Cyclosporine A treated in vitro models induce cholestasis response through comparison of phenotype-directed gene expression analysis of in vivo Cyclosporine A-induced cholestasis

Toxicology Letters

Volumn 221, Issue 3, 2013, Pages 225-236

  Kienhuis, Anne S ^a,b,c   Vitins, Alexa P ^a,c   Pennings, Jeroen L A ^a,c   Pronk, Tessa E ^a,c   Speksnijder, Ewoud N ^d   Roodbergen, Marianne ^a,e   van Delft, Joost H M ^c   Luijten, Mirjam ^a,c   van der Ven, Leo T M ^a,c  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Cholestasis; Cyclosporin A; Hepatotoxicity; In vitro models; Mouse in vivo; Phenotype directed gene expression analysis

Indexed keywords

CYCLOSPORIN A; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BILE ACID; BILIRUBIN; CHOLESTEROL; CYCLOSPORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE METABOLISM; CHOLESTASIS; CONTROLLED STUDY; DRUG INDUCED DISEASE; DRUG METABOLISM; GENE EXPRESSION; GENETIC ANALYSIS; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUALITY CONTROL; TOXIC HEPATITIS; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; COMPARATIVE STUDY; CYTOCHEMISTRY; DRUG EFFECTS; EVALUATION STUDY; GENE EXPRESSION PROFILING; GENETICS; GERMFREE ANIMAL; HEPG2 CELL LINE; HUMAN; PROCEDURES; TOXICITY; TOXICOGENETICS;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BILE ACIDS AND SALTS; BILIRUBIN; CHOLESTASIS; CHOLESTEROL; CYCLOSPORINE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEP G2 CELLS; HISTOCYTOCHEMISTRY; HUMANS; MALE; MICE; MICE, INBRED C57BL; PHENOTYPE; SPECIFIC PATHOGEN-FREE ORGANISMS; TOXICOGENETICS;

EID: 84881262363     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.06.236     Document Type: Article

References (42)

