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Inflammation pp 139-151 | Cite as

The Inflammatory Response in Mycobacterium Tuberculosis Infection

  • Zahra Toossi
Chapter

Abstract

Infection with Mycobacterium tuberculosis (MTB) is accompanied by an intense local inflammatory response which may be critical to the pathogenesis of tuberculosis. Activation of components of the innate immune response, such as recruitment of polymorphonuclear (PMN) and mononuclear phagocytes and induction of pro-inflammatory cytokines, such as tumor necrosis factor α (TNF-α), by MTB occurs early after MTB infection, however, may persist as the organism establishes itself within granulomas. MTB and its protein and non-protein components are potent in induction of cytokines and chemokines from PMN and monocytes. This review focuses on the interaction of MTB and the host with regard to activation of the innate immune response. It also attempts to identify the potential impact of this early response on the subsequent pathogenesis of MTB, and its role in development and extent of tuberculosis. Insights into the initiation and persistent of the inflammatory response may allow the application of anti-inflammatory agents as adjuncts in the treatment of tuberculosis.

Key words

polymorphonuclear monocyte cytokine chemokine tumor necrosis factor α Mycobacterium tuberculosis tuberculosis. 

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References

  1. Abou-Zeid C., Ratliff T. L., Wiker H. G., Harboe M., Bennedsen J. and Rock G. A. W. (1988): Characterization of fibronectin-binding antigens released by Mycobacterium tuberculosis and Mycobacterium bovin BCG. Infect. Immun., 56, 3046–3047.PubMedGoogle Scholar
  2. Actor J. K., Olsen M., Jagannath C. and Hunter R. L. (1999): Relationship of survival, organism containment, and acute murine tuberculosis. J. Interferon Cytokine Res., 19, 1183–1193.PubMedCrossRefGoogle Scholar
  3. Aung H., Toossi Z., Wisnieski J. J., Culp L. A., Phillips N. B., Averill L. E., Daniel T. M. and Ellner J. J. (1996): Induction expression of tumor necrosis factor alpha by the 30 kDa alpha anti- gen of Mycobacaterium tuberculosis synergism with fibronectin. J. Clin. Invest., 98, 1261–1268.PubMedCrossRefGoogle Scholar
  4. Barnes P. F., Chatterjee D., Abrams J. S., Lu S., Want E., Yamamura M., Brennan P. J. and Modin R. L. (1992): Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan. Relationship to chemical structure. J. Immunol., 149, 541–547.Google Scholar
  5. Barnes P. F., Lu S., Abrams J. S., Wang E., Yamamure M. and Modlin R. L. (1993): Cytokine production at the site of the disease in human tuberculosis. Infect. Immun., 61, 3482–3489.PubMedGoogle Scholar
  6. Bogdan C., Paik J., Vodovotz Y. and Nathan C. (1992): Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor f3 and interleukin-10. J. Biol. Chem., 267, 2301–2308.Google Scholar
  7. Boom W. H. (1999): Gammadelta T cells and Mycobacterium tuberculosis. Microbes Infect., 1, 187–195.PubMedCrossRefGoogle Scholar
  8. Byrd T. F. (1997): Tumor necrosis factor (TNF) promotes growth of Mycobacterium tuberculosis in human monocytes. Iron-mediated growth suppression is correlated with decreased release of TNF. J. Clin. Invest., 99, 2528–2529.CrossRefGoogle Scholar
  9. Casatella A. M. (1999): Neutrophil-derived proteins: Selling cytokines by the pound. Adv. Immunol., 73, 369–494.CrossRefGoogle Scholar
  10. Chan J. and Kaufman H. E. (1994): Immune mechanisms of protection. In Bloom A. S. M. (ed.): Tuberculosis: pathogenesis, protection and control. Washington, DC, 389–415.Google Scholar
  11. Dahl K. E., Shiratsuchi H., Hamilton B. D., Ellner J. J. and Toossi Z. (1996): Selective induction of TGF-f3 in human monocytes by lipoarabinomannan of M. tuberculosis. Infect. Immun., 64, 399–405.PubMedGoogle Scholar
