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. 1988 Jun 1;252(2):453–461. doi: 10.1042/bj2520453

Structure and distribution of N-linked oligosaccharide chains on various domains of mouse tumour laminin.

S Fujiwara 1, H Shinkai 1, R Deutzmann 1, M Paulsson 1, R Timpl 1
PMCID: PMC1149166  PMID: 2458101

Abstract

Asparagine-linked oligosaccharides were liberated from laminin and some of its fragments by hydrazinolysis, and after purification characterized by exoglycosidase digestions. This demonstrated the presence of nine forms of complex oligosaccharide chains, which differed in antennary and oligolactosamine structure, and of small amounts of high-mannose-type oligosaccharides. Additional variations were found with regard to substitutions by terminal alpha-galactose and sialic acid residues. Each of the various laminin fragments showed a unique but less complex repertoire of carbohydrate structures. These fragments also differed in mass, carbohydrate content, localization within the laminin molecule and functional activities such as cell-binding (fragments 1 and 6) and heparin- and collagen-binding (fragments 3 and 4). Fragment 7 with a particularly high carbohydrate content (72%) also showed the highest complexity of tri- and tetra-antennary structures. Further differences between the fragments were detected with human antibodies against the Gal alpha 1-3Gal epitope, which was expressed in either a high-affinity or a low-affinity form. Such differences in carbohydrate structure of topologically distinct laminin domains may have implications for their functions and in the regulation of post-translational modification events.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arakawa M., Ogata S., Muramatsu T., Kobata A. Beta-galactosidases from jack bean meal and almond emulsin. Application for the enzymatic distinction of Galbeta1 leads to 4GlcNAc and Galbeta1 leads to 3GlcNAc linkages. J Biochem. 1974 Apr;75(4):707–714. doi: 10.1093/oxfordjournals.jbchem.a130443. [DOI] [PubMed] [Google Scholar]
  2. Arumugham R. G., Hsieh T. C., Tanzer M. L., Laine R. A. Structures of the asparagine-linked sugar chains of laminin. Biochim Biophys Acta. 1986 Aug 6;883(1):112–126. doi: 10.1016/0304-4165(86)90142-x. [DOI] [PubMed] [Google Scholar]
  3. Aumailley M., Nurcombe V., Edgar D., Paulsson M., Timpl R. The cellular interactions of laminin fragments. Cell adhesion correlates with two fragment-specific high affinity binding sites. J Biol Chem. 1987 Aug 25;262(24):11532–11538. [PubMed] [Google Scholar]
  4. Charonis A. S., Tsilibary E. C., Saku T., Furthmayr H. Inhibition of laminin self-assembly and interaction with type IV collagen by antibodies to the terminal domain of the long arm. J Cell Biol. 1986 Nov;103(5):1689–1697. doi: 10.1083/jcb.103.5.1689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Charonis A. S., Tsilibary E. C., Yurchenco P. D., Furthmayr H. Binding of laminin to type IV collagen: a morphological study. J Cell Biol. 1985 Jun;100(6):1848–1853. doi: 10.1083/jcb.100.6.1848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chu M. L., Mann K., Deutzmann R., Pribula-Conway D., Hsu-Chen C. C., Bernard M. P., Timpl R. Characterization of three constituent chains of collagen type VI by peptide sequences and cDNA clones. Eur J Biochem. 1987 Oct 15;168(2):309–317. doi: 10.1111/j.1432-1033.1987.tb13422.x. [DOI] [PubMed] [Google Scholar]
  7. Chung A. E., Jaffe R., Freeman I. L., Vergnes J. P., Braginski J. E., Carlin B. Properties of a basement membrane-related glycoprotein synthesized in culture by a mouse embryonal carcinoma-derived cell line. Cell. 1979 Feb;16(2):277–287. doi: 10.1016/0092-8674(79)90005-9. [DOI] [PubMed] [Google Scholar]
  8. Cooper A. R., Kurkinen M., Taylor A., Hogan B. L. Studies on the biosynthesis of laminin by murine parietal endoderm cells. Eur J Biochem. 1981 Sep;119(1):189–197. doi: 10.1111/j.1432-1033.1981.tb05593.x. [DOI] [PubMed] [Google Scholar]
