Skip to main content
British Journal of Cancer logoLink to British Journal of Cancer
. 1979 Dec;40(6):932–942. doi: 10.1038/bjc.1979.288

Growth pattern of tumours in mice induced by murine Moloney sarcoma-virus and sarcoma-virus-transformed cells.

F Weiland, E Weiland, M Mussgay
PMCID: PMC2010123  PMID: 230854

Abstract

Transplantation of a Moloney sarcoma-virus (MSV-M)-transformed producer cell line (Sac(+)) induced progressively or regressively growing tumours in mice. Progressive growth always occurred after transplantation of an MSV-M non-producer transformant (Sac(-)), whereas the MSV-M released from the producer cells (Sac virus) always induced tumours which regressed. In contrast to the non-producer, the producer transformant Sac(+) as well as Sac virus induced a strong immune response, detected in vitro by cell- and antibody-mediated cytotoxicity assays, and in vivo by transplantation immunity. Implantation of Sac(-) cells led to solid, under-vascularized tumours, consisting histologically of uniform densely packed tumour cells. Sac-virus-induced tumours, however, were very well vascularized and arose by proliferation of different connective-tissue cells. After transplantation of Sac(+) cells, tumours were found to consist of typical tumour cells morphologically similar to Sac(-) cells intermingled with proliferated connective-tissue cells. Cultivation of tumour fragments from Sac(+) and Sac(-) tumours was followed by outgrowth of transformed tumour cells with the properties of the originally implanted cells. Tumour explant cultures from Sac-virus-induced tumours did not lead to growth of stably transformed cells. Co-culture of mouse embryo fibroblasts (MEF) with Sac(+) cells resulted in overgrowth of the transformed cells. Infection of MEF with Sac virus led to transiently transformed cells. It is concluded that Sac(+) cell tumours will resist the strong immune defence mechanisms they induce and grow progressively, if the inoculated cells are able to build up a solid, poorly vascularized nodule in the tissue. This always happens after implantation of 10(6) cells, but only occasionally when fewer cells are inoculated. Sac-virus-induced tumours will always regress owing to the strong immune response. The regression is furthered by the fact that MSV-M infection rarely if ever leads to a stable transformation.