1. Agellon L.B., Drozdowski L., Li L., Iordache C., Luong L., Clandinin M.T., Uwiera R.R., Toth M.J., Thomson A.B. Loss of intestinal fatty acid binding protein increases the susceptibility of male mice to high fat diet-induced fatty liver. Biochimica et Biophysica Acta 2007, 1771:1283-1288.
2. Agellon L.B., Torchia E.C. Intracellular transport of bile acids. Biochimica et Biophysica Acta 2000, 1486:198-209.
3. Anakk S., Watanabe M., Ochsner S.A., McKenna N.J., Finegold M.J., Moore D.D. Combined deletion of Fxr and Shp in mice induces Cyp17a1 and results in juvenile onset cholestasis. The Journal of Clinical Investigation 2011, 121:86-95.
4. Ansede J.H., Smith W.R., Perry C.H., St Claire R.L., Brouwer K.R. An in vitro assay to assess transporter-based cholestatic hepatotoxicity using sandwich-cultured rat hepatocytes. Drug Metabolism and Disposition: The Biological Fate of Chemicals 2010, 38:276-280.
5. Beilke L.D., Aleksunes L.M., Holland R.D., Besselsen D.G., Beger R.D., Klaassen C.D., Cherrington N.J. Constitutive androstane receptor-mediated changes in bile acid composition contributes to hepatoprotection from lithocholic acid-induced liver injury in mice. Drug Metabolism and Disposition: The Biological Fate of Chemicals 2009, 37:1035-1045.
6. Bohan A., Boyer J.L. Mechanisms of hepatic transport of drugs: implications for cholestatic drug reactions. Seminars in Liver Disease 2002, 22:123-136.
7. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193.
8. Cao G., Beyer T.P., Yang X.P., Schmidt R.J., Zhang Y., Bensch W.R., Kauffman R.F., Gao H., Ryan T.P., Liang Y., Eacho P.I., Jiang X.C. Phospholipid transfer protein is regulated by liver X receptors in vivo. The Journal of Biological Chemistry 2002, 277:39561-39565.
9. Chiang J.Y. Bile acids: regulation of synthesis. Journal of Lipid Research 2009, 50:1955-1966.
10. Cline M.S., Smoot M., Cerami E., Kuchinsky A., Landys N., Workman C., Christmas R., Avila-Campilo I., Creech M., Gross B., Hanspers K., Isserlin R., Kelley R., Killcoyne S., Lotia S., Maere S., Morris J., Ono K., Pavlovic V., Pico A.R., Vailaya A., Wang P.L., Adler A., Conklin B.R., Hood L., Kuiper M., Sander C., Schmulevich I., Schwikowski B., Warner G.J., Ideker T., Bader G.D. Integration of biological networks and gene expression data using Cytoscape. Nature Protocols 2007, 2:2366-2382.
11. Davila J.C., Xu J.J., Hoffmaster K.A., O'Brien P.J., Storm S.C. Current in vitro models to study drug-induced liver injury 2008, John Wiley & Sons Ltd, Chichester, UK.
12. Elferink M.G., Olinga P., Draaisma A.L., Merema M.T., Bauerschmidt S., Polman J., Schoonen W.G., Groothuis G.M. Microarray analysis in rat liver slices correctly predicts in vivo hepatotoxicity. Toxicology and Applied Pharmacology 2008, 229:300-309.
13. Fiorucci S., Antonelli E., Rizzo G., Renga B., Mencarelli A., Riccardi L., Orlandi S., Pellicciari R., Morelli A. The nuclear receptor SHP mediates inhibition of hepatic stellate cells by FXR and protects against liver fibrosis. Gastroenterology 2004, 127:1497-1512.
14. Goodwin B., Jones S.A., Price R.R., Watson M.A., McKee D.D., Moore L.B., Galardi C., Wilson J.G., Lewis M.C., Roth M.E., Maloney P.R., Willson T.M., Kliewer S.A. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Molecular Cell 2000, 6:517-526.
15. Hoeke M.O., Plass J.R., Heegsma J., Geuken M., van Rijsbergen D., Baller J.F., Kuipers F., Moshage H., Jansen P.L., Faber K.N. Low retinol levels differentially modulate bile salt-induced expression of human and mouse hepatic bile salt transporters. Hepatology 2009, 49:151-159.
16. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research 2003, 31:e15.
17. Jennen D.G., Magkoufopoulou C., Ketelslegers H.B., van Herwijnen M.H., Kleinjans J.C., van Delft J.H. Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicological Sciences: An Official Journal of the Society of Toxicology 2010, 115:66-79.
18. Kienhuis A.S., van de Poll M.C., Wortelboer H., van Herwijnen M., Gottschalk R., Dejong C.H., Boorsma A., Paules R.S., Kleinjans J.C., Stierum R.H., van Delft J.H. Parallelogram approach using rat-human in vitro and rat in vivo toxicogenomics predicts acetaminophen-induced hepatotoxicity in humans. Toxicological Sciences: An Official Journal of the Society of Toxicology 2009, 107:544-552.
19. Kim T.H., Kim H., Park J.M., Im S.S., Bae J.S., Kim M.Y., Yoon H.G., Cha J.Y., Kim K.S., Ahn Y.H. Interrelationship between liver X receptor alpha, sterol regulatory element-binding protein-1c, peroxisome proliferator-activated receptor gamma, and small heterodimer partner in the transcriptional regulation of glucokinase gene expression in liver. The Journal of Biological Chemistry 2009, 284:15071-15083.
