NOS2-derived nitric oxide regulates the size, quantity and quality of granuloma formation in Mycobacterium avium-infected mice without affecting bacterial loads

Immunology

Volumn 98, Issue 3, 1999, Pages 313-323

  Ehlers, S ^a   Kutsch, S ^a   Benini, J ^a   Cooper, A ^b   Hahn, C ^a   Gerdes, J ^a   Orme, I ^b   Martin, C ^a   Rietschel, E Th ^a  

^a RESEARCH CENTER BORSTEL   (Germany)

^b Immunology and Pathology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GRANULOMA; HISTOPATHOLOGY; HOST RESISTANCE; IMMUNOREGULATION; LIVER; LUNG; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM AVIUM; NONHUMAN; PRIORITY JOURNAL; SPLEEN;

ANALYSIS OF VARIANCE; ANIMALS; CHRONIC DISEASE; CYTOKINES; GRANULOMA; IMMUNOHISTOCHEMISTRY; LIVER; MACROPHAGES; MICE; MICE, INBRED BALB C; MYCOBACTERIUM AVIUM; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUBERCULOSIS, HEPATIC;

EID: 0032722476     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2567.1999.00875.x     Document Type: Article

References (40)

1. 1. NATHAN C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J 6, 3051.
2. 2. BOGDAN C. (1997) Of microbes, macrophages and nitric oxide. Behring Inst Mitt 99, 58.
3. 3. MACMICKING J., XIE W.W, & NATHAN C. (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15, 323.
4. 4. CHAN J., TANAKA K., CAROLL D., FLYNN J, & BLOOM B.R. (1995) Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect Immun 63, 736.
5. 5. FLESCH I.E. & KAUFMANN S.H.E. (1991) Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates. Infect Immun 59, 3213.
6. 6. LIEW F.Y., MILLOTT S., PARKINSON C., PALMER R.M. & MONCADA S. (1990) Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine. J Immunol 144, 4794.
7. 7. MACMICKING J.D., NORTH R.J., LACOURSE R., MUDGETT J.S., SHAH S.K. & NATHAN C. (1997) Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci USA 94, 5243.
8. 8. STENGER S., DONHAUSER N., THÜRING H., RÖLLINGHOFF M. & BOGDAN C. (1996) Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J Exp Med 183, 1501.
9. 9. BOGDAN C. (1998) The multiplex function of nitric oxide in (auto) immunity. J Exp Med 187, 1361.
10. 10. CROSS A.H., MISKO T.P., LIN R.F., HICKEY W.F., TROTTER J.L. & TILTON R.G. (1994) Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis. J Clin Invest 93, 2684.
11. 11. FLORQUIN S., AMRAOUI Z., DUBOIS C., DECUYPER J. & GOLDMAN M. (1994) The protective role of endogenously synthesized nitric oxide in staphylococcal enterotoxin B-induced shock in mice. J Exp Med 180, 1153.
12. 12. HOOPER D.C., BAGASRA O., MARINI J.C. et al. (1997) Prevention of experimental allergic encephalomyelitis by targeting nitric oxide and peroxynitrite: implications for the treatment of multiple sclerosis. Proc Natl Acad Sci USA 94, 2528.
13. 13. LIEW F.Y. (1995) Regulation of lymphocyte functions by nitric oxide. Curr Opin Immunol 7, 396.
14. 14. LYONS C.R. (1995) The role of nitric oxide in inflammation. Adv Immunol 60, 323.
15. 15. NUSSLER A.K. & BILLIAR T.R. (1993) Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 54, 171.
16. 16. BELENKY S.N., ROBBINS R.A. & RUBINSTEIN I. (1993) Nitric oxide synthase inhibitors attenuate human monocyte chemotaxis in vitro. J Leukoc Biol 53, 498.
17. 17. SETOGUCHI K., TAKEYA M., AKAIKE T. et al. (1996) Expression of inducible nitric oxide synthase and its involvement in pulmonary granulomatous inflammation in rats. Am J Pathol 149, 2005.
18. 18. HICKEY M.J., SHARKEY K.A., SIHOTA E.G. et al. (1997) Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J 11, 955.
19. 19. KUBES P., SUZUKI M. & GRANGER D.N. (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88, 4651.
20. 20. FEHSEL K., KRONCKE K.D., MEYER K.L., HUBER H., WAHN V. & KOLB-BACHOFEN V. (1995) Nitric oxide induces apoptosis in mouse thymocytes. J Immunol 155, 2858.
