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Expression of intercellular adhesion molecule 1 (ICAM-1) during the development of invasion and/or metastasis of gastric carcinoma

  • Original Papers
  • Clinical Oncology
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Summary

In this study, using two-color flow-cytometric analysis, we examined the expression of histocompatibility locus antigens (HLA) classes I and II, and intercellular adhesion molecule 1 (ICAM-1) in 10 cases of normal gastric mucosa, 13 cases of primary carcinoma on the stomach, 16 cases of metastatic carcinoma from malignant ascites in patients with gastric carcinoma and 14 samples of their cultured carcinoma cells. Compared with normal gastric mucosa, HLA class I were highly expressed in a considerable number of tumor cells in each experimental group. The expression of HLA class II tended to reduce in the order of normal gastric mucosa, primary gastric carcinoma and peritoneal-effusion-associated carcinoma. Altogether, 85.7% of cases of cultured tumor cells showed abrogation and loss of HLA class II. The ICAM-1 molecule was not detected on normal gastric epithelial cells. In few cases, carcinoma cells from large volumes of tumor located in the stomach showed detectable amounts of ICAM-1. On the other hand, all of the metastatic carcinoma cells from peritoneal effusions showed a high level of expression of the ICAM-1 molecule. The expression of ICAM-1 on adenocarcinoma cells was maintained and/or augmented by in vitro cultivation with tumor-infiltrating lymphocytes (TIL). Furthermore, twocolor fluorescence-activated cell sorting analysis of TIL revealed that significant correlation was observed between the expression of ICAM-1 and the degree of TIL, composed mainly of CD3+ T cells including CD8+ CD11b, CD8+CD28+, CD8+S6F1+ and CD4+Leu8+, and CD57+CD16 and CD57+CD16+ NK cells, and HLA-DR+LeuM3+ macrophages.

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Abbreviations

ICAM-1:

intercellular adhesion molecule 1

CTL:

cytotoxic T lymphocytes

TIL:

tumor-infiltrating lymphocytes

References

  • Billaud M, Calender A, Seigneurine JM, Leonoir GM (1987) LFA-1, LFA-3, and ICAM-1 expression in Burkitt's lymphoma. Lancet 2:1327–1328

    Google Scholar 

  • Björkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–518

    Google Scholar 

  • Clement LT, Dagg HD, Landy A (1984) Characterization of human lymphocyte subpopulations: alloreactive cytotoxic T-lymphocyte precursor and effector cells are phenotypically distinct from Leu 2a+ suppressor cells. J Clin Immunol 131:2296–2300

    Google Scholar 

  • Degener T, Momburg F, Möller P (1988) Differential expression of HLA-DR, HLA-DP, HLA-DQ and associated invariant chain (Ii) in normal colorectal mucosa, adenoma and carcinoma. Virchows Arch [A] 412:315–322

    Google Scholar 

  • Dougherty GJ, Murdoch S, Hogg N (1988) The function of human intercellular adhesion molecule-1 (ICAM-1) in the generation of an immune response. Eur J Immunol 18:35–39

    Google Scholar 

  • Doukas J, Pober JS (1990) Lymphokine-mediated activation of cultured endothelial cells (EC). CD4+ T cells inhibit EC class II MHC expression despite secreting IFN-γ and increasing EC class I MHC and intercellular adhesion molecule-1 expression. J Immunol 145:1088–1098

    Google Scholar 

  • Doyle A, Strominger J (1987) Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature 330:256–259

    Google Scholar 

  • Doyle A, Martin WJ, Gazdar A, Carney D, Martin SE, Linnoila I, Cuttita F, Mulshine J, Bunn P, Minna J (1985) Markedly decreased expression of class I histocompatibility antigens, protein and m RNA in human small cell lung cancer. J Exp Med 161:1135–1151

    Google Scholar 

  • Dustine ML, Rothlein R, Bhan AK, Dinarello CA, Springer TA (1986) Induction by IL 1 and interferon-γ: tissue distribution, biochemistry, and function of a natural adhesion molecule (ICAM-1). J Immunol 137:245–254

    Google Scholar 

  • Ebihara T, Koyama S (1990) Functional and phenotypic characteristics of effusion-associated lymphoid cells cultured in the presence of either recombinant interleukin 2 or T-cell growth factor from malignant pleural and peritoneal effusions in patients with advanced carcinoma. Tohoku J Exp Med 162:49–63

