Skip to main content
NCBI home page
Japanese Journal of Cancer Research : Gann logoLink to Japanese Journal of Cancer Research : Gann
. 1990 Apr;81(4):363–371. doi: 10.1111/j.1349-7006.1990.tb02576.x

Comparative Study of the N‐Linked Oligosaccharides Released from Normal Human Esophageal Epithelium and Esophageal Squamous Carcinoma

Sen Hiraizuni 1,2, Seiichi Takasaki 1, Tetsuro Nishihira 2, Shouzo Mori 2, Akira Kobata 1,✉
PMCID: PMC5918051  PMID: 2114390

Abstract

N‐Linked sugar chains of normal human esophageal epithelium and esophageal squamous carcinoma were quantitatively released as oligosaccharides from their membrane preparations by hydrazinolysis. After being fractionated by serial lectin column chromatography using concanavalin A‐Sepharose and Datura stramonium agglutinin‐Sepharose, their structures were elucidated by exoglycosidase digestion in combination with methylation analysis. Both normal epithelium and esophageal carcinoma contained bi‐, tri‐ and tetraantennary oligosaccharides as well as high mannose‐type oligosaccharides. Interestingly, carcinoma had about 1.6 times larger amounts of tri‐ and tetraantennary oligosaccharides with the GlcNAcβ1→4Manα1→ and/or the GlcNAcβ1→6Manα1→ linkages than normal epithelium. Tri‐ and tetraantennary oligosaccharides with N‐acetyllactosamine repeating units (the Galβ1→4GlcNAcβ1→3Galβ1→4GlcNAc group) were also increased in carcinoma. These data indicated that the altered glycosylation of proteins previously found in transformed rodent cells also occurs widely in human esophageal carcinoma.

Keywords: Sugar chain, Esophageal squamous carcinoma, Normal esophageal epithelium, Datura stramonium agglutinin, Membrane glycoprotein

Full Text

The Full Text of this article is available as a PDF (594.3 KB).