  12. Ding A., Nathan C. and Srimal S. (1990): Macrophage deactivating factor and TGF-f3 inhibit macrophage nitrogen oxide synthesis by IFN gamma. Immunology, 145, 940–945.Google Scholar
  13. Ehlers S., Benini J., Kutsch S., Endres R., Rietschel E. T. and Pfeffer K. (1999): Fatal granuloma necrosis without exacerbated mycobaterial growth in tumor necrosis factor receptor gene deficient mice intravenously infected with Mycobacterium avium. Infect. Immun., 67, 3571–3579.PubMedGoogle Scholar
  14. Ellner J. J. (1997): The human response in tuberculosis. J. Infect. Dis., 176, 1351–1359.PubMedCrossRefGoogle Scholar
  15. Fenhalls G., Wong A., Bezuidenhout J., van Helden P., Bardin P. and Lukey P. T. (2000): In situ production of gamma interleukin-4 and tumor necrosis factor alpha mRNA in human lung tuberculosis granulomas. Infect. Immun., 68 2827–2836.Google Scholar
  16. Fenton M. J., Vermeulen M. W., Kim S., Burdick M., Strieter R. M. and Kornfeld H. (1997): Induction of gamma interferon production in human alveolar macrophages by Mycobacterium tuberculosis. Infect. Immun., 65, 5149–5156.PubMedGoogle Scholar
  17. Flynn J. L. Goldstein M. M., Chan J., Triebold K. J., Pfeffer K., Lowenstein C. J., Schreiber R., Mak T. W. and Bloom B. R. (1995): Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity, 2 561–572.Google Scholar
  18. Fratazzi C., Arbeit R. D., Carini C., Balcewicz-Sablinska M. K., Keane J., Kornfeld H. and Remold H. G. (1999): Macrohpage apoptosis in mycobacterial infections. J. Leukoc. Biol., 66, 763–764.PubMedGoogle Scholar
  19. Fulton S. A., Martin T. D., Redline R. W. and Boom W. H. (2000): Pulmonary immune responses during primary Myco Calmette-Guerin bacillus infection in C57B16 mice. Am. J. Respir. Cell Mol. Biol., 22, 333–343.PubMedGoogle Scholar
  20. Fulton S. A., Johnsen J. M., Wolf S. F., Sieberth D. S. and Boom W. H. (1996): Interleukin-12 production by human infected with Mycobacterium tuberculosis: role of phagocytosis. Infect. Immun., 64, 25–23.Google Scholar
  21. Garrait V., Cadranel J., Esvant H., Herry I., Morinet E, Mayaud C. and Israel-Biet D. (1997): Tuberculosis generates a microenvironment enhancing the productive infection of local lymphocytes by HIV. J. Immunol., 159, 2824–2830.Google Scholar
  22. Hirsch C. S., Ellner J. J., Russell D. G. and Rich E. A. (1994a): Complement receptor-mediated uptake and tumor necrosis a-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J. Immunol., 152, 743–749.PubMedGoogle Scholar
  23. Hirsch C. S., Toossi Z., Othieno C., Johnson J. L., Schwander S. K., Robertson S., Wallis R.S., Edmonds K. A., Mugerwa R., Peters P. and Ellner J. J. (1999): Depressed T-cell interferon--gamma responses in pulmonary tuberculosis analysis of underlying mechanisms and modulation with therapy. J. Infect. Dis., 180, 2069–2073.PubMedCrossRefGoogle Scholar
  24. Hirsch C. S., Yoneda T., Ellner J. J., Averill L. E. and Toossi Z. (1994b): Enhancement of intracellular growth of M. tuberculosis in human monocytes by transforming growth factor beta. J. Infect. Dis., 170, 1229–1237.PubMedCrossRefGoogle Scholar
  25. Howard A. D. and Zwilling B. S. (1998): Cytokine production by CD4 and CD8 T cells during the growth of Mycobacterium tuberculosis in mice. Clin. Exp. Immunol., 113, 443–449.PubMedCrossRefGoogle Scholar
  26. Hunter S. W., Gaylord B. E. and Brennan P. J. (1986): Structure and antigenicity of the phosophorylated lipopolysa antigens from the leprosy and tubercle bacilli. J. Biol. Chem., 261, 12345–12351.PubMedGoogle Scholar
  27. Huygen K., Van Vooren J. P., Turneer M., Bosmans R., Dierckx P. and DeBruyn J. (1988): Specific lymphoproliferation, gamma interferon production, and serum immunoglobulin G directed against a purified 32 kDa mycobacterial protein antigen (P32) in patients with active tuberculosis. Scand. J. Immunol., 27, 187–194.Google Scholar
