1887

Journal of General Virology header logo

Volume 92, Issue 2

Lipopolysaccharide stress induces cell-type specific production of murine leukemia virus type-endogenous retroviral virions in primary lymphoid cells Free

Abstract

Some murine-endogenous retroviruses, making up ∼10 % of the mouse genome, are induced during the course of experimental sepsis in which lipopolysaccharide (LPS), a pathogenic component of Gram-negative bacteria, often plays a critical role. In this study, we investigated whether LPS stress induces the production of murine leukemia virus type-endogenous retrovirus (MuLV-ERV) virions in primary lymphoid cells. LPS treatment of cells (single-cell suspensions and sorted B- and T-cells) isolated from seven lymphoid organs of C57BL/6J mice resulted in a differential increase in the production of MuLV-ERV virions in most cells examined. Interestingly, among the 34 unique MuLV-ERV U3 sequences cloned from the viral genomic RNAs, the nuclear respiratory factor 1 (transcription factor) element was present only in the 20 U3 sequences that were derived from the LPS-induced MuLV-ERV U3 bands. Using the U3 sequences as a probe, 55 putative MuLV-ERV loci were mapped onto the C57BL/6J mouse genome and 15 of them retained full coding potential. Furthermore, one full-length recombinant MuLV-ERV originating from a locus on chromosome 13 was determined to be responsive to LPS stress. The findings from this study suggest that LPS stress differentially activates MuLV-ERV virion production in lymphoid organs in a cell type- and MuLV-ERV-specific manner. Further investigation is needed to define the role of MuLV-ERVs in the LPS signalling pathway(s) in general, as well as in the pathogenesis of sepsis.

  • Received:
  • Accepted:
  • Published Online:
© SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.023416-0
2011-02-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/2/292.html?itemId=/content/journal/jgv/10.1099/vir.0.023416-0&mimeType=html&fmt=ahah

