., Crowley M.F. Applications of computational science for understanding enzymatic deconstruction of cellulose. Curr Opin Biotechnol 2011, 22:231-238.
19. Deshpande N., Wilkins M.R., Packer N., Nevalainen H. Protein glycosylation pathways in filamentous fungi. Glycobiology 2008, 18:626-637.
20. Lommel M., Strahl S., Protein O-mannosylation: conserved from bacteria to humans Glycobiology 2009, 19:816-828.
21. Geysens S., Pakula T., Uusitalo J., Dewerte I., Penttila M., Contreras R. Cloning and characterization of the glucosidase II alpha subunit gene of Trichoderma reesei: a frameshift mutation results in the aberrant glycosylation profile of the hypercellulolytic strain Rut-C30. Appl Environ Microbiol 2005, 71:2910-2924.
22. McCluskey K., Wiest A.E., Grigoriev I.V., Lipzen A., Martin J., Schackwitz W., Baker S.E. Rediscovery by whole genome sequencing: classical mutations and genome polymorphisms in Neurospora crassa. Genes Genomes Genetics 2011, 1:303-316.
23. Goto M. Protein O-glycosylation in fungi: diverse structures and multiple functions. Biosci Biotechnol Biochem 2007, 71:1415-1427.
24. Stals I., Sandra K., Devreese B., Van Beeumen J., Claeyssens M. Factors influencing glycosylation of Trichoderma reesei cellulases II: N-glycosylation of Cel7A core protein isolated from different strains. Glycobiology 2004, 14:725-737.
25. Hui J.P.M., Lanthier P., White T.C., McHugh S.G., Yaguchi M., Roy R., Thibault P. Characterization of cellobiohydrolase I (Cel7A) glycoforms from extracts of Trichoderma reesei using capillary isoelectric focusing and electrospray mass spectrometry. J Chromatogr B 2001, 752:349-368.
26. Hui J.P.M., White T.C., Thibault P. Identification of glycan structure and glycosylation sites in cellobiohydrolase II and endoglucanases I and II from Trichoderma reesei. Glycobiology 2002, 12:837-849.
27. Christiansen M.N., Kolarich D., Nevalainen H., Packer N.H., Jensen P.H. Challenges of determining O-glycopeptide heterogeneity: a fungal glucanase model system. Anal Chem 2010, 82:3500-3509.
28. Harrison M.J., Nouwens A.S., Jardine D.R., Zachara N.E., Gooley A.A., Nevalainen H., Packer N.H. Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei. Eur J Biochem 1998, 256:119-127.
29. Stals I., Samyn B., Sergeant K., White T., Hoorelbeke K., Coorevits A., Devreese B., Claeyssens M., Piens K. Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina. FEMS Microbiol Lett 2010, 303:9-17.
30. Voutilainen S.P., Murray P.G., Tuohy M.G., Koivula A. Expression of Talaromyces emersonii cellobiohydrolase Cel7A in Saccharomyces cerevisiae and rational mutagenesis to improve its thermostability and activity. Protein Eng Des Selection 2010, 23:69-79.
31. Langsford M.L., Gilkes N.R., Singh B., Moser B., Miller R.C., Warren R.A.J., Kilburn D.G. Glycosylation of bacterial cellulases prevents proteolytic cleavage between functional domains. FEBS Lett 1987, 225:163-167.
32. Wang W., Nema S., Teagarden D. Protein aggregation-pathways and influencing factors. Int J Pharm 2010, 390:89-99.
33. Kayser V., Chennamsetty N., Voynov V., Forrer K., Helk B., Trout B.L. Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies. Biotechnol J 2011, 6:38-44.
34. Ioannou Y.A., Zeidner K.M., Grace M.E., Desnick R.J. Human alpha-galactosidase A: glycosylation site 3 is essential for enzyme solubility. Biochem J 1998, 332:789-797.
35. Weintraub B.D., Stannard B.S., Meyers L. Glycosylation of thyroid-stimulating hormone in pituitary-tumor cells-influence of high mannose oligosacharide units on subunit aggregation, combination, and intracellular degradation. Endocrinology 1983, 112:1331-1345.