  28. Jacobs M., Brown N., Allie N. and Ryffel B. (2000): Fatal Mycobacterium bovis BCG infection in TNF LT-alpha-deficient mice. Chest, 117, 103–109.CrossRefGoogle Scholar
  29. Kasahara K., Sato I., Ogura K., Takeuchi H., Kobayashi K. and Adachi M. (1998): Expression of chemokines and rapid cell death in human blood neutrophils by M. tuberculosis. J. Infect. Dis., 178, 127–137.PubMedCrossRefGoogle Scholar
  30. Kasahari V. M., Chen Y. Q., Su M. W., Ramirez F. and Uitto J. (1990): Tumor necrosis factor a and interferon y suppress the activation of human type I collagen gene expression by transforming growth factor 3 1. J. Clin. Invest., 86, 1489–1494.CrossRefGoogle Scholar
  31. Kemp K., Hviid L., Kharazmi A. and Kemp M. (1997): Interferon-gamma production by human T cells and natural killer cells in vitro in response to antigens from the two intracellular pathogens Mycobacterium tuberculosis and Leishmania major. Scand. J. Immunol., 46, 495–499.PubMedCrossRefGoogle Scholar
  32. Kim S. J., Angel P., Lafyatis R. and Roberts A. B. (1990): Autoinduction of transforming growth factor 31 is mediated by the AP-1 complex. Mol. Cell Biol., 10, 1492–1495.PubMedGoogle Scholar
  33. Kindler V., Sappino A. P, Grau G. E., Piguer P. F. and Vassalli P. (1989): The inducing role of tumor necrosis factor in the development of bacterial granulomas during BCG infection. Cell, 56, 731–740.PubMedCrossRefGoogle Scholar
  34. Lawn S. D., Shattock R. J., Acheampong J. W., Lal R. B., Folks T. M., Griffin G. E. and Butera S. T. (1999): Sustained plasma TNF-alpha and HIV-1 load despite resolution of other parame- ters of immune activation during treatment of tuberculosis in Africans. AIDS, 13, 2231–2237.Google Scholar
  35. Lin Y., Zhang H., Gong J. and Barnes P. F. (1996): Absence of a prominent TH2 cytokine response in human tuberculosis. Infect. Immun., 64, 1351–1356.PubMedGoogle Scholar
  36. May M. and Spagnuolo P J. (1987): Evidence for activation of the respiratory burst in the interaction of human neutrophils with M. tuberculosis. Infect. Immun., 55, 2304–2307.Google Scholar
  37. Mustafa T., Phyu S., Nilsen R., Jonsson R. and Bjune G. (2000): In situ expression of cytokine and cellular phenotypes in mice with slowly progressive primary tuberculosis. Scand. J. Immunol., 51, 548–556.Google Scholar
  38. Muthuswamy P, Hu Y. C., Carasso B., Antonio M. and Dandamudi N. (1995): Prednisone as adjunctive therapy in the management of pulmonary tuberculosis report of 12 cases and review of the literature. Chest, 107, 1621–1630.PubMedCrossRefGoogle Scholar
  39. North R. J. (1995): M. tuberculosis strikingly more virulent for mice when given via the respiratory than via the intravenous route. J. Infect. Dis., 172, 1550–1553.Google Scholar
  40. Oppenheim J. J., Zacharie C. O. C., Mokaida N. and Matsamushima K. (1991): Properties of the novel pro-infiamma “intercine” cytokine family. Annu. Rev. Immunol., 9 617–648.Google Scholar
  41. Orme I. M. and Cooper A. M. (1999): Cytokine/chemokine cascades in immunity to tuberculosis. Immunol. Today, 20, 307–312.PubMedCrossRefGoogle Scholar
  42. Othieno C., Hirsch C. S., Hamilton B. D., Wilkinson K., Ellner J. J. and Toossi Z. (1999): Interaction of M. tuberculosis-induced transforming growth factor [31 and interleukin 10. Infect. Immun., 67, 5730–5735.Google Scholar
  43. Rhoades E. R., Frank A. A. and Orme I. M. (1997): Progresion of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber. Lung Dis., 78, 57–66.PubMedCrossRefGoogle Scholar
  44. Rich E. A., Torres M., Sada E., Finegan C. K., Hamilton B. D. and Toossi Z. (1997): Mycobacterium tuberculosis-stimulated expression of inducible nitric oxide synthase and production of nitric oxide by human alveolar macrophages. Tuber. Lung Dis., 78, 247–255.Google Scholar
  45. Riedel D. D. and Kaufmann S. H. (1997): Chemokine secretion by human polymorphonuclear granulocytes after stimulation with M. tuberculosis and lipoarabinomannan. Infect. Immun., 65, 4620–4523.PubMedGoogle Scholar
