Chimeric rodents with humanized liver: bridging the preclinical/clinical trial gap in ADME/toxicity studies

References

• Agoram B, Woltosza WS, Bolger MB. (2001). Predicting the impact of physiological and biochemical processes on oral drug bioavailability. Adv Drug Deliv Rev 50:S41–67
   PubMed Web of Science ®Google Scholar
• Almeida-Porada G, Crapnell K, Porada C, et al. (2005). In vivo haematopoietic potential of human neural stem cells. Br J Haematol 130:276–83
   PubMed Web of Science ®Google Scholar
• Anderson S, Luffer-Atlas D, Knadler MP. (2009). Predicting circulating human metabolites: how good are we? Chem Res Toxicol 22:243–56
   PubMed Web of Science ®Google Scholar
• Ashkenazi A, Pai RC, Fong S, et al. (1999). Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155–62
   PubMed Web of Science ®Google Scholar
• Aurich I, Mueller LP, Aurich H, et al. (2007). Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 56:405–15
   PubMed Web of Science ®Google Scholar
• Austin RP, Barton P, Cockroft SL, et al. (2002). The influence of nonspecific microsomal binding on apparent intrinsic clearance, and its prediction from physicochemical properties. Drug Metab Dispos 30:1497–503
   PubMed Web of Science ®Google Scholar
• Azuma H, Paulk N, Ranade A, et al. (2007). Robust expansion of human hepatocytes in Fah(-/-)/Rag2(-/-)/Il2rg(-/-) mice. Nat Biotechnol 25:903–10
   PubMed Web of Science ®Google Scholar
• Bailey J. (2005). Nonhuman primates in medical research and drug development: a critical review. Biogenic Amines 19:235–55
   Google Scholar
• Baillie TA, Cayen MN, Fouda H, et al. (2002). Drug metabolites in safety testing. Toxicol Appl Pharmacol 182:188–96
   PubMed Web of Science ®Google Scholar
• Bischoff KB. (1986). Physiological pharmacokinetics. Bull Math Biol 48:309–22
   PubMed Web of Science ®Google Scholar
• Bissig KD, Le TT, Woods NB, Verma IM. (2007). Repopulation of adult and neonatal mice with human hepatocytes: a chimeric animal model. Proc Natl Acad Sci USA 104:20507–11
   PubMed Web of Science ®Google Scholar
• Bissig KD, Wieland SF, Tran P, et al. (2010). Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment. J Clin Invest 120:924–30
   PubMed Web of Science ®Google Scholar
• Blight KJ, Kolykhalov AA, Rice CM. (2000). Efficient initiation of HCV RNA replication in cell culture. Science 290:1972–4
   PubMed Web of Science ®Google Scholar
• Bošnjak S. (2001). The Declaration of Helsinki—the cornerstone of research ethics. Arch Oncol 9:179–84
   Google Scholar
• Bussiere JL. (2008). Species selection considerations for preclinical toxicology studies for biotherapeutics. Exp Opin Drug Metab Toxicol 4:871–7
   PubMed Web of Science ®Google Scholar
• Carlile DJ, Zomorodi K, Houston JB. (1997). Scaling factors to relate drug metabolic clearance in hepatic microsomes, isolated hepatocytes, and the intact liver: studies with induced livers involving diazepam. Drug Metab Dispos 25:903–11
   PubMed Web of Science ®Google Scholar
• Cavagnaro JA. (2008). Preclinical safety evaluation of biopharmaceuticals. A science-based approach to facilitating clinical trials. Hoboken (NJ): John-Wiley & Sons
   Google Scholar
• Chappell WR, Mordenti J. (1991). Extrapolation of toxicological and pharmacological data from animals to humans. In: Testa B, ed. Advances in drug research, vol. 20. San Diego (CA): Academic Press Inc., 1–116
   Google Scholar
