Interleukin-10 inhibits tumor metastasis through an NK cell-dependent mechanism

Journal of Experimental Medicine

Volumn 184, Issue 2, 1996, Pages 579-584

  Zheng, L M ^a,c   Ojcius, D M ^b   Garaud, F ^d   Roth, C ^b   Maxwell, E ^a   Li, Z ^a   Rong, H ^a   Chen, J ^a   Wang, X Y ^a   Catino, J J ^a   King, I ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b INSTITUT PASTEUR   (France)

^c Vion Pharmaceuticals Incorporated   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 10;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CANCER IMMUNOLOGY; CANCER TRANSPLANTATION; CONTROLLED STUDY; IMMUNOMODULATION; METASTASIS INHIBITION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 10144247247     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.184.2.579     Document Type: Article

References (37)

1. Fearon, E.R., D.M. Pardoll, T. Itaya, F. Golumbek, H.I. Levitsky, J.W. Simons, H. Karasuyama, B. Vogelstein, and P. Frost. 1990. Interleukin-2 production by tumor cells bypasses T helper function in the generation of an antitumor response. Cell. 60:397-403.
2. Tepper, R.I., P.K. Pattengale, and P. Leder. 1989. Murine interleukin-4 displays potent anti-tumor activity in vivo. Cell. 57:503-512.
3. Blankenstein, T., Z. Qin, K. Überla, W. Müller, H. Rosen, H.-D. Volk, and T. Diamanstein. 1991. Tumor suppression after tumor cell-targeted tumor necrosis factor α gene transfer. J. Exp. Med. 173:1047-1052.
4. Blankenstein, T., D.A. Rowley, and H. Schreiber. 1991. Cytokines and cancer: experimental systems. Curr. Opin. Immunol. 3:694-698.
5. Weber, J.S., G. Jay, K. Tanaka, and S.A. Rosenberg. 1987. Immunotherapy of a murine tumor with interleukin 2. J. Exp. Med. 166:1716-1733.
6. Silagi, S., R. Dutkowski, and A. Schaefer. 1988. Eradication of mouse melanoma by combined treatment with recombinant human interleukin 2 and recombinant murine interferon-gamma. Int. J. Cancer 41:315-322.
7. Roth, C., L.M. Mir, M. Cressent, F. Quintin-Colonna, V. Ley, D. Fradelizi, and P. Kourilsky. 1992. Inhibition of tumor growth by histoincompatible cells expressing interleukin-2. Int. Immunol. 4:1429-1436.
8. Dranoff, G., E. Jaffee, A. Lazenby, P. Golumbek, H. Levitsky, K. Brose, V. Jackson, H. Hamada, D. Pardoll, and R.C. Mulligan. 1993. Vaccination with irradiated tumor cells engineered to secrete murine GM-CSF stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA. 90:3539-3543.
9. Yamada, G., Y. Kitamura, H. Sonoda, H. Harada, S. Taki, R.C. Mulligan, and H. Osawa. 1987. Retroviral expression of the human IL-2 gene in a murine T cell line results in cell growth autonomy and tumorigenicity. EMBO (Eur. Mol. Biol. Organ.) J. 6:2705-2709.
10. de Waal Malefyt, R., J. Haanen, H. Spits, M.G. Roncarolo, A. te Velde, C. Figdor, K. Johnson, R. Kastelein, H. Yssel, and J.E. de Vries. 1991. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174:915-924.
11. Go, N.F., B.E. Castle, R. Barret, R. Kastelein, W. Dang, T.R. Mosmann, K.W. Moore, and M. Howard. 1990. Interleukin 10 (IL-10), a novel B cell stimulatory factor: unresponsiveness of X chromosome-linked immunodeficiency B cells. J. Exp. Med. 172:1625-1631.
12. Moore, K.W., A. O'Garra, R. de Waal Malefyt, P. Vieira, and T.R. Mosmann. 1993. Interleukin-10. Annu. Rev. Immunol. 11:165-190.
13. de Waal Malefyt, R., J. Abrams, B. Bennett, C.G. Figdor, and J.E. de Vries. 1991. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1209-1220.
14. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174:1549-1555.
15. Tripp, C.S., S.F. Wolf, and E.R. Unanue. 1993. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc. Natl. Acad. Sci. USA. 90:3725-3729.
16. Silva, J.S., P.J. Morrissey, K.H. Grabstein, K.M. Mohler, D. Anderson, and S.G. Reed. 1992. Interleukin-10 and interferon-γ regulation of Trypanosoma cruzi infection. J. Exp. Med. 175:169-174.
17. Bermudez, L.F., and J. Champsi. 1993. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect. Immun. 61: 3093-3097.
18. Zheng, L.M., D.M. Ojcius, and J.D.-E. Young. 1993. Distribution of perforin-containing cells in normal and pregnant mice. Eur. J. Immunol. 23:2085-2091.
