Liver sinusoidal endothelial cells (LSECs) function and NAFLD; NO-based therapy targeted to the liver

Pharmacological Reports

Volumn 67, Issue 4, 2015, Pages 689-694

  Maslak, Edyta ^a   Gregorius, Aleksandra ^a   Chlopicki, Stefan ^a,b  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Liver cells crosstalk; Liver sinusoidal endothelial cells; Liver selective therapy; NAFLD

Indexed keywords

BERAPROST; BOSENTAN; NITRIC OXIDE; METFORMIN; NITRIC OXIDE DONOR;

CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; LIVER CELL; LIVER SINUSOID; LIVER SINUSOIDAL ENDOTHELIAL CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHENOTYPE; REVIEW; STELLATE CELL; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; LIVER; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; DRUG DELIVERY SYSTEMS; ENDOTHELIAL CELLS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; LIVER; METFORMIN; NITRIC OXIDE; NITRIC OXIDE DONORS; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84940459551     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/j.pharep.2015.04.010     Document Type: Review

References (77)

1. S. McPherson, T. Hardy, E. Henderson, A.D. Burt, C.P. Day, and Q.M. Anstee Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis & clinical management J Hepatol 62 2014 1148 1155
2. S. Yatsuji, E. Hashimoto, M. Tobari, M. Taniai, K. Tokushige, and K. Shiratori Clinical features and outcomes of cirrhosis due to non-alcoholic steatohepatitis compared with cirrhosis caused by chronic hepatitis C J Gastroenterol Hepatol 24 2009 248 254
3. G. Bedogni, L. Miglioli, F. Masutti, A. Castiglione, L.S. Crocè, C. Tiribelli, and et al. Incidence and natural course of fatty liver in the general population: the dionysos study Hepatology 46 2007 1387 1391
4. R. Haring, H. Wallaschofski, M. Nauck, M. Dörr, S.E. Baumeister, and H. Völzke Ultrasonographic hepatic steatosis increases prediction of mortality risk from elevated serum gamma-glutamyl transpeptidase levels Hepatology 50 2009 1403 1411
5. L. Caballeria, G. Pera, M.A. Auladell, P. Toran, L. Munoz, D. Miranda, and et al. Prevalence and factors associated with the presence of nonalcoholic fatty liver disease in an adult population in Spain Eur J Gastroenterol Hepatol 22 2010 24 32
6. J. Yan, W. Xie, W.-N. Ou, H. Zhao, and J. Cheng 1281 epidemiological survey of prevalence of fatty liver and its risk factors in permanent residents of Beijing J Hepatol 56 2012 S506
7. A. Imhof, W. Kratzer, B. Boehm, K. Meitinger, G. Trischler, G. Steinbach, and et al. Prevalence of non-alcoholic fatty liver and characteristics in overweight adolescents in the general population Eur J Epidemiol 22 2007 889 897
8. M. Pasarín, J.G. Abraldes, A. Rodríguez-Vilarrupla, V. La Mura, J.C. García-Pagán, and J. Bosch Insulin resistance and liver microcirculation in a rat model of early NAFLD J Hepatol 55 2011 1095 1102
9. Y. Sumida, E. Niki, Y. Naito, and T. Yoshikawa Involvement of free radicals and oxidative stress in NAFLD/NASH Free Radic Res 47 2013 869 880
10. H. Malhi, and G.J. Gores Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease Semin Liver Dis 28 2008 360 369
11. D. Compare, P. Coccoli, A. Rocco, O.M. Nardone, S. De Maria, M. Cartenì, and et al. Gut-liver axis: the impact of gut microbiota on non alcoholic fatty liver disease Nutr Metab Cardiovasc Dis 22 2012 471 476
