Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency

Molecular and Cellular Proteomics

Volumn 8, Issue 2, 2009, Pages 357-364

  Schulz, Benjamin L ^a,b   Aebi, Markus ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; FUNGAL ENZYME; GLYCAN; GLYCOPEPTIDE; GLYCOPROTEIN; POLYSACCHARIDE;

ARTICLE; CELL WALL; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EUKARYOTE; FUNCTIONAL PROTEOMICS; LIQUID CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARALOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; GLYCOMICS; GLYCOSYLATION; HEXOSYLTRANSFERASES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDES; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SUBSTRATE SPECIFICITY;

EUKARYOTA;

EID: 61649089751     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M800219-MCP200     Document Type: Article

References (36)

1. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049
2. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867
3. Sharon, N., and Lis, H. (1995) Lectins - proteins with a sweet tooth: functions in cell recognition. Essays Biochem. 30, 59-75
4. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3, 97-130
5. Kelleher, D. J., and Gilmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47R-62R
6. Szymanski, C. M., and Wren, B. W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3, 225-237
7. Kelleher, D. J., Banerjee, S., Cura, A. J., Samuelson, J., and Gilmore, R. (2007) Dolichol-linked oligosaccharide selection by the oligosaccharyl-transferase in protist and fungal organisms. J. Cell Biol. 177, 29-37
8. Chen, W., and Helenius, A. (2000) Role of ribosome and translocon complex during folding of influenza hemagglutinin in the endoplasmic reticulum of living cells. Mol. Biol. Cell 11, 765-772
9. Whitley, P., Nilsson, I., and von Heijne, G. (1996) A nascent secretory protein may traverse the ribosome/endoplasmic reticulum translocase complex as an extended chain. J. Biol. Chem. 271, 6241-6244
10. Kowarik, M., Numao, S., Feldman, M. F., Schulz, B. L., Callewaert, N., Kiermaier, E., Catrein, I., and Aebi, M. (2006) N-Linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 314, 1148-1150
11. Weerapana, E., and Imperiali, B. (2006) Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16, 91R-101R
12. Spirig, U., Bodmer, D., Wacker, M., Burda, P., and Aebi, M. (2005) The 3.4-kDa Ost4 protein is required for the assembly of two distinct oligosaccharyltransferase complexes in yeast. Glycobiology 15, 1396-1406
13. Yan, A., and Lennarz, W. J. (2005) Two oligosaccharyl transferase complexes exist in yeast and associate with two different translocons. Glycobiology 15, 1407-1415
14. Schwarz, M., Knauer, R., and Lehle, L. (2005) Yeast oligosaccharyltransferase consists of two functionally distinct sub-complexes, specified by either the Ost3p or Ost6p subunit. FEBS Lett. 579, 6564-6568
15. Fetrow, J. S., Siew, N., Di Gennaro, J. A., Martinez-Yamout, M., Dyson, H. J., and Skolnick, J. (2001) Genomic-scale comparison of sequence-and structure-based methods of function prediction: does structure provide additional insight? Protein Sci 10, 1005-1014
16. Hägglund, P., Matthiesen, R., Elortza, F., Højrup, P., Roepstorff, P., Jensen, O. N., and Bunkenborg, J. (2007) An enzymatic deglycosylation scheme enabling identification of core fucosylated N-glycans and O-glycosylation site mapping of human plasma proteins. J. Proteome Res. 6, 3021-3031
17. Wada, Y., Tajiri, M., and Yoshida, S. (2004) Hydrophilic affinity isolation and MALDI multiple-stage tandem mass spectrometry of glycopeptides for glycoproteomics. Anal. Chem. 76, 6560-6565
