Scanning the available Dictyostelium discoideum proteome for O-linked GlcNAc glycosylation sites using neural networks

Glycobiology

Volumn 9, Issue 10, 1999, Pages 1009-1022

  Gupta, Ramneek ^a   Jung, Eva ^b   Gooley, Andrew A ^b   Williams, Keith L ^b   Brunak, Søren ^a   Hansen, Jan ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

Dictyostelium; Neural networks; O glycosylation; Prediction; Proteome

Indexed keywords

GLYCOPROTEIN; MEMBRANE PROTEIN; N ACETYLGLUCOSAMINYLTRANSFERASE; PROTEOME; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL NEURAL NETWORK; DATA BASE; DICTYOSTELIUM DISCOIDEUM; HYDROPHILICITY; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN GLYCOSYLATION; VALIDATION PROCESS;

ALGORITHMS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CARBOHYDRATE SEQUENCE; DICTYOSTELIUM; GLYCOPROTEINS; GLYCOSYLATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NEURAL NETWORKS (COMPUTER); PEPTIDE MAPPING; PROTEOME; PROTOZOAN PROTEINS;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; PROTOZOA;

EID: 0032828561     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/9.10.1009     Document Type: Article

References (81)

1. Abola, E.E., Bernstein, F.C., Bryant, S.H., Koetzle, T.F. and Weng, J. (1987) Protein Data Bank. In Allen, F.H., Bergerhoff, G. and Sievers, R. (eds.), Crystallographic Databases - Information Content, Software Systems, Scientific Applications. Data Commission of the International Union of Crystallography, Bonn/Cambridge/Chester, pp. 107-132.
2. Aubert, J.P., Biserte, G. and Loucheux-Lefebur, M.H. (1976) Carbohydrate-peptide linkage in glycoproteins. Arch. Biochem. Biophys, 175, 410-418.
3. Bairoch, A. and Apweiler, R. (1998) The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1998. Nucleic Acids Res., 26, 38-42.
4. Baldi, P. and Brunak, S. (1998) Bioinformatics: The Machine Learning Approach. MIT Press, Cambridge, MA.
5. Barth, A., Muller-Taubenberger, A., Taranto, P. and Gerisch, G. (1994) Replacement of the phospholipid-anchor in the Contact Site A glycoprotein of D.discoideum by a transmembrane region does not impede cell adhesion but reduces time on the cell surface. J. Cell. Biol., 124, 205-215.
6. Bause, A. (1983) Structural requirements of N-glycosylation of proteins. Biochem. J., 209, 331-336.
7. Benson, D.A., Boguski, M.S., Lipman, D.J., Ostell, J. and Ouellette, B.F.F. (1998) GenBank. Nucleic Acids Res., 26, 1-7.
8. Bernstein, F.C., Koetzle, T.F., Williams, G.J.B., Meyer, E.F.Jr., Brice, M.D., Rodgers, J.R., Kennard, O., Shimanouchi, T. and Tasumi, M. (1977) The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol., 112, 535-542.
9. Blom, N., Hansen, J.E., Blaas, D. and Brunak, S. (1996) Cleavage site analysis in picomaviral polyproteins: discovering cellular targets by neural networks. Protein Sci., 5, 2203-2216.
10. Casari, G., Ouzounis, C., Valencia, A. and Sander, C. (1996) Genequiz-II: automatic function assignment for genome sequence analysis. In Proceedings of the First Annual Pacific Symposium on Biocomputing. World Scientific, Hawaii, pp. 707-709.
11. 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 Struct. Funct. Genet., 21, 118-126.
12. Clausen, H. and Bennett, E. (1996) A family of UDP-GalNAc: polypeptide N-acetylgalactosaminyl-transferases control the initiation of mucin-type O-linked glycosylation. Glycobiology, 6, 635-646.
