Home LiteratureArticle Details
PMID: 8386705 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Resistance to nitric oxide in Mycobacterium avium complex and its implication in pathogenesis.

Infection and immunity ·Vol. 61 ·No. 5 ·1993-05-00 ·Pages 1980-9

Doi T, Ando M, Akaike T, Suga M, Sato K, Maeda H

Abstract

Susceptibility of three different strains of Mycobacterium avium complex (MAC), i.e., one strain of M. avium (Mino) and two strains of M. intracellulare (31F093T and KUMS 9007), to nitric oxide (NO) generated by rat alveolar macrophages (M phi) or NO generated chemically by acidification of NO2- was examined in vitro. We also investigated the effects of NO on phagocytosis and superoxide anion (O2-) generation by M phi. The intracellular growth of M. avium Mino was significantly suppressed by NO generated by gamma interferon (IFN-gamma)-stimulated M phi, whereas that of two strains of M. intracellulare (31F093T and KUMS 9007) was not. M. avium Mino was also more susceptible to NO generated chemically by acidification of NO2- than the two M. intracellulare strains. In L-arginine (1 mM)-containing medium, NO release from the M phi assessed by measuring NO2- increased as the concentration of IFN-gamma increased. The enhancing potential of IFN-gamma for NO release became more pronounced when M phi were infected with 31F093T, an NO-resistant strain. A large amount of NO generated by IFN-gamma-stimulated M phi suppressed both phagocytosis and O2- generation by the M phi, especially after infection of the M phi with strain 31F093T. These results indicate that the intracellular growth of MAC is not always inhibited by NO generated by immunologically activated M phi; rather, NO generation induced by infection with an NO-resistant MAC strain suppresses phagocytosis of the M phi, which may allow extracellular spreading of such NO-resistant mycobacteria. Therefore, the pathogenic potential of MAC may be partly attributed to its resistance to NO.

