Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites

Glycobiology

Volumn 15, Issue 2, 2005, Pages 153-164

  Julenius, Karin ^a   Mølgaard, Anne ^a   Gupta, Ramneek ^a   Brunak, Søren ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Machine learning; Mucin type; Neural networks; O glycosylation; Prediction

Indexed keywords

GLYCOSYLTRANSFERASE; MUCIN;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ARTIFICIAL NEURAL NETWORK; CARBOHYDRATE ANALYSIS; CONSENSUS SEQUENCE; CONTROLLED STUDY; GENETIC CODE; HUMAN; IN VIVO STUDY; MAMMAL CELL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN DATABASE; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY;

ALGORITHMS; AMINO ACID MOTIFS; ANIMALS; CONSENSUS SEQUENCE; DATABASES, PROTEIN; GLYCOSYLATION; HUMANS; MAMMALS; MUCINS;

MAMMALIA;

EID: 13644257223     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwh151     Document Type: Article

References (66)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
2. 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.
3. Asker, N., Baeckstrom, D., Axelsson, M.A.B., Carlstedt, I., and Hansson, G.C. (1995) The human MUC2 apoprotein appears to dimerize before O-glycosylation and shares epitopes with the "insoluble" mucin of rat small intestine. Biochem. J., 308, 873-880.
4. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (forthcoming) Improved prediction of signal peptides - signalp 3.0. J. Mol. Biol.
5. Bennett, E.P., Hassan, H., Hollingsworth, M.A., and Clausen, H. (1999) A novel human UDP-N-acetyl-D-galactosamine:polypeptide N-acetyl-galactosaminyltransferase, GalNAc-T7, with specificity for partial GalNAc-glycosylated acceptor substrates. FEBS Lett., 460 226-230.
6. Boeckmann, B., Bairoch, A., Apweiler, R., Blatter, M.C., Estreicher, A., Gasteiger, E., J., M.M., Michoud, K., O'Donovan, C., Phan, I., and others. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res., 31, 365-370.
7. Cai, Y.D. and Chou, K.C. (1996) Artificial neural network model for predicting the specificity of GalNAc-transferase. Anal. Biochem., 243, 284-285.
8. Cai, Y.D., Liu, X.J., Xu, X.B. and Chou, K.C. (2002) Support vector machines for predicting the specificity of GalNAc-transferase. Peptides, 23, 205-208.
9. Cai, Y.D., Yu, H. and Chou, K.C. (1997) Artificial neural network method for predicting the specificity of GalNAc-transferase. J. Protein Chem., 16, 689-700.
10. Carraway, K.L. and Hull, S.R. (1991) Cell surface mucin-type glycoproteins and mucin-like domains. Glycobiology, 1, 131-138.
11. Chothia, C. and Lesk, A.M. (1986) Relationship between the divergence of sequence and structure in proteins. EMBO J., 5, 823-827.
12. Chou, K.C. (1995) A sequence-coupled vector-projection model for predicting the specificity of GalNAc-transferase. Protein Sci., 4, 1365-1383.
13. Chou, K.C., Zhang, C.T., Kezdy, F.J. and Poorman, R.A. (1995) A vector projection method for predicting the specificity of GalNAc-transferase. Proteins, 21, 118-126.
14. Christlet, T.H.T. and Veluraja, K. (2001) Database analysis of O-glycosylation sites in proteins. Biophys. J., 80, 952-960.
15. Coltart, D.M., Royyuru, A.K., Williams, L.J., Glunz, P.W., Sames, D., Kuduk, S.D., Schwarz, J.B., Chen, X.T., Danishefsky, S.J., and Live, D.H. (2002) Principles of mucin architecture: Structural studies on synthetic glycopeptides bearing clustered mono-, di-, tri-, and hexasaccharide glycodomains. J. Am. Chem. Soc., 124, 9833-9844.
16. Dalal, S., Balasubramanian, S. and Regan, L. (1997) Protein alchemy: changing beta-sheet into alpha-helix. Nat. Struct. Biol., 4, 548-552.
17. Elhammer, Å.P., Poorman, R.A., Brown, E., Maggiora, L.L., Hoogerheide, J.G. and Kézdy, F.J. (1993) The specificty of UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase as inferred from a database of in vivo substrates and from the in vitro glycosylation of proteins and peptides. J. Biol. Chem., 268, 10029-10038.
18. Gerbaud, V., Pignol, D., Loret, E., Bertrand, J.A., Berland, Y., Fontecilla-Camps, J.C., Canselier, J.P., Gabas, N., and Verdier, J.M. (2000) Mechanism of calcite crystal growth inhibition by the N-terminal undecapeptide of lithostathine. J. Biol. Chem., 275, 1057-1064.
19. Gerken, T.A. (2004) Kinetic modeling confirms the biosynthesis of mucin core 1 (beta-Gal(1-3)alpha-GalNAc-O-ser/thr) O-glycan structures are modulated by neighboring glycosylation effects. Biochemistry, 43, 4137-4142.
