Compartmentalized bronchoalveolar IFN-γ and IL-12 response in human pulmonary tuberculosis

Tuberculosis

Volumn 89, Issue 1, 2009, Pages 38-47

  Herrera, Maria Teresa ^a   Torres, Martha ^a   Nevels, Denarra ^b   Perez Redondo, Carlos Núñez ^a   Ellner, Jerrold J ^b   Sada, Eduardo ^a   Schwander, Stephan K ^b  

^a INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

BAL cells; Compartmentalization; Human pulmonary tuberculosis; Interferon gamma; Interleukin 10; Interleukin 12; Interleukin 4; Mycobacterium tuberculosis

Indexed keywords

CD56 ANTIGEN; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 12P70; INTERLEUKIN 4; INTERLEUKIN 9; MESSENGER RNA;

ANTIBACTERIAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL SUBPOPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNITY; IMMUNOCOMPETENT CELL; LUNG ALVEOLUS; LUNG LAVAGE; LUNG TUBERCULOSIS; MACROPHAGE; MALE; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH1 CELL;

ADULT; BACTERIOLOGICAL TECHNIQUES; BRONCHI; BRONCHOALVEOLAR LAVAGE FLUID; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-4; INTERLEUKIN-9; LUNG; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; PULMONARY ALVEOLI; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA; TUBERCULOSIS, PULMONARY;

EID: 58149116814     PISSN: 14729792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tube.2008.08.002     Document Type: Article

References (73)

