A histone deacetylase inhibitor, largazole, decreases liver fibrosis and angiogenesis by inhibiting transforming growth factor-β and vascular endothelial growth factor signalling

Liver International

Volumn 33, Issue 4, 2013, Pages 504-515

  Liu, Yuqing ^a   Wang, Zhuo ^a   Wang, Jianing ^a,b   Lam, Wingchi ^a   Kwong, Shuqin ^a   Li, Furong ^c   Friedman, Scott L ^d   Zhou, Shuyan ^c   Ren, Qi ^b   Xu, Zhengshuang ^b   Wang, Xingen ^c   Ji, Ling ^c   Tang, Shoubin ^b   Zhang, Hui ^b   Lui, Eric L ^a   Ye, Tao ^a,b  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b PEKING UNIVERSITY   (China)

^c JINAN UNIVERSITY   (China)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Hepatic stellate cells; Largazole; Liver fibrosis; TGF ; VEGF

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CARBON TETRACHLORIDE; CD34 ANTIBODY; COLLAGEN TYPE 1; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; LARGAZOLE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; SMAD2 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER CELL; LIVER FIBROSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; STELLATE CELL;

EID: 84875052732     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12034     Document Type: Article

References (41)

1. Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008; 134: 1655-69.
2. Yoshiji H, Kuriyama S, Miyamoto Y, et al. Tissue inhibitor of metalloproteinases-1 promotes liver fibrosis development in a transgenic mouse model. Hepatology 2003; 32: 1248-54.
3. Dooley S, Delvoux B, Lahme B, Mangasser-Stephan K, Gressner AM. Modulation of transforming growth factor β response and signaling during transdifferentiation of rat hepatic stellate cells to myofibroblasts. Hepatology 2000; 31: 1094-106.
4. Inagaki Y, Okazaki I. Emerging insights into transforming growth factor β Smad signal in hepatic fibrogenesis. Gut 2007; 56: 284-92.
5. Yata Y, Gotwals P, Koteliansky V, Rockey DC. Dose-dependent inhibition of hepatic fibrosis in mice by a TGF-beta soluble receptor: implications for antifibrotic therapy. Hepatology 2002; 35: 1022-30.
6. Liu Y, Lui ELH, Friedman Sl, et al. PTK787/ZK22258 attenuates stellate cell activation and hepatic fibrosis in vivo by inhibiting VEGF signaling. Lab Invest 2008; 89: 13.
7. Guo C-J, Pan Q, Cheng T, et al. Changes in microRNAs associated with hepatic stellate cell activation status identify signaling pathways. FEBS J 2009; 276: 5163-76.
8. Corpechot C, Barbu V, Wendum D, et al. Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology 2002; 35: 1010-21.
9. Novo E, Cannito S, Zamara E, et al. Proangiogenic cytokines as hypoxia-dependent factors stimulating migration of human hepatic stellate cells. Am J Pathol 2007; 170: 1942-53.
10. Taori K, Paul VJ, Luesch H. Structure and activity of largazole, a potent antiproliferative agent from the Floridian marine cyanobacterium Symploca sp. J Am Chem Soc 2008; 130: 1806-7.
11. Ren Q, Dai L, Zhang H, et al. Total synthesis of largazole. Synlett 2008; 15: 2379-83.
12. Bowers A, West N, Taunton J, et al. Total synthesis and biological mode of action of largazole: a potent class I histone deacetylase inhibitor. J Am Chem Soc 2008; 130: 11219-22.
13. Zeng X, Yin B, Hu Z, et al. Total synthesis and biological evaluation of largazole and derivatives with promising selectivity for cancers cells. Org Lett 2010; 12: 1368-71.
14. Schafer SZO, Gressner AM. The synthesis of proteoglycans in fat-storing cells of rat liver. Hepatology 1987; 7: 680-7.
15. Friedman SL, Rockey DC, Mcguire RF, et al. Isolated hepatic lipocytes and kupffer cells from normal human liver: morphological and functional characteristics in primary culture. Hepatology 1992; 15: 234-43.
16. Liu Y, Wang Z, Kwong SQ, et al. Inhibition of PDGF, TGF-β, and Abl signaling and reduction of liver fibrosis by the small molecule Bcr-Abl tyrosine kinase antagonist Nilotinib. J Hepatol 2011; 55: 612-25.
17. Taura K, De Minicis S, Seki E, et al. Hepatic stellate cells secrete Angiopoietin 1 that Induces angiogenesis in liver fibrosis. Gastroenterology 2008; 135: 1729-38.
