Exploration of archaeal nucleotide sugar epimerases unveils a new and highly promiscuous GDP-Gal4E subgroup

Current Research in Biotechnology - Tập 4 - Trang 350-358 - 2022
Carlos Alvarez Quispe1, Matthieu Da Costa1, Koen Beerens1, Tom Desmet1
1Centre for Synthetic Biology (CSB), Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Gent, Belgium

Tài liệu tham khảo

Allard, 2001, Epimerases: Structure, function and mechanism, Cell. Mol. Life Sci., 58, 1650, 10.1007/PL00000803 Bang, 2009, Functional analysis of mutations in UDP-galactose-4-epimerase (GALE) associated with galactosemia in Korean patients using mammalian GALE-null cells, FEBS J., 276, 1952, 10.1111/j.1742-4658.2009.06922.x Beerens, 2022, GDP-Mannose 3,5-Epimerase: A View on Structure, Mechanism, and Industrial Potential, Front. Mol. Biosci., 8, 1, 10.3389/fmolb.2021.784142 Beerens, 2015, UDP-hexose 4-epimerases: a view on structure, mechanism and substrate specificity, Carbohydr. Res., 414, 8, 10.1016/j.carres.2015.06.006 Beerens, 2013, Characterization and mutational analysis of the UDP-Glc (NAc) 4-epimerase from Marinithermus hydrothermalis, Appl. Microbiol. Biotechnol., 97, 7733, 10.1007/s00253-012-4635-6 Bloom, 2006, Protein stability promotes evolvability, Proc. Natl. Acad. Sci. U. S. A., 103, 5869, 10.1073/pnas.0510098103 Chen, 1999, Cloning, expression and characterization of a UDP-galactose 4-epimerase from Escherichia coli, Biotechnol. Lett., 21, 1131, 10.1023/A:1005678225031 Chung, 2012, Characterization of UDP-glucose 4-epimerase from Pyrococcus horikoshii: Regeneration of UDP to produce UDP-galactose using two-enzyme system with trehalose, Bioresour. Technol., 110, 423, 10.1016/j.biortech.2012.01.046 Da Costa, 2021, Structure-function relationships in NDP-sugar active SDR enzymes: Fingerprints for functional annotation and enzyme engineering, Biotechnol. Adv., 48, 10.1016/j.biotechadv.2021.107705 Daenzer, 2012, UDP-Galactose 4′-epimerase activities toward UDP-Gal and UDP-GalNAc play different roles in the development of Drosophila melanogaster, PLoS Genet., 8, e1002721, 10.1371/journal.pgen.1002721 Demendi, 2005, Towards a better understanding of the substrate specificity of the UDP-N-acetylglucosamine C4 epimerase WbpP, Biochem. J., 389, 173, 10.1042/BJ20050263 Eichler, 2013, Extreme sweetness: Protein glycosylation in archaea, Nat. Rev. Microbiol., 11, 151, 10.1038/nrmicro2957 Friedman, 2012, The Molecular Dynamics of Trypanosoma brucei UDP-Galactose 4′-Epimerase: A Drug Target for African Sleeping Sickness, Chem. Biol. Drug Des., 80, 173, 10.1111/j.1747-0285.2012.01392.x Fushinobu, 2021, Molecular evolution and functional divergence of UDP-hexose 4-epimerases, Curr. Opin. Chem. Biol., 61, 53, 10.1016/j.cbpa.2020.09.007 Gevaert, 2019, Characterization of the First Bacterial and Thermostable GDP-Mannose 3,5-Epimerase, Int. J. Mol. Sci., 20, 3530, 10.3390/ijms20143530 Gevaert, 2020, GDP-altrose as novel product of GDP-mannose 3,5-epimerase: Revisiting its reaction mechanism, Int. J. Biol. Macromol., 165, 1862, 10.1016/j.ijbiomac.2020.10.067 Guindon, 2010, New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0, Syst. Biol., 59, 307, 10.1093/sysbio/syq010 Hoffmeister, 2000, The NDP-sugar co-substrate concentration and the enzyme expression level influence the substrate specificity of glycosyltransferases: cloning and characterization of deoxysugar biosynthetic genes of the urdamycin biosynthetic gene cluster, Chem. Biol., 7, 821, 10.1016/S1074-5521(00)00029-6 Holden, 2003, Structure and Function of Enzymes of the Leloir Pathway for Galactose Metabolism, J. Biol. Chem., 278, 43885, 10.1074/jbc.R300025200 Huson, 2012, Dendroscope 3: An interactive tool for rooted phylogenetic trees and networks, Syst. Biol., 61, 1061, 10.1093/sysbio/sys062 Ishiyama, 2004, Crystal structure of WbpP, a genuine UDP-N-acetylglucosamine 4-epimerase from Pseudomonas aeruginosa: Substrate specificity in UDP-hexose 4-epimerases, J. Biol. Chem., 