Differential expression and localization of nitric oxide synthases in cirrhotic livers of bile duct-ligated rats

Nitric Oxide - Biology and Chemistry

Volumn 7, Issue 2, 2002, Pages 91-102

  Wei, Chang Li ^a   Khoo, Hoon Eng ^a   Lee, Kang Hoe ^a   Hon, Wei Min ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Liver cirrhosis; Nitric oxide; Nitric oxide synthase; Protein expression; Quantitative RT PCR; Regulation

Indexed keywords

CITRULLINE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; BLOOD VESSEL; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIVER CELL; LIVER CIRRHOSIS; LIVER SINUSOID; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BILE DUCTS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOHISTOCHEMISTRY; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; MALE; NITRIC OXIDE SYNTHASE; POLYMERASE CHAIN REACTION; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 0036749813     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1089-8603(02)00103-9     Document Type: Article

References (63)

1. C.J. Lowenstein, J.L. Dinerman, S.H. Snyder, Nitric oxide: a physiologic messenger, Ann. Intern. Med. 120 (1994) 227-237.
2. S. Moncada, R.M. Palmer, E.A. Higgs, Nitric oxide: physiology, pathophysiology, pharmacology, Pharmacol. Rev. 43 (1991) 109-142.
3. D.S. Bredt, P.M. Hwang, C.E. Glatt, C. Lowenstein, R.R. Reed, S.H. Snyder, Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase, Nature 351 (1991) 714-718.
4. S. Lamas, P.A. Marsden, G.K. Li, P. Tempst, T. Michel, Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform, Proc. Natl. Acad. Sci. USA 89 (1992) 6348-6352.
5. C.J. Lowenstein, C.S. Glatt, D.S. Bredt, S.H. Snyder, Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme, Proc. Natl. Acad. Sci. USA 89 (1992) 6711-6715.
6. G. Garcia-Tsao, Portal hypertension, Curr. Opin. Gastroenterol. 16 (2000) 282-289.
7. J. Bosch, J.C. Garcia-Pagan, Pathophysiology of portal hypertension and its complicatons, in: J. Bircher, et al. (Eds.), Oxford Textbook of Clinical Hepatoloy, Oxford University Press, New York, 1999, pp. 653-659.
8. J. Bosch, M. Navasa, J.C. Garcia-Pagan, A.M. DeLacy, J. Rodes, Portal hypertension, Med. Clin. North Am. 73 (1989) 931-953.
9. P. Vallance, S. Moncada, Hyperdynamic circulation in cirrhosis: a role for nitric oxide?, Lancet 337 (1991) 776-778.
10. C. Guarner, G. Soriano, A. Tomas, O. Bulbena, M.T. Novella, J. Balanzo, F. Vilardell, M. Mourelle, S. Moncada, Increased serum nitrite and nitrate levels in patients with cirrhosis: relationship to endotoxemia, Hepatology 18 (1993) 1139-1143.
11. N. Hori, R. Wiest, R.J. Groszmann, Enhanced release of nitric oxide in response to changes in flow and shear stress in the superior mesenteric arteries of portal hypertensive rats, Hepatology 28 (1998) 1467-1473.
12. M. Niederberger, P.Y. Martin, P. Gines, K. Morris, P. Tsai, D.L. Xu, I. McMurtry, R.W. Schrier, Normalization of nitric oxide production corrects arterial vasodilation and hyperdynamic circulation in cirrhotic rats, Gastroenterology 109 (1995) 1624-1630.
13. P.A. Cahill, C. Foster, E.M. Redmond, C. Gingalewski, Y. Wu, J.V. Sitzmann, Enhanced nitric oxide synthase activity in portal hypertensive rabbits, Hepatology 22 (1995) 598-606.