REFERENCES

  • 1. ) Warren , L. , Buck , C. A. and Tuszynski , G. P.Glycopeptide changes and malignant transformation, a possible role for carbohydrate in malignant behavior . Biochim. Biophys. Acta , 516 , 97 – 127 ( 1978. ). [DOI] [PubMed] [Google Scholar]
  • 2. ) Yamashita , K. , Ohkura , T. , Tachibana , Y. , Takasaki , S. and Kobata , A.Comparative study of the oligosaccharides released from baby hamster kidney cells and their polyoma transformant by hydrazinolysis . J. Biol. Chem. , 259 , 10834 – 10840 ( 1984. ). [PubMed] [Google Scholar]
  • 3. ) Pierce , M. and Arango , J.Rous sarcoma virus‐transformed baby hamster kidney cells express higher levels of asparagine‐linked tri‐ and tetraantennary glycopeptides containing [GlcNAc‐β(1,6)Man‐α(1,6)Man] and poly‐N‐acetyllactosamine sequences than baby hamster kidney cells . J. Biol. Chem. , 261 , 10772 – 10777 ( 1986. ). [PubMed] [Google Scholar]
  • 4. ) Humphries , M. J. , Matsumoto , K. , White , S. L. and Olden , K.Oligosaccharide modification by swainsonine treatment inhibits pulmonary colonization by B16‐F10 murine melanoma cells . Proc. Natl. Acad. Sci. USA , 83 , 1752 – 1756 ( 1986. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. ) Dennis , J. W. , Lafertè , S. , Waghone , R. B. , Breitman , M. L. and Kerbel , R.β1–6 Branching of Asn‐linked oligosaccharides is directly associated with metastasis . Science , 236 , 582 – 585 ( 1987. ). [DOI] [PubMed] [Google Scholar]
  • 6. ) Rademacher , T. W. , Parekh , R. B. and Dwek , R. A.Glycobiology . Ann. Rev. Biochem. , 57 , 785 – 838 ( 1988. ). [DOI] [PubMed] [Google Scholar]
  • 7. ) Zhu , B. C. R. and Laine , R. A.Polylactosamine glycosylation on human fetal placental fibronectin weakens the binding affinity of fibronectin to gelatin . J. Biol. Chem. , 260 , 4041 – 4045 ( 1985. ). [PubMed] [Google Scholar]
  • 8. ) Gilbert , C. W. , Zaroukian , M. H. and Esselman , W. J.Poly‐N‐acetyllactosamine structures on murine cell surface T200 glycoprotein participate in natural killer cell binding to YAC‐1 targets . J. Immunol. , 140 , 2821 – 2828 ( 1988. ). [PubMed] [Google Scholar]
  • 9. ) Lafertè , S. and Dennis , J. W.Glycosylation‐dependent collagen‐binding activities of two membrane glycoproteins in MDAY‐D2 tumor cells . Cancer Res. , 78 , 4743 – 4748 ( 1988. ). [PubMed] [Google Scholar]
  • 10. ) Dennis , J. W. and Lafertè , S.Recognition of asparagine‐linked oligosaccharides on murine tumor cells by natural killer cells . Cancer Res. , 45 , 6034 – 6040 ( 1985. ). [PubMed] [Google Scholar]
  • 11. ) Ahrens , P. B. and Ankel , H.The role of asparagine‐linked carbohydrate in natural killer cell‐mediated cytolysis . J. Biol. Chem. , 262 , 7575 – 7579 ( 1987. ). [PubMed] [Google Scholar]
  • 12. ) Yamamoto , K. , Tsuji , T. , Tarutani , O. and Osawa , T.Structural changes of carbohydrate chains of human thyroglobulin accompanying malignanat transformations of thyroid glands . Eur. J. Biochem. , 143 , 133 – 144 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 13. ) Kobata , A.Structures, function, and transformational changes of the sugar chains of glycohormones . J. Cell Biochem. , 37 , 79 – 90 ( 1988. ). [DOI] [PubMed] [Google Scholar]
  • 14. ) Yamashita , K. , Totani , K. , Iwaki , Y. , Takaisawa , I. , Tateishi , N. , Higashi , T. , Sakamoto , Y. and Kobata , A.Comparative study of the sugar chains of γ‐glutamyltrans‐peptidases purified from human hepatocellular carcinoma and from human liver . J. Biochem. , 105 , 728 – 735 ( 1989. ). [DOI] [PubMed] [Google Scholar]
  • 15. ) Yamashita , K. , Koide , N. , Endo , T. , Iwaki , Y. and Kobata , A.Altered glycosylation of serum transferrin of patients with hepatocellular carcinoma . J. Biol. Chem. , 264 , 2415 – 2423 ( 1989. ). [PubMed] [Google Scholar]
  • 16. ) Li , Y‐T. and Li , S‐C.α‐Mannosidase, β‐N‐acetylhexos‐aminidase, and β‐galactosidase from jack bean meal . Methods Enzymol. , 28 , 702 – 713 ( 1972. ). [Google Scholar]
