Nitric oxide and chemically induced hepatotoxicity: Beneficial effects of the liver-selective nitric oxide donor, V-PYRRO/NO

Toxicology

Volumn 208, Issue 2, 2005, Pages 289-297

  Liu, Jie ^a   Waalkes, Michael P ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

eNOS; Hepatoprotection; Hepatotoxicity; iNOS; Nitric oxide; NO donor; V PYRRO NO

Indexed keywords

LIVER PROTECTIVE AGENT; NITRIC OXIDE; NITRIC OXIDE DONOR; O 2 VINYL 1 (PYRROLIDIN 1 YL)DIAZEN 1 IUM 1,2 DIOLATE; PRODRUG; UNCLASSIFIED DRUG;

ACUTE TOXICITY; CELL PROTECTION; CYTOPATHOLOGY; DRUG DESIGN; DRUG EFFECT; DRUG POTENCY; DRUG SYNTHESIS; KNOCKOUT MOUSE; LIVER FUNCTION; LIVER METABOLISM; LIVER PROTECTION; LIVER TOXICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TOXICOKINETICS; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

EID: 13244257106     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2004.11.017     Document Type: Article

References (69)

1. M. Aiba, I. Takeyoshi, S. Ohwada, Y. Kawashima, K. Iwanami, Y. Sunose, T. Yamada, H. Tsutsumi, K. Matsumoto, and Y. Morishita Novel nitric oxide donor (FK409) ameliorates liver damage during extended liver resection with warm ischemia in dogs J. Am. Coll. Surg. 193 2001 264 271
2. R. Anaya-Prado, L.H. Toledo-Pereyra, R.F. Guo, J. Reuben, P.A. Ward, and J. Walsh The attenuation of hemorrhage-induced liver injury by exogenous nitric oxide, l-arginine, and inhibition of inducible nitric oxide synthase J. Invest. Surg. 16 2003 247 261
3. I. Bohlinger, M. Leist, J. Barsig, S. Uhlig, G. Tiegs, and A. Wendel Tolerance against tumor necrosis factor alpha (TNF)-induced hepatotoxicity in mice: the role of nitric oxide Toxicol. Lett. 82/83 1995 227 231
4. K.M. Brown, J.J. Brems, F.N. Moazzam, G.G. Hartman, R.L. Gamelli, and J.W. Ding The nitric oxide donor molsidomine improves survival and reduces hepatocyte apoptosis in cholestasis and endotoxemia J. Am. Coll. Surg. 197 2003 261 269
5. G.S. Buzard, and K.S. Kasprzak Possible roles of nitric oxide and redox cell signaling in metal-induced toxicity and carcinogenesis: a review J. Environ. Pathol. Toxicol. Oncol. 19 2000 179 199
6. B. Chang, M. Nishikawa, E. Sato, and M. Inoue Mice lacking inducible nitric oxide synthase show strong resistance to anti-Fas antibody-induced fulminant hepatitis Arch. Biochem. Biophys. 411 2003 63 72
7. T. Chen, R. Zamora, B. Zuckerbraun, and T.R. Billiar Role of nitric oxide in liver injury Curr. Mol. Med. 3 2003 519 526
8. L.D. Deleve, X. Wang, G.C. Kanel, Y. Ito, N.W. Bethea, M.K. McCuskey, Z.A. Tokes, J. Tsai, and R.S. McCuskey Decreased hepatic nitric oxide production contributes to the development of rat sinusoidal obstruction syndrome Hepatology 38 2003 900 908
9. H. Farghali, N. Canova, N. Gaier, D. Lincova, E. Kmonickova, P. Strestikova, and K. Masek Inhibition of endotoxemia-induced nitric oxide synthase expression by cyclosporin A enhances hepatocyte injury in rats: amelioration by NO donors Int. Immunopharmacol. 2 2002 117 127
10. R. Farzaneh-Far, and K. Moore Nitric oxide and the liver Liver 21 2001 161 174