12. S.K. Mantena, D.P. Vaughn, K.K. Andringa, H.B. Eccleston, A.L. King, G.A. Abrams, and et al. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo Biochem J 417 2009 183 193
13. S. Francque, W. Laleman, L. Verbeke, C. Van Steenkiste, C. Casteleyn, W. Kwanten, and et al. Increased intrahepatic resistance in severe steatosis: endothelial dysfunction, vasoconstrictor overproduction and altered microvascular architecture Lab Investig 92 2012 1428 1439
14. E.R. Regan, and W.C. Aird Dynamical systems approach to endothelial heterogeneity Circ Res 111 2012 110 130
15. E. Wisse An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids J Ultrastruct Res 31 1970 125 150
16. E. Wisse An ultrastructural characterization of the endothelial cell in the rat liver sinusoid under normal and various experimental conditions, as a contribution to the distinction between endothelial and Kupffer cells J Ultrastruct Res 38 1972 528 562
17. D. Svistounov, A. Warren, G.P. McNerney, D.M. Owen, D. Zencak, S.N. Zykova, and et al. The Relationship between fenestrations, sieve plates and rafts in liver sinusoidal endothelial cells PLoS ONE 7 2012 e46134
18. D.G. Le Couteur, R. Fraser, V.C. Cogger, and A.J. McLean Hepatic pseudocapillarisation and atherosclerosis in ageing Lancet 359 2002 1612 1615
19. R. Fraser, A.G. Bosanquet, and W.A. Day Filtration of chylomicrons by the liver may influence cholesterol metabolism and atherosclerosis Atherosclerosis 29 1978 113 123
20. V.C. Cogger, S.N. Hilmer, D. Sullivan, M. Muller, R. Fraser, and D.G. Le Couteur Hyperlipidemia and surfactants: the liver sieve is a link Atherosclerosis 189 2006 273 281
21. G. Xie, X. Wang, L. Wang, L. Wang, R.D. Atkinson, G.C. Kanel, and et al. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats Gastroenterology 142 2012 918 927.e6
22. L.P. Ganesan, S. Mohanty, J. Kim, K.R. Clark, J.M. Robinson, and C.L. Anderson Rapid and efficient clearance of blood-borne virus by liver sinusoidal endothelium PLoS Pathog 7 2011 e1002281
23. J. Simon-Santamaria, C.H. Rinaldo, P. Kardas, R. Li, I. Malovic, K. Elvevold, and et al. Efficient uptake of blood-borne BK and JC polyomavirus-like particles in endothelial cells of liver sinusoids and renal vasa recta PLOS ONE 9 2014 e111762
24. K.K. Sørensen, P. McCourt, T. Berg, C. Crossley, D. Le Couteur, K. Wake, and et al. The scavenger endothelial cell: a new player in homeostasis and immunity Am J Physiol Regul Integr Comp Physiol 303 2012 R1217 R1230
25. T. Seternes, K. Sørensen, and B. Smedsrød Scavenger endothelial cells of vertebrates: a nonperipheral leukocyte system for high-capacity elimination of waste macromolecules Proc Natl Acad Sci U S A 99 2002 7594 7597
26. K. Elvevold, B. Smedsrød, and I. Martinez The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity Am J Physiol Gastrointest Liver Physiol 294 2008 G391 G400
27. L. Schild, F. Dombrowski, U. Lendeckel, C. Schulz, A. Gardemann, and G. Keilhoff Impairment of endothelial nitric oxide synthase causes abnormal fat and glycogen deposition in liver Biochim Biophys Acta 1782 2008 180 187
28. L.D. DeLeve, X. Wang, and Y. Guo Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence Hepatology 48 2008 920 930
29. 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
