Abstract
Friend erythroleukemia cells (FLC) (H-2d) injected intravenously into adult syngeneic DBA/2 or allogeneic C57B1/6 (H-2b) or C3H (H-2k) mice lodge in the liver but only multiply in the liver of syngeneic mice. Our results indicated that endogenous IFN-alpha/beta was a crucial factor in preventing the multiplication of FLC in the liver of adult allogeneic mice. (a) Treatment of allogeneic adult C57B1/6 or C3H mice with polyclonal antibody to mouse IFN-alpha/beta (but not antibody to IFN-gamma) completely abrogated the resistance to the multiplication of FLC in the liver and 87% of tumor-injected, antibody-treated C57B1/6 mice died with extensive tumor involvement of the liver. In contrast, after intravenous inoculation FLC do not multiply at all (or very rarely) in the liver of adult C57B1/6 mice left untreated or treated with a variety of control globulins, and no deaths occurred. (b) 8 h after intravenous inoculation of FLC, poly(A)+ RNA hybridizable with specific DNA probes for mouse IFN-alpha or -beta (but not -gamma) was present in the liver of injected C57B1/6 mice. Using the expression of the Mx protein as an indicator of the presence of IFN-alpha/beta, we showed that Mx+ congenic C57B1/6 mice injected with FLC exhibited a marked increase in the expression of the Mx protein in the liver, spleen, kidney and lung, and this increase was blocked by treatment of mice with antibody to IFN-alpha/beta. The possibility that different host mechanisms are elicited depending on the site of tumor growth in allogeneic mice is discussed. IFN-alpha/beta appears to be of particular importance in determining the resistance of the liver to FLC in allogeneic mice.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Affabris E., Jemma C., Rossi G. B. Isolation of interferon-resistant variants of Friend erythroleukemia cells: effects of interferon and ouabain. Virology. 1982 Jul 30;120(2):441–452. doi: 10.1016/0042-6822(82)90044-7. [DOI] [PubMed] [Google Scholar]
- Amici C., Ferrantini M., Benedetto A., Belardelli F., Gresser I. Biologic and biochemical differences between in vitro and in vivo passaged Friend erythroleukemia cells. II. Changes in cell surface glycoproteins associated with a highly malignant phenotype. Int J Cancer. 1984 Sep 15;34(3):397–402. doi: 10.1002/ijc.2910340317. [DOI] [PubMed] [Google Scholar]
- Bach F. H., Sachs D. H. Current concepts: immunology. Transplantation immunology. N Engl J Med. 1987 Aug 20;317(8):489–492. doi: 10.1056/NEJM198708203170807. [DOI] [PubMed] [Google Scholar]
- Belardelli F., Ferrantini M., Maury C., Santurbano L., Gresser I. Biologic and biochemical differences between in vitro and in vivo passaged Friend erythroleukemia cells. I. Tumorigenicity and capacity to metastasize. Int J Cancer. 1984 Sep 15;34(3):389–395. doi: 10.1002/ijc.2910340316. [DOI] [PubMed] [Google Scholar]
- Belardelli F., Gresser I., Maury C., Maunoury M. T. Antitumor effects of interferon in mice injected with interferon-sensitive and interferon-resistant Friend leukemia cells. I. Int J Cancer. 1982 Dec 15;30(6):813–820. doi: 10.1002/ijc.2910300621. [DOI] [PubMed] [Google Scholar]
- Belardelli F., Vignaux F., Proietti E., Gresser I. Injection of mice with antibody to interferon renders peritoneal macrophages permissive for vesicular stomatitis virus and encephalomyocarditis virus. Proc Natl Acad Sci U S A. 1984 Jan;81(2):602–606. doi: 10.1073/pnas.81.2.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berger R., Knapp W., Kirchner H. Interferon induction in human mixed leukocyte-tumor-cell reactions: evidence for restriction to a certain lineage expressing glycophorin A. Int J Cancer. 1984 Jul 15;34(1):39–47. doi: 10.1002/ijc.2910340108. [DOI] [PubMed] [Google Scholar]
