1887

Abstract

Lactate dehydrogenase-elevating virus (LDV) exacerbates mouse susceptibility to endotoxin shock through enhanced tumour necrosis factor (TNF) production by macrophages exposed to lipopolysaccharide (LPS). However, the enhancement of TNF production in response to LPS induced by the virus largely exceeds that found with cells derived from infected animals. Infection was followed by a moderate increase of Toll-like receptor (TLR)-4/MD2, but not of membrane CD14 expression on peritoneal macrophages. Peritoneal macrophages from LDV-infected mice unresponsive to type I interferons (IFNs) did not show enhanced expression of TLR-4/MD2 nor of CD14, and did not produce more TNF in response to LPS than cells from infected normal counterparts, although the response of these animals to LPS was strongly enhanced. In contrast, the virus triggered a sharp increase of soluble CD14 and of LPS-binding protein serum levels in normal mice. However, production of these LPS soluble receptors was similar in LDV-infected type I IFN-receptor deficient mice and in their normal counterparts. Moreover, serum of LDV-infected mice that contained these soluble receptors had little effect if any on cell response to LPS. These results suggest that enhanced response of LDV-infected mice to LPS results mostly from mechanisms independent of LPS receptor expression.

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2012-01-01
2022-01-26
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References

  1. Azeredo E. L., Neves-Souza P. C., Alvarenga A. R., Reis S. R. N. I., Torrentes-Carvalho A., Zagne S.-M. O., Nogueira R. M. R., Oliveira-Pinto L. M., Kubelka C. F. 2010; Differential regulation of Toll-like receptor-2, Toll-like receptor-4, CD16 and human leucocyte antigen-DR on peripheral blood monocytes during mild and severe dengue fever. Immunology 130:202–216 [View Article][PubMed]
    [Google Scholar]
  2. Benten D., Follenzi A., Bhargava K. K., Kumaran V., Palestro C. J., Gupta S. 2005; Hepatic targeting of transplanted liver sinusoidal endothelial cells in intact mice. Hepatology 42:140–148 [View Article][PubMed]
    [Google Scholar]
  3. Chaby R. 2004; Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cell Mol Life Sci 61:1697–1713 [View Article][PubMed]
    [Google Scholar]
  4. de Waal Malefyt R., Figdor C. G., Huijbens R., Mohan-Peterson S., Bennett B., Culpepper J., Dang W., Zurawski G., de Vries J. E. 1993; Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol 151:6370–6381[PubMed]
    [Google Scholar]
  5. Doughty L. A., Nguyen K. B., Durbin J. E., Biron C. A. 2001; A role for IFN-α β in virus infection-induced sensitization to endotoxin. J Immunol 166:2658–2664[PubMed] [CrossRef]
    [Google Scholar]
  6. El Azami El Idrissi M., Mazza G., Monteyne P., Elson C. J., Day M. J., Pfau C. J., Coutelier J.-P. 1998; Lymphocytic choriomeningitis virus-induced alterations of T helper-mediated responses in mice developing autoimmune hemolytic anemia during the course of infection. Proc Soc Exp Biol Med 218:349–356[PubMed] [CrossRef]
    [Google Scholar]
  7. Fearns C., Loskutoff D. J. 1997; Role of tumor necrosis factor alpha in induction of murine CD14 gene expression by lipopolysaccharide. Infect Immun 65:4822–4831[PubMed]
    [Google Scholar]
  8. Grohmann U., Van Snick J., Campanile F., Silla S., Giampietri A., Vacca C., Renauld J.-C., Fioretti M. C., Puccetti P. 2000; IL-9 protects mice from Gram-negative bacterial shock: suppression of TNF-α, IL-12, and IFN-γ, and induction of IL-10. J Immunol 164:4197–4203[PubMed] [CrossRef]
    [Google Scholar]
  9. Gutsmann T., Müller M., Carroll S. F., MacKenzie R. C., Wiese A., Seydel U. 2001; Dual role of lipopolysaccharide (LPS)-binding protein in neutralization of LPS and enhancement of LPS-induced activation of mononuclear cells. Infect Immun 69:6942–6950 [View Article][PubMed]
    [Google Scholar]
  10. 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]
  11. 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]
  12. Lien E., Aukrust P., Sundan A., Müller F., Frøland S. S., Espevik T. 1998; Elevated levels of serum-soluble CD14 in human immunodeficiency virus type 1 (HIV-1) infection: correlation to disease progression and clinical events. Blood 92:2084–2092[PubMed]
    [Google Scholar]
