Molecular basis for glycan recognition and reaction priming of eukaryotic oligosaccharyltransferase.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
26 11 2022
26 11 2022
Historique:
received:
03
10
2022
accepted:
17
11
2022
entrez:
26
11
2022
pubmed:
27
11
2022
medline:
30
11
2022
Statut:
epublish
Résumé
Oligosaccharyltransferase (OST) is the central enzyme of N-linked protein glycosylation. It catalyzes the transfer of a pre-assembled glycan, GlcNAc
Identifiants
pubmed: 36435935
doi: 10.1038/s41467-022-35067-x
pii: 10.1038/s41467-022-35067-x
pmc: PMC9701220
doi:
Substances chimiques
dolichyl-diphosphooligosaccharide - protein glycotransferase
EC 2.4.99.18
Hexosyltransferases
EC 2.4.1.-
Polysaccharides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7296Informations de copyright
© 2022. The Author(s).
Références
Schwarz, F. & Aebi, M. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 21, 576–582 (2011).
pubmed: 21978957
doi: 10.1016/j.sbi.2011.08.005
Cherepanova, N., Shrimal, S. & Gilmore, R. N-linked glycosylation and homeostasis of the endoplasmic reticulum. Curr. Opin. Cell Biol. 41, 57–65 (2016).
pubmed: 27085638
pmcid: 4983500
doi: 10.1016/j.ceb.2016.03.021
Aebi, M. N-linked protein glycosylation in the ER. Biochim. Biophys. Acta 1833, 2430–2437 (2013).
pubmed: 23583305
doi: 10.1016/j.bbamcr.2013.04.001
Kukuruzinska, M. A. et al. Antisense RNA to the first N-glycosylation gene, ALG7, inhibits protein N-glycosylation and secretion by Xenopus oocytes. Biochem. Biophys. Res. Commun. 198, 1248–1254 (1994).
pubmed: 7509600
doi: 10.1006/bbrc.1994.1176
Revers, L., Wilson, I. B. H., Webberley, M. C. & Flitsch, S. L. The potential dolichol recognition sequence of β−1,4-mannosyltransferase is not required for enzymic activity using phytanyl-pyrophosphoryl-α-N,N’-diacetylchitobioside as acceptor. Biochem. J. 299, 23–27 (1994).
pubmed: 8166646
pmcid: 1138015
doi: 10.1042/bj2990023
Aebi, M., Gassenhuber, J., Domdey, H. & Te Heesen, S. Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 6, 439–444 (1996).
pubmed: 8842708
doi: 10.1093/glycob/6.4.439
Burda, P. et al. Stepwise assembly of the lipid-linked oligosaccharide in the endoplasmic reticulum of Saccharomyces cerevisiae: Identification of the ALG9 gene encoding a putative mannosyl transferase. Proc. Natl. Acad. Sci. USA 93, 7160–7165 (1996).
pubmed: 8692962
pmcid: 38953
doi: 10.1073/pnas.93.14.7160
Burda, P. & Aebi, M. The ALG10 locus of Saccharomyces cerevisiae encodes the α−1,2 glucosyltransferase of the endoplasmic reticulum: the terminal glucose of the lipid-linked oligosaccharide is required for efficient N-linked glycosylation. Glycobiology 8, 455–462 (1998).
pubmed: 9597543
doi: 10.1093/glycob/8.5.455
Burda, P., Jakob, C. A., Beinhauer, J., Hegemann, J. H. & Aebi, M. Ordered assembly of the asymmetrically branched lipid-linked oligosaccharide in the endoplasmic reticulum is ensured by the substrate specificity of the individual glycosyltransferases. Glycobiology 9, 617–625 (1999).
pubmed: 10336995
doi: 10.1093/glycob/9.6.617
Yamazaki, H., Shiraishi, N., Takeuchi, K., Ohnishi, Y. & Horinouchi, S. Characterization of alg2 encoding a mannosyltransferase in the zygomycete fungus Rhizomucor pusillus. Gene 221, 179–184 (1998).
pubmed: 9795208
doi: 10.1016/S0378-1119(98)00456-9
Cipollo, J. F., Trimble, R. B., Chi, J. H., Yan, Q. & Dean, N. The yeast ALG11 gene specifies addition of the terminal α1,2-man to the Man5GlcNAc2-PP-dolichol N-glycosylation intermediate formed on the cytosolic side of the endoplasmic reticulum. J. Biol. Chem. 276, 21828–21840 (2001).
