Nitric oxide and portal hypertension: Interface of vasoreactivity and angiogenesis

Journal of Hepatology

Volumn 44, Issue 1, 2006, Pages 209-216

  Langer, Daniel A ^a   Shah, Vijay H ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; INFLIXIMAB; NCX 1000; NITRATE; NITRIC OXIDE; NORFLOXACIN; TERLIPRESSIN; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID DERIVATIVE;

ANGIOGENESIS; BIOLOGY; BLOOD VESSEL REACTIVITY; CARDIOMYOPATHY; CIRCULATION; CLINICAL TRIAL; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HEPATIC ENCEPHALOPATHY; HEPATOPULMONARY SYNDROME; HEPATORENAL SYNDROME; HUMAN; LIVER SINUSOID; MORBIDITY; MORTALITY; PATHOPHYSIOLOGY; PORTAL HYPERTENSION; PRIORITY JOURNAL; REVIEW; SPLANCHNIC BLOOD FLOW; STELLATE CELL; STOMACH DISEASE;

ANIMALS; HUMANS; HYPERTENSION, PORTAL; LIVER; LIVER CIRCULATION; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; VASCULAR RESISTANCE;

EID: 28844507587     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2005.10.004     Document Type: Review

References (88)

1. D.C. Rockey Cell and molecular mechanisms of increased intrahepatic resistance and hemodynamic correlates A.J. Sanyal V.H. Shah Portal hypertension: pathobiology, evaluation, and treatment 2005 Humana Press Totowa, NJ 37 50
2. E. Albanis, R. Safadi, and S.L. Friedman Treatment of hepatic fibrosis: almost there Curr Gastroenterol Rep 5 2003 48 56
3. P.S. Bhathal, and H.J. Grossman Reduction of the increased portal vascular resistance of the isolated perfused cirrhotic rat liver by vasodilators J Hepatol 1 1985 325 337
4. M. Morales-Ruiz, P. Cejudo-Martn, G. Fernandez-Varo, S. Tugues, J. Ros, and P. Angeli Transduction of the liver with activated Akt normalizes portal pressure in cirrhotic rats Gastroenterology 125 2003 522 531
5. J. Bosch, and J.C. Garcia-Pagan Complications of cirrhosis. I. Portal hypertension J Hepatol 32 2000 141 156
6. V. Shah Cellular and molecular basis of portal hypertension Clin Liver Dis 5 2001 629 644
7. R. Wiest, and R.J. Groszmann The paradox of nitric oxide in cirrhosis and portal hypertension: too much, not enough Hepatology 35 2002 478 491
8. L.J. Ignarro Endothelium-derived nitric oxide: actions and properties Fed Am Soc Exp Biol J 3 1989 31 36
9. D.S. Bredt, and S.H. Snyder Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme Proc Natl Acad Sci USA 87 1990 682 685
10. V. Shah, G. Lyford, G. Gores, and G. Farrugia Nitric oxide in gastrointestinal health and disease Gastroenterology 126 2004 903 913
11. D.C. Rockey, and J.J. Chung Reduced nitric oxide production by endothelial cells in cirrhotic rat liver: endothelial dysfunction in portal hypertension Gastroenterology 114 1998 344 351
12. D. Kapoor, and S.K. Sarin Pathophysiology of portal hypertension J Gastroenterol Hepatol 17 Suppl. 2002 S482 S487
13. W.C. Sessa eNOS at a glance J Cell Sci 117 2004 2427 2429
14. D.G. Harrison, and H. Cai Endothelial control of vasomotion and nitric oxide production Cardiol Clin 21 2003 289 302
15. C.J. Lowenstein, and E. Padalko iNOS (NOS2) at a glance J Cell Sci 117 2004 2865 2867
16. I.N. Mungrue, and D.S. Bredt nNOS at a glance: implications for brain and brawn J Cell Sci 117 2004 2627 2629
17. A.A. Dudenhoefer, M.R. Loureiro-Silva, G.W. Cadelina, T. Gupta, and R.J. Groszmann Bioactivation of nitroglycerin and vasomotor response to nitric oxide are impaired in cirrhotic rat livers Hepatology 36 2002 381 385
