Production of interleukin-10 and transforming growth factor beta by peripheral blood mononuclear cells in Q fever endocarditis (original) (raw)

Abstract

The pathophysiology of Q fever endocarditis is characterized by the suppression of antigen-specific cell-mediated immune responses. We investigated the production of interleukin-10 (IL-10) and transforming growth factor beta (TGF-beta), known to interfere with the development of protective cell immunity. IL-10 was markedly released by unstimulated peripheral blood mononuclear cells (PBMC) from patients with Q fever endocarditis. This release resulted from the upregulation of IL-10 gene transcription. Similarly, the release of TGF-beta1 and TGF-beta2 was significantly higher in patient PBMC than in control cells, but the expression of their respective mRNA was not enhanced in patient cells. In contrast, lipopolysaccharide-stimulated transcription and release of IL-10 and TGF-beta were similar in patients and controls. The release of IL-10 by PBMC but not that of TGF-beta was correlated with the clinical status of the patients. First, IL-10 production was correlated with specific antibody levels. Second, IL-10 release remained elevated in patients prone to relapse. Taken together, our results suggest that the release of IL-10 and TGF-beta is upregulated in Q fever endocarditis. IL-10 might be considered as a marker of disease relapses and might be instrumental in monitoring the efficiency of the treatment.

Full Text

The Full Text of this article is available as a PDF (229.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Assoian R. K., Fleurdelys B. E., Stevenson H. C., Miller P. J., Madtes D. K., Raines E. W., Ross R., Sporn M. B. Expression and secretion of type beta transforming growth factor by activated human macrophages. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6020–6024. doi: 10.1073/pnas.84.17.6020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brouqui P., Dupont H. T., Drancourt M., Berland Y., Etienne J., Leport C., Goldstein F., Massip P., Micoud M., Bertrand A. Chronic Q fever. Ninety-two cases from France, including 27 cases without endocarditis. Arch Intern Med. 1993 Mar 8;153(5):642–648. doi: 10.1001/archinte.153.5.642. [DOI] [PubMed] [Google Scholar]
  3. Capo C., Zugun F., Stein A., Tardei G., Lepidi H., Raoult D., Mege J. L. Upregulation of tumor necrosis factor alpha and interleukin-1 beta in Q fever endocarditis. Infect Immun. 1996 May;64(5):1638–1642. doi: 10.1128/iai.64.5.1638-1642.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dahl K. E., Shiratsuchi H., Hamilton B. D., Ellner J. J., Toossi Z. Selective induction of transforming growth factor beta in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect Immun. 1996 Feb;64(2):399–405. doi: 10.1128/iai.64.2.399-405.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dupont H. T., Thirion X., Raoult D. Q fever serology: cutoff determination for microimmunofluorescence. Clin Diagn Lab Immunol. 1994 Mar;1(2):189–196. doi: 10.1128/cdli.1.2.189-196.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hirsch C. S., Yoneda T., Averill L., Ellner J. J., Toossi Z. Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-beta 1. J Infect Dis. 1994 Nov;170(5):1229–1237. doi: 10.1093/infdis/170.5.1229. [DOI] [PubMed] [Google Scholar]
  7. Izzo A. A., Marmion B. P. Variation in interferon-gamma responses to Coxiella burnetii antigens with lymphocytes from vaccinated or naturally infected subjects. Clin Exp Immunol. 1993 Dec;94(3):507–515. doi: 10.1111/j.1365-2249.1993.tb08226.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Koster F. T., Williams J. C., Goodwin J. S. Cellular immunity in Q fever: modulation of responsiveness by a suppressor T cell-monocyte circuit. J Immunol. 1985 Aug;135(2):1067–1072. [PubMed] [Google Scholar]
