1887

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Volume 95, Issue 7

Modulation of the host microenvironment by a common non-oncolytic mouse virus leads to inhibition of plasmacytoma development through NK cell activation Free

Abstract

Although many cells undergo transformation, few actually develop into tumours, due to successful mechanisms of immunosurveillance. To investigate whether an infectious agent may play a role in this process, the growth of a plasmacytoma was investigated in mice infected by lactate dehydrogenase-elevating virus. Acutely infected animals were significantly protected against tumour development. The mechanisms responsible for this protection were analysed in mice deficient for relevant immune cells or molecules and after cell depletion. This protection by viral infection correlated with NK cell activation and with IFN-γ production. It might also be related to activation of NK/T-cells, although this remains to be proven formally. Therefore, our results indicated that infections with benign micro-organisms may protect the host against cancer development, through non-specific stimulation of the host's innate immune system and especially of NK cells.

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
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/content/journal/jgv/10.1099/vir.0.063990-0
2014-07-01
2024-04-19
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References

  1. Ammann C. G., Messer R. J., Peterson K. E., Hasenkrug K. J. 2009; Lactate dehydrogenase-elevating virus induces systemic lymphocyte activation via TLR7-dependent IFNα responses by plasmacytoid dendritic cells. PLoS ONE 4:e6105 [View Article][PubMed]
     [Google Scholar]
  2. Bindea G., Mlecnik B., Fridman W.-H., Pagès F., Galon J. 2010; Natural immunity to cancer in humans. Curr Opin Immunol 22:215–222 [View Article][PubMed]
     [Google Scholar]
  3. Brinton-Darnell M., Brand I. 1977; Delayed foreign-body tumorigenesis in mice infected with lactate dehydrogenase-elevating virus: brief communication. J Natl Cancer Inst 59:1027–1029[PubMed]
     [Google Scholar]
  4. Cancro M., Potter M. 1976; The requirement of an adherent cell substratum for the growth of developing plasmacytoma cells in vivo . J Exp Med 144:1554–1567 [View Article][PubMed]
     [Google Scholar]
  5. Coutelier J.-P., Brinton M. A. 2007; Lactate dehydrogenase-elevating virus. In The Mouse in Biomedical Research, 2nd edn. vol. 2 pp. 215–234 Edited by Fox J. G., Barthold S. W., Davisson M. T., Newcomer C. E., Quimby F. W., Smith A. L. London: Academic Press; [View Article]
     [Google Scholar]
  6. Coutelier J.-P., Van Broeck J., Wolf S. F. 1995; Interleukin-12 gene expression after viral infection in the mouse. J Virol 69:1955–1958[PubMed]
     [Google Scholar]
  7. Dalton D. K., Pitts-Meek S., Keshav S., Figari I. S., Bradley A., Stewart T. A. 1993; Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739–1742 [View Article][PubMed]
     [Google Scholar]
  8. Dunn T. B., Potter M. 1957; A transplantable mast-cell neoplasm in the mouse. J Natl Cancer Inst 18:587–601[PubMed]
     [Google Scholar]
  9. Dunn G. P., Koebel C. M., Schreiber R. D. 2006; Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6:836–848 [View Article][PubMed]
     [Google Scholar]
  10. Eberl G., MacDonald H. R. 2000; Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells. Eur J Immunol 30:985–992 [View Article][PubMed]
     [Google Scholar]
  11. Kaplan D. H., Shankaran V., Dighe A. S., Stockert E., Aguet M., Old L. J., Schreiber R. D. 1998; Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A 95:7556–7561 [View Article][PubMed]
     [Google Scholar]
  12. Kiessling R., Klein E., Wigzell H. 1975; “Natural” killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 5:112–117 [View Article][PubMed]
     [Google Scholar]
  13. Le-Thi-Phuong T., Dumoutier L., Renauld J.-C., Van Snick J., Coutelier J.-P. 2007a; Divergent roles of IFNs in the sensitization to endotoxin shock by lactate dehydrogenase-elevating virus. Int Immunol 19:1303–1311 [View Article][PubMed]
     [Google Scholar]
