Site directed processing: Role of amino acid sequences and glycosylation of acceptor glycopeptides in the assembly of extended mucin type O-glycan core 2

Biochimica et Biophysica Acta - General Subjects

Volumn 1790, Issue 10, 2009, Pages 1244-1257

  Brockhausen, Inka ^a   Dowler, Thomas ^a   Paulsen, Hans ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

4 Gal transferase; Core 1 3 Gal transferase; Core 2 6 GlcNAc transferase; O glycopeptide; Polypeptide GalNAc transferase; Specificity

Indexed keywords

GALACTOSYLTRANSFERASE; GLYCAN; GLYCOPEPTIDE; MUCIN; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATTLE; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GALACTOSYLTRANSFERASES; GLYCOPEPTIDES; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; MUCIN-2; N-ACETYLGALACTOSAMINYLTRANSFERASES; N-ACETYLGLUCOSAMINYLTRANSFERASES; PEPTIDE FRAGMENTS; POLYSACCHARIDES; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY;

EID: 69949105150     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2009.05.020     Document Type: Article

References (62)

1. Hollingsworth M.A., and Swansson B.J. Mucins in cancer: protection and control of the cell surface. Nat. Rev., Cancer 4 (2004) 45-60
2. Brockhausen I., Schutzbach J.S., and Kuhns W. Glycoproteins and their relationship to human disease. Acta Anat. 161 (1998) 36-78
3. Kumar R., Camphausen R.T., Sullivan F.X., and Cumming D.A. Core 2 β1,6-N-acetylglucosaminyltransferase enzyme activity is critical for P-selectin glycoprotein ligand-1 binding to P-selectin. Blood 88 (1996) 3872-3879
4. Allahverdian S., Wojcik K.R., and Dorscheid D.R. Airway epithelial wound repair: role of carbohydrate sialyl Lewis x. Am. J. Physiol., Lung Cell Mol. Physiol. 291 (2006) L828-L836
5. Scharfman A., Arora S.K., Delmotte P., Van Brussel E., Mazurier J., Ramphal R., and Roussel P. Recognition of Lewis x derivatives present on mucins by flagellar components of Pseudomonas aeruginosa. Infect. Immun. 69 (2001) 5243-5248
6. Thomsson K.A., Carlstedt I., Karlsson N.G., Karlsson H., and Hansson G.C. Different O-glycosylation of respiratory mucin glycopeptides from a patient with cystic fibrosis. Glycoconj. J. 15 (1998) 823-833
7. Xia B., Royall J.A., Damera G., Sachdev G.P., and Cummings R.D. Altered O-glycosylation and sulfation of airway mucins associated with cystic fibrosis. Glycobiology 15 (2005) 747-775
8. Brockhausen I. Glycosyltransferases involved in the synthesis of mucin type O-glycans in human cancer cells. EMBO Rep. 7 (2006) 599-604
9. Campbell B.J., Yu L.G., and Rhodes J.M. Altered glycosylation in inflammatory bowel disease: a possible role in cancer development. Glycoconj. J. 18 (2001) 851-858
10. I. Brockhausen, Biosynthesis of complex mucin-type O-glycans. Comprehensive Natural Products Chemistry II Volume 5, Carbohydrates, nucleosides and nucleic acids. G. Wang Ed. Elsevier pub in Press (2009).
11. Brockhausen I., Toki D., Brockhausen J., Peters S., Bielfeldt T., Kleen A., Paulsen H., Meldal M., Hagen F., and Tabak L.A. Specificity of O-glycosylation by bovine colostrum UDP-GalNAc: polypeptide alpha-N-acetylgalactosaminyltransferase using synthetic glycopeptide substrates. Glycoconj. J. 13 (1996) 849-856
12. Brockhausen I., Möller G., Merz G., Adermann K., and Paulsen H. Control of mucin synthesis: the peptide portion of synthetic O-glycopeptide substrates influences the activity of O-glycan core 1 UDP-galactose: N-acetyl-alpha-galactosaminyl-R β3-galactosyl-transferase. Biochemistry 29 (1990) 10206-10212
13. Granovsky M., Bielfeldt T., Peters S., Paulsen H., Meldal M., Brockhausen J., and Brockhausen I. UDP-galactose: glycoprotein-N-acetyl-d-galactosamine 3-β-d-galactosyltransferase activity synthesizing O-glycan core 1 is controlled by the amino acid sequence and glycosylation of glycopeptide substrates. Eur. J. Biochem. 221 (1994) 1039-1046