19. Richter, G., S. Kruger Krasagakes, G. Hein, C. Huls, E. Schmitt, T. Diamantstein, and T. Blankenstein. 1993. Interleukin 10 transfected into Chinese hamster ovary cells prevents tumor growth and macrophage infiltration. Cancer Res. 53:4134-4137.
20. Giovarelli, M., P. Musiani, A. Modesti, P. Dellabona, G. Casorati, A. Allione, M. Consalvo, F. Cavallo, F. di Pierro, C. De Giovanni et al., 1995. Local release of IL-10 by transfected mouse mammary adenocarcinoma cells does not suppress but enhances antitumor reaction and elicits a strong cytotoxic lymphocyte and antibody-dependent immune memory. J. Immunol. 155:3112-3123.
21. Hock, H., M. Dorsch, U. Kunzendorf, Z. Qin, T. Diamantstein, and T. Blankenstein. 1993. Mechanisms of rejection induced by tumor cell-targeted gene transfer of interleukin 2, interleukin 4, interleukin 7, tumor necrosis factor, or interferon γ. Proc. Natl. Acad. Sci. USA. 90:2774-2778.
22. + T cell-dependent tumor rejection. J. Exp. Med. 174:1291-1298.
23. Kharkevitch, D.D., D. Seito, G.C. Balch, T. Maeda, C.M. Balch, and K. Itoh. 1994. Characterization of autologous tumor-specific T-helper 2 cells in tumor-infiltrating lymphocytes from a patient with metastatic melanoma. Int. J. Cancer 58:317-323.
24. Moormeier, J.A., and H.M. Golomb. 1991. Interferons: clinical applications. Hairy cell leukemia. In Biologic therapy of cancer. V. DeVita, S. Hellman and S. Rosenberg, editor. Lippincott, Philadelphia. 275-288.
25. Nabioullin, R., S. Sone, K. Mizuno, S. Yano, Y. Nishioka, T. Haku, and T. Ogura. 1994. Interleukin-10 is a potent inhibitor of tumor cytotoxicity by human monocytes and alveolar macrophages. J. Leukoc. Biol. 55:437-442.
26. Alleva, D.G., and K.D. Elgert. 1995. Promotion of macrophage-stimulated autoreactive T cell proliferation by interleukin-10: counteraction of macrophage suppressor activity during tumor growth. Immunobiol. 192:155-171.
27. Ding, L., P.S. Linsley, L.-Y. Huang, R.N. Germain, and E.M. Shevach. 1993. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 151:1224-1234.
28. Denis, M., and E. Ghadirian. 1993. IL-10 neutralization augments mouse resistance to systemic Mycobacterium avium infections. J. Immunol. 151:5425-5430.
29. Bejarano, M.T., R. de Waal Malefyt, J.S. Abrams, M. Bigler, R. Bacchetta, J.E. de Vries, and M.G. Roncarolo. 1992. Interleukin 10 inhibits allogeneic proliferative and cytotoxic T cell responses generated in primary mixed lymphocyte cultures. Int. Immunol. 4:1389-1397.
30. Beissert, S., J. Hosoi, S. Grabbe, A. Asahina, and R.D. Granstein. 1995. IL-10 inhibits tumor antigen presentation by epidermal antigen-presenting cells. J. Immunol. 154:1280-1286.
31. Carson, G.E., M.J. Lindemann, R. Baiocchi, M. Linett, J.C. Tan, C.-C. Chou, S. Narula, and M.A. Caligiuri. 1995. The functional characterization of interleukin-10 receptor expression on human natural killer cells. Blood. 85:3577-3585.
32. Salazar-Onfray, F., M. Petersson, L. Franksson, M. Matsuda, T. Blankenstein, K. Kärre, and R. Kiessling. 1995. IL-10 converts mouse lymphoma cells to a CTL-resistant, NK-sensitive phenotype with low but peptide-inducible MHC class I expression. J. Immunol. 154:6291-6298.
33. Rice, G.E., and M.P. Bevilacqua. 1989. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science (Wash. DC). 246:1303-1306.
34. Burrows, F.J., D.O. Haskard, I.R. Hart, J.F. Marshall, S. Selkirk, S. Poole, and P.E. Thorpe. 1991. Influence of tumor-derived interleukin 1 on melanoma-endothelial cell interactions in vitro. Cancer Res. 51:4768-4775.
35. Van Vlasselaer, P., B. Borremans, U. van Gorp, J.R. Dasch, and R. De Waal-Malefyt. 1994. Interleukin 10 inhibits transforming growth factor-β (TGF-β) synthesis required for osteogenic commitment of mouse bone marrow cells. J. Cell Biol. 124:569-577.
36. Moses, H.L., E.Y. Yang, and J.A. Pietenpol. 1990. TGF-β stimulation and inhibition of cell proliferation: new mechanistic insights. Cell. 63:245-247.
37. Sulitzeanu, D. 1993. Immunosuppressive factors in human cancer. Adv. Cancer Res. 60:247-267.