MeSH Terms
Animals Arginine/analogs & derivatives,pharmacology Drug Resistance, Microbial Hydrogen-Ion Concentration Immunity, Cellular Interferon-gamma/pharmacology Macrophage Activation Macrophages, Alveolar/immunology,microbiology Male Mycobacterium avium/drug effects,pathogenicity Nitric Oxide/pharmacology Nitrites/pharmacology Phagocytosis/drug effects Rats Rats, Inbred F344 Rats, Wistar Recombinant Proteins Respiratory Burst/drug effects Superoxides/metabolism Tetradecanoylphorbol Acetate/pharmacology Tuberculosis/immunology omega-N-Methylarginine
Chemicals
Nitrites Recombinant Proteins Superoxides omega-N-Methylarginine Nitric Oxide Interferon-gamma Arginine Tetradecanoylphorbol Acetate
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Doi T
Department of Microbiology, Kumamoto University School of Medicine, Japan.
Ando M
Akaike T
Suga M
Sato K
Maeda H
References (43)
43 references, click to expand
  1. Gamma interferon activates human macrophages to become tumoricidal and leishmanicidal but enhances replication of macrophage-associated mycobacteria.
    Infect Immun. 1985 Oct;50(1):1-8 PMID: 3930401
  2. Antagonistic action of imidazolineoxyl N-oxides against endothelium-derived relaxing factor/.NO through a radical reaction.
    Biochemistry. 1993 Jan 26;32(3):827-32 PMID: 8422387
  3. L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells.
    J Immunol. 1987 Jan 15;138(2):550-65 PMID: 2432129
  4. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite.
    Science. 1987 Jan 23;235(4787):473-6 PMID: 2432665
  5. Mycobacterial growth inhibition by interferon-gamma-activated bone marrow macrophages and differential susceptibility among strains of Mycobacterium tuberculosis.
    J Immunol. 1987 Jun 15;138(12):4408-13 PMID: 3108389
  6. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor.
    Nature. 1987 Jun 11-17;327(6122):524-6 PMID: 3495737
  7. Induction of nitrite/nitrate synthesis in murine macrophages by BCG infection, lymphokines, or interferon-gamma.
    J Immunol. 1987 Jul 15;139(2):518-25 PMID: 3110273
  8. Specific amino acid (L-arginine) requirement for the microbiostatic activity of murine macrophages.
    J Clin Invest. 1988 Apr;81(4):1129-36 PMID: 3280600
  9. Differentiation of murine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells.
    J Immunol. 1988 Apr 15;140(8):2829-38 PMID: 2451695
  10. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-gamma, is associated with macrophage killing of Mycobacterium avium complex.
    J Immunol. 1988 May 1;140(9):3006-13 PMID: 2834450
  11. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production.
    J Immunol. 1988 Oct 1;141(7):2407-12 PMID: 3139757
  12. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide.
    J Exp Med. 1989 Mar 1;169(3):1011-20 PMID: 2784476
  13. Regulation of macrophage functions by L-arginine.
    J Exp Med. 1989 Mar 1;169(3):1021-9 PMID: 2538541
  14. Molecular mechanism of complex infection by bacteria and virus analyzed by a model using serratial protease and influenza virus in mice.
    J Virol. 1989 May;63(5):2252-9 PMID: 2522998
  15. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells.
    J Exp Med. 1989 May 1;169(5):1543-55 PMID: 2497225
  16. A rapid colorimetric assay for serum lactic dehydrogenase.
    Clin Chim Acta. 1965 Aug;12(2):210-5 PMID: 5856284
  17. The indirect fluorescent antibody test for the detection of antibody in human cryptococcal disease.
    J Infect Dis. 1966 Dec;116(5):573-80 PMID: 5334249
  18. Activation of alveolar macrophages exposed to lavage-procured immunoglobulin G obtained from normal rabbit lungs.
    Infect Immun. 1978 May;20(2):476-84 PMID: 27460
  19. Enhanced resistance to acute infection with Trypanosoma cruzi in mice treated with an interferon inducer.
    Infect Immun. 1982 Feb;35(2):588-93 PMID: 6173326
  20. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids.
    Anal Biochem. 1982 Oct;126(1):131-8 PMID: 7181105
  21. A simple method for counting adherent cells: application to cultured human monocytes, macrophages and multinucleated giant cells.
    J Immunol Methods. 1983 Jan 28;56(2):261-8 PMID: 6827097
  22. Experimental chemotherapy in chronic Mycobacterium avium-intracellulare infection of mice.
    Am Rev Respir Dis. 1984 Mar;129(3):453-9 PMID: 6703503
  23. Recombinant murine gamma interferon induces enhanced resistance to Listeria monocytogenes infection in neonatal mice.
    Infect Immun. 1989 Aug;57(8):2345-9 PMID: 2501217
  24. Enhancement of growth of Mycobacterium lepraemurium in macrophages by gamma interferon.
    Infect Immun. 1989 Aug;57(8):2586-7 PMID: 2501220
  25. Interactions between endogenous gamma interferon and tumor necrosis factor in host resistance against primary and secondary Listeria monocytogenes infections.
    Infect Immun. 1989 Nov;57(11):3331-7 PMID: 2509360
  26. Regulation of macrophage physiology by L-arginine: role of the oxidative L-arginine deiminase pathway.
    J Immunol. 1989 Dec 1;143(11):3641-6 PMID: 2584712
  27. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1620-4 PMID: 2154753
  28. Dependence on O2- generation by xanthine oxidase of pathogenesis of influenza virus infection in mice.
    J Clin Invest. 1990 Mar;85(3):739-45 PMID: 2155924
  29. Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine.
    J Immunol. 1990 Apr 1;144(7):2725-9 PMID: 2319133
  30. NG-methyl-L-arginine inhibits tumor necrosis factor-induced hypotension: implications for the involvement of nitric oxide.
    Proc Natl Acad Sci U S A. 1990 May;87(9):3629-32 PMID: 2333306
  31. Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine.
    J Immunol. 1990 Jun 15;144(12):4794-7 PMID: 2351828
  32. Localization of nitric oxide synthase indicating a neural role for nitric oxide.
    Nature. 1990 Oct 25;347(6295):768-70 PMID: 1700301
  33. Leishmania major amastigotes initiate the L-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha.
    J Immunol. 1990 Dec 15;145(12):4290-7 PMID: 2124240
  34. Reaction of NO with O2-. implications for the action of endothelium-derived relaxing factor (EDRF).
    Free Radic Res Commun. 1990;10(4-5):221-6 PMID: 1963161
  35. Tumor necrosis factor and granulocyte macrophage-colony stimulating factor stimulate human macrophages to restrict growth of virulent Mycobacterium avium and to kill avirulent M. avium: killing effector mechanism depends on the generation of reactive nitrogen intermediates.
    J Leukoc Biol. 1991 Apr;49(4):380-7 PMID: 1900522
  36. Inhibition of Cryptococcus neoformans replication by nitrogen oxides supports the role of these molecules as effectors of macrophage-mediated cytostasis.
    Infect Immun. 1991 Jul;59(7):2291-6 PMID: 2050398
  37. Interferon decreases the growth inhibition of Mycobacterium avium-intracellulare complex by fresh human monocytes but not by culture-derived macrophages.
    J Infect Dis. 1991 Jul;164(1):152-7 PMID: 1905332
  38. Interferon-gamma-treated murine macrophages inhibit growth of tubercle bacilli via the generation of reactive nitrogen intermediates.
    Cell Immunol. 1991 Jan;132(1):150-7 PMID: 1905984
  39. Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates.
    Infect Immun. 1991 Sep;59(9):3213-8 PMID: 1908829
  40. L-arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes.
    J Infect Dis. 1992 Mar;165(3):513-7 PMID: 1538156
  41. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages.
    J Exp Med. 1992 Apr 1;175(4):1111-22 PMID: 1552282
  42. Evaluation of nitrite production by human monocyte-derived macrophages.
    Biochem Biophys Res Commun. 1992 Jul 31;186(2):775-81 PMID: 1497665
  43. Chronic infection due to Mycobacterium intracellulare in mice: association with macrophage release of prostaglandin E2 and reversal by injection of indomethacin, muramyl dipeptide, or interferon-gamma.
    J Immunol. 1986 Mar 1;136(5):1820-7 PMID: 3005400
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1993-05-00
Pages
1980-9
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC280792
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]