• Chaturvedi PR, Decker CJ, Odinecs A. (2001). Prediction of pharmacokinetic properties using experimental approaches during early drug discovery. Curr Opin Chem Biol 5:452–63
   PubMed Web of Science ®Google Scholar
• Chayama K, Hayes CN, Hiraga N, et al. (2011). Animal model for study of human hepatitis viruses. J Gastroenterol Hepatol 26:13–18
   PubMed Web of Science ®Google Scholar
• Chen AA, Thomas DK, Onga LL, et al. (2011). Humanized mice with ectopic artificial liver tissues. Proc Natl Acad Sci USA 108:11842–7
   PubMed Web of Science ®Google Scholar
• Cheung C, Gonzalez FJ. (2008). Humanized mouse lines and their application for prediction of human drug metabolism and toxicological risk assessment. J Pharmacol Exp Ther 327:288–99
   PubMed Web of Science ®Google Scholar
• Corchero J, Granvil CP, Akiyama TE, et al. (2001). The CYP2D6 humanized mouse: effect of the human CYP2D6 transgene and HNF4alpha on the disposition of debrisoquine in the mouse. Mol Pharmacol 60:1260–7
   PubMed Web of Science ®Google Scholar
• Dalvie D, Obach RS, Kang P, et al. (2009). Assessment of three human in vitro systems in the generation of major human excretory and circulating metabolites. Chem Res Toxicol 22:357–68
   PubMed Web of Science ®Google Scholar
• Daly AK, Day CP. (2012). Genetic association studies in drug-induced liver injury. Drug Metab Rev 44:116–26
   PubMed Web of Science ®Google Scholar
• Dandri M, Burda MR, Török E, et al. (2001). Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 33:981–8
   PubMed Web of Science ®Google Scholar
• Dandri M, Petersen J. (2012). Chimeric mouse model of hepatitis B virus infection. J Hepatol 56:493–5
   PubMedGoogle Scholar
• De Buck SS, Sinha VK, Fenu LA, et al. (2007). Prediction of human pharmacokinetics using physiologically based modeling: a retrospective analysis of 26 clinically tested drugs. Drug Metab Dispos 35:1766–80
   PubMed Web of Science ®Google Scholar
• De Serres M, Bowers G, Boyle G, et al. (2011). Evaluation of a chimeric (uPA+/+)/SCID mouse model with a humanized liver for prediction of human metabolism. Xenobiotica 41:464–75
   PubMed Web of Science ®Google Scholar
• Dimberg LY, Anderson CK, Camidge R, et al. (2013). On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene 32:1341–50
   PubMed Web of Science ®Google Scholar
• Dixon RL. (1976). Problems in extrapolating toxicity data for laboratory animals to man. Environ Hlth Perspect 13:43–50
   PubMed Web of Science ®Google Scholar
• Drenth JPH. (2013). HCV treatment – no more room for interferonologists? N Engl J Med 368:1931–2
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. (2009). ICH guideline M3(R2) on non-clinical safety studies for the conduct of human clinical trials and marketing authorisation for pharmaceuticals. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500002720.pdf [last accessed 29 May 2013]
   Google Scholar
• European Medicines Agency. (2007). Guideline on requirements for first-in-man clinical trials for potential high-risk medicinal products. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500002989.pdf Doc. Ref.EMEA/CHMP/SWP/28367/2007 Corr. [last accessed on 8 August 2013]
   Google Scholar
• Faustman EM, Omenn GS. (2008). Risk assessment. In: Klaassen CD, ed. Casarett and Doull’s toxicology. The basic science of poisons. New York: McGraw-Hill, 107–28
   Google Scholar
• Foster JR, Jacobsen M, Kenna G, et al. (2012). Differential effect of troglitazone on the human bile acid transporters, MRP2 and BSEP, in the PXB hepatic chimeric mouse. Toxicol Pathol 40:1106–16