18. T.K. Gupta, M. Toruner, M.K. Chung, and R.J. Groszmann Endothelial dysfunction and decreased production of nitric oxide in the intrahepatic microcirculation of cirrhotic rats Hepatology 28 1998 926 931
19. V. Shah, M. Toruner, F. Haddad, G. Cadelina, A. Papapetropoulos, and K. Choo Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat Gastroenterology 117 1999 1222 1228
20. H. Yokomori, M. Oka, K. Yoshimura, M. Nomura, G. Wakabayashi, and M. Kitajima Elevated expression of caveolin-1 at protein and mRNA level in human cirrhotic liver: relation with nitric oxide J Gastroenterol 38 2003 854 860
21. H. Hendrickson, S. Chatterjee, S. Cao, M. Morales Ruiz, W.C. Sessa, and V. Shah Influence of caveolin on constitutively activated recombinant eNOS: insights into eNOS dysfunction in BDL rat liver Am J Physiol Gastrointest Liver Physiol 285 2003 G652 G660
22. Perri RE, Langer DA, Chatterjee S, Gibbons SJ, Gadgil J, Cao S, et al. Defects in cGMP-PKG pathway contribute to impaired NO dependent responses in hepatic stellate cells upon activation. Am J Physiol Gastrointest Liver Physiol 2005;10.1152/ajpgi.00297.2005 [Epub ahead of print].
23. P. Failli, F.R. De, A. Caligiuri, A. Gentilini, R.G. Romanelli, and F. Marra Nitrovasodilators inhibit platelet-derived growth factor-induced proliferation and migration of activated human hepatic stellate cells Gastroenterology 119 2000 479 492
24. Y. Iwakiri, J.G. Abraldes, M. Loureiro-Silva, O. Haq, and R.J. Groszmann Vascular Endothelial Growth Factor (VEGF) Up-Regulates Endothelial Nitric Oxide Synthase (eNOS) in the intestinal microcirculatory bed leading to the hyperdynamic circulatory syndrome in mild portal hypertension Gastroenterology 128 2005 A-681
25. Q. Yu, R. Shao, H.S. Qian, S.E. George, and 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
26. M. Van de Casteele, A. Omasta, S. Janssens, T. Roskams, V. Desmet, and F. Nevens In vivo gene transfer of endothelial nitric oxide synthase decreases portal pressure in anaesthetised carbon tetrachloride cirrhotic rats Gut 51 2002 440 445
27. R.J. Groszmann, and G. Garcia-Tsao Endoscopic variceal banding vs. pharmacological therapy for the prevention of recurrent variceal hemorrhage: what makes the difference? Gastroenterology 123 2002 1388 1391
28. C. Merkel Nonselective beta-blockers plus nitrates in portal hypertension: an open question Hepatology 37 2003 1254 1256
29. M. Angelico, and R. Lionetti Long-acting nitrates in portal hypertension: to be or not to be? Dig Liver Dis 33 2001 205 211
30. S. Fiorucci, E. Antonelli, V. Brancaleone, L. Sanpaolo, S. Orlandi, and E. Distrutti NCX-1000, a nitric oxide-releasing derivative of ursodeoxycholic acid, ameliorates portal hypertension and lowers norepinephrine-induced intrahepatic resistance in the isolated and perfused rat liver J Hepatol 39 2003 932 939
31. S. Fiorucci, E. Antonelli, O. Morelli, A. Mencarelli, A. Casini, and T. Mello 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 USA 98 2001 8897 8902
32. L.D. DeLeve, X. Wang, G.C. Kanel, Y. Ito, N.W. Bethea, and M.K. McCuskey Decreased hepatic nitric oxide production contributes to the development of rat sinusoidal obstruction syndrome Hepatology 38 2003 900 908
33. C. Zafra, J.G. Abraldes, J. Turnes, A. Berzigotti, M. Fernandez, and J.C. Garca-Pagan Simvastatin enhances hepatic nitric oxide production and decreases the hepatic vascular tone in patients with cirrhosis Gastroenterology 126 2004 749 755
