Regular Article

British Journal of Cancer (1999) 80, 1494–1500. doi:10.1038/sj.bjc.6690551 www.bjcancer.com
Published online 25 June 1999

The role of human melanoma cell ICAM-1 expression on lymphokine activated killer cell-mediated lysis, and the effect of retinoic acid

C L Alexander1, M Edward1 and R M MacKie1

1Department of Dermatology, The Robertson Building, University of Glasgow, Glasgow, G12 8QQ, UK

Received 9 March 1998; Revised 26 January 1999; Accepted 27 January 1999.

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Abstract

Intercellular adhesion molecule (ICAM-1) exists as a membrane-associated form (mICAM-1) on the surface of tumour cells as well as a soluble form (sICAM-1). This study analyses the ability of all- trans retinoic acid (RA) to alter both sICAM and mICAM-1 expression in C8161 and Hs294T human melanoma cell lines and investigates the involvement of ICAM-1 in the interaction between tumour and lymphokine-activated killer (LAK) cells using the Cr-51 release assay. Our data showed that 4-day pretreatment of the tumour cells with 10–7 M RA and 10–6 M RA induced an increase in lysis of both cell lines and also increased mICAM-1 expression without having any effect on sICAM-1 levels. Addition of blocking ICAM-1 antibody (10 mug ml–1) to the C8161 cells at an effector:tumour cell ratio of 40:1 caused a 2.3-fold reduction in lysis of tumour cells and a 3-fold reduction in lysis of RA-treated cells. Blocking ICAM-1 antibody at optimum concentrations of 5 mug ml–1 reduced lysis 1.8-fold in control Hs294T cells and 1.3-fold in RA-treated cells. Blocking the HLA–ABC complex had no effect on lysis. The more highly metastatic C8161 cells were found to secrete 4-fold greater levels of sICAM-1 than the poorly metastatic Hs294T cells and addition of sICAM-1 to the assay failed to affect lysis of either cell line but did induce a 2-fold decrease in lysis of RA-treated C8161 cells. Collectively, these data provide further evidence for ICAM-1 involvement in the tumour/LAK cell response and indicates that the RA-induced increase in mICAM-1 levels are partly responsible for the increase in susceptibility of the tumour cells. sICAM-1 appears to be unimportant in evasion of the tumour cells from LAK cell lysis, but may play a role in evasion of RA-treated C8161 cells.

Keywords:

