Skip to main content
SpringerLink
Log in

src-specific immunity in inbred chickens bearing v-src DNA- and RSV-induced tumors

  • Original Papers
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The growth pattern (progression/regression) of v-src DNA- and Rous sarcoma virus (RSV)-induced tumors was analogous on a panel of inbred chicken lines. The decisive role of the major histocompatibility complex [Mhc(B)] alleles in resistance to the progression of these tumors was formally proved in segregating backcross populations. The immune mechanism of tumor regression was demonstrated by both in vivo and in vitro assays. A protective effect of v-src-specific immunity against RSV challenge was shown in Rous sarcoma regressor line CB (B 12/B 12). Immune cells from regressors of v-src DNA-induced tumors can protect syngeneic hosts from the development of tumor after challenge with both v-src DNA and RSV. Suppression of RSV-induced tumor cell growth in vitro was also achieved by the use of cocultivation with spleen cells from chickens in which v-src DNA-induced tumors had regressed. This in vitro sarcoma-specific response was Mhc(B)-restricted. Chickens of the congenic Rous sarcoma progressor line CC (B 4/B 4) are sometimes able to regress v-src DNA-induced tumors, but immune cells can only slow the growth of v-src DNA-induced tumors in syngeneic hosts. This suggests that the primary reason for the susceptibility of CC chickens is a weak v-src-specific immune response. Furthermore, some of the v-src DNA-induced tumors were transplantable across the Mhc(B) barrier. The growth of tumor allografts was able to be facilitated when immunological tolerance to the B-F/L region antigens (class I and class II) had been established. This demonstrated that a high tumorigenicity of the transplantable tumor was not due to the lack of Mhc(B) antigens on tumor cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bishop, J. M. Viral oncogenes. Cell 42: 23–38, 1985

    Google Scholar 

  • Briles, W. E., Bumstead, N., Ewert, D. L., Gilmour, D. G., Gogusev, J., Hála, K., Koch, C., Longenecker, B. M., Nordskog, A. V., Pink, J. R. L., Schierman, L. W., Simonsen, M., Toivanen, A., Toivanen, P., Vainio, O., and Wick, G. Nomenclature for chicken major histocompatibility (B) complex. Immunogenetics 15: 441–447, 1982

    Google Scholar 

  • Chaussé, A. M., Coudert, F., Dambrine, G., Guillemot, F., Miller, M. M., and Auffray, C. Molecular genotyping of four chicken B-complex haplotypes with B-Lβ, B-F, and B-G probes. Immunogenetics 29: 127–130, 1989

    Google Scholar 

  • Chen, C. and Okayama, H. High efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7: 2745–2752, 1987

    Google Scholar 

  • Collins, W. M., Briles, W. E., Zsigray, R. M., Dunlop, W. R., Corbert, A. C., Clark, K. K., Marks, J. L., and McGrail, T. P. The B locus (MHC) in the chicken: association with the fate of RSV-induced tumors. Immunogenetics 5: 333–343, 1977

    Google Scholar 

  • Fung, Y. K. T., Crittenden, L. B., Fadly, A. M., and Kung, H. J. Tumor induction by direct injection of cloned v-src DNA into chickens. Proc Natl Acad Sci USA 80: 353–357, 1983

    Google Scholar 

  • Gelman, I. H. and Hanafusa, H. Suppression of Rous sarcoma virus-induced tumor formation by preinfection with viruses encoding src protein with novel N termini. J Virol 63: 2461–2468, 1989

    Google Scholar 

  • Gelman, I. H. and Hanafusa, H. src-specific immune regression of Rous sarcoma virus-induced tumors. Cancer Res 53: 915–920, 1993

    Google Scholar 

  • Halpern, M. S., Ewert, D. L., and England, J. M. Wing web or intravenous inoculation of chickens with v-src DNA induces visceral sarcomas. Virology 175: 328–331, 1990

    Google Scholar 

  • Halpern, M. S., England, J. M., Coates, L., Stoltzfus, C. M., and Mason, W. S. Regression of v-src DNA-induced sarcomas is under host genetic control. Virology 180: 857–860, 1991

    Google Scholar 

  • Halpern, M. S., Wisner, T. W., Brown, I. P., and England, J. M. Immune-based resistance to the formation of v-src-induced distal tumors. Virology 197: 480–484, 1993

    Google Scholar 

  • Heinzelmann, E. W., Zsigray, R. M., and Collins, W. M. Increased growth of RSV-induced tumors in chickens partially tolerant to MHC alloantigens. Immunogenetics 12: 275–284, 1981

    Google Scholar 

  • Kuzumaki, N., Fujita, H., Dosaka, H., Katabami, M., and Levinson, A. D. Transplantation resistance to a Rous sarcoma virus-induced tumor in mice immunized with v-src protein. J Natl Cancer Inst 80: 959–962, 1988

    Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J. Molecular Cloning: A Laboratory Manual, 2nd edn, pp. 1.38–1.46, Cold Spring Harbor Laboratory, Cold Spring Harbor, 1989

    Google Scholar 

  • Plachý, J. Hierarchy of the B (MHC) haplotypes controlling resistance to Rous sarcomas in a model of inbred lines of chickens. Folia Biol (Praha) 30: 412–425, 1984

    Google Scholar 

  • Plachý, J. An analysis of the response of recombinant congenic lines of chickens to RSV challenge provides evidence for further complexity of the genetic structure of the chicken MHC. (B). Folia Biol (Praha) 34: 170–181, 1988

    Google Scholar 

  • Plachý, J. and Benda, V. Location of the gene responsible for Rous sarcoma regression in the B-F region of the B complex (MHC) of the chicken. Folia Biol (Praha) 27: 363–368, 1981

