Carbon Monoxide Protects against Liver Failure through Nitric Oxide-induced Heme Oxygenase 1

Journal of Experimental Medicine

Volumn 198, Issue 11, 2003, Pages 1707-1716

  Zuckerbraun, Brian S ^a   Billiar, Timothy R ^a,d   Otterbein, Sherrie L ^a   Kim, Peter K M ^a   Liu, Fang ^a   Choi, Augustine M K ^a   Bach, Fritz H ^b   Otterbein, Leo E ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Carbon monoxide; Heme oxygenase; Hepatitis; iNOS; Nitric oxide

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIVER PROTECTIVE AGENT; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VITRO STUDY; INFLAMMATION; LIVER CELL; LIVER FAILURE; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CARBON MONOXIDE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME INDUCTION; HEME OXYGENASE (DECYCLIZING); LIVER FAILURE; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; NITRIC OXIDE;

EID: 0344737602     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031003     Document Type: Article

References (35)

1. Saavedra, J.E., T.R. Billiar, D.L. Williams, Y.M. Kim, S.C. Watkins, and L.K. Keefer. 1997. Targeting nitric oxide (NO) delivery in vivo. Design of a liver-selective NO donor prodrug that blocks tumor necrosis factor-alpha-induced apoptosis and toxicity in the liver. J. Med. Chem. 40:1947-1954.
2. Mojena, M., S. Hortelano, A. Castrillo, M.J. Diaz-Guerra, M.J. Garcia-Barchino, G.T. Saez, and L. Bosca. 2001. Protection by nitric oxide against liver inflammatory injury in animals carrying a nitric oxide synthase-2 transgene. FASEB J. 15:583-585.
3. Otterbein, L., S.L. Sylvester, and A.M. Choi. 1995. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J. Respir. Cell Mol. Biol. 13:595-601.
4. Tamion, F., V. Richard, Y. Lacoume, and C. Thuillez. 2002. Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G408-G414.
5. Amersi, F., R. Buelow, H. Kato, B. Ke, A.J. Coito, X.D. Shen, D. Zhao, J. Zaky, J. Melinek, and C.R. Lassman. 1999. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J. Clin. Invest. 104:1631-1639.
6. Vogt, B.A., T.P. Shanley, A. Croatt, J. Alam, K.J. Johnson, and K.A. Nath. 1996. Glomerular inflammation induces resistance to tubular injury in the rat. A novel form of acquired, heme oxygenase-dependent resistance to renal injury. J. Clin. Invest. 98:2139-2145.
7. Soares, M.P., Y. Lin, J. Anrather, E. Csizmadia, K. Takigami, K. Sato, S.T. Grey, R.B. Colvin, A.M. Choi, K.D. Poss, et al. 1998. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat. Med. 4:1073-1077.
8. Otterbein, L.E., F.H. Bach, J. Alam, M. Soares, L.H. Tao, M. Wysk, R.J. Davis, R.A. Flavell, and A.M. Choi. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:422-428.
9. Fujita, T., K. Toda, A. Karimova, S.F. Yan, Y. Naka, S.F. Yet, and D.J. Pinsky. 2001. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 7:598-604.
10. Naughton, P., R. Foresti, S.K. Bains, M. Hoque, C.J. Green, and R. Motterlini. 2002. Induction of heme oxygenase 1 by nitrosative stress. A role for nitroxyl anion. J. Biol. Chem. 277:40666-40674.
11. Kim, Y.M., H.A. Bergonia, C. Muller, B.R. Pitt, W.D. Watkins, and J.R. Lancaster, Jr. 1995. Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 270:5710-5713.
12. Maulik, N., D.T. Engelman, M. Watanabe, R.M. Engelman, and D.K. Das. 1996. Nitric oxide-a retrograde messenger for carbon monoxide signalling in ischemic heart. Mol. Cell. Biochem. 157:75-86.
13. Kim, Y.M., M.E. de Vera, S.C. Watkins, and T.R. Billiar. 1997. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272:1402-1411.
14. Hellerbrand, C., C. Jobin, Y. Iimuro, L. Licato, R.B. Sartor, and D.A. Brenner. 1998. Inhibition of NFkappaB in activated rat hepatic stellate cells by proteasome inhibitors and an IkappaB super-repressor. Hepatology. 27:1285-1295.