13. Connolly, M.L. (1993) The molecular surface package. J. Mol. Graph., 11, 139-141.
14. Elhammer, A.P., Poorman, R.A., Brown, E., Maggiora, L.L., Hoogerheide, J.G. and Kezdy, F.J. (1993) The specificity 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.
15. Fang, H., Higa, M., Suzuki, K., Aiba, K., Urushihara, H. and Yanagisawa, K. (1993) Molecular cloning and characterization of two genes encoding gp138, a cell surface glycoprotein involved in the sexual cell fusion of Dictyostelium discoideum. Dev. Biol., 156, 201-208.
16. Fucini, P., Renner, C., Herberhold, C. and Noegel, A.A. (1997) The repeating segments of the F-actin cross-linking gelation factor (ABP-120) have an immunoglobulin-like fold. Nature Struct. Biol., 4, 223-230.
17. Giorda, R., Ohmachi, T., Shaw, D.R. and Ennis, H.L. (1990) A shared internal threonine-glutamic acid-threonine-proline repeat defines a family of Dictyostelium discoideum spore germination specific proteins. Biochemistry, 29, 7264-7269.
18. Goochee, C.F., Gramer, M.J., Anderson, D.C., Bahr, J.B. and Rasmussen, J.R. (1991) The oligosaccharides of glycoproteins: bioprocess factors affecting oligosaccharide structure and their effect on glycoprotein properties. Biol Technology, 9, 1347-1355.
19. Gooley, A.A. and Williams, K.L. (1994) Towards characterizing O-glycans: the relative merits of in vivo and in vitro approaches in seeking peptide motifs specifying O-glycosylation sites. Glycobiology, 4, 413-417.
20. Gooley, A.A. and Williams, K.L. (1997) How to find, identify and quantitate the sugars on proteins. Nature, 385, 557-559.
21. Gooley, A.A., Classon, B.J., Marschalek, R. and Williams, K.L. (1991) Glycosylation sites identified by detection of glycosylated amino acids released from Edman degradation: the identification of Xaa-Pro-Xaa-Xaa as a motif for Thr-O-glycosylation. Biochem. Biophys. Res. Commun., 178, 1194-1201.
22. Gooley, A.A., Marschalek, R. and Williams, K.L. (1992) Size polymorphisms due to changes in the number of O-glycosylated tandem repeats in the Dictyostelium discoideum glycoprotein PsA. Genetics, 130, 749-756.
23. Haltiwanger, R.S., Blomberg, M.A. and Hart, G.W. (1992) Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide β-N-acetylglucosaminyltransferase. J. Biol. Chem., 267, 9005-9013.
24. Handman, E., Barnett, L.D., Osborn, A.H., Goding, J.W. and Murray, P.J. (1993) Identification, characterisation and genomic cloning of a O-linked N-acetylglucosamine-containing cytoplasmic Leishmania glycoprotein. Mol. Biochem. Parasitol., 62, 61-72.
25. Hansen, J.E., Lund, O., Rapacki, K., Clausen, H., Mosekilde, E., Nielsen, J.O. and Hansen, J.E.S. (1994) Glycosylation and Protein Conformation. In Bohr, H. and Brunak, S. (eds.), Protein Structure by Distance Analysis. IOS Press, Amsterdam, pp. 247-254.
26. Hansen, J.E., Lund, O., Engelbrecht, J., Bohr, H., Nielsen, J.O., Hansen, J.E.S. and Brunak, S. (1995) Prediction of O-glycosylation of mammalian proteins: specificity patterns of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase. Biochem. J., 308, 801-813.
27. Hansen, J.E., Lund, O., Nilsson, J., Rapacki, K. and Brunak, S. (1998a) O-GLYCBASE Version 3.0: a revised database of O-glycosylated proteins. Nucleic Acids Res., 26, 387-389.
28. Hansen, J.E., Lund, O., Tolstrup, N., Gooley, A.A., Williams, K.L. and Brunak, S. (1998b) NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconjugate J., 15, 115-130.