   PubMed Web of Science ®Google Scholar
• Goldstein RS, Drukker M, Reubinoff BE, et al. (2002). Integration and differentiation of human embryonic stem cells transplanted to the chick embryo. Dev Dyn 225:80–6
   PubMed Web of Science ®Google Scholar
• Hao C, Song JH, Hsi B, et al. (2004). TRAIL inhibits tumor growth but is nontoxic to human hepatocytes in chimeric mice. Cancer Res 64:8502–6
   PubMed Web of Science ®Google Scholar
• Hasegawa M, Kawai K, Mitsui T, et al. (2011). The reconstituted 'humanized liver' in TK-NOG mice is mature and functional. Biochem Biophys Res Commun 405:405–10
   PubMed Web of Science ®Google Scholar
• Hasegawa M, Tahara H, Inoue R, et al. (2012). Investigation of drug-drug interactions caused by human pregnane X receptor-mediated induction of CYP3A4 and CYP2C subfamilies in chimeric mice with a humanized liver. Drug Metab Dispos 40:474–80
   PubMed Web of Science ®Google Scholar
• Heckel JL, Sandgren EP, Degen JL, et al. (1990). Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 62:447–56
   PubMed Web of Science ®Google Scholar
• Higuchi Y, Kawai K, Yamazaki H, et al. (2013). The human hepatic cell line HepaRG as a possible cell source for the generation of humanized liver TK-NOG mice. Xenobiotica. [Epub ahead of print]. doi: 10.3109/00498254.2013.836257
   PubMed Web of Science ®Google Scholar
• Hiraga N, Imamura M, Hatakeyama T, et al. (2009). Absence of viral interference and different susceptibility to interferon between hepatitis B virus and hepatitis C virus in human hepatocyte chimeric mice. J Hepatol 51:1046–54
   PubMed Web of Science ®Google Scholar
• Holme E, Lindstedt S. (1998). Tyrosinaemia type I and NTBC (2 -(2-nitro-4-trifluoromethylbenzoyl)-1,3-cyclohexanedione). J Inherit Metab Dis 21:507–17
   PubMed Web of Science ®Google Scholar
• Holt MP, Ju C. (2006). Mechanisms of drug-induced liver injury. AAPS J 8:E48–54
   PubMed Web of Science ®Google Scholar
• Houston BJ, Carlile DJ. (1997). Prediction of hepatic clearance from microsomes, hepatocytes and liver slices. Drug Metab Rev 29: 891–922
   PubMed Web of Science ®Google Scholar
• Houston JB. (1994). Utility of in vitro drug metabolism data in predicting in vivo metabolic clearance. Biochem Pharmacol 47:1469–79
   PubMed Web of Science ®Google Scholar
• Hu Y, Wu M, Nishimura T, et al. (2013). Human pharmacogenetic analysis in chimeric mice with ‘humanized livers’. Pharmacokinet Genomics 23:78–83
   PubMed Web of Science ®Google Scholar
• Hussaini SH, Farrington EA. (2007). Idiosyncratic drug-induced liver injury: an overview. Expert Opin Drug Saf 6: 673–84
   PubMed Web of Science ®Google Scholar
• Igarashi Y, Tateno C, Tanaka Y, et al. (2008). Engraftment of human hepatocytes in the livers of rats reconstructed with bone marrow cells from an immunodeficient mouse. Xenotransplant 15:235–45
   PubMed Web of Science ®Google Scholar
• Inoue T, Nitta K, Sugihara K, et al. (2008). CYP2C9-catalyzed metabolism of (S)-warfarin to 7-hydroxywarfarin in vivo and in vitro in chimeric mice with humanized liver. Drug Metab Dispos 36:2429–33
   PubMed Web of Science ®Google Scholar
• Inoue T, Sugihara K, Ohshita H, et al. (2009). Prediction of human disposition toward S-3 H-Warfarin using chimeric mice with humanized liver. Drug Metab Pharmacokinet 24:153–60
   PubMed Web of Science ®Google Scholar