- De Maeyer-Guignard J., Tovey M. G., Gresser I., De Maeyer E. Purification of mouse interferon by sequential affinity chromatography on poly(U)--and antibody--agarose columns. Nature. 1978 Feb 16;271(5646):622–625. doi: 10.1038/271622a0. [DOI] [PubMed] [Google Scholar]
- Galabru J., Robert N., Buffet-Janvresse C., Rivière Y., Hovanessian A. G. Continuous production of interferon in normal mice: effect of anti-interferon globulin, sex, age, strain and environment on the levels of 2-5A synthetase and p67K kinase. J Gen Virol. 1985 Apr;66(Pt 4):711–718. doi: 10.1099/0022-1317-66-4-711. [DOI] [PubMed] [Google Scholar]
- Gray P. W., Goeddel D. V. Cloning and expression of murine immune interferon cDNA. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5842–5846. doi: 10.1073/pnas.80.19.5842. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gresser I., Belardelli F., Maury C., Maunoury M. T., Tovey M. G. Injection of mice with antibody to interferon enhances the growth of transplantable murine tumors. J Exp Med. 1983 Dec 1;158(6):2095–2107. doi: 10.1084/jem.158.6.2095. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gresser I., Belardelli F., Maury C., Tovey M. G., Maunoury M. T. Anti-tumor effects of interferon in mice injected with interferon-sensitive and interferon-resistant friend leukemia cells. IV. Definition of optimal treatment regimens. Int J Cancer. 1986 Aug 15;38(2):251–257. doi: 10.1002/ijc.2910380216. [DOI] [PubMed] [Google Scholar]
- Gresser I. How does interferon inhibit tumor growth? Interferon. 1985;6:93–126. [PubMed] [Google Scholar]
- Gresser I., Maury C., Woodrow D., Moss J., Grütter M. G., Vignaux F., Belardelli F., Maunoury M. T. Interferon treatment markedly inhibits the development of tumor metastases in the liver and spleen and increases survival time of mice after intravenous inoculation of Friend erythroleukemia cells. Int J Cancer. 1988 Jan 15;41(1):135–142. doi: 10.1002/ijc.2910410124. [DOI] [PubMed] [Google Scholar]
- Gresser I., Tovey M. G., Bandu M. E., Maury C., Brouty-Boyé D. Role of interferon in the pathogenesis of virus diseases in mice as demonstrated by the use of anti-interferon serum. I. Rapid evolution of encephalomyocarditis virus infection. J Exp Med. 1976 Nov 2;144(5):1305–1315. doi: 10.1084/jem.144.5.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gresser I., Vignaux F., Belardelli F., Tovey M. G., Maunoury M. T. Injection of mice with antibody to mouse interferon alpha/beta decreases the level of 2'-5' oligoadenylate synthetase in peritoneal macrophages. J Virol. 1985 Jan;53(1):221–227. doi: 10.1128/jvi.53.1.221-227.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haller O., Arnheiter H., Gresser I., Lindenmann J. Genetically determined, interferon-dependent resistance to influenza virus in mice. J Exp Med. 1979 Mar 1;149(3):601–612. doi: 10.1084/jem.149.3.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haller O. Inborn resistance of ice to orthomyxoviruses. Curr Top Microbiol Immunol. 1981;92:25–52. doi: 10.1007/978-3-642-68069-4_3. [DOI] [PubMed] [Google Scholar]
- Higashi Y., Sokawa Y., Watanabe Y., Kawade Y., Ohno S., Takaoka C., Taniguchi T. Structure and expression of a cloned cDNA for mouse interferon-beta. J Biol Chem. 1983 Aug 10;258(15):9522–9529. [PubMed] [Google Scholar]
- Horisberger M. A., Hochkeppel H. K. An interferon-induced mouse protein involved in the mechanism of resistance to influenza viruses. Its purification to homogeneity and characterization by polyclonal antibodies. J Biol Chem. 1985 Feb 10;260(3):1730–1733. [PubMed] [Google Scholar]
