Hypoxia, hypoxia-inducible factors and fibrogenesis in chronic liver diseases

Histology and Histopathology

Volumn 29, Issue 1, 2014, Pages 33-44

  Cannito, Stefania ^a,b   Paternostro, Claudia ^a,b   Busletta, Chiara ^a,b   Bocca, Claudia ^a,b   Colombatto, Sebastiano ^a,b   Miglietta, Antonella ^a,b   Novo, Erica ^a,b   Parola, Maurizio ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Chronic liver diseases; Hypoxia; Hypoxia inducible factors; Liver angiogenesis; Liver fibrogenesis

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HIF3A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1;

ANIMAL; CELL HYPOXIA; CHRONIC DISEASE; HUMAN; LIVER CIRRHOSIS; LIVER DISEASE; METABOLISM; MYOFIBROBLAST; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CHRONIC DISEASE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; LIVER CIRRHOSIS; LIVER DISEASES; MYOFIBROBLASTS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84890943300     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (87)

1. Aleffi S., Petrai I., Bertolani C., Parola M., Colombatto S., Novo E., Vizzutti F., Anania F.A., Milani S., Rombouts K., Laffi G., Pinzani M. and Marra F. (2005). Upregulation of proinflammatory and proangiogenic cytokines by leptin in human hepatic stellate cells. Hepatology 42, 1339-1348.
2. Aleffi S., Navari N., Delogu W., Galastri S., Novo E., Rombouts K., Pinzani M., Parola M. and Marra F. (2011). Mammalian target of rapamycin mediates the angiogenic effects of leptin in human hepatic stellate cells. Am. J. Physiol. Gastrointest. Liver. Physiol. 301, G210-219.
3. Ankoma-Sey V., Wang Y. and Dai Z. (2000). Hypoxic stimulation of vascular endothelial growth factor expression in activated rat hepatic stellate cells. Hepatology 31, 141-148.
4. Archer S.L., Gomberg-Maitland M., Maitland M.L., Rich S., Garcia J.G. and Weir E.K. (2008). Mitochondrial metabolism, redox signaling, and fusion: a mitochondria-ROS-HIF-1a-Kv1.5 O2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am. J. Physiol. Heart Circ. Physiol. 294, H570-H578.
5. Bozova S. and Elpek G.O. (2007). Hypoxia-inducible factor-1alpha expression in experimental cirrhosis: correlation with vascular endothelial growth factor expression and angiogenesis. APMIS 115, 795-801.
6. Busletta C., Novo E., Valfrè Di Bonzo L., Povero D., Paternostro C., Ievolella M., Mareschi K., Ferrero I., Cannito S., Compagnone A., Bandino A., Colombatto S., Fagioli F. and Parola M. (2011). Dissection of the biphasic nature of hypoxia-induced motogenic action in bone marrow-derived human mesenchymal stem cells. Stem Cells 29, 952-963.
7. Carmeliet P. (2003). Angiogenesis in health and disease. Nature Med. 9, 653-660.
8. Carmeliet P. and Jain R.K. (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473, 298-307.
9. Copple B.L., Kaska S. and Wentling C. (2012). Hypoxia-inducible factor activation in myeloid cells contributes to the development of liver fibrosis in cholestatic mice. J. Pharmacol. Exp. Ther. 341, 307-316.
10. Coriat R., Gouya H., Mir O., Ropert S., Vignaux O., Chaussade S., Sogni P., Pol S., Blanchet B., Legmann P. and Goldwasser F. (2011). Reversible decrease of portal venous flow in cirrhotic patients: a positive side effect of sorafenib. PLoS One 6:e16978.
11. Corpechot C., Barbu V., Wendum D., Kinnman N., Rey C., Poupon R., Housset C. and Rosmorduc O. (2002a). Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology 35, 1010-1021.
12. Corpechot C., Barbu V., Wendum D., Chignard N., Housset C., Poupon R. and Rosmorduc O. (2002b). Hepatocyte growth factor and c-Met inhibition by hepatic cell hypoxia: a potential mechanism for liver regeneration failure in experimental cirrhosis. Am. J. Pathol. 160, 613-620.
