Core glycosylation of collagen is initiated by two β(1-O) galactosyltransferases

Molecular and Cellular Biology

Volumn 29, Issue 4, 2009, Pages 943-952

  Schegg, Belinda ^a   Hülsmeier, Andreas J ^a   Rutschmann, Christoph ^a   Maag, Charlotte ^a   Hennet, Thierry ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; COLLAGEN; GALACTOSE; GALACTOSYLTRANSFERASE; GLT25D1 ENZYME; GLT25D2 ENZYME; HYDROXYLYSINE; MANNOSE BINDING LECTIN; PROCOLLAGEN GLUCOSYLTRANSFERASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACULOVIRUS; CHICKEN; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INSECT CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; CATTLE; CHICK EMBRYO; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLLAGEN; GALACTOSYLTRANSFERASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE SILENCING; GLYCOSYLATION; HELA CELLS; HUMANS; KINETICS; MANNOSE-BINDING LECTIN; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; TIME FACTORS;

EID: 59449103217     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02085-07     Document Type: Article

References (48)

1. Anttinen, H. 1976. Stimulation of collagen galactosyltransferase and glucosyltransferase activities by lysophosphatidylcholine. Biochem. J. 160: 29-35.
2. Bank, R. A., B. Beekman, R. Tenni, and J. M. TeKoppele. 1997. Pre-column derivatisation method for the measurement of glycosylated hydroxylysines of collagenous proteins. J. Chromatogr. B Biomed. Sci. Appl. 703:267-272.
3. Bennett, E. P., H. Hassan, U. Mandel, E. Mirgorodskaya, P. Roepstorff, J. Burchell, J. Taylor-Papadimitriou, M. A. Hollingsworth, G. Merkx, A. G. van Kessel, H. Eiberg, R. Steffensen, and H. Clausen. 1998. Cloning of a human UDP-N-acetyl-alpha-D-galactosamine:polypeptide N-acetylgalac- tosaminyltransferase that complements other GalNAc-transferases in complete O-glycosylation of the MUC1 tandem repeat. J. Biol. Chem. 273: 30472-30481.
4. Bon, S., A. Ayon, J. Leroy, and J. Massoulie. 2003. Trimerization domain of the collagen tail of acetylcholinesterase. Neurochem. Res. 28:523-535.
5. Cabral, W. A., W. Chang, A. M. Barnes, M. Weis, M. A. Scott, S. Leikin, E. Makareeva, N. V. Kuznetsova, K. N. Rosenbaum, C. J. Tifft, D. I. Bulas, C. Kozma, P. A. Smith, D. R. Eyre, and J. C. Marini. 2007. Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat. Genet. 39:359-365.
6. Colley, K. J., and J. U. Baenziger. 1987. Post-translational modifications of the core-specific lectin. Relationship to assembly, ligand binding, and secretion. J. Biol. Chem. 262:10296-10303.
7. Edge, A. S., C. R. Faltynek, L. Hof, L. E. Reichert, Jr., and P. Weber. 1981. Deglycosylation of glycoproteins by trifluoromethanesulfonic acid. Anal. Biochem. 118:131-137.
8. Gay, S., J. D. Fine, and J. S. Storer. 1988. Autoantibodies to extracellular collagen matrix components in epidermolysis bullosa and other bullous diseases. Arch. Dermatol. Res. 280:333-337.
9. Grassmann, W., and H. Schleich. 1935. Uber den Kohlenhydratgehalt des Kollagens II. Biochem. Z 277:320-328.
10. Haeuptle, M. A., F. M. Pujol, C. Neupert, B. Winchester, A. J. Kastaniotis, M. Aebi, and T. Hennet. 2008. Human RFT1 deficiency leads to a disorder of N-linked glycosylation. Am. J. Hum. Genet. 82:600-606.
11. Hakansson, K., and K. B. Reid. 2000. Collectin structure: a review. Protein Sci. 9:1607-1617.
12. Heikkinen, J., M. Risteli, C. Wang, J. Latvala, M. Rossi, M. Valtavaara, and R. Myllyla. 2000. Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J. Biol. Chem. 275:36158-36163.
