Structure and Dynamics of a Promiscuous Xanthan Lyase from Paenibacillus nanensis and the Design of Variants with Increased Stability and Activity

Cell Chemical Biology - Tập 26 - Trang 191-202.e6 - 2019
Pernille Foged Jensen1, Anders Kadziola2, Gerard Comamala1, Dorotea R. Segura3, Lars Anderson3, Jens-Christian N. Poulsen2, Kim Krighaar Rasmussen2, Shilpi Agarwal3, Rajendra K. Sainathan3, Rune Nygaard Monrad3, Allan Svendsen3, Jens Erik Nielsen3, Leila Lo Leggio2, Kasper D. Rand1
1Protein Analysis Group, Department of Pharmacy, University of Copenhagen, Copenhagen 2100, Denmark
2Department of Chemistry, University of Copenhagen, Copenhagen 2100, Denmark
3Novozymes A/S, Krogshøjvej 36, Bagsværd 2880, Denmark

Tài liệu tham khảo

Abbott, 2014, Using structure to inform carbohydrate binding module function, Curr. Opin. Struct. Biol., 28, 32, 10.1016/j.sbi.2014.07.004 Adams, 2010, PHENIX: a comprehensive Python-based system for macromolecular structure solution, Acta Crystallogr. D Biol. Crystallogr., 66, 213, 10.1107/S0907444909052925 Baba Hamed, 2009, Rheological properties of biopolymers drilling fluids, J. Pet. Sci. Eng., 67, 84, 10.1016/j.petrol.2009.04.001 Bendtsen, 2004, Improved prediction of signal peptides: SignalP 3.0, J. Mol. Biol., 340, 783, 10.1016/j.jmb.2004.05.028 Bernadó, 2007, Structural characterization of flexible proteins using small-angle X-ray scattering, J. Am. Chem. Soc., 129, 5656, 10.1021/ja069124n Boraston, 2004, Carbohydrate-binding modules: fine-tuning polysaccharide recognition, Biochem. J., 382, 769, 10.1042/BJ20040892 Correia, 2010, Signature active site architectures illuminate the molecular basis for ligand specificity in family 35 carbohydrate binding module, Biochemistry, 49, 6193, 10.1021/bi1006139 Elmabrouk, 2011, Crystal structures of a family 8 polysaccharide lyase reveal open and highly occluded substrate-binding cleft conformations, Proteins, 79, 965, 10.1002/prot.22938 Emsley, 2010, Features and development of Coot, Acta Crystallogr. D Biol. Crystallogr., 66, 486, 10.1107/S0907444910007493 Féthière, 1999, Crystal structure of chondroitin AC lyase, a representative of a family of glycosaminoglycan degrading enzymes, J. Mol. Biol., 288, 635, 10.1006/jmbi.1999.2698 Franke, 2009, DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering, J. Appl. Crystallogr., 42, 342, 10.1107/S0021889809000338 Guttman, 2013, Analysis of overlapped and noisy hydrogen/deuterium exchange mass spectra, J. Am. Soc. Mass Spectrom., 24, 1906, 10.1007/s13361-013-0727-5 Harju, 2012, Lactose hydrolysis and other conversions in dairy products: technological aspects, Int. Dairy J., 22, 104, 10.1016/j.idairyj.2011.09.011 Harris, 2014, New enzyme insights drive advances in commercial ethanol production, Curr. Opin. Chem. Biol., 19, 162, 10.1016/j.cbpa.2014.02.015 Hashimoto, 1998, Xanthan lyase of Bacillus sp. strain GL1 liberates pyruvylated mannose from xanthan side chains, Appl. Environ. Microbiol., 64, 3765, 10.1128/AEM.64.10.3765-3768.1998 Hashimoto, 2003, Crystal structure of Bacillus sp. GL1 xanthan lyase, which acts on the side chains of xanthan, J. Biol. Chem., 278, 7663, 10.1074/jbc.M208100200 Henshaw, 2004, The family 6 carbohydrate binding module CmCBM6-2 contains two ligand-binding sites with distinct specificities, J. Biol. Chem., 279, 21552, 10.1074/jbc.M401620200 Huang, 2003, Crystal structure of Proteus vulgaris chondroitin sulfate ABC lyase I at 1.9 Å resolution, J. Mol. Biol., 328, 623, 10.1016/S0022-2836(03)00345-0 Imeson, 2009 Ito, 1997, Alkaline cellulases from alkaliphilic Bacillus: enzymatic properties, genetics, and application to detergents, Extremophiles, 1, 61, 10.1007/s007920050015 Jensen, 2016, Hydrogen exchange: a sensitive analytical window into protein conformation and dynamics, 1 Kabsch, 2010, XDS, Acta Crystallogr. D Biol. Crystallogr., 66, 125, 10.1107/S0907444909047337 Kelley, 2015, The Phyre2 web portal for protein modeling, prediction and analysis, Nat. Protoc., 10, 845, 10.1038/nprot.2015.053 Konarev, 2003, PRIMUS: a Windows PC-based system for small-angle scattering data analysis, J. Appl. Crystallogr., 36, 1277, 10.1107/S0021889803012779 Konermann, 2011, Hydrogen exchange mass spectrometry for studying protein structure and dynamics, Chem. Soc. Rev., 40, 1224, 10.1039/C0CS00113A Kool, 2014, Characterization of an acetyl esterase from Myceliophthora