Precision-cut liver slices as a model for the early onset of liver fibrosis to test antifibrotic drugs

Toxicology and Applied Pharmacology

Volumn 274, Issue 2, 2014, Pages 328-338

  Westra, Inge M ^a   Oosterhuis, Dorenda ^a   Groothuis, Geny M M ^a   Olinga, Peter ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Antifibrotic drugs; Early onset of fibrosis; Ex vivo model; Liver fibrosis; Precision cut liver slices

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA SMOOTH MUSCLE ACTIN; ANTIFIBROTIC AGENT; COLCHICINE; COLLAGEN TYPE 1; HEAT SHOCK PROTEIN 47; IMATINIB; PERINDOPRIL; PIRFENIDONE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BB; PROCOLLAGEN; PROCOLLAGEN 1 A1; ROSMARINIC ACID; SORAFENIB; SUNITINIB; TETRANDRINE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; DRUG MECHANISM; GENE EXPRESSION; LIVER FIBROSIS; LIVER SLICE; MALE; NONHUMAN; PRECISION CUT LIVER SLICE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

EID: 84891046304     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.11.017     Document Type: Article

References (66)

1. Armendariz-Borunda J., Islas-Carbajal M.C., Meza-Garcia E., Rincon A.R., Lucano S., Sandoval A.S., Salazar A., Berumen J., Alvarez A., Covarrubias A., Arechiga G., Garcia L. A pilot study in patients with established advanced liver fibrosis using pirfenidone. Gut 2006, 55:1663-1665.
2. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
3. Bataller R., Gines P., Nicolas J.M., Gorbig M.N., Garcia-Ramallo E., Gasull X., Bosch J., Arroyo V., Rodes J. Angiotensin II induces contraction and proliferation of human hepatic stellate cells. Gastroenterology 2000, 118:1149-1156.
4. Beljaars L., Molema G., Weert B., Bonnema H., Olinga P., Groothuis G.M., Meijer D.K., Poelstra K. Albumin modified with mannose 6-phosphate: a potential carrier for selective delivery of antifibrotic drugs to rat and human hepatic stellate cells. Hepatology 1999, 29:1486-1493.
5. Borkham-Kamphorst E., Herrmann J., Stoll D., Treptau J., Gressner A.M., Weiskirchen R. Dominant-negative soluble PDGF-beta receptor inhibits hepatic stellate cell activation and attenuates liver fibrosis. Lab. Invest. 2004, 84:766-777.
6. Brigstock D.R. Connective tissue growth factor (CCN2, CTGF) and organ fibrosis: lessons from transgenic animals. J. Cell Commun. Signal. 2010, 4:1-4.
7. Buchdunger E., Cioffi C.L., Law N., Stover D., Ohno-Jones S., Druker B.J., Lydon N.B. Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J. Pharmacol. Exp. Ther. 2000, 295:139-145.
8. Chen Y., Li D., Wu J., Chen Y., Lu H. Tetrandrine inhibits activation of rat hepatic stellate cells stimulated by transforming growth factor-beta in vitro via up-regulation of Smad 7. J. Ethnopharmacol. 2005, 100:299-305.
9. Chung K.Y., Kang D.S. Regulation of type I collagen and interstitial collagenase mRNA expression in human dermal fibroblasts by colchicine and D-penicillamine. Yonsei Med. J. 1999, 40:490-495.
10. Cong M., Iwaisako K., Jiang C., Kisseleva T. Cell signals influencing hepatic fibrosis. Int. J. Hepatol. 2012, 2012:158547.
11. de Graaf I.A., Olinga P., de Jager M.H., Merema M.T., de Kanter R., van de Kerkhof E.G., Groothuis G.M. Preparation and incubation of precision-cut liver and intestinal slices for application in drug metabolism and toxicity studies. Nat. Protoc. 2010, 5:1540-1551.
12. Deng Z.Y., Li J., Jin Y., Chen X.L., Lu X.W. Effect of oxymatrine on the p38 mitogen-activated protein kinases signalling pathway in rats with CCl4 induced hepatic fibrosis. Chin. Med. J. (Engl) 2009, 122:1449-1454.
13. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 1993, 122:103-111.