  13. Liu D.-F., Wei W., Song L.-H. 2006; Protective effect of paeoniflorin on immunological liver injury induced by bacillus Calmette-Guerin plus lipopolysaccharide: modulation of tumour necrosis factor-α and interleukin-6 MRNA. Clin Exp Pharmacol Physiol 33:332–339 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. McGettrick A. F., O’Neill L. A. J. 2010; Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22:20–27 [View Article][PubMed]
    [Google Scholar]
  16. Miyake K. 2007; Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin Immunol 19:3–10 [View Article][PubMed]
    [Google Scholar]
  17. Monick M. M., Yarovinsky T. O., Powers L. S., Butler N. S., Carter A. B., Gudmundsson G., Hunninghake G. W. 2003; Respiratory syncytial virus up-regulates TLR4 and sensitizes airway epithelial cells to endotoxin. J Biol Chem 278:53035–53044 [View Article][PubMed]
    [Google Scholar]
  18. Müller U., Steinhoff U., Reis L. F. L., Hemmi S., Pavlovic J., Zinkernagel R. M., Aguet M. 1994; Functional role of type I and type II interferons in antiviral defense. Science 264:1918–1921 [View Article][PubMed]
    [Google Scholar]
  19. Nansen A., Christensen J. P., Marker O., Thomsen A. R. 1997; Sensitization to lipopolysaccharide in mice with asymptomatic viral infection: role of T cell-dependent production of interferon-γ. J Infect Dis 176:151–157 [View Article][PubMed]
    [Google Scholar]
  20. Peterson V. W., Adamovicz J. J., Elliott T. B., Moore M. M., Madonna G. S., Jackson III W. E., Ledney G. D, Gause W. C. 1994; Gene expression of hematoregulatory cytokines is elevated endogenously after sublethal gamma irradiation and is differentially enhanced by therapeutic administration of biologic response modifiers. J Immunol 153:2321–2330 [View Article][PubMed]
    [Google Scholar]
  21. Raza M. W., El Ahmer O. R., Ogilvie M. M., Blackwell C. C., Saadi A. T., Elton R. A., Weir D. M. 1999; Infection with respiratory syncytial virus enhances expression of native receptors for non-pilate Neisseria meningitidis on HEp-2 cells. FEMS Immunol Med Microbiol 23:115–124 [View Article][PubMed]
    [Google Scholar]
  22. Tamai R., Sakuta T., Matsushita K., Torii M., Takeuchi O., Akira S., Akashi S., Espevik T., Sugawara S., Takada H. 2002; Human gingival CD14+ fibroblasts primed with gamma interferon increase production of interleukin-8 in response to lipopolysaccharide through up-regulation of membrane CD14 and MyD88 mRNA expression. Infect Immun 70:1272–1278 [View Article][PubMed]
    [Google Scholar]
  23. Tamai R., Sugawara S., Takeuchi O., Akira S., Takada H. 2003; Synergistic effects of lipopolysaccharide and interferon-γ in inducing interleukin-8 production in human monocytic THP-1 cells is accompanied by up-regulation of CD14, Toll-like receptor 4, MD-2 and MyD88 expression. J Endotoxin Res 9:145–153[PubMed]
    [Google Scholar]
  24. Tapping R. I., Tobias P. S. 2000; Soluble CD14-mediated cellular responses to lipopolysaccharide. Chem Immunol 74:108–121 [View Article][PubMed]
    [Google Scholar]
  25. Ulevitch R. J., Tobias P. S. 1999; Recognition of Gram-negative bacteria and endotoxin by the innate immune system. Curr Opin Immunol 11:19–22 [View Article][PubMed]
    [Google Scholar]
  26. Van Gucht S., van Reeth K., Pensaert M. 2003; Interaction between porcine reproductive-respiratory syndrome virus and bacterial endotoxin in the lungs of pigs: potentiation of cytokine production and respiratory disease. J Clin Microbiol 41:960–966 [View Article][PubMed]
    [Google Scholar]
  27. Van Gucht S., Labarque G., Van Reeth K. 2004; The combination of PRRS virus and bacterial endotoxin as a model for multifactorial respiratory disease in pigs. Vet Immunol Immunopathol 102:165–178 [View Article][PubMed]
    [Google Scholar]
  28. Van Gucht S., Van Reeth K., Nauwynck H., Pensaert M. 2005; Porcine reproductive and respiratory syndrome virus infection increases CD14 expression and lipopolysaccharide-binding protein in the lungs of pigs. Viral Immunol 18:116–126 [View Article][PubMed]
    [Google Scholar]
  29. Virchow J. C. Jr, Julius P., Matthys H., Kroegel C., Luttmann W. 1998; CD14 expression and soluble CD14 after segmental allergen provocation in atopic asthma. Eur Respir J 11:317–323 [View Article][PubMed]
    [Google Scholar]
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