Inhibition of inducible nitric oxide synthase protects against liver injury induced by mycobacterial infection and endotoxins

Journal of Hepatology

Volumn 41, Issue 5, 2004, Pages 773-781

  Guler, Reto ^a   Olleros, Maria L ^a   Vesin, Dominique ^a   Parapanov, Roumen ^a   Vesin, Christian ^a   Kantengwa, Salomé ^a   Rubbia Brandt, Laura ^a   Mensi, Noury ^b   Angelillo Scherrer, Anne ^b   Martinez Soria, Eduardo ^a   Tacchini Cottier, Fabienne ^c   Garcia, Irene ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ENDOTOXIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; LIVER GRANULOMA; LIVER INJURY; LIVER PROTECTION; LIVER TOXICITY; MACROPHAGE; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; WILD TYPE;

ANIMALS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LIVER; LIVER DISEASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM BOVIS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; SPLEEN; TH1 CELLS; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 7244251960     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2004.07.031     Document Type: Article

References (46)

1. J. Chan, K. Tanaka, D. Carroll, J.L. Flynn, and B.R. Bloom Effect of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis Infect Immun 63 1995 736 740
2. I. Garcia, R. Guler, D. Vesin, M.L. Olleros, P. Vassalli, and Y. Chvatchko Lethal Mycobacterium bovis Bacillus Calmette Guerin infection in nitric oxide synthase 2-deficient mice: cell-mediated immunity requires nitric oxide synthase 2 Lab Invest 80 2000 1385 1397
3. J.D. MacMicking, R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah, and C.F. Nathan Identification of nitric oxide synthase as a protective locus against tuberculosis Proc Natl Acad Sci USA 94 1997 5243 5248
4. S. Saito, and M. Nakano Nitric oxide production by peritoneal macrophages of Mycobacterium bovis BCG-infected or non-infected mice: regulatory role of T lymphocytes and cytokines J Leukoc Biol 59 1996 908 915
5. J. Ferluga Tuberculin hypersensitivity hepatitis in mice infected with Mycobacterium bovis (BCG) Am J Pathol 105 1981 82 90
6. M. Bopst, I. Garcia, R. Guler, M.L. Olleros, T. Rulicke, and M. Muller Differential effects of TNF and LTalpha in the host defense against M. bovis BCG Eur J Immunol 31 2001 1935 1943
7. R. Kamijo, J. Le, D. Shapiro, E.A. Havell, S. Huang, and M. Aguet Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette Guerin and subsequent challenge with lipopolysaccharide J Exp Med 178 1993 1435 1440
8. B.S. Taylor, L.H. Alarcon, and T.R. Billiar Inducible nitric oxide synthase in the liver: regulation and function Biochemistry 63 1998 766 781
9. T. Michel, and O. Feron Nitric oxide synthases: which, where, how, and why? J Clin Invest 100 1997 2146 2152
10. C. Bogdan Nitric oxide and the immune response Nat Immunol 2 2001 907 916
11. H.B. Peng, M. Spiecker, and J.K. Liao Inducible nitric oxide: an auto-regulatory feedback inhibitor of vascular inflammation J Immunol 161 1998 1970 1976
12. M. Colasanti, T. Persichini, M. Menegazzi, S. Mariotto, E. Giordano, and C.M. Caldarera Induction of nitric oxide synthase mRNA expression: suppression by exogenous nitric oxide J Biol Chem 270 1995 26731 26733
13. H.B. Peng, P. Libby, and J.K. Liao Induction and stabilization of IkBa by nitric oxide mediates inhibition of NF-kB J Biol Chem 270 1995 14214 14219
14. F. Chen, D.C. Kuhn, S.C. Sun, L.J. Gaydos, and L.M. Demers Dependence and reversal of nitric oxide production on NF-kappa B in silica and lipopolysaccharide-induced macrophages Biochem Biophys Res Commun 214 1995 839 846
