Journal of Surgical Research
Volume 138, Issue 1 , Pages 15-21 , March 2007

Glycochenodeoxycholate (GCDC) Inhibits Cytokine Induced iNOS Expression in Rat Hepatocytes

Presented at the 1st Annual Academic Surgical Congress (Association for Academic Surgery), San Diego, CA, February 7–11, 2006.

Received 8 January 2006

References 

  1. Schlottman K, Wachs FP, Krieg RC, Kullmann F, Scholmerich J, Rogler G. Characterization of bile salt-induced apoptosis in colon cancer cell lines. Cancer Res. 2000;60:4270
  2. Roberts LR, Kurosawa H, Bronk SF, et al. Cathepsin B contributes to bile salt-induced apoptosis of rat hepatocytes. Gastroenterology. 1997;113:1714
  3. Webster CR, Anwer MS. Cyclic adenosine monophosphate-mediated protection against bile acid-induced apoptosis in cultured rat hepatocytes. Hepatology. 1998;27:1324
  4. Jones BA, Rao YP, Stravitz RT, Gores GJ. Bile salt-induced apoptosis of hepatocytes involves activation of protein kinase C. Am J Physiol. 1997;272:G1109
  5. Sodeman T, Bronk SF, Roberts PJ, Miyoshi H, Gores GJ. Bile salts mediate hepatocyte apoptosis by increasing cell surface trafficking of Fas. Am J Physiol Gastrointest Liver Physiol. 2000;278:G992
  6. Baker PR, Wilton JC, Jones CE, Stenzel DJ, Watson N, Smith GJ. Bile acids influence the growth, oestrogen receptor and oestrogen-regulated proteins of MCF-7 human breast cancer cells. Br J Cancer. 1992;65:566
  7. Yerushalmi B, Dahl R, Devereaux MW, Gumpricht E, Sokol RJ. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology. 2001;33:616
  8. Takikawa Y, Miyoshi H, Rust C, et al. The bile acid-activated phosphatidylinositol 3-kinase pathway inhibits Fas apoptosis upstream of bid in rodent hepatocytes. Gastroenterology. 2001;120:1810
  9. Gurantz D, Hofmann AF. Influence of bile acid structure on bile flow and biliary lipid secretion in the hamster. Am J Physiol. 1984;247:G736
  10. Qiao L, Studer E, Leach K, et al. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and FAS receptor in primary hepatocytes: Inhibition of EGFR/mitogen-activated protein kinase-signaling module enhances DCA-induced apoptosis. Mol Biol Cell. 2001;12:2629
  11. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998;17:1675
  12. Li J, Bombeck CA, Yang S, Kim YM, Billiar TR. Nitric oxide suppresses apoptosis via interrupting caspase activation and mitochondrial dysfunction in cultured hepatocytes. J Biol Chem. 1999;274:17325
  13. Zamora R, Alarcon L, Vodovotz Y, et al. Nitric oxide suppresses the expression of Bcl-2 binding protein BNIP3 in hepatocytes. J Biol Chem. 2001;276:46887
  14. Arnett HA, Hellendall RP, Matsushima GK, et al. The protective role of nitric oxide in a neurotoxicant-induced demyelinating model. J Immunol. 2002;168:427
  15. Gardner CR, Heck DE, et al. Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology. 1998;27:748
  16. Li J, Billiar TR. The role of nitric oxide in apoptosis. Semin Perinatol. 2000;24:46
  17. Farzaneh-Far R, Moore K. Nitric oxide and the liver. Liver. 2001;21:161
  18. Beltran B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S. The effect of nitric oxide on cell respiration: A key to understanding its role in cell survival or death. Proc Natl Acad Sci USA. 2000;97:14602
  19. Salvucci O, Carsana M, Bersani I, Tragni G, Anichini A. Antiapoptotic role of endogenous nitric oxide in human melanoma cells. Cancer Res. 2001;61:318
  20. Li J, Billiar TR. The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death Differ. 1999;6:952
  21. Kim YM, Kim TH, Chung HT, Talanian RV, Yin XM, Billiar TR. Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology. 2000;32:770
  22. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem. 1997;272:31138
  23. Lee YJ, Lee KH, Kim HR, et al. Sodium nitroprusside enhances TRAIL-induced apoptosis via a mitochondria-dependent pathway in human colorectal carcinoma CX-1 cells. Oncogene. 2001;20:1476