  14. Le-Thi-Phuong T., Thirion G., Coutelier J.-P. 2007b; Distinct gamma interferon-production pathways in mice infected with lactate dehydrogenase-elevating virus. J Gen Virol 88:3063–3066 [View Article][PubMed]
     [Google Scholar]
  15. Markine-Goriaynoff D., Nguyen T. D., Bigaignon G., Van Snick J., Coutelier J.-P. 2001; Distinct requirements for IL-6 in polyclonal and specific Ig production induced by microorganisms. Int Immunol 13:1185–1192 [View Article][PubMed]
     [Google Scholar]
  16. Markine-Goriaynoff D., Hulhoven X., Cambiaso C. L., Monteyne P., Briet T., Gonzalez M.-D., Coulie P., Coutelier J.-P. 2002; Natural killer cell activation after infection with lactate dehydrogenase-elevating virus. J Gen Virol 83:2709–2716[PubMed]
     [Google Scholar]
  17. Meite M., Léonard S., Idrissi M. E., Izui S., Masson P. L., Coutelier J.-P. 2000; Exacerbation of autoantibody-mediated hemolytic anemia by viral infection. J Virol 74:6045–6049 [View Article][PubMed]
     [Google Scholar]
  18. Michaelides M. C., Schlesinger S. 1974; Effect of acute or chronic infection with lactic dehydrogenase virus (LDV) on the susceptibility of mice to plasmacytoma MOPC-315. J Immunol 112:1560–1564[PubMed]
     [Google Scholar]
  19. Miyamoto M., Emoto M., Brinkmann V., van Rooijen N., Schmits R., Kita E., Kaufmann S. H. E. 2000; Cutting edge: contribution of NK cells to the homing of thymic CD4+NKT cells to the liver. J Immunol 165:1729–1732 [View Article][PubMed]
     [Google Scholar]
  20. Musaji A., Cormont F., Thirion G., Cambiaso C. L., Coutelier J.-P. 2004; Exacerbation of autoantibody-mediated thrombocytopenic purpura by infection with mouse viruses. Blood 104:2102–2106 [View Article][PubMed]
     [Google Scholar]
  21. Orange J. S., Biron C. A. 1996; Characterization of early IL-12, IFN-alphabeta, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J Immunol 156:4746–4756[PubMed]
     [Google Scholar]
  22. Smiley S. T., Kaplan M. H., Grusby M. J. 1997; Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science 275:977–979 [View Article][PubMed]
     [Google Scholar]
  23. Smyth M. J., Crowe N. Y., Godfrey D. I. 2001; NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 13:459–463 [View Article][PubMed]
     [Google Scholar]
  24. Stanford M. M., Breitbach C. J., Bell J. C., McFadden G. 2008; Innate immunity, tumor microenvironment and oncolytic virus therapy: friends or foes?. Curr Opin Mol Ther 10:32–37[PubMed]
     [Google Scholar]
  25. Street S. E. A., Trapani J. A., MacGregor D., Smyth M. J. 2002; Suppression of lymphoma and epithelial malignancies effected by interferon γ. J Exp Med 196:129–134 [View Article][PubMed]
     [Google Scholar]
  26. Stueckemann J. A., Ritzi D. M., Holth M., Smith M. S., Swart W. J., Cafruny W. A., Plagemann P. G. W. 1982; Replication of lactate dehydrogenase-elevating virus in macrophages. 1. Evidence for cytocidal replication. J Gen Virol 59:245–262 [View Article][PubMed]
     [Google Scholar]
  27. Su D., Le-Thi-Phuong T., Coutelier J.-P. 2012; Modulation of lipopolysaccharide receptor expression by lactate dehydrogenase-elevating virus. J Gen Virol 93:106–112 [View Article][PubMed]
     [Google Scholar]
  28. Ullrich E., Ménard C., Flament C., Terme M., Mignot G., Bonmort M., Plumas J., Chaperot L., Chaput N., Zitvogel L. 2008; Dendritic cells and innate defense against tumor cells. Cytokine Growth Factor Rev 19:79–92 [View Article][PubMed]
     [Google Scholar]
  29. Weiland E., Grossmann A., Thiel H.-J., Weiland F. 1990; Lactate dehydrogenase-elevating virus induces antibodies reactive with a surface antigen of aetiologically unrelated murine cell transformants. J Gen Virol 71:1233–1236 [View Article][PubMed]
     [Google Scholar]
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Modulation of the host microenvironment by a common non-oncolytic mouse virus leads to inhibition of plasmacytoma development through NK cell activation
J. Gen. Virol. 95, 1504 (2014); https://doi.org/10.1099/vir.0.063990-0
/content/journal/jgv/10.1099/vir.0.063990-0
/content/journal/jgv/10.1099/vir.0.063990-0
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