CD4+CD25highforkhead box protein 3+ regulatory T lymphocytes suppress interferon-γ and CD107 expression in CD4+ and CD8+ T cells from tuberculous pleural effusions

Clinical and Experimental Immunology

Volumn 175, Issue 2, 2014, Pages 235-245

  Geffner, L ^a   Basile, J I ^a   Yokobori, N ^a   Sabio y Garcia C ^a   Musella, R ^b   Castagnino, J ^b   Sasiain, M C ^a   De la Barrera, S ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b HOSPITAL F J MUÑIZ   (Argentina)

Author keywords

CD107; Pleural effusions; T regulatory; Tuberculosis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; TRANSCRIPTION FACTOR FOXP3;

ADULT; ARTICLE; CD4 CD8 RATIO; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; DEGRANULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; MONONUCLEAR CELL; MYCOBACTERIUM TUBERCULOSIS; PLEURA FLUID; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; TUBERCULOUS PLEURISY; YOUNG ADULT;

CD107; PLEURAL EFFUSIONS; T REGULATORY; TUBERCULOSIS;

ADULT; CD8-POSITIVE T-LYMPHOCYTES; CELL DEGRANULATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LEUKOCYTES, MONONUCLEAR; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MYCOBACTERIUM TUBERCULOSIS; PLEURAL EFFUSION; T-LYMPHOCYTES, REGULATORY; TUBERCULOSIS, PLEURAL; YOUNG ADULT;

EID: 84891605700     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12227     Document Type: Article

References (47)