14. Hanisch F.G., Müller S., Hassan H., Clausen H., Zachara N., Gooley A.A., Paulsen H., Alving K., and Peter-Katalinic J. Dynamic epigenetic regulation of initial O-glycosylation by UDP-N-Acetylgalactosamine:Peptide N-acetylgalactosaminyltransferases site-specific glycosylation of MUC1 repeat peptide influences the substrate qualities at adjacent or distant Ser/Thr positions. J. Biol. Chem. 274 (1999) 9946-9954
15. Fritz T., Hurley J., Trinh L., Shiloach J., and Tabak L. The beginnings of mucin biosynthesis: the crystal structure of UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferase-T1. Proc. Natl. Acad. Sci. U. S. A. 43 (2004) 15307-15312
16. Fritz T.A., Raman J., and Tabak L.A. Dynamic association between the catalytic and lectin domains of human UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferase-2. J. Biol. Chem. 281 (2006) 8613-8619
17. Kubota T., Shiba T., Sugioka S., Furukawa S., Sawaki H., Kato R., Wakatsuki S., and Narimatsu H. Structural basis of carbohydrate transfer activity by human UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferase (pp-GalNAc-T10). J. Mol. Biol. 359 (2006) 708-727
18. Ten Hagen K., Fritz T., and Tabak L. All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13 (2003) 1R-16R
19. Raman J., Fritz T.A., Gerken T.A., Jamison O., Live D., Liu M., and Tabak L.A. The catalytic and lectin domains of UDP-GalNAc:polypeptide alpha-N-Acetylgalactosaminyltransferase function in concert to direct glycosylation site selection. J. Biol. Chem. 283 (2008) 22942-22951
20. Hassan H., Reis C.A., Bennett E.P., Mirgorodskaya E., Roepstorff P., Hollingsworth M.A., Burchell J., Taylor-Papadimitriou J., and Clausen H. The lectin domain of UDP-N-acetyl-d-galactosamine: polypeptide N-acetylgalactosaminyltransferase-T4 directs its glycopeptide specificities. J. Biol. Chem. 275 (2000) 38197-38205
21. Iida S., Takeuchi H., Hassan H., Clausen H., and Irimura T. Incorporation of N-acetylgalactosamine into consecutive threonine residues in MUC2 tandem repeat by recombinant human N-acetyl-d-galactosamine transferase-T1, T2 and T3. FEBS Lett. 449 (1999) 230-234
22. Takeuchi H., Kato K., Hassan H., Clausen H., and Irimura T. O-GalNAc incorporation into a cluster acceptor site of three consecutive threonines. Distinct specificity of GalNAc-transferase isoforms. Eur. J. Biochem. 269 (2002) 6173-6183
23. Iida S., Takeuchi H., Kato K., Yamamoto K., and Irimura T. Order and maximum incorporation of N-acetyl-d-galactosamine into threonine residues of MUC2 core peptide with microsome fraction of human-colon-carcinoma LS174T cells. Biochem. J. 347 Pt. 2 (2000) 535-542
24. Kato K., Takeuchi H., Kanoh A., Mandel U., Hassan H., Clausen H., and Irimura T. N-acetylgalactosamine incorporation into a peptide containing consecutive threonine residues by UDP-N-acetylgalactosaminide:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 11 (2001) 821-829
25. Gerken T.A., Zhang J., Levine J., and Elhammer A. Mucin core O-glycosylation is modulated by neighboring residue glycosylation status. Kinetic modeling of the site-specific glycosylation of the apo-porcine submaxillary mucin tandem repeat by UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases T1 and T2. J. Biol. Chem. 277 (2002) 49850-49862
26. Gerken T., Tep C., and Rarick J. Role of peptide sequence and neighboring residue glycosylation on the substrate specificity of the uridine 5′-diphosphate-alpha-N-acetylgalactosamine:polypeptide N-acetylgalactosaminyl transferases T1 and T2: kinetic modeling of the porcine and canine submaxillary gland mucin tandem repeats. Biochemistry 43 (2004) 9888-9900
27. Gerken T.A., Owens C.L., and Pasumarthy M. Site-specific core 1 O-glycosylation pattern of the porcine submaxillary gland mucin tandem repeat. Evidence for the modulation of glycan length by peptide sequence. J. Biol. Chem. 273 (1998) 26580-26588
28. Yeh J.C., Ong E., and Fukuda M. Molecular cloning and expression of a novel beta-1, 6-N-acetylglucosaminyltransferase that forms core 2, core 4, and I branches. J. Biol. Chem. 274 (1999) 3215-3221
29. Schwientek T T., Yeh J.C., Levery S.B., Keck B., Merkx G., van Kessel A.G., Fukuda M., and Clausen H. Control of O-glycan branch formation. Molecular cloning and characterization of a novel thymus-associated core 2 beta1, 6-n-acetylglucosaminyltransferase. J. Biol. Chem. 275 (2000) 11106-11113