11. S. Fiorucci, E. Antonelli, O. Morelli, A. Mencarelli, A. Casini, T. Mello, B. Palazzetti, D. Tallet, P. del Soldato, and A. Morelli NCX-1000, a NO-releasing derivative of ursodeoxycholic acid, selectively delivers NO to the liver and protects against development of portal hypertension Proc. Natl. Acad. Sci. U.S.A. 98 2001 8897 8902
12. S. Fiorucci, A. Mencarelli, B. Palazzetti, P. Del Soldato, A. Morelli, and L.J. Ignarro An NO derivative of ursodeoxycholic acid protects against Fas-mediated liver injury by inhibiting caspase activity Proc. Natl. Acad. Sci. U.S.A. 98 2001 2652 2657
13. S. Fiorucci, A. Elisabetta, C. Carlo, S. Laura, O. Stefano, B. Monia, D.S. Piero, and M. Antonio NCX-1000, a no-releasing derivative of UDCA, exerts anticholestatic effects in a rodent model of chronic cholangitis Hepatology 36 Suppl. 2002 719
14. S. Fiorucci, E. Antonelli, A. Mencarelli, B. Palazzetti, L. Alvarez-Miller, M. Muscara, P. del Soldato, L. Sanpaolo, J.L. Wallace, and A. Morelli A NO-releasing derivative of acetaminophen spares the liver by acting at several checkpoints in the Fas pathway Br. J. Pharmacol. 135 2002 589 599
15. S. Fiorucci, E. Antonelli, and A. Morelli Nitric oxide and portal hypertension: a nitric oxide-releasing derivative of ursodeoxycholic acid that selectively releases nitric oxide in the liver Digest. Liver Dis. 35 Suppl. 2 2003 S61 S69
16. A.L. Fitzhugh, and L.K. Keefer Diazeniumdiolates: pro- and antioxidant applications of the "NONOates" Free Radic. Biol. Med. 28 2000 1463 1469
17. L.E. Futter, O.A. al-Swayeh, and P.K. Moore A comparison of the effect of nitroparacetamol and paracetamol on liver injury Br. J. Pharmacol. 132 2001 10 12
18. C.R. Gardner, D.E. Heck, C.S. Yang, P.E. Thomas, X.J. Zhang, G.L. DeGeorge, J.D. Laskin, and D.L. Laskin Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat Hepatology 27 1998 748 754
19. C.R. Gardner, J.D. Laskin, D.M. Dambach, M. Sacco, S.K. Durham, M.K. Bruno, S.D. Cohen, M.K. Gordon, D.R. Gerecke, P. Zhou, and D.L. Laskin Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: potential role of tumor necrosis factor-alpha and interleukin-10 Toxicol. Appl. Pharmacol. 184 2002 27 36
20. E. Gumpricht, R. Dahl, B. Yerushalmi, M.W. Devereaux, and R.J. Sokol Nitric oxide ameliorates hydrophobic bile acid-induced apoptosis in isolated rat hepatocytes by non-mitochondrial pathways J. Biol. Chem. 277 2002 25823 25830
21. Y. Gundersen, C.O. Corso, R. Leiderer, M. Dorger, P. Lilleaasen, A.O. Aasen, and K. Messmer The nitric oxide donor sodium nitroprusside protects against hepatic microcirculatory dysfunction in early endotoxaemia Intens. Care Med. 24 1998 1257 1263
22. E.B. Harstad, and C.D. Klaassen iNOS-null mice are not resistant to cadmium chloride-induced hepatotoxicity Toxicology 175 2002 83 90
23. M.J. Hickey, K.A. Sharkey, E.G. Sihota, P.H. Reinhardt, J.D. Macmicking, C. Nathan, and P. Kubes Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia FASEB J. 11 1997 955 964