• International Conference on Harmonisation. (2009). ICH guideline M3(R2) – guidance on nonclinical safety studies for the conduct of human clinical trials and marketing authorisation for pharmaceuticals. Available from: http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Multidisciplinary/M3_R2/Step4/M3_R2__Guideline.pdf
   Google Scholar
• International Conference on Harmonisation. (2011). ICH guideline S6 (R1) – preclinical safety evaluation of biotechnology-derived pharmaceuticals. Available from: http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Safety/S6_R1/Step4/S6_R1_Guideline.pdf
   Google Scholar
• Jemnitz K, Veres Z, Monostory K, et al. (2008). Interspecies differences in acetaminophen sensitivity of human, rat and mouse primary hepatocytes. Toxicol In Vitro 22:961–7
   PubMed Web of Science ®Google Scholar
• Jiang L, Li JG, Lan L, et al. (2010). Human hepatoma HepaRG cell line engraftment in severe combined immunodeficient × beige mice using mouse-specific anti-Fas antibody. Transplant Proc 42:3773–8
   PubMed Web of Science ®Google Scholar
• Jo M, Kim TH, Seol DW, et al. (2000). Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat Med 6:564–7
   PubMed Web of Science ®Google Scholar
• Kakuni M, Morita M, Matsuo K, et al. (2012). Chimeric mice with a humanized liver as an animal model of troglitazone-induced liver injury. Toxicol Lett 214:9–18
   PubMed Web of Science ®Google Scholar
• Kamimura H, Nakada N, Suzuki K, et al. (2010). Assessment of chimeric mice with humanized liver as a tool for predicting circulating human metabolites. Drug Metab Pharmacokinet 25:223–35
   PubMed Web of Science ®Google Scholar
• Kaplowitz N. (2004). Drug-induced liver injury. Clin Infect Dis 38:S44–8
   PubMed Web of Science ®Google Scholar
• Katoh M, Matsui T, Okumura H, et al. (2005). Expression of human phase II enzymes in chimeric mice with humanized liver. Drug Metab Dispos 33:1333–40
   PubMed Web of Science ®Google Scholar
• Katoh M, Yokoi T. (2007). Application of chimeric mice with humanized liver for predictive ADME. Drug Metab Rev 39:145–57
   PubMed Web of Science ®Google Scholar
• Katoh M, Sawada T, Soeno Y, et al. (2007). In vivo drug metabolism model for human cytochrome P450 enzyme using chimeric mice with humanized liver. J Pharm Sci 96:428–37
   PubMed Web of Science ®Google Scholar
• Kneteman NM, Weiner AJ, O'Connell J, et al. (2006). Anti-HCV therapies in chimeric scid-Alb/uPA mice parallel outcomes in human clinical application. Hepatology 43:1346–53
   PubMed Web of Science ®Google Scholar
• Kneteman NM, Howe AYM, Gao T, et al. (2009). HCV796: A selective nonstructural protein 5B polymerase inhibitor with potent anti-hepatitis C virus activity In Vitro, in mice with chimeric human livers, and in humans infected with hepatitis C virus. Hepatology 49:745–52
   PubMed Web of Science ®Google Scholar
• Knight A. (2008). The beginning of the end for chimpanzee experiments? Philos Ethics Humanit Med 3:16
   PubMedGoogle Scholar
• Lavé T, Coassolo P, Reigner B. (1999). Prediction of hepatic metabolic clearance based on interspecies allometric scaling techniques and in vitro-in vivo correlations. Clin Pharmacokinet 36:211–31
   PubMed Web of Science ®Google Scholar
• Law M, Maruyama T, Lewis J, et al. (2008). Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 14:25–7
   PubMed Web of Science ®Google Scholar
• Lindstedt S, Holme E, Lock EA, et al. (1992). Treatment of hereditary tyrosinaemia type I by inhibition of 4-hydroxyphenylpyruvate dioxygenase. Lancet 340:813–17
   PubMed Web of Science ®Google Scholar
