1887

Abstract

Mouse mammary tumour virus (MMTV) is a member of the genus , infects rodent cells and uses mouse tranferrin receptor 1 for cell entry. Several MMTV strains have been shown to productively infect, in addition to murine cells, various heterologous cell lines including those of human origin, albeit less efficiently than murine cells. Here, we analysed whether MMTV from C3H mice [MMTV(C3H)], reported previously to be incapable of infecting human cells, could productively infect human cells. Using a recently described high-titre MMTV-based vector carrying MMTV(C3H) envelope protein (Env), we successfully transduced cells of human origin. Furthermore, WT MMTV(C3H) was able to infect human cells, albeit less efficiently than mouse cells. The established infection was, however, sufficient to enable virus spread to every cell in culture. The infectivity of WT MMTV(C3H) and MMTV-based vectors carrying MMTV(C3H)Env was blocked by heat inactivation, an inhibitor of reverse transcription (3′-azido-3′-deoxythymidine) and pre-incubation with neutralizing anti-MMTV antibodies that did not neutralize vectors pseudotyped with amphotropic murine leukemia virus Env, providing evidence for an authentic, receptor-mediated and reverse transcriptase-dependent infection process. Persistently infected human Hs578T cells produced infectious virions capable of infecting naïve human breast cells in culture, the infectivity of which could also be blocked by neutralizing anti-MMTV antibodies, demonstrating that virus particles released by the persistently infected Hs578T cells were related antigenically to the virus produced from murine cells. Taken together, our results show that MMTV(C3H), like MMTV(GR) and MMTV(RIII), is able not only to infect but also to replicate in cultured human breast cells.

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2015-03-01
2024-04-20
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References

