A biosynthetic route for polysialylating proteins in Escherichia coli

Angata, 2002, Cloning and characterization of human Siglec-11. A recently evolved signaling molecule that can interact with SHP-1 and SHP-2 and is expressed by tissue macrophages, including brain microglia, J. Biol. Chem., 277, 24466, 10.1074/jbc.M202833200 Antoine, 2003, Large-scale in vivo synthesis of the carbohydrate moieties of gangliosides GM1 and GM2 by metabolically engineered Escherichia coli, Chembiochem Eur. J. Chem. Biol., 4, 406, 10.1002/cbic.200200540 Antoine, 2005, Highly efficient biosynthesis of the oligosaccharide moiety of the GD3 ganglioside by using metabolically engineered Escherichia coli, Angew. Chem. Int. Ed. Engl., 44, 1350, 10.1002/anie.200461507 Blixt, 2005, Chemoenzymatic synthesis of 2-azidoethyl-ganglio-oligosaccharides GD3, GT3, GM2, GD2, GT2, GM1, and GD1a, Carbohydr. Res., 340, 1963, 10.1016/j.carres.2005.06.008 Borujeni, 2014, Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites, Nucleic Acids Res., 42, 2646, 10.1093/nar/gkt1139 Chen, 2015, The sweet branch of metabolic engineering: cherry-picking the low-hanging sugary fruits, Microb. Cell Factor., 14, 197, 10.1186/s12934-015-0389-z Chen, 2012, Glycoengineering approach to half-life extension of recombinant biotherapeutics, Bioconjug. Chem., 23, 1524, 10.1021/bc200624a Chiu, 2004, Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog, Nat. Struct. Mol. Biol., 11, 163, 10.1038/nsmb720 Choi, 2010, The Actinobacillus pleuropneumoniae HMW1C-like glycosyltransferase mediates N-linked glycosylation of the Haemophilus influenzae HMW1 adhesin, PloS One, 5, e15888, 10.1371/journal.pone.0015888 Constantinou, 2008, Modulation of antibody pharmacokinetics by chemical polysialylation, Bioconjug. Chem., 19, 643, 10.1021/bc700319r Deuschle, 1986, Promoters of Escherichia coli: a hierarchy of in vivo strength indicates alternate structures, EMBO J., 5, 2987, 10.1002/j.1460-2075.1986.tb04596.x Farasat, 2014, Efficient search, mapping, and optimization of multi‐protein genetic systems in diverse bacteria, Mol. Syst. Biol., 10, 731, 10.15252/msb.20134955 Feldman, 2005, Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli, Proc. Natl. Acad. Sci. USA, 102, 3016, 10.1073/pnas.0500044102 Fernandes, 1997, Polysialylated asparaginase: preparation, activity and pharmacokinetics, Biochim. Biophys. Acta, 1341, 26, 10.1016/S0167-4838(97)00056-3 Freiberger, 2007, Biochemical characterization of a Neisseria meningitidis polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases, Mol. Microbiol., 65, 1258, 10.1111/j.1365-2958.2007.05862.x Garay, 2012, Antibodies against polyethylene glycol in healthy subjects and in patients treated with PEG-conjugated agents, Expert Opin. Drug Deliv., 9, 1319, 10.1517/17425247.2012.720969 Gilbert, 2000, Biosynthesis of ganglioside mimics in Campylobacter jejuni OH4384. Identification of the glycosyltransferase genes, enzymatic synthesis of model compounds, and characterization of nanomole amounts by 600-mhz (1)h and (13)c NMR analysis, J. Biol. Chem., 275, 3896, 10.1074/jbc.275.6.3896 Grass, 2010, The Haemophilus influenzae HMW1C protein is a glycosyltransferase that transfers hexose residues to asparagine sites in the HMW1 adhesin, PLoS Pathog., 6, e1000919, 10.1371/journal.ppat.1000919 He, 2015, Production of chondroitin in metabolically engineered E. coli, Metab. Eng., 27, 92, 10.1016/j.ymben.2014.11.003 Hildebrandt, 2013, Polysialic acid in brain development and synaptic plasticity, Top. Curr. Chem., 10.1007/128_2013_446 Ihssen, 2015, Increased efficiency of Campylobacter jejuni N-oligosaccharyltransferase PglB by structure-guided engineering, Open Biol., 5, 140227, 10.1098/rsob.140227 Ilyushin, 2013, Chemical polysialylation of human recombinant butyrylcholinesterase delivers a long-acting bioscavenger for nerve agents in vivo, Proc. Natl. Acad. Sci. USA, 110, 1243, 10.1073/pnas.1211118110 Johnson, 2005, Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion, J. Biol. Chem., 280, 137, 10.1074/jbc.M410216200 Kallolimath, 2016, Engineering of complex protein sialylation in plants, Proc. Natl. Acad. Sci., 10.1073/pnas.1604371113 Keys, 2017, Engineering protein glycosylation in prokaryotes, Curr. Opin. Syst. Biol., 5, 23, 10.1016/j.coisb.2017.05.016 Keys, 2012, A high-throughput screen for polysialyltransferase activity, Anal. Biochem., 427, 60, 10.1016/j.ab.2012.04.033 Keys, 2014, Engineering the product profile of a polysialyltransferase, Nat. Chem. Biol., 10, 437, 10.1038/nchembio.1501 Knop, 2010, Poly(ethylene glycol) in drug delivery: pros and cons as well as potential alternatives, Angew. Chem. Int. Ed. Engl., 49, 6288, 10.1002/anie.200902672 Lau, 2010, Highly efficient chemoenzymatic synthesis of β1–4-linked galactosides with promiscuous bacterial β1–4-galactosyltransferases, Chem. Commun., 46, 6066, 10.1039/c0cc01381a Lefebre, 2002, Construction and evaluation of plasmid vectors optimized for