- Jack A. S., McVeigh K. L. A demonstration of a strain related restriction effect in the formation of experimental metastases. J Pathol. 1987 May;152(1):37–45. doi: 10.1002/path.1711520106. [DOI] [PubMed] [Google Scholar]
- Kamada N. The immunology of experimental liver transplantation in the rat. Immunology. 1985 Jul;55(3):369–389. [PMC free article] [PubMed] [Google Scholar]
- Kawade Y. An analysis of neutralization reaction of interferon by antibody: a proposal on the expression of neutralization titer. J Interferon Res. 1980 Fall;1(1):61–70. doi: 10.1089/jir.1980.1.61. [DOI] [PubMed] [Google Scholar]
- Landolfo S., Cofano F., Giovarelli M., Prat M., Cavallo G., Forni G. Inhibition of interferon-gamma may suppress allograft reactivity by T lymphocytes in vitro and in vivo. Science. 1985 Jul 12;229(4709):176–179. doi: 10.1126/science.3160110. [DOI] [PubMed] [Google Scholar]
- Locardi C., Belardelli F., Federico M., Romeo G., Affabris E., Gresser I. Effect of mouse interferon alpha/beta on the expression of H-2 (class I) antigens and on the levels of 2'-5' oligoadenylate synthetase activity in interferon-sensitive and interferon-resistant Friend leukemia cell tumors in mice. J Biol Regul Homeost Agents. 1987 Oct-Dec;1(4):189–194. [PubMed] [Google Scholar]
- Reid L. M., Minato N., Gresser I., Holland J., Kadish A., Bloom B. R. Influence of anti-mouse interferon serum on the growth and metastasis of tumor cells persistently infected with virus and of human prostatic tumors in athymic nude mice. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1171–1175. doi: 10.1073/pnas.78.2.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reyes V. E., Klimpel G. R. Interferon alpha/beta synthesis during acute graft-versus-host disease. Transplantation. 1987 Mar;43(3):412–416. doi: 10.1097/00007890-198703000-00018. [DOI] [PubMed] [Google Scholar]
- Shaw G. D., Boll W., Taira H., Mantei N., Lengyel P., Weissmann C. Structure and expression of cloned murine IFN-alpha genes. Nucleic Acids Res. 1983 Feb 11;11(3):555–573. doi: 10.1093/nar/11.3.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spitalny G. L., Havell E. A. Monoclonal antibody to murine gamma interferon inhibits lymphokine-induced antiviral and macrophage tumoricidal activities. J Exp Med. 1984 May 1;159(5):1560–1565. doi: 10.1084/jem.159.5.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staeheli P., Dreiding P., Haller O., Lindenmann J. Polyclonal and monoclonal antibodies to the interferon-inducible protein Mx of influenza virus-resistant mice. J Biol Chem. 1985 Feb 10;260(3):1821–1825. [PubMed] [Google Scholar]
- Staeheli P., Haller O., Boll W., Lindenmann J., Weissmann C. Mx protein: constitutive expression in 3T3 cells transformed with cloned Mx cDNA confers selective resistance to influenza virus. Cell. 1986 Jan 17;44(1):147–158. doi: 10.1016/0092-8674(86)90493-9. [DOI] [PubMed] [Google Scholar]
- Staeheli P., Haller O. Interferon-induced Mx protein: a mediator of cellular resistance to influenza virus. Interferon. 1987;8:1–23. [PubMed] [Google Scholar]
- Tovey M. G., Streuli M., Gresser I., Gugenheim J., Blanchard B., Guymarho J., Vignaux F., Gigou M. Interferon messenger RNA is produced constitutively in the organs of normal individuals. Proc Natl Acad Sci U S A. 1987 Jul;84(14):5038–5042. doi: 10.1073/pnas.84.14.5038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trinchieri G., Santoli D., Knowles B. B. Tumour cell lines induce interferon in human lymphocytes. Nature. 1977 Dec 15;270(5638):611–613. doi: 10.1038/270611a0. [DOI] [PubMed] [Google Scholar]