1. Ellner JJ, Barnes PF, Wallis RS, Modlin RL. The immunology of tuberculous pleurisy. Semin Respir Infect 1988; 3:335-342.
2. Berger HW, Mejia E. Tuberculous pleurisy. Chest 1973; 63:88-92.
3. Pettersson T, Klockars M, Hellstrom PE, Riska H, Wangel A. T and B lymphocytes in pleural effusions. Chest 1978; 73:49-51.
4. Lucivero G, Pierucci G, Bonomo L. Lymphocyte subsets in peripheral blood and pleural fluid. Eur Respir J 1988; 1:337-340.
5. Barnes PF, Mistry SD, Cooper CL, Pirmez C, Rea TH, Modlin RL. Compartmentalization of a CD4+ T lymphocyte subpopulation in tuberculous pleuritis. J Immunol 1989; 142:1114-1119.
6. Mitra DK, Sharma SK, Dinda AK, Bindra MS, Madan B, Ghosh B. Polarized helper T cells in tubercular pleural effusion: phenotypic identity and selective recruitment. Eur J Immunol 2005; 35:2367-2375.
7. Sharma SK, Mitra DK, Balamurugan A, Pandey RM, Mehra NK. Cytokine polarization in miliary and pleural tuberculosis. J Clin Immunol 2002; 22:345-352.
8. Jalapathy KV, Prabha C, Das SD. Correlates of protective immune response in tuberculous pleuritis. FEMS Immunol Med Microbiol 2004; 40:139-145.
9. Zhang M, Gately MK, Wang E etal. Interleukin 12 at the site of disease in tuberculosis. J Clin Invest 1994; 93:1733-1739.
10. Okamoto M, Kawabe T, Iwasaki Y etal. Evaluation of interferon-gamma, interferon-gamma-inducing cytokines, and interferon-gamma-inducible chemokines in tuberculous pleural effusions. J Lab Clin Med 2005; 145:88-93.
11. Barbosa T, Arruda S, Chalhoub M etal. Correlation between interleukin-10 and in situ necrosis and fibrosis suggests a role for interleukin-10 in the resolution of the granulomatous response of tuberculous pleurisy patients. Microbes Infect 2006; 8:889-897.
12. Guyot-Revol V, Innes JA, Hackforth S, Hinks T, Lalvani A. Regulatory T cells are expanded in blood and disease sites in patients with tuberculosis. Am J Respir Crit Care Med 2006; 173:803-810.
13. Hougardy JM, Place S, Hildebrand M etal. Regulatory T cells depress immune responses to protective antigens in active tuberculosis. Am J Respir Crit Care Med 2007; 176:409-416.
14. Hougardy JM, Verscheure V, Locht C, Mascart F. In vitro expansion of CD4+CD25highFOXP3+CD127low/- regulatory T cells from peripheral blood lymphocytes of healthy Mycobacterium tuberculosis-infected humans. Microbes Infect 2007; 9:1325-1332.
15. Roberts T, Beyers N, Aguirre A, Walzl G. Immunosuppression during active tuberculosis is characterized by decreased interferon-gamma production and CD25 expression with elevated forkhead box P3, transforming growth factor-beta, and interleukin-4 mRNA levels. J Infect Dis 2007; 195:870-878.
16. Qin XJ, Shi HZ, Liang QL, Huang LY, Yang HB. CD4+CD25+ regulatory T lymphocytes in tuberculous pleural effusion. Chin Med J (Engl) 2008; 121:581-586.
17. Semple PL, Binder AB, Davids M, Maredza A, van Zyl-Smit RN, Dheda K. Regulatory T cells attenuate mycobacterial stasis in alveolar and blood-derived macrophages from patients with tuberculosis. Am J Respir Crit Care Med 2013; 187:1249-1258.
18. Canaday DH, Wilkinson RJ, Li Q, Harding CV, Silver RF, Boom WH. CD4(+) and CD8(+) T cells kill intracellular Mycobacterium tuberculosis by a perforin and Fas/Fas ligand-independent mechanism. J Immunol 2001; 167:2734-2742.
19. Stenger S, Mazzaccaro RJ, Uyemura K etal. Differential effects of cytolytic T cell subsets on intracellular infection. Science 1997; 276:1684-1687.
20. Stenger S, Hanson DA, Teitelbaum R etal. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998; 282:121-125.
21. Geffner L, Yokobori N, Basile J etal. Patients with multidrug resistant tuberculosis display impaired Th1 response and enhanced regulatory T cells levels in response to M and Ra outbreak multidrug resistant Mycobacterium tuberculosis strains. Infect Immun 2009; 77:5025-5034.
22. Wolint P, Betts MR, Koup RA, Oxenius A. Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J Exp Med 2004; 199:925-936.
23. Betts MR, Brenchley JM, Price DA etal. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003; 281:65-78.
24. Schierloh P, Yokobori N, Aleman M etal. Increased susceptibility to apoptosis of CD56dimCD16+ NK cells induces the enrichment of IFN-gamma-producing CD56bright cells in tuberculous pleurisy. J Immunol 2005; 175:6852-6860.