constitutive and regulated gene expression in Burkholderia cepacia complex isolates, Appl. Environ. Microbiol., 68, 5956, 10.1128/AEM.68.12.5956-5964.2002 Lewis, 2009, Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structure, Proc. Natl. Acad. Sci., 106, 13552, 10.1073/pnas.0902431106 Lindhout, 2011, Site-specific enzymatic polysialylation of therapeutic proteins using bacterial enzymes, Proc. Natl. Acad. Sci. USA, 108, 7397, 10.1073/pnas.1019266108 Lizak, 2017, X-ray crystallographic structure of a bacterial polysialyltransferase provides insight into the biosynthesis of capsular polysialic acid, Sci. Rep., 7, 10.1038/s41598-017-05627-z Lomino, 2013, A two-step enzymatic glycosylation of polypeptides with complex N-glycans, Bioorg. Med. Chem., 21, 2262, 10.1016/j.bmc.2013.02.007 Mazmanian, 2006, The love-hate relationship between bacterial polysaccharides and the host immune system, Nat. Rev. Immunol., 6, 849, 10.1038/nri1956 Moolenaar, 1990, Expression of neural cell adhesion molecule-related sialoglycoprotein in small cell lung cancer and neuroblastoma cell lines H69 and CHP-212, Cancer Res., 50, 1102 Mühlenhoff, 2013, Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2, Neurochem. Res., 38, 1134, 10.1007/s11064-013-0979-2 Naegeli, 2015, Current approaches to engineering N-linked protein glycosylation in bacteria, Methods Mol. Biol. Clifton NJ, 1321, 3, 10.1007/978-1-4939-2760-9_1 Naegeli, 2014, Molecular analysis of an alternative N-glycosylation machinery by functional transfer from Actinobacillus pleuropneumoniae to Escherichia coli, J. Biol. Chem., 289, 2170, 10.1074/jbc.M113.524462 Naegeli, 2014, Substrate specificity of cytoplasmic N-glycosyltransferase, J. Biol. Chem., 289, 24521, 10.1074/jbc.M114.579326 Pedelacq, 2002, Engineering soluble proteins for structural genomics, Nat. Biotechnol., 20, 927, 10.1038/nbt732 Plückthun, 2015, Designed ankyrin repeat proteins (DARPins): binding proteins for research, diagnostics, and therapy, Annu. Rev. Pharmacol. Toxicol., 55, 489, 10.1146/annurev-pharmtox-010611-134654 Priem, 2002, A new fermentation process allows large-scale production of human milk oligosaccharides by metabolically engineered bacteria, Glycobiology, 12, 235, 10.1093/glycob/12.4.235 Ravenscroft, 2016, Purification and characterization of a Shigella conjugate vaccine, produced by glycoengineering Escherichia coli, Glycobiology, 26, 51 Ray, 2014, Complete structural elucidation of an oxidized polysialic acid drug intermediate by nuclear magnetic resonance spectroscopy, Bioconjug. Chem., 25, 665, 10.1021/bc400456g Richard, 2016, Bacterial synthesis of polysialic acid lactosides in recombinant Escherichia coli K-12, Glycobiology, 26, 723, 10.1093/glycob/cww027 Rutishauser, 2008, Polysialic acid in the plasticity of the developing and adult vertebrate nervous system, Nat. Rev. Neurosci., 9, 26, 10.1038/nrn2285 Schwarz, 2011, Cytoplasmic N-glycosyltransferase of Actinobacillus pleuropneumoniae is an inverting enzyme and recognizes the NX(S/T) consensus sequence, J. Biol. Chem., 286, 35267, 10.1074/jbc.M111.277160 Schwarz, 2017, Paired Siglec receptors generate opposite inflammatory responses to a human-specific pathogen, EMBO J., 10.15252/embj.201695581 Smirnov, 2015, 389 Stahl, 2012, Highly potent VEGF-A-antagonistic DARPins as anti-angiogenic agents for topical and intravitreal applications, Angiogenesis, 16, 101, 10.1007/s10456-012-9302-0 Stummeyer, 2005, Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F, Nat. Struct. Mol. Biol., 12, 90, 10.1038/nsmb874 Varki, 2015, Symbol nomenclature for graphical representations of glycans, Glycobiology, 25, 1323, 10.1093/glycob/cwv091 Vogel, 1996, Sialic acids of both the capsule and the sialylated lipooligosaccharide of Neisseria meningitis serogroup B are prerequisites for virulence of meningococci in the infant rat, Med. Microbiol. Immunol. (Berl.), 185, 81, 10.1007/s004300050018 Wacker, 2014, Prevention of Staphylococcus aureus infections by glycoprotein vaccines synthesized in Escherichia coli, J. Infect. Dis., 209, 1551, 10.1093/infdis/jit800 Wakarchuk, 1996, Functional relationships of the genetic locus encoding the glycosyltransferase enzymes involved in expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis, J. Biol. Chem., 271, 19166, 10.1074/jbc.271.32.19166 Welch, 2009, Design parameters to control synthetic gene expression in Escherichia coli, PLoS One, 4, e7002, 10.1371/journal.pone.0007002 Wiśniewski, 2009, Universal sample preparation method for proteome analysis, Nat. Methods, 6, 359, 10.1038/nmeth.1322 Xu, 2012, ePathBrick: a synthetic biology platform for engineering metabolic pathways in E. coli, ACS Synth. Biol., 1, 256, 10.1021/sb300016b Xu, 2013, Modular optimization of multi-gene pathways for fatty acids production in E. coli, Nat. Commun., 4, 1409, 10.1038/ncomms2425 Yanisch-Perron, 1985, Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors, Gene, 33, 103, 10.1016/0378-1119(85)90120-9