24. C. Hierholzer, B. Harbrecht, J.M. Menezes, J. Kane, J. MacMicking, C.F. Nathan, A.B. Peitzman, T.R. Billiar, and D.J. Tweardy Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock J. Exp. Med. 187 1998 917 928
25. I.N. Hines, S. Kawachi, H. Harada, K.P. Pavlick, J.M. Hoffman, S. Bharwani, R.E. Wolf, and M.B. Grisham Role of nitric oxide in liver ischemia and reperfusion injury Mol. Cell. Biochem. 234/235 2002 229 237
26. J.A. Hinson, S.L. Pike, N.R. Pumford, and P.R. Mayeux Nitrotyrosine-protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice Chem. Res. Toxicol. 11 1998 604 607
27. J.A. Hinson, T.J. Bucci, L.K. Irwin, S.L. Michael, and P.R. Mayeux Effect of inhibitors of nitric oxide synthase on acetaminophen-induced hepatotoxicity in mice Nitric Oxide 6 2002 160 167
28. D.R. Janero Nitric oxide (NO)-related pharmaceuticals: contemporary approaches to therapeutic NO modulation Free Radic. Biol. Med. 28 2000 1495 1506
29. M.S. Joshi, J.L. Ponthier, and J.R. Lancaster Jr. Cellular antioxidant and pro-oxidant actions of nitric oxide Free Radic. Biol. Med. 27 1999 1357 1366
30. S. Kawachi, I.N. Hines, F.S. Laroux, J. Hoffman, S. Bharwani, L. Gray, D. Leffer, and M.B. Grisham Nitric oxide synthase and postischemic liver injury Biochem. Biophys. Res. Commun. 276 2000 851 854
31. L.K. Keefer Progress toward clinical application of the nitric oxide-releasing diazeniumdiolates Annu. Rev. Pharmacol. Toxicol. 43 2003 585 607
32. Y.M. Kim, M.E. de Vera, S.C. Watkins, and T.R. Billiar Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression J. Biol. Chem. 272 1997 1402 1411
33. Y.M. Kim, T.-H. Kim, H.-T. Chung, R.V. Talanian, X.-M. Yin, and T.R. Billiar Nitric oxide prevents tumor necrosis factor α-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8 Hepatology 32 2000 770 778
34. P.K. Kim, and T.R. Billiar Give me iNOS or give me death Hepatology 34 2001 436 437
35. 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
36. N.H. Kumins, J. Hunt, R.L. Gamelli, and J.P. Filkins Molsidomine increases endotoxic survival and decreases cytokine production Shock 7 1997 200 205
37. D.L. Laskin, del Valle M. Rodriguez, D.E. Heck, S.M. Hwang, S.T. Ohnishi, S.K. Durham, N.L. Goller, and J.D. Laskin Hepatic nitric oxide production following acute endotoxemia in rats is mediated by increased inducible nitric oxide synthase gene expression Hepatology 22 1995 223 234
38. J.D. Laskin, D.E. Heck, C.R. Gardner, and D. Laskin Prooxidant and antioxidant functions of nitric oxide in liver toxicity Antioxid. Redox. Signal 3 2001 261 271
39. V.G. Lee, M.L. Johnson, J. Baust, V.E. Laubach, S.C. Watkins, and T.R. Billiar The roles of iNOS in liver ischemia-reperfusion injury Shock. 16 2001 355 360
40. 2-vinyl 1-(pyrrolidin-1-yl)diazen-1-ium-1,2-diolate protection against d-galactosamine/endotoxin-induced hepatotoxicity in mice: genomic analysis using microarrays J. Pharmacol. Exp. Ther. 300 2002 18 25
41. J. Liu, C. Li, M.P. Waalkes, J. Clark, P. Myers, J.E. Saavedra, and L.K. Keefer The nitric oxide donor, V-PYRRO/NO, protects against acetaminophen- induced hepatotoxicity in mice Hepatology 37 2003 324 333
