DOI QR코드

DOI QR Code

Association between Elevated Pleural Interleukin-33 Levels and Tuberculous Pleurisy

  • Lee, Koung-Sun (Department of Laboratory Medicine, Wonkwang University School of Medicine) ;
  • Kim, Hak-Ryul (Department of Internal Medicine, Wonkwang University School of Medicine) ;
  • Kwak, Seongae (Department of Laboratory Medicine, Wonkwang University School of Medicine) ;
  • Choi, Keum-Ha (Department of Pathology, Wonkwang University School of Medicine) ;
  • Cho, Ji-Hyun (Department of Laboratory Medicine, Wonkwang University School of Medicine) ;
  • Lee, Young-Jin (Department of Laboratory Medicine, Wonkwang University School of Medicine) ;
  • Lee, Mi-Kyung (Department of Thoracic Surgery, Wonkwang University School of Medicine) ;
  • Lee, Jea-Hoon (Department of Otorhinolaryngology-Head and Neck Surgery, Wonkwang University School of Medicine) ;
  • Park, Seok-Don (Department of Dermatology, Wonkwang University School of Medicine) ;
  • Park, Do-Sim (Department of Laboratory Medicine, Wonkwang University School of Medicine)
  • Published : 2013.01.02

Abstract

Background: Interferon-${\gamma}$ (IFN-${\gamma}$) plays a crucial role in Mycobacterium tuberculosis induced pleural responses. Interleukin (IL)-33 up-regulates the production of IFN-${\gamma}$. We aimed to identify whether an association between pleural IL-33 levels and tuberculous pleurisy exists and determine its diagnostic value. Methods: Pleural IL-33, ST2 (a receptor of IL-33), adenosine deaminase (ADA), and IFN-${\gamma}$, as well as serum IL-33 and ST2 were measured in 220 patients with pleural effusions (PEs). Patients with malignant (MPEs), parapneumonic (PPEs), tuberculous (TPEs), and cardiogenic (CPEs) pleural effusions were included. Results: Pleural and serum IL-33 levels were highest or tended to be higher in patients with TPEs than in those with other types of PEs. The median pleural fluid-to-serum IL-33 ratio was higher in TPE cases (${\geq}0.91$) than in other PE cases (${\leq}0.56$). Pleural IL-33 levels correlated with those of pleural ADA and IFN-${\gamma}$. However, the diagnostic accuracies of pleural IL-33 (0.74) and pleural fluid-to-serum IL-33 ratio (0.75) were lower than that of ADA (0.95) or IFN-${\gamma}$ (0.97). Pleural ST2 levels in patients with MPEs were higher than in patients with TPEs. Serum ST2 levels did not differ among the groups. Conclusions: We identified an association between elevated pleural IL-33 levels and tuberculous pleurisy. However, we recommend conventional pleural markers (ADA or IFN-${\gamma}$) as diagnostic markers of TPE.