  46. Rollins B. J. (1997): Chemokines. Blood, 90, 909–928.Google Scholar
  47. Rook G. A. W. and Hernandez-Pando R. (1996): The pathogenesis of tuberculosis. Annu. Rev. Microbiol., 50, 259–284.PubMedCrossRefGoogle Scholar
  48. Sadek M. I., Sada E., Toossi Z., Schwander S. K. and Rich E. A. (1997): Chemokines induced by infection of mono phagocytes with M. tuberculosis and in the lungs during active pulmonary tuberculosis. Tuber. Lung Dis., 78, 247–255.CrossRefGoogle Scholar
  49. Schwander S. K., Sada E., Torres M., Escobedo D., Sierra J. G. and Alt Rich E. A. (1996): T lymphocytic and immature macrophage alveolitis in active pulmonary tuberculosis. J. Infect. Dis., 173, 1267–1272.PubMedCrossRefGoogle Scholar
  50. Schwander S. K., Torres M., Carranza C., Escobedo D., Tary-Lehmann M., Anderson P., Toossi Z., Ellner J. J., Rich E. A. and Sada E. (2000): Pulmonary mononuclear cell responses to antigens of Mycobacterium tuberculosis in healthy household contacts of patients with active tuberculosis and healthy controls from the community. J. Immunol., 165, 1479–1485.PubMedGoogle Scholar
  51. Senderovitz T. and Viskum K. (1994): Corticosteroids and tuberculosis. Res. Med., 88, 561–569.CrossRefGoogle Scholar
  52. Silver R. F., Li Q and Ellner J. J. (1998): Expression of virulence of Mycobacerium tuberculosis with human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis factor alpha but not with evasion of lymphocyte-dependent monocyte effector functions. Infect. Immun., 66, 1190–1199.PubMedGoogle Scholar
  53. Smith D. W., Wiegeshaus E. H., Navalkar R. and Grover A. A. (1966): Host-parasite relationships in experimental airborne tuberculosis. I. Preliminary studies in BCG-vaccinated and non-vaccinated animals. J. Bacteriol., 91, 718–724.PubMedGoogle Scholar
  54. Snider D. E., Raviglione M. and Kochi A. (1994): Global burden of tuberculosis. In Bloom A. S. M. (ed.): Tuberculosis: pathogenesis, protection and control. Washington DC, 3–11.Google Scholar
  55. Solis-Herruzo J. A., Brenner D. A. and Chojkier M. (1998): Tumor necrosis factor a inhibits collagen gene transcription and collagen synthesis in cultured human fibroblasts. J. Biol. Chem., 163, 5841–5847.Google Scholar
  56. Sporn M. B., Roberts A. M., Wakefield L. M. and Assoian R. K. (1986): Transforming growth factor 13 biological function and chemical structure. Science, 233, 532–535.PubMedCrossRefGoogle Scholar
  57. Tavares J. L., Wangoo A., Dilworth P., Marshall B., Kotecha S. and Shaw R. J. (1997): Thalidomide reduces tumor necrosis factor a alpha production by human alveolar macrophages. Respir. Med., 91, 31–39.PubMedCrossRefGoogle Scholar
  58. Toossi Z. (1996): Cytokine circuits in tuberculosis. Infect. Agents Dis., 5, 98–107.PubMedGoogle Scholar
  59. Toossi Z., Gogate P., Shiratsuchi H., Young T. and Ellner J. J. (1995): Enhanced production of transforming growth factor 3 (TGF13) by blood monocytes from patients with active tuberculosis and presence of TGF13 in tuberculosis granulomatous lung lesions. J. Immunol., 154, 465–473.PubMedGoogle Scholar
  60. Toossi Z., Hirsch C. S., Hamilton B. D., Knuth C. K., Friedlander M. A. and Rich E. A. (1996): Decreased production of transforming growth factor 131 (TGFf31) in human alveolar macrophages. J. Immunol., 156, 3461–3468.PubMedGoogle Scholar
  61. Toossi Z., Xia L. and Salvekar A. (1999): Transcriptional activities of human immunodeficiency virus (HIV) by Mycobacterium tuberculosis in human monocytes. Clin. Exp. Immunol., 117, 324–330.PubMedCrossRefGoogle Scholar
  62. Torres M., Herrera T., Villareal H. and Sada E. (1998): Cytokine profiles for peripheral blood lymphocytes from patients with active pulmonary tuberculosis and healthy household contacts in response to 30 kD antigen of Mycobacterium tuberculosis. Infect. Immun., 66, 176–180.PubMedGoogle Scholar
