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The American Journal of Pathology logoLink to The American Journal of Pathology
. 1990 Aug;137(2):393–401.

Recognition of N-glycosidic carbohydrates on esophageal carcinoma cells by macrophage cell line THP-1.

R Takano 1, M Nose 1, H Kanno 1, T Nishihira 1, S Hiraizumi 1, A Kobata 1, M Kyogoku 1
PMCID: PMC1877603  PMID: 2167012

Abstract

Cell-to-cell contact between macrophages and tumor cells is an important initial reaction in a host defense mechanism against tumor cells. The authors have studied cell surface components of human esophageal carcinoma cells recognized by macrophages. Superoxide release from THP-1 cells, a human macrophage cell line, was analyzed in their interaction with a battery of human squamous cell carcinoma cell lines (TE) originated from esophageal cancer patients. The macrophage-triggering ability of TE 1 cell line, a high stimulant, was reduced after treatment with trypsin or tunicamycin, an inhibitor of N-glycosidic glycosylation. Addition of monosaccharides was efficient in competitive inhibition of these cellular interaction. Moreover, con-A-resistant mutation of TE 1 cells was found to reduce their macrophage-triggering ability, associated with increase of L-PHA-binding capacity, suggesting substitution to the GlcNAc beta(1----6)-linked lactosamine antenna in N-glycosidic carbohydrates. These findings suggest that terminal residues of N-glycosidic carbohydrates on some esophageal carcinoma cells may contribute to the recognition sites of macrophages.

