Prominent role for T cell-derived Tumour Necrosis Factor for sustained control of Mycobacterium tuberculosis infection

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Allie, Nasiema ^a,g   Grivennikov, Sergei I ^b,c,d   Keeton, Roanne ^a   Hsu, Nai Jen ^a   Bourigault, Marie Laure ^b,c   Court, Nathalie ^b,c   Fremond, Cecile ^b,c   Yeremeev, Vladimir ^b,c   Shebzukhov, Yuriy ^d,e   Ryffel, Bernhard ^b,c   Nedospasov, Sergei A ^d,e   Quesniaux, Valerie F J ^b,c   Jacobs, Muazzam ^a,f  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b CNRS   (France)

^c UNIVERSITÉ D'ORLÉANS   (France)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e A Leibniz Institute   (Germany)

^f NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

^g UNIVERSITY OF THE WESTERN CAPE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; INTEGRASE; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; BONE MARROW CELL; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; PNEUMONIA; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUBERCULOSIS; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; INTEGRASES; LUNG; MACROPHAGES; MICE; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; MYELOID CELLS; NEUTROPHILS; PNEUMONIA; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877754497     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01809     Document Type: Article

References (68)

1. Moreno, C. et al. Lipoarabinomannan from Mycobacterium tuberculosis induces the production of tumour necrosis factor from human and murine macrophages. Clin Exp Immunol 76, 240-245 (1989). (Pubitemid 19150395)
2. Roach, T. I., Barton, C. H., Chatterjee, D. & Blackwell, J. M. Macrophage activation: lipoarabinomannan from avirulent and virulent strains of Mycobacterium tuberculosis differentially induces the early genes c-fos, KC, JE, and tumor necrosis factor-alpha. J Immunol 150, 1886-1896 (1993). (Pubitemid 23129666)
3. Falcone, V., Bassey, E. B., Toniolo, A., Conaldi, P. G. & Collins, F. M. Differential release of tumor necrosis factor-alpha from murine peritoneal macrophages stimulated with virulent and avirulent species of mycobacteria. FEMS Immunol Med Microbiol 8, 225-232 (1994). (Pubitemid 24097633)
4. Oswald, I. P.,Dozois, C. M., Fournout, S., Petit, J. F.& Lemaire, G. Tumor necrosis factor is required for the priming of peritoneal macrophages by trehalose dimycolate. Eur Cytokine Netw 10, 533-540 (1999).
5. Flesch, I. E. & Kaufmann, S. H. Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor. Infect Immun 58, 2675-2677 (1990). (Pubitemid 20228256)
6. Bean, A. G. et al. Structural deficiencies in granuloma formation in TNF genetargeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol 162, 3504-3511 (1999). (Pubitemid 29313602)
7. Kindler, V., Sappino, A. P., Grau, G. E., Piguet, P. F. & Vassalli, P. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 56, 731-740 (1989). (Pubitemid 19082507)
8. Flynn, J. L. et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2, 561-572 (1995).
9. Jacobs, M. et al. Correction of defective host response to Mycobacterium bovis BCG infection in TNF-deficient mice by bone marrow transplantation. Laboratory investigation; a journal of technical methods and pathology 80, 901-914 (2000). (Pubitemid 30421807)
10. Locksley, R. M., Killeen, N. & Lenardo, M. J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487-501 (2001). (Pubitemid 32201945)
11. Allie, N. et al. Limited role for lymphotoxin alpha in the host immune response to Mycobacterium tuberculosis. J Immunol 185, 4292-4301 (2010).
12. Bopst, M. et al. Differential effects of TNF and LTalpha in the host defense against M. bovis BCG. Eur J Immunol 31, 1935-1943 (2001). (Pubitemid 32547355)
13. Bazzoni, F. & Beutler, B. How do tumor necrosis factor receptors work? J Inflamm 45, 221-238 (1995). (Pubitemid 26042205)
14. Dempsey, P. W., Doyle, S. E., He, J. Q. & Cheng, G. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev 14, 193-209 (2003). (Pubitemid 36693141)
15. Black, R. A. et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733 (1997). (Pubitemid 27098094)
16. Moss, M. L. et al. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature 385, 733-736 (1997). (Pubitemid 27098095)
17. Allie, N. et al. Protective role of membrane tumour necrosis factor in the host's resistance to mycobacterial infection. Immunology 125, 522-534 (2008).
18. Dambuza, I. et al. Efficacy of membrane TNF mediated host resistance is dependent on mycobacterial virulence. Tuberculosis (Edinb) 88, 221-234 (2008). (Pubitemid 351635899)