20. Gerken, T.A., Owen, C.L., and Pasumarthy, M. (1997) Determination of the site-specific O-glycosylation pattern of the porcine submaxillary mucin tandem repeat glycopeptide. J. Biol. Chem., 272, 9709-9719.
21. Gerstein, M. and Levitt, M. (1998) Comprehensive assessment of automatic structural alignment against a manual standard; the scop classification of proteins. Protein Sci., 7, 445-456.
22. Gorodkin, J., Lund, O., Andersen, C.A., and Brunak, S. (1999) Using sequence motifs for enhanced neural network prediction of protein distance constraints. In Lengauer, T., Schneider, R., Bork, P., Brutlag, D., Glasgow, J., Mewes, H.W., and Zimmer, R. (Eds.), Proceedings of the Seventh International Conference for Molecular Biology. pp. 95-105.
23. Gupta, R., Birch, H., Rapacki, K., Brunak, S., and Hansen, J.E. (1999) O-GLYCBASE version 4.0: a revised database of O-glycosylated proteins. Nucleic Acids Res., 27, 370-372.
24. Hanisch, F.G., Reis, C.A., Clausen, H., and Paulsen, H. (2001) Evidence for glycosylation-dependent activities of polypeptide N-acetylgalacto-saminyltransferases rGalNAc-T2 and -T4 on mucin glycopeptides. Glycobiology, 11, 731-740.
25. Hansen, J.E., Lund, O., Engelbrecht, J., Bohr, H., Nielsen, J.O., Hansen, J.E., and Brunak, S. (1995) Prediction of O-glycosylation of mammalian proteins: specificity patterns of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase. Biochem. J., 308, 801-813.
26. Hansen, J.E., Lund, O., Gooley, A.A., Williams, K.L., and Brunak, S. (1998) NetOGlyc. Prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj. J., 15, 115-130.
27. Hart, G.W. (1992) Glycosylation. Curr. Opin. Cell Biol. 4, 1017-1023.
28. Henikoff, S. and Henikoff, J.G. (1992) Amino acid subsitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA, 89, 10915-10919.
29. Hertz, J., Krogh, A., and Palmer, R. (1991) Introduction to the theory of neural computation. Redwood City, CA: Addison-Wesley.
30. Jensen, L.J., Gupta, R., Blom, N., Devos, D., Tamames, J., Kesmir, C., Nielsen, H., Stærfeldt, H.H., Rapacki, K., Workman, C., and others. (2002) Prediction of human protein function from post-translational modifications and localization features. J. Mol. Biol., 319, 1257-1265.
31. Jensen, L.J., Gupta, R., Stærfeldt, H.H., and Brunak, S. (2003) Prediction of human protein function according to Gene Ontology categories. Bioinformatics, 19, 635-642.
32. Jentoft, N. (1990) Why are proteins O-glycosylated? Trends Biochem. Sci., 15, 291-294.
33. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol., 292 195-202.
34. Kato, K., Takeuchi, H., Miyahara, N., Kanoh, A., Hassan, H., Clausen, H., and Irimura T. (2001) Distinct orders of GalNAc incorporation into a peptide with consecutive threonines. Biochem. Biophys. Res. Commun., 287, 110-115.
35. Kinarsky, L., Suryanarayanan, G., Prakash, O., Paulsen, H., Clausen, H., Hanisch, F.G., Hollingsworth, M.A., and Sherman, S. (2003) Conformational studies on the MUC1 tandem repeat glycopeptides: implication for the enzymatic O-glycosylation of the mucin protein core. Glycobiology, 13, 929 939.
36. Kirnarsky, L., Nomoto, M., Ikematsu, Y., Hassan, H., Bennet, E.P., Cerny, R.L., Clausen, H., Hollingsworth, M.A., and Sherman, S. (1998) Structural analysis of peptide substrates for mucin-type O-glycosylation. Biochemistry, 37, 12811-12817.
37. Knepper, T.P., Arbogast, B., Schreurs, J., and Deinzer, M.L. (1992) Determination of the glycosylation patterns, disulphide linkages, and protein heterogeneities of baculovirus- expressed mouse interleukin-3 by mass spectrometry. Biochemistry, 31, 11651-11659.
38. Matthews, BW. (1975) Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim. Biophys. Acta, 405, 442-451.
39. McGuffin, L.J., Bryson, K., and Jones, D.T. (2000) The PSIPRED protein structure prediction server. Bioinformatics, 16 404-405.
40. Neumann, G.M., Marinaro, J.A., and Bach, L.A. (1998) Identification of O-glycosylation sites and partial characterization of carbohydrate structure and disulfide linkages of human insulin-like growth factor binding protein 6. Biochemistry, 37, 6572-6585.
41. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng., 10, 1-6.
42. Nishimori, I., Johnson, N.R., Sanderson, S.D., Perini, F., Mountjoy, K., Cerny, R.L., Gross, M.L., and Hollingsworth, M.A. (1994) Influence of acceptor substrate primary amino acid sequence on the activity of human UDP-N-acetylgalactosamine:polypeptide N-Acetylgalactos-aminyltransferase. J. Biol. Chem., 269, 16123-16130.