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Selected References

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  1. Ahrens P. B., Ankel H. The role of asparagine-linked carbohydrate in natural killer cell-mediated cytolysis. J Biol Chem. 1987 Jun 5;262(16):7575–7579. [PubMed] [Google Scholar]
  2. Allen R. C., Stjernholm R. L., Steele R. H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972 May 26;47(4):679–684. doi: 10.1016/0006-291x(72)90545-1. [DOI] [PubMed] [Google Scholar]
  3. Armstrong C. A., Klostergaard J., Granger G. A. Isolation and initial characterization of tumoricidal monokine(s) from the human monocytic leukemia cell line THP-1. J Natl Cancer Inst. 1985 Jan;74(1):1–9. [PubMed] [Google Scholar]
  4. Badwey J. A., Karnovsky M. L. Active oxygen species and the functions of phagocytic leukocytes. Annu Rev Biochem. 1980;49:695–726. doi: 10.1146/annurev.bi.49.070180.003403. [DOI] [PubMed] [Google Scholar]
  5. Cummings R. D., Kornfeld S. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem. 1982 Oct 10;257(19):11230–11234. [PubMed] [Google Scholar]
  6. Denizot F., Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986 May 22;89(2):271–277. doi: 10.1016/0022-1759(86)90368-6. [DOI] [PubMed] [Google Scholar]
  7. Dennis J. W., Laferté S. Recognition of asparagine-linked oligosaccharides on murine tumor cells by natural killer cells. Cancer Res. 1985 Dec;45(12 Pt 1):6034–6040. [PubMed] [Google Scholar]
  8. Dennis J. W., Laferté S., Waghorne C., Breitman M. L., Kerbel R. S. Beta 1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science. 1987 May 1;236(4801):582–585. doi: 10.1126/science.2953071. [DOI] [PubMed] [Google Scholar]
  9. Garoff H., Schwarz R. T. Glycosylation is not necessary for membrane insertion and cleavage of Semliki Forest virus membrane proteins. Nature. 1978 Aug 3;274(5670):487–490. doi: 10.1038/274487a0. [DOI] [PubMed] [Google Scholar]
  10. Heifetz A., Keenan R. W., Elbein A. D. Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry. 1979 May 29;18(11):2186–2192. doi: 10.1021/bi00578a008. [DOI] [PubMed] [Google Scholar]
  11. Helfand S. L., Werkmeister J., Roder J. C. Chemiluminescence response of human natural killer cells. I. The relationship between target cell binding, chemiluminescence, and cytolysis. J Exp Med. 1982 Aug 1;156(2):492–505. doi: 10.1084/jem.156.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hemmi H., Nakamura T., Tamura K., Shimizu Y., Kato S., Miki T., Takahashi N., Muramatsu M., Numao N., Sugamura K. Lymphotoxin: induction of terminal differentiation of the human myeloid leukemia cell lines HL-60 and THP-1. J Immunol. 1987 Feb 1;138(3):664–666. [PubMed] [Google Scholar]
  13. Imaizumi M., Breitman T. R. A combination of a T cell-derived lymphokine differentiation-inducing activity and a physiologic concentration of retinoic acid induces HL-60 to differentiate to cells with functional chemotactic peptide receptors. Blood. 1986 May;67(5):1273–1280. [PubMed] [Google Scholar]
  14. McCord J. M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969 Nov 25;244(22):6049–6055. [PubMed] [Google Scholar]
  15. Mercurio A. M. Disruption of oligosaccharide processing in murine tumor cells inhibits their susceptibility to lysis by activated mouse macrophages. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2609–2613. doi: 10.1073/pnas.83.8.2609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Misra H. P., Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972 May 25;247(10):3170–3175. [PubMed] [Google Scholar]
  17. Nakamura T., Hemmi H., Aso H., Ishida N. Variants of a human monocytic leukemia cell line (THP-1): induction of differentiation by retinoic acid, interferon-gamma, and T-lymphocyte-derived differentiation-inducing activity. J Natl Cancer Inst. 1986 Jul;77(1):21–27. [PubMed] [Google Scholar]
  18. Nathan C. F., Brukner L. H., Silverstein S. C., Cohn Z. A. Extracellular cytolysis by activated macrophages and granulocytes. I. Pharmacologic triggering of effector cells and the release of hydrogen peroxide. J Exp Med. 1979 Jan 1;149(1):84–99. doi: 10.1084/jem.149.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nathan C. F., Root R. K. Hydrogen peroxide release from mouse peritoneal macrophages: dependence on sequential activation and triggering. J Exp Med. 1977 Dec 1;146(6):1648–1662. doi: 10.1084/jem.146.6.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nathan C. F., Silverstein S. C., Brukner L. H., Cohn Z. A. Extracellular cytolysis by activated macrophages and granulocytes. II. Hydrogen peroxide as a mediator of cytotoxicity. J Exp Med. 1979 Jan 1;149(1):100–113. doi: 10.1084/jem.149.1.100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nishihira T., Kasai M., Mori S., Watanabe T., Kuriya Y., Suda M., Kitamura M., Hirayama K., Akaishi T., Sasaki T. Characteristics of two cell lines (TE-1 and TE-2) derived from human squamous cell carcinoma of the esophagus. Gan. 1979 Oct;70(5):575–584. [PubMed] [Google Scholar]
  22. Nose M., Gidlund M., Hosein Z., Axberg I., Wigzell H., Yogeeswaran G. The effect of tunicamycin on target cell susceptibility to natural killer cell cytotoxicity. Scand J Immunol. 1987 Feb;25(2):149–157. doi: 10.1111/j.1365-3083.1987.tb01058.x. [DOI] [PubMed] [Google Scholar]
  23. Ogata S., Muramatsu T., Kobata A. Fractionation of glycopeptides by affinity column chromatography on concanavalin A-sepharose. J Biochem. 1975 Oct;78(4):687–696. doi: 10.1093/oxfordjournals.jbchem.a130956. [DOI] [PubMed] [Google Scholar]
  24. Pick E., Mizel D. Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. J Immunol Methods. 1981;46(2):211–226. doi: 10.1016/0022-1759(81)90138-1. [DOI] [PubMed] [Google Scholar]
  25. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415–7419. doi: 10.1073/pnas.77.12.7415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roder J. C., Helfand S. L., Werkmeister J., McGarry R., Beaumont T. J., Duwe A. Oxygen intermediates are triggered early in the cytolytic pathway of human NK cells. Nature. 1982 Aug 5;298(5874):569–572. doi: 10.1038/298569a0. [DOI] [PubMed] [Google Scholar]
  27. Roder J. C., Rosén A., Fenyö E. M., Troy F. A. Target-effector interaction in the natural killer cell system: isolation of target structures. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1405–1409. doi: 10.1073/pnas.76.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sagone A. L., Jr, King G. W., Metz E. N. A comparison of the metabolic response to phagocytosis in human granulocytes and monocytes. J Clin Invest. 1976 May;57(5):1352–1358. doi: 10.1172/JCI108403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schlepper-Schäfer J., Holl N., Kolb-Bachofen V., Friedrich E., Kolb H. Role of carbohydrates in rat leukemia cell-liver macrophage cell contacts. Biol Cell. 1984;52(3):253–258. doi: 10.1111/j.1768-322x.1985.tb00344.x. [DOI] [PubMed] [Google Scholar]
  30. Stanley P., Caillibot V., Siminovitch L. Selection and characterization of eight phenotypically distinct lines of lectin-resistant Chinese hamster ovary cell. Cell. 1975 Oct;6(2):121–128. doi: 10.1016/0092-8674(75)90002-1. [DOI] [PubMed] [Google Scholar]
  31. Stutman O., Dien P., Wisun R. E., Lattime E. C. Natural cytotoxic cells against solid tumors in mice: blocking of cytotoxicity by D-mannose. Proc Natl Acad Sci U S A. 1980 May;77(5):2895–2898. doi: 10.1073/pnas.77.5.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. TAKAHASHI K. Squamous cell carcinoma of the esophagus. Stromal inflammatory cell infiltration as a prognostic factor. Cancer. 1961 Sep-Oct;14:921–933. doi: 10.1002/1097-0142(196109/10)14:5<921::aid-cncr2820140504>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  33. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tsuchiya S., Yamabe M., Yamaguchi Y., Kobayashi Y., Konno T., Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer. 1980 Aug;26(2):171–176. doi: 10.1002/ijc.2910260208. [DOI] [PubMed] [Google Scholar]
  35. Vernachio J., Li M., Donnenberg A. D., Soloski M. J. Qa-2 expression in the adult murine thymus. A unique marker for a mature thymic subset. J Immunol. 1989 Jan 1;142(1):48–56. [PubMed] [Google Scholar]
  36. Warr G. A. A macrophage receptor for (mannose/glucosamine)-glycoproteins of potential importance in phagocytic activity. Biochem Biophys Res Commun. 1980 Apr 14;93(3):737–745. doi: 10.1016/0006-291x(80)91139-0. [DOI] [PubMed] [Google Scholar]
  37. Yagel S., Feinmesser R., Waghorne C., Lala P. K., Breitman M. L., Dennis J. W. Evidence that beta 1-6 branched Asn-linked oligosaccharides on metastatic tumor cells facilitate invasion of basement membranes. Int J Cancer. 1989 Oct 15;44(4):685–690. doi: 10.1002/ijc.2910440422. [DOI] [PubMed] [Google Scholar]

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