30. Brockhausen I., Benn M., Bhat S., Marone S., Riley J.G., Montoya-Peleaz P., Vlahakis J.Z., Paulsen H., Schutzbach J.S., and Szarek W. UDP-Gal: GlcNAc-R β1,4-Galactosyltransferase - a target enzyme for drug design. Acceptor specificity and inhibition of the enzyme. Glycoconj. J. 23 (2006) 523-539
31. Molock K.E., and Lillehoj E.P. Biochemical interactions among intercellular adhesion molecules expressed by airway epithelial cells. Biochem. Biophys. Res. Commun. 343 (2006) 513-519
32. Joyce Yip, MSc thesis, Biochemistry Department, Queen's University (2004), Kingston, Ontario, Canada.
33. Beum P.V., Bastola D.R., and Cheng P.W. Mucin biosynthesis: epidermal growth factor downregulates core 2 enzymes in a human airway adenocarcinoma cell line. Am. J. Respir. Cell Mol. Biol. 29 (2003) 48-56
34. Beum P.V., Basma H., Bastola D.R., and Cheng P.W. Mucin biosynthesis: upregulation of core 2 beta 1,6 N-acetylglucosaminyltransferase by retinoic acid and Th2 cytokines in a human airway epithelial cell line. Am. J. Physiol., Lung Cell Mol. Physiol. 288 (2005) L116-L124
35. Falkenberg V.R., and Fregien N. Control of core 2 beta1,6 N-acetylglucosaminyltransferase-I transcription by Sp1 in lymphocytes and epithelial cells. Glycoconj. J. 24 (2007) 511-519
36. Mathieux N., Paulsen H., Meldal M., and Bock K. Synthesis of glycopeptide sequences of repeating units of the mucins MUC 2 and MUC 3 containing oligosaccharide side-chains with core 1, core 2, core 3, core 4 and core 6 structure. J. Chem. Soc., Perkin Trans. 1 (1997) 2359-2368
37. Homa F.L., Baker C.A., Thomsen D.R., and Elhammer A.P. Conversion of a bovine UDP-GalNAc:polypeptide, N-acetylgalactosaminyltransferase to a soluble, secreted enzyme, and expression in Sf9 cells. Protein Expr. Purif. 6 (1995) 141-148
38. Toki D., Sarkar M., Yip B., Reck F., Joziasse D., Fukuda M., Schachter H., and Brockhausen I. Expression of stable human O-glycan core 2 β1,6-N-acetylglucosaminyltransferase in Sf9 insect cells. Biochem. J. 325 (1997) 63-69
39. Brockhausen I., Lehotay M., Yang J., Qin W., Young D.S., Lucien J., Coles J., and Paulsen H. Glycoprotein biosynthesis in porcine aortic endothelial cells and changes in the apoptotic cell population. Glycobiology 12 (2002) 33-45
40. Yang X., Qin W., Lehotay M., Toki D., Dennis P., Schutzbach J.S., and Brockhausen I. Soluble human core 2 β6-N-acetylglucosaminyltransferase C2GnT1 requires its conserved cysteine residues for full activity. Biochim. Biophys. Acta 1648 (2003) 62-74
41. Brockhausen I., Carran J., McEleney K., Lehotay M., Yang X., Yin L., and Anastassiades T. N-acyl derivatives of glucosamine as acceptor substrates for galactosyltransferase from bone and cartilage cells. Carbohydr. Res. 340 (2005) 1997-2003
42. Hennebicq S., Tetaert D., Soudan B., Boersma A., Briand G., Richet C., Gagnon J., and Degand P. Influence of the amino acid sequence on the MUC5AC motif peptide O-glycosylation by human gastric UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase(s). Glycoconj. J. 15 (1998) 275-282
43. Nishimori I., Johnson N.R., Sanderson S.D., Perini F., Mountjoy K., Cerny R.L., Gross M.L., and Hollingsworth M.A. Influence of acceptor substrate primary amino acid sequence on the activity of human UDP-N-acetylgalactosamine:polypeptide N-acetylgalactosaminyltransferase. Studies with the MUC1 tandem repeat. J. Biol. Chem. 269 (1994) 16123-16130
44. Yoshida A., Suzuki M., Ikenaga H., and Takeuchi M. Discovery of the shortest sequence motif for high level mucin-type O-glycosylation. J. Biol. Chem. 272 (1997) 16884-16888
45. Tenno M., Saeki A., Kezdy F., Elhammer A., and Kurobaka A. The lectin domain of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase 1 is involved in O-glycosylation of a polypeptide with multiple acceptor sites. J. Biol. Chem. 277 (2002) 47088-47096