42. 2-vinyl 1-(pyrrolidin-1-yl)diazen-1-ium-1,2-diolate (V-PYRRO/NO), protects against cadmium-induced hepatotoxicity in mice J. Pharmacol. Exp. Therap. 310 2004 18 24
43. M. Loureiro-Silva, G.W. Cadelina, and Y. Iwakiri A liver-specific nitric oxide donor improves the intra-hepatic vascular response to increase portal blood flow and methoxamine in cirrhotic rats Hepatology 38 suppl. 2003 44
44. S.L. Michael, P.R. Mayeux, T.J. Bucci, A.R. Warbritton, L.K. Irwin, N.R. Pumford, and J.A. Hinson Acetaminophen-induced hepatotoxicity in mice lacking inducible nitric oxide synthase activity Nitric Oxide 5 2001 432 441
45. F. Moal, D. Chappard, J. Wang, E. Vuillemin, S. Michalak-Provost, M.C. Rousselet, F. Oberti, and P. Cales Fractal dimension can distinguish models and pharmacologic changes in liver fibrosis in rats Hepatology 36 2002 840 849
46. P.K. Moore, and M. Marshall Nitric oxide releasing acetaminophen (nitroacetaminophen) Digest. Liver Dis. 35 Suppl. 2 2003 S49 S60
47. L.A. Morio, H. Chiu, K.A. Sprowles, P. Zhou, D.E. Heck, M.K. Gordon, and D.L. Laskin Distinct roles of tumor necrosis factor-alpha and nitric oxide in acute liver injury induced by carbon tetrachloride in mice Toxicol. Appl. Pharmacol. 172 2001 44 51
48. H. Ohmori, D.K. Dhar, Y. Nakashima, M. Hashimoto, S. Masumura, and N. Nagasue Beneficial effects of FK409, a novel nitric oxide donor, on reperfusion injury of rat liver Transplantation 66 1998 579 585
49. J. Ou, T.M. Carlos, S.C. Watkins, J.E. Saavedra, L.K. Keefer, Y.M. Kim, B.G. Harbrecht, and T.R. Billiar Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and neutrophil accumulation during endotoxemia Nitric Oxide 1 1997 404 416
50. H. Ozturk, Y. Yagmur, H. Buyukbayram, A.I. Dokucu, and A. Gurel Effects of the nitric oxide donor molsidomine on the early stages of liver damage in rats with bile duct ligation: a biochemical and immunohistochemical approach Eur. Surg. Res. 34 2002 285 290
51. C. Peralta, R. Rull, A. Rimola, R. Deulofeu, J. Rosello-Catafau, E. Gelpi, and J. Rodes Endogenous nitric oxide and exogenous nitric oxide supplementation in hepatic ischemia-reperfusion injury in the rat Transplantation 71 2001 529 536
52. R.M. Rai, F.Y. Lee, A. Rosen, S.Q. Yang, H.Z. Lin, A. Koteish, F.Y. Liew, C. Zaragoza, C. Lowenstein, and A.M. Diehl Impaired liver regeneration in inducible nitric oxide synthasedeficient mice Proc. Natl. Acad. Sci. U.S.A. 95 1998 13829 13834
53. R. Ricciardi, D.P. Foley, S.H. Quarfordt, J.E. Saavedra, L.K. Keefer, S.M. Wheeler, S.E. Donohue, M.P. Callery, and W.C. Meyers V-PYRRO/NO: a hepato-selective nitric oxide donor improves porcine liver hemodynamics and function after ischemia reperfusion Transplantation 71 2001 193 198
54. D.C. Rockey Vascular mediators in the injured liver Hepatology 37 2003 4 12
55. B. Rosenkranz, B.R. Winkelmann, and M.J. Parnham Clinical pharmacokinetics of molsidomine Clin. Pharmacokinet. 30 1996 372 384