25. Sakaguchi S, Sakaguchi N. Regulatory T cells in immunologic self-tolerance and autoimmune disease. Int Rev Immunol 2005; 24:211-226.
26. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008; 133:775-787.
27. Sharma PK, Saha PK, Singh A, Sharma SK, Ghosh B, Mitra DK. FoxP3+ regulatory T cells suppress effector T-cell function at pathologic site in miliary tuberculosis. Am J Respir Crit Care Med 2009; 179:1061-1070.
28. Chen X, Zhou B, Li M etal. CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol 2007; 123:50-59.
29. Saha PK, Sharma PK, Sharma SK, Singh A, Mitra DK. Recruitment of Th1 effector cells in human tuberculosis: hierarchy of chemokine receptor(s) and their ligands. Cytokine 2013; 63:43-51.
30. El Fenniri L, Toossi Z, Aung H etal. Polyfunctional Mycobacterium tuberculosis-specific effector memory CD4+ T cells at sites of pleural TB. Tuberculosis (Edinb) 2011; 91:224-230.
31. Williams MA, Bevan MJ. Effector and memory CTL differentiation. Annu Rev Immunol 2007; 25:171-192.
32. Mescher MF, Curtsinger JM, Agarwal P etal. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 2006; 211:81-92.
33. Mutis T, Cornelisse YE, Ottenhoff TH. Mycobacteria induce CD4+ T cells that are cytotoxic and display Th1-like cytokine secretion profile: heterogeneity in cytotoxic activity and cytokine secretion levels. Eur J Immunol 1993; 23:2189-2195.
34. Ottenhoff TH, Mutis T. Specific killing of cytotoxic T cells and antigen-presenting cells by CD4+ cytotoxic T cell clones. A novel potentially immunoregulatory T-T cell interaction in man. J Exp Med 1990; 171:2011-2024.
35. De La Barrera SS, Finiasz M, Frias A etal. Specific lytic activity against mycobacterial antigens is inversely correlated with the severity of tuberculosis. Clin Exp Immunol 2003; 132:450-461.
36. Bastian M, Braun T, Bruns H, Rollinghoff M, Stenger S. Mycobacterial lipopeptides elicit CD4+ CTLs in Mycobacterium tuberculosis-infected humans. J Immunol 2008; 180:3436-3446.
37. Wu C, Zhou Q, Qin XJ, Qin SM, Shi HZ. CCL22 is involved in the recruitment of CD4+CD25 high T cells into tuberculous pleural effusions. Respirology 2010; 15:522-529.
38. Zheng SG, Wang JH, Gray JD, Soucier H, Horwitz DA. Natural and induced CD4+CD25+ cells educate CD4+CD25- cells to develop suppressive activity: the role of IL-2, TGF-beta, and IL-10. J Immunol 2004; 172:5213-5221.
39. Piccirillo CA, Shevach EM. Cutting edge: control of CD8+ T cell activation by CD4+CD25+ immunoregulatory cells. J Immunol 2001; 167:1137-1140.
40. Trzonkowski P, Szmit E, Mysliwska J, Dobyszuk A, Mysliwski A. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. Clin Immunol 2004; 112:258-267.
41. Skapenko A, Kalden JR, Lipsky PE, Schulze-Koops H. The IL-4 receptor alpha-chain-binding cytokines, IL-4 and IL-13, induce forkhead box P3-expressing CD25+CD4+ regulatory T cells from CD25-CD4+ precursors. J Immunol 2005; 175:6107-6116.
42. Dlugovitzky D, Bay ML, Rateni L etal. In vitro synthesis of interferon-gamma, interleukin-4, transforming growth factor-beta and interleukin-1 beta by peripheral blood mononuclear cells from tuberculosis patients: relationship with the severity of pulmonary involvement. Scand J Immunol 1999; 49:210-217.
43. Seah GT, Scott GM, Rook GA. Type 2 cytokine gene activation and its relationship to extent of disease in patients with tuberculosis. J Infect Dis 2000; 181:385-389.
44. Nolan A, Fajardo E, Huie ML etal. Increased production of IL-4 and IL-12p40 from bronchoalveolar lavage cells are biomarkers of Mycobacterium tuberculosis in the sputum. PLoS ONE 2013; 8:e59461.
45. Green AM, Mattila JT, Bigbee CL, Bongers KS, Lin PL, Flynn JL. CD4(+) regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection. J Infect Dis 2010; 202:533-541.
46. Singh A, Dey AB, Mohan A, Sharma PK, Mitra DK. Foxp3+ regulatory T cells among tuberculosis patients: impact on prognosis and restoration of antigen specific IFN-gamma producing T cells. PLOS ONE 2012; 7:e44728.
47. Masood KI, Rottenberg ME, Salahuddin N etal. Expression of M. tuberculosis-induced suppressor of cytokine signaling (SOCS) 1, SOCS3, FoxP3 and secretion of IL-6 associates with differing clinical severity of tuberculosis. BMC Infect Dis 2013; 13:13.