pubmed: 11278778
doi: 10.1074/jbc.M010896200
Gao, X.-D., Nishikawa, A. & Dean, N. Physical interactions between the Alg1, Alg2, and Alg11 mannosyltransferases of the endoplasmic reticulum. Glycobiology 14, 559–570 (2004).
pubmed: 15044395
doi: 10.1093/glycob/cwh072
Frank, C. G. & Aebi, M. ALG9 mannosyltransferase is involved in two different steps of lipid-linked oligosaccharide biosynthesis. Glycobiology 15, 1156–1163 (2005).
pubmed: 15987956
doi: 10.1093/glycob/cwj002
Samuelson, J. et al. The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets glycosyltranferases. Proc. Natl Acad. Sci. USA 102, 1548–1553 (2005).
pubmed: 15665075
pmcid: 545090
doi: 10.1073/pnas.0409460102
Izquierdo, L., Mehlert, A. & Ferguson, M. A. The lipid-linked oligosaccharide donor specificities of Trypanosoma brucei oligosaccharyltransferases. Glycobiology 22, 696–703 (2012).
pubmed: 22241825
pmcid: 3311286
doi: 10.1093/glycob/cws003
Izquierdo, L. et al. Distinct donor and acceptor specificities of Trypanosoma brucei oligosaccharyltransferases. EMBO J. 28, 2650–2661 (2009).
pubmed: 19629045
pmcid: 2722254
doi: 10.1038/emboj.2009.203
Zielinska, D. F., Gnad, F., Wiśniewski, J. R. & Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897–907 (2010).
pubmed: 20510933
doi: 10.1016/j.cell.2010.04.012
Taguchi, Y. et al. The structure of an archaeal oligosaccharyltransferase provides insight into the strict exclusion of proline from the N-glycosylation sequon. Commun. Biol. 4, 1–11 (2021).
doi: 10.1038/s42003-021-02473-8
Trimble, R. B., Byrd, J. C. & Maley, F. Effect of glucosylation of lipid intermediates on oligosaccharide transfer in solubilized microsomes from Saccharomyces cerevisiae. J. Biol. Chem. 255, 11892–11895 (1980).
pubmed: 7002929
doi: 10.1016/S0021-9258(19)70218-X
Karaoglu, D., Kelleher, D. J. & Gilmore, R. Allosteric regulation provides a molecular mechanism for preferential utilization of the fully assembled dolichol-linked oligosaccharide by the yeast oligosaccharyltransferase. Biochemistry 40, 12193–12206 (2001).
pubmed: 11580295
doi: 10.1021/bi0111911
Kelleher, D. J., Karaoglu, D., Mandon, E. C. & Gilmore, R. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12, 101–111 (2003).
pubmed: 12887896
doi: 10.1016/S1097-2765(03)00243-0
Burda, P. & Aebi, M. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426, 239–257 (1999).
pubmed: 9878760
doi: 10.1016/S0304-4165(98)00127-5
Poljak, K. et al. Quantitative profiling of N-linked glycosylation machinery in yeast Saccharomyces cerevisiae. Mol. Cell. Proteom. 17, 18–30 (2018).
doi: 10.1074/mcp.RA117.000096
Haeuptle, M. A. & Hennet, T. Human mutation congenital disorders of glycosylation: an update on defects affecting the biosynthesis of dolichol-linked oligosaccharides. Hum. Mutat. 30, 1628–1641 (2009).
pubmed: 19862844
doi: 10.1002/humu.21126
Hennet, T. Diseases of glycosylation beyond classical congenital disorders of glycosylation. Biochim. Biophys. Acta 1820, 1306–1317 (2012).
pubmed: 22343051
doi: 10.1016/j.bbagen.2012.02.001
Kelleher, D. J., Karaoglu, D. & Gilmore, R. Large-scale isolation of dolichol-linked oligosaccharides with homogeneous oligosaccharide structures: determination of steady-state dolichol-linked oligosaccharide compositions. Glycobiology 11, 321–333 (2001).
pubmed: 11358881
doi: 10.1093/glycob/11.4.321
Mueller, S. et al. Protein degradation corrects for imbalanced subunit stoichiometry in OST complex assembly. Mol. Biol. Cell 26, 2596–2608 (2015).