Keywords

References

  1. Caramori G, Lasagna L, Casalini AG, Adcock IM, Casolari P, Contoli M, et al. Immune response to Mycobacterium tuberculosis infection in the parietal pleura of patients with tuberculous pleurisy. PLoS One 2011;6: e22637. https://doi.org/10.1371/journal.pone.0022637
  2. Baumann MH, Nolan R, Petrini M, Lee YC, Light RW, Schneider E. Pleural tuberculosis in the United States: incidence and drug resistance. Chest 2007;131:1125-32. https://doi.org/10.1378/chest.06-2352
  3. Sahn SA. State of the art. The pleura. Am Rev Respir Dis 1988;138:184-234. https://doi.org/10.1164/ajrccm/138.1.184
  4. Sneller MC. Granuloma formation, implications for the pathogenesis of vasculitis. Cleve Clin J Med 2002;69(S2):S40-3.
  5. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM. Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog 2008;4:e1000239. https://doi.org/10.1371/journal.ppat.1000239
  6. Schierloh P, Yokobori N, Aleman M, Landoni V, Geffner L, Musella RM, et al. Mycobacterium tuberculosis-induced gamma interferon production by natural killer cells requires cross talk with antigen-presenting cells involving Toll-like receptors 2 and 4 and the mannose receptor in tuberculous pleurisy. Infect Immun 2007;75:5325-37. https://doi.org/10.1128/IAI.00381-07
  7. Feng CG, Kaviratne M, Rothfuchs AG, Cheever A, Hieny S, Young HA, et al. NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. J Immunol 2006;177:7086-93.
  8. Orme IM and Cooper AM. Cytokine/chemokine cascades in immunity to tuberculosis. Immunol Today 1999;20:307-12. https://doi.org/10.1016/S0167-5699(98)01438-8
  9. Pasquinelli V, Townsend JC, Jurado JO, Alvarez IB, Quiroga MF, Barnes PF, et al. IFN-gamma production during active tuberculosis is regulated by mechanisms that involve IL-17, SLAM, and CREB. J Infect Dis 2009; 199:661-5. https://doi.org/10.1086/596742
  10. Asano M, Nakane A, Minagawa T. Endogenous gamma interferon is essential in granuloma formation induced by glycolipid-containing mycolic acid in mice. Infect Immun 1993;61:2872-8.
  11. van Crevel R, Ottenhoff TH, van der Meer JW. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev 2002;15:294-309. https://doi.org/10.1128/CMR.15.2.294-309.2002
  12. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor- related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005;23:479-90. https://doi.org/10.1016/j.immuni.2005.09.015
  13. Bourgeois E, Van LP, Samson M, Diem S, Barra A, Roga S, et al. The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 2009;39:1046-55. https://doi.org/10.1002/eji.200838575
  14. Smith DE. IL-33: a tissue derived cytokine pathway involved in allergic inflammation and asthma. Clin Exp Allergy 2010;40:200-8. https://doi.org/10.1111/j.1365-2222.2009.03384.x
  15. Prefontaine D, Lajoie-Kadoch S, Foley S, Audusseau S, Olivenstein R, Halayko AJ, et al. Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J Immunol 2009; 183:5094-103. https://doi.org/10.4049/jimmunol.0802387
  16. Masamune A, Watanabe T, Kikuta K, Satoh K, Kanno A, Shimosegawa T. Nuclear expression of interleukin-33 in pancreatic stellate cells. Am J Physiol Gastrointest Liver Physiol 2010;299:G821-32. https://doi.org/10.1152/ajpgi.00178.2010
  17. Wood IS, Wang B, Trayhurn P. IL-33, a recently identified interleukin-1 gene family member, is expressed in human adipocytes. Biochem Biophys Res Commun 2009;384:105-9. https://doi.org/10.1016/j.bbrc.2009.04.081
  18. Wong CF, Yew WW, Leung SK, Chan CY, Hui M, Au-Yeang C, et al. Assay of pleural fluid interleukin-6, tumour necrosis factor-alpha and interferon- gamma in the diagnosis and outcome correlation of tuberculous effusion. Respir Med 2003;97:1289-95. https://doi.org/10.1016/j.rmed.2003.07.003
  19. Orphanidou D, Gaga M, Rasidakis A, Dimakou K, Toumbis M, Latsi P, et al. Tumour necrosis factor, interleukin-1 and adenosine deaminase in tuberculous pleural effusion. Respir Med 1996;90:95-8. https://doi.org/10.1016/S0954-6111(96)90205-X
  20. Barnes PF, Fong SJ, Brennan PJ, Twomey PE, Mazumder A, Modlin RL. Local production of tumor necrosis factor and IFN-gamma in tuberculous pleuritis. J Immunol 1990;145:149-54.
