Home LiteratureArticle Details
PMID: 7520472 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major.

The Journal of experimental medicine ·Vol. 180 ·No. 3 ·1994-09-01 ·Pages 783-93

Stenger S, Thüring H, Röllinghoff M, Bogdan C

Abstract

Previous studies with inhibitors of inducible nitric oxide synthase (iNOS) suggested that high-output production of nitric oxide (NO) is an important antimicrobial effector pathway in vitro and in vivo. Here, we investigated the tissue expression of iNOS in mice after infection with Leishmania major. Immunohistochemical staining with an iNOS-specific antiserum revealed that in the cutaneous lesion and draining lymph nodes (LN) of clinically resistant mice (C57BL/6), iNOS protein is found earlier during infection and in significantly higher amounts than in the nonhealing BALB/c strain. Similar differences were seen on the mRNA level as quantitated by competitive polymerase chain reaction. Anti-CD4 treatment of BALB/c mice not only induced resistance to disease, but also restored the expression of iNOS in the tissue. In situ, few or no parasites were found in those regions of the skin lesion and the draining LN which were highly positive for iNOS. By double labeling experiments, macrophages were identified as iNOS expressing cells in vivo. In the lesions of BALB/c mice, cells staining positively for transforming growth factor beta (TGF-beta), a potent inhibitor of iNOS in vitro, were strikingly more prominent than in C57BL/6, whereas no such difference was found for interleukin 4 or interferon gamma (IFN-gamma). In vitro, production of NO was approximately threefold higher in C57BL/6 than in BALB/c macrophages after stimulation with IFN-gamma. We conclude that the pronounced expression of iNOS in resistant mice is an important mechanism for the elimination of Leishmania in vivo. The relative lack of iNOS in susceptible mice might be a consequence of macrophage deactivation by TGF-beta and reduced responsiveness to IFN-gamma.