14. P.A. Cahill, E.M. Redmond, R. Hodges, S. Zhang, J.V. Sitzmann, Increased endothelial nitric oxide synthase activity in the hyperemic vessels of portal hypertensive rats, J. Hepatol. 25 (1996) 370-378.
15. P.Y. Martin, D.L. Xu, M. Niederberger, A. Weigert, P. Tsai, J. St. John, P. Gines, R.W. Schrier, Upregulation of endothelial constitutive NOS: a major role in the increased NO production in cirrhotic rats, Am. J. Physiol. 270 (1996) F494-F499.
16. M. Niederberger, P. Gines, P. Tsai, P.Y. Martin, K. Morris, A. Weigert, I. McMurtry, R.W. Schrier, Increased aortic cyclic guanosine monophosphate concentration in experimental cirrhosis in rats: evidence for a role of nitric oxide in the pathogenesis of arterial vasodilation in cirrhosis, Hepatology 21 (1995) 1625-1631.
17. J. Ros, W. Jimenez, S. Lamas, J. Claria, V. Arroyo, F. Rivera, J. Rodes, Nitric oxide production in arterial vessels of cirrhotic rats, Hepatology 21 (1995) 554-560.
18. A.C. Gadano, P. Sogni, S. Yang, S. Cailmail, R. Moreau, P. Nepveux, D. Couturier, D. Lebrec, Endothelial calcium- calmodulin dependent nitric oxide synthase in the in vitro vascular hyporeactivity of portal hypertensive rats, J. Hepatol. 26 (1997) 678-686.
19. C.C. Sieber, J.C. Lopez-Talavera, R.J. Groszmann, Role of nitric oxide in the in vitro splanchnic vascular hyporeactivity in ascitic cirrhotic rats, Gastroenterology 104 (1993) 1750-1754.
20. M. Morales-Ruiz, W. Jimenez, D. Perez-Sala, J. Ros, A. Leivas, S. Lamas, F. Rivera, V. Arroyo, Increased nitric oxide synthase expression in arterial vessels of cirrhotic rats with ascites, Hepatology 24 (1996) 1481-1486.
21. M. Niederberger, P. Gines, P.Y. Martin, P. Tsai, K. Morris, I. McMurtry, R.W. Schrier, Comparison of vascular nitric oxide production and systemic hemodynamics in cirrhosis versus prehepatic portal hypertension in rats, Hepatology 24 (1996) 947-951.
22. R. Wiest, R.J. Groszmann, Nitric oxide and portal hypertension: its role in the regulation of intrahepatic and splanchnic vascular resistance, Semin. Liver Dis. 19 (1999) 411-426.
23. R. Wiest, S. Das, G. Cadelina, G. Garcia-Tsao, S. Milstien, R.J. Groszmann, Bacterial translocation in cirrhotic rats stimulates eNOS-derived NO production and impairs mesenteric vascular contractility, J. Clin. Invest. 104 (1999) 1223-1233.
24. L. Xu, E.P. Carter, M. Ohara, P.Y. Martin, B. Rogachev, K. Morris, M. Cadnapaphornchai, M. Knotek, R.W. Schrier, Neuronal nitric oxide synthase and systemic vasodilation in rats with cirrhosis, Am. J. Physiol. Renal Physiol. 279 (2000) F1110-F1115.
25. A.L. Gerbes, M. Bilzer, V. Gulberg, Intrahepatic modulation of portal pressure and its role in portal hypertension. Role of endothelins, Digestion 59 (1998) 410-412.
26. M.K. Mittal, T.K. Gupta, F.Y. Lee, C.C. Sieber, R.J. Groszmann, Nitric oxide modulates hepatic vascular tone in normal rat liver, Am. J. Physiol. 267 (1994) G416-G422.
27. T.K. Gupta, M. Toruner, M.K. Chung, R.J. Groszmann, Endothelial dysfunction and decreased production of nitric oxide in the intrahepatic microcirculation of cirrhotic rats, Hepatology 28 (1998) 926-931.
28. D.C. Rockey, J.J. Chung, Reduced nitric oxide production by endothelial cells in cirrhotic rat liver: endothelial dysfunction in portal hypertension, Gastroenterology 114 (1998) 344-351.