19. Fremond, C. et al. Membrane TNF confers protection to acute mycobacterial infection. Respir Res 6, 136 (2005).
20. Vassalli, P. The pathophysiology of tumor necrosis factors. Annu Rev Immunol 10, 411-452 (1992).
21. Keane, J. TNF-blocking agents and tuberculosis: new drugs illuminate an old topic. Rheumatology (Oxford) 44, 714-720 (2005). (Pubitemid 41487198)
22. Keane, J. et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 345, 1098-1104 (2001).
23. Kaufmann, S. H. & Flesch, I. E. The role of T cell-macrophage interactions in tuberculosis. Springer seminars in immunopathology 10, 337-358 (1988).
24. North, R. J. & Jung, Y. J. Immunity to tuberculosis. Annu Rev Immunol 22, 599-623 (2004). (Pubitemid 38680435)
25. Saunders, B. M., Briscoe, H. & Britton,W. J. T cell-derived tumour necrosis factor is essential, but not sufficient, for protection against Mycobacterium tuberculosis infection. Clinical and experimental immunology 137, 279-287 (2004). (Pubitemid 39013073)
26. Grivennikov, S. I. et al. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22, 93-104 (2005). (Pubitemid 40143454)
27. Roach, D. R. et al. TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol 168, 4620-4627 (2002). (Pubitemid 34441368)
28. Flesch, I. E. et al. Early interleukin 12 production by macrophages in response to mycobacterial infection depends on interferon gamma and tumor necrosis factor alpha. J Exp Med 181, 1615-1621 (1995).
29. Freeman, S. et al. Mycobacterium tuberculosis H37Ra and H37Rv differential growth and cytokine/chemokine induction in murine macrophages in vitro. J Interferon Cytokine Res 26, 27-33 (2006). (Pubitemid 43201734)
30. Eriks, I. S. & Emerson, C. L. Temporal effect of tumor necrosis factor alpha on murine macrophages infected with Mycobacterium avium. Infect Immun 65, 2100-2106 (1997). (Pubitemid 27237284)
31. Hirsch, C. S., Ellner, J. J., Russell, D. G. & Rich, E. A. Complement receptormediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J Immunol 152, 743-753 (1994). (Pubitemid 24072978)
32. Denis, M., Gregg, E. O. & Ghandirian, E. Cytokinemodulation of Mycobacterium tuberculosis growth in human macrophages. International journal of immunopharmacology 12, 721-727 (1990). (Pubitemid 20285890)
33. Denis, M. & Gregg, E. O. Recombinant tumour necrosis factor-alpha decreases whereas recombinant interleukin-6 increases growth of a virulent strain of Mycobacterium avium in humanmacrophages. Immunology 71, 139-141 (1990). (Pubitemid 20296085)
34. Stein, M. & Gordon, S. Regulation of tumor necrosis factor (TNF) release by murine peritoneal macrophages: role of cell stimulation and specific phagocytic plasma membrane receptors. Eur J Immunol 21, 431-437 (1991).
35. Tachibana, K., Chen,G. J., Huang, D. S., Scuderi, P.&Watson, R. R. Production of tumor necrosis factor alpha by resident and activated murine macrophages. J Leukoc Biol 51, 251-255 (1992).
36. Togbe, D. et al. T cell-derived TNF down-regulates acute airway response to endotoxin. Eur J Immunol 37, 768-779 (2007). (Pubitemid 46916943)
37. Cooper, A. M. & Flynn, J. L. The protective immune response to Mycobacterium tuberculosis. Current opinion in immunology 7, 512-516 (1995).
38. Cooper, A. M. T cells in mycobacterial infection and disease. Current opinion in immunology 21, 378-384 (2009).
39. Xing, Z.,Wang, J., Croitoru, K. &Wakeham, J. Protection by CD4 or CD8 T cells against pulmonary Mycobacterium bovis bacillus Calmette-Guerin infection. Infection and immunity 66, 5537-5542 (1998). (Pubitemid 29044656)
40. Feng, C. G., Bean, A. G., Hooi, H., Briscoe, H. & Britton, W. J. Increase in gamma interferon-secreting CD8(1), as well as CD4(1), T cells in lungs following aerosol infection with Mycobacterium tuberculosis. Infection and immunity 67, 3242-3247 (1999). (Pubitemid 29291487)
41. Mulligan, M. S., Vaporciyan, A. A., Miyasaka, M., Tamatani, T. & Ward, P. A. Tumor necrosis factor alpha regulates in vivo intrapulmonary expression of ICAM-1. Am J Pathol 142, 1739-1749 (1993). (Pubitemid 24057068)
42. Cooper, A. M. et al. Disseminated tuberculosis in interferon gamma genedisrupted mice. The Journal of experimental medicine 178, 2243-2247 (1993). (Pubitemid 23344885)
43. Flynn, J. L. et al. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. The Journal of experimental medicine 178, 2249-2254 (1993). (Pubitemid 23344886)