    Google Scholar 

  • Ebihara T, Koyama S, Fukao K, Osuga T (1989) Lymphokine-activated suppressor (LAS) cells in patients with gastric carcinoma. Cancer Immunol Immunother 28:218–224

    Google Scholar 

  • Ebihara T, Fukao K, Koyama S (1990) Functional and phenotypic characteristics of recombinant interleukin-2 or T-cell growth factor-activated splenic lymphoid cells from patients with gastric or hepatocellular carcinoma. Cancer 66:923–929

    Google Scholar 

  • Ebihara T, Sakai N, Koyama S (1991) Suppression by sorted CD8+ CD11b cells from T-cell growth factor-activated peripheral blood lymphocytes on cytolytic activity against tumour in patients with gastric carcinoma. Eur J Cancer 27:1654–1657

    Google Scholar 

  • Festenstein H (1987) The biological consequences of altered MHC expression of tumour. Br Med Bull 43:217–227

    Google Scholar 

  • Hämmerling GJ, Klar D, Katzaw S, Segal S, Feldman M, Wallich R, Hämmerling A (1986) Manipulation of metastasis and tumor growth by transfection with histocompatibility class I antigens. J Immunogenet 153–157

  • Hämmerling GJ, Klar D, Pülm W, Momburg F, Moldenhauer G (1987) The influence of major histocompatibility complex class I antigens on tumor growth and metastasis. Biochim Biophys Acta 907:245–259

    Google Scholar 

  • Harding CV, Unaue ER (1989) Antigen processing and intercellular Ia: possible roles of endocytosis and protein synthesis in Ia function. J Immunol 142:12–19

    Google Scholar 

  • Johnson JP, Stade BG, Holzmann B, Schwable W, Riethmüller G (1989) De novo expression of intercellular adhesion molecule 1 in melanoma correlates with increased risk of metastasis. proc Natl Acad Sci USA 86:641–644

    Google Scholar 

  • Koide J, Engelman EG (1990) Differences in surface phenotype and mechanism of action between alloantigen-specific CD8+ cytotoxic and suppressor T cell clones. J Immunol 144:32–40

    Google Scholar 

  • Koyama S, Fujimoto S, Tada T, Sakita T (1981) Effect of bacillus Calmette-Guerin cell wall skeleton on the induction of the cytotoxic and suppressor T cells against syngeneic tumor in the mouse. Int J Cancer 27:829–835

    Google Scholar 

  • Koyama S, Yoshioka T, Sakita T (1982) Suppression of cell-mediated antitumor immunity by complete Freund's adjuvant. Cancer Res 42:3215–3219

    Google Scholar 

  • Koyama S, Mukai R, Fukao K, Arimura H, Iwasaki Y, Osuga T (1987) Monoclonal antibody against human gallbladder carcinoma-associated antigen. Cancer Res 47:4667–4673

    Google Scholar 

  • Koyama S, Ebihara T, Fukao K, Osuga T (1989) Differential activation of lymphokine-activated killer cells with different surface phenotypes by cultivation with recombinant interleukin 2 or T-cell growth factor in gastric cancer patients. Jpn J Cancer Res 80:150–157

    Google Scholar 

  • Maio M, Gulwani B, Langer A, Kerbel RS, Duigou GJ, Fisher PB, Ferrone S (1989) Modulation by interferons of HLA antigen, high-molecular-weight melanoma-associated antigen, and intercellular adhesion molecule 1 expression by cultured melanoma cells with different metastatic potential. Cancer Res 49:2980–2987

    Google Scholar 

  • Marlin SD, Springer TA (1987) Purified intercellular adhesion molecule 1 (ICAM-1) is a ligand for lymphocyte function-associated antigen-1 (LFA-1). Cell 51:813–819

    Google Scholar 

  • Meuer SC, Schlossman SF, Reinherz EL (1982) Clonal analysis of human cytotoxis T lymphocytes: T4+ and T8+ effector T cells recognize products of different major histocompatibility complex regions. Proc Natl Acad Sci USA 79:4395–4399

    Google Scholar 

  • Möller P, Herrman B, Moldenhauer G, Momburg F (1987) Defective expression of MHC class I antigens is frequent in B cell lymphomas of high-grade malignancy. Int J Cancer 40:32–39