43. O'Connell, B., Tabak, L.A., and Ramasubbu, N. (1991) The influence of flanking sequences on O-glycosylation. Biochem. Biophys. Res. Commun., 180, 1024-1030.
44. O'Connell, B.C., Hagen, F.K., and Tabak, L.A. (1992) The influence of flanking sequence on the O-glycosylation of threonine in vitro. J. Biol. Chem., 267, 25010-25018.
45. Peters, B.P., Krzesicki, R.F., Perini, F., and Ruddon, R.W. (1989) O-glycosylation of the α-subunit does not limit the assembly of chorionic gonadotropin αβ dimer in human malignant and nonmalignant trophoblast cells. Endocrinology, 124, 1602-1612.
46. Qian, N. and Sejnowski, T.J. (1988) Prediction the secondary structure of globular proteins using neural network models. J. Mol. Biol., 202, 865-884.
47. Riesner, D. (2003). Biochemistry and structure of prp(c) and prp(sc). Br. Med. Bull., 66, 21-33.
48. Schuman, J., Qiu, D., Koganty, R.R., Longenecker, B.M., and Campbell, A.P. (2000) Glycosylations versus conformational preferences of cancer associated mucin core. Glycoconj. J., 17, 835-848.
49. Schuman, J., Campbell, A.P., Koganty, R.R., and Longenecker, B.M. (2003) Probing the conformational and dynamical effects of O-glycosylation within the immunodominant region of a MUC1 peptide tumor antigen. J. Peptide Res., 61, 91-108.
50. Seitz, O. (2000) Glycopeptide synthesis and the effects of glycosylation on protein structure and activity. Chembiochem., 1 214-246.
51. Sørensen, T., White, T., Wandall, H.H., Kristensen, A.K., Roepstorff, P., and Clausen, H. (1995) UDP-N-acetyl-a-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase. J. Biol. Chem., 270, 24166-24173.
52. Spiro, R.G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology, 12, 43R-56R.
53. Strous, G.J. and Dekker, J. (1992) Mucin-type glycoproteins. Crit. Rev. Biochem. Mol. Biol., 27, 57 92.
54. Tagashira, M., Iijimia, H., and Toma, K. (2002) An NMR study of O-glycosylation induced structural changes in the α-helix of calcitonin. Glycoconj. J., 19, 43-52.
55. Takeuchi, H., Kato, K., Hassan, H., Clausen, H., and Irimura, T. (2002) O-GalNAc incorporation into a cluster acceptor site of three consecutive threonines. Distinct specificity of GalNAc-transferase isoforms. Eur. J. Biochem, 269, 6173-6193.
56. Ten Hagen, K.G., Tetaert, D., Hagen, F.K., Richet, C., Beres, T.M., Gagnon, J., Balys, M.M., VanWuyckhuyse, B., Bedi, G.S., Degand, P., and Tabak, L.A. (1999) Characterization of a UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase that displays glycopeptide N-acetylgalactosaminyltransferase activity. J. Biol. Chem., 274 27867-27874.
57. Ten Hagen, K.G., Bedi, G.S., Tetaert, D., Kingsley, P.D., Hagen, F.K., Balys, M,M., Beres, T.M., Degand, P., and Tabak, L.A. (2001) Cloning and characterization of a ninth membre of the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase family, ppGaNTase-T9. J. Biol. Chem., 276, 17395-17404.
58. Ten Hagen, K.G., Fritz, T.A., and Tabak, L.A. (2003) All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology, 13, 1R-16R.
59. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
60. Van den Steen, P., Rudd, P.M., Dwek, R.A., and Opdenakker, G. (1998) Concepts and principles of O-linked glycosylation. Crit. Rev. Biochem. Mol. Biol., 33, 151-208.
61. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology, 3, 97-130.
62. Wang, H., Tachibana, K., Zhang, Y., Iwasaki, H., Kameyama, A., Cheng, L., Guo, J., Hiruma, T., Togayachi, A., Kudo, T., and others. (2003) Cloning and characterization of a novel UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase, pp-GalNAc-T14. Biochem. Biophys. Res. Commun., 300, 738-744.
63. Westbrook, J., Feng, Z., Chen, L., Yang, H., and Berman, H.M. (2003) The Protein Data Bank and structural genomics. Nucleic Acids Res., 31, 489-491.
64. Wilson, I.B., Gavel, Y., and von Heijne, G. (1991) Amino acid distributions around O-linked glycosylation sites. Biochem. J., 275, 529-534.
65. Yoshida, A., Suzuki, M., Ikenaga, H., and Takeuchi, M. (1997) Discovery of the shortest sequence motif for high level mucin-type O-glycosylation. J. Biol. Chem., 272, 16884-16888.
66. Young, J.D., Tsuchiya, D., Sandlin, D.E., and Holroyde, M.J. (1979) Enzymic O-glycosylation of synthetic peptides from sequences in basic myelin protein. Biochemistry, 18, 4444-4448.