29. J. Kountouras, B.H. Billing, P.J. Scheuer, Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat, Br. J. Exp. Pathol. 65 (1984) 305-311.
30. S.S. Lee, K.A. Sharkey, Capsaicin treatment blocks development of hyperkinetic circulation in portal hypertensive and cirrhotic rats, Am. J. Physiol. 264 (1993) G868-G873.
31. J.F. Brown, B.L. Tepperman, P.J. Hanson, B.J. Whittle, S. Moncada, Differential distribution of nitric oxide synthase between cell fractions isolated from the rat gastric mucosa, Biochem. Biophys. Res. Commun. 184 (1992) 680-685.
32. M. Salter, R.G. Knowles, S. Moncada, Widespread tissue distribution, species distribution and changes in activity of Ca(2+)-dependent and Ca(2+)-independent nitric oxide synthases, FEBS Lett. 291 (1991) 145-149.
33. F.J. Esteban, J.A. Pedrosa, A. Jimenez, A.P. Fernandez, M.L. Bentura, R. Martinez-Murillo, J. Rodrigo, M.A. Peinado, Distribution of neuronal nitric oxide synthase in the rat liver, Neurosci. Lett. 226 (1997) 99-102.
34. V. Shah, F.G. Haddad, G. Garcia-Cardena, J.A. Frangos, A. Mennone, R.J. Groszmann, W.C. Sessa, Liver sinusoidal endothelial cells are responsible for nitric oxide modulation of resistance in the hepatic sinusoids, J. Clin. Invest. 100 (1997) 2923-2930.
35. W.C. Sessa, The nitric oxide synthase family of proteins, J. Vasc. Res. 31 (1994) 131-143.
36. A.l. Sarela, F.M. Mihaimeed, J.J. Batten, B.R. Davidson, R.T. Mathie, Hepatic and splanchnic nitric oxide activity in patients with cirrhosis, Gut 44 (1999) 749-753.
37. M.A. Awolesi, W.C. Sessa, B.E. Sumpio, Cyclic strain upregulates nitric oxide synthase in cultured bovine aortic endothelial cells, J. Clin. Invest. 96 (1995) 1449-1454.
38. N. Inoue, R.C. Venema, H.S. Sayegh, Y. Ohara, T.J. Murphy, D.G. Harrison, Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1, Arterioscler. Thromb. Vasc. Biol. 15 (1995) 1255-1261.
39. S.K. Kostyk, S. Kourembanas, E.L. Wheeler, D. Medeiros, L.P. McQuillan, P.A. D'Amore, S.J. Braunhut, Basic fibroblast growth factor increases nitric oxide synthase production in bovine endothelial cells, Am. J. Physiol. 269 (1995) H1583-H1589.
40. M. Uematsu, Y. Ohara, J.P. Navas, K. Nishida, T.J. Murphy, R.W. Alexander, R.M. Nerem, D.G. Harrison, Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress, Am. J. Physiol. 269 (1995) C1371-C1378.
41. C.P. Weiner, I. Lizasoain, S.A. Baylis, R.G. Knowles, I.G. Charles, S. Moncada, Induction of calcium-dependent nitric oxide synthases by sex hormones, Proc. Natl. Acad. Sci. USA 91 (1994) 5212-5216.
42. D.J. Stuehr, Mammalian nitric oxide synthases, Biochim. Biophys. Acta 1411 (1999) 217-230.
43. G. Garcia-Cardena, P. Oh, J. Liu, J.E. Schnitzer, W.C. Sessa, Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling, Proc. Natl. Acad. Sci. USA 93 (1996) 6448-6453.
44. G. Garcia-Cardena, P. Martasek, B.S. Masters, P.M. Skidd, J. Couet, S. Li, M.P. Lisanti, W.C. Sessa, Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo, J. Biol. Chem. 272 (1997) 25437-25440.
45. H. Ju, R. Zou, V.J. Venema, R.C. Venema, Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity, J. Biol. Chem. 272 (1997) 18522-18525.
46. V. Shah, M. Toruner, F. Haddad, G. Cadelina, A. Papapetropoulos, K. Choo, W.C. Sessa, R.J. Groszmann, Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat, Gastroenterology 117 (1999) 1222-1228.