  24. Beltran B, Quintero M, Garcia-Zaragoza E, O’Connor E, Esplugues JV, Moncada S. Inhibition of mitochondrial respiration by endogenous nitric oxide: A critical step in Fas signaling. Proc Natl Acad Sci USA. 2002;99:8892
  25. Payne CM, Crowley C, Washo-Stultz D, et al. The stress-response proteins poly(ADP-ribose) polymerase and NF-kappaB protect against bile salt-induced apoptosis. Cell Death Differ. 1998;5:623
  26. Pope M, Marsden PA, Cole E, et al. Resistance to murine hepatitis virus strain 3 is dependent on production of nitric oxide. J Virol. 1998;72:7084
  27. Washo-Stultz D, Hoglen N, Bernstein H, Bernstein C, Payne CM. Role of nitric oxide and peroxynitrite in bile salt-induced apoptosis: Relevance to colon carcinogenesis. Nutr Cancer. 1999;35:180
  28. Suzuki H, Menegazzi M, Carcereri DP, Mariotto S, Armato U. Nitric oxide in the liver: Physiopathological roles. Adv Neuroimmunol. 1995;5:379
  29. Secchiero P, Gonelli A, Celeghini C, et al. Activation of the nitric oxide synthase pathway represents a key component of tumor necrosis factor-related apoptosis-inducing ligand-mediated cytotoxicity on hematologic malignancies. Blood. 2001;98:2220
  30. Feng X, Guo Z, Nourbakhsh M, et al. Identification of a negative response element in the human inducible nitric-oxide synthase (hiNOS) promoter: The role of NF-kappa B-repressing factor (NRF) in basal repression of the hiNOS gene. Proc Natl Acad Sci USA. 2002;99:14212
  31. Tzeng E, Billiar TR, Williams DL, Li J, Lizonova A, Kovesdi I, et al. Adenovirus-mediated inducible nitric oxide synthase gene transfer inhibits hepatocyte apoptosis. Surgery. 1998;124:278
  32. Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem. 1994;269:4705
  33. Taylor BS, de Vera ME, Ganster RW, et al. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem. 1998;273:15148
  34. Ganster RW, Taylor BS, Shao L, Geller DA. Complex regulation of human inducible nitric oxide synthase gene transcription by Stat 1 and NF-kappa B. Proc Natl Acad Sci USA. 2001;98:8638
  35. Invernizzi P, Salzman AL, Szabo C, Ueta I, O’Connor M, Setchell KD. Ursodeoxycholate inhibits induction of NOS in human intestinal epithelial cells and in vivo. Am J Physiol. 1997;273:G131
  36. Ma J, Nakajima T, Iida H, et al. Inhibitory effects of ursodeoxygholic acid on the induction of nitric oxide synthase in vascular smooth muscle cells. Eur J Pharmacol. 2003;464:79
  37. Miyoshi H, Rust C, Guicciardi ME, Gores GJ. NF-kappaB is activated in cholestasis and functions to reduce liver injury. Am J Pathol. 2001;158:967
  38. Schoemaker MH, Gommans WM, de la Rosa LC, et al. Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation. J Hepatol. 2003;39:153
  39. Higuchi H, Miyashi H, Bronk SF, Zhang H, Dean N, Gores GJ. Bid antisense bile acid-induced apoptosis and cholestatic liver injury. J Pharmacol Exp Ther. 2001;299:866
  40. Gumpricht E, Dahl R, Yerushalmi B, Devereaux MW, Sokol RJ. Nitric oxide ameliorates hydrophobic bile acid-induced apoptosis in isolated rat hepatocytes by non-mitochondrial pathways. J Biol Chem. 2002;277:25823
  41. Baron V, Hernandez J, Noyola M, Escalante B, Muriel P. Nitric oxide and inducible nitric oxide synthase expression are downregulated in acute cholestasis in the rat accompanied by liver ischemia. Comp Biochem Physiol C Toxicol Pharmacol. 2000;127:243
  42. Ozturk H, Yagmur Y, Buyukbayram H, Dokucu AI, Gurel A. 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. 2002;34:285
  43. Taylor BS, Geller DA. Molecular regulation of the human inducible nitric oxide synthase (iNOS) gene. Shock. 2000;13:413
  44. Kim PK, Zamora R, Petrosko P, Billiar TR. The regulatory role of nitric oxide in apoptosis. Int Immunopharmacol. 2001;1:1421
  45. Kim YM, de Vera ME, Watkins SC, Billiar TR. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J Biol Chem. 1997;272:1402

PII: S0022-4804(06)00255-1

doi: 10.1016/j.jss.2006.05.015

Journal of Surgical Research
Volume 138, Issue 1 , Pages 15-21 , March 2007