14. Di Sario A., Bendia E., Baroni G., Ridolfi F., Casini A., Ceni E., Saccomanno S., Marzioni M., Trozzi L., Sterpetti P., Taffetani S., Benedetti A. Effect of pirfenidone on rat hepatic stellate cell proliferation and collagen production. J. Hepatol. 2002, 37:584-591.
15. Distler J.H., Jungel A., Huber L.C., Schulze-Horsel U., Zwerina J., Gay R.E., Michel B.A., Hauser T., Schett G., Gay S., Distler O. Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis Rheum. 2007, 56:311-322.
16. Dokmanovic M., Clarke C., Marks P.A. Histone deacetylase inhibitors: overview and perspectives. Mol. Cancer Res. 2007, 5:981-989.
17. Domitrovic R., Skoda M., Marchesi V.V., Cvijanovic O., Pugel E.P., Stefan M.B. Rosmarinic acid ameliorates acute liver damage and fibrogenesis in carbon tetrachloride-intoxicated mice. Food Chem. Toxicol. 2012, 51:370-378.
18. Dooley S., Ten Dijke P. TGF-beta in progression of liver disease. Cell Tissue Res. 2012, 347:245-256.
19. Fisher R., Nau H., Gandolfi A.J., Brendel K. Toxicity of valproic acid in liver slices from Sprague-Dawley rats and domestic pigs. Toxicol. In Vitro 1991, 5:201-205.
20. Friedman S.L. Liver fibrosis-from bench to bedside. J. Hepatol. 2003, 38(Suppl. 1):S38-S53.
21. Friedman S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008, 134:1655-1669.
22. Friedman S.L. Antifibrotic activity of sorafenib in experimental hepatic fibrosis-refinement of targets, dosing and window of efficacy in vivo. Hepatology 2011, 54:360A-1455A.
23. Garcia L., Hernandez I., Sandoval A., Salazar A., Garcia J., Vera J., Grijalva G., Muriel P., Margolin S., Armendariz-Borunda J. Pirfenidone effectively reverses experimental liver fibrosis. J. Hepatol. 2002, 37:797-805.
24. Helmy A., Jalan R., Newby D.E., Hayes P.C., Webb D.J. Role of angiotensin II in regulation of basal and sympathetically stimulated vascular tone in early and advanced cirrhosis. Gastroenterology 2000, 118:565-572.
25. Hennenberg M., Trebicka J., Kohistani Z., Stark C., Nischalke H.D., Kramer B., Korner C., Klein S., Granzow M., Fischer H.P., Heller J., Sauerbruch T. Hepatic and HSC-specific sorafenib effects in rats with established secondary biliary cirrhosis. Lab. Invest. 2010, 91:241-251.
26. Hsu Y., Chiu Y., Cheng C., Wu C., Lin Y., Huang Y. Antifibrotic effects of tetrandrine on hepatic stellate cells and rats with liver fibrosis. J. Gastroenterol. Hepatol. 2007, 22:99-111.
27. Huang M.L., Li X., Meng Y., Xiao B., Ma Q., Ying S.S., Wu P.S., Zhang Z.S. Upregulation of angiotensin-converting enzyme (ACE) 2 in hepatic fibrosis by ACE inhibitors. Clin. Exp. Pharmacol. Physiol. 2010, 37:e1-e6.
28. Iyer S.N., Wild J.S., Schiedt M.J., Hyde D.M., Margolin S.B., Giri S.N. Dietary intake of pirfenidone ameliorates bleomycin-induced lung fibrosis in hamsters. J. Lab. Clin. Med. 1995, 125:779-785.
29. Kawada N., Kuroki T., Kobayashi K., Inoue M., Nakatani K., Kaneda K., Nagata K. Expression of heat-shock protein 47 in mouse liver. Cell Tissue Res. 1996, 284:341-346.
30. Kim Y., Fiel M.I., Albanis E., Chou H.I., Zhang W., Khitrov G., Friedman S.L. Anti-fibrotic activity and enhanced interleukin-6 production by hepatic stellate cells in response to imatinib mesylate. Liver Int. 2012, 32:1008-1017.
31. Kuo W.L., Yu M.C., Lee J.F., Tsai C.N., Chen T.C., Chen M.F. Imatinib mesylate improves liver regeneration and attenuates liver fibrogenesis in CCL4-treated mice. J. Gastrointest. Surg. 2012, 16:361-369.
32. Lee S.J., Kim Y.G., Kang K.W., Kim C.W., Kim S.G. Effects of colchicine on liver functions of cirrhotic rats: beneficial effects result from stellate cell inactivation and inhibition of TGF beta1 expression. Chem. Biol. Interact. 2004, 147:9-21.
33. Leveque D., Maloisel F. Clinical pharmacokinetics of imatinib mesylate. In Vivo 2005, 19:77-84.
