Augmentation of apoptosis and interferon-gamma production at sites of active Mycobacterium tuberculosis infection in human tuberculosis.

Pleural tuberculosis (TB) was employed as a model to study T cell apoptosis at sites of active Mycobacterium tuberculosis (MTB) infection in human immunodeficiency virus (HIV)-coinfected (HIV/TB) patients and patients infected with TB alone. Apoptosis in blood and in pleural fluid mononuclear cells and cytokine immunoreactivities in plasma and in pleural fluid were evaluated. T cells were expanded at the site of MTB infection, irrespective of HIV status. Apoptosis of CD4 and non-CD4 T cells in the pleural space occurred in both HIV/TB and TB. Interferon (IFN)-gamma levels were increased in pleural fluid, compared with plasma. Spontaneous apoptosis correlated with specific loss of MTB-reactive, IFN-gamma-producing pleural T cells. Immunoreactivities of molecules potentially involved in apoptosis, such as tumor necrosis factor-alpha, Fas-ligand, and Fas, were increased in pleural fluid, compared with plasma. These data suggest that continued exposure of immunoreactive cells to MTB at sites of infection may initiate a vicious cycle in which immune activation and loss of antigen-responsive T cells occur concomitantly, thus favoring persistence of MTB infection.

[1]  S. Nagata,et al.  Fas-mediated apoptosis of CD4+ and CD8+ T cells from human immunodeficiency virus-infected persons: differential in vitro preventive effect of cytokines and protease antagonists. , 1996, Blood.

[2]  C. Raker,et al.  HIV type 1 infection of human fetal bone marrow cells induces apoptotic changes in hematopoietic precursor cells and suppresses their in vitro differentiation and capacity to engraft SCID mice. , 1999, AIDS research and human retroviruses.

[3]  A. Kimchi,et al.  Death associated proteins (DAPs): from gene identification to the analysis of their apoptotic and tumor suppressive functions , 1998, Oncogene.

[4]  I. Orme,et al.  Materials and Methods Briefdefinitive Report Disseminated Tuberculosis in Interferon 7 Gene-disrupted Mice , 2022 .

[5]  W. Rom,et al.  Copyright © 1997, American Society for Microbiology Effects of Mycobacteria on Regulation of Apoptosis in , 1997 .

[6]  E. Clementi,et al.  Mycobacterium tuberculosisexploits the CD95/CD95 ligand system of γ δ T cells to cause apoptosis , 1998 .

[7]  Z. Toossi,et al.  Depressed T-cell interferon-gamma responses in pulmonary tuberculosis: analysis of underlying mechanisms and modulation with therapy. , 1999, The Journal of infectious diseases.

[8]  B. Graovac.  [Classification of pulmonary tuberculosis]. , 1956, Tuberkuloza.

[9]  L. Praloran.  [Classification of pulmonary tuberculosis]. , 1953, Minerva medica.

[10]  T. Imir,et al.  Involvement of the Fas/Fas Ligand Pathway in Activation-Induced Cell Death of Mycobacteria-Reactive Human γδ T Cells: A Mechanism for the Loss of γδ T Cells in Patients with Pulmonary Tuberculosis , 1998, The Journal of Immunology.

[11]  R. Nuesch,et al.  The Fas receptor in HIV infection: expression on peripheral blood lymphocytes and role in the depletion of T cells , 1996, AIDS.

[12]  B. Williams,et al.  Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Arbeit,et al.  Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. , 1997, Journal of immunology.

[14]  G. Evan,et al.  A License to Kill , 1996, Cell.

[15]  Z. Toossi,et al.  Cross-modulation by transforming growth factor beta in human tuberculosis: suppression of antigen-driven blastogenesis and interferon gamma production. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  H. Macdonald,et al.  Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. , 1998, Journal of immunology.

[17]  J. Flynn,et al.  An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection , 1993, The Journal of experimental medicine.

[18]  Martin Raff,et al.  Cell suicide for beginners , 1998, Nature.

[19]  Lloyd N. Friedman,et al.  Diagnostic standards and classification of tuberculosis. , 1991, The American review of respiratory disease.

[20]  M. Lenardo,et al.  Induction of apoptosis in mature T cells by tumour necrosis factor , 1995, Nature.