15. R. De Caterina, P. Libby, H.B. Peng, V.J. Thannickal, T.B. Rajavashisth, and M.A. Gimbrone Jr Nitric oxide decreases cytokine-induced endothelial activation: nitric oxide selectively reduces endothelial expression and adhesion molecules and pro-inflammatory cytokines J Clin Invest 96 1995 60 68
16. M. Modolell, I.M. Corraliza, F. Link, G. Soler, and K. Eichmann Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by Th1 and Th2 cytokines Eur J Immunol 25 1995 1101 1104
17. F.C. Fang Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity J Clin Invest 99 1997 2818 2825
18. L. McNaughton, L. Puttagunta, M.A. Martinez-Cuesta, N. Kneteman, I. Mayers, and R. Moqbel Distribution of nitric oxide synthase in normal and cirrhotic human liver Proc Natl Acad Sci USA 99 2002 17161 17166
19. L. Leifeld, M. Fielenbach, F.L. Dumoulin, N. Speidel, T. Sauerbruch, and U. Spengler Inducible nitric oxide synthase (iNOS) and endothelial nitric oxide synthase (eNOS) expression in fulminant hepatic failure J Hepatol 37 2002 613 619
20. N.A. Mohammed, S. Abd El-Aleem, I. Appleton, M.M. Maklouf, M. Said, and R.F. McMahon Expression of nitric oxide synthase isoforms in human liver cirrhosis J Pathol 200 2003 647 655
21. J. Li, and T.R. Billiar Nitric oxide. IV. Determinants of nitric oxide protection and toxicity in liver Am J Physiol 76 1999 G1069 G1073
22. I. Garcia, Y. Miyazaki, K. Araki, M. Araki, R. Lucas, and G.E. Grau Transgenic mice expressing high levels of soluble TNF-R1 fusion protein are protected from lethal septic shock and cerebral malaria, and are highly sensitive to Listeria monocytogenes and Leishmania major infections Eur J Immunol 25 1995 2401 2407
23. H.U. Bergmeyer, M. Horder, and R. Rej IFCC method for aspartate aminotransferase J Clin Chem Clin Biochem 24 1986 497 510
24. M.L. Olleros, R. Guler, N. Corazza, D. Vesin, H.P. Eugster, and G. Marchal Transmembrane TNF induces an efficient cell-mediated immunity and resistance to Mycobacterium bovis Bacillus Calmette Guerin infection in the absence of secreted TNF and lymphotoxin-alpha J Immunol 168 2002 3394 3401
25. A.A. Nanji, S.S. Greenberg, S.R. Tahan, F. Fogt, J. Loscalzo, and S.M. Sadrzadeh Nitric oxide production in experimental alcoholic liver disease in the rat: role in protection from injury Gastroenterology 109 1995 899 907
26. I. Bohlinger, M. Leist, J. Barsig, S. Uhlig, G. Tiegs, and A. Wendel Interleukin-1 and nitric oxide protect against tumor necrosis factor alpha-induced liver injury through distinct pathways Hepatology 22 1995 1829 1837
27. M. Mojena, S. Hortelano, A. Castrillo, M.J.M. Diaz-Guerra, M.J. Garcia-Barchino, and G.T. Saez Protection by nitric oxide against liver inflammatory injury in animals carrying a nitric oxide synthase-2 transgene FASEB J 15 2001 583 585
28. R.M. Rai, F.Y. Lee, A. Rosen, S.Q. Yang, H.Z. Lin, and A. Koteish Impaired liver regeneration in inducible nitric oxide synthase deficient mice Proc Natl Acad Sci USA 95 1998 13829 13834
29. M. Zeini, S. Hortelano, P.G. Traves, P. Martin-Sanz, and L. Bosc Simultaneous abrogation of NOS-2 and COX-2 activities is lethal in partially hepatectomised mice J Hepatol 40 2004 926 933
30. P. Muriel Nitric oxide protection of rat liver from peroxidation, collagen accumulation, and liver damage induced by carbon tetrachloride Biochem Pharmacol 56 1998 773 779
