Liver fibrosis: a balance of ACEs?

There is an increasing body of evidence to suggest that the RAS (renin-angiotensin system) contributes to tissue injury and fibrosis in chronic liver disease. A number of studies have shown that components of a local hepatic RAS are up-regulated in fibrotic livers of humans and in experimental animal models. Angiotensin II, the main physiological effector molecule of this system, mediates liver fibrosis by stimulating fibroblast proliferation (myofibroblast and hepatic stellate cells), infiltration of inflammatory cells, and the release of inflammatory cytokines and growth factors such as TGF (transforming growth factor)-beta1, IL (interleukin)-1beta, MCP (monocyte chemoattractant protein)-1 and connective tissue growth factor. Furthermore, blockade of the RAS by ACE (angiotensin-converting enzyme) inhibitors and angiotensin type 1 receptor antagonists significantly attenuate liver fibrosis in experimental models of chronic liver injury. In 2000 ACE2 (angiotensin-converting enzyme 2), a human homologue of ACE, was identified. ACE2 efficiently degrades angiotensin II to angiotensin-(1-7), a peptide which has recently been shown to have both vasodilatory and tissue protective effects. This suggests that ACE2 and its products may be part of an alternate enzymatic pathway in the RAS, which counterbalances the generation and actions of angiotensin II, the ACE2-angiotensin-(1-7)-Mas axis. This review focuses on the potential roles of the RAS, angiotensin II and ACE2 in chronic liver injury and fibrogenesis.

[1]  D. Averill,et al.  Upregulation of Angiotensin-Converting Enzyme 2 After Myocardial Infarction by Blockade of Angiotensin II Receptors , 2004, Hypertension.

[2]  M. Jamaluddin,et al.  Angiotensin II Induces Nuclear Factor (NF)-κB1 Isoforms to Bind the Angiotensinogen Gene Acute-Phase Response Element: A Stimulus-Specific Pathway for NF-κB Activation , 2000 .

[3]  K. Robison,et al.  A Novel Angiotensin-Converting Enzyme–Related Carboxypeptidase (ACE2) Converts Angiotensin I to Angiotensin 1-9 , 2000, Circulation research.

[4]  N. Minamino,et al.  Significance of increased plasma adrenomedullin concentration in patients with cirrhosis. , 1998, Journal of hepatology.

[5]  P. Angus,et al.  Up-regulation of components of the renin-angiotensin system in the bile duct-ligated rat liver. , 2002, Gastroenterology.

[6]  P. Angus,et al.  Effect of angiotensin II type 1 receptor blockade on experimental hepatic fibrogenesis. , 2001, Journal of hepatology.

[7]  H. Saito,et al.  Anti-fibrogenic effect of an angiotensin converting enzyme inhibitor on chronic carbon tetrachloride-induced hepatic fibrosis in rats. , 2001, Hepatology research : the official journal of the Japan Society of Hepatology.

[8]  R. Bataller,et al.  Angiotensin II induces contraction and proliferation of human hepatic stellate cells. , 2000, Gastroenterology.

[9]  H. Yoshiji,et al.  Combined effect of an ACE inhibitor, perindopril, and interferon on liver fibrosis markers in patients with chronic hepatitis C , 2005, Journal of Gastroenterology.

[10]  Ji-lin Cheng,et al.  The regulatory role of AT 1 receptor on activated HSCs in hepatic fibrogenesis:effects of RAS inhibitors on hepatic fibrosis induced by CCl(4). , 2000, World journal of gastroenterology.

[11]  M. Bristow,et al.  Angiotensin-(1-7) Formation in the Intact Human Heart: In Vivo Dependence on Angiotensin II as Substrate , 2003, Circulation.

[12]  J. Ménard,et al.  Immunocytochemical localization of angiotensinogen in rat liver and kidney , 2004, Cell and Tissue Research.

