Modulation of Spontaneous and Lipopolysaccharide-Induced Nitric Oxide Production and Apoptosis by D-Galactosamine in Rat Hepatocyte Culture: The Significance of Combinations of Different Methods

REFERENCES

• Abou-Elella A. M., Siendones E., Padillo J., Montero J. L., De la Mata M., Muntane Relat J. Tumour necrosis factor-alpha and nitric oxide mediate apoptosis by D-galactosamine in a primary culture of rat hepatocytes: exacerbation of cell death by cocultured Kupffer cells. Can. J. Gastroenterol. 2002; 16(11)791–799
   Google Scholar
• Ayala A., Evans T. A., Chaudry I. H. Does hepatocellular injury in sepsis involve apoptosis? J. Surg. Res. 1998; 76(2)165–173
   Google Scholar
• Azzaroli F., Mehal W., Soroka C. J., Wang L., Lee J., Crispe N., Boyer J. L. Ursodeoxycholic acid diminishes Fas-ligand induced apoptosis in mouse hepatocytes. Hepatology 2002; 36(1)49–54
   Google Scholar
• Bilodeau M. Liver cell death: update on apoptosis. Can. J. Gastroenterol. 2003; 17(8)501–506
   Google Scholar
• Chung H. T., Pae H. O., Choi B. M., Billiar T. R., Kim Y. M. Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 2001; 282(5)1075–1079
   PubMed Web of Science ®Google Scholar
• Decker K., Keppler D. Galactosamine induced liver injury. Prog. Liver Dis. 1972; 4: 183–199
   PubMedGoogle Scholar
• Dilworth C., Bigot-Lasserre D., Bars R. Spontaneous nitric oxide in hepatocyte monolayers and inhibition of compound-induced apoptosis. Toxicol. In Vitro 2001; 15(6)623–630
   Google Scholar
• Farghali H., Buchar E., Machkova Z., Kamenikova L., Masek K. Muramyl dipeptide and carbon tetrachloride hepatotoxicity in rats: involvement of plasma membrane and calcium homeostasis in protective effect. Method Find. Exp. Clin. Pharmacol. 1986; 8(8)469–477
   Google Scholar
• Farghali H., Canova N., Gaier N., Lincova D., Kmonickova E., Strestikova P., Masek K. Inhibition of endotoxemia-induced nitric oxide synthase expression by cyclosporin A enhances hepatocyte injury in rats: amelioration by NO donors. Int. Immunopharmacol. 2002; 2(1)117–127
   Google Scholar
• Farghali H., Canova N., Kucera T., Martinek J., Masek K. Nitric oxide synthase inhibitors modulate lipopolysaccharide-induced hepatocyte injury: dissociation between in vivo and in vitro effects. Int. Immunopharmacol. 2003; 3(12)1627–1638
   Google Scholar
• Farghali H., Zidek Z., Hynie S. Effects of nitroprusside as a nitric oxide donor on anoxia/reoxygenation and D-galactosamine hepatic injuries: a study in perfused hepatocytes. Physiol. Res. 1997; 46(5)363–369
   Google Scholar
• Freudenberg M. A., Galanos C. Tumor necrosis factor alpha mediates lethal activity of killed gram-negative and gram-positive bacteria in D-galactosamine-treated mice. Infect. Immun. 1991; 59(6)2110–2115
   Google Scholar
• Galanos C., Freudenberg M. A., Reutter W. Galactosamine-induced sensitization to the lethal effects of endotoxin. Proc. Natl. Acad. Sci. U S A 1979; 76(11)5939–5943
   PubMed Web of Science ®Google Scholar
• Gujral J. S., Farhood A., Jaeschke H. Oncotic necrosis and caspase-dependent apoptosis during galactosamine-induced liver injury in rats. Toxicol. Appl. Pharmacol. 2003; 190(1)37–46
   Google Scholar
• Hamada E., Nishida T., Uchiyama Y., Nakamura J., Isahara K., Kazuo H., Huang T. P., Momoi T., Ito T., Matsuda H. Activation of Kupffer cells and caspase-3 involved in rat hepatocyte apoptosis induced by endotoxin. J. Hepatol. 1999; 30(5)807–818
   Google Scholar