  1. Abraham J., Kwong J. A., Albariño C. G., Lu J. G., Radoshitzky S. R., Salazar-Bravo J., Farzan M., Spiropoulou C. F., Choe H. 2009; Host-species transferrin receptor 1 orthologs are cellular receptors for nonpathogenic New World clade B arenaviruses. PLoS Pathog 5:e1000358 [View Article][PubMed]
    [Google Scholar]
  2. Aisen P. 2004; Transferrin receptor 1. Int J Biochem Cell Biol 36:2137–2143 [View Article][PubMed]
    [Google Scholar]
  3. Allison A. B., Harbison C. E., Pagan I., Stucker K. M., Kaelber J. T., Brown J. D., Ruder M. G., Keel M. K., Dubovi E. J.other authors 2012; Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. J Virol 86:865–872 [View Article][PubMed]
    [Google Scholar]
  4. Bentvelzen P., Daams J. H., Hageman P., Calafat J. 1970; Genetic transmission of viruses that incite mammary tumor in mice. Proc Natl Acad Sci U S A 67:377–384 [View Article][PubMed]
    [Google Scholar]
  5. Brookes S., Piaczek M., Moore R., Dixon M., Dickson C., Peters G. 1986; Insertion elements and transitions in cloned mouse mammary tumour virus DNA: further delineation of the poison sequences. Nucleic Acids Res 14:8231–8245 [View Article][PubMed]
    [Google Scholar]
  6. Charrel R. N., de Lamballerie X. 2003; Arenaviruses other than Lassa virus. Antiviral Res 57:89–100 [View Article][PubMed]
    [Google Scholar]
  7. Choe H., Jemielity S., Abraham J., Radoshitzky S. R., Farzan M. 2011; Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. Curr Opin Microbiol 14:476–482 [View Article][PubMed]
    [Google Scholar]
  8. Cosset F. L., Takeuchi Y., Battini J. L., Weiss R. A., Collins M. K. 1995; High-titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol 69:7430–7436[PubMed]
    [Google Scholar]
  9. Crandell R. A., Fabricant C. G., Nelson-Rees W. A. 1973; Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro 9:176–185 [View Article][PubMed]
    [Google Scholar]
  10. Demogines A., Abraham J., Choe H., Farzan M., Sawyer S. L. 2013; Dual host–virus arms races shape an essential housekeeping protein. PLoS Biol 11:e1001571 [View Article][PubMed]
    [Google Scholar]
  11. Flanagan M. L., Oldenburg J., Reignier T., Holt N., Hamilton G. A., Martin V. K., Cannon P. M. 2008; New World clade B arenaviruses can use transferrin receptor 1 (TfR1)-dependent and -independent entry pathways, and glycoproteins from human pathogenic strains are associated with the use of TfR1. J Virol 82:938–948 [View Article][PubMed]
    [Google Scholar]
  12. Golovkina T. V., Prescott J. A., Ross S. R. 1993; Mouse mammary tumor virus-induced tumorigenesis in sag transgenic mice: a laboratory model of natural selection. J Virol 67:7690–7694[PubMed]
    [Google Scholar]
  13. Hayward J. A., Tachedjian M., Cui J., Field H., Holmes E. C., Wang L. F., Tachedjian G. 2013; Identification of diverse full-length endogenous betaretroviruses in megabats and microbats. Retrovirology 10:35 [View Article][PubMed]
    [Google Scholar]
  14. Held W., Waanders G. A., Shakhov A. N., Scarpellino L., Acha-Orbea H., MacDonald H. R. 1993; Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell 74:529–540 [View Article][PubMed]
    [Google Scholar]
  15. Hook L. M., Agafonova Y., Ross S. R., Turner S. J., Golovkina T. V. 2000; Genetics of mouse mammary tumor virus-induced mammary tumors: linkage of tumor induction to the gag gene. J Virol 74:8876–8883 [View Article][PubMed]
    [Google Scholar]
  16. Howard D. K., Schlom J. 1978; Isolation of host-range variants of mouse mammary tumor viruses that efficiently infect cells in vitro. Proc Natl Acad Sci U S A 75:5718–5722 [View Article][PubMed]
    [Google Scholar]
  17. Howard D. K., Colcher D., Teramoto Y. A., Young J. M., Schlom J. 1977; Characterization of mouse mammary tumor viruses propagated in heterologous cells. Cancer Res 37:2696–2704[PubMed]
    [Google Scholar]
  18. Hsu W. L., Lin H. Y., Chiou S. S., Chang C. C., Wang S. P., Lin K. H., Chulakasian S., Wong M. L., Chang S. C. 2010; Mouse mammary tumor virus-like nucleotide sequences in canine and feline mammary tumors. J Clin Microbiol 48:4354–4362 [View Article][PubMed]
    [Google Scholar]
  19. Hueffer K., Parker J. S., Weichert W. S., Geisel R. E., Sgro J. Y., Parrish C. R. 2003; The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J Virol 77:1718–1726 [View Article][PubMed]
    [Google Scholar]
  20. Indik S., Günzburg W. H., Salmons B., Rouault F. 2005a; Mouse mammary tumor virus infects human cells. Cancer Res 65:6651–6659 [View Article][PubMed]
    [Google Scholar]
  21. Indik S., Günzburg W. H., Salmons B., Rouault F. 2005b; A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 337:1–6 [View Article][PubMed]
    [Google Scholar]
  22. Indik S., Günzburg W. H., Kulich P., Salmons B., Rouault F. 2007; Rapid spread of mouse mammary tumor virus in cultured human breast cells. Retrovirology 4:73 [View Article][PubMed]
    [Google Scholar]
  23. Janeway C. 1991; MIs: makes a little sense. Nature 349:459–461 [View Article][PubMed]
    [Google Scholar]
  24. Kaelber J. T., Demogines A., Harbison C. E., Allison A. B., Goodman L. B., Ortega A. N., Sawyer S. L., Parrish C. R. 2012; Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog 8:e1002666 [View Article][PubMed]
    [Google Scholar]
  25. Konstantoulas C., Indik S. 2014; Mouse mammary tumor virus infects non-dividing cells, enters the nucleus via a TNPO3-independent pathway and integrates in a less biased fashion than other retroviruses. Retrovirology 11:34 [View Article][PubMed]
    [Google Scholar]
  26. Kozak C., Peters G., Pauley R., Morris V., Michalides R., Dudley J., Green M., Davisson M., Prakash O.other authors 1987; A standardized nomenclature for endogenous mouse mammary tumor viruses. J Virol 61:1651–1654[PubMed]
    [Google Scholar]
  27. Lasfargues E. Y., Coutinho W. G., Dion A. S. 1979; A human breast tumor cell line (BT-474) that supports mouse mammary tumor virus replication. In Vitro 15:723–729 [View Article][PubMed]
    [Google Scholar]
  28. Marrack P., Kushnir E., Kappler J. 1991; A maternally inherited superantigen encoded by a mammary tumour virus. Nature 349:524–526 [View Article][PubMed]
    [Google Scholar]
  29. Müllner M., Salmons B., Günzburg W. H., Indik S. 2008; Identification of the Rem-responsive element of mouse mammary tumor virus. Nucleic Acids Res 36:6284–6294 [View Article][PubMed]
    [Google Scholar]
  30. Owens R. B., Hackett A. J. 1972; Tissue culture studies of mouse mammary tumor cells and associated viruses. J Natl Cancer Inst 49:1321–1332[PubMed]
    [Google Scholar]
  31. Parker J. S., Murphy W. J., Wang D., O’Brien S. J., Parrish C. R. 2001; Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virol 75:3896–3902 [View Article][PubMed]
    [Google Scholar]
  32. Radoshitzky S. R., Kuhn J. H., Spiropoulou C. F., Albariño C. G., Nguyen D. P., Salazar-Bravo J., Dorfman T., Lee A. S., Wang E.other authors 2008; Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. Proc Natl Acad Sci U S A 105:2664–2669 [View Article][PubMed]
    [Google Scholar]
  33. Ringold G., Lasfargues E. Y., Bishop J. M., Varmus H. E. 1975; Production of mouse mammary tumor virus by cultured cells in the absence and presence of hormones: assay by molecular hybridization. Virology 65:135–147 [View Article][PubMed]
    [Google Scholar]
  34. Ross S. R., Schofield J. J., Farr C. J., Bucan M. 2002; Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc Natl Acad Sci U S A 99:12386–12390 [View Article][PubMed]
    [Google Scholar]
  35. Sena-Esteves M., Tebbets J. C., Steffens S., Crombleholme T., Flake A. W. 2004; Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 122:131–139 [View Article][PubMed]
    [Google Scholar]
  36. Wang E., Albritton L., Ross S. R. 2006; Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J Biol Chem 281:10243–10249 [View Article][PubMed]
    [Google Scholar]
  37. Wang E., Obeng-Adjei N., Ying Q., Meertens L., Dragic T., Davey R. A., Ross S. R. 2008; Mouse mammary tumor virus uses mouse but not human transferrin receptor 1 to reach a low pH compartment and infect cells. Virology 381:230–240 [View Article][PubMed]
    [Google Scholar]
  38. Zapata J. C., Salvato M. S. 2013; Arenavirus variations due to host-specific adaptation. Viruses 5:241–278 [View Article][PubMed]
    [Google Scholar]
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