34. Li G.S., Jiang W.L., Tian J.W., Qu G.W., Zhu H.B., Fu F.H. In vitro and in vivo antifibrotic effects of rosmarinic acid on experimental liver fibrosis. Phytomedicine 2010, 17:282-288.
35. Liu Y., Wen X.M., Lui E.L., Friedman S.L., Cui W., Ho N.P., Li L., Ye T., Fan S.T., Zhang H. Therapeutic targeting of the PDGF and TGF-beta-signaling pathways in hepatic stellate cells by PTK787/ZK22258. Lab. Invest. 2009, 89:1152-1160.
36. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
37. Mannaerts I., Nuytten N.R., Rogiers V., Vanderkerken K., van Grunsven L.A., Geerts A. Chronic administration of valproic acid inhibits activation of mouse hepatic stellate cells in vitro and in vivo. Hepatology 2010, 51:603-614.
38. Minkin P., Zhao M., Chen Z., Ouwerkerk J., Gelderblom H., Baker S.D. Quantification of sunitinib in human plasma by high-performance liquid chromatography-tandem mass spectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2008, 874:84-88.
39. Navarro-Partida J., Martinez-Rizo A.B., Gonzalez-Cuevas J., Arrevillaga-Boni G., Ortiz-Navarrete V., Armendariz-Borunda J. Pirfenidone restricts Th2 differentiation in vitro and limits Th2 response in experimental liver fibrosis. Eur. J. Pharmacol. 2012, 678:71-77.
40. Neef M., Ledermann M., Saegesser H., Schneider V., Widmer N., Decosterd L.A., Rochat B., Reichen J. Oral imatinib treatment reduces early fibrogenesis but does not prevent progression in the long term. J. Hepatol. 2006, 44:167-175.
41. Olinga P., Groothuis G.M.M. Use of human tissue slices in drug targeting research. Drug Target. Organ-Specif. Strateg. 2001, 12:309-331.
42. Olinga P., Merema M.T., de Jager M.H., Derks F., Melgert B.N., Moshage H., Slooff M.J., Meijer D.K., Poelstra K., Groothuis G.M. Rat liver slices as a tool to study LPS-induced inflammatory response in the liver. J. Hepatol. 2001, 35:187-194.
43. Osakabe N., Yasuda A., Natsume M., Yoshikawa T. Rosmarinic acid inhibits epidermal inflammatory responses: anticarcinogenic effect of Perilla frutescens extract in the murine two-stage skin model. Carcinogenesis 2004, 25:549-557.
44. Rodriguez L., Cerbon-Ambriz J., Munoz M.L. Effects of colchicine and colchiceine in a biochemical model of liver injury and fibrosis. Arch. Med. Res. 1998, 29:109-116.
45. Schaefer C.J., Ruhrmund D.W., Pan L., Seiwert S.D., Kossen K. Antifibrotic activities of pirfenidone in animal models. Eur. Respir. Rev. 2011, 20:85-97.
46. Sonnylal S., Shi-Wen X., Leoni P., Naff K., Van Pelt C.S., Nakamura H., Leask A., Abraham D., Bou-Gharios G., de Crombrugghe B. Selective expression of connective tissue growth factor in fibroblasts in vivo promotes systemic tissue fibrosis. Arthritis Rheum. 2010, 62:1523-1532.
47. Strumberg D., Clark J.W., Awada A., Moore M.J., Richly H., Hendlisz A., Hirte H.W., Eder J.P., Lenz H.J., Schwartz B. Safety, pharmacokinetics, and preliminary antitumor activity of sorafenib: a review of four phase I trials in patients with advanced refractory solid tumors. Oncologist 2007, 12:426-437.
48. Terasaki M., Chen L.B., Fujiwara K. Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 1986, 103:1557-1568.
49. Tsukada S., Parsons C.J., Rippe R.A. Mechanisms of liver fibrosis. Clin. Chim. Acta 2006, 364:33-60.
50. Tugues S., Fernandez-Varo G., Munoz-Luque J., Ros J., Arroyo V., Rodes J., Friedman S.L., Carmeliet P., Jimenez W., Morales-Ruiz M. Antiangiogenic treatment with sunitinib ameliorates inflammatory infiltrate, fibrosis, and portal pressure in cirrhotic rats. Hepatology 2007, 46:1919-1926.