20. Li T., Chiang J.Y. Nuclear receptors in bile acid metabolism. Drug Metabolism Reviews 2013, 45:145-155.
21. Lu T.T., Makishima M., Repa J.J., Schoonjans K., Kerr T.A., Auwerx J., Mangelsdorf D.J. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Molecular Cell 2000, 6:507-515.
22. Martin W., Gernot Z., Michael Trauner G.Z. New molecular insights into the mechanisms of cholestasis. Journal of Hepatology 2009, 51:565-580.
23. Medina I., Carbonell J., Pulido L., Madeira S.C., Goetz S., Conesa A., Tarraga J., Pascual-Montano A., Nogales-Cadenas R., Santoyo J., Garcia F., Marba M., Montaner D., Dopazo J. Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Research 2010, 38:W210-W213.
24. Milona A., Owen B.M., Cobbold J.F., Willemsen E.C., Cox I.J., Boudjelal M., Cairns W., Schoonjans K., Taylor-Robinson S.D., Klomp L.W., Parker M.G., White R., van Mil S.W., Williamson C. Raised hepatic bile acid concentrations during pregnancy in mice are associated with reduced farnesoid X receptor function. Hepatology 2010, 52:1341-1349.
25. Mindnich R., Drury J.E., Penning T.M. The effect of disease associated point mutations on 5beta-reductase (AKR1D1) enzyme function. Chemico-Biological Interactions 2011, 191:250-254.
26. Nicolaou M., Andress E.J., Zolnerciks J.K., Dixon P.H., Williamson C., Linton K.J. Canalicular ABC transporters and liver disease. The Journal of Pathology 2012, 226:300-315.
27. Parks D.J., Blanchard S.G., Bledsoe R.K., Chandra G., Consler T.G., Kliewer S.A., Stimmel J.B., Willson T.M., Zavacki A.M., Moore D.D., Lehmann J.M. Bile acids: natural ligands for an orphan nuclear receptor. Science 1999, 284:1365-1368.
28. Rakhshandehroo M., Sanderson L.M., Matilainen M., Stienstra R., Carlberg C., de Groot P.J., Muller M., Kersten S. Comprehensive analysis of PPARalpha-dependent regulation of hepatic lipid metabolism by expression profiling. PPAR Research 2007, 2007:26839.
29. Renga B., Mencarelli A., Migliorati M., Cipriani S., D'Amore C., Distrutti E., Fiorucci S. SHP-dependent and -independent induction of peroxisome proliferator-activated receptor-gamma by the bile acid sensor farnesoid X receptor counter-regulates the pro-inflammatory phenotype of liver myofibroblasts. Inflammatory Research 2011.
30. Rhodes D.R., Kalyana-Sundaram S., Tomlins S.A., Mahavisno V., Kasper N., Varambally R., Barrette T.R., Ghosh D., Varambally S., Chinnaiyan A.M. Molecular concepts analysis links tumors, pathways, mechanisms, and drugs. Neoplasia 2007, 9:443-454.
31. Rogue A., Spire C., Brun M., Claude N., Guillouzo A. Gene Expression Changes Induced by PPAR Gamma Agonists in Animal and Human Liver. PPAR Research 2010, 2010:325183.
32. Slob W. Dose-response modeling of continuous endpoints. Toxicological Sciences: An Official Journal of the Society of Toxicology 2002, 66:298-312.
33. Smid M., Dorssers L.C., Jenster G. Venn Mapping: clustering of heterologous microarray data based on the number of co-occurring differentially expressed genes. Bioinformatics 2003, 19:2065-2071.
34. Staudinger J.L., Goodwin B., Jones S.A., Hawkins-Brown D., MacKenzie K.I., LaTour A., Liu Y., Klaassen C.D., Brown K.K., Reinhard J., Willson T.M., Koller B.H., Kliewer S.A. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3369-3374.
35. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:15545-15550.
36. Tay S., Dickmann L., Dixit V., Isoherranen N. A comparison of the roles of peroxisome proliferator-activated receptor and retinoic acid receptor on CYP26 regulation. Mol Pharmacol 2010, 77:218-227.
37. Urizar N.L., Dowhan D.H., Moore D.D. The farnesoid X-activated receptor mediates bile acid activation of phospholipid transfer protein gene expression. The Journal of Biological Chemistry 2000, 275:39313-39317.
38. Wagner M., Zollner G., Trauner M. Nuclear receptor regulation of the adaptive response of bile acid transporters in cholestasis. Seminars in Liver Disease 2010, 30:160-177.
39. Yang X., Zhang B., Molony C., Chudin E., Hao K., Zhu J., Gaedigk A., Suver C., Zhong H., Leeder J.S., Guengerich F.P., Strom S.C., Schuetz E., Rushmore T.H., Ulrich R.G., Slatter J.G., Schadt E.E., Kasarskis A., Lum P.Y. Systematic genetic and genomic analysis of cytochrome P450 enzyme activities in human liver. Genome Research 2010, 20:1020-1036.
40. Zimmerman H.J. Hepatotoxicity: The Adverse Effects of Drugs and Other Chemicals on the Liver 1999, Lippincott Williams & Wilkins, Philadelphia.
41. Zollner G., Trauner M. Mechanisms of cholestasis. Clinical Liver Disease 2008, 12:1-26.
42. Zollner G., Trauner M. Nuclear receptors as therapeutic targets in cholestatic liver diseases. British Journal of Pharmacology 2009, 156:7-27.