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The Role of Interleukin-10 During Systemic Inflammation and Bacterial Infection

  • F. N. Lauw
  • S. J. H. van Deventer
  • T. van der Poll

Abstract

Sepsis is a clinical syndrome that results from a systemic response of the host to an infection. Activation of several host inflammatory mediator systems, including the cytokine network, is considered to play an important role in the pathogenesis of sepsis. Cytokines are a family of small proteins which function in a complex network in which they can influence each other’s production and activity. Pro-inflammatory cytokines, of which tumour necrosis factor-α(TNF) and interleukin-1 (IL-1) are studied most extensively, stimulate inflammatory processes and facilitate the immune response against invading pathogens. However, excessive systemic release of pro-inflammatory cytokines during sepsis syndrome has been found to contribute to the development of tissue damage. The production of these pro-inflammatory cytokines can be inhibited by so-called anti-inflammatory cytokines. The prototype of this group of mediators is IL-10. In this article we will discuss the role of IL-10 in the pathogenesis of sepsis and severe bacterial infections.

Keywords

Major Histocompatibility Complex Systemic Inflammation Staphylococcal Enterotoxin Severe Bacterial Infection Clinical Sepsis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse helper T cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th 1 clones. J Exp Med 170: 2081–2095PubMedCrossRefGoogle Scholar
  2. 2.
    Yssel H, De Waal Malefyt R, Roncarolo MG, et al (1992) IL-10 is produced by subsets of human CD4+ T cell clones and peripheral blood T cells. J Immunol 149: 2378–2384PubMedGoogle Scholar
  3. 3.
    Moore KW,, de Waal Malefyt R, Coffman RL et al (2001) Interleukin-10 and the Interleukin-10 receptor. Annu Rev Immunol 19: 683–765PubMedCrossRefGoogle Scholar
  4. 4.
    Marchant A, Deviere J, Byl B, et al (1994) Interleukin-10 production during septicaemia. Lancet 434: 707–708CrossRefGoogle Scholar
  5. 5.
    Derkx B, Marchant A, Goldman M, et al (1995) High levels of interleukin-10 during the initial phase of fulminant meningococcal septic shock. J Infect Dis 171: 229–232PubMedCrossRefGoogle Scholar
  6. 6.
    van der Poll T,, de Waal Malefyt R, Coyle SM et al (1997) Antiinflammatory cytokine responses during clinical sepsis and experimental endotoxemia: sequential measurements of plasma soluble interleukin-1 (IL)-1 receptor type II, IL-10 and IL-13 concentrations. J Infect Dis 175: 118–122PubMedCrossRefGoogle Scholar
  7. 7.
    Friedman G, Jankowski S, Marchant A, et al (1997) Blood interleukin-10 levels parallel the severity of septic shock. J Crit Care 12: 183–187PubMedCrossRefGoogle Scholar
  8. 8.
    van der Poll T, van Deventer SJH (1999) Endotoxemia in healthy subjects as a human model of inflammation. In: Cohen J, Marshall J (ed) The Immune Response in the Critically Ill:335–357Google Scholar
  9. 9.
    van der Poll T, Jansen J, Levi M, et al (1994) Regulation of interleukin 10 release by tumor necrosis factor in humans and chimpanzees. J Exp Med 180: 1985–1988PubMedCrossRefGoogle Scholar
  10. 10.
    van der Poll T, Coyle SM, Barbosa K, et al (1996) Epinephrine inhibits tumor necrosis factor-alpha and potentiates interleukin-10 production during human endotoxemia. J Clin Invest 97: 713–719PubMedCrossRefGoogle Scholar
  11. 11.
    van der Poll T, Barber AE, Coyle SM, et al (1996) Hypercortisolemia increases plasma interleukin-10 concentrations during human endotoxemia clinical research center study. J Clin Endocrin Metab 81: 3604–3606CrossRefGoogle Scholar
  12. 12.
    van der Pouw Kraan TCTM, Boeije LCM, Smeenk RJT, et al (1995) Prostaglandin-E2 is a potent inhibitor of human interleukin-12 production. J Exp Med 181: 775–779PubMedCrossRefGoogle Scholar
  13. 13.
    de Waal Malefyt R, Abrams J, Bennett B, et al (1991) Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174: 1209–1220PubMedCrossRefGoogle Scholar
  14. 14.
    D. Andrea A, Aste-Amezaga M, Valiante NM, et al (1993) Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041–1048PubMedCrossRefGoogle Scholar