    Google Scholar 

  • Plachý, J., Benda, V., Karakoz, Z., and Špatenková, Z. Different importance of primary lymphoid organs for Rous sarcoma regression in inbred lines of chickens. Folia Biol (Praha) 30: 177–188, 1984

    Google Scholar 

  • Plachý, J., Chaussé, A. M., Thoraval, P., and Coudert, F. Molecular genotyping of recombinant congenic lines provides evidence for crossing-over within the B-G region of the major histocompatibility complex of the chicken. Immunogenetics 36: 270–273, 1992a

    Google Scholar 

  • Plachý, J., Hála, K., and Benda, V., Regression of tumors induced by Rous sarcoma virus in different inbred lines of chickens. Folia Biol (Praha) 25: 335–336, 1979

    Google Scholar 

  • Plachý, J., Karakoz, Z., and Benda, V. Concomitant immunity leads to retardation or acceleration of the growth of Rous sarcomas in genetically resistant or susceptible inbred lines of chickens. Folia Biol (Praha) 32: 334–348, 1986

    Google Scholar 

  • Plachý, J., Pink, J. R. L., and Hála, K. Biology of the chicken MHC (B complex). Crit Rev Immunol 12: 47–79, 1992b

    Google Scholar 

  • Plachý, J., and Špatenková, Z. Failure to confirm the role of immunological tolerance to B(MHC) alloantigens in the growth of RSV-induced tumors in chickens. Folia Biol (Praha) 28: 283–288, 1982

    Google Scholar 

  • Plachý, J., Vilhelmová, M., Karakoz, I., and Schulmannová, J. Prague inbred lines of chickens: A biological model for MHC research. Folia Biol (Praha) 35: 177–196, 1989

    Google Scholar 

  • Pontén, J. The in vivo growth mechanism of avian Rous sarcoma. Natl Cancer Inst Monogr 17: 131–145, 1964

    Google Scholar 

  • Schierman, L. W., Watanabe, D. H., and McBride, R. A. Genetic control of Rous sarcoma regression in chickens: linkage with the major histocompatibility complex. Immunogenetics 5: 325–332, 1977

    Google Scholar 

  • Simonsen, M., Crone, M., Koch, C., and Hála, K. The MHC haplotypes of the chicken. Immunogenetics 16: 513–532, 1982

    Google Scholar 

  • Stéhelin, D., Varmus, H. E., and Bishop, J. M. DNA related to the transforming gene(s) of avian sarcoma virus is present in normal avian DNA. Nature 260: 170–173, 1976

    Google Scholar 

  • Stoker, A. W., and Sieweke, M. H. v-src induces clonal sarcomas and rapid metastasis following transduction with a replication-defective retrovirus. Proc Natl Acad Sci USA 86: 10123–10127, 1989

    Google Scholar 

  • Suda, T., Shimizu, J., Mizushima, Y., Fujiwara, H., and Hamaoka, T. Separation of the tumor rejection antigen of Rous sarcoma virus-induced murine fibrosarcoma. Jpn J Cancer Res 79: 365–374, 1988

    Google Scholar 

  • Svoboda, J., Lhoták, V., Geryk, J., Saule, S., Raes, M. B., and Stéhelin, D. Characterization of exogenous proviral sequences in hamster tumor cell lines transformed by Rous sarcoma virus rescued from XC cells. Virology 128: 195–209, 1983

    Google Scholar 

  • Svoboda, J., Plachý, J., Hejnar, J., Karakoz, I., Guntaka, R. V., and Geryk, J. Tumor induction by LTR, v-src, LTR DNA in four B (MHC) congenic lines of chickens. Immunogenetics 35: 309–315, 1992

    Google Scholar 

  • Taylor, R. L., Ewert, D. L., England, J. M., and Halpern, M. S. Major histocompatibility (B) complex control of the growth pattern of v-src DNA-induced primary tumors. Virology 191: 477–479, 1992

    Google Scholar 

  • Wainberg, M. A. and Halpern, M. S. Avian sarcomas: immune responsiveness and pathology. In G. F. deBoer (ed.): Avian Leukosis, p. 132, Martinus Nijhoff Publishing, Boston, 1986

    Google Scholar 

  • Wainberg, M. A., Markson, Y., Weiss, D. W., and Doljanski, F. Cellular immunity against Rous sarcomas of chickens. Preferential reactivity against autochthonous target cells as determined by lymphocyte adherence and cytotoxicity tests in vitro. Proc Natl Acad Sci USA 71: 3565–3569, 1974

    Google Scholar 

  • Winn, H. J. Immune mechanisms in homotransplantation. II. Quantitative assay of the immunologic activity of lymphoid cells stimulated by tumor homografts. J Immunol 86: 228–239, 1961

    Google Scholar 

  • Wisner, T. W., England, J. M., Pan, D., Stoker, A. W., and Halpern, M. S. Tumor immunity generated in the course of regression of v-src-induced sarcomas. J Virol 65: 7020–7024, 1991

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cellular and Viral Genetics, Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Flemingovo nám. 2, 16637, Prague 6, Czech Republic

    Jiří Plachý, Jiří Hejnar, Josef Geryk & Jan Svoboda

  2. Institute for General and Experimental Pathology, University of Innsbruck, Medical School, Fritz-Pregl-Strasse 3, A-6020, Innsbruck, Austria

    Karel Hála

Authors
  1. Jiří Plachý
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karel Hála
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiří Hejnar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josef Geryk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jan Svoboda
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Plachý, J., Hála, K., Hejnar, J. et al. src-specific immunity in inbred chickens bearing v-src DNA- and RSV-induced tumors. Immunogenetics 40, 257–265 (1994). https://doi.org/10.1007/BF00189970

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00189970

Keywords

Search

Navigation