47. Y. Wang, D.C. Newton, P.A. Marsden, Neuronal NOS: gene structure, mRNA diversity, functional relevance, Crit. Rev. Neurobiol. 13 (1999) 21-43.
48. Q. Yu, R. Shao, H.S. Qian, S.E. George, D.C. Rockey, Gene transfer of the neuronal NO synthase isoform to cirrhotic rat liver ameliorates portal hypertension, J. Clin. Invest. 105 (2000) 741-748.
49. J. Li, T.R. Billiar, Nitric oxide. IV. Determinants of nitric oxide protection and toxicity in liver, Am. J. Physiol. 276 (1999) G1069-G1073.
50. M.G. Clemens, Nitric oxide in liver injury, Hepatology 30 (1999) 1-5.
51. V. Shah, G. Garcia-Cardena, W.C. Sessa, R.J. Groszmann, The hepatic circulation in health and disease: report of a single-topic symposium, Hepatology 27 (1998) 279-288.
52. M. Mizumoto, S. Arii, M. Furutani, T. Nakamura, S. Ishigami, K. Monden, S. Ishiguro, S. Fujita, M. Imamura, NO as an indicator of portal hemodynamics and the role of iNOS in increased NO production in CCl4-induced liver cirrhosis, J. Surg. Res. 70 (1997) 124-133.
53. D.C. Rockey, J.J. Chung, Regulation of inducible nitric oxide synthase and nitric oxide during hepatic injury and fibrogenesis, Am. J. Physiol. 273 (1997) G124-G130.
54. M.M. Arriero, A. Lopez-Farre, O. Fryeiro, J.A. Rodriguez-Feo, S. Velasco, M. Garcia-Duran, J. Fortes, J.C. DeLa Pinta, L.E. Munoz, A. Celdran, Expression of inducible nitric oxide synthase in the liver of bile duct- ligated Wistar rats with modulation by lymphomononuclear cells, Surgery 129 (2001) 255-266.
55. P. Mayoral, M. Criado, F. Hidalgo, O. Flores, M.A. Arevalo, N. Eleno, A. Sanchez-Rodriguez, J.M. Lopez-Novoa, A. Esteller, Effects of chronic nitric oxide activation or inhibition on early hepatic fibrosis in rats with bile duct ligation, Clin. Sci. (Colch.) 96 (1999) 297-305.
56. W. Coers, W. Timens, C. Kempinga, P.A. Klok, H. Moshage, Specificity of antibodies to nitric oxide synthase isoforms in human, guinea pig, rat, mouse tissues, J. Histochem. Cytochem. 46 (1998) 1385-1392.
57. I.R. Wanless, J. Belgiorno, P.M. Huet, Hepatic sinusoidal fibrosis induced by cholesterol and stilbestrol in the rabbit. 1. Morphology and inhibition of fibrogenesis by dipyridamole, Hepatology 24 (1996) 855-864.
58. S.M. Morris, T.R. Billiar, New insights into the regulation of inducible nitric oxide synthesis, Am. J. Physiol. 266 (1994) E829-E839.
59. C. Nathan, Q.W. Xie, Regulation of biosynthesis of nitric oxide, J. Biol. Chem. 269 (1994) 13725-13728.
60. T. Michel, O. Feron, Nitric oxide synthases: which, where, how, why?, J. Clin. Invest. 100 (1997) 2146-2152.
61. F.Y. Lee, S.S. Wang, M.C. Yang, Y.T. Tsai, S.L. Wu, R.H. Lu, C.Y. Chan, S.D. Lee, Role of endotoxaemia in hyperdynamic circulation in rats with extrahepatic or intrahepatic portal hypertension, J. Gastroenterol. Hepatol. 11 (1996) 152-158.
62. R.S. Lin, F.Y. Lee, S.D. Lee, Y.T. Tsai, H.C. Lin, R.H. Lu, W.C. Hsu, C.C. Huang, S.S. Wang, K.J. Lo, Endotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, hyperdynamic circulation, J. Hepatol. 22 (1995) 165-172.
63. A.B. Lumsden, J.M. Henderson, M.H. Kutner, Endotoxin levels measured by a chromogenic assay in portal, hepatic and peripheral venous blood in patients with cirrhosis, Hepatology 8 (1988) 232-236.