Tumor necrosis factor blockade in chronic murine tuberculosis enhances granulomatous inflammation and disorganizes granulomas in the lungs

Infection and Immunity

Volumn 76, Issue 3, 2008, Pages 916-926

  Chakravarty, Soumya D ^a   Zhu, Guofeng ^a   Tsai, Ming C ^a,e   Mohan, Vellore P ^a,f   Marino, Simeone ^b   Kirschner, Denise E ^b   Huang, Luqi ^c   Flynn, JoAnne ^d   Chan, John ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c INSTITUTE OF CHINESE MATERIA MEDICA   (China)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f FLORIDA DEPARTMENT OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GRANULOMATOUS INFLAMMATION; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOREGULATION; INFLAMMATORY CELL; INFLAMMATORY INFILTRATE; LASER CAPTURE MICRODISSECTION; LUNG GRANULOMA; LUNG PARENCHYMA; LUNG TUBERCULOSIS; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; GENE EXPRESSION PROFILING; GENETICS; GRANULOMA; IMMUNOLOGY; INFLAMMATION; LUNG; MICROBIOLOGY; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS;

ANIMALS; B-LYMPHOCYTES; CYTOKINES; FEMALE; GENE EXPRESSION PROFILING; GRANULOMA; INFLAMMATION; LUNG; MACROPHAGES; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 40749108974     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01011-07     Document Type: Article

References (46)