[13]  M. Huentelman,et al.  Protection from angiotensin II‐induced cardiac hypertrophy and fibrosis by systemic lentiviral delivery of ACE2 in rats , 2005, Experimental physiology.

[14]  Kenzo Sato,et al.  Are transcription factors NF-kappaB and AP-1 involved in the ANG II-stimulated production of proinflammatory cytokines induced by LPS in dehydrated rats? , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[15]  I. Rusyn,et al.  NADPH oxidase-derived free radicals are key oxidants in alcohol-induced liver disease. , 2000, The Journal of clinical investigation.

[16]  N. Hooper,et al.  Circulating Activities of Angiotensin-Converting Enzyme, Its Homolog, Angiotensin-Converting Enzyme 2, and Neprilysin in a Family Study , 2006, Hypertension.

[17]  K. Yasuda,et al.  Endogenous avidin found in the magnum gland of the hen oviduct , 1983, Cell and Tissue Research.

[18]  K. Chayama,et al.  Anti-fibrogenic function of angiotensin II type 2 receptor in CCl4-induced liver fibrosis. , 2006, Biochemical and biophysical research communications.

[19]  Shoko Kuroda,et al.  An angiotensin II type 1 receptor antagonist, olmesartan medoxomil, improves experimental liver fibrosis by suppression of proliferation and collagen synthesis in activated hepatic stellate cells , 2003, British journal of pharmacology.

[20]  G. Díaz-Araya,et al.  Enalapril Attenuates Downregulation of Angiotensin-Converting Enzyme 2 in the Late Phase of Ventricular Dysfunction in Myocardial Infarcted Rat , 2006, Hypertension.

[21]  P. Deddish,et al.  N-domain-specific substrate and C-domain inhibitors of angiotensin-converting enzyme: angiotensin-(1-7) and keto-ACE. , 1998, Hypertension.

[22]  D. Ron,et al.  Transcriptional regulation of hepatic angiotensinogen gene expression by the acute-phase response , 1990, Molecular and Cellular Endocrinology.

[23]  M. Ohsawa,et al.  Expression of angiotensin II type 1 receptor in human cirrhotic livers: Its relation to fibrosis and portal hypertension. , 2005, Hepatology research : the official journal of the Japan Society of Hepatology.

[24]  R D Smith,et al.  Angiotensin II receptor subtypes. , 1992, American journal of hypertension.

[25]  S. Friedman,et al.  Liver fibrosis -- from bench to bedside. , 2003, Journal of hepatology.

[26]  T. Parsons,et al.  Hydrolysis of Biological Peptides by Human Angiotensin-converting Enzyme-related Carboxypeptidase* , 2002, The Journal of Biological Chemistry.

[27]  M. Raizada,et al.  Prevention of angiotensin II-induced cardiac remodeling by angiotensin-(1-7). , 2007, American journal of physiology. Heart and circulatory physiology.

[28]  R. Britto,et al.  Role of angiotensin-(1-7) in the modulation of the baroreflex in renovascular hypertensive rats. , 1997, Hypertension.

[29]  Y. Wei,et al.  Effect of Losartan, an Angiotensin II Antagonist, on Hepatic Fibrosis Induced by CCl4 in Rats , 2004, Digestive Diseases and Sciences.

[30]  James F. Riordan,et al.  Ace revisited: A new target for structure-based drug design , 2003, Nature Reviews Drug Discovery.

[31]  R. Santos,et al.  Angiotensin-(1–7): an update , 2000, Regulatory Peptides.

[32]  Y. Tokusashi,et al.  Therapeutic efficacy of an angiotensin II receptor antagonist in patients with nonalcoholic steatohepatitis , 2004, Hepatology.

[33]  D. Brenner,et al.  Role of Kupffer cells and gut‐derived endotoxins in alcoholic liver injury1 , 2000, Journal of gastroenterology and hepatology.

[34]  E. Tallant,et al.  Inhibition of human lung cancer cell growth by angiotensin-(1-7). , 2004, Carcinogenesis.