29. Hart, G.W. (1997) Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Annu. Rev. Biochem., 66, 315-335.
30. Hart, G.W., Greis, K.D., Dong, L.Y., Blomberg, M.A., Chou, T.Y., Jiang, M.S., Roquemore, E.P., Snow, D.M., Kreppel, L.K. and Cole, R.N. (1995) O-Linked N-acetylglucosamine: the "yin-yang" of Ser/Thr phosphorylation? Nuclear and cytoplasmic glycosylation. Adv. Exp. Med. Biol., 376, 115-123.
31. Haynes, P.A., Gooley, A.A., Ferguson, M.A., Redmond, J.W. and Williams, K.L. (1993) Post-translational modifications of the Dictyostelium discoideum glycoprotein PsA. Glycosylphosphatidylinositol membrane anchor and composition of O-linked oligosaccharides. Eur. J. Biochem., 216, 729-737.
32. Horton, P. and Nakai, K. (1997) Better prediction of protein cellular localization sites with the k nearest neighbor classifier. In Proc. Fifth Int. Conf. on Intelligent Systems for Molecular Biology. Volume 5. AAAI Press, Menlo Park, CA, pp. 147-152.
33. Hounsell, E.F., Davies, M.J. and Renouf, D.V. (1996) O-linked protein glycosylation structure and function. Glycoconjugate J., 13, 19-26.
34. Jung, E. and Williams, K.L. (1997) The production of recombinant glycoproteins with special reference to simple eukaryotes including Dictyostelium discoideum. Biotechnol. Appl. Biochem., 25, 3-8.
35. Jung, E., Gooley, A.A., Packer, N.H., Slade, M.B., Williams, K.L. and Dittrich, W. (1997) An in vivo approach for the identification of acceptor sites for O-glycosyltransferases: motifs for the addition of O-GlcNAc in Dictyostelium discoideum. Biochemistry, 36, 4034-4040.
36. Jung, E., Gooley, A.A., Packer, N.H., Karuso, P. and Williams, K.L. (1998) Rules for the addition of O-linked N-acetylglucosamine to secreted proteins in Dictyostelium discoideum. Studies on glycosylation of mucin MUC1 and MUC2 repeats. Eur. J. Biochem., 253, 517-524.
37. Kornfeld, R. and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem., 54, 631-664.
38. Kozarov, E., van der Wel, H., Field, M., Gritzali, M., Brown R.D. Jr. and West, C.M. (1995) Characterization of FP21, a cytosolic glycoprotein from Dictyostelium. J. Biol. Chem., 270, 3022-3030.
39. Kreppel, L.K., Blomberg, M.A. and Hart, G.W. (1997) Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem., 272, 9308-9315.
40. Kullback, S. and Leibler, R.A. (1951) On information theory and sufficiency. Ann. Math. Stat., 22, 79-86.
41. Lis, H. and Sharon, N. (1993) Protein glycosylation: structural and functional aspects. Curr. J. Biochem., 218, 1-27.
42. Loomis, W.F. and Smith, D.W. (1995) Consensus phylogeny of Dictyostelium. Experientia, 51, 1110-1115.
43. Lubas, W.A., Frank, D.W., Krause, M. and Hanover, J.A. (1997) O-Linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J. Biol. Chem., 272, 9316-9324.
44. Mang, C. (1995) Analyse der Kohlenhydratstrukturen des Zelladhaesionsproteins contact Site A. PhD thesis. Ludwig Maximilians University, Munich, Germany.
45. Matthews, B.W. (1975) Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim. Biophys. Acta, 405, 442-451.
46. Mehta, D.P., Etchison, J.R., Wu, R. and Freeze, H.H. (1997) UDP-GlcNAc:Ser-protein N-acetylglucosamine-1-phosphotransferase from Dictyostelium discoideum recognizes serine-containing peptides and eukaryotic cysteine proteinases. Biotechnol. Gen. Eng. Rev., 14, 1-35.
