Differential effect of troglitazone on the human bile acid transporters, MRP2 and BSEP, in the PXB hepatic chimeric mouse

Toxicologic Pathology

Volumn 40, Issue 8, 2012, Pages 1106-1116

  Foster, John R ^a   Jacobsen, Matt ^a   Kenna, Gerry ^a   Schulz Utermoehl, Timothy ^a   Morikawa, Yoshio ^b   Salmu, Juuso ^b   Wilson, Ian D ^a  

^a ASTRAZENECA   (United Kingdom)

^b PhoenixBio USA Corporation   (Japan)

Author keywords

BSEP; CYP; human mouse chimeric liver; MRP2; PXB mouse; troglitazone

Indexed keywords

BILE ACID; BSEP PROTEIN; CYTOCHROME P450 1A1; CYTOCHROME P450 2B1; CYTOCHROME P450 3A2; LIVER PROTEIN; MULTIDRUG RESISTANCE PROTEIN 2; TROGLITAZONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ELECTRON; FEMALE; HUMAN; LIVER; LIVER CELL; MALE; MICROSCOPY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CHILD, PRESCHOOL; CHROMANS; CYTOCHROME P-450 ENZYME SYSTEM; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; HEPATOCYTES; HUMANS; LIVER; MALE; MICE; MICE, SCID; MICE, TRANSGENIC; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; ORGAN SIZE; PPAR GAMMA; SPECIES SPECIFICITY; THIAZOLIDINEDIONES; TRANSPLANTATION CHIMERA;

MURINAE;

EID: 84870043730     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623312447542     Document Type: Article

References (45)