  9. Dennis J. W., Waller C. A., Schirrmacher V. Identification of asparagine-linked oligosaccharides involved in tumor cell adhesion to laminin and type IV collagen. J Cell Biol. 1984 Oct;99(4 Pt 1):1416–1423. doi: 10.1083/jcb.99.4.1416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Engel J., Odermatt E., Engel A., Madri J. A., Furthmayr H., Rohde H., Timpl R. Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J Mol Biol. 1981 Jul 25;150(1):97–120. doi: 10.1016/0022-2836(81)90326-0. [DOI] [PubMed] [Google Scholar]
  11. Engvall E., Krusius T., Wewer U., Ruoslahti E. Laminin from rat yolk sac tumor: isolation, partial characterization, and comparison with mouse laminin. Arch Biochem Biophys. 1983 Apr 15;222(2):649–656. doi: 10.1016/0003-9861(83)90562-3. [DOI] [PubMed] [Google Scholar]
  12. Fujiwara S., Wiedemann H., Timpl R., Lustig A., Engel J. Structure and interactions of heparan sulfate proteoglycans from a mouse tumor basement membrane. Eur J Biochem. 1984 Aug 15;143(1):145–157. doi: 10.1111/j.1432-1033.1984.tb08353.x. [DOI] [PubMed] [Google Scholar]
  13. Galili U., Basbaum C. B., Shohet S. B., Buehler J., Macher B. A. Identification of erythrocyte Gal alpha 1-3Gal glycosphingolipids with a mouse monoclonal antibody, Gal-13. J Biol Chem. 1987 Apr 5;262(10):4683–4688. [PubMed] [Google Scholar]
  14. Goodman S. L., Deutzmann R., von der Mark K. Two distinct cell-binding domains in laminin can independently promote nonneuronal cell adhesion and spreading. J Cell Biol. 1987 Jul;105(1):589–598. doi: 10.1083/jcb.105.1.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Graf J., Iwamoto Y., Sasaki M., Martin G. R., Kleinman H. K., Robey F. A., Yamada Y. Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell. 1987 Mar 27;48(6):989–996. doi: 10.1016/0092-8674(87)90707-0. [DOI] [PubMed] [Google Scholar]
  16. HUGHES R. C., JEANLOZ R. W. THE EXTRACELLULAR GLYCOSIDASES OF DIPLOCOCCUS PNEUMONIAE. I. PURIFICATION AND PROPERTIES OF A NEURAMINIDASE AND A BETA-GALACTOSIDASE. ACTION ON THE ALPHA-1-ACID GLYCOPROTEIN OF HUMAN PLASMA. Biochemistry. 1964 Oct;3:1535–1543. doi: 10.1021/bi00898a025. [DOI] [PubMed] [Google Scholar]
  17. Howe C. C. Functional role of laminin carbohydrate. Mol Cell Biol. 1984 Jan;4(1):1–7. doi: 10.1128/mcb.4.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Martin G. R., Timpl R. Laminin and other basement membrane components. Annu Rev Cell Biol. 1987;3:57–85. doi: 10.1146/annurev.cb.03.110187.000421. [DOI] [PubMed] [Google Scholar]
  19. Mizuochi T., Taniguchi T., Fujii-Kadowaki J., Yonemasu K., Sasaki T., Kobata A. Structures of the asparagine-linked sugar chains of subcomponent C1q of the first component of bovine complement. J Biol Chem. 1982 Nov 25;257(22):13300–13305. [PubMed] [Google Scholar]
  20. Mizuochi T., Yonemasu K., Yamashita K., Kobata A. The asparagine-linked sugar chains of subcomponent C1q of the first component of human complement. J Biol Chem. 1978 Oct 25;253(20):7404–7409. [PubMed] [Google Scholar]
  21. Muramatsu H., Ishihara H., Miyauchi T., Gachelin G., Fujisaki T., Tejima S., Muramatsu T. Glycoprotein-bound large carbohydrates of early embryonic cells: structural characteristic of the glycan isolated from F9 embryonal carcinoma cells. J Biochem. 1983 Sep;94(3):799–810. doi: 10.1093/oxfordjournals.jbchem.a134422. [DOI] [PubMed] [Google Scholar]
  22. Muramatsu H., Muramatsu T., Avner P. Biochemical properties of the high-molecular-weight glycopeptides released from the cell surface of human teratocarcinoma cells. Cancer Res. 1982 May;42(5):1749–1752. [PubMed] [Google Scholar]
  23. Nishigaki M., Yamashita K., Matsuda I., Arashima S., Kobata A. Urinary oligosaccharides of fucosidosis. Evidence of the occurrence of X-antigenic determinant in serum-type sugar chains of glycoproteins. J Biochem. 1978 Oct;84(4):823–834. doi: 10.1093/oxfordjournals.jbchem.a132194. [DOI] [PubMed] [Google Scholar]
