Differential Induction of Nitric Oxide Synthase in Various Organs of the Mouse During Endotoxaemia: Role of TNF-alpha and IL-1-beta

Overview

Journal Immunology

Specialty Allergy & Immunology

Date 1994 Feb 1

PMID 7512527

Citations 56

Authors

F Q Cunha

J Assreuy

D W Moss

D Rees

L M Leal

S Moncada

M Carrier

C A ODonnell

F Y Liew

Affiliations

Soon will be listed here.

Abstract

BALB/c mice injected intraperitoneally with bacterial lipopolysaccharide (LPS) developed lethal septic shock. This was accompanied by significantly elevated concentrations of nitrite and nitrate in the plasma and expression of high levels of nitric oxide (NO) synthase activity in the lungs, heart, spleen and peritoneal macrophages. Mice pretreated with anti-tumour necrosis factor-alpha (TNF-alpha) monoclonal antibody or anti-interleukin-1 beta (IL-1 beta) polyclonal antibody were protected, in a dose-dependent manner, from endotoxin-induced mortality. This effect was accompanied by a significant reduction in plasma levels of nitrite and nitrate. Antibody treatment also reduced the level of NO synthase activity in peritoneal macrophages, spleen and heart but had no effect on enzyme expression in the lung. These results demonstrate that TNF-alpha and IL-1 beta play an important role in the induction of NO following administration of LPS and in the development of endotoxin-induced shock. In addition, NO synthase activity is differentially expressed in various organs and this may not always require TNF-alpha and IL-1 beta.

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References

Palmer R, Ferrige A, Moncada S . Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987; 327(6122):524-6. DOI: 10.1038/327524a0. View

Beutler B, Milsark I, Cerami A . Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science. 1985; 229(4716):869-71. DOI: 10.1126/science.3895437. View

Michie H, Manogue K, Spriggs D, Revhaug A, ODwyer S, Dinarello C . Detection of circulating tumor necrosis factor after endotoxin administration. N Engl J Med. 1988; 318(23):1481-6. DOI: 10.1056/NEJM198806093182301. View

Mathison J, Wolfson E, Ulevitch R . Participation of tumor necrosis factor in the mediation of gram negative bacterial lipopolysaccharide-induced injury in rabbits. J Clin Invest. 1988; 81(6):1925-37. PMC: 442645. DOI: 10.1172/JCI113540. View

Ding A, Nathan C, Stuehr D . 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; 141(7):2407-12. View

Drapier J, Wietzerbin J, Hibbs Jr J . Interferon-gamma and tumor necrosis factor induce the L-arginine-dependent cytotoxic effector mechanism in murine macrophages. Eur J Immunol. 1988; 18(10):1587-92. DOI: 10.1002/eji.1830181018. View

Schmidt H, Wilke P, Evers B, Bohme E . Enzymatic formation of nitrogen oxides from L-arginine in bovine brain cytosol. Biochem Biophys Res Commun. 1989; 165(1):284-91. DOI: 10.1016/0006-291x(89)91067-x. View

Kilbourn R, Gross S, Jubran A, Adams J, Griffith O, Levi R . 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; 87(9):3629-32. PMC: 53955. DOI: 10.1073/pnas.87.9.3629. View

Bogdan C, Moll H, Solbach W, Rollinghoff M . Tumor necrosis factor-alpha in combination with interferon-gamma, but not with interleukin 4 activates murine macrophages for elimination of Leishmania major amastigotes. Eur J Immunol. 1990; 20(5):1131-5. DOI: 10.1002/eji.1830200528. View

10.

Knowles R, Merrett M, Salter M, Moncada S . Differential induction of brain, lung and liver nitric oxide synthase by endotoxin in the rat. Biochem J. 1990; 270(3):833-6. PMC: 1131810. DOI: 10.1042/bj2700833. View

11.

Kilbourn R, Jubran A, Gross S, Griffith O, Levi R, Adams J . Reversal of endotoxin-mediated shock by NG-methyl-L-arginine, an inhibitor of nitric oxide synthesis. Biochem Biophys Res Commun. 1990; 172(3):1132-8. DOI: 10.1016/0006-291x(90)91565-a. View

12.

Ohlsson K, Bjork P, Bergenfeldt M, Hageman R, Thompson R . Interleukin-1 receptor antagonist reduces mortality from endotoxin shock. Nature. 1990; 348(6301):550-2. DOI: 10.1038/348550a0. View

13.

Liew F, Li Y, Millott S . Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J Immunol. 1990; 145(12):4306-10. View

14.

Wakabayashi G, Gelfand J, Burke J, Thompson R, Dinarello C . A specific receptor antagonist for interleukin 1 prevents Escherichia coli-induced shock in rabbits. FASEB J. 1991; 5(3):338-43. DOI: 10.1096/fasebj.5.3.1825816. View

15.

Dinarello C . The proinflammatory cytokines interleukin-1 and tumor necrosis factor and treatment of the septic shock syndrome. J Infect Dis. 1991; 163(6):1177-84. DOI: 10.1093/infdis/163.6.1177. View

16.

Moncada S, Palmer R, Higgs E . Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991; 43(2):109-42. View

17.

Bone R . The pathogenesis of sepsis. Ann Intern Med. 1991; 115(6):457-69. DOI: 10.7326/0003-4819-115-6-457. View

18.

Glauser M, Zanetti G, Baumgartner J, Cohen J . Septic shock: pathogenesis. Lancet. 1991; 338(8769):732-6. DOI: 10.1016/0140-6736(91)91452-z. View

19.

LESSLAUER W, Tabuchi H, Gentz R, Brockhaus M, Schlaeger E, Grau G . Recombinant soluble tumor necrosis factor receptor proteins protect mice from lipopolysaccharide-induced lethality. Eur J Immunol. 1991; 21(11):2883-6. DOI: 10.1002/eji.1830211134. View

20.

Salter M, Knowles R, Moncada S . Widespread tissue distribution, species distribution and changes in activity of Ca(2+)-dependent and Ca(2+)-independent nitric oxide synthases. FEBS Lett. 1991; 291(1):145-9. DOI: 10.1016/0014-5793(91)81123-p. View