30. H. Yokomori, K. Yoshimura, S. Ohshima, T. Nagai, K. Fujimaki, M. Nomura, and et al. The endothelin-1 receptor-mediated pathway is not involved in the endothelin-1-induced defenestration of liver sinusoidal endothelial cells Liver Int 26 2006 1268 1276
31. M.S. Shafiei, S. Lui, and D.C. Rockey Integrin-linked kinase regulates endothelial cell nitric oxide synthase expression in hepatic sinusoidal endothelial cells Liver Int 35 2014 1213 1221
32. M. Suematsu, and Y. Ishimura The heme oxygenase-carbon monoxide system: a regulator of hepatobiliary function Hepatology 31 2000 3 6
33. Y. Iwakiri Endothelial dysfunction in the regulation of cirrhosis and portal hypertension Liver Int 32 2012 199 213
34. R.J. Gryglewski Prostaglandins, platelets, and atherosclerosis CRC Crit Rev Biochem 7 1980 291 338
35. A.A. Nanji, S. Khwaja, and S.M. Sadrzadeh Decreased prostacyclin production by liver non-parenchymal cells precedes liver injury in experimental alcoholic liver disease Life Sci 54 1994 455 461
36. Y. Iwakiri, and R.J. Groszmann Vascular endothelial dysfunction in cirrhosis J Hepatol 46 2007 927 934
37. Y. Iwakiri, and R.J. Groszmann The hyperdynamic circulation of chronic liver diseases: from the patient to the molecule Hepatology 43 2006 121 131
38. Y. Yokoyama, H. Xu, N. Kresge, S. Keller, A.H. Sarmadi, R. Baveja, and et al. Role of thromboxane A2 in early BDL-induced portal hypertension Am J Physiol Gastrointest Liver Physiol 284 2003 G453 G460
39. M. Graupera, S. March, P. Engel, J. Rodés, J. Bosch, and J.-C. García-Pagán Sinusoidal endothelial COX-1-derived prostanoids modulate the hepatic vascular tone of cirrhotic rat livers Am J Physiol Gastrointest Liver Physiol 288 2005 G763 G770
40. D. Rockey The cellular pathogenesis of portal hypertension: stellate cell contractility, endothelin, and nitric oxide Hepatology 25 1997 2 5
41. S. Yeligar, H. Tsukamoto, and V.K. Kalra Ethanol-induced expression of ET-1 and ET-BR in liver sinusoidal endothelial cells and human endothelial cells involves hypoxia-inducible factor-1alpha and microrNA-199 J Immunol 183 2009 5232 5243
42. S. Liu, R.T. Premont, and D.C. Rockey Endothelial nitric-oxide synthase (eNOS) is activated through G-protein-coupled receptor kinase-interacting protein 1 (GIT1) tyrosine phosphorylation and Src protein J Biol Chem 289 2014 18163 18174
43. W. Kwok, S.H. Lee, C. Culberson, K. Korneszczuk, and M.G. Clemens Caveolin-1 mediates endotoxin inhibition of endothelin-1-induced endothelial nitric oxide synthase activity in liver sinusoidal endothelial cells Am J Physiol Gastrointest Liver Physiol 297 2009 G930 G939
44. J. Gracia-Sancho, B. Laviña, A. Rodríguez-Vilarrupla, H. García-Calderó, J. Bosch, and J.C. García-Pagán Enhanced vasoconstrictor prostanoid production by sinusoidal endothelial cells increases portal perfusion pressure in cirrhotic rat livers J Hepatol 47 2007 220 227
45. R. Fraser, B.R. Dobbs, and G.W. Rogers Lipoproteins and the liver sieve: the role of the fenestrated sinusoidal endothelium in lipoprotein metabolism, atherosclerosis, and cirrhosis Hepatology 21 1995 863 874
46. S.A. Clark, H.B. Angus, H.B. Cook, P.M. George, R.B. Oxner, and R. Fraser Defenestration of hepatic sinusoids as a cause of hyperlipoproteinaemia in alcoholics Lancet 2 1988 1225 1227
