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. 1992 Feb;118(2):141–146. doi: 10.1007/BF01187503

Tumours induced by Moloney murine sarcoma virus are clonal in rats, not clonal in mice

Emma D'Andrea 1,✉, Lino Tessarollo 1, Chiara Menin 1, Luigi Chieco-Bianchi 1
PMCID: PMC12200080  PMID: 1735735

Abstract

Moloney murine sarcoma virus (M-MSV) induces rapidly growing tumours in adult mice of most conventional strains. Rats are less susceptible to M-MSV oncogenesis, but the few rhabdomyosarcomas that do develop after viral inoculation of newborn animals closely resemble conventional malignancies: they develop after a long latency, grow progressively, and metastasize to regional lymph nodes and lungs. Southern blot analysis with a v-mos-specific probe of M-MSV-induced tumours in both species demonstrated an oligo-, monoclonal pattern of exogenous v-mos integration only in the rat system, while mouse tumours were not clonal in origin. Furthermore, the same type of analysis of lymph node and lung metastases showed that cell clones already present in the primary rat lesion colonized secondary sites during tumour progression. Apparently, Moloney murine leukemia virus (M-MuLV) was not involved in rhabdomyosarcoma pathogenesis since M-MuLV-specific DNA sequences could not be demonstrated in three of the six rat tumours. Finally, in all mouse tumours, unintegrated linear M-MSV proviruses could be readily detected.