1. Bates J.H. Transmission and pathogenesis of tuberculosis. Clin Chest Med 1 (1980) 167-174
2. Sodhi A., Gong J., Silva C., Qian D., and Barnes P.F. Clinical correlates of interferon gamma production in patients with tuberculosis. Clin Infect Dis 25 (1997) 617-620
3. Hirsch C.S., Toossi Z., Othieno C., Johnson J.L., Schwander S.K., Robertson S., et al. Depressed T-cell interferon-gamma responses in pulmonary tuberculosis: analysis of underlying mechanisms and modulation with therapy. J Infect Dis 180 (1999) 2069-2073
4. Torres M., Herrera T., Villareal H., Rich E.A., and Sada E. Cytokine profiles for peripheral blood lymphocytes from patients with active pulmonary tuberculosis and healthy household contacts in response to the 30-kilodalton antigen of Mycobacterium tuberculosis. Infect Immun 66 (1998) 176-180
5. Ellner J.J. Suppressor adherent cells in human tuberculosis. J Immunol 121 (1978) 2573-2579
6. Ellner J.J. Regulation of the human immune response during tuberculosis. J Lab Clin Med 130 (1997) 469-475
7. Fujiwara H., Kleinhenz M.E., Wallis R.S., and Ellner J.J. Increased interleukin-1 production and monocyte suppressor cell activity associated with human tuberculosis. Am Rev Respir Dis 133 (1986) 73-77
8. Toossi Z., Kleinhenz M.E., and Ellner J.J. Defective interleukin 2 production and responsiveness in human pulmonary tuberculosis. J Exp Med 163 (1986) 1162-1172
9. Hirsch C.S., Hussain R., Toossi Z., Dawood G., Shahid F., and Ellner J.J. Cross-modulation by transforming growth factor beta in human tuberculosis: suppression of antigen-driven blastogenesis and interferon gamma production. Proc Natl Acad Sci U S A 93 (1996) 3193-3198
10. Zhang M., Lin Y., Iyer D.V., Gong J., Abrams J.S., and Barnes P.F. T-cell cytokine responses in human infection with Mycobacterium tuberculosis. Infect Immun 63 (1995) 3231-3234
11. Hirsch C.S., Yoneda T., Averill L., Ellner J.J., and Toossi Z. Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-beta 1. J Infect Dis 170 (1994) 1229-1237
12. Othieno C., Hirsch C.S., Hamilton B.D., Wilkinson K., Ellner J.J., and Toossi Z. Interaction of Mycobacterium tuberculosis-induced transforming growth factor beta1 and interleukin-10. Infect Immun 67 (1999) 5730-5735
13. Hirsch C.S., Ellner J.J., Blinkhorn R., and Toossi Z. In vitro restoration of T cell responses in tuberculosis and augmentation of monocyte effector function against Mycobacterium tuberculosis by natural inhibitors of transforming growth factor beta. Proc Natl Acad Sci U S A 94 (1997) 3926-3931
14. Toossi Z., Gogate P., Shiratsuchi H., Young T., and 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 (Baltimore, Md.: 1950) 154 (1995) 465-473
15. Schwander S.K., Sada E., Torres M., Escobedo D., Sierra J.G., Alt S., et al. T lymphocytic and immature macrophage alveolitis in active pulmonary tuberculosis. J Infect Dis 173 (1996) 1267-1272
16. Schwander S.K., Torres M., Sada E., Carranza C., Ramos E., Tary-Lehmann M., et al. Enhanced responses to Mycobacterium tuberculosis antigens by human alveolar lymphocytes during active pulmonary tuberculosis. J Infect Dis 178 (1998) 1434-1445
17. Condos R., Rom W.N., Liu Y.M., and Schluger N.W. Local immune responses correlate with presentation and outcome in tuberculosis. Am J Respir Crit Care Med 157 (1998) 729-735
18. Mazzarella G., Bianco A., Perna F., D'Auria D., Grella E., Moscariello E., et al. T lymphocyte phenotypic profile in lung segments affected by cavitary and non-cavitary tuberculosis. Clin Exp Immunol 132 (2003) 283-288
19. Ribeiro-Rodrigues R., Resende C.T., Johnson J.L., Ribeiro F., Palaci M., Sa R.T., et al. Sputum cytokine levels in patients with pulmonary tuberculosis as early markers of mycobacterial clearance. Clin Diagn Lab Immunol 9 (2002) 818-823
20. Aubert-Pivert E.M., Chedevergne F.M., Lopez-Ramirez G.M., Colle J.H., Scheinmann P.L., Gicquel B.M., et al. Cytokine transcripts in pediatric tuberculosis: a study with bronchoalveolar cells. Tuber Lung Dis 80 (2000) 249-258
21. Taha R.A., Kotsimbos T.C., Song Y.L., Menzies D., and Hamid Q. IFN-gamma and IL-12 are increased in active compared with inactive tuberculosis. Am J Respir Crit Care Med 155 (1997) 1135-1139
22. Giacomini E., Iona E., Ferroni L., Miettinen M., Fattorini L., Orefici G., et al. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 166 (2001) 7033-7041
23. Yin X.J., Schafer R., Ma J.Y., Antonini J.M., Weissman D.D., Siegel P.D., et al. Alteration of pulmonary immunity to Listeria monocytogenes by diesel exhaust particles (DEPs). I. Effects of DEPs on early pulmonary responses. Environ Health Perspect 110 (2002) 1105-1111