31. S.E. McKim, E. Gabele, F. Isayama, J.C. Lambert, L.M. Tucker, and M.D. Wheeler Inducible nitric oxide synthase is required in alcohol-induced liver injury: studies with knockout mice Gastroenterology 125 2003 1834 1844
32. J. Menezes, C. Hierholzer, S.C. Watkins, V. Lyons, A.B. Peitzman, and T.R. Billiar A novel nitric oxide scavenger decreases liver injury and improves survival after hemorrhagic shock Am J Physiol 277 1999 G144 G151
33. M. Isobe, T. Katsuramaki, K. Hirata, H. Kimura, M. Nagayama, and T. Matsuno Beneficial effects of inducible nitric oxide synthase inhibitor on reperfusion injury in the pig liver Transplantation 68 1999 803 813
34. C. Thiemermann, H. Ruetten, C.C. Wu, and J.R. Vane The multiple organ dysfunction syndrome caused by endotoxin in the rat: attenuation of liver dysfunction by inhibitors of nitric oxide synthase Br J Pharmacol 116 1995 2845 2851
35. A. Morikawa, Y. Kato, T. Sugiyama, N. Koide, D. Chakravortty, and T. Yoshida Role of nitric oxide in lipopolysaccharide-induced hepatic injury in d-galactosamine-sensitized mice as an experimental endotoxic shock model Infect Immun 67 1999 1018 1024
36. G.S. Wang, and G.T. Liu Role of nitric oxide in immunological liver damage in mice Biochem Pharmacol 49 1995 1277 1281
37. M.J. Vazquez-Gil, M.J. Mesonero, O. Flores, M. Criado, F. Hidalgo, and M.A. Arevalo Sequential changes in redox status and nitric oxide synthases expression in the liver after bile duct ligation Life Sci 75 2004 717 732
38. M. Nowak, G.C. Gaines, J. Rosenberg, R. Minter, F.R. Bahjat, and J. Rectenwald LPS-induced liver injury in d-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor Am J Physiol Regul Integr Comp Physiol 278 2000 R1202 R1209
39. K. Koerber, G. Sass, A.K. Kiemer, A.M. Vollmar, and G. Tiegs In vivo regulation of inducible NO synthase in immune-mediated liver injury in mice Hepatology 36 2002 1061 1069
40. Y. Shimizu, J.A. Margenthaler, K. Landeros, N. Otomo, G. Doherty, and M.W. Flye The resistance of P. acnes-primed Interferon γ-deficient mice to low-dose lipopolysaccharide-induced acute liver injury Hepatology 35 2002 805 814
41. H. Tsuji, A. Harada, N. Mukaida, Y. Nakanuma, H. Bluethmann, and S. Kaneko Tumor necrosis factor receptor p55 is essential for intrahepatic granuloma formation and hepatocellular apoptosis in a murine model of bacterium-induced fulminant hepatitis Infect Immun 65 1997 1892 1998
42. A.P.M. Van der Meijden, P.A. Steerenberg, W.H. de Jong, and F.M.J. Debruyne Inrtavesical Bacillus Calmette Guérin treatment for superficial bladder cancer: Results after 15 years of experience Anticancer Res 11 1991 1253 1258
43. D.L. Lamm, A.P.M. van der Meijden, and Morales Incidence and treatment complications of Bacillus Calmette Guérin intravesical therapy in superficial bladder cancer J Urol 147 1992 596 600
44. J.T. Kamphuis, A.G. Buiting, J.F. Misere, D.P. van Berge Henegouwen, D. van Soolingen, and P.L. Rensma BCG immunotherapy: be cautious of granulomas. Disseminated BCG infection and mycotic aneurysm as late complications of intravesical BCG instillations Neth J Med 58 2001 71 75
45. O.Y. Gonzalez, D.M. Musher, I. Brar, S. Furgeson, M.R. Boktour, and E.J. Septimus Spectrum of Bacille Calmette Guerin (BCG) infection after intravesical BCG immunotherapy Clin Infect Dis 36 2003 140 148
46. B.R. Oh, K. Nakajima, K.Y. Ahn, S.B. Ryu, Y.I. Park, and R. Dahiya Nitric oxide synthase gene and protein expression are upregulated by Bacille Calmette Guerin in the rat bladder Eur Urol 39 2001 349 356