34. Y. Kureishi, Z. Luo, I. Shiojima, A. Bialik, D. Fulton, and D.J. Lefer The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals Nat Med 6 2000 1004 1010
35. C.C. Sieber, J.C. Lopez-Talavera, and R.J. Groszmann Role of nitric oxide in the in vitro splanchnic vascular hyporeactivity in ascitic cirrhotic rats Gastroenterology 104 1993 1750 1754
36. C.C. Sieber, L.T. Sumanovski, C. Moll-Kaufmann, and G.A. Stalder Hyposensitivity to nerve stimulation in portal hypertensive rats: role of nitric oxide Eur J Clin Invest 27 1997 902 907
37. N.M. Atucha, V. Shah, G. Garcia-Cardena, W.E. Sessa, and R.J. Groszmann Role of endothelium in the abnormal response of mesenteric vessels in rats with portal hypertension and liver cirrhosis Gastroenterology 111 1996 1627 1632
38. L. Jurzik, M. Froh, R.H. Straub, J. Scholmerich, and R. Wiest Up-regulation of nNOS and associated increase in nitrergic vasodilation in superior mesenteric arteries in pre-hepatic portal hypertension J Hepatol 2005
39. R. Moreau, E. Barriere, K.A. Tazi, B. Lardeux, D. Dargere, and W. Urbanowicz Terlipressin inhibits in vivo aortic iNOS expression induced by lipopolysaccharide in rats with biliary cirrhosis Hepatology 36 2002 1070 1078
40. Y. Iwakiri, G. Cadeline, W. Sessa, and R. Groszmann Mice with targeted deletion of eNOS develop hyperdynamic circulation associated with portal hypertension Am J Physiol 283 2002 G1074 G1081
41. N. Theodorakis, Y. Wang, N. Skill, M. Metz, P. Cahill, and E. Redmond The role of nitric oxide synthase isoforms in extrahepatic portal hypertension: studies in gene knock-out mice Gastroenterology 124 2003 1500 1508
42. Y. Iwakiri, J.G. Abraldes, M. Loureiro-Silva, O. Haq, and R.J. Groszmann Vascular Endothelial Growth Factor (VEGF) Up-Regulates Endothelial Nitric Oxide Synthase (eNOS) in the intestinal microcirculatory bed leading to the hyperdynamic circulatory syndrome in mild portal hypertension Gastroenterology 128 2005 A-681
43. I. Fleming, and R. Busse Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase Am J Physiol Regul Integr Comp Physiol 284 2003 R1 R12
44. Y.C. Boo, and H. Jo Flow-dependent regulation of endothelial nitric oxide synthase: role of protein kinases Am J Physiol Cell Physiol 285 2003 C499 C508
45. H. Kawanaka, M.K. Jones, I.L. Szabo, D. Baatar, R. Pai, and K. Tsugawa Activation of eNOS in rat portal hypertensive gastric mucosa is mediated by TNF-alpha via the PI 3-kinase-Akt signaling pathway Hepatology 35 2002 393 402
46. R. Wiest, G. Cadelina, S. Milstien, R.S. McCuskey, G. Garcia-Tsao, and R.J. Groszmann Bacterial translocation up-regulates GTP-cyclohydrolase I in mesenteric vasculature of cirrhotic rats Hepatology 38 2003 1508 1515
47. M. Fernandez, F. Vizzutti, J.C. Garcia-Pagan, J. Rodes, and J. Bosch Anti-VEGF receptor-2 monoclonal antibody prevents portal-systemic collateral vessel formation in portal hypertensive mice Gastroenterology 126 2004 886 894
48. P. Cales, A. Braillon, C. Girod, and D. Lebrec Acute effect of propranolol on splanchnic circulation in normal and portal hypertensive rats J Hepatol 1 1985 349 357
49. D. Pateron, K.A. Tazi, P. Sogni, J. Heller, C. Chagneau, and O. Poirel Role of aortic nitric oxide synthase 3 (eNOS) in the systemic vasodilation of portal hypertension Gastroenterology 119 2000 196 200
50. S. Batkai, Z. Jarai, J.A. Wagner, S.K. Goparaju, K. Varga, and J. Liu Endocannabinoids acting at vascular CB1 receptors mediate the vasodilated state in advanced liver cirrhosis Nat Med 7 2001 827 832