13. Hennet, T., A. Dinter, P. Kuhnert, T. S. Mattu, P. M. Rudd, and E. G. Berger. 1998. Genomic cloning and expression of three murine UDP-galac- tose: β-N-acetylglucosamine β1,3-galactosyltransferase genes. J. Biol. Chem. 273:58-65.
14. Ihme, A., L. Risteli, T. Krieg, J. Risteli, U. Feldmann, K. Kruse, and P. K. Muller. 1983. Biochemical characterization of variants of the Ehlers-Danlos syndrome type VI. Eur. J. Clin. Investig. 13:357-362.
15. Kamath, R. S., A. G. Fraser, Y. Dong, G. Poulin, R. Durbin, M. Gotta, A. Kanapin, N. Le Bot, S. Moreno, M. Sohrmann, D. P. Welchman, P. Zipperlen, and J. Ahringer. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231-237.
16. Kivirikko, K. I., and R. Myllyla. 1979. Collagen glycosyltransferases. Int. Rev. Connect. Tissue Res. 8:23-72.
17. Kukkola, L., R. Hieta, K. I. Kivirikko, and J. Myllyharju. 2003. Identification and characterization of a third human, rat, and mouse collagen prolyl 4-hydroxylase isoenzyme. J. Biol. Chem. 278:47685-47693.
18. Lane, E. B., and W. H. McLean. 2004. Keratins and skin disorders. J. Pathol. 204:355-366.
19. Lee, Y. A., F. Ruschendorf, C. Windemuth, M. Schmitt-Egenolf, A. Stadelmann, G. Nurnberg, M. Stander, T. F. Wienker, A. Reis, and H. Traupe. 2000. Genomewide scan in German families reveals evidence for a novel psoriasis-susceptibility locus on chromosome 19p13. Am. J. Hum. Genet. 67:1020-1024.
20. Mizuno, K., T. Hayashi, and H. P. Bachinger. 2003. Hydroxylation-induced stabilization of the collagen triple helix. Further characterization of peptides with 4(R)-hydroxyproline in the Xaa position. J. Biol. Chem. 278:32373-32379.
21. Myllyharju, J., and K. I. Kivirikko. 2004. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20:33-43.
22. Myllyla, R., H. Anttinen, L. Risteli, and K. I. Kivirikko. 1977. Isolation of collagen glucosyltransferase as a homogeneous protein from chick embryos. Biochim. Biophys. Acta 480:113-121.
23. Myllyla, R., L. Risteli, and K. I. Kivirikko. 1975. Assay of collagen-galactosyltransferase and collagen-glucosyltransferase activities and preliminary characterization of enzymic reactions with transferases from chick-embryo cartilage. Eur. J. Biochem. 52:401-410.
24. Myllyla, R., L. Risteli, and K. I. Kivirikko. 1976. Collagen glucosyltrans-ferase. Partial purification and characterization of the enzyme from whole chick embryos and chick-embryo cartilage. Eur. J. Biochem. 61:59-67.
25. Norman, K. R., and D. G. Moerman. 2000. The let-268 locus of Caenorhabditis elegans encodes a procollagen lysyl hydroxylase that is essential for type IV collagen secretion. Dev. Biol. 227:690-705.
26. Qasba, P. K., B. Ramakrishnan, and E. Boeggeman. 2005. Substrate-induced conformational changes in glycosyltransferases. Trends Biochem. Sci. 30: 53-62.
27. Rautavuoma, K., K. Takaluoma, K. Passoja, A. Pirskanen, A. P. Kvist, K. I. Kivirikko, and J. Myllyharju. 2002. Characterization of three fragments that constitute the monomers of the human lysyl hydroxylase isoenzymes 1-3. The 30-kDa N-terminal fragment is not required for lysyl hydroxylase activity. J. Biol. Chem. 277:23084-23091.
28. Reiser, K., R. J. McCormick, and R. B. Rucker. 1992. Enzymatic and non-enzymatic cross-linking of collagen and elastin. FASEB J. 6:2439-2449.
29. Richards, A. A., T. Stephens, H. K. Charlton, A. Jones, G. A. Macdonald, J. B. Prins, and J. P. Whitehead. 2006. Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol. Endocrinol. 20:1673-1687.
30. Risteli, L. 1978. Further characterization of collagen galactosyltransferase from chick embryos. Biochem. J. 169:189-196.