13. Dewhirst M.W., Cao Y. and Moeller B. (2008). Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nature Rev. Cancer 8, 425-437.
14. Diez H., Fischer A., Winkler A., Hu C.J., Hatzopoulos A.K., Breier G. and Gessler M. (2007). Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp. Cell Res. 313, 1-9.
15. Dranoff J.A. and Wells R.G. (2010). Portal fibroblasts: Underappreciated mediators of biliary fibrosis. Hepatology 51, 1438-1444.
16. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z. and Bergers G. (2008). HIF1a induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13, 206-220.
17. Dufour J.-F. and Johnson P. (2010). Liver cancer: from molecular pathogenesis to new therapies: summary of the EASL single topic conference. J. Hepatol. 52, 296-304.
18. Duffy A., Wilkerson J. and Greten T.F. (2013). Hemorrhagic events in hepatocellular carcinoma patients treated with antiangiogenic therapies. Hepatology 57, 1068-1077.
19. El-Serag H.B. and Rudolph K.L. (2007). Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132, 2557-2576.
20. Fernández M., Semela D., Bruix J., Colle I., Pinzani M. and Bosch J. (2009). Angiogenesis in liver disease. J. Hepatol. 50, 604-620.
21. Ferrara N., Gerber H. and LeCouter J. (2003). The biology of VEGF and its receptors. Nature Med. 9, 669-676.
22. Forbes S.J. and Parola M. (2011). Liver fibrogenic cells. Best. Pract. Res. Clin. Gastroenterol. 25, 207-218.
23. Fraisl P., Mazzone M., Schmidt T. and Carmeliet P. (2009). Regulation of angiogenesis by oxygen and metabolism. Dev. Cell. 16, 167-179.
24. Friedman S.L. (2008). Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88, 125-172.
25. Huang H.C., Wang S.S., Hsin I.F., Chang C.C., Lee F.Y., Lin H.C., Chuang C.L., Lee J.Y., Hsieh H.G. and Lee S.D. (2012). Cannabinoid receptor 2 agonist ameliorates mesenteric angiogenesis and portosystemic collaterals in cirrhotic rats. Hepatology 56, 248-258.
26. Jagavelu K., Routray C., Shergill U., O'Hara S.P., Faubion W. and Shah V.H. (2010). Endothelial cell toll-like receptor 4 regulates fibrosisassociated angiogenesis in the liver. Hepatology 52, 590-601.
27. Jain R.K. (2003). Molecular regulation of vessel maturation. Nature Med. 9, 685-693.
28. Jiang B.H., Rue E., Wang G.L., Roe R. and Semenza G.L. (1996). Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271, 17771-17778.
29. Jungermann K. and Kietzmann T. (2000). Oxygen: modulator of metabolic zonation and disease of the liver. Hepatology 31, 255-260.
30. Kaelin W.G. Jr. and Ratcliffe P.J. (2008). Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402.
31. Kaur S., Tripathi D., Dongre K., Garg V., Rooge S., Mukopadhyay A., Sakhuja P. and Sarin S.K. (2013). Increased number and function of endothelial progenitor cells stimulate angiogenesis by resident liver sinusoidal endothelial cells (SECs) in cirrhosis through paracrine factors. J. Hepatol. 57, 1193-1198.
32. Keith B., Johnson R.S. and Simon M.C. (2012). HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nature Rev. Cancer 12, 9-22.
33. Kitade M., Yoshiji H., Kojima H., Ikenaka Y., Noguchi R., Kaji K., Yoshii J., Yanase K., Namisaki T., Asada K., Yamazaki M., Tsujimoto T., Akahane T., Uemura M. and Fukui H. (2006). Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology 44, 983-991.
34. Krones A., Jungermann K. and Kietzmann T. (2001). Cross-talk between the signals hypoxia and glucose at the glucose response element of the Ltype pyruvate kinase gene. Endocrinology 142, 2707-2718.
35. Lando D., Peet D.J., Gorman J.J., Whelan D.A., Whitelaw M.L. and Bruick R.K. (2002). FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471.
36. Lee U.E. and Friedman S.L. (2011). Mechanisms of hepatic fibrogenesis. Best. Pract. Res. Clin. Gastroenterol. 25, 195-206.