51. J. Ros, J. Claria, J. To-Figueras, A. Planaguma, P. Cejudo-Martin, and G. Fernandez-Varo Endogenous cannabinoids: a new system involved in the homeostasis of arterial pressure in experimental cirrhosis in the rat Gastroenterology 122 2002 85 93
52. B. Rasaratnam, D. Kaye, G. Jennings, F. Dudley, and J. Chin-Dusting The effect of selective intestinal decontamination on the hyperdynamic circulatory state in cirrhosis. A randomized trial Ann Intern Med 139 2003 186 193
53. R.P. Mookerjee, S. Sen, N.A. Davies, S.J. Hodges, R. Williams, and R. Jalan Tumour necrosis factor alpha is an important mediator of portal and systemic haemodynamic derangements in alcoholic hepatitis Gut 52 2003 1182 1187
54. M. Morales-Ruiz, and W. Jimenez Neovascularization, angiogenesis, and vascular remodeling in portal hypertension A.J. Sanyal V.H. Shah Portal hypertension: pathobiology, evaluation, and treatment 2005 Humana Press Totowa, NJ 99 112
55. C.C. Sieber, L.T. Sumanovski, M. Stumm, M. van der Kooij, and E. Battegay In vivo angiogenesis in normal and portal hypertensive rats: role of basic fibroblast growth factor and nitric oxide J Hepatol 34 2001 644 650
56. L.T. Sumanovski, E. Battegay, M. Stumm, M. van der Kooij, and C.C. Sieber Increased angiogenesis in portal hypertensive rats: role of nitric oxide Hepatology 29 1999 1044 1049
57. A. Aicher, C. Heeschen, C. Mildner-Rihm, C. Urbich, C. Ihling, and K. Technau-Ihling Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells Nat Med 9 2003 1370 1376
58. D.G. Duda, D. Fukumura, and R.K. Jain Role of eNOS in neovascularization: NO for endothelial progenitor cells Trends Mol Med 10 2004 143 145
59. F.Y. Lee, L.A. Colombato, A. Albillos, and R.J. Groszmann Administration of N omega-nitro-L-arginine ameliorates portal-systemic shunting in portal-hypertensive rats Gastroenterology 105 1993 1464 1470
60. P. Mosca, F.Y. Lee, A.J. Kaumann, and R.J. Groszmann Pharmacology of portal-systemic collaterals in portal hypertensive rats: role of endothelium Am J Physiol 263 1992 G544 G550
61. C.C. Chan, F.Y. Lee, S.S. Wang, F.Y. Chang, H.C. Lin, and C.J. Chu Effects of vasopressin on portal-systemic collaterals in portal hypertensive rats: role of nitric oxide and prostaglandin Hepatology 30 1999 630 635
62. P. Cales, A. Braillon, M.I. Jiron, and D. Lebrec Superior portosystemic collateral circulation estimated by azygos blood flow in patients with cirrhosis. Lack of correlation with oesophageal varices and gastrointestinal bleeding. Effect of propranolol J Hepatol 1 1985 37 46
63. G. Fernandez-Varo, J. Ros, M. Morales-Ruiz, P. Cejudo-Martin, V. Arroyo, and M. Sole Nitric oxide synthase 3-dependent vascular remodeling and circulatory dysfunction in cirrhosis Am J Pathol 162 2003 1985 1993
64. R.D. Rudic, E.G. Shesely, N. Maeda, O. Smithies, S.S. Segal, and W.C. Sessa Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling J Clin Invest 101 1998 731 736
65. J. Lee, N. Decker, S. Chatterjee, J. Yao, S. Friedman, and V. Shah Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts Am J Pathol 166 2005 1861 1870
66. P. Carmeliet Angiogenesis in health and disease Nat Med 9 2003 653 660
67. R.K. Jain Molecular regulation of vessel maturation Nat Med 9 2003 685 693
68. C. Urbich, and S. Dimmeler Endothelial progenitor cells: characterization and role in vascular biology Circ Res 95 2004 343 353