31. Risteli, L., R. Myllya, and K. I. Kivirikko. 1976. Partial purification and characterization of collagen galactosyltransferase from chick embryos. Biochem. J. 155:145-153.
32. Risteli, L., R. Myllyla, and K. I. Kivirikko. 1976. Affinity chromatography of collagen glycosyltransferases on collagen linked to agarose. Eur. J. Biochem. 67:197-202.
33. Risteli, M., O. Niemitalo, H. Lankinen, A. H. Juffer, and R. Myllyla. 2004. Characterization of collagenous peptides bound to lysyl hydroxylase iso-forms. J. Biol. Chem. 279:37535-37543.
34. Shevchenko, A., H. Tomas, J. Havlis, J. V. Olsen, and M. Mann. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1:2856-2860.
35. Shinkai, H., and K. Yonemasu. 1979. Hydroxylysine-linked glycosides of human complement subcomponent C1q and various collagens. Biochem. J. 177:847-852.
36. Simmer, F., C. Moorman, A. M. van der Linden, E. Kuijk, P. V. van den Berghe, R. S. Kamath, A. G. Fraser, J. Ahringer, and R. H. Plasterk. 2003. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1:77-84.
37. Soderhall, C., I. Marenholz, T. Kerscher, F. Ruschendorf, J. Esparza-Gordillo, M. Worm, C. Gruber, G. Mayr, M. Albrecht, K. Rohde, H. Schulz, U. Wahn, N. Hubner, and Y. A. Lee. 2007. Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis. PLoS Biol. 5:1952-1961.
38. Sojar, H. T., and O. P. Bahl. 1987. Chemical deglycosylation of glycoproteins. Methods Enzymol. 138:341-350.
39. Spiro, R. G. 1969. Characterization and quantitative determination of the hydroxylysine-linked carbohydrate units of several collagens. J. Biol. Chem. 244:602-612.
40. Spiro, R. G. 1967. The structure of the disaccharide unit of the renal glomerular basement membrane. J. Biol. Chem. 242:4813-4823.
41. Starzyk, R. M., C. Rosenow, J. Frye, M. Leismann, E. Rodzinski, S. Putney, and E. I. Tuomanen. 2000. Cerebral cell adhesion molecule: a novel leukocyte adhesion determinant on blood-brain barrier capillary endothelium. J. Infect. Dis. 181:181-187.
42. Tenni, R., D. Rimoldi, G. Zanaboni, G. Cetta, and A. A. Castellani. 1984. Hydroxylysine glycosides: preparation and analysis by reverse phase high performance liquid chromatography. Ital. J. Biochem. 33:117-127.
43. Valtavaara, M., C. Szpirer, J. Szpirer, and R. Myllyla. 1998. Primary structure, tissue distribution, and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J. Biol. Chem. 273:12881-12886.
44. van der Slot, A. J., A. M. Zuurmond, A. F. Bardoel, C. Wijmenga, H. E. Pruijs, D. O. Sillence, J. Brinckmann, D. J. Abraham, C. M. Black, N. Verzijl, J. DeGroot, R. Hanemaaijer, J. M. TeKoppele, T. W. Huizinga, and R. A. Bank. 2003. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J. Biol. Chem. 278:40967-40972.
45. Veit, G., B. Kobbe, D. R. Keene, M. Paulsson, M. Koch, and R. Wagener. 2006. Collagen XXVIII, a novel von Willebrand factor A domain-containing protein with many imperfections in the collagenous domain. J. Biol. Chem. 281:3494-3504.
46. Vranka, J. A., L. Y. Sakai, and H. P. Bachinger. 2004. Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J. Biol. Chem. 279:23615-23621.
47. Wang, C., H. Luosujarvi, J. Heikkinen, M. Risteli, L. Uitto, and R. Myllyla. 2002. The third activity for lysyl hydroxylase 3: galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol. 21:559-566.
48. Zhou, D., M. Malissard, E. G. Berger, and T. Hennet. 2000. Secretion and purification of recombinant β1-4 galactosyltransferase from insect cells using pFmel-protA, a novel transposition-based baculovirus transfer vector. Arch. Biochem. Biophys. 374:3-7.