18. Vijayraghavan, U., Company, M., and Abelson, J. (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev. 3, 1206-1216
19. Yin, Q. Y., de Groot, P. W., Dekker, H. L., de Jong, L., Klis, F. M., and de Koster, C. G. (2005) Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J. Biol. Chem. 280, 20894-20901
20. Cuff, J. A., Clamp, M. E., Siddiqui, A. S., Finlay, M., and Barton, G. J. (1998) JPred: a consensus secondary structure prediction server. Bioinformatics 14, 892-893
21. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
22. Sjolander, K. (1998) Phylogenetic inference in protein superfamilies: analysis of SH2 domains. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 165-174
23. Krokhin, O. V., Antonovici, M., Ens, W., Wildins, J. A., and Standing, K. G. (2006) Deamidation of -Asn-Gly- sequences during sample preparation for proteomics: consequences for MALDI and HPLC-MALDI analysis. Anal. Chem. 78, 6645-6650
24. Robinson, N. E., Robinson, Z. W., Robinson, B. R., Robinson, A. L., Robinson, J. A., Robinson, M. L., and Robinson, A. B. (2004) Structure-dependent nonenzymatic deamidation of glutaminyl and asparaginyl pentapeptides. J. Pept. Res. 63, 426-436
25. Hütsmeier, A. J., Paesold-Burda, P., and Hennet, T. (2007) N-Glycosylation site occupancy in serum glycoproteins using multiple reaction monitoring liquid chromatography mass spectrometry. Mol. Cell. Proteomics 6, 2132-2138
26. Ben-Dor, S., Esterman, N., Rubin, E., and Sharon, N. (2004) Biases and complex patterns in the residues flanking protein N-glycosylation sites. Glycobiology 14, 95-101
27. 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
28. Karaoglu, D., Kelleher, D. J., and Gilmore, R. (1995) Functional characterization of Ost3p. Loss of the 34-kD subunit of the Saccharomyces cerevisiae oligosaccharyltransferase results in biased underglycosylation of acceptor substrates. J. Cell Biol. 130, 567-577
29. Kelleher, D. J., Karaoglu, D., Mandon, E. C., and Gilmore, R. (2003) Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12, 101-111
30. Garshasbi, M., Hadavi, V., Habibi, H., Kahrizi, K., Kariminejad, R., Behjati, F., Tzschach, A., Najmabadi, H., Ropers, H. H., and Kuss, A. W. (2008) A defect in the TUSC3 gene is associated with autosomal recessive mental retardation. Am. J. Hum. Genet. 82, 1158-1164
31. Molinari, F., Foulquier, F., Tarpey, P. S., Morelle, W., Boissel, S., Teague, J., Edkins, S., Futreal, P. A., Stratton, M. R., Turner, G., Matthijs, G., Gecz, J., Munnich, A., and Colleaux, L. (2008) Oligosaccharyltransferase-subunit mutations in non-syndromic mental retardation. Am. J. Hum. Genet. 82, 1150-1157
32. Bause, E., and Legler, G. (1981) The role of the hydroxy amino acid in the triplet sequence Asn-Xaa-Thr(Ser) for the N-glycosylation step during glycoprotein biosynthesis. Biochem. J. 195, 639-644
33. Caragea, C., Sinapov, J., Silvescu, A., Dobbs, D., and Honavar, V. (2007) Glycosylation site prediction using ensembles of Support Vector Machine classifiers. BMC Bioinformatics 9, 438
34. Kasturi, L., Chen, H., and Shakin-Eshleman, S. H. (1997) Regulation of N-linked core glycosylation: use of a site-directed mutagenesis approach to identify Asn-Xaa-Ser/Thr sequons that are poor oligosaccharide acceptors. Biochem. J. 323, 415-419
35. Mellquist, J. L., Kasturi, L., Spitalnik, S. L., and Shakin-Eshleman, S. H. (1998) The amino acid following an Asn-X-Ser/Thr sequon is an important determinant of N-linked core glycosylation efficiency. Biochemistry 37, 6833-6837
36. Shakin-Eshleman, S. H., Spitalnik, S. L., and Kasturi, L. (1996) The amino acid at the X position of an Asn-X-Ser sequon is an important determinant of N-linked core-glycosylation efficiency. J. Biol. Chem. 271, 6363-6366