  63. Tramontana J. M., Utaipat U., Molly A., Akarasewi P., Burroughs M., Makonkawkeypoon S., Johnson B., Klausner J. D., Rom W. and Kaplan G. (1995): Thalidomide treatment reduces tumor necrosis factor alpha production and enhances weight gain in patients with pulmonary tuberculosis. Mol. Med., 1, 384–397.PubMedGoogle Scholar
  64. Tsao T. C., Hong J., Huang C., Yang P., Liao S. K. and Chang K. S. (1999): Increased TNF-alpha, IL-1 beta and IL-6 levels in bronchoalveolar lavage fluid with the upregulation of their mRNA in macrophages lavaged from patients active pulmonary tuberculosis. Tuber. Lung Dis., 79, 279–285.PubMedCrossRefGoogle Scholar
  65. Valone S. E., Rich E. A., Wallis R. S. and Ellner J. J. (1988): Expression of tumor necrosis factor in vitro by human mononuclear phagocytes stimulated with whole Mycobacterium bovis BCG and mycobacterial antigens. Infect. Immun., 56, 3313–3333.PubMedGoogle Scholar
  66. Vanham G., Edmonds K. E., Qing L., Hom D., Toossi Z., Joness B., Daley C., Huebner R., Kestens L., Gigase P. and Ellner J. J. (1996): Generalized immune activation in pulmonary tuberculosis: co-activation with HIV infection. Clin. Exp. Immunol., 103, 30–34.PubMedCrossRefGoogle Scholar
  67. Vicenzi E., Biswas P., Mengozzi M. and Poli G. (1997): Role of pro-inflammatory cytokines and 13-chemokines in controlling HIV replication. J. Leukoc. Biol., 62, 34–40.PubMedGoogle Scholar
  68. Wahl S. M., Allen J. B., Weeks B. S., Wong H. L. and Klotman P. E. (1993): Transforming growth factor (3 enhances integrin expression and type IV collagenase secretion in human monocytes. Proc. Natl. Acad. Sci. USA, 90, 4577–4581.PubMedCrossRefGoogle Scholar
  69. Wallis R. S., Fujiwara H. and Ellner J. J. (1996a): Direct stimulation of monocyte release of interleukin 1 by mycobacterial protein antigens. J. Immunol., 136, 193–196.Google Scholar
  70. Wallis C. C., Nsubuga R, Whalen C. C., Mugerwa R. D., Okwera A., Oette D., Jackson J. L., Johnson J. J. and Ellner J. J. (1996b): Pentoxifylline therapy in human immunodeficiency virus-serpositive persons with tuberculosis: a randomized controlled trial. J. Infect. Dis., 174, 727–733.PubMedCrossRefGoogle Scholar
  71. Wallis R. S., Paranjape R. and Phillips M. (1993): Identification by two-dimensional gel electrophoresis of a 58-kilodalton tumor necrosis factor-inducing protein of Mycobacterium tuberculosis. Infect. Immun., 61, 627–632.Google Scholar
  72. Whalen C., Horsburgh C. R., Hom D., Lahart C., Simberkoff M. and Ellner J. J. (1995): Accelerated course of human immunodeficiency virus infection after tuberculosis. Am. J. Respir. Crit. Care Med., 151, 129–135.PubMedGoogle Scholar
  73. Zabel A. and Ulrich Schade F. (1993): Inhibition of endogenous TNF formation by Pentoxifylline. Immunobiology, 187, 447–463.PubMedCrossRefGoogle Scholar
  74. Zhang Y., Broser M., Cohen H., Bodkin M., Law K., Reibman J. and Rom W. N. (1995): Enhanced interleukin and gene expression in macrophage after exposure to Mycobacterium tuberculosis and its comp. J. Clin. Invest., 95, 586–592.PubMedCrossRefGoogle Scholar
  75. Zhu W., Downey J. S., Gu J., Di Padova F., Gram H. and Han J. (2000): Regulation of TNF expression by multiple mitogen-activated protein kinase pathways. J. Immunol., 164, 6349–6358.PubMedGoogle Scholar
  76. Zugmaier G., Paik S., Wilding G., Knabbe C., Bano M., Lupu R., Deschauer B., Simpson S., Dickson R. B. and Lippman M. (1991): Transforming growth factor 13 1 induces cachexia and systemic fibrosis without an antitumor effect in nude mice. Cancer Res., 51, 3590–3594.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2001

Authors and Affiliations

  • Zahra Toossi
    • 1
  1. 1.Department of Medicine Case Western UniversityVeterans Administration HospitalClevelandUSA

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