melanoma, ICAM-1, LAK cells, retinoic acid

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References

  1. Altomonte, M., Gloghini, A., Bertola, G., Gasparollo, A., Carbone, A., Ferrone, S. & Maio, M. (1993). Differential expression of cell adhesion molecules CD54/CD11a and CD58/CD2 by human melanoma cells and functional role in their interaction with cytotoxic cells. Cancer Res 53: 3343–3348. | PubMed |
  2. Aoudjit, F., Bousse, M., Stratowa, C., Voraberger, G. & Audette, M. (1994). Regulation of intercellular adhesion molecule-1 expression by retinoic acid: analysis of the 5' regulatory region of the gene. Int J Cancer 58: 543–549. | Article | PubMed | ChemPort |
  3. Babina, M., Weber, S. & Henz, B. M. (1997). Retinoic acids and dexamethasone alter cell-surface density of beta-2 integrins and ICAM-1 on human leukemic (HMC-1) mast cells. Arch Derm Res 289: 111–115.
  4. Banks, R. E., Gearing, A. J. H., Hemingway, I. K., Norfolk, D. R., Perren, T. J. & Selby, P. J. (1993). Circulating ICAM-1, E-selectin and vascular cell adhesion molecule (VCAM) in human malignancies. Br J Cancer 68: 122–124. | PubMed | ISI | ChemPort |
  5. Bassi, V., Vitale, M., Feliciello, A., Deriu, S., Rossi, G. & Fenzi, G. (1995). Retinoic acid induces ICAM-1 hyperexpression in human thyroid carcinoma cell lines. J Clin Endocrinol Metabol 80: 1129–1135.
  6. Becker, J. C., Dummer, R., Schmidt, R. E., Burg, G. & Hartmann, A. A. (1992). Shedding of intercellular adhesion molecule-1 (ICAM-1) from melanoma cell lines – functional consequences on cell-mediated cytotoxicity. Immun Infect 20: 62–63.
  7. Bouillon, M., Tessier, P., Boulianne, R., Destrempe, R. & Audette, M. (1991). Regulation by retinoic acid of ICAM-1 expression on human tumour cell lines. Biochim Biophys Acta 1097: 95–102.
  8. Budnik, A., Grewe, M., Gyufko, K. & Krutmann, J. (1996). Analysis of the production of soluble ICAM-1 molecules by human cells. Exp Hematol 24: 352–359.
  9. Cao, X. T., Chen, G. Y., He, L., Zhang, W. P., Yu, Y. Z. & Wang, J. L. (1997). Involvement of MHC class 1 molecule and ICAM-1 in the enhancement of adhesion and cytotoxic susceptibility to immune effector cells transfected with the interleukin (IL)-2, IL-4 or IL-6 gene. J Cancer Res Clin Oncol 123: 602–608. | PubMed |
  10. Cilenti, L., Toniato, E., Ruggiero, P., Fusco, C., Farina, A. R., Tiberio, A., Hatday, A. C., Gulino, A., Frati, L. & Martinotti, S. (1995). Transcriptional modulation of the human intercellular adhesion molecule gene-1 (ICAM-1) by retinoic acid. Exp Cell Res 218: 263–270. | Article | PubMed | ISI | ChemPort |
  11. Creasey, A. A., Smith, H. S., Hackett, A. J., Fukuyama, K., Epstein, W. L. & Madin, S. H. (1979). Biological properties of human melanoma cells in culture. In vitro Cell Dev Biol 15: 342–350.
  12. Eisenthal, A., Marder, O., Maymon, B., Misonzhnik, F., Skornick, Y., Brazowski, E., Czernobilsky, B., Walt, H. & Lifschitz-Mercer, B. (1998). The effect of interferon gamma and tumour necrosis factor alpha on the expression of ICAM-1 and HLA-DR molecules on cells of a human germ cell neoplasm and their susceptibility to lysis by lymphokine-activated killer cells. Pathobiology 66: 205–208.
  13. Gao, Z. & MacKenzie, I. C. (1996). Influence of retinoic acid on the expression of cytokeratins, vimentin and ICAM-1 in human gingival epithelia in-vitro. J Peridont Res 31: 81–89.
  14. Giavazzi, R., Chirivi, R. G. S., Garofalo, A., Rambaldi, A., Hemingway, I., Pigott, R. & Gearing, A. J. H. (1992). Soluble intercellular adhesion molecule-1 is released by human melanoma cells and is associated with tumour growth in nude mice. Cancer Res 52: 2628–2630. | PubMed | ISI | ChemPort |
  15. Gwin, J. L., Taylor, C. G., Taylor, D. D. & Eisenberg, B. (1996). Role of LFA-3, ICAM-1 and MHC class 1 on the sensitivity of human tumour cells to LAK cells. J Surg Res 60: 129–136.
  16. Harning, R., Mainolfi, E., Bystryn, J. C., Henn, M., Merluzzi, V. J. & Rothlein, R. (1991). Serum levels of circulating ICAM-1 in human malignant melanoma. Cancer Res 51: 5003–5005. | PubMed | ISI | ChemPort |
  17. Heymann, D., Godard, A., Raher, S., Ringeard, S., Lassort, D., Blanchard, F. & Harb, J. (1995). Human interleukin for DA cells leukemia inhibitory factor and oncostatin-M enhance membrane expression of intercellular adhesion molecule-1 on melanoma cell but not the shedding of its soluble form. Cytokine 7: 111–117.
  18. Ishiwata, N., Takio, K., Katayama, H., Watanabe, K., Titani, K., Ikeda, Y. & Handa, M. (1994). An alternatively spliced isoform of P-selectin is present in vivo as a soluble molecule. J Biol Chem 269: 23708–23715. | PubMed | ISI | ChemPort |