279, 22635, 10.1074/jbc.M401642200 Kuipers, 2010, 3DM: Systematic analysis of heterogeneous superfamily data to discover protein functionalities, Proteins Struct. Funct. Bioinforma., 78, 2101 Liu, 2011, Functional expression of L-fucokinase/guanosine 5′-diphosphate-L-fucose pyrophosphorylase from Bacteroides fragilis in Saccharomyces cerevisiae for the production of nucleotide sugars from exogenous monosaccharides, Glycobiology, 21, 1228, 10.1093/glycob/cwr057 Mirdita, M., Ovchinnikov, S., Steinegger, M., 2021. ColabFold - Making protein folding accessible to all. bioRxiv 2021.08.15.456425. https://doi.org/10.1101/2021.08.15.456425. Nam, 2019, Structural basis for broad substrate specificity of UDP-glucose 4-epimerase in the human milk oligosaccharide catabolic pathway of Bifidobacterium longum, Sci. Rep., 9, 11081, 10.1038/s41598-019-47591-w Niou, 2009, Role of galE on biofilm formation by Thermus spp, Biochem. Biophys. Res. Commun., 390, 313, 10.1016/j.bbrc.2009.09.120 Ohashi, 2017, Effective Synthesis of Guanosine 5’-Diphospho-β-L-galactose using Bacterial L-Fucokinase/Guanosine 5’-diphosphate-L-fucose Pyrophosphorylase, Adv. Synth. Catal., 359, 4227, 10.1002/adsc.201700901 Pacinelli, 2002, Relationship of Yersinia pseudotuberculosis O antigens IA, IIA, and IVB: The IIA gene cluster was derived from that of IVB, Infect. Immun., 70, 3271, 10.1128/IAI.70.6.3271-3276.2002 Rapp, 2020, Expanding the Enzyme Repertoire for Sugar Nucleotide Epimerization: The CDP-Tyvelose 2-Epimerase from Thermodesulfatator atlanticus for Glucose/Mannose Interconversion, Appl. Environ. Microbiol., 87, 10.1128/AEM.02131-20 Sakuraba, 2011, Crystal structure of UDP-galactose 4-epimerase from the hyperthermophilic archaeon Pyrobaculum calidifontis, Arch. Biochem. Biophys., 512, 126, 10.1016/j.abb.2011.05.013 Sato, 2011, Novel metabolic pathways in Archaea, Curr. Opin. Microbiol., 14, 307, 10.1016/j.mib.2011.04.014 Shin, 2015, The structural basis of substrate promiscuity in UDP-hexose 4-epimerase from the hyperthermophilic Eubacterium Thermotoga maritima, Arch. Biochem. Biophys., 585, 39, 10.1016/j.abb.2015.08.025 Sievers, 2018, Clustal Omega for making accurate alignments of many protein sequences, Protein Sci., 27, 135, 10.1002/pro.3290 Szklarczyk, 2019, STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets, Nucleic Acids Res., 47, D607, 10.1093/nar/gky1131 Tanner, 2002, Understanding nature’s strategies for enzyme-catalyzed racemization and epimerization, Acc. Chem. Res., 35, 237, 10.1021/ar000056y Thoden, 1996, Molecular structure of the NADH/UDP-glucose abortive complex of UDP-galactose 4-epimerase from Escherichia coli: Implications for the catalytic mechanism, Biochemistry, 35, 5137, 10.1021/bi9601114 Thoden, 2000, Crystallographic evidence for Tyr 157 functioning as the active site base in human UDP-galactose 4-epimerase, Biochemistry, 39, 5691, 10.1021/bi000215l Tokuriki, 2009, Protein Dynamism and Evolvability, Science, 324, 203, 10.1126/science.1169375 Van Overtveldt, 2020, Determinants of the Nucleotide Specificity in the Carbohydrate Epimerase Family 1, Biotechnol. J., 15, 1, 10.1002/biot.202000132 Van Overtveldt, 2015, A structural classification of carbohydrate epimerases: From mechanistic insights to practical applications, Biotechnol. Adv., 33, 1814, 10.1016/j.biotechadv.2015.10.010 Verhees, C.H., Kengen, S.W., Tuininga, J.E., Schut, G.J., Adams, M.W., Vos, D., W.m, Oost, V. Der, J, 2003. The unique features of glycolytic pathways. Archaea. Biochem J 375, 231–246. https://doi.org/10.1042/BJ20021472. Wolucka, 2001, Partial purification and identification of GDP-mannose 3″,5″-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway, Proc. Natl. Acad. Sci. U. S. A., 98, 14843, 10.1073/pnas.011578198 Zhu, 2018, KfoA, the UDP-glucose-4-epimerase of Escherichia coli strain O5:K4:H4, shows preference for acetylated substrates, Appl. Microbiol. Biotechnol., 102, 751, 10.1007/s00253-017-8639-0