  24. Ott U., Odermatt E., Engel J., Furthmayr H., Timpl R. Protease resistance and conformation of laminin. Eur J Biochem. 1982 Mar;123(1):63–72. doi: 10.1111/j.1432-1033.1982.tb06499.x. [DOI] [PubMed] [Google Scholar]
  25. Paulson J. C., Prieels J. P., Glasgow L. R., Hill R. L. Sialyl- and fucosyltransferases in the biosynthesis of asparaginyl-linked oligosaccharides in glycoproteins. Mutually exclusive glycosylation by beta-galactoside alpha2 goes to 6 sialyltransferase and N-acetylglucosaminide alpha1 goes to 3 fucosyltransferase. J Biol Chem. 1978 Aug 25;253(16):5617–5624. [PubMed] [Google Scholar]
  26. Paulsson M., Deutzmann R., Dziadek M., Nowack H., Timpl R., Weber S., Engel J. Purification and structural characterization of intact and fragmented nidogen obtained from a tumor basement membrane. Eur J Biochem. 1986 May 2;156(3):467–478. doi: 10.1111/j.1432-1033.1986.tb09605.x. [DOI] [PubMed] [Google Scholar]
  27. Paulsson M., Deutzmann R., Timpl R., Dalzoppo D., Odermatt E., Engel J. Evidence for coiled-coil alpha-helical regions in the long arm of laminin. EMBO J. 1985 Feb;4(2):309–316. doi: 10.1002/j.1460-2075.1985.tb03630.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rao C. N., Goldstein I. J., Liotta L. A. Lectin-binding domains on laminin. Arch Biochem Biophys. 1983 Nov;227(1):118–124. doi: 10.1016/0003-9861(83)90354-5. [DOI] [PubMed] [Google Scholar]
  29. Rao C. N., Margulies I. M., Tralka T. S., Terranova V. P., Madri J. A., Liotta L. A. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed] [Google Scholar]
  30. Rohde H., Bächinger H. P., Timpl R. Characterization of pepsin fragments of laminin in a tumor basement membrane. Evidence for the existence of related proteins. Hoppe Seylers Z Physiol Chem. 1980 Nov;361(11):1651–1660. doi: 10.1515/bchm2.1980.361.2.1651. [DOI] [PubMed] [Google Scholar]
  31. Sasaki M., Kato S., Kohno K., Martin G. R., Yamada Y. Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc Natl Acad Sci U S A. 1987 Feb;84(4):935–939. doi: 10.1073/pnas.84.4.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sasaki M., Yamada Y. The laminin B2 chain has a multidomain structure homologous to the B1 chain. J Biol Chem. 1987 Dec 15;262(35):17111–17117. [PubMed] [Google Scholar]
  33. Shinkai H., Lapiere C. M. Characterization of oligosaccharide units of p-N-collagen type III from dermatosparactic bovine skin. Biochim Biophys Acta. 1983 Jul 5;758(1):30–36. doi: 10.1016/0304-4165(83)90006-5. [DOI] [PubMed] [Google Scholar]
  34. Shinkai H., Nakamura T., Matsunaga E. Evidence for the presence and structure of asparagine-linked oligosaccharide units in the core protein of proteodermatan sulphate. Biochem J. 1983 Aug 1;213(2):297–304. doi: 10.1042/bj2130297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Timpl R., Dziadek M. Structure, development, and molecular pathology of basement membranes. Int Rev Exp Pathol. 1986;29:1–112. [PubMed] [Google Scholar]
  36. Timpl R., Johansson S., van Delden V., Oberbäumer I., Hök M. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes. J Biol Chem. 1983 Jul 25;258(14):8922–8927. [PubMed] [Google Scholar]
  37. Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
  38. Towbin H., Rosenfelder G., Wieslander J., Avila J. L., Rojas M., Szarfman A., Esser K., Nowack H., Timpl R. Circulating antibodies to mouse laminin in Chagas disease, American cutaneous leishmaniasis, and normal individuals recognize terminal galactosyl(alpha 1-3)-galactose epitopes. J Exp Med. 1987 Aug 1;166(2):419–432. doi: 10.1084/jem.166.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yoshima H., Matsumoto A., Mizuochi T., Kawasaki T., Kobata A. Comparative study of the carbohydrate moieties of rat and human plasma alpha 1-acid glycoproteins. J Biol Chem. 1981 Aug 25;256(16):8476–8484. [PubMed] [Google Scholar]

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