    Google Scholar 

  • Morimoto C, Rudd CE, Letven NL, Schlossman SF (1987) A novel epitope of the LFA-1 antigen which can distinguish killer effector and suppressor cells in human CD8 cells. Nature 330:479–482

    Google Scholar 

  • Mortarini R, Belli F, Parmiani G, Anichini A (1990) Cytokine-mediated modulation of HLA class II, ICAM-1, LFA-3 and tumor-associated antigen profile of melanoma cells. Comparison with anti-proliferative activity by rIL 1β, rTNF-α, rIFN-γ, rIL 4 and their combinations. Int J Cancer 45:334–341

    Google Scholar 

  • Natali P, Nicotra MR, Cavaliere R, Biotti A, Romano G, Temponi M, Ferrone S (1990) Differential expression of intercellular adhesion molecule 1 in primary and metastatic melanoma lesions. Cancer Res 50:1271–1278

    Google Scholar 

  • Norment AM, Salter RD, Parham P, Engelhard VH, Littman DR (1988) Cell-cell adhesion mediated by CD8 and MHC class I molecules. Nature 336:79–81

    Google Scholar 

  • Nuchterm JG, Biddison WE, Klausner RD (1990) Class-II MHC molecules can use the endogenous pathway of antigen presentation. Nature 343:74–76

    Google Scholar 

  • Patarroyo M, Makgoba W (1989) Leukocyte adhesion to cells, molecular basis, physiological relevance and abnormalities. Scand J Immunol 30:129–164

    Google Scholar 

  • Pircher H, Groscurth P, Baumhutter S, Aguet M, Zinkernagel RM, Hengartner H (1986) A monoclonal antibody against altered LFA-1 induced proliferation and lymphokine release of cloned T cells. Eur J Immunol 16:172–181

    Google Scholar 

  • Rivoltini L, Cattoretti G, Arienti F, Mastroianni A, Melani C, Colombo MP, Parmiani G (1991) The high lysability by LAK cells for colon-carcinoma cells resistant to doxorubicin is associated with a high expression of ICAM-1, IFA-3, NCA and a less-differentiated phenotype. Int J Cancer 47:746–754

    Google Scholar 

  • Rothlein L, Czajkowski M, O'Neill MM, Marlin SD, Mainolfi E, Merluzzi VJ (1988) Induction of intercellular adhesion molecule 1 on primary and continuous cell lines by proinflammatory cytokines. Regulation by pharmacologic agents and neutralizing antibodies. J Immunol 141:1665–1669

    Google Scholar 

  • Spits J, Van Schooten W, Keiser H, Van Seventer G, Van de Rijn M, Terhorst C, De Vries DE (1986) Alloantigen recognition is preceded by nonspecific adhesion of cytotoxic T cells and target cells. Science 232:403–405

    Google Scholar 

  • Stockinger B, Pessara U, Lin RW, Habicht J, Grez M, Koch N (1989) A role of Ia-associated invariant chains in antigen processing and presentation. Cell 56:683–689

    Google Scholar 

  • Sweetser MT, Morrison LA, Braciale VL, Braciale TJ (1989) Recognition of pre-processed endogenous antigen by class-I but not class-II MHC-restricted T cells. Nature 342:180–182

    Google Scholar 

  • Tomita Y, Nishiyama T, Watanabe H, Fujiwara M, Sato S (1990) Expression of intercellular adhesion molecule-1 (ICAM-1) on renal-cell cancer: possible significance in host immune responses. Int J Cancer 46:1001–1006

    Google Scholar 

  • Vogetseder W, Feitinger H, Schulz TF, Schwaeble W, Tabaczewski P, Mitterer M, Böck G, Marth C, Dapunt O, Mikuz G, Dierich MP (1989) Expression of 7F7-antigen, a human adhesion molecule identical to intercellular adhesion molecule-1 (ICAM-1) in human carcinoma and their stromal fibroblasts. Int J Cancer 43:768–773

    Google Scholar 

  • Zinkernagel RM, Doherty PC (1979) MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction specificity, function, and responsiveness. Adv Immunol 27:51–177

    Google Scholar 

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Koyama, S., Ebihara, T. & Fukao, K. Expression of intercellular adhesion molecule 1 (ICAM-1) during the development of invasion and/or metastasis of gastric carcinoma. J Cancer Res Clin Oncol 118, 609–614 (1992). https://doi.org/10.1007/BF01211806

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  • DOI: https://doi.org/10.1007/BF01211806

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