24. Yin X.J., Schafer R., Ma J.Y., Antonini J.M., Roberts J.R., Weissman D.N., et al. Alteration of pulmonary immunity to Listeria monocytogenes by diesel exhaust particles (DEPs). II. Effects of DEPs on T-cell-mediated immune responses in rats. Environ Health Perspect 111 (2003) 524-530
25. Rich E.A., Panuska J.R., Wallis R.S., Wolf C.B., Leonard M.L., and Ellner J.J. Dyscoordinate expression of tumor necrosis factor-alpha by human blood monocytes and alveolar macrophages. Am Rev Respir Dis 139 (1989) 1010-1016
26. Law K., Weiden M., Harkin T., Tchou-Wong K., Chi C., and Rom W.N. Increased release of interleukin-1 beta, interleukin-6, and tumor necrosis factor-alpha by bronchoalveolar cells lavaged from involved sites in pulmonary tuberculosis. Am J Respir Crit Care Med 153 (1996) 799-804
27. Vankayalapati R., Wizel B., Lakey D.L., Zhang Y., Coffee K.A., Griffith D.E., et al. T cells enhance production of IL-18 by monocytes in response to an intracellular pathogen. J Immunol 166 (2001) 6749-6753
28. Zissel G., Baumer I., Schlaak M., and Muller-Quernheim J. In vitro release of interleukin-15 by broncho-alveolar lavage cells and peripheral blood mononuclear cells from patients with different lung diseases. Eur Cytokine Netw 11 (2000) 105-112
29. Gately M.K., Renzetti L.M., Magram J., Stern A.S., Adorini L., Gubler U., et al. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 16 (1998) 495-521
30. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3 (2003) 133-146
31. Watford W.T., Moriguchi M., Morinobu A., and O'Shea J.J. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 14 (2003) 361-368
32. Desai B.B., Quinn P.M., Wolitzky A.G., Mongini P.K., Chizzonite R., and Gately M.K. IL-12 receptor. II. Distribution and regulation of receptor expression. J Immunol 148 (1992) 3125-3132
33. Presky D.H., Minetti L.J., Gillessen S., Wilkinson V.L., Wu C.Y., Gubler U., et al. Analysis of the multiple interactions between IL-12 and the high affinity IL-12 receptor complex. J Immunol 160 (1998) 2174-2179
34. Presky D.H., Yang H., Minetti L.J., Chua A.O., Nabavi N., Wu C.Y., et al. A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proc Natl Acad Sci U S A 93 (1996) 14002-14007
35. Rogge L., Barberis-Maino L., Biffi M., Passini N., Presky D.H., Gubler U., et al. Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J Exp Med 185 (1997) 825-831
36. Rogge L., Papi A., Presky D.H., Biffi M., Minetti L.J., Miotto D., et al. Antibodies to the IL-12 receptor beta 2 chain mark human Th1 but not Th2 cells in vitro and in vivo. J Immunol 162 (1999) 3926-3932
37. Szabo S.J., Dighe A.S., Gubler U., and Murphy K.M. Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J Exp Med 185 (1997) 817-824
38. Boehm U., Klamp T., Groot M., and Howard J.C. Cellular responses to interferon-gamma. Annu Rev Immunol 15 (1997) 749-795
39. Cooper A.M., Dalton D.K., Stewart T.A., Griffin J.P., Russell D.G., and Orme I.M. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178 (1993) 2243-2247
40. Flynn J.L., Chan J., Triebold K.J., Dalton D.K., Stewart T.A., and Bloom B.R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178 (1993) 2249-2254
41. Altare F., Durandy A., Lammas D., Emile J.F., Lamhamedi S., Le Deist F., et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280 (1998) 1432-1435
42. Altare F., Ensser A., Breiman A., Reichenbach J., Baghdadi J.E., Fischer A., et al. Interleukin-12 receptor beta1 deficiency in a patient with abdominal tuberculosis. J Infect Dis 184 (2001) 231-236
43. Fieschi C., Dupuis S., Catherinot E., Feinberg J., Bustamante J., Breiman A., et al. Low penetrance, broad resistance, and favorable outcome of interleukin 12 receptor beta1 deficiency: medical and immunological implications. J Exp Med 197 (2003) 527-535
44. van de Vosse E., Hoeve M.A., and Ottenhoff T.H. Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and salmonellae. Lancet Infect Dis 4 (2004) 739-749
45. Jouanguy E., Lamhamedi-Cherradi S., Altare F., Fondaneche M.C., Tuerlinckx D., Blanche S., et al. Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guerin infection and a sibling with clinical tuberculosis. J Clin Invest 100 (1997) 2658-2664
46. Jouanguy E., Altare F., Lamhamedi-Cherradi S., and Casanova J.L. Infections in IFNGR-1-deficient children. J Interferon Cytokine Res 17 (1997) 583-587
47. Caragol I., Raspall M., Fieschi C., Feinberg J., Larrosa M.N., Hernandez M., et al. Clinical tuberculosis in 2 of 3 siblings with interleukin-12 receptor beta1 deficiency. Clin Infect Dis 37 (2003) 302-306
48. Picard C., Fieschi C., Altare F., Al Jumaah S., Al Hajjar S., Feinberg J., et al. Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet 70 (2002) 336-348
49. Classification of pulmonary tuberculosis. Diagnostic standards and classification of tuberculosis (1969), National Tuberculosis and Respiratory Disease Association, New York 68-74