Key words: v-mos, Acute retrovirus, Tumour clonality

Abbreviations

M-MSV

Moloney murine sarcoma virus

M-MuLV

Moloney murine leukemia virus

References

  1. Azzarello G, Sartore S, Saggin L, Gorza L, D'Andrea E, Chieco-Bianchi L, Schiaffino S (1987) Myosin isoform expression in rat rhabdomyosarcoma induced by Moloney murine sarcoma virus. J Cancer Res Clin Oncol 113:417–429 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Becker S, Haskill S (1980) Characterization of the presumptive sarcoma cells in primary MSV tumors. Int J Cancer 25:543–550 [DOI] [PubMed] [Google Scholar]
  3. Chieco-Bianchi L, Collavo D (1976) Some illustrative system of viral oncogenesis: the leukemia-sarcoma virus complex in the mouse. In: Symington T, Carter RL (eds) Scientific foundations of oncology. Heinemann, London, pp 388–393 [Google Scholar]
  4. Chieco-Bianchi L, Collavo D, Biasi G (1988) Immunologic unresponsiveness to murine leukemia virus antigens: mechanisms and role in tumor development. Adv Cancer Res 51:275–306 [DOI] [PubMed] [Google Scholar]
  5. Colombatti A, Collavo D, Biasi G, Chieco-Bianchi L (1975) Genetic control of oncogenesis by murine sarcoma virus Moloney pseudotype. Genetic resistance in AKR mice. Int J Cancer 16:427–434 [DOI] [PubMed] [Google Scholar]
  6. D'Andrea E, Saggioro D, Fleissner E, Chieco-Bianchi L (1987) Abelson murine leukemia virus induced thymic lymphomas: transformation of a primitive lymphoid precursor. JNCI 79:189–195 [PubMed] [Google Scholar]
  7. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction fragments to high specific activity. Anal Biochem 132:6–13 [DOI] [PubMed] [Google Scholar]
  8. Flyer DC, Burakoff SJ, Faller DV (1983) Cytotoxic T lymphocyte recognition of transfected cells expressing a cloned retroviral gene. Nature 305:815–818 [DOI] [PubMed] [Google Scholar]
  9. Flyer DC, Burakoff SJ, Faller DV (1985) Expression and CTL recognition of cloned subgenomic fragments of Moloney murine leukemia virus in murine cells. Surv Immunol Res 4:168–172 [DOI] [PubMed] [Google Scholar]
  10. Green PL, Kaehler DA, Risser R (1987) Clonal dominance and progression in Abelson murine leukemia virus lymphomagenesis. J Virol 61:2192–2197 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Green PK, Kaehler DA, Bennet LM, Risser R (1989) Multisteps are required for the induction of tumors by Abelson murine leukemia virus. J Virol 63:1989–1994 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanahan D (1989) Transgenic mice as probes into complex systems. Science 246:1265–1275 [DOI] [PubMed] [Google Scholar]
  13. Hartley JW, Rowe WP (1975) Clonal cell lines from feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology 65:128–134 [DOI] [PubMed] [Google Scholar]
  14. Iannaccone PM, Weinberg WC, Deamant FD (1987) On the clonal origin of tumors: a review of experimental models. Int J Cancer 39:778–784 [DOI] [PubMed] [Google Scholar]
  15. Jones M, Bosselman RA, Van Der Hoorn FA, Berns A, Fan H, Verma IM (1980) Identification and molecular cloning of Moloney mouse sarcoma virus-specific sequences from uninfected mouse cells. Proc Natl Acad Sci USA 77:2651–2655 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Keshet E, Temin HM (1979) Cell killing by spleen necrosis virus is correlated with a transient accumulation of spleen necrosis virus DNA. J Virol 31:376–388 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lasneret J (1967) Etudes des tumeurs provoquées chez le rat par le virus du sarcome de Moloney. Bull Cancer 54:193–200 [Google Scholar]
  18. Linial M, Blair D (1984) Genetics of retroviruses. In: Weiss R, Teich N, Varmus H, Coffin J (eds) Molecular biology of tumor viruses. RNA tumor viruses 1/text. Cold Spring Harbor Laboratory, New York, pp 649–783 [Google Scholar]
  19. Mullins JI, Chen CS, Hoover EA (1986) Disease-specific and tissue-specific production of unintegrated feline leukemia virus variant DNA in feline AIDS. Nature 319:333–336 [DOI] [PubMed] [Google Scholar]
  20. Nowell PC (1986) Mechanisms of tumor progression. Cancer Res 46:2203–2207 [PubMed] [Google Scholar]
  21. Nowell PC (1989) The clonal nature of neoplasia. Cancer Cells 1:29–30 [PubMed] [Google Scholar]
  22. Papkoff J, Ringold GM (1984) Use of the mouse mammary tumor virus long terminal repeat to promote steroid-inducible expression of v-mos. J Virol 52:420–430 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Papkoff J, Verma IM, Hunter T (1982) Detection of a transforming gene product in cells transformed by Moloney murine sarcoma virus. Cell 29:417–426 [DOI] [PubMed] [Google Scholar]
  24. Pauza CD, Galindo JE, Richman DD (1990) Reinfection results in accumulation of unintegrated viral DNA in cytopathic and persistent human immunodeficiency virus type 1 infection in CEM cells. J Exp Med 172:1035–1042 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pennelli N, Chieco-Bianchi L, Collavo D, Cecchetto A (1975) Studio istopatologico e ultrastrutturale dei tumori indotti da virus del sarcoma murino (MSV). Tumori 61:129–150 [DOI] [PubMed] [Google Scholar]
  26. Perk K, Shachat DA, Moloney JB (1968) Pathogenesis of a rhabdomyosarcoma (undifferentiated type) in rats induced by murine sarcoma virus (Moloney). Cancer Res 28:1197–1206 [PubMed] [Google Scholar]
  27. Saggioro D, Zamarchi R, D'Andrea E, Chieco-Bianchi L (1988) In vitro malignant progression of cells derived from Abelson murine leukemia virus induced thymic lymphomas. Br J Cancer 58:152–157 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, New York, pp 914–919 [Google Scholar]
  29. Southern EM (1975) Detection of specific sequences among fragments separated by gel electrophoresis. J Mol Biol 98:503–517 [DOI] [PubMed] [Google Scholar]
  30. Teich N, Wyke J, Mak T, Bernstein A, Hardy W (1984) Pathogenesis of retrovirus-induced disease. In: Weiss R, Teich N, Varmus H, Coffin J (eds) Molecular biology of tumor viruses. RNA tumor viruses 1/text. Cold Spring Harbor Laboratory, New York, pp 785–998 [Google Scholar]
  31. Weller SK, Joy AE, Temin HM (1980) Correlation between cell killing and massive second-round superinfection by members of some subgroups of avian leukosis virus. J Virol 33:494–506 [DOI] [PMC free article] [PubMed] [Google Scholar]

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