  19. Jackson, A. M., Alexandrov, A. B., Prescott, S., James, K. & Chisholm, G. D. (1992). Role of adhesion molecules in lymphokine-activated killer cell killing of bladder cancer cells: further evidence for a third ligand for leukocyte function associated antigen-1. Immunology 76: 286–291.
  20. Jackson, A. M., Alexandrov, A. B., Gribben, S. C., Esuvarnathan, K. & James, K. (1993). Expression and shedding of ICAM-1 in bladder cancer cells and its role in immunotherapy. Int J Cancer 55: 921–925. | PubMed | ChemPort |
  21. Johnson, J. P., Stade, B. G., Holzmann, B., Schwable, W. & Riethmuller, G. (1989). De novo expression of ICAM-1 in melanoma correlates with increased risk of metastasis. Proc Natl Acad Sci USA 86: 641–644. | Article | PubMed | ChemPort |
  22. Kageshita, T., Yoshii, A., Kimura, T., Kuriya, N., Ono, T., Tsujisaki, M., Imai, K. & Ferrone, S. (1993). Clinical relevance of ICAM-1 expression in primary lesions and serum of patients with malignant melanoma. Cancer Res 53: 4927–4932.
  23. Kaufman, D. S. (1995). Inhibition of selective signalling events in natural killer cells recognising MHC class 1. Proc Natl Acad Sci (USA) 92: 6484–6488.
  24. Lefor, A. T. & Fabian, D. F. (1998). Enhanced cytolytic activity of tumour infiltrating lymphocytes (TILs) derived from an ICAM-1 transfected tumour in a murine model. J Surg Res 75: 49–53. | Article | PubMed | ISI | ChemPort |
  25. Maio, M., Tessitori, G., Pinto, A., Temponi, M., Colombatti, A. & Ferrone, S. (1989). Differential role of distinct determinants of ICAM-1 in immunologic phenomena. J Immunol 143: 181–188. | PubMed | ChemPort |
  26. Marlin, S. D. & Springer, T. A. (1987). Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function associated antigen (LFA-1). Cell 51: 813–819. | Article | PubMed | ISI | ChemPort |
  27. Pandolfi, F., Trentin, L., Boyle, L. A., Stamenkovie, I., Byres, H. R., Colvin, R. B. & Kurnick, T. J. (1992). Expression of cell adhesion molecules in human melanoma cell lines and their role in cytotoxicity mediated by tumour infiltrating lymphocytes. Cancer 69: 1165–1173. | PubMed |
  28. Rothlein, R. M., Czajkowski, M. M., O'Neili, S. D., Marlin, E., Mainolfi, E. A. & Merluzzi, V. J. (1988). Induction of intercellular adhesion molecule-1 on primary and continuous cell lines by pro-inflammatory cytokines. Regulation by pharmacologic agents and neutralizing antibodies. J Immunol 141: 1665–1669. | PubMed | ChemPort |
  29. Rothlein, R. M., Mainolfi, E. A., Czajkowski, M. & Marlin, S. D. (1991). A form of circulating ICAM-1 in human serum. J Immunol 147: 3788–3793. | PubMed | ISI | ChemPort |
  30. Sanchez-Rovira, P., Jimenez, E., Carracedo, J., Barneto, I. C., Ramirez, R. & Aranda, E. (1998). Serum levels of intercellular adhesion molecule 1 (ICAM-1) in patients with colorectal cancer: inhibitory effect on cytotoxicity. Eur J Cancer 34: 394–398. | PubMed |
  31. Smith, M. A., Parkinson, D. R., Cheson, B. D. & Friedman, M. A. (1992). Retinoids in cancer therapy. J Clin Oncol 10: 839–864. | PubMed | ISI | ChemPort |
  32. Staunton, D. E., Marlin, S. D., Stratowa, C., Dustin, M. L. & Springer, T. A. (1988). Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 52: 925–933. | Article | PubMed | ISI | ChemPort |
  33. Vanky, F., Wang, P., Patarroyo, M. & Klein, E. (1990). Expression of adhesion molecule ICAM-1 and MHC class 1 antigens on human tumour cells is required for their interaction with autologous lymphocytes in vitro. Cancer Immunol Immunother 31: 19–27. | PubMed | ISI | ChemPort |
  34. Wang, Z. G., Cao, Y., Durso, C. M. & Ferrone, S. (1992). Differential susceptibility of cultured human melanoma cell lines to enhancement by retinoic acid of intercellular adhesion molecule-1 expression. Cancer Res 52: 4766–4772.
  35. Webb, D. S. A., Mostowski, H. S. & Gerrard, T. L. (1991). Cytokine induced enhancement of ICAM-1 expression results in increased vulnerability of tumour cells to monocyte mediated lysis. J Immunol 146: 3682–3686.
  36. Welch, D. R., Bisi, J. E., Miller, B. E., Conaway, D., Seftor, E. A. & Yohem, K. H. (1991). Characterisation of a highly invasive and spontaneously metastatic human malignant melanoma cell line. Int J Cancer 47: 227–237. | PubMed | ISI | ChemPort |
  37. Young, D. G., Jackson, A. M. & James, K. (1997). Purification and characterisation of soluble intercellular adhesion molecule-1 (sICAM-1) and its effect on cell mediated cytolysis of tumour cells. Int J Oncol 10: 827–834.