References

  1. Alexander, C. & Rietschel, E. T.(2001). Bacterial lipopolysaccharides and innate immunity. J Endotoxin Res 7, 167–202. [Google Scholar]
  2. Andersson, J., Coutinho, A. & Melchers, F.(1977). Frequencies of mitogen-reactive B cells in the mouse. I. Distribution in different lymphoid organs from different inbred strains of mice at different ages. J Exp Med 145, 1511–1519.[CrossRef] [Google Scholar]
  3. Boeke, J. D. & Stoye, J. P.(1997). Retrotransposons, endogenous retroviruses, and the evolution of retroelements. In Retroviruses, pp. 343–435. Edited by Coffin, J. M., Hughes, S. H. & Varmus, H. E.. Cold Spring Harbor, NY. : Cold Spring Harbor Laboratory Press. [Google Scholar]
  4. Chaby, R. & Girard, R.(1993). Interaction of lipopolysaccharides with cells of immunological interest. Eur Cytokine Netw 4, 399–414. [Google Scholar]
  5. Cho, K., Zipkin, R. I., Adamson, L. K., McMurtry, A. L., Griffey, S. M. & Greenhalgh, D. G.(2000). Differential regulation of c-jun expression in liver and lung of mice after thermal injury. Shock 14, 182–186.[CrossRef] [Google Scholar]
  6. Cho, K., Pham, T. N., Crivello, S. D., Jeong, J., Green, T. L. & Greenhalgh, D. G.(2004). Involvement of CD14 and Toll-like receptor 4 in the acute phase response of serum amyloid A proteins and serum amyloid P component in the liver after burn injury. Shock 21, 144–150. [Google Scholar]
  7. Cho, K., Lee, Y. K. & Greenhalgh, D. G.(2008). Endogenous retroviruses in systemic response to stress signals. Shock 30, 105–116.[CrossRef] [Google Scholar]
  8. Cho, K., Chiu, S., Lee, Y. K., Greenhalgh, D. & Nemzek, J.(2009). Experimental polymicrobial peritonitis-associated transcriptional regulation of murine endogenous retroviruses. Shock 32, 147–158.[CrossRef] [Google Scholar]
  9. Corcoran, L. M., Adams, J. M., Dunn, A. R. & Cory, S.(1984). Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion. Cell 37, 113–122.[CrossRef] [Google Scholar]
  10. Dhar, S. S., Ongwijitwat, S. & Wong-Riley, M. T.(2008). Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J Biol Chem 283, 3120–3129.[CrossRef] [Google Scholar]
  11. Dolei, A.(2005). MSRV/HERV-W/syncytin and its linkage to multiple sclerosis: the usability and the hazard of a human endogenous retrovirus. J Neurovirol 11, 232–235.[CrossRef] [Google Scholar]
  12. Evans, M. J. & Scarpulla, R. C.(1990). NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev 4, 1023–1034.[CrossRef] [Google Scholar]
  13. Frankel, W. N., Stoye, J. P., Taylor, B. A. & Coffin, J. M.(1990). A linkage map of endogenous murine leukemia proviruses. Genetics 124, 221–236. [Google Scholar]
  14. Griffiths, D. J.(2001). Endogenous retroviruses in the human genome sequence. Genome Biol 2, reviews1017–reviews1017.5. [Google Scholar]
  15. Harada, F., Peters, G. G. & Dahlberg, J. E.(1979). The primer tRNA for Moloney murine leukemia virus DNA synthesis. Nucleotide sequence and aminoacylation of tRNAPro. J Biol Chem 254, 10979–10985. [Google Scholar]
  16. Hartley, J. W., Evans, L. H., Green, K. Y., Naghashfar, Z., Macias, A. R., Zerfas, P. M. & Ward, J. M.(2008). Expression of infectious murine leukemia viruses by RAW264.7 cells, a potential complication for studies with a widely used mouse macrophage cell line. Retrovirology 5, 1.[CrossRef] [Google Scholar]
  17. Herniou, E., Martin, J., Miller, K., Cook, J., Wilkinson, M. & Tristem, M.(1998). Retroviral diversity and distribution in vertebrates. J Virol 72, 5955–5966. [Google Scholar]
  18. Jern, P., Stoye, J. P. & Coffin, J. M.(2007). Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses. PLoS Genet 3, 2014–2022. [Google Scholar]
  19. Jongstra, J. & Moroni, C.(1981). Lipopolysaccharide induces retroviral antigen expression in 129/J mouse lymphocytes: evidence for assembly of a defective viral particle. J Virol 37, 1044–1050. [Google Scholar]
  20. Knerr, I., Huppertz, B., Weigel, C., Dotsch, J., Wich, C., Schild, R. L., Beckmann, M. W. & Rascher, W.(2004). Endogenous retroviral syncytin: compilation of experimental research on syncytin and its possible role in normal and disturbed human placentogenesis. Mol Hum Reprod 10, 581–588.[CrossRef] [Google Scholar]
  21. Kozak, C. A. & Rowe, W. P.(1980). Genetic mapping of xenotropic murine leukemia virus-inducing loci in five mouse strains. J Exp Med 152, 219–228.[CrossRef] [Google Scholar]
  22. Krieg, A. M., Khan, A. S. & Steinberg, A. D.(1988). Multiple endogenous xenotropic and mink cell focus-forming murine leukemia virus-related transcripts are induced by polyclonal immune activators. J Virol 62, 3545–3550. [Google Scholar]
  23. Kwon, D. N., Greenhalgh, D. G. & Cho, K.(2009). Cloning and characterization of endogenous retroviruses associated with postinjury stress signals in lymphoid tissues. Shock 32, 80–88.[CrossRef] [Google Scholar]
  24. Larsson, E. & Andersson, G.(1998). Beneficial role of human endogenous retroviruses: facts and hypotheses. Scand J Immunol 48, 329–338.[CrossRef] [Google Scholar]
  25. Lee, Y. K., Chew, A., Fitzsimon, L., Thomas, R., Greenhalgh, D. & Cho, K.(2007). Genome-wide changes in expression profile of murine endogenous retroviruses (MuERVs) in distant organs after burn injury. BMC Genomics 8, 440.[CrossRef] [Google Scholar]
  26. Lee, Y. K., Chew, A., Phan, H., Greenhalgh, D. G. & Cho, K.(2008). Genome-wide expression profiles of endogenous retroviruses in lymphoid tissues and their biological properties. Virology 373, 263–273.[CrossRef] [Google Scholar]
  27. Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H., Racie, L., LaVallie, E., Tang, X. Y., Edouard, P. & other authors(2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785–789.[CrossRef] [Google Scholar]