  • 17. ) Glasgow , L. R. , Paulson , J. C. and Hill , R. L.Systematic purification of five glycosidases from Streptococcus (Diplococcus) pneumoniae . J. Biol. Chem. , 252 , 8615 – 8623 ( 1977. ). [PubMed] [Google Scholar]
  • 18. ) Kobata , A. and Amano , J.α‐Mannosidases I and II from Aspergillus saitoi . Methods Enzymol. , 138 , 779 – 785 ( 1987. ). [DOI] [PubMed] [Google Scholar]
  • 19. ) Kitamikado , M. , Ito , M. and Li , Y‐T.Endo‐β‐galactosidase from Flavobacterium keratolyticus . Methods Enzymol. , 38 , 619 – 625 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 20. ) Uchida , Y. , Tsukada , Y. and Sugimori , T.Production of microbial neuraminidases induced by colonimic acid. Biochim. Biophys . Acta , 250 , 425 – 431 ( 1974. ). [DOI] [PubMed] [Google Scholar]
  • 21. ) Yamashita , K. , Hitoi , A. , Matsuda , Y. , Tsuji , A. , Katunuma , N. and Kobata , A.Structural studies of the carbohydrate moieties of rat kidney γ‐glutamyltranspeptidase . J. Biol Chem. , 258 , 1098 – 1107 ( 1983. ). [PubMed] [Google Scholar]
  • 22. ) Ogata , S. , Muramatsu , T. and Kobata , A.Fractionation of glycopeptides by affinity column chromatography on concanavalin A‐Sepharose . J. Biochem. , 78 , 687 – 696 ( 1975. ). [DOI] [PubMed] [Google Scholar]
  • 23. ) Cummings , R. D. and Kornfeld , S.Fractionation of asparagine‐linked oligosaccharides by serial lectin‐agarose affinity chromatography . J. Biol. Chem. , 257 , 11235 – 11240 ( 1982. ). [PubMed] [Google Scholar]
  • 24. ) Yamashita , K. , Totani , K. , Ohkura , T. , Takasaki , S. , Goldstein , I. J. and Kobata , A.Carbohydrate binding properties of complex‐type oligosaccharides on immobilized Datura stramonium lectin . J. Biol. Chem. , 262 , 1602 – 1607 ( 1987. ). [PubMed] [Google Scholar]
  • 25. ) Yamashita , K. , Mizuochi , T. and Kobata , A.Analysis of oligosaccharides by gel filtration . Methods Enzymol. , 83 , 105 – 126 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 26. ) Endo , Y. , Yamashita , K. , Tachibana , Y. , Tojo , S. and Kobata , A.Structures of the asparagine‐linked sugar chains of human chorionic gonadotropin . J. Biochem. , 85 , 669 – 679 ( 1979. ). [PubMed] [Google Scholar]
  • 27. ) Takasaki , S. and Kobata , A.Asparagine‐linked sugar chains of fetuin: occurrence of tetrasialyl triantennary sugar chains containing the Galβ1′3GlcNAc sequence . Biochemistry , 25 , 5709 – 5715 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 28. ) Ohkura , T. , Yamashita , K. , Mishima , Y. and Kobata , A.Purification of hamster melanoma tyrosinases and structural studies of their asparagine‐linked sugar chains . Arch. Biochem. Biophys. , 235 , 63 – 77 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 29. ) Hitoi , A. , Yamashita , K. , Niwata , Y. , Irie , M. , Kochibe , N. and Kobata , A.The carbohydrate moieties of human urinary ribonuclease Ul . J. Biochem. , 101 , 29 – 41 ( 1987. ). [DOI] [PubMed] [Google Scholar]
  • 30. ) Takasaki , S. , Mizuochi , T. and Kobata , A.Hydrazinolysis of asparagine‐linked sugar chains to produce free oligosaccharides . Methods Enzymol. , 83 , 263 – 268 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 31. ) Yamashita , K. , Ohkura , T. , Yoshima , H. and Kobata , A.Substrate specificity of diplococcal β‐N‐acetylhexosaminidase, a useful enzyme for the structural studies of complex type asparagine‐linked sugar chains . Biochem. Biophys. Res. Commun. , 100 , 226 – 232 ( 1981. ). [DOI] [PubMed] [Google Scholar]
  • 32. ) Katayama , M. , Akaishi , T. , Nishihira , T. , Kasai , M. , Kan , M. and Yamane , I.Primary culture of human esophageal epithelial cells . Tohoku J. Exp. Med. , 143 , 129 – 140 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 33. ) Yamashita , K. , Tachibana , Y. , Ohkura , T. and Kobata , A.Enzymatic basis for the structural changes of asparagine‐linked sugar chains of membrane glycoproteins of baby hamster kidney cells induced by polyoma transformation . J. Biol. Chem. , 260 , 3963 – 3969 ( 1985. ). [PubMed] [Google Scholar]

Articles from Japanese Journal of Cancer Research : Gann are provided here courtesy of Wiley

RESOURCES