15. Chow, J.C., D.W. Young, D.T. Golenbock, W.J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689-10692.
16. Lowenstein, C.J., E.W. Alley, P. Raval, A.M. Snowman, S.H. Snyder, S.W. Russell, and W.J. Murphy. 1993. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA. 90:9730-9734.
17. Taylor, B.S., M.E. de Vera, R.W. Ganster, Q. Wang, R.A. Shapiro, S.M. Morris, Jr., T.R. Billiar, and D.A. Geller. 1998. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 273:15148-15156.
18. Otterbein, L.E., J.K. Kolls, L.L. Mantell, J.L. Cook, J. Alam, and A.M.K. Choi. 1999. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung. J. Clin. Invest. 103:1047-1054.
19. Pannen, B.H., N. Kohler, B. Hole, M. Bauer, M.G. Clemens, and K.K. Geiger. 1998. Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J. Clin. Invest. 102:1220-1228.
20. Sass, G., K. Koerber, and G. Tiegs. 2002. TNF tolerance and cytotoxicity in the liver: the role of interleukin-1beta, inducible nitric oxide-synthase and heme oxygenase-in D-galactosamine-sensitized mice. Inflamm. Res. 51:229-235.
21. Brouard, S., L.E. Otterbein, J. Anrather, E. Tobiasch, F.H. Bach, A.M. Choi, and M.P. Soares. 2000. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 192:1015-1026.
22. Gunther, L., P.O. Berberat, M. Haga, S. Brouard, R.N. Smith, M.P. Soares, F.H. Bach, and E. Tobiasch. 2002. Carbon monoxide protects pancreatic beta-cells from apoptosis and improves islet function/survival after transplantation. Diabetes. 51:994-999.
23. Petrache, I., L.E. Otterbein, J. Alam, G.W. Wiegand, and A.M. Choi. 2000. Heme oxygenase-1 inhibits TNF-alpha-induced apoptosis in cultured fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L312-L319.
24. Otterbein, L.E., B.S. Zuckerbraun, M. Haga, F. Liu, R. Song, A. Usheva, C. Stachulak, N. Bodyak, R.N. Smith, E. Csizmadia, et al. 2003. Carbon monoxide prevents intimal thickening associated with chronic graft rejection and with balloon injury. Nat. Med. 9:183-190.
25. Beg, A.A., W.C. Sha, R.T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature. 376:167-170.
26. Beg, A.A., and D. Baltimore. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 274:782-784.
27. Van Antwerp, D.J., S.J. Martin, T. Kafri, D.R. Green, and I.M. Verma. 1996. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science. 274:787-789.
28. Kim, Y.M., T.H. Kim, D.W. Seol, R.V. Talanian, and T.R. Billiar. 1998. Nitric oxide suppression of apoptosis occurs in association with an inhibition of Bcl-2 cleavage and cytochrome c release. J. Biol. Chem. 273:31437-31441.
29. Kim, Y.M., R.V. Talanian, and T.R. Billiar. 1997. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272: 31138-31148.
30. Sass, G., K. Koerber, R. Bang, H. Guehring, and G. Tiegs. 2001. Inducible nitric oxide synthase is critical for immune-mediated liver injury in mice. J. Clin. Invest. 107:439-447.
31. Otterbein, L.E., M.P. Soares, K. Yamashita, and F.H. Bach. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24:449-455.
32. Stenger, S., N. Donhauser, H. Thuring, M. Rollinghoff, and C. Bogdan. 1996. Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183: 1501-1514.
33. Hinson, J.A., D.W. Roberts, R.W. Benson, K. Dalhoff, S. Loft, and H.E. Poulsen. 1990. Mechanism of paracetamol toxicity. Lancet. 335:732.
34. Zhang, J., W. Huang, S.S. Chua, P. Wei, and D.D. Moore. 2002. Modulation of acetominophen-induced hepatotoxicity by the xenobiotic receptor CAR. Science. 298:422-424.
35. Henderson, C.J., C.P., Wolf, N. Kitteringham, H. Powell, D. Otto, and B.K. Park. 2000. Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc. Natl. Acad. Sci. USA. 7:12741-12745.