51. van de Bovenkamp M., Groothuis G.M., Draaisma A.L., Merema M.T., Bezuijen J.I., van Gils M.J., Meijer D.K., Friedman S.L., Olinga P. Precision-cut liver slices as a new model to study toxicity-induced hepatic stellate cell activation in a physiologic milieu. Toxicol. Sci. 2005, 85:632-638.
52. van de Bovenkamp M., Groothuis G.M.M., Meijer D.K.F., Olinga P. Precision-cut fibrotic rat liver slices as a new model to test the effects of anti-fibrotic drugs in vitro. J. Hepatol. 2006, 45:696-703.
53. van de Bovenkamp M., Groothuis G.M., Meijer D.K., Olinga P. Liver slices as a model to study fibrogenesis and test the effects of anti-fibrotic drugs on fibrogenic cells in human liver. Toxicol. In Vitro 2008, 22:771-778.
54. Vickers A.E., Saulnier M., Cruz E., Merema M.T., Rose K., Bentley P., Olinga P. Organ slice viability extended for pathway characterization: an in vitro model to investigate fibrosis. Toxicol. Sci. 2004, 82:534-544.
55. Vonk L.A., Doulabi B.Z., Huang C.L., Helder M.N., Everts V., Bank R.A. Endoplasmic reticulum stress inhibits collagen synthesis independent of collagen-modifying enzymes in different chondrocyte populations and dermal fibroblasts. Biochem. Cell Biol. 2010, 88:539-552.
56. Wang Y., Gao J., Zhang D., Zhang J., Ma J., Jiang H. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J. Hepatol. 2010, 53:132-144.
57. Warner F.J., Lubel J.S., McCaughan G.W., Angus P.W. Liver fibrosis: a balance of ACEsα. Clin. Sci. (Lond.) 2007, 113:109-118.
58. Watanabe T., Tajima H., Hironori H., Nakagawara H., Ohnishi I., Takamura H., Ninomiya I., Kitagawa H., Fushida S., Tani T., Fujimura T., Ota T., Wakayama T., Iseki S., Harada S. Sodium valproate blocks the transforming growth factor (TGF)-beta1 autocrine loop and attenuates the TGF-beta1-induced collagen synthesis in a human hepatic stellate cell line. Int. J. Mol. Med. 2011, 28:919-925.
59. Xu W., Song S., Huang Y., Gong Z. Effects of perindopril and valsartan on expression of transforming growth factor-beta-Smads in experimental hepatic fibrosis in rats. J. Gastroenterol. Hepatol. 2006, 21:1250-1256.
60. Yang M.D., Chiang Y.M., Higashiyama R., Asahina K., Mann D.A., Mann J., Wang C.C., Tsukamoto H. Rosmarinic acid and baicalin epigenetically derepress peroxisomal proliferator-activated receptor gamma in hepatic stellate cells for their antifibrotic effect. Hepatology 2012, 55:1271-1281.
61. Yeki M., Koda M., Matono T., Sugihara T., Maeda K., Murawaki Y. Preventative and therapeutic effects of perindopril on hepatic fibrosis induced by bile duct ligation in rats. Mol. Med. Rep. 2009, 2:857-864.
62. Yoshiji H., Kuriyama S., Yoshii J., Ikenaka Y., Noguchi R., Nakatani T., Tsujinoue H., Fukui H. Angiotensin-II type 1 receptor interaction is a major regulator for liver fibrosis development in rats. Hepatology 2001, 34:745-750.
63. Yoshiji H., Kuriyama S., Noguchi R., Yoshii J., Ikenaka Y., Yanase K., Namisaki T., Kitade M., Yamazaki M., Tsujinoue H. Combination of interferon-beta and angiotensin-converting enzyme inhibitor, perindopril, attenuates the murine liver fibrosis development. Liver Int. 2005, 25:153-161.
64. Yoshiji H., Noguchi R., Kuriyama S., Ikenaka Y., Yoshii J., Yanase K., Namisaki T., Kitade M., Masaki T., Fukui H. Imatinib mesylate (STI-571) attenuates liver fibrosis development in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288:G907-G913.
65. Zhang J.J., Wang Y.L., Feng X.B., Song X.D., Liu W.B. Rosmarinic acid inhibits proliferation and induces apoptosis of hepatic stellate cells. Biol. Pharm. Bull. 2011, 34:343-348.
66. Zhao X.Y., Zeng X., Li X.M., Wang T.L., Wang B.E. Pirfenidone inhibits carbon tetrachloride- and albumin complex-induced liver fibrosis in rodents by preventing activation of hepatic stellate cells. Clin. Exp. Pharmacol. Physiol. 2009, 36:963-968.