• Heyninck K., Wullaert A., Beyaert R. Nuclear factor-kappa B plays a central role in tumour necrosis factor-mediated liver disease. Biochem. Pharmacol. 2003; 66(8)1409–1415
   PubMed Web of Science ®Google Scholar
• Iio S., Hayashi N., Mita E., Ueda K., Mochizuki K., Hiramatsu N., Kanto T., Sasaki Y., Kasahara A., Hori M. Serum levels of soluble Fas antigen in chronic hepatitis C patients. J. Hepatol. 1998; 29(4)517–523
   Google Scholar
• Ilan E., Tirosh O., Madar Z. Triacylglycerol-mediated oxidative stress inhibits nitric oxide production in rat isolated hepatocytes. J. Nutr. 2005; 135(9)2090–2095
   Google Scholar
• Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am. J. Physiol. Gastrointest. Liver Physiol. 2003; 284(1)G15–26
   PubMed Web of Science ®Google Scholar
• Kaplowitz N. Biochemical and cellular mechanisms of toxic liver injury. Semin. Liver Dis. 2002; 22(2)137–144
   PubMed Web of Science ®Google Scholar
• Katunuma N., Matsui A., Le Q. T., Utsumi K., Salvesen G., Ohashi A. Novel procaspase-3 activating cascade mediated by lysoapoptases and its biological significances in apoptosis. Adv. Enzyme Regul. 2001; 41: 237–250
   PubMedGoogle Scholar
• Keppler D. O., Pausch J., Decker K. Selective uridine triphosphate deficiency induced by D-galactosamine in liver and reversed by pyrimidine nucleotide precursors. Effect on ribonucleic acid synthesis. J. Biol. Chem. 1974; 249(1)211–216
   Google Scholar
• Kim P. K., Zamora R., Petrosko P., Billiar T. R. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 2001; 1(8)1421–1441
   PubMed Web of Science ®Google Scholar
• Kim Y. M., Talanian R. V., Billiar T. R. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 1997; 272(49)31138–31148
   PubMed Web of Science ®Google Scholar
• Kishikawa H., Sakamoto A., Ogawa R. Nitric oxide suppresses hepatocyte apoptosis induced by free radicals. Biomed. Res. (Tokyo) 2001; 22(2)83–89
   Google Scholar
• Kucera O., Cervinkova Z., Lotkova H., Krivakova P., Rousar T., Muzakova V., Hezova R., Kandar R., Rudolf E. Protective effect of S-adenosylmethionine against D-galactosamine-induced injury of rat hepatocytes in primary culture. Physiol. Res. 2006; 55(5)551–560
   Google Scholar
• Kumar A., Takada Y., Boriek A. M., Aggarwal B. B. Nuclear factor-kappaB: its role in health and disease. J. Mol. Med. 2004; 82(7)434–448
   PubMed Web of Science ®Google Scholar
• Kuwabara T., Imajoh-Ohmi S. LPS-induced apoptosis is dependent upon mitochondrial dysfunction. Apoptosis 2004; 9(4)467–474
   Google Scholar
• Lemaire C., Andreau K., Souvannavong V., Adam A. Inhibition of caspase activity induces a switch from apoptosis to necrosis. FEBS Lett. 1998; 425(2)266–270
   Google Scholar
• Li J., Billiar T. R. Nitric oxide. IV. Determinants of nitric oxide protection and toxicity in liver. Am. J. Physiol. 1999; 276(5 Pt 1)G1069–1073
   Google Scholar
• Liao C. H., Sang S., Liang Y. C., Ho C. T., Lin J. K. Suppression of inducible nitric oxide synthase and cyclooxygenase-2 in downregulating nuclear factor-kappa B pathway by Garcinol. Mol. Carcinog. 2004; 41(3)140–149
   PubMed Web of Science ®Google Scholar
• Liu J., Li C., Waalkes M. P., Clark J., Myers P., Saavedra J. E., Keefer L. K. The nitric oxide donor, V-PYRRO/NO, protects against acetaminophen-induced hepatotoxicity in mice. Hepatology 2003; 37(2)324–333
   PubMed Web of Science ®Google Scholar
• Liu J., Waalkes M. P. Nitric oxide and chemically induced hepatotoxicity: beneficial effects of the liver-selective nitric oxide donor, V-PYRRO/NO. Toxicology 2005; 208(2)289–297