21. 21. OKUDA Y., SAKODA S., SHIMAOKA M. & YNAGIHARA T. (1996) Nitric oxide induces apoptosis in mouse splenic T lymphocytes. Immunol Lett 52, 135.
22. 22. TOMIOKA H., SATO K., MAW W.W. & SAITO H. (1995) The role of tumor necrosis factor, interferon-γ, transforming growth factor-β, and nitric oxide in the expression of immunosuppressive functions of splenic macrophages induced by Mycobacterium avium complex infection. J Leukoc Biol 58, 704.
23. 23. XIONG H., KAWAMURA I., NISHIBORI T. & MITSUYAMA M. (1996) Suppression of IFN-gamma production from Listeria monocytogenes-specific T cells by endogenously produced nitric oxide. Cell Immunol 172, 118.
24. 24. EHLERS S. & SETTZER U. (1998) Measuring immune responses in vivo. In: Methods in Microbiology, (eds. S. KAUFMANN & D. KABELITZ), vol. 25, p. 365, Academic Press, London.
25. 25. TSUJI M., DIMOV V.B. & YOSHIDA T. (1995) In vivo expression of monokine and inducible nitric oxide synthase in experimentally induced pulmonary granulomatous inflammation: evidence for sequential production of interleukin-1, inducible nitric oxide synthase, and tumor necrosis factor. Am J Pathol 147, 1001.
26. 26. HOGABOAM C.M., CHENSUE S.W., STEINHAUSER M.L. et al. (1997) Alteration of the cytokine phenotype in an experimental lung granuloma model by inhibiting nitric oxide. J Immunol 159, 5585.
27. 27. INDERLIED C.B., KEMPER C.A. & BERMUDEZ L.E. (1993) The Mycobacterium avium complex. Clin Microbiol Rev 6, 266.
28. 28. DOI T., ANDO M., AKAIKE T., SUGA M., SATO K. & MAEDA H. (1993) Resistance to nitric oxide in Mycobacterium avium complex and its implication in pathogenesis. Infect Immun 61, 1980.
29. 29. HÄNSCH H.C.R., SMITH D.A., MIELKE M.E.A., HAHN H., BANCROFT G.J. & EHLERS S. (1996) Mechanisms of granuloma formation in murine Mycobacterium avium infection: the contribution of CD4+ T cells. Int Immunol 8, 1299.
30. 30. PEDROSA J., FLORIDO M., KUNZE Z.M. et al. (1994) Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice. Clin Exp Immunol 98, 210.
31. 6-(1-iminoethyl)-lysine potently inhibits inducible nitric oxide synthase and is superior to NG-monomethyl-arginine in vitro and in vivo. Eur J Pharmacol 294, 703.
32. 32. KOSCO-VILBOIS M.H., ZENTGRAF H., GERDES J. & BONNEFOY J.Y. (1997) To 'B' or not to 'B' a germinal center? Immunol Today 18, 225.
33. 33. APPELBERG R., CASTRO A.G., PEDROSA J., SILVA R.A., ORME I.M. & MINOPRIO P. (1994) Role of gamma interferon and tumor necrosis factor alpha during T-cell-independent and -dependent phases of Mycobacterium avium infection. Infect Immun 62, 3962.
34. 34. SMITH D.A., HÄNSCH H., BANCROFT G.J. & EHLERS S. (1997) T-cell-independent granuloma formation in response to Mycobacterium avium: role of tumour necrosis factor-α and interferon-γ. Immunology 92, 413.
35. 35. FLESCH I.E., HESS J.H., HUANG S. et al. (1995) 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.
36. 36. MILLS C.D. (1991) Molecular basis of 'suppressor' macrophages. Arginine metabolism via the nitric oxide synthetase pathway. J Immunol 146, 2719.
37. 37. GOMES M.S., FLORIDO M., PAIS T.F. & APPELBERG R. (1999) Improved clearance of Mycobacterium avium upon disruption of the inducible nitric oxide synthase gene. J Immunol 162, 6734.
38. 38. IUVONE T., CARNUCCIO R. & DIROSA M. (1994) Modulation of granuloma formation by endogenous nitric oxide. Eur J Pharmacol 265, 89.
39. 39. DOHERTY T.M. & SHER A. (1997) Defects in cell-mediated immunity affect chronic, but not innate, resistance of mice to Mycobacterium avium infection. J Immunol 158, 4822.
40. 40. APPELBERG R. & SARMENTO A.M. (1990). The role of macrophage activation and of Bcg-encoded macrophage function(s) in the control of Mycobacterium avium infection in mice. Clin Exp Immunol 80, 324.