47. Moore, J.P., McKeating, J.A., Jones, I.M., Stephens, P.E., Clements, G., Thomson, S. and Weiss, R.A. (1990) Characterization of recombinant gp120 and gp160 from HIV-1: binding to monoclonal antibodies and soluble CD4. AIDS, 4, 307-315.
48. Nakai, K. and Kanehisa, M. (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics, 14, 897-911.
49. Nehrke, K., Hagen, F.K. and Tabak, L.A. (1996) Charge distribution of flanking amino acids influences O-glycan acquisition in vivo. J. Biol. Chem., 271, 7061-7065.
50. 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.
51. Nielsen, H., Brunak, S. and von Heijne, G. (1999) Machine learning approaches for prediction of signal peptides and other protein signals. Protein Eng., 12, 3-9.
52. O'Connell, B.C., Tabak, L.A. and Ramasubbu, N. (1991) The influence of flanking sequence on the O-glycosylation of threonine in vitro. J. Biol. Chem., 180, 1024-1030.
53. O'Connell, B.C., Hagan, F.K. and Tabak, L.A. (1992) The influence of flanking sequence on O-glycosylation. Biochem. Biophys. Res. Commun., 267, 25010-25018.
54. Packer, N.H., Pawlak, A., Kett, W.C., Gooley, A.A., Redmond, J.W. and Williams, K.L. (1997) Proteome analysis of glycoforms: a review of strategies for the microcharacterisation of glycoproteins separated by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis, 18, 452-460.
55. Pisano, A., Redmond, J.W., Williams, K.L. and Gooley, A.A. (1993) Glycosylation sites identified by solid-phase Edman degradation: O-linked glycosylation motifs on human glycophorin A. Glycobiology, 3, 429-435.
56. Presnell, S.R. and Cohen, F.E. (1993) Artificial neural networks for pattern recognition in biochemical sequences. Annu. Rev. Biophy. Biomol. Struct., 22, 283-298.
57. Previato, J.O., Sola-Penna, M., Agrellos, O.A., Jones, C., Oeltmann, T., Travasos, L.R. and Mendonca-Previato, L. (1998) Biosynthesis of O-N-acetylglucosamine-linked glycans in Trypanosoma cruzi. Characterization of the novel uridine diphospho-N-acetylglucosamine:polypeptide N-acetylglucosaminyltransferase-catalyzing formation of N-acetylglucosamine alpha 1 → O-threonine. J. Biol. Chem., 273, 14982-14988.
58. Qian, N. and Sejnowski, T.J. (1988) Predicting the secondary structure of globular proteins using neural network models. J. Mol. Biol., 202, 865-884.
59. Ramalingam, R. and Ennis, H.L. (1997) Characterization of the Dictyostelium discoideum cellulose-binding protein CelB and regulation of gene expression. J. Biol. Chem., 272, 26166-26172.
60. Rose, G.D., Geselowitz, A.R., Lesser, G.J., Lee, R.H. and Zehfus, M.H. (1985) Hydrophobicity of amino acid residues in globular proteins. Science, 229, 834-838.
61. Rost, B. and Sander, C. (1994) Combining evolutionary information and neural networks to predict protein secondary structure. Proteins, 19, 55-72.
62. Roth, J., Wang, Y., Eckhardt, A.E. and Hill, R.L. (1994) Subcellular localization of the UDP-N-acetyl-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase-mediated O-glycosylation reaction in the submaxillary gland. Proc. Natl. Acad. Sci. USA, 91, 8935-8939.
63. Röttger, S., White, J., Wandall, H.H., Olivo, J.C., Stark, A., Bennett, E.R., Whitehouse, C., Berger, E.G., Clausen, H. and Nilsson, T. (1998) Localisation of three human polypeptide GalNAc-transferases in HeLa cells suggests initiation of O-linked glycosylation throughout the Golgi apparatus. J. Cell Sci., 111, 45-60.
64. Rudd, P.M. and Dwek, R.A. (1997) Glycosylation: Heterogeneity and the 3D structure of proteins. Crit. Rev. Biochem. Mol. Biol., 32, 1-100.