69. H. Fujii, T. Hirose, S. Oe, K. Yasuchika, H. Azuma, and T. Fujikawa Contribution of bone marrow cells to liver regeneration after partial hepatectomy in mice J Hepatol 36 2002 653 659
70. M. Abid, J. Tsai, K. Spokes, S. Deshpande, K. Irani, and W. Aird Vascular endothelial growth factor induces manganese-superoxide dismutase expression in endothelial cells by a Rac1-regulated NADPH oxidase-dependent mechanism Fed Am Soc Exp Biol J 15 2001 2548 2550
71. V.L. Rao, R.M. Audet, and R.F. Butterworth Increased neuronal nitric oxide synthase expression in brain following portacaval anastomosis Brain Res 765 1997 169 172
72. V.L. Rao, and R.F. Butterworth Neuronal nitric oxide synthase and Hepatic Encephalopathy Metab Brain Dis 13 1998 175 189
73. V.L. Rao Nitric oxide in hepatic encephalopathy and hyperammonemia Neurochem Int 41 2002 161 170
74. R. Rodrigo, C. Montoliu, N. Chatauret, R. Butterworth, S. Behrends, and J.A. Del Olmo Alterations in soluble guanylate cyclase content and modulation by nitric oxide in liver disease Neurochem Int 45 2004 947 953
75. I. Suarez, G. Bodega, M. Rubio, V. Felipo, and B. Fernandez Neuronal and inducible nitric oxide synthase expression in the rat cerebellum following portacaval anastomosis Brain Res 1047 2005 205 213
76. M.B. Fallon, and G.A. Abrams Pulmonary dysfunction in chronic liver disease Hepatology 32 2000 859 865
77. M.B. Fallon, G.A. Abrams, B. Luo, Z. Hou, J. Dai, and D.D. Ku The role of endothelial nitric oxide synthase in the pathogenesis of a rat model of hepatopulmonary syndrome Gastroenterology 113 1997 606 614
78. P. Schenk, C. Madl, S. Rezaie-Majd, S. Lehr, and C. Muller Methylene blue improves the hepatopulmonary syndrome Ann Intern Med 133 2000 701 706
79. B. Sztrymf, A. Rabiller, H. Nunes, L. Savale, D. Lebrec, and A. Le Pape Prevention of hepatopulmonary syndrome and hyperdynamic state by pentoxifylline in cirrhotic rats Eur Respir J 23 2004 752 758
80. M.M. Hoeper, M.J. Krowka, and C.P. Strassburg Portopulmonary hypertension and hepatopulmonary syndrome Lancet 363 2004 1461 1468
81. P. Kanthapillai, T. Lasserson, and E. Walters Sildenafil for pulmonary hypertension Cochrane Database Syst Rev 2004 [CD003562]
82. M.B. Fallon Mechanisms of cardiopulmonary hemodynamics and dysfunction in portal hypertension A.J. Sanyal V.H. Shah Portal hypertension: pathobiology, evaluation, and treatment 2005 Humana Press Totowa, NJ 113 125
83. L. Ruiz-del-Arbol, J. Urman, J. Fernandez, M. Gonzalez, M. Navasa, and A. Monescillo Systemic, renal, and hepatic hemodynamic derangement in cirrhotic patients with spontaneous bacterial peritonitis Hepatology 38 2003 1210 1218
84. R.W. Schrier, V. Arroyo, M. Bernardi, M. Epstein, J.H. Henriksen, and J. Rodes Peripheral arterial vasodilation hypothesis: a proposal for the initiation of renal sodium and water retention in cirrhosis Hepatology 8 1988 1151 1157
85. S.S. Lee Cardiac dysfunction in spontaneous bacterial peritonitis: a manifestation of cirrhotic cardiomyopathy? Hepatology 38 2003 1089 1091
86. H. Liu, Z. Ma, and S.S. Lee Contribution of nitric oxide to the pathogenesis of cirrhotic cardiomyopathy in bile duct-ligated rats Gastroenterology 118 2000 937 944
87. M. Ohta, A.S. Tarnawski, R. Itani, R. Pai, M. Tomikawa, and K. Sugimachi Tumor necrosis factor alpha regulates nitric oxide synthase expression in portal hypertensive gastric mucosa of rats Hepatology 27 1998 906 913
88. P. Gines, M. Guevara, and F. Perez-Villa Management of hepatorenal syndrome: another piece of the puzzle Hepatology 40 2004 16 18