pubmed: 25995378
pmcid: 4501358
doi: 10.1091/mbc.E15-03-0168
Wild, R. et al. Structure of the yeast oligosaccharyltransferase complex gives insight into eukaryotic N-glycosylation. Science 359, 545–550 (2018).
pubmed: 29301962
doi: 10.1126/science.aar5140
Bai, L., Wang, T., Zhao, G., Kovach, A. & Li, H. The atomic structure of a eukaryotic oligosaccharyltransferase complex. Nature 555, 328–333 (2018).
pubmed: 29466327
pmcid: 6112861
doi: 10.1038/nature25755
Ramírez, A. S., Kowal, J. & Locher, K. P. Cryo-electron microscopy structures of human oligosaccharyltransferase complexes OST-A and OST-B. Science 366, 1372–1375 (2019).
pubmed: 31831667
doi: 10.1126/science.aaz3505
Neuhaus, J. D. et al. Functional analysis of Ost3p and Ost6p containing yeast oligosaccharyltransferases. Glycobiology 31, 1604–1615 (2021).
pubmed: 34974622
doi: 10.1093/glycob/cwab084
Quellhorst, G. J., Piotrowski, J. S., Steffen, S. E. & Krag, S. S. Identification of Schizosaccharomyces pombe prenol as dolichol-16,17. Biochem. Biophys. Res. Commun. 244, 546–550 (1998).
pubmed: 9514857
doi: 10.1006/bbrc.1998.8098
Rip, J. W., Rupar, C. A., Ravi, K. & Carroll, K. K. Distribution, metabolism and function of dolichol and polyprenols. Prog. Lipid Res. 24, 269–309 (1985).
pubmed: 2819898
doi: 10.1016/0163-7827(85)90008-6
Schenk, B., Fernandez, F. & Waechter, C. J. The ins(ide) and outs(ide) of dolichyl phosphate biosynthesis and recycling in the endoplasmic reticulum. Glycobiology 11, 61R–70R (2001).
pubmed: 11425794
doi: 10.1093/glycob/11.5.61R
Boltje, T. J., Buskas, T. & Boons, G. J. Opportunities and challenges in synthetic oligosaccharide and glycoconjugate research. Nat. Chem. 1, 611–622 (2009).
pubmed: 20161474
pmcid: 2794050
doi: 10.1038/nchem.399
Shivatare, S. S. et al. Modular synthesis of N-glycans and arrays for the hetero-ligand binding analysis of HIV antibodies. Nat. Chem. 8, 338–346 (2016).
pubmed: 27001729
pmcid: 4806563
doi: 10.1038/nchem.2463
Ramírez, A. S. et al. Characterization of the single-subunit oligosaccharyltransferase STT3A from Trypanosoma brucei using synthetic peptides and lipid-linked oligosaccharide analogs. Glycobiology 27, 525–535 (2017).
pubmed: 28204532
pmcid: 5421464
doi: 10.1093/glycob/cwx017
Ramírez, A. S. et al. Chemo-enzymatic synthesis of lipid-linked GlcNAc2Man5 oligosaccharides using recombinant Alg1, Alg2 and Alg11 proteins. Glycobiology 27, 726–733 (2017).
pubmed: 28575298
pmcid: 5881667
doi: 10.1093/glycob/cwx045
Bloch, J. S. et al. Structure and mechanism of the ER-based glucosyltransferase ALG6. Nature 579, 443–447 (2020).
pubmed: 32103179
pmcid: 8712213
doi: 10.1038/s41586-020-2044-z
Eyring, J. et al. Substrate specificities and reaction kinetics of the yeast oligosaccharyltransferase isoforms. J. Biol. Chem. 296, 100809 (2021).
pubmed: 34023382
pmcid: 8191290
doi: 10.1016/j.jbc.2021.100809
Bause, E., Breuer, W. & Peters, S. Investigation of the active site of oligosaccharyltransferase from pig liver using synthetic tripeptides as tools. Biochem. J. 312, 979–985 (1995).
pubmed: 8554547
pmcid: 1136209
doi: 10.1042/bj3120979
Lizak, C. et al. Unexpected reactivity and mechanism of carboxamide activation in bacterial N-linked protein glycosylation. Nat. Commun. 4, 2627 (2013).