  9. Koster F. T., Williams J. C., Goodwin J. S. Cellular immunity in Q fever: specific lymphocyte unresponsiveness in Q fever endocarditis. J Infect Dis. 1985 Dec;152(6):1283–1289. doi: 10.1093/infdis/152.6.1283. [DOI] [PubMed] [Google Scholar]
  10. Krishnan L., Guilbert L. J., Russell A. S., Wegmann T. G., Mosmann T. R., Belosevic M. Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. J Immunol. 1996 Jan 15;156(2):644–652. [PubMed] [Google Scholar]
  11. Lonnemann G., Behme T. C., Lenzner B., Floege J., Schulze M., Colton C. K., Koch K. M., Shaldon S. Permeability of dialyzer membranes to TNF alpha-inducing substances derived from water bacteria. Kidney Int. 1992 Jul;42(1):61–68. doi: 10.1038/ki.1992.261. [DOI] [PubMed] [Google Scholar]
  12. Maeda H., Shiraishi A. TGF-beta contributes to the shift toward Th2-type responses through direct and IL-10-mediated pathways in tumor-bearing mice. J Immunol. 1996 Jan 1;156(1):73–78. [PubMed] [Google Scholar]
  13. Magnan A., Mege J. L., Escallier J. C., Brisse J., Capo C., Reynaud M., Thomas P., Meric B., Garbe L., Badier M. Balance between alveolar macrophage IL-6 and TGF-beta in lung-transplant recipients. Marseille and Montréal Lung Transplantation Group. Am J Respir Crit Care Med. 1996 Apr;153(4 Pt 1):1431–1436. doi: 10.1164/ajrccm.153.4.8616577. [DOI] [PubMed] [Google Scholar]
  14. Marchant A., Devière J., Byl B., De Groote D., Vincent J. L., Goldman M. Interleukin-10 production during septicaemia. Lancet. 1994 Mar 19;343(8899):707–708. doi: 10.1016/s0140-6736(94)91584-9. [DOI] [PubMed] [Google Scholar]
  15. Matsuoka M., Yoshida K., Maeda T., Usuda S., Sakano H. Switch circular DNA formed in cytokine-treated mouse splenocytes: evidence for intramolecular DNA deletion in immunoglobulin class switching. Cell. 1990 Jul 13;62(1):135–142. doi: 10.1016/0092-8674(90)90247-c. [DOI] [PubMed] [Google Scholar]
  16. Maurin M., Benoliel A. M., Bongrand P., Raoult D. Phagolysosomal alkalinization and the bactericidal effect of antibiotics: the Coxiella burnetii paradigm. J Infect Dis. 1992 Nov;166(5):1097–1102. doi: 10.1093/infdis/166.5.1097. [DOI] [PubMed] [Google Scholar]
  17. Meade R., Askenase P. W., Geba G. P., Neddermann K., Jacoby R. O., Pasternak R. D. Transforming growth factor-beta 1 inhibits murine immediate and delayed type hypersensitivity. J Immunol. 1992 Jul 15;149(2):521–528. [PubMed] [Google Scholar]
  18. Miller-Graziano C. L., Zhu D., Kodys K. Differential induction of human monocyte transforming growth factor beta 1 production and its regulation by interleukin 4. J Clin Immunol. 1994 Jan;14(1):61–72. doi: 10.1007/BF01541176. [DOI] [PubMed] [Google Scholar]
  19. Miossec P., Briolay J., Dechanet J., Wijdenes J., Martinez-Valdez H., Banchereau J. Inhibition of the production of proinflammatory cytokines and immunoglobulins by interleukin-4 in an ex vivo model of rheumatoid synovitis. Arthritis Rheum. 1992 Aug;35(8):874–883. doi: 10.1002/art.1780350805. [DOI] [PubMed] [Google Scholar]
  20. Moore K. W., O'Garra A., de Waal Malefyt R., Vieira P., Mosmann T. R. Interleukin-10. Annu Rev Immunol. 1993;11:165–190. doi: 10.1146/annurev.iy.11.040193.001121. [DOI] [PubMed] [Google Scholar]
  21. Mosmann T. R., Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today. 1996 Mar;17(3):138–146. doi: 10.1016/0167-5699(96)80606-2. [DOI] [PubMed] [Google Scholar]
  22. Racult D., Stein A. Q fever during pregnancy--a risk for women, fetuses, and obstetricians. N Engl J Med. 1994 Feb 3;330(5):371–371. doi: 10.1056/nejm199402033300518. [DOI] [PubMed] [Google Scholar]
  23. Raoult D. Host factors in the severity of Q fever. Ann N Y Acad Sci. 1990;590:33–38. doi: 10.1111/j.1749-6632.1990.tb42204.x. [DOI] [PubMed] [Google Scholar]