thermophila C1 able to deacetylate xanthan, Carbohydr. Polym., 111, 222, 10.1016/j.carbpol.2014.04.064 Kozin, 2001, Automated matching of high- and low-resolution structural models, J. Appl. Crystallogr., 34, 33, 10.1107/S0021889800014126 Krissinel, 2004, Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions, Acta Crystallogr. D Biol. Crystallogr., 60, 2256, 10.1107/S0907444904026460 Lever, 1973, Colorimetric and fluorometric carbohydrate determination with p-hydroxybenzoic acid hydrazide, Biochem. Med., 7, 274, 10.1016/0006-2944(73)90083-5 Li, 2001, Hyaluronan binding and degradation by Streptococcus agalactiae hyaluronate lyase, J. Biol. Chem., 276, 41407, 10.1074/jbc.M106634200 Li, 2000, Structural basis of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase, EMBO J., 19, 1228, 10.1093/emboj/19.6.1228 Lombard, 2010, A hierarchical classification of polysaccharide lyases for glycogenomics, Biochem. J., 432, 437, 10.1042/BJ20101185 Lombard, 2014, The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res., 42, D490, 10.1093/nar/gkt1178 Lunin, 2004, High-resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: an enzyme-substrate complex defines the catalytic mechanism, J. Mol. Biol., 337, 367, 10.1016/j.jmb.2003.12.071 Maruyama, 2005, Crystal structure of Bacillus sp. GL1 xanthan lyase complexed with a substrate: insights into the enzyme reaction mechanism, J. Mol. Biol., 350, 974, 10.1016/j.jmb.2005.05.055 Maruyama, 2007, A structural factor responsible for substrate recognition by Bacillus sp. GL1 xanthan lyase that acts specifically on pyruvated side chains of xanthan, Biochemistry, 46, 781, 10.1021/bi0619775 Montanier, 2009, Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function, Proc. Natl. Acad. Sci. U S A, 106, 3065, 10.1073/pnas.0808972106 Moroz, 2017, The structure of a calcium-dependent phosphoinositide-specific phospholipase C from Pseudomonas sp. 62186, the first from a Gram-negative bacterium, Acta Crystallogr. D Biol. Crystallogr., 73, 32, 10.1107/S2059798316019616 Moroz, 2018, Structural dynamics and catalytic properties of a multimodular xanthanase, ACS Catal., 8, 6021, 10.1021/acscatal.8b00666 Panjkovich, 2016, Deciphering conformational transitions of proteins by small angle X-ray scattering and normal mode analysis, Phys. Chem. Chem. Phys., 18, 5707, 10.1039/C5CP04540A Petri, 2015, Xanthan gum: a versatile biopolymer for biomedical and technological applications, J. Appl. Polym. Sci., 132, 10.1002/app.42035 Raventos, D.R.S., Anderson, L., Palmen, L.G., Christiansen, L.S., Hallin, P.F., Murphy, L., Overgaard, M.L.D., Monrad, R.N., O'Connell, T., Tondera, S., et al., inventors; Novozymes A/S assignee. Polypeptides having Xanthan degrading activity and polynucleotides encoding same. World patent WO 2017/046260 A1. March 23, 2017. English. Ruijssenaars, 1999, A pyruvated mannose-specific xanthan lyase involved in xanthan degradation by paenibacillus alginolyticus XL-1, Appl. Environ. Microbiol., 65, 2446, 10.1128/AEM.65.6.2446-2452.1999 Schrödinger LLC, 2010 Segura, D.R., Boisen, A., Murphy, L., Anderson, L., Palmen, L.G., and Madsen, K.R., inventors; Novozymes A/S, assignee, Polypeptides having anti-redeposition effect and polynucleotides encoding same. United States patent US 2016/0152925 A1. June 2, 2016. Shaya, 2008, Composite active site of chondroitin lyase ABC accepting both epimers of uronic acid, Glycobiology, 18, 270, 10.1093/glycob/cwn002 Sutherland, 1995, Polysaccharide lyases, FEMS Microbiol. Rev., 16, 323, 10.1111/j.1574-6976.1995.tb00179.x Suzuki, 2003, Derivatization of carbohydrates, 41 Svergun, 1992, Determination of the regularization parameter in indirect-transform methods using perceptual criteria, J. Appl. Crystallogr., 25, 495, 10.1107/S0021889892001663 Svergun, 1995, CRYSOL—a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates, J. Appl. Crystallogr., 28, 768, 10.1107/S0021889895007047 Tria, 2007, Structural characterization of flexible proteins using small angle X ray scattering, IUCrJ, 2, 207, 10.1107/S205225251500202X Volkov, 2003, Uniqueness of ab initio shape determination in small-angle scattering, J. Appl. Crystallogr., 36, 860, 10.1107/S0021889803000268 Widner, 2000, Strains of Bacillus subtilis capable of secreting high levels of industrial enzymes, J. Ind. Microbiol. Biotechnol., 25, 204, 10.1038/sj.jim.7000051 Wuestenberg, 2014