18. Dubuisson L, Desmoulière A, Decourt B, et al. Inhibition of rat liver fibrogenesis through noradrenergic antagonism. Hepatology 2002; 35: 325-31.
19. Niki T, Pekny M, Hellemans K, et al. Class VI intermediate filament protein nestin is induced during activation of rat hepatic stellate cells. Hepatology 1999; 29: 520-7.
20. Sakaida I, Uchida K, Matsumura Y, Okita K. Interferon gamma treatment prevents procollagen gene expression without affecting transforming growth factor-β1 expression in pig serum-induced rat liver fibrosis in vivo. J Hepatol 1998; 28: 471-9.
21. Sakaida I, Matsumura Y, Kubota M, et al. The prolyl 4-hydroxylase inhibitor HOE 077 prevents activation of Ito cells, reducing procollagen gene expression in rat liver fibrosis induced by choline-deficient L-amino acid-defined diet. Hepatology 1996; 23: 755-63.
22. Kanitakis J, Narvaez D, Claudy A. Expression of the CD34 antigen distinguishes Kaposi's sarcoma from pseudo-Kaposi's sarcoma (acroangiodermatitis). Br J Dermatol 1996; 134: 44-6.
23. Souto JA, Vaz E, Lepore I, et al. Synthesis and biological characterization of the histone deacetylase inhibitor largazole and C7-modified analogues. J Med Chem 2010; 53: 4654-67.
24. Mannaerts I, Nuytten NR, Rogiers V, et al. Chronic administration of valproic acid inhibits activation of mouse hepatic stellate cells in vitro and in vivo. Hepatology 2010; 51: 12.
25. Rombouts K, Knittel T, Machesky L, et al. Actin filament formation, reorganization and migration are impaired in hepatic stellate cells under influence of trichostatin A, a histone deactylase inhibitor. J Hepatol 2002; 37: 788.
26. Niki T, Rombouts K, De Bleser P, et al. A histone deactylase inhibitor, Trichostatin A, suppresses myofibroblastic differentiation of rat hepatic stellate cells in primary culture. Hepatology 1999; 29: 9.
27. Venturelli S, Armeanu S, Pathil A, et al. Epigenetic combination therapy as a tumor-selective treatment approach for hepatocellular carcinoma. Cancer 2007; 109: 2132-41.
28. Armeanu S, Pathil A, Venturelli S, et al. Apoptosis on hepatoma cells but not on primary hepatocytes by histone deacetylase inhibitors valproate and ITF2357. J Hepatol 2005; 42: 210-7.
29. Papeleu P, Vanhaecke T, Elaut G, et al. Differential effects of histone deacetylase inhibitors in tumor and normal cells-what is the toxicological relevance? Crit Rev Toxicol 2005; 35: 363-78.
30. Benelkebir H, Marie S, Hayden AL, et al. Total synthesis of largazole and analogues: HDAC inhibition, antiproliferative activity and metabolic stability. Bioorg Med Chem 2011; 19: 3650-8.
31. Issa R, Williams E, Trim N, et al. Apoptosis of hepatic stellate cells: involvement in resolution of biliary fibrosis and regulation by soluble growth factors. Gut 2001; 48: 548-57.
32. Uemura M, Swenson ES, Gaca MDA, et al. Smad2 and Smad3 play different roles in rat hepatic stellate cell function and α-smooth muscle actin organization. Mol Biol Cell 2005; 16: 4214-24.
33. S6k. Am J Physiol Gastrointest Liver Physiol 2004; 287: G974-87.
34. Reif S, Lang A, Lindquist J, et al. The role of focal adhesion Kinase-Phosphatidylinositol 3-Kinase-Akt signaling in hepatic stellate cell proliferation and type I collagen expression. J Biol Chem 2002; 278: 8083-90.
35. Lee JS, Semela D, Iredale J, Shah VH. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte? Hepatology 2007; 45: 817-25.
36. Kitade M, Yoshiji H, Kojima H, et al. Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology 2006; 44: 983-91.
37. Yoshiji H, Kuriyama S, Yoshii J, et al. Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrogenesis. Gut 2003; 52: 1347-54.
38. Ferrara N, Gerber H-P, Lecouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-76.
39. Ankoma-Sey V, Matli M, Chang KB, et al. Coordinated induction of VEGF receptors in mesenchymal cell types during rat hepatic wound healing. Oncogene 1998; 17: 115-21.
40. Yang S, Xin X, Zlot C, et al. Vascular endothelial cell growth factor-driven endothelial tube formation is mediated by vascular endothelial cell growth factor receptor-2, a kinase insert domain-containing receptor. Artherioscier Thromb Vasc Biol 2001; 21: 1934-40.
41. Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 1997; 18: 2221-30.