37. Lee J.S., Semela D., Iredale J. and Shah V.H. (2007). Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte? Hepatology 45, 817-825.
38. Liu Y., Wang Z., Wang J., Lam W., Kwong S., Li F., Friedman S.L., Zhou S., Ren Q., Xu Z., Wang X., Ji L., Tang S., Zhang H., Lui E.L. and Ye T. (2013). A histone deacetylase inhibitor, largazole, decreases liver fibrosis and angiogenesis by inhibiting transforming growth factor-, and vascular endothelial growth factor signalling. Liver Int. 33, 504-515.
39. Llovet J.M., Burroughs A. and Bruix J. (2003). Hepatocellular carcinoma. Lancet 362, 1907-1917.
40. Loenarz C., Coleman M.L., Boleininger A., Schierwater B., Holland P.W., Ratcliffe P.J. and Schofield C.J. (2011). The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep. 12, 63-70.
41. Majumder S., Piguet A.C., Dufour J.F. and Chatterjee S. (2013). Study of the cellular mechanism of Sunitinib mediated inactivation of activated hepatic stellate cells and its implications in angiogenesis. Eur. J. Pharmacol. 705, 86-95.
42. Medina J., Arroyo A.G., Sanchez-Madrid F. and Moreno-Otero R. (2004). Angiogenesis in chronic inflammatory liver diseases. Hepatology 39, 1185-1195.
43. Mejias M., Garcia-Pras E., Tiani C., Miquel R., Bosch J. and Fernandez M. (2009). Beneficial effects of sorafenib on splanchnic, intrahepatic, and portocollateral circulations in portal hypertensive and cirrhotic rats. Hepatology 49, 1245-1256.
44. Melgar-Lesmes P., Casals G., Pauta M., Ros J., Reichenbach V., Bataller R., Morales-Ruiz M. and Jimenez W. (2010). Apelin mediates the induction of profibrogenic genes in human hepatic stellate cells. Endocrinology 151, 5306-5314.
45. Moon J.-K., Welch T.P., Gonzalez F.J. and Copple B.L. (2009). Reduced Liver Fibrosis in Hypoxia-inducible Factor-1α-Deficient Mice. Am. J. Physiol.-Gastrointest. Liver Physiol. 296, G582-592.
46. Nath B. and Szabo G. (2012). Hypoxia and hypoxia inducible factors: diverse roles in liver diseases. Hepatology 55, 622-633.
47. Novo E., Cannito S., Zamara E., Valfrè di Bonzo L., Caligiuri A., Cravanzola C., Compagnone A., Colombatto S., Marra F., Pinzani M. and Parola M. (2007). Proangiogenic cytokines as hypoxia dependent factors stimulating migration of human hepatic stellate cells. Am. J. Pathol. 170, 1942-1953.
48. Novo E., Povero D., Busletta C., Paternostro C., Valfrè di Bonzo L., Cannito S., Compagnone A., Bandino A., Marra F., Colombatto S., David E., Pinzani M. and Parola M. (2012). The biphasic nature of hypoxia-induced directional migration of activated human hepatic stellate cells. J. Pathol. 54, 964-974.
49. Parola M., Marra F. and Pinzani M. (2008). Myofibroblast-like cells and liver fibrogenesis: emerging concepts in a rapidly moving scenario. Mol. Asp. Med. 29, 59-67.
50. Patel S.A. and Simon M.C. (2008). Biology of hypoxia-inducible factor-2alpha in development and disease. Cell Death Differ. 15, 628-634.
51. Paternostro C., David E., Novo E. and Parola M. (2010). Hypoxia, angiogenesis and liver fibrogenesis in the progression of chronic liver diseases. World J. Gastroenterol. 16, 281-288.
52. Pouysségur J. and Mechta-Grigoriou F. (2006) Redox regulation of the hypoxia-inducible factor. Biol. Chem. 387, 1337-1346.
53. Pouyssegur J., Dayan F. and Mazure N.M. (2006). Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437-443.
54. Povero D., Busletta C., Novo E., Valfrè di Bonzo L., Cannito S., Paternostro C. and Parola M. (2010). Liver fibrosis: a dynamic and potentially reversible process. Histol. Histopathol. 25, 1075-1091.
