Substrate specificity of cytoplasmic N-glycosyltransferase

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24521-24532

  Naegeli, Andreas ^a   Michaud, Gaëlle ^b   Schubert, Mario ^a   Lin, Chia Wei ^a   Lizak, Christian ^a,c   Darbre, Tamis ^b   Reymond, Jean Louis ^b   Aebi, Markus ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; CELL PROLIFERATION; ENZYMES; GLYCOSYLATION; PEPTIDES;

ACTINOBACILLUS PLEUROPNEUMONIAE; CATALYZED REACTIONS; GLYCOSYL TRANSFERASE; INTEGRAL MEMBRANE PROTEINS; OLIGOSACCHARYLTRANSFERASE; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN GLYCOSYLATION; SUBSTRATE SPECIFICITY;

SUBSTRATES;

GLYCOSYLTRANSFERASE; GUANOSINE DIPHOSPHATE MANNOSE; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE; URIDINE DIPHOSPHATE XYLOSE; BACTERIAL PROTEIN; GLUCOSYLTRANSFERASE; N-GLYCOSYLTRANSFERASE, NOCARDIA AEROCOLONIGENES;

ACTINOBACILLUS PLEUROPNEUMONIAE; ARTICLE; BIOCHEMISTRY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME SPECIFICITY; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; AMINO ACID SEQUENCE; CHEMISTRY; CYTOPLASM; ENZYMOLOGY; HYDROLYSIS; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYTOPLASM; GLUCOSYLTRANSFERASES; GLYCOSYLATION; HYDROLYSIS; KINETICS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTON MAGNETIC RESONANCE SPECTROSCOPY; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84906875240     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.579326     Document Type: Article

References (46)

1. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8
2. Aebi, M., Bernasconi, R., Clerc, S., and Molinari, M. (2010) N-Glycan structures: recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82
3. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049 (Pubitemid 39050393)
4. Sharon, N., and Lis, H. (1995) Lectins-proteins with a sweet tooth: functions in cell recognition. Essays Biochem. 30, 59-75
5. Kaneko, Y., Nimmerjahn, F., and Ravetch, J. V. (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313, 670-673 (Pubitemid 44201145)
6. Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A., and Dwek, R. A. (2001) Glycosylation and the immune system. Science 291, 2370-2376 (Pubitemid 32231792)
7. Marshall, R. D. (1972) Glycoproteins. Annu. Rev. Biochem. 41, 673-702
8. Nothaft, H., and Szymanski, C. M. (2010) Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8, 765-778
9. Calo, D., Kaminski, L., and Eichler, J. (2010) Protein glycosylation in Archaea: sweet and extreme. Glycobiology 20, 1065-1076
10. Kelleher, D. J., and Gilmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47R-62R
11. Imperiali, B., Shannon, K. L., Unno, M., and Rickert, K. W. (1992) A mechanistic proposal for asparagine-linked glycosylation. J. Am. Chem. Soc. 114, 7944-7945
12. Bause, E., Breuer, W., and Peters, S. (1995) Investigation of the active site of oligosaccharyltransferase from pig liver using synthetic tripeptides as tools. Biochem. J. 312, 979-985 (Pubitemid 26006014)
13. Lizak, C., Gerber, S., Numao, S., Aebi, M., and Locher, K. P. (2011) X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350-355
14. Matsumoto, S., Shimada, A., Nyirenda, J., Igura, M., Kawano, Y., and Kohda, D. (2013) Crystal structures of an archaeal oligosaccharyltransferase provide insights into the catalytic cycle of N-linked protein glycosylation. Proc. Natl. Acad. Sci. U.S.A. 110, 17868-17873
15. Gerber, S., Lizak, C., Michaud, G., Bucher, M., Darbre, T., Aebi, M., Reymond, J. L., and Locher, K. P. (2013) Mechanism of bacterial oligosaccharyltransferase: in vitro quantification of sequon binding and catalysis. J. Biol. Chem. 288, 8849-8861
16. Lizak, C., Gerber, S., Michaud, G., Schubert, M., Fan, Y. Y., Bucher, M., Darbre, T., Aebi, M., Reymond, J. L., and Locher, K. P. (2013) Unexpected reactivity and mechanism of carboxamide activation in bacterial N-linked protein glycosylation. Nat. Commun. 4, 2627
17. Grass, S., Buscher, A. Z., Swords, W. E., Apicella, M. A., Barenkamp, S. J., Ozchlewski, N., and St. Geme, J. W., 3rd. (2003) The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol. Microbiol. 48, 737-751 (Pubitemid 36819059)
18. Grass, S., Lichti, C. F., Townsend, R. R., Gross, J., and St Geme, J. W., 3rd. (2010) The Haemophilus influenzae HMW1C protein is a glycosyltransferase that transfers hexose residues to asparagine sites in the HMW1 adhesin. PLoS Pathog. 6, e1000919
19. Gross, J., Grass, S., Davis, A. E., Gilmore-Erdmann, P., Townsend, R. R., and St Geme, J. W., 3rd. (2008) The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual N-linked carbohydrate modification. J. Biol. Chem. 283, 26010-26015
20. Choi, K. J., Grass, S., Paek, S., St. Geme, J. W., 3rd, and Yeo, H. J. (2010) The Actinobacillus pleuropneumoniae HMW1C-like glycosyltransferase mediates N-linked glycosylation of the Haemophilus influenzae HMW1 adhesin. PLoS One 5, e15888
21. Schwarz, F., Fan, Y. Y., Schubert, M., and Aebi, M. (2011) Cytoplasmic N-glycosyltransferase of Actinobacillus pleuropneumoniae is an inverting enzyme and recognizes the NX(S/T) consensus sequence. J. Biol. Chem. 286, 35267-35274
22. Kawai, F., Grass, S., Kim, Y., Choi, K. J., St Geme, J. W., 3rd, and Yeo, H. J. (2011) Structural insights into the glycosyltransferase activity of the Actinobacillus pleuropneumoniae HMW1C-like protein. J. Biol. Chem. 286, 38546-38557
23. Naegeli, A., Neupert, C., Fan, Y. Y., Lin, C. W., Poljak, K., Papini, A. M., Schwarz, F., and Aebi, M. (2014) Molecular analysis of an alternative Nglycosylation machinery by functional transfer from Actinobacillus pleuropneumoniae to Escherichia coli. J. Biol. Chem. 289, 2170-2179
24. Gawthorne, J. A., Tan, N. Y., Bailey, U. M., Davis, M. R., Wong, L. W., Naidu, R., Fox, K. L., Jennings, M. P., and Schulz, B. L. (2014) Selection against glycosylation sites in potential target proteins of the general HMWC N-glycosyltransferase in Haemophilus influenzae. Biochem. Biophys. Res. Commun. 445, 633-638
25. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