Full text

PDF
932

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aaronson S. A., Bassin R. H., Weaver C. Comparison of murine sarcoma viruses in nonproducer and S + L - -transformed cells. J Virol. 1972 Apr;9(4):701–704. doi: 10.1128/jvi.9.4.701-704.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bather R., Leonard A., Yang J. Characteristics of the in vitro assay of murine sarcoma virus (Moloney) and virus-infected cells. J Natl Cancer Inst. 1968 Mar;40(3):551–560. [PubMed] [Google Scholar]
  3. Berman L. D., Allison A. C. Studies on Murine Sarcoma Virus; a morphological comparison of tumorigenesis by the Harvey and Moloney strains in mice, and the establishment of tumor cell lines. Int J Cancer. 1969 Nov 15;4(6):820–836. doi: 10.1002/ijc.2910040611. [DOI] [PubMed] [Google Scholar]
  4. Collavo D., Colombatti A., Biasi G., Chieco-Bianchi L., Davies A. J. Immune reactivity in the Moloney strain of murine sarcoma virus oncogenesis: requirement of thymus-derived lymphocytes for in vivo protection. J Natl Cancer Inst. 1976 Mar;56(3):603–608. doi: 10.1093/jnci/56.3.603. [DOI] [PubMed] [Google Scholar]
  5. Davis S. Moloney sarcoma virus-induced tumors in athymic (nude) mice: growth pattern and antibody responses. J Natl Cancer Inst. 1975 Mar;54(3):793–794. doi: 10.1093/jnci/54.3.793. [DOI] [PubMed] [Google Scholar]
  6. Fefer A., McCoy J. L., Glynn J. P. Induction and regression of primary moloney sarcoma virus-induced tumors in mice. Cancer Res. 1967 Sep;27(9):1626–1631. [PubMed] [Google Scholar]
  7. Gabbiani G., Hirschel B. J., Ryan G. B., Statkov P. R., Majno G. Granulation tissue as a contractile organ. A study of structure and function. J Exp Med. 1972 Apr 1;135(4):719–734. doi: 10.1084/jem.135.4.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gazdar A. F., Stull H. B., Kilton L. J., Bachrach U. Increased ornithine decarboxylase activity in murine sarcoma virus infected cells. Nature. 1976 Aug 19;262(5570):696–698. doi: 10.1038/262696a0. [DOI] [PubMed] [Google Scholar]
  9. Hartley J. W., Rowe W. P. Production of altered cell foci in tissue culture by defective Moloney sarcoma virus particles. Proc Natl Acad Sci U S A. 1966 Apr;55(4):780–786. doi: 10.1073/pnas.55.4.780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Herberman R. B. Immunogenicity of tumor antigens. Biochim Biophys Acta. 1977 Dec 23;473(2):93–119. doi: 10.1016/0304-419x(77)90002-6. [DOI] [PubMed] [Google Scholar]
  11. Holden H. T., Haskill J. S., Kirchner H., Herberman R. B. Two functionally distinct anti-tumor effector cells isolated from primary murine sarcoma virus-induced tumors. J Immunol. 1976 Aug;117(2):440–446. [PubMed] [Google Scholar]
  12. Jainchill J. L., Aaronson S. A., Todaro G. J. Murine sarcoma and leukemia viruses: assay using clonal lines of contact-inhibited mouse cells. J Virol. 1969 Nov;4(5):549–553. doi: 10.1128/jvi.4.5.549-553.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Law L. W., Ting R. C., Stanton M. F. Some biologic, immunogenic, and morphologic effects in mice after infection with a murine sarcoma virus. I. Biologic and immunogenic studies. J Natl Cancer Inst. 1968 May;40(5):1101–1112. [PubMed] [Google Scholar]
  14. Parkman R., Levy J. A., Ting R. C. Murine sarcoma virus: the question of defectiveness. Science. 1970 Apr 17;168(3929):387–389. doi: 10.1126/science.168.3929.387. [DOI] [PubMed] [Google Scholar]
  15. Peeples P. T., Gerwin B. I., Papageorge A. G., Smith S. G. Murine sarcoma virus defectiveness. Viral polymerase expression murine and nonmurine host cells transformed by S+L-type murine sarcoma virus. Virology. 1975 Oct;67(2):344–355. doi: 10.1016/0042-6822(75)90436-5. [DOI] [PubMed] [Google Scholar]
  16. Pennelli N., Chieco-Bianchi L., Collavo D., Cecchetto A. Studio istopatologico e ultrastrutturale dei tumori indotti da virus del sarcoma murino (MSV) Tumori. 1975 Mar-Apr;61(2):129–150. doi: 10.1177/030089167506100202. [DOI] [PubMed] [Google Scholar]
  17. Rapp U. R., Todaro C. Generation of new mouse sarcoma viruses in cell culture. Science. 1978 Sep 1;201(4358):821–824. doi: 10.1126/science.210501. [DOI] [PubMed] [Google Scholar]
  18. Rowe W. P., Pugh W. E., Hartley J. W. Plaque assay techniques for murine leukemia viruses. Virology. 1970 Dec;42(4):1136–1139. doi: 10.1016/0042-6822(70)90362-4. [DOI] [PubMed] [Google Scholar]
  19. Siegler R. Pathogenesis of virus-induced murine sarcoma. I. Light microscopy. J Natl Cancer Inst. 1970 Jul;45(1):135–147. [PubMed] [Google Scholar]
  20. Simons P. J., McCully D. J. Pathologic and virologic studies of tumors induced in mice by two strains of murine sarcoma virus. J Natl Cancer Inst. 1970 Jun;44(6):1289–1303. [PubMed] [Google Scholar]
  21. Simons P. J. The behaviour of two strains of murine sarcoma virus in vitro. Aust J Exp Biol Med Sci. 1970 Feb;48(1):105–114. doi: 10.1038/icb.1970.10. [DOI] [PubMed] [Google Scholar]
  22. Stanton M. F., Law L. W., Ting R. C. Some biologic, immunogenic, and morphologic effects in mice after infection with a murine sarcoma virus. II. Morphologic studies. J Natl Cancer Inst. 1968 May;40(5):1113–1129. [PubMed] [Google Scholar]
  23. Stutman O. Delayed tumour appearance and absence of regression in nude mice infected with murine sarcoma virus. Nature. 1975 Jan 10;253(5487):142–144. doi: 10.1038/253142a0. [DOI] [PubMed] [Google Scholar]
  24. Ting R. C., Bader A. V. A quantitative study on transformation of hamster embryo cells in vitro by murine sarcoma viruses (Harvey and Moloney). Virology. 1969 Oct;39(2):194–203. doi: 10.1016/0042-6822(69)90039-7. [DOI] [PubMed] [Google Scholar]
  25. Toyoshima K., Vogt P. K. Temperature sensitive mutants of an avian sarcoma virus. Virology. 1969 Dec;39(4):930–931. doi: 10.1016/0042-6822(69)90030-0. [DOI] [PubMed] [Google Scholar]
  26. Weil R. Viral 'tumor antigens': A novel type of mammalian regulator protein. Biochim Biophys Acta. 1978 Nov 17;516(3):301–388. doi: 10.1016/0304-419x(78)90012-4. [DOI] [PubMed] [Google Scholar]
  27. Weiland E., Mussgay M. Detection of cytotoxic lymphoid spleen cells from STU-mice with Moloney sarcoma by a 3H-proline microcytotoxicity assay. Med Microbiol Immunol. 1976 Jun 1;162(2):81–87. doi: 10.1007/BF02121319. [DOI] [PubMed] [Google Scholar]
  28. Weiland E., Mussgay M. Tumor inhibiting capacity of spleen and lymph node cells from mice with murine sarcoma virus (MSV-M)-induced tumors. Z Immunitatsforsch Exp Klin Immunol. 1975 Nov;150(5):414–423. [PubMed] [Google Scholar]
  29. Weiland E., Mussgay M., Weiland F. Nonproducer malignant tumor cells with rescuable sarcoma virus genome isolated from a recurrent Moloney sarcoma. J Exp Med. 1978 Aug 1;148(2):408–423. doi: 10.1084/jem.148.2.408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zavada J., Macpherson I. Transformation of hamster cell lines in vitro by a hamster sarcoma virus. Nature. 1970 Jan 3;225(5227):24–26. doi: 10.1038/225024a0. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Cancer are provided here courtesy of Cancer Research UK

RESOURCES