MeSH Terms
Amino Acid Oxidoreductases/biosynthesis,genetics Animals Base Sequence Cells, Cultured Female Interferon-gamma/pharmacology Leishmania major Leishmaniasis, Cutaneous/immunology Macrophages/enzymology Mice Mice, Inbred BALB C Mice, Inbred C57BL Molecular Sequence Data NADPH Dehydrogenase/metabolism Nitric Oxide Synthase RNA, Messenger/analysis Transforming Growth Factor beta/biosynthesis
Chemicals
RNA, Messenger Transforming Growth Factor beta Interferon-gamma Nitric Oxide Synthase Amino Acid Oxidoreductases NADPH Dehydrogenase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Stenger S
Institute of Clinical Microbiology and Immunology, University of Erlangen, Germany.
Thüring H
Röllinghoff M
Bogdan C
References (61)
61 references, click to expand
  1. Advantages of measuring changes in the number of viable parasites in murine models of experimental cutaneous leishmaniasis.
    Infect Immun. 1983 Mar;39(3):1087-94 PMID: 6840835
  2. Leishmania major-specific CD8+ T cells are inducers and targets of nitric oxide produced by parasitized macrophages.
    Eur J Immunol. 1994 Mar;24(3):746-52 PMID: 7510243
  3. Therapeutic effect of anti-L3T4 monoclonal antibody GK1.5 on cutaneous leishmaniasis in genetically-susceptible BALB/c mice.
    J Immunol. 1985 Sep;135(3):2108-14 PMID: 3926895
  4. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice.
    Parasite Immunol. 1985 Sep;7(5):545-55 PMID: 3877902
  5. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide.
    Proc Natl Acad Sci U S A. 1985 Nov;82(22):7738-42 PMID: 3906650
  6. Nucleotide sequence of a full-length cDNA for mouse cytoskeletal beta-actin mRNA.
    Nucleic Acids Res. 1986 Mar 25;14(6):2829 PMID: 3754329
  7. Cytokines in leishmaniasis: a complex network of stimulatory and inhibitory interactions.
    Immunobiology. 1993 Nov;189(3-4):356-96 PMID: 8125517
  8. Regulation of the immune response by nitric oxide differentially produced by T helper type 1 and T helper type 2 cells.
    Eur J Immunol. 1994 Apr;24(4):980-4 PMID: 8149966
  9. Assembly and regulation of NADPH oxidase and nitric oxide synthase.
    Curr Opin Immunol. 1994 Feb;6(1):131-9 PMID: 7513523
  10. Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation.
    J Immunol. 1993 Oct 1;151(7):3672-81 PMID: 7690809
  11. Effect of T-lymphocyte suppression on the parasite burden in Leishmania major-infected, genetically susceptible BALB/c mice.
    Infect Immun. 1986 Dec;54(3):909-12 PMID: 3491051
  12. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  13. 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
  14. Immunoregulation of cutaneous leishmaniasis. T cell lines that transfer protective immunity or exacerbation belong to different T helper subsets and respond to distinct parasite antigens.
    J Exp Med. 1988 Nov 1;168(5):1675-84 PMID: 2903212
  15. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets.
    J Exp Med. 1989 Jan 1;169(1):59-72 PMID: 2521244
  16. Administration of monoclonal anti-IFN-gamma antibodies in vivo abrogates natural resistance of C3H/HeN mice to infection with Leishmania major.
    J Immunol. 1989 Jul 1;143(1):266-74 PMID: 2499629
  17. Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine-dependent killing mechanism.
    J Immunol. 1990 Jan 1;144(1):278-83 PMID: 2104889
  18. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon gamma-independent mechanism.
    J Exp Med. 1990 Jan 1;171(1):115-27 PMID: 2104918
  19. 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
  20. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2725-9 PMID: 2181447
  21. 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
  22. Macrophage deactivating factor and transforming growth factors-beta 1 -beta 2 and -beta 3 inhibit induction of macrophage nitrogen oxide synthesis by IFN-gamma.
    J Immunol. 1990 Aug 1;145(3):940-4 PMID: 2115549
  23. Resistance to murine cutaneous leishmaniasis is mediated by TH1 cells, but disease-promoting CD4+ cells are different from TH2 cells.
    Eur J Immunol. 1990 Sep;20(9):2067-74 PMID: 1976523
  24. Patterns of cytokine secretion in murine leishmaniasis: correlation with disease progression or resolution.
    Infect Immun. 1990 Dec;58(12):3863-70 PMID: 2123823
  25. Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide.
    J Immunol. 1990 Dec 15;145(12):4306-10 PMID: 2175327
  26. Cloned murine T lymphocytes synthesize a molecule with the biological characteristics of nitric oxide.
    Biochem Biophys Res Commun. 1990 Dec 14;173(2):660-5 PMID: 2175602
  27. Urinary nitrate excretion in relation to murine macrophage activation. Influence of dietary L-arginine and oral NG-monomethyl-L-arginine.
    J Immunol. 1991 Feb 15;146(4):1294-302 PMID: 1991968
  28. Neuronal NADPH diaphorase is a nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2811-4 PMID: 1707173