1. Barth H., Robinet E., Liang T. J., Baumert T. F.. Mouse models for the study of HCV infection and virus-host interactions. J Hepatol. 2008 ; 49: 134-42
2. Bowen W. P., Carey J. E., Miah A., McMurray H. F., Munday P. W., James R. S., Coleman R. A., Brown A. M.. Measurement of cytochrome P450 gene induction in human hepatocytes using quantitative real-time reverse transcriptase- polymerase chain reaction. Drug Metab Dispos. 2000 ; 28: 781-88
3. Berk P. D., Javitt N. B.. Hyperbilirubinemia and cholestasis. Am J Med. 1978 ; 64: 311-26
4. Cohen J. C., Horton J. D., Hobbs H. H.. Human fatty liver disease: Old questions and new insights. Science. 2011 ; 332: 1519-23
5. French S. W.. Biochemical basis for alcohol-induced liver injury. Clin Biochem. 1989 ; 22: 41-49
6. Fujii T.. Toxicological correlation between changes in blood biochemical parameters and liver histopathological findings. J Toxicol Sci. 1997 ; 22: 161-83
7. Funk C., Pantze M., Jehle L., Ponelle C., Scheuermann G., Lazendic M., Gasser R.. Troglitazone-induced intrahepatic cholestasis by an interference with the hepatobiliary export of bile acids in male and female rats. Correlation with the gender difference in troglitazone sulfate formation and the inhibition of the canalicular bile salt export pump (Bsep) by troglitazone and troglitazone sulfate. Toxicology. 2001b ; 167: 83-98
8. Funk C., Ponelle C., Scheuermann G., Pantze M.. Cholestatic potential of troglitazone as a possible factor contributing to troglitazone-induced hepatotoxicity: In vivo and in vitro interaction at the canalicular bile salt export pump (Bsep) in the rat. Mol Pharmacol. 2001a ; 59: 627-35
9. Gitlin N., Julie N. L., Spurr C. L., Lim K. N., Juarbe H. M.. Two cases of severe clinical and histological hepatotoxicity associated with troglitazone. Ann Intern Med. 1998 ; 129: 36-38
10. Greer M. L., Barber J., Eakins J., Kenna J. G.. Cell based approaches for evaluation of drug-induced liver injury. Toxicology. 2010 ; 268: 125-31
11. Handler J. A., Kossor D. C., Goldstein R. S.. Assessment of hepatobiliary function in vivo and ex vivo in the rat. J Pharmacol Toxicol Methods. 1994 ; 31: 11-19
12. Haskins J. R., Rowse P., Rahbari R., de la Iglesia F. A.. Thiazolidinedione toxicity to isolated hepatocytes revealed by coherent multiprobe fluorescence microscopy and correlated with multiparameter flow cytometry of peripheral leukocytes. Arch Toxicol. 2001 ; 75: 425-38
13. Hayashi H., Takada T., Suzuki H., Onuki R., Hofmann A. F., Sugiyama Y.. Transport by vesicles of glycine- and taurine-conjugated bile salts and taurolithocholate 3-sulfate: A comparison of human BSEP with rat Bsep. Biochim Biophys Acta. 2005 ; 1738: 54-62
14. He K., Woolf T. F., Kindt E. K., Fielder A. E., Talaat R. E.. Troglitazone quinone formation catalyzed by human and rat CYP3A: An atypical CYP oxidation reaction. Biochem Pharmacol. 2001 ; 62: 191-98
15. Herman J. R., Dethloff L. A., McGuire E. J., Parker R. F., Walsh K. M., Gough A. W., Masuda H., De La Iglesia F. A.. Rodent carcinogenicity with the thiazolidinedione anti-diabetic agent troglitazone. Toxicol Sci. 2002 ; 68: 226-36
16. Honma W., Kamiyama Y., Yoshinari K., Sasano H., Shimada M., Nagata K., Yamazoe Y.. Enzymatic characterization and interspecies difference of phenol sulfotransferases, ST1A forms. Drug Metab Dispos. 2001 ; 29: 274-81
17. Horikawa M., Kato Y., Tyson C. A., Sugiyama Y.. Potential cholestatic activity of various therapeutic agents assessed by bile canalicular membrane vesicles isolated from rats and humans. Drug Metab Pharmacokin. 2003 ; 18: 16-22
18. Jemnitz K., Veres Z., Tugyi R., Vereczkey L.. Biliary efflux transporters involved in the clearance of rosuvastatin in sandwich culture of primary rat hepatocytes. Toxicol In Vitro. 2010 ; 24: 605-10
19. Kohlroser J., Mathai J., Reichheld J., Banner B. F., Bonkovsky H. L.. Hepatotoxicity Due to Troglitazone: Report of Two Cases and Review of Adverse Events Reported to the United States Food and Drug Administration. Am. J. GastroEnt. 2000 ; 95: 272-76
20. Kopec K. L., Burns D.. Non-alcoholic Fatty liver disease: A review of the spectrum of disease, diagnosis, and therapy. Nutr Clin Pract. 2011 ; 26: 565-76
21. Mace K., Aguilar F., Wang J. S., Vautravers P., Gomez-Lechon M., Gonzalez F. J., Groopman J., Harris C. C., Pfeifer A. M.. Aflatoxin B1-induced DNA adduct formation and p53 mutations in CYP450-expressing human liver cell lines. Carcinogenesis. 1997 ; 18: 1291-97