55. Principe A., Melgar-Lesmes P., Fernández-Varo G., del Arbol L.R., Ros J., Morales-Ruiz M., Bernardi M., Arroyo V. and Jiménez W. (2008). The hepatic apelin system: a new therapeutic target for liver disease. Hepatology 48, 1193-1201.
56. Pugh C.W. and Ratcliffe P.(2003). Regulation of angiogenesis by hypoxia: role of the HIF system. Nature Med. 9, 677-684.
57. Qu A., Taylor M., Xue X., Matsubara T., Metzger D., Chambon P., Gonzalez F.J. and Shah Y.M. (2011). Hypoxia-inducible transcription factor 2· promotes steatohepatitis through augmenting lipid accumulation, inflammation, and fibrosis. Hepatology 54, 472-483.
58. Ramirez-Bergeron D.L., Runge A., Dahl K.D., Fehling H.J., Keller G. and Simon M.C. (2004). Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131, 4623-4634.
59. Reichenbach V., Ros J., Fernández-Varo G., Casals G., Melgar-Lesmes P., Campos T., Makriyannis A., Morales-Ruiz M. and Jiménez W. (2012). Prevention of fibrosis progression in CCl4-treated rats: role of the hepatic endocannabinoid and apelin systems. J. Pharmacol. Exp. Ther. 340, 629-637.
60. Rosmorduc O. and Housset C. (2010). Hypoxia: a link between fibrogenesis, angiogenesis, and carcinogenesis in liver disease. Semin. Liver Dis. 30, 258-270.
61. Sahin H., Borkham-Kamphorst E., Kuppe C., Zaldivar M.M., Grouls C., Al-samman M., Nellen A., Schmitz P., Heinrichs D., Berres M.L., Doleschel D., Scholten D., Weiskirchen R., Moeller M.J., Kiessling F., Trautwein C. and Wasmuth H.E. (2012). Chemokine Cxcl9 attenuates liver fibrosis-associated angiogenesis in mice. Hepatology 55, 1610-1619.
62. Seki E., De Minicis S., Osterreicher C.H., Kluwe J., Osawa Y., Brenner D.A. and Schwabe R.F. (2007). TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nature Med. 13, 1324-1332.
63. Semela D., Das A., Langer D., Kang N., Leof E. and Shah V. (2008). Platelet-derived growth factor signaling through ephrin-b2 regulates hepatic vascular structure and function. Gastroenterology 135, 671-679.
64. Semenza G.L. (2001). Hypoxia-inducible factor 1: oxygen homeostasis and disease patho-physiology. Trends Mol. Med. 7, 345-350.
65. Semenza G.L. (2004). Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 19, 176-182.
66. Semenza G.L. (2011). Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365, 537-547.
67. Semenza G.L. (2012). Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408.
68. Semenza G.L., Jiang B.H., Leung S.W., Passantino R., Concordet J.P., Maire P. and Giallongo A. (1996). Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271, 32529-32537.
69. Shah V.H. and Bruix J. (2009). Antiangiogenic therapy: not just for cancer anymore? Hepatology 49, 1066-1068.
70. Sharp F.R. and Bernaudin M. (2004). HIF1 and oxygen sensing in the brain. Nature Rev. Neurosci. 5, 437-448.
71. Talks K.L., Turley H., Gatter K.C., Maxwell P.H., Pugh C.W., Ratcliffe P.J. and Harris A.L. (2000). The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am. J. Pathol. 157, 411-421.
72. Taura K., De Minicis S., Seki E., Hatano E., Iwaisako K., Osterreicher C.H., Kodama Y., Miura K., Ikai I., Uemoto S. and Brenner D.A. (2008). Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology 135, 1729-1738.
73. Tiani C., Garcia-Pras E., Mejias M., de Gottardi A., Berzigotti A., Bosch J. and Fernandez M. (2009). Apelin signaling modulates splanchnic angiogenesis and portosystemic collateral vessel formation in rats with portal hypertension. J. Hepatol. 50, 296-305.