  29. Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation. Role of IFN-gamma in the induction of the nitric oxide-synthesizing pathway.
    J Immunol. 1991 Jul 1;147(1):144-8 PMID: 1904899
  30. Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7011-5 PMID: 1908085
  31. A possible novel pathway of regulation by murine T helper type-2 (Th2) cells of a Th1 cell activity via the modulation of the induction of nitric oxide synthase on macrophages.
    Eur J Immunol. 1991 Oct;21(10):2489-94 PMID: 1717284
  32. IFN-gamma modulates the early development of Th1 and Th2 responses in a murine model of cutaneous leishmaniasis.
    J Immunol. 1991 Nov 1;147(9):3149-55 PMID: 1833466
  33. Macrophage deactivation by interleukin 10.
    J Exp Med. 1991 Dec 1;174(6):1549-55 PMID: 1744584
  34. Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages.
    Eur J Immunol. 1991 Dec;21(12):3009-14 PMID: 1721024
  35. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages.
    J Immunol. 1992 Mar 15;148(6):1792-6 PMID: 1541819
  36. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages.
    Science. 1992 Apr 10;256(5054):225-8 PMID: 1373522
  37. Mammalian nitric oxide synthases.
    Adv Enzymol Relat Areas Mol Biol. 1992;65:287-346 PMID: 1373932
  38. Transforming growth factor-beta in leishmanial infection: a parasite escape mechanism.
    Science. 1992 Jul 24;257(5069):545-8 PMID: 1636092
  39. Nitric oxide as a secretory product of mammalian cells.
    FASEB J. 1992 Sep;6(12):3051-64 PMID: 1381691
  40. Low response of BALB/c macrophages to priming and activating signals.
    J Leukoc Biol. 1992 Sep;52(3):315-22 PMID: 1381743
  41. Nitric oxide mediates suppression of T cell responses in murine Trypanosoma brucei infection.
    Eur J Immunol. 1992 Oct;22(10):2741-4 PMID: 1396977
  42. Persistence of virulent Leishmania major in murine cutaneous leishmaniasis: a possible hazard for the host.
    Infect Immun. 1993 Jan;61(1):220-6 PMID: 8093358
  43. Parasitism of epidermal Langerhans cells in experimental cutaneous leishmaniasis with Leishmania major.
    J Infect Dis. 1993 Feb;167(2):418-25 PMID: 8421175
  44. Neutralization of gamma interferon and tumor necrosis factor alpha blocks in vivo synthesis of nitrogen oxides from L-arginine and protection against Francisella tularensis infection in Mycobacterium bovis BCG-treated mice.
    Infect Immun. 1993 Feb;61(2):689-98 PMID: 8423095
  45. Release of nitric oxide during the T cell-independent pathway of macrophage activation. Its role in resistance to Listeria monocytogenes.
    J Immunol. 1993 Feb 1;150(3):888-95 PMID: 7678626
  46. Reactive nitrogen intermediates suppress the primary immunologic response to Listeria.
    J Immunol. 1993 Apr 1;150(7):2901-9 PMID: 7681083
  47. In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants.
    Eur J Immunol. 1993 Apr;23(4):882-7 PMID: 8458376
  48. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3024-7 PMID: 7681993
  49. Nitric oxide synthase structure and mechanism.
    J Biol Chem. 1993 Jun 15;268(17):12231-4 PMID: 7685338
  50. Interleukin-4 but not gamma interferon production correlates with the severity of murine cutaneous leishmaniasis.
    Infect Immun. 1993 Aug;61(8):3459-65 PMID: 8335376
  51. Effect of in vivo inhibition of nitric oxide production in murine leishmaniasis.
    J Immunol. 1993 Jul 15;151(2):907-15 PMID: 8335918
  52. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta.
    J Exp Med. 1993 Aug 1;178(2):605-13 PMID: 7688028
  53. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase.
    Science. 1993 Sep 10;261(5127):1445-8 PMID: 7690156
  54. Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity.
    Biochem Biophys Res Commun. 1993 Sep 15;195(2):1035-40 PMID: 7690549
  55. Interleukin-4 and interleukin-10 synergize to inhibit cell-mediated immunity in vivo.
    Eur J Immunol. 1993 Nov;23(11):3043-9 PMID: 8223881
  56. The L-arginine-nitric oxide pathway.
    N Engl J Med. 1993 Dec 30;329(27):2002-12 PMID: 7504210
  57. Modulation of murine macrophage function by IL-13.
    J Immunol. 1993 Dec 15;151(12):7151-60 PMID: 7903102
  58. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection.
    J Exp Med. 1994 Feb 1;179(2):447-56 PMID: 7905017
  59. Mechanism of suppression of nitric oxide synthase expression by interleukin-4 in primary mouse macrophages.
    J Leukoc Biol. 1994 Feb;55(2):227-33 PMID: 7507968
  60. Nitric oxide produced during murine listeriosis is protective.
    Infect Immun. 1994 Mar;62(3):1089-100 PMID: 7509315
  61. Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes.
    J Immunol. 1985 Jul;135(1):564-9 PMID: 2582050
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1994-09-01
Pages
783-93
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2191630
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: product@genelibs.com