[35]  Y Ando,et al.  Angiotensin-converting enzyme inhibition attenuates the progression of rat hepatic fibrosis. , 2001, Gastroenterology.

[36]  R. Schwabe,et al.  NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. , 2003, The Journal of clinical investigation.

[37]  Ji-lin Cheng,et al.  Effects of AT1 receptor antagonist, losartan, on rat hepatic fibrosis induced by CCl(4). , 2000, World journal of gastroenterology.

[38]  H. Pieterman,et al.  Metabolism and Production of Angiotensin I in Different Vascular Beds in Subjects With Hypertension , 1990, Hypertension.

[39]  Thomas Walther,et al.  Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  L. Skeggs,et al.  THE ISOLATION AND ASSAY OF HYPERTENSIN FROM BLOOD , 1952, The Journal of experimental medicine.

[41]  G. Navis,et al.  Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis , 2004, The Journal of pathology.

[42]  K. Chayama,et al.  AT1A-deficient mice show less severe progression of liver fibrosis induced by CCl(4). , 2003, Biochemical and biophysical research communications.

[43]  C. Ferrario Commentary on Tikellis et al: There is more to discover about angiotensin-converting enzyme. , 2003, Hypertension.

[44]  T. Sakata,et al.  Diagnostic significance of serum angiotensin-converting enzyme activity in biochemical tests with special reference of chronic liver diseases. , 1991, Japanese journal of medicine.

[45]  X. Forns,et al.  Beneficial Effect of Angiotensin-Blocking Agents on Graft Fibrosis in Hepatitis C Recurrence after Liver Transplantation , 2004, Transplantation.

[46]  P. Leung,et al.  A local pancreatic renin-angiotensin system: endocrine and exocrine roles. , 2003, The international journal of biochemistry & cell biology.

[47]  P. Sexton,et al.  G-Protein–Coupled Receptor Mas Is a Physiological Antagonist of the Angiotensin II Type 1 Receptor , 2005, Circulation.

[48]  P. Leung The peptide hormone angiotensin II: its new functions in tissues and organs. , 2004, Current protein & peptide science.

[49]  F. Ramalho,et al.  Effect of losartan, an angiotensin II antagonist, on secondary biliary cirrhosis. , 2002, Hepato-gastroenterology.

[50]  H. Yoshiji,et al.  Angiotensin-II induces the tissue inhibitor of metalloproteinases-1 through the protein kinase-C signaling pathway in rat liver fibrosis development. , 2003, Hepatology research : the official journal of the Japan Society of Hepatology.

[51]  D. Chappard,et al.  Hemodynamic and antifibrotic effects of losartan in rats with liver fibrosis and/or portal hypertension. , 2002, Journal of hepatology.

[52]  C. Ferrario,et al.  Angiotensin II AT1 receptors regulate ACE2 and angiotensin-(1-7) expression in the aorta of spontaneously hypertensive rats. , 2005, American journal of physiology. Heart and circulatory physiology.

[53]  M. Raizada,et al.  ACE2 gene transfer attenuates hypertension-linked pathophysiological changes in the SHR. , 2006, Physiological genomics.

[54]  Li Xu,et al.  Expression of Angiotensin II Type 1 Receptor in Rat Hepatic Stellate Cells and Its Effects on Cell Growth and Collagen Production , 2003, Hormone Research in Paediatrics.

[55]  F. Ramalho,et al.  Effect of angiotensin-converting enzyme inhibitors on liver regeneration in rats. , 2002, Hepato-gastroenterology.

[56]  M. Rossi,et al.  Captopril reduces collagen and mast cell and eosinophil accumulation in pig serum‐induced rat liver fibrosis , 1994, Pathology international.

[57]  S. Milani,et al.  Increased expression of monocyte chemotactic protein-1 during active hepatic fibrogenesis: correlation with monocyte infiltration. , 1998, The American journal of pathology.

