Skip to main content
Log in

Bacterial lipopolysaccharide activates CD57-negative human NK cells

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

NK cells play an important regulatory role in sepsis by induction and augmentation of proinflammatory reactions in early stages of the septic process and by suppression of immune response in later stages of inflammation. The present work was aimed at the effect of bacterial lipopolysaccharide (LPS), the main pathogenic factor of sepsis development, on human NK cells ex vivo. We show that LPS activates immature CD57-negative NK cells, which typically constitute less than half of the normal NK cell population in human peripheral blood. Under conditions of NK cell stimulation with IL-2, addition of LPS provokes an increase in IFN-γ production. However, LPS both increased and inhibited NK cell cytotoxic activity. It is important to note that the activation of NK cells on LPS addition was observed in the absence of TLR4 on the NK cell surface. These results confirm our previous data arguing for a direct interaction of LPS with NK cells and evidence an atypical mechanism of LPS-induced NK cell activation without the involvement of surface TLR4.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Yarilin, A. A. (2010) Immunology [in Russian], GEOTAR-Media, Moscow.

    Google Scholar 

  2. Thale, C., and Kiderlen, A. F. (2005) Sources of interferon-gamma (IFN-gamma) in early immune response to Listeria monocytogenes, Immunobiology, 210, 673–683.

    Article  PubMed  Google Scholar 

  3. Artavanis-Tsakonas, K., and Riley, E. M. (2002) Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes, J. Immunol., 169, 2956–2963.

    Article  CAS  PubMed  Google Scholar 

  4. Abakushina, E. V., Kuzmina, E. G., and Kovalenko, E. I. (2012) The main properties and functions of human NK cells, Immunologiya, 4, 220–225.

    Google Scholar 

  5. Chiche, L., Forel, J. M., Thomas, G., Farnarier, C., Vely, F., Blery, M., Papazian, L., and Vivier, E. (2011) The role of natural killer cells in sepsis, J. Biomed. Biotechnol., 2011, 986491.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Emoto, M., Miyamoto, M., Yoshizawa, I., Emoto, Y., Schaible, U. E., Kita, E., and Kaufmann, S. H. (2002) Critical role of NK cells rather than V alpha 14(+)NKT cells in lipopolysaccharide-induced lethal shock in mice, J. Immunol., 169, 1426–1432.

    Article  CAS  PubMed  Google Scholar 

  7. Cooper, M. A., Fehniger, T. A., Fuchs, A., Colonna, M., and Caligiuri, M. A. (2004) NK cell and DC interactions, Trends Immunol., 25, 47–52.

    Article  CAS  PubMed  Google Scholar 

  8. Gerosa, F., Baldani-Guerra, B., Nisii, C., Marchesini, V., Carra, G., and Trinchieri, G. (2002) Reciprocal activating interaction between natural killer cells and dendritic cells, J. Exp. Med., 195, 327–333.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Goodier, M. R., and Londei, M. (2000) Lipopolysaccharide stimulates the proliferation of human CD56+CD3-NK cells: a regulatory role of monocytes and IL-10, J. Immunol., 165, 139–147.

    Article  CAS  PubMed  Google Scholar 

  10. Godshall, C. J., Scott, M. J., Burch, P. T., Peyton, J. C., and Cheadle, W. G. (2003) Natural killer cells participate in bacterial clearance during septic peritonitis through interactions with macrophages, Shock, 19, 144–149.

    Article  PubMed  Google Scholar 

  11. Tu, Z., Bozorgzadeh, A., Pierce, R. H., Kurtis, J., Crispe, I. N., and Orloff, M. S. (2008) TLR-dependent cross talk between human Kupffer cells and NK cells, J. Exp. Med., 205, 233–244.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Chalifour, A., Jeannin, P., Gauchat, J. F., Blaecke, A., Malissard, M., N’Guyen, T., Thieblemont, N., and Delneste, Y. (2004) Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers α-defensin production, Blood, 104, 1778–1783.

    Article  CAS  PubMed  Google Scholar 

  13. Lauzon, N. M., Mian, F., MacKenzie, R., and Ashkar, A. A. (2006) The direct effects of Toll-like receptor ligands on human NK cell cytokine production and cytotoxicity, Cell Immunol., 241, 102–112.

    Article  CAS  PubMed  Google Scholar 

  14. Saikh, K. U., Lee, J. S., Kissner, T. L., Dyas, B., and Ulrich, R. G. (2003) Toll-like receptor and cytokine expression patterns of CD56+ T cells are similar to natural killer cells in response to infection with Venezuelan equine encephalitis virus replicons, J. Infect. Dis., 188, 1562–1570.