• Lohmann V, Körner F, Koch J-O, et al. (1999). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110–13
   PubMed Web of Science ®Google Scholar
• Lootens L, Meuleman P, Pozo OJ, et al. (2009a). uPA+/+-SCID mouse with humanized liver as a model for in vivo metabolism of exogenous steroids: methandienone as a case study. Clin Chem 55:1783–93
   PubMed Web of Science ®Google Scholar
• Lootens L, Van Eenoo P, Meuleman P, et al. (2009b). The uPA(+/+)-SCID mouse with humanized liver as a model for in vivo metabolism of 4-androstene-3,17-dione. Drug Metab Dispos 37:2367–74
   PubMed Web of Science ®Google Scholar
• Lootens L, Meuleman P, Leroux-Roels G, et al. (2011). Metabolic studies with promagnon, methylclostebol and methasterone in the uPA+/+-SCID chimeric mice. J Steroid Biochem Mol Biol 127:374–81
   PubMed Web of Science ®Google Scholar
• Lütgehetmann M, Mancke LV, Volz T, et al. (2012). Humanized chimeric uPA mouse model for the study of hepatitis B and D virus interactions and preclinical drug evaluation. Hepatology 55:685–94
   PubMed Web of Science ®Google Scholar
• Matsuura Y, Yagi H, Matsuda S, et al. (2011). Human liver-specific nanocarrier in a novel mouse xenograft model bearing noncancerous human liver tissue. Eur Surg Res 46:65–72
   PubMed Web of Science ®Google Scholar
• McKinnon RA, Nebert DW. (1998). Cytochrome P450 knockout mice: new toxicological models. Clin Exp Pharmacol Physiol 25:783–7
   PubMed Web of Science ®Google Scholar
• Mercer DF, Schiller DE, Elliott JF, et al. (2001). Hepatitis C virus replication in mice with chimeric human livers. Nat Med 7:927–33
   PubMed Web of Science ®Google Scholar
• Meuleman P, Libbrecht L, De Vos R, et al. (2005). Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 41:847–56
   PubMed Web of Science ®Google Scholar
• Meuleman P, Leroux-Roels G. (2008). The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res 80: 231–8
   PubMed Web of Science ®Google Scholar
• Milton MN, Horvath CJ. (2009). The EMEA guideline on first-in-human clinical trials and its impact on pharmaceutical development. Toxicol Pathol 37:363–71
   PubMed Web of Science ®Google Scholar
• Morosan S, Hez-Deroubaix S, Lunel F, et al. (2006). Liver-stage development of Plasmodium falciparum in a humanized mouse model. J Infect Dis 193:996–1004
   PubMed Web of Science ®Google Scholar
• Muruganandan S, Sinal CJ. (2008). Mice as clinically relevant models for the study of cytochrome P450-dependent metabolism. Clin Pharmacol Ther 83:818–28
   PubMed Web of Science ®Google Scholar
• Nishimura M, Yoshitsugu H, Yokoi T, et al. (2005). Evaluation of mRNA expression of human drug-metabolizing enzymes and transporters in chimeric mouse with humanized liver. Xenobiotica 35:877–90
   PubMed Web of Science ®Google Scholar
• Nishimura T, Hu Y, Wu M, et al. (2013). Using chimeric mice with humanized livers to predict human drug metabolism and a drug–drug interaction. J Pharmacol Exp Ther 344:388–96
   PubMed Web of Science ®Google Scholar
• Obach RS, Baxter JG, Liston TE, et al. (1997). The prediction of human pharmacokinetic parameters from preclinical and in vitro metabolism data. J Pharmacol Exp Ther 283:46–58
   PubMed Web of Science ®Google Scholar
• OECD. (2011). 40 Years of chemical safety at the OECD: quality and efficiency. Available from: http://www.oecd.org/env/ehs/48153344.pdf [last accessed 28 May 2013]
   Google Scholar