36. Endo Y., Nagai H., Watanabe Y., Ochi K., Takagi T. Heat-induced aggregation of recombinant erythropoietin in the intact and deglycosylated states as monitored by gel-permeation chromatography combined with a low-angle laser-light scattering technique. J Biochem 1992, 112:700-706.
37. Hoiberg-Nielsen R., Fuglsang C.C., Arleth L., Westh P. Interrelation ships of glycosylation and aggregation kinetics for Peniophora lycii phytase. Biochemistry 2006, 45:5057-5066.
38. Gupta R., Baldock S.J., Fielden P.R., Grieve B.D. Capillary zone electrophoresis for the analysis of glycoforms of cellobiohydrolase. J Chromatogr A 2011, 1218:5362-5368.
39. Culyba E.K., Price J.L., Hanson S.R., Dhar A., Wong C.H., Gruebele M., Powers E.T., Kelly J.W. Protein native-state stabilization by placing aromatic side chains in N-glycosylated reverse turns. Science 2011, 331:571-575.
40. Linder M., Mattinen M.L., Kontteli M., Lindeberg G., Stahlberg J., Drakenberg T., Reinikainen T., Pettersson G., Annila A. Identification of functionally important amino-acids in the cellulose-binding domain of Trichoderma reesei cellobiohydrolase I. Protein Sci 1995, 4:1056-1064.
41. Linder M., Teeri T.T. 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 1996, 93:12251-12255.
42. Beckham G.T., Matthews J.F., Bomble Y.J., Bu L.T., Adney W.S., Himmel M.E., Nimlos M.R., Crowley M.F. Identification of amino acids responsible for processivity in a Family 1 carbohydrate-binding module from a fungal cellulase. J Phys Chem B 2010, 114:1447-1453.
43. Taylor C.B., Talib M.F., McCabe C., Bu L., Adney W.S., Himmel M.E., Crowley M.F., Beckham G.T. Computational investigation of glycosylation effects on a Family 1 carbohydrate-binding module. J Biol Chem 2012, 10.1074/jbc.M111.270389.
44. Radivojac P., Iakoucheva L.M., Oldfield C.J., Obradovic Z., Uversky V.N., Dunker A.K. Intrinsic disorder and functional proteomics. Biophys J 2007, 92:1439-1456.
45. Beckham G.T., Bomble Y.J., Matthews J.F., Taylor C.B., Resch M.G., Yarbrough J.M., Decker S.R., Bu L.T., Zhao X.C., McCabe C., et al. The O-glycosylated linker from the Trichoderma reesei Family 7 cellulase is a flexible disordered protein. Biophys J 2010, 99:3773-3781.
46. Gokhale R.S., Khosla C. Role of linkers in communication between protein modules. Curr Opin Chem Biol 2000, 4:22-27.
47. Ma B.Y., Tsai C.J., Haliloglu T., Nussinov R. Dynamic allostery: linkers are not merely flexible. Structure 2011, 19:907-917.
48. Liu J., Nussinov R. The mechanism of ubiquitination in the cullin-RING E3 ligase machinery: conformational control of substrate orientation. PLoS Comput Biol 2009, 5:10.
49. Liu J., Nussinov R. Molecular dynamics reveal the essential role of linker motions in the function of cullin-RING E3 ligases. J Mol Biol 2010, 396:1508-1523.
50. Payne C.M., Bomble Y.J., Taylor C.B., McCabe C., Himmel M.E., Crowley M.F., Beckham G.T. Multiple functions of aromatic-carbohydrate interactions in a processive cellulase examined with molecular simulation. J Biol Chem 2011, 286:41028-41035.
51. Lin Y., Silvestre-Ryan J., Himmel M.E., Crowley M.F., Beckham G.T., Chu J.W. Protein: allostery at the solid-liquid interface: endoglucanase attachment to cellulose affects glucan clenching in the binding cleft. J Am Chem Soc 2011, 133:16617-16624.
52. Phillips C.M., Iavarone A.T., Marletta M.A. Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J Proteome Res 2011, 10:4177-4185.