44. Das, G., Sheridan, S. & Janeway, C. A., Jr. The source of early IFN-gamma that plays a role in Th1 priming. J Immunol 167, 2004-2010 (2001). (Pubitemid 32747507)
45. Tsukaguchi, K., de Lange, B. & Boom, W. H. Differential regulation of IFNgamma, TNF-alpha, and IL-10 production by CD4(1) alphabetaTCR1 T cells and vdelta2(1) gammadelta T cells in response to monocytes infected with Mycobacterium tuberculosis-H37Ra. Cellular immunology 194, 12-20 (1999). (Pubitemid 29283972)
46. Tracey, K. J. & Cerami, A. Tumor necrosis factor, other cytokines and disease. Annual review of cell biology 9, 317-343 (1993).
47. Tsai, M. C. et al. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cellular microbiology 8, 218-232 (2006). (Pubitemid 43356045)
48. Ladel, C. H., Szalay, G., Riedel, D. & Kaufmann, S. H. Interleukin-12 secretion by Mycobacterium tuberculosis-infected macrophages. Infection and immunity 65, 1936-1938 (1997). (Pubitemid 27193622)
49. Fenton, M. J. et al. Induction of gamma interferon production in human alveolar macrophages by Mycobacterium tuberculosis. Infection and immunity 65, 5149-5156 (1997). (Pubitemid 27513563)
50. Bradbury, M. G. &Moreno, C. Effect of lipoarabinomannan and mycobacteria on tumour necrosis factor production by different populations of murine macrophages. Clinical and experimental immunology 94, 57-63 (1993). (Pubitemid 23308365)
51. Britton, W. J., Meadows, N., Rathjen, D. A., Roach, D. R. & Briscoe, H. A tumor necrosis factor mimetic peptide activates amurine macrophage cell line to inhibit mycobacterial growth in a nitric oxide-dependent fashion. Infection and immunity 66, 2122-2127 (1998). (Pubitemid 28194111)
52. Sugawara, I., Udagawa, T. &Yamada, H. Rat neutrophils prevent the development of tuberculosis. Infect Immun 72, 1804-1806 (2004). (Pubitemid 38263807)
53. Martineau, A. R. et al. Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest 117, 1988-1994 (2007). (Pubitemid 47036333)
54. Sawant, K. V. & McMurray, D. N. Guinea pig neutrophils infected with Mycobacterium tuberculosis produce cytokines which activate alveolar macrophages in noncontact cultures. Infection and immunity 75, 1870-1877 (2007). (Pubitemid 46559456)
55. Engele, M. et al. Induction of TNF in human alveolar macrophages as a potential evasion mechanism of virulent Mycobacterium tuberculosis. J Immunol 168, 1328-1337 (2002). (Pubitemid 34094503)
56. Orme, I.M., Roberts, A. D.,Griffin, J. P.&Abrams, J. S. Cytokine secretion by CD4 T lymphocytes acquired in response to Mycobacterium tuberculosis infection. J Immunol 151, 518-525 (1993). (Pubitemid 23207017)
57. Andersen, P. & Smedegaard, B. CD4(1) T-cell subsets that mediate immunological memory to Mycobacterium tuberculosis infection in mice. Infection and immunity 68, 621-629 (2000). (Pubitemid 30056515)
58. Flesch, I. & Kaufmann, S. H. Mycobacterial growth inhibition by interferongamma-activated bone marrow macrophages and differential susceptibility among strains of Mycobacterium tuberculosis. J Immunol 138, 4408-4413 (1987). (Pubitemid 17096447)
59. Bonecini-Almeida, M. G. et al. Induction of in vitro human macrophage anti-Mycobacterium tuberculosis activity: requirement for IFN-gamma and primed lymphocytes. J Immunol 160, 4490-4499 (1998). (Pubitemid 28217308)
60. Egen, J. G. et al. Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28, 271-284 (2008).
61. Barnes, P. F. et al. Patterns of cytokine production by mycobacterium-reactive human T-cell clones. Infection and immunity 61, 197-203 (1993). (Pubitemid 23015417)
62. Zganiacz, A. et al. TNF-alpha is a critical negative regulator of type 1 immune activation during intracellular bacterial infection. J Clin Invest 113, 401-413 (2004). (Pubitemid 38544184)
63. Bekker, L. G. et al. Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 68, 6954-6961 (2000).
64. Fremond, C. M. et al. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 114, 1790-1799 (2004). (Pubitemid 40385535)
65. Fremond, C. M. et al. IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 179, 1178-1189 (2007).
66. Gonzalez-Juarrero, M. et al. Immune response to Mycobacterium tuberculosis and identification of molecular markers of disease. American journal of respiratory cell and molecular biology 40, 398-409 (2009).
67. Kang, D. D., Lin, Y., Moreno, J. R., Randall, T. D. & Khader, S. A. Profiling early lung immune responses in the mouse model of tuberculosis. PloS one 6, e16161 (2011).
68. Filen, S. et al. Activating transcription factor 3 is a positive regulator of human IFNG gene expression. J Immunol 184, 4990-4999 (2010).