• Okumura H, Katoh M, Sawada T, et al. (2007). Humanization of excretory pathway in chimeric mice with humanized liver. Toxicol Sci 97:533–8
   PubMed Web of Science ®Google Scholar
• Ourednik V, Ourednik J, Flax JD, et al. (2001). Segregation of human neural stem cells in the developing primate forebrain. Science 293:1820–4
   PubMed Web of Science ®Google Scholar
• Ouyang EC, Wu CH, Walton C, et al. (2001). Transplantation of human hepatocytes into tolerized genetically immunocompetent rats. World J Gastroenterol 7:324–30
   PubMed Web of Science ®Google Scholar
• Pajvani UB, Trujillo ME, Combs TP, et al. (2005). Fat apoptosis through targeted activation of caspase 8: a new mouse model of inducible and reversible lipoatrophy. Nat Med 11:797–803
   PubMed Web of Science ®Google Scholar
• Peltz G. (2013). Can ‘humanized’ mice improve drug development in the 21st century? Trends Pharmacol Sci 34:255–60
   PubMed Web of Science ®Google Scholar
• Poulin P, Schoenlein K, Theil F-P. (2001). Prediction of adipose tissue: plasma partition coefficients for structurally unrelated drugs. J Pharmaceut Sci 90:436–47
   PubMed Web of Science ®Google Scholar
• Poulin P, Theil F-P. (2002). Prediction of pharmacokinetics prior to in vivo studies.1. Mechanism-based prediction of volume of distribution. J Pharmaceut Sci 91:129–56
   PubMed Web of Science ®Google Scholar
• Pozo OJ, Van Eenoo P, Deventer K, et al. (2009a). Detection and structural investigation of metabolites of stanozolol in human urine by liquid chromatography tandem mass spectrometry. Steroids 74:837–52
   PubMed Web of Science ®Google Scholar
• Pozo OJ, Van Eenoo P, Deventer K, et al. (2009b). Detection and characterization of a new metabolite of 17α-methyltestosterone. Drug Metab Dispos 37:2153–62
   PubMed Web of Science ®Google Scholar
• Pybus BS, Marcsisin SR, Jin X, et al. (2013). The metabolism of primaquine to its active metabolite is dependent on CYP 2D6. Malaria J 12:212
   PubMed Web of Science ®Google Scholar
• Rahmani R, Richard B, Fabre G, et al. (1988). Extrapolation of preclinical pharmacokinetic data to therapeutical drug use. Xenobiotica 18:71–8
   PubMed Web of Science ®Google Scholar
• Rhim JA, Sandgren EP, Degen JL, et al. (1994). Replacement of diseased mouse liver by hepatic cell transplantation. Science 263:1149–52
   PubMed Web of Science ®Google Scholar
• Rhim JA, Sandgren EP, Palmiter RD, et al. (1995). Complete reconstitution of mouse liver with xenogeneic hepatocytes. Proc Natl Acad Sci USA 92:4942–6
   PubMed Web of Science ®Google Scholar
• Robinet E, Baumert TF. (2011). A first step towards a mouse model for hepatitis C virus infection containing a human immune system. J Hepatol 55:718–20
   PubMed Web of Science ®Google Scholar
• Rodgers T, Leahy D, Rowland M. (2005). Physiologically based pharmacokinetic modeling 1: Predicting the tissue distribution of moderate-to-strong bases. J Pharmaceut Sci 94:1259–76
   PubMed Web of Science ®Google Scholar
• Sacci JB Jr, Alam U, Douglas D, et al. (2006). Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. Int J Parasitol 36:353–60
   PubMed Web of Science ®Google Scholar
• Samuelsson K, Pickup K, Sarda S, et al. (2012). Pharmacokinetics and metabolism of midazolam in chimeric mice with humanized livers. Xenobiotica 42:1128–37
   PubMed Web of Science ®Google Scholar
• Sandgren EP, Palmiter RD, Heckel JL, et al. (1991). Complete hepatic regeneration after somatic deletion of an albumin-plasminogen activator transgene. Cell 66:245–56
   PubMed Web of Science ®Google Scholar