1. Algood, H. M., J. Chan, and J. L. Flynn. 2003. Chemokines and tuberculosis. Cytokine Growth Factor Rev. 14:467-477.
2. Algood, H. M., P. L. Lin, and J. L. Flynn. 2005. Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis. Clin. Infect. Dis. 41(Suppl. 3):S189-S193.
3. + cells in vivo during Mycobacterium tuberculosis infection. J. Immunol. 172:6846-6857.
4. Aloisi, F., and R. Pujol-Borrell. 2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol 6:205-217.
5. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174:1549-1555.
6. Bromley, S. K., D. A. Peterson, M. D. Gunn, and M. L. Dustin. 2000. Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation. J. Immunol. 165:15-19.
7. Chakravarty, S. D., J. Xu, B. Lu, C. Gerard, J. Flynn, and J. Chan. 2007. The chemokine receptor CXCR3 attenuates the control of chronic Mycobacterium tuberculosis infection in BALB/c mice. J. Immunol. 178:1723-1735.
8. Chan, J., Y. Xing, R. S. Magliozzo, and B. R. Bloom. 1992. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175:1111-1122.
9. Cope, A. P., R. S. Liblau, X. D. Yang, M. Congia, C. Laudanna, R. D. Schreiber, L. Probert, G. Kollias, and H. O. McDevitt. 1997. Chronic tumor necrosis factor alters T cell responses by attenuating T cell receptor signaling. J. Exp. Med. 185:1573-1584.
10. de Vries, J. E. 1995. Immunosuppressive and anti-inflammatory properties of interleukin 10. Ann. Med. 27:537-541.
11. Drayton, D. L., S. Liao, R. H. Mounzer, and N. H. Ruddle. 2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7:344-353.
12. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
13. Flynn, J. L., M. M. Goldstein, J. Chan, K. J. Triebold, K. Pfeffer, C. J. Lowenstein, R. Schreiber, T. W. Mak, and B. R. Bloom. 1995. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2:561-572.
14. Flynn, J. L., C. A. Scanga, K. E. Tanaka, and J. Chan. 1998. Effects of aminoguanidine on latent murine tuberculosis. J. Immunol. 160:1796-1803.
15. Gonzalez-Juarrero, M., O. C. Turner, J. Turner, P. Marietta, J. V. Brooks, and I. M. Orme. 2001. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect. Immun. 69:1722-1728.
16. Hodge-Dufour, J., M. W. Marino, M. R. Horton, A. Jungbluth, M. D. Burdick, R. M. Strieter, P. W. Noble, C. A. Hunter, and E. Pure. 1998. Inhibition of interferon gamma induced interleukin 12 production: a potential mechanism for the anti-inflammatory activities of tumor necrosis factor. Proc. Natl. Acad. Sci. USA 95:13806-13811.
17. Kaplan, G., F. A. Post, A. L. Moreira, H. Wainwright, B. N. Kreiswirth, M. Tanverdi, B. Mathema, S. V. Ramaswamy, G. Walther, L. M. Steyn, C. E. Barry III, and L. G. Bekker. 2003. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect. Immun. 71:7099-7108.
18. Kassiotis, G., and G. Kollias. 2001. TNF and receptors in organ-specific autoimmune disease: multi-layered functioning mirrored in animal models. J. Clin. Investig. 107:1507-1508.
19. Kassiotis, G., and G. Kollias. 2001. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 193:427-434.
20. Keane, J., S. Gershon, R. P. Wise, E. Mirabile-Levens, J. Kasznica, W. D. Schwieterman, J. N. Siegel, and M. M. Braun. 2001. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N. Engl. J. Med. 345:1098-1104.
21. Kindler, V., A. P. Sappino, G. E. Grau, P. F. Piguet, and P. Vassalli. 1989. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 56:731-740.
22. Lancet. 2006. XDR-TB - a global threat. Lancet 368:964.
23. Liu, P. T., S. Stenger, H. Li, L. Wenzel, B. H. Tan, S. R. Krutzik, M. T. Ochoa, J. Schauber, K. Wu, C. Meinken, D. L. Kamen, M. Wagner, R. Bals, A. Steinmeyer, U. Zugel, R. L. Gallo, D. Eisenberg, M. Hewison, B. W. Hollis, J. S. Adams, B. R. Bloom, and R. L. Modlin. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311:1770-1773.
24. Mackay, C. R. 2001. Chemokines: immunology's high impact factors. Nat. Immunol. 2:95-101.
25. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94:5243-5248.
26. Maglione, P. J., J. Xu, and J. Chan. 2007. B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J. Immunol. 178:7222-7234.
27. Marino, S., D. Sud, H. Plessner, P. L. Lin, J. Chan, J. L. Flynn, and D. E. Kirschner. 2007. Differences in reactivation of tuberculosis induced from anti-TNF treatments are based on bioavailability in granulomatous tissue. PLoS Comput. Biol. 3:1909-1924.
28. Means, T. K., S. Wang, E. Lien, A. Yoshimura, D. T. Golenbock, and M. J. Fenton. 1999. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163:3920-3927.
29. Mebius, R. E. 2003. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3:292-303.
30. Mohan, V. P., C. A. Scanga, K. Yu, H. M. Scott, K. E. Tanaka, E. Tsang, M. M. Tsai, J. L. Flynn, and J. Chan. 2001. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect. Immun. 69:1847-1855.
31. Moser, B., and P. Loetscher. 2001. Lymphocyte traffic control by chemokines. Nat. Immunol. 2:123-128.
32. Poznansky, M. C., I. T. Olszak, R. Foxall, R. H. Evans, A. D. Luster, and D. T. Scadden. 2000. Active movement of T cells away from a chemokine. Nat. Med. 6:543-548.
33. Proudfoot, A. E. 2002. Chemokine receptors: multifaceted therapeutic targets. Nat. Rev. Immunol. 2:106-115.
34. Scanga, C. A., V. P. Mohan, H. Joseph, K. Yu, J. Chan, and J. L. Flynn. 1999. Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect. Immun. 67:4531-4538.
35. Sedgwick, J. D., D. S. Riminton, J. G. Cyster, and H. Korner. 2000. Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol. Today 21:110-113.
36. Shiloh, M. U., and C. F. Nathan. 2000. Reactive nitrogen intermediates and the pathogenesis of Salmonella and mycobacteria. Curr. Opin. Microbiol. 3:35-42.
37. Stenger, S., and R. L. Modlin. 2002. Control of Mycobacterium tuberculosis through mammalian Toll-like receptors. Curr. Opin. Immunol. 14:452-457.
38. Tsai, M. C., S. Chakravarty, G. Zhu, J. Xu, K. Tanaka, C. Koch, J. Tufariello, J. Flynn, and J. Chan. 2006. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8:218-232.
39. Turner, J., M. Gonzalez-Juarrero, D. L. Ellis, R. J. Basaraba, A. Kipnis, I. M. Orme, and A. M. Cooper. 2002. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J. Immunol. 169:6343-6351.
40. Ulrichs, T., G. A. Kosmiadi, V. Trusov, S. Jorg, L. Pradl, M. Titukhina, V. Mishenko, N. Gushina, and S. H. Kaufmann. 2004. Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung. J. Pathol. 204:217-228.
41. Underhill, D. M., A. Ozinsky, K. D. Smith, and A. Aderem. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96:14459-14463.
42. WHO. 2007. Global tuberculosis control: surveillance, planning, financing. WHO/HTM/TB/2007.376. World Health Organization, Geneva, Switzerland.
43. Williams, I. R. 2006. CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann. N. Y. Acad. Sci. 1072:52-61.
44. Zganiacz, A., M. Santosuosso, J. Wang, T. Yang, L. Chen, M. Anzulovic, S. Alexander, B. Gicquel, Y. Wan, J. Bramson, M. Inman, and Z. Xing. 2004. TNF-alpha is a critical negative regulator of type 1 immune activation during intracellular bacterial infection. J. Clin. Investig. 113:401-413.
45. Zhu, G., H. Xiao, V. P. Mohan, K. Tanaka, S. Tyagi, F. Tsen, P. Salgame, and J. Chan. 2003. Gene expression in the tuberculous granuloma: analysis by laser capture microdissection and real-time PCR. Cell. Microbiol. 5:445-453.
46. Zlotnik, A., and O. Yoshie. 2000. Chemokines: a new classification system and their role in immunity. Immunity 12:121-127.