[58]  N. Hooper,et al.  Angiotensin-converting Enzyme 2 (ACE2), But Not ACE, Is Preferentially Localized to the Apical Surface of Polarized Kidney Cells* , 2005, Journal of Biological Chemistry.

[59]  D. Gouma,et al.  Cholestatic interleukin-6-deficient mice succumb to endotoxin-induced liver injury and pulmonary inflammation. , 2004, American journal of respiratory and critical care medicine.

[60]  Kai Wei,et al.  Effects of lipopolysaccharides stimulated Kupffer cells on activation of rat hepatic stellate cells. , 2004, World journal of gastroenterology.

[61]  Nigel M. Hooper,et al.  A Human Homolog of Angiotensin-converting Enzyme , 2000, The Journal of Biological Chemistry.

[62]  C. Ferrario,et al.  Angiotensin-(1-7) dilates canine coronary arteries through kinins and nitric oxide. , 1996, Hypertension.

[63]  Christopher J. Parsons,et al.  Systemic infusion of angiotensin II exacerbates liver fibrosis in bile duct–ligated rats , 2005, Hepatology.

[64]  W. Jiménez,et al.  Assessment of the renin-angiotensin system in cirrhotic patients. Comparison between plasma renin activity and direct measurement of immunoreactive renin. , 1992, Journal of hepatology.

[65]  D. Brenner,et al.  Attenuated hepatic inflammation and fibrosis in angiotensin type 1a receptor deficient mice. , 2005, Journal of hepatology.

[66]  K. Clark,et al.  Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme , 2002, FEBS letters.

[67]  R. Nada,et al.  Association of celiac disease with non‐cirrhotic portal fibrosis , 2006, Journal of gastroenterology and hepatology.

[68]  K. Chayama,et al.  Angiotensin II Participates in Hepatic Inflammation and Fibrosis through MCP-1 Expression , 2005, Digestive Diseases and Sciences.

[69]  S. Uğraş,et al.  Anti-fibrogenic effects of captopril and candesartan cilexetil on the hepatic fibrosis development in rat. The effect of AT1-R blocker on the hepatic fibrosis. , 2003, Experimental and toxicologic pathology : official journal of the Gesellschaft fur Toxikologische Pathologie.

[70]  S. Friedman,et al.  Activation of rat hepatic stellate cells leads to loss of glutathion S‐transferases and their enzymatic activity against products of oxidative stress , 1999, Hepatology.

[71]  R. Santos,et al.  Potentiation of the hypotensive effect of bradykinin by angiotensin-(1–7)-related peptides , 1999, Peptides.

[72]  T. Mak,et al.  CARMA3/Bcl10/MALT1-dependent NF-κB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells , 2007, Proceedings of the National Academy of Sciences.

[73]  P. Angus,et al.  Chronic liver injury in rats and humans upregulates the novel enzyme angiotensin converting enzyme 2 , 2005, Gut.

[74]  S. Sakuta,et al.  Effect of angiotensin receptor antagonist on liver fibrosis in early stages of chronic hepatitis C , 2002, Hepatology.

[75]  H. Yoshiji,et al.  The angiotensin-I-converting enzyme inhibitor perindopril suppresses tumor growth and angiogenesis: possible role of the vascular endothelial growth factor. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[76]  H. Yoshiji,et al.  Suppression of the renin-angiotensin system attenuates vascular endothelial growth factor-mediated tumor development and angiogenesis in murine hepatocellular carcinoma cells. , 2002, International journal of oncology.

[77]  P. Timmermans,et al.  Angiotensin II receptors and functional correlates. , 1992, American journal of hypertension.

[78]  D. Brenner,et al.  Prolonged infusion of angiotensin II into normal rats induces stellate cell activation and proinflammatory events in liver. , 2003, American journal of physiology. Gastrointestinal and liver physiology.