  24. Raoult D., Levy P. Y., Dupont H. T., Chicheportiche C., Tamalet C., Gastaut J. A., Salducci J. Q fever and HIV infection. AIDS. 1993 Jan;7(1):81–86. doi: 10.1097/00002030-199301000-00012. [DOI] [PubMed] [Google Scholar]
  25. Raoult D., Levy P. Y., Harlé J. R., Etienne J., Massip P., Goldstein F., Micoud M., Beytout J., Gallais H., Remy G. Chronic Q fever: diagnosis and follow-up. Ann N Y Acad Sci. 1990;590:51–60. doi: 10.1111/j.1749-6632.1990.tb42206.x. [DOI] [PubMed] [Google Scholar]
  26. Raoult D., Marrie T. Q fever. Clin Infect Dis. 1995 Mar;20(3):489–496. doi: 10.1093/clinids/20.3.489. [DOI] [PubMed] [Google Scholar]
  27. Raoult D. Treatment of Q fever. Antimicrob Agents Chemother. 1993 Sep;37(9):1733–1736. doi: 10.1128/aac.37.9.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raoult D., Vestris G., Enea M. Isolation of 16 strains of Coxiella burnetii from patients by using a sensitive centrifugation cell culture system and establishment of the strains in HEL cells. J Clin Microbiol. 1990 Nov;28(11):2482–2484. doi: 10.1128/jcm.28.11.2482-2484.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Reed S. G., Brownell C. E., Russo D. M., Silva J. S., Grabstein K. H., Morrissey P. J. IL-10 mediates susceptibility to Trypanosoma cruzi infection. J Immunol. 1994 Oct 1;153(7):3135–3140. [PubMed] [Google Scholar]
  30. Roman M. J., Coriz P. D., Baca O. G. A proposed model to explain persistent infection of host cells with Coxiella burnetii. J Gen Microbiol. 1986 May;132(5):1415–1422. doi: 10.1099/00221287-132-5-1415. [DOI] [PubMed] [Google Scholar]
  31. Sanguedolce M. V., Capo C., Bongrand P., Mege J. L. Zymosan-stimulated tumor necrosis factor-alpha production by human monocytes. Down-modulation by phorbol ester. J Immunol. 1992 Apr 1;148(7):2229–2236. [PubMed] [Google Scholar]
  32. Takashima T., Ueta C., Tsuyuguchi I., Kishimoto S. Production of tumor necrosis factor alpha by monocytes from patients with pulmonary tuberculosis. Infect Immun. 1990 Oct;58(10):3286–3292. doi: 10.1128/iai.58.10.3286-3292.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Toossi Z., Gogate P., Shiratsuchi H., Young T., Ellner J. J. Enhanced production of TGF-beta by blood monocytes from patients with active tuberculosis and presence of TGF-beta in tuberculous granulomatous lung lesions. J Immunol. 1995 Jan 1;154(1):465–473. [PubMed] [Google Scholar]
  34. Tripp C. S., Beckerman K. P., Unanue E. R. Immune complexes inhibit antimicrobial responses through interleukin-10 production. Effects in severe combined immunodeficient mice during Listeria infection. J Clin Invest. 1995 Apr;95(4):1628–1634. doi: 10.1172/JCI117837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wanidworanun C., Strober W. Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis. J Immunol. 1993 Dec 15;151(12):6853–6861. [PubMed] [Google Scholar]
  36. Warwick-Davies J., Lowrie D. B., Cole P. J. Selective deactivation of human monocyte functions by TGF-beta. J Immunol. 1995 Sep 15;155(6):3186–3193. [PubMed] [Google Scholar]
  37. Yamamura M., Uyemura K., Deans R. J., Weinberg K., Rea T. H., Bloom B. R., Modlin R. L. Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science. 1991 Oct 11;254(5029):277–279. doi: 10.1126/science.254.5029.277. [DOI] [PubMed] [Google Scholar]
  38. de Caestecker M. P., Bottomley M., Telfer B. A., Hutchinson I. V., Vose B. M., Ballardie F. W. Detection of abnormal peripheral blood mononuclear cell cytokine networks in human IgA nephropathy. Kidney Int. 1993 Dec;44(6):1298–1308. doi: 10.1038/ki.1993.382. [DOI] [PubMed] [Google Scholar]
  39. van der Poll T., Jansen J., Levi M., ten Cate H., ten Cate J. W., van Deventer S. J. Regulation of interleukin 10 release by tumor necrosis factor in humans and chimpanzees. J Exp Med. 1994 Nov 1;180(5):1985–1988. doi: 10.1084/jem.180.5.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]