46. 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. Principles of mucin architecture: structural studies on synthetic glycopeptides bearing clustered mono-, di-, tri-, and hexasaccharide glycodomains. J. Am. Chem. Soc. 124 (2002) 9833-9844
47. Kinarsky L., Suryanarayanan G., Prakash O., Paulsen H., Clausen H., Hanisch F.G., Hollingsworth M.A., and Sherman S. Conformational studies on the MUC1 tandem repeat glycopeptides: implication for the enzymatic O-glycosylation of the mucin protein core. Glycobiology 13 (2003) 929-939
48. Pollex-Krüger A., Meyer B., Stuike-Prill R., Sinnwell V., Matta K.L., and Brockhausen I. Preferred conformations and dynamics of five core structures of mucin-type O-glycans determined by NMR spectroscopy and force field calculations. Glycoconj. J. 10 (1993) 365-380
49. Otvos Jr. L., and Cudic M. Conformation of glycopeptides. Mini Rev. Med. Chem. 3 (2003) 703-711
50. Naganagowda G.A., Gururaja T.L., Satyanarayana J., and Levine M.J. NMR analysis of human salivary mucin (MUC7) derived O-linked model glycopeptides: comparison of structural features and carbohydrate-peptide interactions. J. Pept. Res. 54 (1999) 290-310
51. Pratt M.R., Hang H.C., Ten Hagen K.G., Rarick J., Gerken T.A., Tabak L.A., and Bertozzi C.R. Deconvoluting the functions of polypeptide N-alpha-acetylgalactosaminyltransferase family members by glycopeptide substrate profiling. Chem. Biol. 11 (2004) 1009-1016
52. Wandall H.H., Irazoqui F., Tarp M.A., Bennett E.P., Mandel U., Takeuchi H., Kato K., Irimura T., Suryanarayanan G., Hollingsworth M.A., and Clausen H. The lectin domains of polypeptide GalNAc-transferases exhibit carbohydrate-binding specificity for GalNAc: lectin binding to GalNAc-glycopeptide substrates is required for high density GalNAc-O-glycosylation. Glycobiology 17 (2007) 374-387
53. Perrine C., Ju T., Cummings R.D., and Gerken T.A. Systematic determination of the peptide acceptor preferences for the human UDP-Gal: glycoprotein-{alpha}-GalNAc {beta}3 galactosyltranferase (T-synthase). Glycobiology 19 (2009) 321-328
54. Ju T., Aryal R.P., Stowell C.J., and Cummings R.D. Regulation of protein O-glycosylation by the endoplasmic reticulum-localized molecular chaperone Cosmc. J. Cell Biol. 182 (2008) 531-542
55. Pak J.E., Arnoux P., Zhou S., Sivarajah P., Satkunarajah M., Xing X., and Rini J.M. X-ray crystal structure of leukocyte type core 2 beta1,6-N-acetylglucosaminyltransferase. Evidence for a convergence of metal ion-independent glycosyltransferase mechanism. J. Biol. Chem. 281 (2006) 26693-26701
56. Li C.M., Adler K.B., and Cheng P.W. Mucin biosynthesis: molecular cloning and expression of bovine lung mucin core 2 N-acetylglucosaminyltransferase cDNA. Am. J. Respir. Cell Mol. Biol. 18 (1998) 343-352
57. Ramakrishnan B., Balaji P.V., and Qasba P.K. Crystal structure of beta1,4-galactosyltransferase complex with UDP-Gal reveals an oligosaccharide acceptor binding site. J. Mol. Biol. 318 (2002) 491-502
58. Ujita M., McAuliffe J., Schwientek T., Almeida R., Hindsgaul O., Clausen H., and Fukuda M. Synthesis of poly-N-acetyllactosamine in core 2 branched O-glycans. The requirement of novel beta-1,4-galactosyltransferase IV and beta-1,3-N-acetylglucosaminyltransferase. J. Biol. Chem. 273 (1998) 34843-34849
59. Röttger S., White J., Wandall H.H., Olivo J.C., Stark A., Bennett E.P., Whitehouse C., Berger E.G., Clausen H., and Nilsson T. Localization of three human polypeptide GalNAc-transferases in HeLa cells suggests initiation of O-linked glycosylation throughout the Golgi apparatus. J. Cell. Sci. 111 (1998) 45-60
60. Piller V., Piller F., and Fukuda M. Biosynthesis of truncated O-glycans in the T cell line Jurkat. Localization of O-glycan initiation. J. Biol. Chem. 265 (1990) 9264-9271
61. Skrincosky D., Kain R., El-Battari A., Exner M., Kerjaschki D., and Fukuda M. Altered Golgi localization of core 2 beta-1,6-N-acetylglucosaminyltransferase leads to decreased synthesis of branched O-glycans. J. Biol. Chem. 272 (1997) 22695-22702
62. Roth J., and Berger E.G. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae. J. Cell Biol. 93 (1982) 223-229