47. L. Herrnberger, R. Hennig, W. Kremer, C. Hellerbrand, A. Goepferich, H.R. Kalbitzer, and et al. Formation of fenestrae in murine liver sinusoids depends on plasmalemma vesicle-associated protein and is required for lipoprotein passage PLOS ONE 9 2014 e115005
48. K. Enomoto, Y. Nishikawa, Y. Omori, T. Tokairin, M. Yoshida, N. Ohi, and et al. Cell biology and pathology of liver sinusoidal endothelial cells Med Electron Microsc 37 2004 208 215
49. R. Li, A. Oteiza, K.K. Sørensen, P. McCourt, R. Olsen, B. Smedsrød, and et al. Role of liver sinusoidal endothelial cells and stabilins in elimination of oxidized low-density lipoproteins Am J Physiol Gastrointest Liver Physiol 300 2011 G71 G81
50. V. Bieghs, S.M.A. Walenbergh, T. Hendrikx, P.J. van Gorp, F. Verheyen, S.W. Olde Damink, and et al. Trapping of oxidized LDL in lysosomes of Kupffer cells is a trigger for hepatic inflammation Liver Int 33 2013 1056 1061
51. L. Venkatraman, and L. Tucker-Kellogg The CD47-binding peptide of thrombospondin-1 induces defenestration of liver sinusoidal endothelial cells Liver Int 33 2013 1386 1397
52. E. Rosado, A. Rodríguez-Vilarrupla, J. Gracia-Sancho, M. Monclús, J. Bosch, and J.C. García-Pagán Interaction between NO and COX pathways modulating hepatic endothelial cells from control and cirrhotic rats J Cell Mol Med 16 2012 2461 2470
53. J. Funyu, S. Mochida, M. Inao, A. Matsui, and K. Fujiwara VEGF can act as vascular permeability factor in the hepatic sinusoids through upregulation of porosity of endothelial cells Biochem Biophys Res Commun 280 2001 481 485
54. B.-S. Ding, D.J. Nolan, J.M. Butler, D. James, A.O. Babazadeh, Z. Rosenwaks, and et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration Nature 468 2010 310 315
55. E.R. García-Trevijano, M.L. Martínez-Chantar, M.U. Latasa, J.M. Mato, and M.A. Avila NO sensitizes rat hepatocytes to proliferation by modifying S-adenosylmethionine levels Gastroenterology 122 2002 1355 1363
56. N.A. Hutchins, C.-S. Chung, J.N. Borgerding, C.A. Ayala, and A. Ayala Kupffer cells protect liver sinusoidal endothelial cells from Fas-dependent apoptosis in sepsis by down-regulating gp130 Am J Pathol 182 2013 742 754
57. S. Tateya, N.O. Rizzo, P. Handa, A.M. Cheng, V. Morgan-Stevenson, G. Daum, and et al. Endothelial NO/cGMP/VASP signaling attenuates Kupffer cell activation and hepatic insulin resistance induced by high-fat feeding Diabetes 60 2011 2792 2801
58. O. Tirosh, E. Ilan, N. Budick-Harmelin, G. Ramadori, and Z. Madar Downregulation of eNOS in a nutritional model of fatty liver E SPEN Eur E J Clin Nutr Metab 4 2009 e101 e104
59. H. Duplain, R. Burcelin, C. Sartori, S. Cook, M. Egli, M. Lepori, and et al. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase Circulation 104 2001 342 345
60. J.E. Saavedra, T.R. Billiar, D.L. Williams, Y. 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-r-induced apoptosis and toxicity in the liver J Med Chem 2623 1997 1947 1954
61. K. Inami, R.W. Nims, A. Srinivasan, M.L. Citro, J.E. Saavedra, A.I. Cederbaum, and et al. Metabolism of a liver-selective nitric oxide-releasing agent, V-PYRRO/NO, by human microsomal cytochromes P450 Nitric Oxide 14 2006 309 315
