Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages

doi:10.1084/jem.175.4.1111

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Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages

J Chan, Y Xing, RS Magliozzo and BR Bloom
Department of Medicine, University of Medicine and Dentistry of New Jersey, Newark 07103.

Tuberculosis remains one of the major infectious causes of morbidity and mortality in the world, yet the mechanisms by which macrophages defend against Mycobacterium tuberculosis have remained obscure. Results from this study show that murine macrophages, activated by interferon gamma, and lipopolysaccharide or tumor necrosis factor alpha, both growth inhibit and kill M. tuberculosis. This antimycobacterial effect, demonstrable both in murine macrophage cell lines and in peritoneal macrophages of BALB/c mice, is independent of the macrophage capacity to generate reactive oxygen intermediates (ROI). Both the ROI-deficient murine macrophage cell line D9, and its ROI-generating, parental line J774.16, expressed comparable antimycobacterial activity upon activation. In addition, the oxygen radical scavengers superoxide dismutase (SOD), catalase, mannitol, and diazabicyclooctane had no effect on the antimycobacterial activity of macrophages. These findings, together with the results showing the relative resistance of M. tuberculosis to enzymatically generated H2O2, suggest that ROI are unlikely to be significantly involved in killing M. tuberculosis. In contrast, the antimycobacterial activity of these macrophages strongly correlates with the induction of the L-arginine- dependent generation of reactive nitrogen intermediates (RNI). The effector molecule(s) that could participate in mediating this antimycobacterial function are toxic RNI, including NO, NO2, and HNO2, as demonstrated by the mycobacteriocidal effect of acidified NO2. The oxygen radical scavenger SOD adventitiously perturbs RNI production, and cannot be used to discriminate between cytocidal mechanisms involving ROI and RNI. Overall, our results provide support for the view that the L-arginine-dependent production of RNI is the principal effector mechanism in activated murine macrophages responsible for killing and growth inhibiting virulent M. tuberculosis.
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van Crevel, R., Ottenhoff, T. H. M., van der Meer, J. W. M. (2002). Innate Immunity to Mycobacterium tuberculosis. Clin. Microbiol. Rev. 15: 294-309 [Abstract] [Full Text]
Portales-Perez, D. P., Baranda, L., Layseca, E., Fierro, N. A., de la Fuente, H., Rosenstein, Y., Gonzalez-Amaro, R. (2002). Comparative and Prospective Study of Different Immune Parameters in Healthy Subjects at Risk for Tuberculosis and in Tuberculosis Patients. CVI 9: 299-307 [Abstract] [Full Text]
Pasula, R., Wisniowski, P., Martin II, W. J. (2002). Fibronectin Facilitates Mycobacterium tuberculosis Attachment to Murine Alveolar Macrophages. Infect. Immun. 70: 1287-1292 [Abstract] [Full Text]
Engele, M., Castiglione, K., Schwerdtner, N., Wagner, M., Bolcskei, P., Rollinghoff, M., Stenger, S. (2002). Induction of TNF in Human Alveolar Macrophages As a Potential Evasion Mechanism of Virulent Mycobacterium tuberculosis. J. Immunol. 168: 1328-1337 [Abstract] [Full Text]
EDWARDS, K. M., CYNAMON, M. H., VOLADRI, R. K. R., HAGER, C. C., DESTEFANO, M. S., THAM, K. T., LAKEY, D. L., BOCHAN, M. R., KERNODLE, D. S. (2001). Iron-cofactored Superoxide Dismutase Inhibits Host Responses to Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med. 164: 2213-2219 [Abstract] [Full Text]
Holscher, C., Atkinson, R. A., Arendse, B., Brown, N., Myburgh, E., Alber, G., Brombacher, F. (2001). A Protective and Agonistic Function of IL-12p40 in Mycobacterial Infection. J. Immunol. 167: 6957-6966 [Abstract] [Full Text]
Waters, W. R., Nonnecke, B. J., Rahner, T. E., Palmer, M. V., Whipple, D. L., Horst, R. L. (2001). Modulation of Mycobacterium bovis-Specific Responses of Bovine Peripheral Blood Mononuclear Cells by 1,25-Dihydroxyvitamin D3. CVI 8: 1204-1212 [Abstract] [Full Text]
Chan, E. D., Chan, J., Schluger, N. W. (2001). What is the Role of Nitric Oxide in Murine and Human Host Defense against Tuberculosis? . Current Knowledge. Am. J. Respir. Cell Mol. Bio. 25: 606-612 [Abstract] [Full Text]
Raman, S., Song, T., Puyang, X., Bardarov, S., Jacobs, W. R. Jr., Husson, R. N. (2001). The Alternative Sigma Factor SigH Regulates Major Components of Oxidative and Heat Stress Responses in Mycobacterium tuberculosis. J. Bacteriol. 183: 6119-6125 [Abstract] [Full Text]
Springer, B., Master, S., Sander, P., Zahrt, T., McFalone, M., Song, J., Papavinasasundaram, K. G., Colston, M. J., Boettger, E., Deretic, V. (2001). Silencing of Oxidative Stress Response in Mycobacterium tuberculosis: Expression Patterns of ahpC in Virulent and Avirulent Strains and Effect of ahpC Inactivation. Infect. Immun. 69: 5967-5973 [Abstract] [Full Text]
Musso, T., Badolato, R., Ravarino, D., Stornello, S., Panzanelli, P., Merlino, C., Savoia, D., Cavallo, R., Ponzi, A. N., Zucca, M. (2001). Interaction of Bartonella henselae with the Murine Macrophage Cell Line J774: Infection and Proinflammatory Response. Infect. Immun. 69: 5974-5980 [Abstract] [Full Text]
Peteroy-Kelly, M., Venketaraman, V., Connell, N. D. (2001). Effects of Mycobacterium bovis BCG Infection on Regulation of L-Arginine Uptake and Synthesis of Reactive Nitrogen Intermediates in J774.1 Murine Macrophages. Infect. Immun. 69: 5823-5831 [Abstract] [Full Text]
Harris, N. B., Barletta, R. G. (2001). Mycobacterium avium subsp. paratuberculosis in Veterinary Medicine. Clin. Microbiol. Rev. 14: 489-512 [Abstract] [Full Text]
Orme, I. M. (2001). The search for new vaccines against tuberculosis. J. Leukoc. Biol. 70: 1-10 [Abstract] [Full Text]
Flynn, J. L., Chan, J. (2001). Tuberculosis: Latency and Reactivation. Infect. Immun. 69: 4195-4201 [Full Text]