  15. 15.
    de Waal Malefyt R, Haanen J, Spits H, et al (1991) Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 174: 915–924PubMedCrossRefGoogle Scholar
  16. 16.
    Willems F, Marchant A, Delville JP, et al (1994) Interleukin-10 inhibits B7 and intracellular adhesion molecule-1 expression on human monocytes. Eur J Immunol 24: 1007–1009PubMedCrossRefGoogle Scholar
  17. 17.
    Pradier O, Gérard C, Delvaux A, et al (1993) Interleukin-10 inhibits the induction of monocyte procoagulant activity by bacterial lipopolysaccharide. Eur J Immunol 23: 2700–2703PubMedCrossRefGoogle Scholar
  18. 18.
    Gazzinelli RT, Oswald IP, James SL, et al (1992) IL-10 inhibits parasite killing and nitrogen oxide production by IFN-g activated macrophages. J Immunol 148: 1792–1796PubMedGoogle Scholar
  19. 19.
    Gerard C, Bruyns C, Marchant A, et al (1993) Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J Exp Med 177: 547–550PubMedCrossRefGoogle Scholar
  20. 20.
    Howard M, Muchamuel T, Andrade S, et al (1993) Interleukin 10 protects mice from lethal endotoxemia. J Exp Med 177: 1205–1208PubMedCrossRefGoogle Scholar
  21. 21.
    Pajkrt D, Camoglio L, Tiel-van Buul MC, et al (1997) Attenuation of proinflammatory response by recombinant human IL-10 in human endotoxemia: effect of timing of recombinant human IL-10 administration. J Immunol 158: 3971–3977PubMedGoogle Scholar
  22. 22.
    Pajkrt D, van der Poll T, Levi M, et al (1997) Interleukin-10 inhibits activation of coagulation and fibrinolysis during human endotoxemia. Blood 89: 2701–2705PubMedGoogle Scholar
  23. 23.
    Groux H, Bigler M,, de Vries JE et al (1998) Inhibitory and stimulatory effects of IL-10 on human CD8+ T cells. J Immunol 160: 3188–3193PubMedGoogle Scholar
  24. 24.
    Shibata Y, Foster LA, Kurimoto M, et al (1998) Immunoregulatory roles of IL-10 in innate immunity: IL-10 inhibits macrophage production of IFN-gamma-inducing factors but enhances NK cell production of IFN-gamma. J Immunol 161: 4283–4288PubMedGoogle Scholar
  25. 25.
    Lauw FN, Pajkrt D, Hack CE, et al (2000) Proinflammatory effects of IL-10 during human endotoxemia. J Immunol 165: 2783–2789PubMedGoogle Scholar
  26. 26.
    Marchant A, Bniyns C, Vandenabeele P, et al (1994) IL-10 controls IFN-? and TNF production during experimental endotoxemia. Eur J Immunol 24: 1167–1171PubMedCrossRefGoogle Scholar
  27. 27.
    Standiford TJ, Strieter RM, Lukacs NW, et al (1995) Neutralization of IL- 1rfincreases lethality in endotoxemia. Cooperative effects of macrophage inflammatory protein-2 and tumor necrosis factor. J Immunol 155Google Scholar
  28. 28.
    Berg DJ, Kühn R, Rajewsky K, et al (1995) Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Schwartzman reaction but not endotoxin tolerance. J CLin Invest 96: 2339–2347PubMedCrossRefGoogle Scholar
  29. 29.
    Florquin S, Amraoui Z, Abramowicz D, et al (1994) Systemic release and protective role of IL-10 in staphylococcal enterotoxin B-induced shock in mice. J Immunol 153: 2618–2623PubMedGoogle Scholar
  30. 30.
    Hasko G, Virag L, Egnaczyk G, et al (1998) The crucial role of IL-10 in the suppression of the immunological response in mice exposed to enterotoxin B. Eur J Immunol 28: 1417–1425PubMedCrossRefGoogle Scholar
  31. 31.
    Greenberger MJ, Strieter RM, Kunkel SL, et al (1995) Neutralization of IL-10 increases survival in a murine model of Klebsiella pneumonia. J Immunol 55: 722–729Google Scholar
  32. 32.
    van der Poll T, Marchant A, Keogh CV, et al (1996) Interleukin-10 impairs host defense in murine pneumococcal pneumonia. J Infect Dis 174: 994–1000PubMedCrossRefGoogle Scholar
  33. 33.
    Sewnath ME, Olszyna DP, Birjmohun R, et al (2001) IL-10-deficient mice demonstrate multiple organ failure and increased mortality during Escherichia coli peritonitis despite an accelerated bacterial clearence. J Immunol 166: 6323–6331PubMedGoogle Scholar

Copyright information

© Springer-Verlag Italia, Milano 2002

Authors and Affiliations

  • F. N. Lauw
  • S. J. H. van Deventer
  • T. van der Poll

There are no affiliations available

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