  28. Morrison, D. C. & Ulevitch, R. J.(1978). The effects of bacterial endotoxins on host mediation systems. A review. Am J Pathol 93, 526–618. [Google Scholar]
  29. Neviere, R. R., Cepinskas, G., Madorin, W. S., Hoque, N., Karmazyn, M., Sibbald, W. J. & Kvietys, P. R.(1999). LPS pretreatment ameliorates peritonitis-induced myocardial inflammation and dysfunction: role of myocytes. Am J Physiol 277, H885–H892. [Google Scholar]
  30. Nikbakht, K. N., Ou, C. Y., Boone, L. R., Glover, P. L. & Yang, W. K.(1985). Nucleotide sequence analysis of endogenous murine leukemia virus-related proviral clones reveals primer-binding sites for glutamine tRNA. J Virol 54, 889–893. [Google Scholar]
  31. O'Neill, L. A.(2003). Therapeutic targeting of Toll-like receptors for inflammatory and infectious diseases. Curr Opin Pharmacol 3, 396–403.[CrossRef] [Google Scholar]
  32. Phillips, S. M., Stephenson, J. R., Greenberger, J. S., Lane, P. E. & Aaronson, S. A.(1976). Release of xenotropic type C RNA virus in response to lipopolysaccharide: activity of lipid-A portion upon B lymphocytes. J Immunol 116, 1123–1128. [Google Scholar]
  33. Quandt, K., Frech, K., Karas, H., Wingender, E. & Werner, T.(1995). MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23, 4878–4884.[CrossRef] [Google Scholar]
  34. Scarpulla, R. C.(1997). Nuclear control of respiratory chain expression in mammalian cells. J Bioenerg Biomembr 29, 109–119.[CrossRef] [Google Scholar]
  35. Schwacha, M. G.(2003). Macrophages and post-burn immune dysfunction. Burns 29, 1–14.[CrossRef] [Google Scholar]
  36. Selten, G., Cuypers, H. T. & Berns, A.(1985). Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J 4, 1793–1798. [Google Scholar]
  37. Shinnick, T. M., Lerner, R. A. & Sutcliffe, J. G.(1981). Nucleotide sequence of Moloney murine leukaemia virus. Nature 293, 543–548.[CrossRef] [Google Scholar]
  38. Skalet, A. H., Isler, J. A., King, L. B., Harding, H. P., Ron, D. & Monroe, J. G.(2005). Rapid B cell receptor-induced unfolded protein response in nonsecretory B cells correlates with pro- versus antiapoptotic cell fate. J Biol Chem 280, 39762–39771.[CrossRef] [Google Scholar]
  39. Stoye, J. P. & Coffin, J. M.(1987). The four classes of endogenous murine leukemia virus: structural relationships and potential for recombination. J Virol 61, 2659–2669. [Google Scholar]
  40. Sverdlov, E. D.(2000). Retroviruses and primate evolution. Bioessays 22, 161–171.[CrossRef] [Google Scholar]
  41. Tokusumi, Y., Zhou, S. & Takada, S.(2004). Nuclear respiratory factor 1 plays an essential role in transcriptional initiation from the hepatitis B virus x gene promoter. J Virol 78, 10856–10864.[CrossRef] [Google Scholar]
  42. Tomonaga, K. & Coffin, J. M.(1998). Structure and distribution of endogenous nonecotropic murine leukemia viruses in wild mice. J Virol 72, 8289–8300. [Google Scholar]
  43. Tomonaga, K. & Coffin, J. M.(1999). Structures of endogenous nonecotropic murine leukemia virus (MLV) long terminal repeats in wild mice: implication for evolution of MLVs. J Virol 73, 4327–4340. [Google Scholar]
  44. Tristem, M.(2000). Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database. J Virol 74, 3715–3730.[CrossRef] [Google Scholar]
  45. Trusko, S. P., Hoffman, E. K. & George, D. L.(1989). Transcriptional activation of cKi-ras proto-oncogene resulting from retroviral promoter insertion. Nucleic Acids Res 17, 9259–9265.[CrossRef] [Google Scholar]
  46. Urisman, A., Molinaro, R. J., Fischer, N., Plummer, S. J., Casey, G., Klein, E. A., Malathi, K., Magi-Galluzzi, C., Tubbs, R. R. & other authors(2006). Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog 2, e25.[CrossRef] [Google Scholar]
  47. Verstrepen, L., Adib-Conquy, M., Kreike, M., Carpentier, I., Adrie, C., Cavaillon, J. M. & Beyaert, R.(2008). Expression of the NF-κB inhibitor ABIN-3 in response to TNF and Toll-like receptor 4 stimulation is itself regulated by NF-κB. J Cell Mol Med 12, 316–329. [Google Scholar]
  48. Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M. & other authors(2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562.[CrossRef] [Google Scholar]
  49. Wells, C. A., Ravasi, T., Faulkner, G. J., Carninci, P., Okazaki, Y., Hayashizaki, Y., Sweet, M., Wainwright, B. J. & Hume, D. A.(2003). Genetic control of the innate immune response. BMC Immunol 4, 5.[CrossRef] [Google Scholar]
  50. Yang, Y., Tung, J. W., Ghosn, E. E. & Herzenberg, L. A.(2007). Division and differentiation of natural antibody-producing cells in mouse spleen. Proc Natl Acad Sci U S A 104, 4542–4546.[CrossRef] [Google Scholar]
  51. Yee, J. K., Friedmann, T. & Burns, J. C.(1994). Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 43, 99–112. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.023416-0
Loading
Lipopolysaccharide stress induces cell-type specific production of murine leukemia virus type-endogenous retroviral virions in primary lymphoid cells
J. Gen. Virol. 92, 292 (2011); https://doi.org/10.1099/vir.0.023416-0
/content/journal/jgv/10.1099/vir.0.023416-0
/content/journal/jgv/10.1099/vir.0.023416-0
Loading

Data & Media loading...

Supplements

[ PDF file containing Supplementary Figs S1 and S3 and Supplementary Tables S1–S3.] (3.65 MB) [ PDF file containing Supplementary Fig. S2.] (485 KB)

PDF

[ PDF file containing Supplementary Figs S1 and S3 and Supplementary Tables S1–S3.] (3.65 MB) [ PDF file containing Supplementary Fig. S2.] (485 KB)

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error