74. Tillmanns J., Rota M., Hosoda T., Misao Y., Esposito G., Gonzalez A., Vitale S., Parolin C., Yasuzawa-Amano S., Muraski J., De Angelis A., Lecapitaine N., Siggins R.W., Loredo M., Bearzi C., Bolli R., Urbanek K., Leri A., Kajstura J. and Anversa P. (2008). Formation of large coronary arteries by cardiac progenitor cells. Proc. Natl. Acad. Sci. USA 105, 1668-1673.
75. Tugues S., Fernandez-Varo G., Muñoz-Luque J., Ros J., Arroyo V., Rodés J., Friedman S.L., Carmeliet P., Jiménez W. and Morales-Ruiz M. (2007). Antiangiogenic treatment with sunitinib ameliorates inflammatory infiltrate, fibrosis, and portal pressure in cirrhotic rats. Hepatology 46, 1919-1926.
76. Valfrè di Bonzo L., Novo E., Cannito S., Busletta C., Paternostro C., Povero D. and Parola M. (2009). Angiogenesis and liver fibrogenesis. Histol. Histopathol. 23, 1324-1341.
77. Van Steenkiste C., Ribera J., Geerts A., Pauta M., Tugues S., Casteleyn C., Libbrecht L., Olievier K., Schroyen B., Reynaert H., van Grunsven L.A., Blomme B., Coulon S., Heindryckx F., De Vos M., Stassen J.M., Vinckier S., Altamirano J., Bataller R., Carmeliet P., Van Vlierberghe H., Colle I., and Morales-Ruiz M. (2011). Inhibition of placental growth factor activity reduces the severity of fibrosis, inflammation, and portal hypertension in cirrhotic mice. Hepatology 53, 1629-1640.
78. 2 tension. Proc. Natl. Acad. Sci. USA 92, 5510-5514.
79. Wang Y.Q., Luk J.M., Ikeda K., Man K., Chu A.C., Kaneda K. and Fan S.T. (2004). Regulatory role of vHL/HIF-1alpha in hypoxia-induced VEGF production in hepatic stellate cells. Biochem. Biophys. Res. Commun. 317, 358-362.
80. Ward J.P. (2008). Oxygen sensors in context. Biochim. Biophys. Acta 1777, 1-14.
81. Weir E.K., Lopez-Barneo. J., Buckler K.J. and Archer S.L. (2005). Acute oxygen-sensing mechanisms. N. Engl. J. Med. 353, 2042-2055.
82. Weis S.M. and Cheresh D.A. (2011). Tumor angiogenesis: molecular pathways and therapeutic targets. Nature Med. 17, 1359-1370.
83. Witek R.P., Yang L., Liu R., Jung Y., Omenetti A., Syn W.K., Choi S.S., Cheong Y., Fearing C.M., Agboola K.M., Chen W., Diehl A.M. (2009). Liver cell-derived microparticles activate hedgehog signaling and alter gene expression in hepatic endothelial cells. Gastroenterology 136, 320-330.
84. Yokomori H., Oda M., Yoshimura K., Machida S., Kaneko F. and Hibi T. (2011). Overexpression of apelin receptor (APJ/AGTRL1) on hepatic stellate cells and sinusoidal angiogenesis in human cirrhotic liver. J. Gastroenterol. 46, 222-231.
85. Yoshiji H., Kuriyama S., Yoshii J., Ikenaka Y., Noguchi R., Hicklin D.J., Wu Y., Yanase K., Namisaki T., Yamazaki M., Tsujinoue H., Imazu H., Masaki T. and Fukui H. (2003). Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrogenesis. Gut 52, 1347-1354.
86. Zhu P., Huang L., Ge X., Yan F., Wu R. and Ao Q. (2006). Transdifferentiation of pulmonary arteriolar endothelial cells into smooth muscle-like cells regulated by myocardin involved in hypoxia-induced pulmonary vascular remodelling. Int. J. Exp. Pathol. 87, 463-474.
87. Zhu Q., Zou L., Jagavelu K., Simonetto D.A., Huebert R.C., Jiang Z.D., DuPont H.L. and Shah V.H. (2012). Intestinal decontamination inhibits TLR4 dependent fibronectin-mediated cross-talk between stellate cells and endothelial cells in liver fibrosis in mice. J. Hepatol. 56, 893-899.