65. Rumelhart, D.E., Hinton, G.E. and Williams, R.J. (1986) Learning internal representations by error propagation. In Rumelhart, D., McClelland, J. and the PDP Research Group (eds.), Parallel Distributed Processing: Explorations in the Microstructure of Cognition. 1. Foundations. MIT Press, Cambridge, MA., pp. 318-362.
66. Scharf, M., Schneider, R., Casari, G., Bork, P., Valencia, A., Ouzounis, C. and Sander, C. (1994) Genequiz: a workbench for sequence analysis. In Proc. of Second Int. Conf. on Intelligent Systems for Molecular Biology. AAAI Press, Menlo Park, CA, pp. 348-353.
67. 2+ at 2.2 A: implications for water-mediated specificity. Biochemistry, 35, 9716-9727.
68. Schneider, T.D. and Stephens, R.M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100.
69. Schnuchel, A., Wiltscheck, R., Eichinger, L., Schleicher, M. and Holak, T.A. (1995) Structure of severin domain 2 in solution. J. Mol. Biol., 247, 21-27.
70. Slade, M.B., Emslie, K.R. and Williams, K.L. (1997) Expression of recombinant glycoproteins in the simple eukaryote Dictyostelium discoideum. Biotechnol. Gen. Eng. Rev., 14, 1-35.
71. Snow, D.M. and Hart, G.W. (1998) Nuclear and cytoplasmic glycosylation. Int. Rev. Cytol., 181, 43-74.
72. Sonnhammer, E.L., von Heijne, G. and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. In Proc. Sixth Int. Conf. on Intelligent Systems for Molecular Biology AAAI Press, Menlo Park, CA, pp. 175-182.
73. Teng-umnuay, P., Morris, H.R., Dell, A., Panico, M., Paxton, T. and West, C.M. (1998) The cytoplasmic F-box binding protein SKP1 contains a novel pentasaccharide linked to hydroxyproline in Dictyostelium. J. Biol. Chem., 273, 18242-18249.
74. Ti, Z.C., Wilkins, M.R., Vardy, P.H., Gooley, A.A. and Williams, K.L. (1995) Glycoprotein complexes interacting with cellulose in the "cell print" zones of the Dictyostelium discoideum extracellular matrix. Dev. Biol., 168, 332-341.
75. 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.
76. Wandall, H.H., Hassan, H., Mirgorodskaya, E., Kristensen, A.K., Roepstorff, P., Bennett, E.P., Nielsen, P.A., Hollingsworth, M.A., Burchell, J., Taylor-Papadimitriou, J. and Clausen, H. (1997) Substrate specificities of three members of the human UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase family, GalNAc-T1, -T2 and -T3. J. Biol. Chem., 272, 23503-23514.
77. Wang, Y., Agrawal, N., Eckhardt, A.E., Stevens, R.D. and Hill, R.L. (1993) The acceptor substrate specificity of porcine submaxillary UDP-GalNAc:polypeptide N-acetylgalactosaminyitransferase is dependent on the amino acid sequences adjacent to serine and threonine residues. J. Biol. Chem., 268, 22979-22983.
78. Wilson, I.B.H., Gavel, Y. and von Heijne, G. (1991) Amino acid distributions around O-linked glycosylation sites. Biochem. J., 275, 529-534.
79. 2+ dependent cell-cell adhesion molecule, in Dictyostelium discoideum. J. Biol. Chem., 271, 16399-16408.
80. Wu, C.H. (1997) Artificial neural networks for molecular sequence analysis. Comput. Chem., 21, 237-256.
81. Zachara, N.E., Packer, N.H., Temple, M.D., Slade, M.B., Jardine, D.R., Karuso, P., Moss, C.J., Mabbutt, B.C., Curmi, P.M.G., Williams, K.L. and Gooley, A.A. (1996) Recombinant prespore specific antigen from Dictyostelium discoideum is a β-sheet glycoprotein with a spacer peptide modified by O-linked N-acetylglucosamine. Eur. J. Biochem., 238, 511-518.