  21. Espinassous Q, Garcia-de-Paco E, Garcia-Verdugo I, Synguelakis M, von Aulock S, Sallenave JM, et al. IL-33 enhances lipopolysaccharide-induced inflammatory cytokine production from mouse macrophages by regulating lipopolysaccharide receptor complex. J Immunol 2009; 183:1446-55. https://doi.org/10.4049/jimmunol.0803067
  22. Xu D, Jiang HR, Kewin P, Li Y, Mu R, Fraser AR, et al. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc Natl Acad Sci U S A 2008;105:10913-8. https://doi.org/10.1073/pnas.0801898105
  23. Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE. IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol 2008;20:1019-30. https://doi.org/10.1093/intimm/dxn060
  24. Cooper AM, Solache A, Khader SA. Interleukin-12 and tuberculosis: an old story revisited. Curr Opin Immunol 2007;19:441-7. https://doi.org/10.1016/j.coi.2007.07.004
  25. Valdes L, San Jose E, Alvarez Dobano JM, Golpe A, Valle JM, Penela P, et al. Diagnostic value of interleukin-12 p40 in tuberculous pleural effusions. Eur Respir J 2009;33:816-20. https://doi.org/10.1183/09031936.00085008
  26. Oshikawa K, Yanagisawa K, Ohno S, Tominaga S, Sugiyama Y. Expression of ST2 in helper T lymphocytes of malignant pleural effusions. Am J Respir Crit Care Med 2002;165:1005-9. https://doi.org/10.1164/ajrccm.165.7.2105109
  27. Okamoto M, Hasegawa Y, Hara T, Hashimoto N, Imaizumi K, Shimokata K, et al. T-helper type 1/T-helper type 2 balance in malignant pleural effusions compared to tuberculous pleural effusions. Chest 2005;128: 4030-5. https://doi.org/10.1378/chest.128.6.4030
  28. Aoe K, Hiraki A, Murakami T, Eda R, Maeda T, Sugi K, et al. Diagnostic significance of interferon-gamma in tuberculous pleural effusions. Chest 2003;123:740-4. https://doi.org/10.1378/chest.123.3.740
  29. Greco S, Girardi E, Masciangelo R, Capoccetta GB, Saltini C. Adenosine deaminase and interferon gamma measurements for the diagnosis of tuberculous pleurisy: a meta-analysis. Int J Tuberc Lung Dis 2003;7:777-86.
  30. Boonyagars L and Kiertiburanakul S. Use of adenosine deaminase for the diagnosis of tuberculosis: a review. J Infect Dis Antimicrob Agents 2010;27:111-8.
  31. Light RW, Macgregor MI, Luchsinger PC, Ball WC Jr. Pleural effusions: the diagnostic separation of transudates and exudates. Ann Intern Med 1972;77:507-13. https://doi.org/10.7326/0003-4819-77-4-507
  32. Oboki K, Ohno T, Kajiwara N, Saito H, Nakae S. IL-33 and IL-33 receptors in host defense and diseases. Allergol Int 2010;59:143-60. https://doi.org/10.2332/allergolint.10-RAI-0186
  33. Miller AM. Role of IL-33 in inflammation and disease. J Inflamm 2011; 8:22. https://doi.org/10.1186/1476-9255-8-22
  34. Chen YM, Yang WK, Ting CC, Tsai WY, Yang DM, Whang-Peng J, et al. Cross regulation by IL-10 and IL-2/IL-12 of the helper T cells and the cytolytic activity of lymphocytes from malignant effusions of lung cancer patients. Chest 1997;112:960-6. https://doi.org/10.1378/chest.112.4.960
  35. Moussion C, Ortega N, Girard JP. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS One 2008;3:e3331. https://doi.org/10.1371/journal.pone.0003331
  36. Joshi AD, Oak SR, Hartigan AJ, Finn WG, Kunkel SL, Duffy KE, et al. Interleukin-33 contributes to both M1 and M2 chemokine marker expression in human macrophages. BMC Immunol 2010;11:52. https://doi.org/10.1186/1471-2172-11-52

Cited by

  1. IL-33 levels differentiate tuberculous pleurisy from malignant pleural effusions vol.8, pp.1, 2014, https://doi.org/10.3892/ol.2014.2109
  2. Alarmin IL-33 elicits potent TB-specific cell-mediated responses vol.11, pp.8, 2013, https://doi.org/10.1080/21645515.2015.1026499
  3. Pleural fluid tests to diagnose tuberculous pleuritis vol.22, pp.4, 2016, https://doi.org/10.1097/mcp.0000000000000277
  4. Diagnostic value of interleukins for tuberculous pleural effusion: a systematic review and meta-analysis vol.17, pp.None, 2013, https://doi.org/10.1186/s12890-017-0530-3
  5. Diagnostic accuracy of interleukin-33 for tuberculous pleural effusion : A systematic review and meta-analysis vol.100, pp.31, 2021, https://doi.org/10.1097/md.0000000000026755
  6. Diagnostic value of combined pleural interleukin-33, adenosine deaminase and peripheral blood tuberculosis T cell spot detection TB for tuberculous pleurisy vol.21, pp.1, 2013, https://doi.org/10.1186/s12879-021-06575-w