pubmed: 24149797
doi: 10.1038/ncomms3627
Napiórkowska, M. et al. Molecular basis of lipid-linked oligosaccharide recognition and processing by bacterial oligosaccharyltransferase. Nat. Struct. Mol. Biol. 24, 1100–1106 (2017).
pubmed: 29058712
doi: 10.1038/nsmb.3491
Lehle, L. & Bause, E. Primary structural requirements for N- and O-glycosylation of yeast mannoproteins. BBA - Gen. Subj. 799, 246–251 (1984).
doi: 10.1016/0304-4165(84)90267-8
Napiórkowska, M., Boilevin, J., Darbre, T., Reymond, J.-L. & Locher, K. P. Structure of bacterial oligosaccharyltransferase PglB bound to a reactive LLO and an inhibitory peptide. Sci. Rep. 8, 16297 (2018).
pubmed: 30389987
pmcid: 6215017
doi: 10.1038/s41598-018-34534-0
Matsumoto, S., Taguchi, Y., Shimada, A., Igura, M. & Kohda, D. Tethering an N-glycosylation sequon-containing peptide creates a catalytically competent oligosaccharyltransferase complex. Biochemistry 56, 602–611 (2017).
pubmed: 27997792
doi: 10.1021/acs.biochem.6b01089
Gerber, S. et al. Mechanism of bacterial oligosaccharyltransferase: In vitro quantification of seqon binding and catalysis. J. Biol. Chem. 288, 8849–8861 (2013).
pubmed: 23382388
pmcid: 3610960
doi: 10.1074/jbc.M112.445940
Lizak, C., Gerber, S., Numao, S., Aebi, M. & Locher, K. P. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350–355 (2011).
pubmed: 21677752
doi: 10.1038/nature10151
Fernandez, F. et al. The CWH8 gene encodes a dolichyl pyrophosphate phosphatase with a luminally oriented active site in the endoplasmic reticulum of Saccharomyces cerevisiae. J. Biol. Chem. 276, 41455–41464 (2001).
pubmed: 11504728
doi: 10.1074/jbc.M105544200
Braunger, K. et al. Structural basis for coupling protein transport and N-glycosylation at the mammalian endoplasmic reticulum. Science 360, 215–219 (2018).
pubmed: 29519914
pmcid: 6319373
doi: 10.1126/science.aar7899
Puschnik, A. S. et al. A small-molecule oligosaccharyltransferase inhibitor with pan-flaviviral activity. Cell Rep. 21, 3032–3039 (2017).
pubmed: 29241533
pmcid: 5734657
doi: 10.1016/j.celrep.2017.11.054
Baro, M., Sambrooks, C. L., Quijano, A., Mark Saltzman, W. & Contessa, J. Oligosaccharyltransferase inhibition reduces receptor tyrosine kinase activation and enhances glioma radiosensitivity. Clin. Cancer Res. 25, 784–795 (2019).
pubmed: 29967251
doi: 10.1158/1078-0432.CCR-18-0792
Schägger, H. Tricine–SDS-PAGE. Nat. Protoc. 1, 16–22 (2006).
pubmed: 17406207
doi: 10.1038/nprot.2006.4
Kohda, D., Yamada, M., Igura, M., Kamishikiryo, J. & Maenaka, K. New oligosaccharyltransferase assay method. Glycobiology 17, 1175–1182 (2007).
pubmed: 17693440
doi: 10.1093/glycob/cwm087
Scheres, S. H. W. RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
pubmed: 23000701
pmcid: 3690530
doi: 10.1016/j.jsb.2012.09.006
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
pubmed: 26592709
pmcid: 4711343
doi: 10.1016/j.jsb.2015.11.003
Brown, A. et al. Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions. Acta Crystallogr. Sect. D. Biol. Crystallogr. 71, 136–153 (2015).
doi: 10.1107/S1399004714021683
Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. Sect. D. Biol. Crystallogr. 68, 352–367 (2012).
doi: 10.1107/S0907444912001308
EF, P. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
doi: 10.1002/pro.3943
Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000).
doi: 10.1016/S0168-9525(00)02024-2
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).
pubmed: 19151095
pmcid: 2672624
doi: 10.1093/bioinformatics/btp033