   Google Scholar
• McDonald J. R., Thayer K. J., White C. Inhibition of galactosamine cytotoxicity in an in vivo/in vitro hepatocellular toxicity model. Toxicol. Appl. Pharmacol. 1987; 89(2)269–277
   Google Scholar
• McMillan J. M. Galactosamine decreases nitric oxide formation in cultured rat hepatocytes: lack of involvement in cytotoxicity. J. Biochem. Mol. Toxicol. 1999a; 13(3–4)135–142
   Google Scholar
• McMillan J. M. Galactosamine decreases nitric oxide formation in cultured rat hepatocytes: mechanism of suppression. J. Biochem. Mol. Toxicol. 1999b; 13(3–4)143–148
   Google Scholar
• McMillan J. M., Jollow D. J. Macrophage enhancement of galactosamine hepatotoxicity using a rat hepatocyte culture system. Res. Commun. Mol. Pathol. Pharmacol. 1995; 88(3)327–338
   Google Scholar
• McMillan J. M., McMillan D. C. S-Adenosylmethionine but not glutathione protects against galactosamine-induced cytotoxicity in rat hepatocyte cultures. Toxicology 2006; 222(3)175–184
   Google Scholar
• McNaughton L., Puttagunta L., Martinez-Cuesta M. A., Kneteman N., Mayers I., Moqbel R., Hamid Q., Radomski M. W. Distribution of nitric oxide synthase in normal and cirrhotic human liver. Proc. Natl. Acad. Sci. U S A 2002; 99(26)17161–17166
   Google Scholar
• Minana J., Gomez-Cambronero L., Lloret A., Pallardo F. V., Del Olmo J., Escudero A., Rodrigo J. M., Pelliin A., Vina J. R., Vina J., Sastre J. Mitochondrial oxidative stress and CD95 ligand: a dual mechanism for hepatocyte apoptosis in chronic alcoholism. Hepatology 2002; 35(5)1205–1214
   Google Scholar
• Moldeus P., Hogberg J., Orrenius S. Isolation and use of liver cells. Methods in Enzymology, S. Fleisher, L. Packer. Academic Press, New York 1978; 52: 60–71
   Google Scholar
• Morikawa A., Kato Y., Sugiyama T., Koide N., Chakravortty D., Yoshida T., Yokochi T. Role of nitric oxide in lipopolysaccharide-induced hepatic injury in D-galactosamine-sensitized mice as an experimental endotoxic shock model. Infect. Immun. 1999; 67(3)1018–1024
   PubMed Web of Science ®Google Scholar
• Natori S., Rust C., Stadheim L., Srinivasan A., Burgart L. J., Gores G. J. Hepatocyte apoptosis is a pathologic feature of human alcoholic hepatitis. J. Hepatol. 2001; 34(2)248–253
   PubMed Web of Science ®Google Scholar
• Rodriguez-Ariza A., Lopez-Sanchez L. M., Gonzalez R., Corrales F. J., Lopez P., Bernardos A., Muntane J. Altered protein expression and protein nitration pattern during D-galactosamine-induced cell death in human hepatocytes: a proteomic analysis. Liver Int. 2005; 25(6)1259–1269
   Google Scholar
• Sass G., Koerber K., Bang R., Guehring H., Tiegs G. Inducible nitric oxide synthase is critical for immune-mediated liver injury in mice. J. Clin. Invest. 2001; 107(4)439–447
   PubMed Web of Science ®Google Scholar
• Schoemaker M. H., Gommans W. M., Conde de la Rosa L., Homan M., Klok P., Trautwein C., van Goor H., Poelstra K., Haisma H. J., Jansen P. L., Moshage H. Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation. J. Hepatol. 2003; 39(2)153–161
   Google Scholar
• Siendones E., Fouad D., Abou-Elella A. M., Quintero A., Barrera P., Muntane J. Role of nitric oxide in D-galactosamine-induced cell death and its protection by PGE1 in cultured hepatocytes. Nitric Oxide 2003; 8(2)133–143
   Web of Science ®Google Scholar