22. Machado M. V., Cortez-Pinto H.. Cell death and nonalcoholic steatohepatitis: Where is ballooning relevant?. Expert Rev Gastroenterol Hepatol. 2011 ; 5: 213-22
23. Madsen K. G., Grönberg G., Skonberg C., Jurva U., Hansen S. H., Olsen J.. Electrochemical oxidation of troglitazone: Identification and characterization of the major reactive metabolite in liver microsomes. Chem Res Toxicol. 2008 ; 21: 2035-41
24. Meuleman P., Libbrecht L., De Vos R., de Hemptinne B., Gevaert K., Vandekerckhove J., Roskams T., Leroux-Roels G.. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatol. 2005 ; 41: 847-56
25. Neuschwander-Tetri B.A., Bridle K.R., Wells L.D., Marcu M., Ramm G.A.. Troglitazone-induced hepatic failure leading to liver transplantation. Ann Intern Med. 1998 ; 129: 38-41
26. Ong M. M., Latchoumycandane C., Boelsterli U. A.. Troglitazone-induced hepatic necrosis in an animal model of silent genetic mitochondrial abnormalities. Toxicol Sci. 2007 ; 97: 205-13
27. Park B. K., Kitteringham N. R., Maggs J. L., Pirmohamed M., Williams D. P.. The role of metabolic activation in drug-induced hepatotoxicity. Annu Rev Pharmacol Toxicol. 2005 ; 45: 177-202
28. Preininger K., Stingl H., Englisch R., Furnsinn C., Graf J., Waldhausl W., Roden M.. Acute troglitazone action in isolated perfused rat liver. Br J Pharmacol. 1999 ; 126: 372-78
29. Reynolds E. S.. The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J Cell Biol. 1963 ; 17: 208-12
30. Ritchie R. F. Putman F. W., ed. New York: Academic Press ; 1975: 375-425.
31. Roth R. A., Ganey P. E.. Intrinsic versus idiosyncratic drug-induced hepatotoxicity - two villains or one?. J Pharmacol Exp Ther. 2010 ; 332: 692-97
32. Sato Y., Yamada H., Iwasaki K., Tateno C., Yokoi T., Yoshizato K., Horii I.. Human hepatocytes can repopulate mouse liver: Histopathology of the liver in human hepatocyte-transplanted chimeric mice and toxicologic responses to acetaminophen. Toxicol Pathol. 2008 ; 36: 581-91
33. Schulz-Utermoehl T., Sarda S., Foster J. R., Jacobsen M., Kenna J. G., Morikawa Y., Salmu J, Gross G., Wilson I. D.. Evaluation of the pharmacokinetics, biotransformation and hepatic transporter effects of troglitazone in mice with humanised livers. Xenobiotica. 2012 ; 42: 503-17
34. Smith M. T.. Mechanisms of troglitazone hepatotoxicity. Chem Res Toxicol. 2003 ; 16: 679-87
35. Snow K. L., Moseley R. H.. Effect of thiazolidinediones on bile acid transport in rat liver. Life Sci. 2007 ; 80: 732-40
36. Stieger B., Meier Y., Meier P. J.. The bile salt export pump. Pflugers Arch-Eur J Physiol. 2007 ; 453: 611-20
37. Tateno C., Yasumi Yoshizane Y., Saito N., Kataoka M., Utoh R., Yamasaki C., Tachibana A., Soeno Y., Asahina K., Hino H., Asahara T., Yokoi T., Furukawa T., Yoshizato K.. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol. 2004 ; 165: 901-12
38. Vignati L., Turlizzi E., Monaci S., Grossi P., Kanter R., Monshouwer M.. An in vitro approach to detect metabolite toxicity due to CYP3A4-dependent bioactivation of xenobiotics. Toxicology. 2005 ; 216: 154-67
39. Warner K. A., Fernstrom M. J., Ruch R. J.. Inhibition of mouse hepatocyte gap junctional intercellular communication by phenobarbital correlates with strain-specific hepatocarcinogenesis. Toxicol Sci. 2003 ; 71: 190-97
40. Watkins P. B.. Idiosyncratic liver injury: Challenges and approaches. Tox Path. 2005 ; 33: 1-5
41. Watkins P. B., Whitcomb R. W.. Hepatic dysfunction associated with troglitazone [letter]. N Engl J.Med. 1998 ; 338: 916-17
42. Yamamoto Y., Yamazaki H., Ikeda T., Watanabe T., Iwabuchi H., Nakajima M., Yokoi T.. Formation of a novel quinone epoxide metabolite of troglitazone with cytotoxicity to HepG2 cells. Drug Metab Dispos. 2002 ; 30: 155-60
43. Yamazaki H., Shibata A., Suzuki M., Nakajima M., Shimada N., Guengerich F. P., Yokoi T.. Oxidation of troglitazone to a quinone-type metabolite catalyzed by cytochrome P-450 2C8 and P-450 3A4 in human liver microsomes. Drug Metab Dispos. 1999 ; 27: 1260-66
44. Yokoi T.. Troglitazone. Handb Exp Pharmacol. 2010 ; 196: 419-35
45. Yoshizato K., Tateno C., Utoh R.. Mice with liver composed of human hepatocytes as an animal model for drug testing. Curr Drug Discov Technol. 2012 ; 9: 637-76