[79]  N. Hooper,et al.  Evaluation of angiotensin-converting enzyme (ACE), its homologue ACE2 and neprilysin in angiotensin peptide metabolism. , 2004, The Biochemical journal.

[80]  Q. Lin,et al.  Increased Angiotensin-(1-7)–Forming Activity in Failing Human Heart Ventricles: Evidence for Upregulation of the Angiotensin-Converting Enzyme Homologue ACE2 , 2003, Circulation.

[81]  C. Ferrario,et al.  Angiotensin-(1-7) inhibits growth of cardiac myocytes through activation of the mas receptor. , 2005, American journal of physiology. Heart and circulatory physiology.

[82]  G. Chisolm,et al.  Angiotensin-(1-7) inhibits vascular smooth muscle cell growth. , 1996, Hypertension.

[83]  A. Rivas-Estilla,et al.  PGE2 alleviates kidney and liver damage, decreases plasma renin activity and acute phase response in cirrhotic rats with acute liver damage. , 2005, Experimental and toxicologic pathology : official journal of the Gesellschaft fur Toxikologische Pathologie.

[84]  X. D. Wang Chronic alcohol intake interferes with retinoid metabolism and signaling. , 2009, Nutrition reviews.

[85]  M. Teixeira,et al.  The renin-angiotensin system in a rat model of hepatic fibrosis: evidence for a protective role of Angiotensin-(1-7). , 2007, Journal of hepatology.

[86]  P. B. Lai,et al.  Expression and localization of AT1 receptors in hepatic Kupffer cells: its potential role in regulating a fibrogenic response , 2003, Regulatory Peptides.

[87]  N. Hooper,et al.  Tumor Necrosis Factor-α Convertase (ADAM17) Mediates Regulated Ectodomain Shedding of the Severe-acute Respiratory Syndrome-Coronavirus (SARS-CoV) Receptor, Angiotensin-converting Enzyme-2 (ACE2) , 2005, Journal of Biological Chemistry.

[88]  D. Diz,et al.  Downloaded from http://hyper.ahajournals.org / by guest on February 20, 2013Impaired Heart Rate Baroreflex in Older Rats Role of Endogenous Angiotensin-(1–7) at the Nucleus Tractus Solitarii , 2022 .

[89]  H. Yoshiji,et al.  Angiotensin‐II type 1 receptor interaction is a major regulator for liver fibrosis development in rats , 2001, Hepatology.

[90]  Bin Li,et al.  Effects of transmitters and interleukin-10 on rat hepatic fibrosis induced by CCl4. , 2003, World journal of gastroenterology.

[91]  V. Campese,et al.  Effects of omapatrilat on the renin-angiotensin system in salt-sensitive hypertension. , 2002, American journal of hypertension.

[92]  S. Friedman,et al.  Mechanisms and therapy of hepatic fibrosis: Report of the AASLD single topic basic research conference , 2000, Hepatology.

[93]  D. Diz,et al.  Effect of Angiotensin-Converting Enzyme Inhibition and Angiotensin II Receptor Blockers on Cardiac Angiotensin-Converting Enzyme 2 , 2005, Circulation.

[94]  R. Ardaillou Active fragments of angiotensin II: enzymatic pathways of synthesis and biological effects. , 1997, Current opinion in nephrology and hypertension.

[95]  R. Bataller,et al.  Activated human hepatic stellate cells express the renin-angiotensin system and synthesize angiotensin II. , 2003, Gastroenterology.

[96]  Y. Tokusashi,et al.  Inhibitory effect of angiotensin II receptor antagonist on hepatic stellate cell activation in non-alcoholic steatohepatitis. , 2006, World journal of gastroenterology.

[97]  A. Brasier,et al.  Transcription factors modulating angiotensinogen gene expression in hepatocytes. , 1994, Kidney international.

[98]  B. Morris,et al.  Localization of angiotensinogen in rat liver by immunocytochemistry. , 1979, Endocrinology.