50. Boyum A. Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol Suppl. 5 (1976) 9-15
51. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162 (1987) 156-159
52. Barry S.M., Lipman M.C., Bannister B., Johnson M.A., and Janossy G. Purified protein derivative-activated type 1 cytokine-producing CD4+ T lymphocytes in the lung: a characteristic feature of active pulmonary and nonpulmonary tuberculosis. J Infect Dis 187 (2003) 243-250
53. Morosini M., Meloni F., Marone B.A., Paschetto E., Uccelli M., Pozzi E., et al. The assessment of IFN-gamma and its regulatory cytokines in the plasma and bronchoalveolar lavage fluid of patients with active pulmonary tuberculosis. Int J Tuberc Lung Dis 7 (2003) 994-1000
54. Zhang M., Gately M.K., Wang E., Gong J., Wolf S.F., Lu S., et al. Interleukin 12 at the site of disease in tuberculosis. J Clin Invest 93 (1994) 1733-1739
55. Taha R.A., Minshall E.M., Olivenstein R., Ihaku D., Wallaert B., Tsicopoulos A., et al. Increased expression of IL-12 receptor mRNA in active pulmonary tuberculosis and sarcoidosis. Am J Respir Crit Care Med 160 (1999) 1119-1123
56. Singhal A., Jaiswal A., Arora V.K., and Prasad H.K. Modulation of interferon gamma receptor 1 by Mycobacterium tuberculosis: a potential immune evasive mechanism. Infect Immun (2007)
57. Carranza C., Juarez E., Torres M., Ellner J.J., Sada E., and Schwander S.K. Mycobacterium tuberculosis growth control by lung macrophages and CD8 cells from patient contacts. Am J Respir Crit Care Med 173 (2005) 238-245
58. Condos R., Rom W.N., and Schluger N.W. Treatment of multidrug-resistant pulmonary tuberculosis with interferon-gamma via aerosol. Lancet 349 (1997) 1513-1515
59. Dheda K., Chang J.S., Breen R.A., Kim L.U., Haddock J.A., Huggett J.F., et al. In vivo and in vitro studies of a novel cytokine, interleukin 4delta2, in pulmonary tuberculosis. Am J Respir Crit Care Med 172 (2005) 501-508
60. Kampmann B., Hemingway C., Stephens A., Davidson R., Goodsall A., Anderson S., et al. Acquired predisposition to mycobacterial disease due to autoantibodies to IFN-gamma. J Clin Invest 115 (2005) 2480-2488
61. Wu B., Huang C., Kato-Maeda M., Hopewell P.C., Daley C.L., Krensky A.M., et al. IL-9 is associated with an impaired Th1 immune response in patients with tuberculosis. Clin Immunol (2007)
62. Ribeiro-Rodrigues R., Resende C.T., Rojas R., Toossi Z., Dietze R., Boom W.H., et al. A role for CD4+ CD25+ T cells in regulation of the immune response during human tuberculosis. Clin Exp Immunol 144 (2006) 25-34
63. Stenger S., Niazi K.R., and Modlin R.L. Down-regulation of CD1 on antigen-presenting cells by infection with Mycobacterium tuberculosis. J Immunol 161 (1998) 3582-3588
64. Kincaid E.Z., and Ernst J.D. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J Immunol 171 (2003) 2042-2049
65. Noss E.H., Pai R.K., Sellati T.J., Radolf J.D., Belisle J., Golenbock D.T., et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 167 (2001) 910-918
66. Pai R.K., Pennini M.E., Tobian A.A., Canaday D.H., Boom W.H., and Harding C.V. Prolonged toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits gamma interferon-induced regulation of selected genes in macrophages. Infect Immun 72 (2004) 6603-6614
67. Pennini M.E., Pai R.K., Schultz D.C., Boom W.H., and Harding C.V. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 176 (2006) 4323-4330
68. Pai R.K., Convery M., Hamilton T.A., Boom W.H., and Harding C.V. Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 171 (2003) 175-184
69. Gehring A.J., Rojas R.E., Canaday D.H., Lakey D.L., Harding C.V., and Boom W.H. The Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits gamma interferon-regulated HLA-DR and Fc gamma R1 on human macrophages through toll-like receptor 2. Infect Immun 71 (2003) 4487-4497
70. Fletcher H.A., Owiafe P., Jeffries D., Hill P., Rook G.A., Zumla A., et al. Increased expression of mRNA encoding interleukin (IL)-4 and its splice variant IL-4delta2 in cells from contacts of Mycobacterium tuberculosis, in the absence of in vitro stimulation. Immunology 112 (2004) 669-673
71. Dheda K., Chang J.S., Huggett J.F., Kim L.U., Johnson M.A., Zumla A., et al. The stability of mRNA encoding IL-4 is increased in pulmonary tuberculosis, while stability of mRNA encoding the antagonistic splice variant, IL-4delta2, is not. Tuberculosis (Edinburgh) 87 (2007) 237-241
72. Seah G.T., and Rook G.A. IL-4 influences apoptosis of mycobacterium-reactive lymphocytes in the presence of TNF-alpha. J Immunol 167 (2001) 1230-1237
73. Seah G.T., Scott G.M., and Rook G.A. Type 2 cytokine gene activation and its relationship to extent of disease in patients with tuberculosis. J Infect Dis 181 (2000) 385-389