56. J.E. Saavedra, T.R. Billiar, D.L. Williams, Y.M. Kim, S.C. Watkins, and L.K. Keefer 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 1997 1947 1954
57. G. Sass, K. Koerber, R. Bang, H. Guehring, and G. Tiegs Inhibition of endotoxemia-induced nitric oxide synthase expression by cyclosporin A enhances hepatocyte injury in rats: amelioration by NO donors Int. Immunopharmacol. 2 2002 117 127
58. M.B. Sewer, T.B. Barclay, and E.T. Morgan Down-regulation of cytochrome P450 mRNAs and proteins in mice lacking a functional NOS2 gene Mol. Pharmacol. 54 1998 273 279
59. T. Shimamura, Y. Zhu, S. Zhang, M.B. Jin, N. Ishizaki, A. Urakami, E. Totsuka, A. Kishida, R. Lee, V. Subbotin, H. Furukawa, T.E. Starzl, and S. Todo Protective role of nitric oxide in ischemia and reperfusion injury of the liver J. Am. Coll. Surg. 188 1999 43 52
60. H.S. So, B.H. Jung, H.S. Song, S. Myung Kim, J.S. Park, K.M. Chae, J.H. Lee, S.Y. Chung, H.J. Chae, H.R. Kim, and R. Park Nitric oxide prevents the IFN-gamma/LPS-induced hepatotoxicity in a protein kinase G-independent manner Immunopharmacol. Immunotoxicol. 23 2001 321 334
61. J.A. Spitzer, M. Zheng, J.K. Kolls, C. Vande Stouwe, and J.J. Spitzer Ethanol and LPS modulate NF-kappaB activation, inducible NO synthase and COX-2 gene expression in rat liver cells in vivo Front Biosci. 7 2002 99 108
62. S.F. Stinson, T. House, C. Bramhall, J.E. Saavedra, L.K. Keefer, and R.W. Nims Plasma pharmacokinetics of a liver-selective nitric oxide-donating diazeniumdioate in the male C57BL/6 mouse Xenobiotica 32 2002 339 347
63. N. Tanaka, K. Tanaka, Y. Nagashima, M. Kondo, and H. Sekihara Nitric oxide increases hepatic arterial blood flow in rats with carbon tetrachloride-induced acute hepatic injury Gastroenterology 117 1999 173 180
64. N.G. Theodorakis, Y.N. Wang, N.J. Skill, M.A. Metz, P.A. Cahill, E.M. Redmond, and J.V. Sitzmann The role of nitric oxide synthase isoforms in extrahepatic portal hypertension: studies in gene-knockout mice Gastroenterology 124 2003 1500 1508
65. Y. Wang, W.R. Mathews, D.M. Guido, A. Farhood, and H. Jaeschke Inhibition of nitric oxide synthesis aggravates reperfusion injury after hepatic ischemia and endotoxemia Shock 4 1995 282 288
66. L.W. Weber, M. Boll, and A. Stampfl Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model Crit. Rev. Toxicol. 33 2003 105 136
67. G.M. Wray, C.G. Millar, C.J. Hinds, and C. Thiemermann Selective inhibition of the activity of inducible nitric oxide synthase prevents the circulatory failure, but not the organ injury/dysfunction, caused by endotoxin Shock 9 1998 329 335
68. G.P. Yagnik, Y. Takahashi, G. Tsoulfas, K. Reid, N. Murase, and D.A. Geller Blockade of the l-arginine/NO synthase pathway worsens hepatic apoptosis and liver transplant preservation injury Hepatology 36 2002 573 581
69. R. Zamora, Y. Vodovotz, K.S. Aulak, P.K. Kim, J.M. Kane III, L. Alarcon, D.J. Stuehr, and T.R. Billiar A DNA microarray study of nitric oxide-induced genes in mouse hepatocytes: implications for hepatic heme oxygenase-1 expression in ischemia-reperfusion Nitric Oxide 7 2002 165 186