• Siendones E., Fouad D., Diaz-Guerra M. J., de la Mata M., Bosca L., Muntane J. PGE1-induced NO reduces apoptosis by D-galactosamine through attenuation of NF-kappaB and NOS-2 expression in rat hepatocytes. Hepatology 2004; 40(6)1295–1303
   Google Scholar
• Siendones E., Jimenez-Gomez Y., Montero J. L., Gomez-Diaz C., Villalba J. M., Muntane J. PGE1 abolishes the mitochondrial-independent cell death pathway induced by D-galactosamine in primary culture of rat hepatocytes. J. Gastroenterol. Hepatol. 2005; 20(1)108–116
   Google Scholar
• Stachlewitz R. F., Seabra V., Bradford B., Bradham C.A., Rusyn I., Germolec D., Thurman R. G. Glycine and uridine prevent D-galactosamine hepatotoxicity in the rat: role of Kupffer cells. Hepatology 1999; 29(3)737–745
   Google Scholar
• Stramentinoli G., Gualano M., Ideo G. Protective role of S-adenosyl-L-methionine on liver injury induced by D-galactosamine in rats. Biochem. Pharmacol. 1978; 27(10)1431–1433
   Google Scholar
• Taylor B. S., Liu S., Villavicencio R. T., Ganster R. W., Geller D. A. The role of protein phosphatases in the expression of inducible nitric oxide synthase in the rat hepatocyte. Hepatology 1999; 29(4)1199–1207
   Google Scholar
• Tsutsui S., Itagaki S., Kawamura S., Harada K., Karaki H., Doi K., Yoshikawa Y. D-Galactosamine induced hepatocyte apoptosis is inhibited in vivo and in cell culture by a calcium calmodulin antagonist, chlorpromazine, and a calcium channel blocker, verapamil. Exp. Anim. 2003; 52(1)43–52
   PubMed Web of Science ®Google Scholar
• Tunon M. J., Sanchez-Campos S., Gutierrez B., Culebras J. M., Gonzalez-Gallego J. Effects of FK506 and rapamycin on generation of reactive oxygen species, nitric oxide production and nuclear factor kappa B activation in rat hepatocytes. Biochem. Pharmacol. 2003; 66(3)439–445
   PubMed Web of Science ®Google Scholar
• Tzeng E., Billiar T. R., Williams D. L., Li J., Lizonova A., Kovesdi I., Kim Y. M. Adenovirus-mediated inducible nitric oxide synthase gene transfer inhibits hepatocyte apoptosis. Surgery 1998; 124(2)278–283
   Google Scholar
• Wang H., Gao X., Fukumoto S., Tademoto S., Sato K., Hirai K. Post-isolation inducible nitric oxide synthase gene expression due to collagenase buffer perfusion and charaterization of the gene regulation in primary cultured murine hepatocytes. J. Biochem. (Tokyo) 1998; 124(5)892–899
   Google Scholar
• Wu J., Soderbergh H., Karlsson K., Danielsson A. Protective effect of S-adenosyl-L-methionine on bromobenzene- and D-galactosamine-induced toxicity to isolated rat hepatocytes. Hepatology 1996; 23(2)359–365
   Google Scholar
• Wyllie A., Donahue V., Fisher B., Hill D., Keesey J., Manzow S. Apoptosis and cell proliferation, 2nd ed. Biochemica, Menheim 1998; 1–114, Boehringer Menheim GmbH
   Google Scholar
• Yao Y., Zhang D., Luo Y., Zhang D., Huang A., Zhou W., Ren H. Fas ligand expression and apoptosis in primary rat hepatocytes induced by lipopolysaccharide. Zhonghua Gan Zang Bing Za Zhi 2000; 8(5)285–287
   Google Scholar
• Zamora R., Vodovotz Y., Aulak K. S., Kim P. K., Kane J. M., 3rd, Alarcon L., Stuehr D. J., Billiar T. R. A DNA micoarray study of nitric oxide-induced genes in mouse hepatocytes: implications for hepatic heme oxygenase-1 expression in ischemia/reperfusion. Nitric Oxide 2002; 7(3)165–186
   Google Scholar
• Zhao Y., Li S., Childs E. E., Kuharsky D. K., Yin X. M. Activation of pro-death Bcl-2 family proteins and mitochondria apoptosis pathway in tumor necrosis factor-α-induced liver injury. J. Biol. Chem. 2001; 276(29)27432–27440
   Web of Science ®Google Scholar