    Article  CAS  PubMed  Google Scholar 

  15. Mian, M. F., Lauzon, N. M., Andrews, D. W., Lichty, B. D., and Ashkar, A. A. (2010) FimH can directly activate human and murine natural killer cells via TLR4, Mol. Ther., 18, 1379–1388.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. O’Connor, G. M., Hart, O. M., and Gardiner, C. M. (2005) Putting the natural killer cells in its place, Immunology, 117, 1–10.

    Article  Google Scholar 

  17. Souza-Fonseca-Guimaraes, F., Parlato, M., Philippart, F., Misset, B., Cavaillon, J. M., and Adib-Conquy, M. (2012) Toll-like receptors expression and interferon-γ production by NK cells in human sepsis, Crit. Care, 16, R206.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Tadema, H., Abdulahad, W. H., Stegeman, C. A., Kallenberg, C. G., and Heeringa, P. (2011) Increased expression of Toll-like receptors by monocytes and natural killer cells in ANCA-associated vasculitis, PLoS One, 6, e24315.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Kanevskiy, L. M., Telford, W. G., Sapozhnikov, A. M., and Kovalenko, E. I. (2013) Lipopolysaccharide induces IFN-γ production in human NK cells, Front. Immunol., 4, 11.

    Article  PubMed Central  PubMed  Google Scholar 

  20. Shibata, T., Motoi, Y., Tanimura, N., Yamakawa, N., Akashi-Takamura, S., and Miyake, K. (2011) Intracellular TLR4/MD-2 in macrophages senses Gram-negative bacteria and induces a unique set of LPS-dependent genes, Int. Immunol., 23, 503–510.

    Article  CAS  PubMed  Google Scholar 

  21. Hornef, M. W., Normark, B. H., Vandewalle, A., and Normark, S. (2003) Intracellular recognition of lipopolysaccharide by Toll-like receptor 4 in intestinal epithelial cells, J. Exp. Med., 198, 1225–1235.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Abo, T., and Balch, C. M. (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1), J. Immunol., 127, 1024–1029.

    CAS  PubMed  Google Scholar 

  23. Luetke-Eversloh, M., Killig, M., and Romagnani, C. (2013) Signatures of human NK cell development and terminal differentiation, Front. Immunol., 4, 499.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Cavaillon, J. M., and Adib-Conquy, M. (2006) Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis, Crit. Care, 10, 233.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E., and Caligiuri, M. A. (2001) Human natural killer cells: a unique innate immunoregulatory role for the CD56 (bright) subset, Blood, 97, 3146–3151.

    Article  CAS  PubMed  Google Scholar 

  26. Voshol, H., van Zuylen, C. W., Orberger, G., Vliegenthart, J. F., and Schachner, M. (1996) Structure of the HNK-1 carbohydrate epitope on bovine peripheral myelin glycoprotein P0, J. Biol. Chem., 271, 22957–22960.

    Article  CAS  PubMed  Google Scholar 

  27. Nielsen, C. M., White, M. J., Goodier, M. R., and Riley, E. M. (2013) Functional significance of CD57 expression on human NK cells and relevance to disease, Front. Immunol., 4, 422.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Lopez-Verges, S., Milush, J. M., Pandey, S., York, V. A., Arakawa-Hoyt, J., Pircher, H., Norris, P. J., Nixon, D. F., and Lanier, L. L. (2010) CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK cell subset, Blood, 116, 3865–3874.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Gayoso, I., Sanchez-Correa, B., Campos, C., Alonso, C., Pera, A., Casado, J. G., Morgado, S., Tarazona, R., and Solana, R. (2011) Immunosenescence of human natural killer cells, J. Innate Immun., 3, 337–343.

    Article  CAS  PubMed  Google Scholar 

  30. Kovalenko, E. I., Abakushina, E. V., Telford, W., Kapoor, V., Korchagina, E. Yu., Khaidukov, S. V., Molotkovskaya, I. M., Sapozhnikov, A. M., Vlaskin, P. A., and Bovin, N. V. (2007) Clustered carbohydrates as a target for natural killer cells: a model system, Histochem. Cell. Biol., 127, 313–326.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. I. Kovalenko.

Additional information

Published in Russian in Biokhimiya, 2014, Vol. 79, No. 12, pp. 1636–1647.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanevskiy, L.M., Erokhina, S.A., Streltsova, M.A. et al. Bacterial lipopolysaccharide activates CD57-negative human NK cells. Biochemistry Moscow 79, 1339–1348 (2014). https://doi.org/10.1134/S0006297914120074

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297914120074

Key words

Navigation