[21]  C. Rogier,et al.  Plasmodium falciparum induces apoptosis in human mononuclear cells , 1996, Infection and immunity.

[22]  G. Vanham,et al.  Generalized immune activation in pulmonary tuberculosis: co‐activation with HIV infection , 1996, Clinical and experimental immunology.

[23]  J. Keane,et al.  Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis , 1997, Infection and immunity.

[24]  S. Dorman,et al.  Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. , 1998, The Journal of clinical investigation.

[25]  E. Clementi,et al.  Mycobacterium tuberculosis exploits the CD95/CD95 ligand system of gammadelta T cells to cause apoptosis. , 1998, European journal of immunology.

[26]  I. Herr,et al.  Activation of the CD95 (APO-1/Fas) system in T cells from human immunodeficiency virus type-1-infected children. , 1996, Blood.

[27]  J. Abrams,et al.  T-cell cytokine responses in human infection with Mycobacterium tuberculosis , 1995, Infection and immunity.

[28]  G. Kaplan,et al.  Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin , 1994, The Journal of experimental medicine.

[29]  G. Vanham,et al.  Apoptosis and T cell hyporesponsiveness in pulmonary tuberculosis. , 1999, The Journal of infectious diseases.

[30]  I. Orme,et al.  Disseminated tuberculosis in interferon gamma gene-disrupted mice , 1993, The Journal of experimental medicine.

[31]  F. Cunha,et al.  Gamma Interferon Modulates CD95 (Fas) and CD95 Ligand (Fas-L) Expression and Nitric Oxide-Induced Apoptosis during the Acute Phase ofTrypanosoma cruzi Infection: a Possible Role in Immune Response Control , 1999, Infection and Immunity.

[32]  T. Imir,et al.  Involvement of the Fas/Fas ligand pathway in activation-induced cell death of mycobacteria-reactive human gamma delta T cells: a mechanism for the loss of gamma delta T cells in patients with pulmonary tuberculosis. , 1998, Journal of immunology.

[33]  W. Rom,et al.  Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication by transcriptional activation at the long terminal repeat. , 1995, The Journal of clinical investigation.

[34]  V. Gil,et al.  Pleural tuberculosis in HIV-infected patients. , 1995, Chest.

[35]  E. Tschachler,et al.  The cell death regulatory protein bak is expressed in endothelial cells in inflamed tissues and Is induced by IFN-gamma in vitro. , 1999, Biochemical and biophysical research communications.

[36]  M. Torres,et al.  Enhanced responses to Mycobacterium tuberculosis antigens by human alveolar lymphocytes during active pulmonary tuberculosis. , 1998, The Journal of infectious diseases.

[37]  Dinakar,et al.  T cell cytokine responses in persons with tuberculosis and human immunodeficiency virus infection. , 1994, The Journal of clinical investigation.

[38]  M. Torres,et al.  Comparison of the immune response against Mycobacterium tuberculosis antigens between a group of patients with active pulmonary tuberculosis and healthy household contacts , 1994, Clinical and experimental immunology.

[39]  M. Torres,et al.  T lymphocytic and immature macrophage alveolitis in active pulmonary tuberculosis. , 1996, The Journal of infectious diseases.

[40]  P. Georgii‐Hemming,et al.  Fas/APO-1 (CD95)-mediated apoptosis is activated by interferon-gamma and interferon- in interleukin-6 (IL-6)-dependent and IL-6-independent multiple myeloma cell lines. , 1998, Blood.

[41]  B. Williams,et al.  Identification of genes differentially regulated by interferon α, β, or γ using oligonucleotide arrays , 1998 .

[42]  J. Robinson,et al.  Deficient immune interferon production in tuberculosis. , 1985, Clinical and experimental immunology.

[43]  Craig B. Thompson,et al.  Hierarchical Control of Lymphocyte Survival , 1996, Science.

[44]  P. Dierckx,et al.  Specific Lymphoproliferation, Gamma Interferon Production, and Serum Immunoglobulin G Directed against a Purified 32 kDa Mycobacterial Protein Antigen (P32) in Patients with Active Tuberculosis , 1988, Scandinavian journal of immunology.

[45]  J. Abrams,et al.  Cytokine production at the site of disease in human tuberculosis , 1993, Infection and immunity.