62. K. Kus, M. Walczak, E. Maslak, A. Zakrzewska, A. Gonciarz-Dytman, P. Zabielski, and et al. Hepatoselective NO-donors, V-PYRRO/NO and V-PROLI/NO in nonalcoholic fatty liver disease: a comparison of anti-steatotic effects with the biotransformation and pharmacokinetics Drug Metab Dispos 43 7 2015 1028 1036
63. R. Ricciardi, D.P. Foley, S.H. Quarfordt, J.E. Saavedra, L.K. Keefer, S.M. Wheeler, and et al. V-PYRRO/NO: an hepato-selective nitric oxide donor improves porcine liver hemodynamics and function after ischemia reperfusion Transplantation 71 2001 193 198
64. F. Moal, N. Veal, E. Vuillemin, E. Barrière, J. Wang, L. Fizanne, and et al. Hemodynamic and anti fi brotic effects of a selective liver nitric oxide donor V-PYRRO/NO in bile duct ligated rats World J Gastroenterol 12 2006 6639 6645
65. 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 alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8 Hepatology 32 2000 770 778
66. J. Liu, W. Qu, J.E. Saavedra, and M.P. Waalkes The nitric oxide donor, O2-vinyl 1-(pyrrolidin-1-yl)diazen-1-ium-1,2-diolate (V-PYRRO/NO), protects against cadmium-induced hepatotoxicity in mice J Pharmacol Exp Ther 310 2004 18 24
67. J. Liu, C. Li, M.P. Waalkes, J. Clark, P. Myers, J.E. Saavedra, and et al. The nitric oxide donor, V-PYRRO/NO, protects against acetaminophen-induced hepatotoxicity in mice Hepatology 37 2003 324 333
68. E. Maslak, P. Zabielski, K. Kochan, K. Kus, A. Jasztal, B. Sitek, and et al. The liver-selective NO donor, V-PYRRO/NO, protects against liver steatosis and improves postprandial glucose tolerance in mice fed high fat diet Biochem Pharmacol 93 2015 389 400
69. K. Konstantynowicz, A. Mikłosz, T. Stepek, and A. Chabowski The role of hepatic lipid accumulation in the development of insulin resistance in the liver Postepy Hig Med Dosw 65 2011 236 243
70. J. Araya, R. Rodrigo, L.A. Videla, L. Thielemann, M. Orellana, P. Pettinelli, and et al. Increase in long-chain polyunsaturated fatty acid n - 6/n - 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease Clin Sci (Lond) 106 2004 635 643
71. L.A. Videla, R. Rodrigo, J. Araya, and J. Poniachik Oxidative stress and depletion of hepatic long-chain polyunsaturated fatty acids may contribute to nonalcoholic fatty liver disease Free Radic Biol Med 37 2004 1499 1507
72. Y. Joe, M. Zheng, S.-K. Kim, S. Kim, J.M.D. Uddin, T.S. Min, and et al. The role of carbon monoxide in metabolic disease Ann N Y Acad Sci 1229 2011 156 161
73. E. Inoue, T. Ichiki, K. Takeda, H. Matsuura, T. Hashimoto, J. Ikeda, and et al. Beraprost sodium, a stable prostacyclin analogue, improves insulin resistance in high-fat diet-induced obese mice J Endocrinol 213 2012 285 291
74. N. Sato, M. Kaneko, M. Tamura, and H. Kurumatani The prostacyclin analog beraprost sodium ameliorates characteristics of metabolic syndrome in obese Zucker (fatty) rats Diabetes 59 2010 1092 1100
75. E. Demirci, I. Ferah, C. Gundogdu, S. Ozkanlar, N.K. Baygutalp, Y. Bayir, and et al. Endothelin receptor inhibition with bosentan delays onset of liver injury in streptozotocin-induced diabetic condition Drug Res (Stuttg) 65 5 2015 272 280
76. S.L. Friedman Mechanisms of disease: mechanisms of hepatic fibrosis and therapeutic implications Nat Clin Pract Gastroenterol Hepatol 1 2 2004 98 105
77. J.P. Iredale Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ J Clin Invest 117 3 2007 539 548