26. Hart, G. W., Housley, M. P., and Slawson, C. (2007) Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022 (Pubitemid 46676063)
27. Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., Wright, P. E., and Wüthrich, K. (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids: IUPAC-IUBMB-IUPAB Inter-Union Task Group on the standardization of data bases of protein and nucleic acid structures determined by NMR spectroscopy. J. Biomol. NMR 12, 1-23 (Pubitemid 128512831)
28. Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V., and Notredame, C. (2006) Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 34, W604-W608 (Pubitemid 44529841)
29. Lazarus, M. B., Jiang, J., Kapuria, V., Bhuiyan, T., Janetzko, J., Zandberg, W. F., Vocadlo, D. J., Herr, W., and Walker, S. (2013) HCF-1 is cleaved in the active site of O-GlcNAc transferase. Science 342, 1235-1239
30. Dorfmueller, H. C., Borodkin, V. S., Blair, D. E., Pathak, S., Navratilova, I., and van Aalten, D. M. (2011) Substrate and product analogues as human O-GlcNAc transferase inhibitors. Amino Acids 40, 781-792
31. Lairson, L. L., Henrissat, B., Davies, G. J., and Withers, S. G. (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
32. Lolli, F., Mazzanti, B., Pazzagli, M., Peroni, E., Alcaro, M. C., Sabatino, G., Lanzillo, R., Brescia Morra, V., Santoro, L., Gasperini, C., Galgani, S., D'Elios, M. M., Zipoli, V., Sotgiu, S., Pugliatti, M., Rovero, P., Chelli, M., and Papini, A. M. (2005) The glycopeptide CSF114(Glc) detects serum antibodies in multiple sclerosis. J. Neuroimmunol. 167, 131-137 (Pubitemid 41242294)
33. Soya, N., Shoemaker, G. K., Palcic, M. M., and Klassen, J. S. (2009) Comparative study of substrate and product binding to the human ABO(H) blood group glycosyltransferases. Glycobiology 19, 1224-1234
34. Kubota, T., Shiba, T., Sugioka, S., Furukawa, S., Sawaki, H., Kato, R., Wakatsuki, S., and Narimatsu, H. (2006) Structural basis of carbohydrate transfer activity by human UDP-GalNAc: polypeptide α-N- acetylgalactosaminyltransferase (pp-GalNAc-T10). J. Mol. Biol. 359, 708-727 (Pubitemid 43767270)
35. Raman, J., Fritz, T. A., Gerken, T. A., Jamison, O., Live, D., Liu, M., and Tabak, L. A. (2008) The catalytic and lectin domains of UDP-GalNAc: polypeptide α-N-acetylgalactosaminyltransferase function in concert to direct glycosylation site selection. J. Biol. Chem. 283, 22942-22951
36. Moréra, S., Imberty, A., Aschke-Sonnenborn, U., Rüger, W., and Freemont, P. S. (1999) T4 phageß-glucosyltransferase: substrate binding and proposed catalytic mechanism. J. Mol. Biol. 292, 717-730 (Pubitemid 29457331)
37. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P., and Walker, S. (2011) Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564-567
38. Sun, H. Y., Lin, S. W., Ko, T. P., Pan, J. F., Liu, C. L., Lin, C. N., Wang, A. H., and Lin, C. H. (2007) Structure and mechanism of Helicobacter pylori fucosyltransferase: a basis for lipopolysaccharide variation and inhibitor design. J. Biol. Chem. 282, 9973-9982 (Pubitemid 47104602)
39. Petrescu, A. J., Milac, A. L., Petrescu, S. M., Dwek, R. A., and Wormald, M. R. (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14, 103-114 (Pubitemid 38263095)
40. Zielinska, D. F., Gnad, F., Wiśniewski, J. R., and Mann, M. (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907
41. Kasturi, L., Eshleman, J. R., Wunner, W. H., and Shakin-Eshleman, S. H. (1995) The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein. J. Biol. Chem. 270, 14756-14761
42. Valliere-Douglass, J. F., Eakin, C. M., Wallace, A., Ketchem, R. R., Wang, W., Treuheit, M. J., and Balland, A. (2010) Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs. J. Biol. Chem. 285, 16012-16022
43. Kirby, A. J., Komarov, I. V., and Feeder, N. (2001) Synthesis, structure and reactions of the most twisted amide. J. Chem. Soc. Perkin Trans. 2, 522-529
44. Schimpl, M., Zheng, X., Borodkin, V. S., Blair, D. E., Ferenbach, A. T., Schüttelkopf, A. W., Navratilova, I., Aristotelous, T., Albarbarawi, O., Robinson, D. A., Macnaughtan, M. A., and van Aalten, D. M. (2012) O-GlcNAc transferase invokes nucleotide sugar pyrophosphate participation in catalysis. Nat. Chem. Biol. 8, 969-974
45. Landström, J., Persson, K., Rademacher, C., Lundborg, M., Wakarchuk, W., Peters, T., and Widmalm, G. (2012) Small molecules containing hetero-bicyclic ring systems compete with UDP-Glc for binding to WaaG glycosyltransferase. Glycoconj. J. 29, 491-502
46. Goddard, T. D. and Kneller, D. G. (2008) Sparky, Version 3, University of California, San Francisco, CA