• Sanoh S, Horiguchi A, Sugihara K, et al. (2012a). Prediction of in vivo hepatic clearance and half-life of drug candidates in human using chimeric mice with humanized liver. Drug Metab Dispos 40:322–8
   PubMed Web of Science ®Google Scholar
• Sanoh S, Horiguchi A, Sugihara K, et al. (2012b). Predictability of metabolism of ibuprofen and naproxen using chimeric mice with human hepatocytes. Drug Metab Dispos 40:2267–72
   PubMed Web of Science ®Google Scholar
• Sanoh S, Nozaki K, Murai H, et al. (2012c). Prediction of human metabolism of FK3453 by aldehyde oxidase using chimeric mice transplanted with human or rat hepatocytes. Drug Metab Dispos 40:76–82
   PubMed Web of Science ®Google Scholar
• Sato Y, Yamada H, Iwasaki K, et al. (2008). Human hepatocytes can repopulate mouse liver: histopathology of the liver in human hepatocyte-transplanted chimeric mice and toxicologic responses to acetaminophen. Toxicol Pathol 36:581–91
   PubMed Web of Science ®Google Scholar
• Schulz-Utermoehl T, Sarda S, Foster JR, et al. (2012). Evaluation of the pharmacokinetics, biotransformation and hepatic transporter effects of troglitazone in mice with humanized livers. Xenobiotica 42:503–17
   PubMed Web of Science ®Google Scholar
• Shanks N, Greek R, Greek J. (2009). Are animal models predictive for humans? Philos Ethics Humanit Med 4:2
   PubMedGoogle Scholar
• Shoda J, Okada K, Inada Y, et al. (2007). Bezafibrate induces multidrug-resistance P-glycoprotein 3 expression in cultured human hepatocytes and humanized livers of chimeric mice. Hepatol Res 37:548–56
   PubMed Web of Science ®Google Scholar
• Smith D, Combes R, Depelchin O, et al. (2005). Optimising the design of preliminary toxicity studies for pharmaceutical safety testing in the dog. Toxicol Pharmacol 41:95–101
   Google Scholar
• Steenbergen RHG, Joyce MA, Lund G, et al. (2010). Lipoprotein profiles in SCID/uPA mice transplanted with human hepatocytes become human-like and correlate with HCV infection success. Am J Physiol Gastrointest Liver Physiol 299:G844–54
   Web of Science ®Google Scholar
• Strom SC, Davila J, Grompe M. (2010). Chimeric mice with humanized liver: tools for the study of drug metabolism, excretion, and toxicity. Methods Mol Biol 640:491–509
   PubMedGoogle Scholar
• Suemizu H, Hasegawa M, Kawai K, et al. (2008). Establishment of a humanized model of liver using NOD/Shi-scid IL2Rgnull mice. Biochem Biophys Res Commun 377:248–52
   PubMed Web of Science ®Google Scholar
• Tachibana A, Tateno C, Yoshizato K. (2013). Repopulation of the immunosuppressed retrorsine-treated infant rat liver with human hepatocytes. Xenotransplant 20:227–38
   PubMed Web of Science ®Google Scholar
• Tatematsu K, Tanaka Y, Sugiyama M, et al. (2011). Host sphingolipid biosynthesis is a promising therapeutic target for the inhibition of hepatitis B virus replication. J Med Virol 83:587–93
   PubMed Web of Science ®Google Scholar
• Tateno C, Miya F, Wake K, et al. (2013). Morphological and microarray analyses of human hepatocytes from xenogeneic host livers. Lab Invest 93:54–71
   PubMed Web of Science ®Google Scholar
• Tateno C, Yoshizane Y, Saito N, et al. (2004). Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol 165:901–12
   PubMed Web of Science ®Google Scholar
• Theil F-P, Guentert TW, Haddad S, et al. (2003). Utility of physiologically based pharmacokinetic models to drug development and rational drug discovery candidate selection. Toxicol Lett 138:29–49
   PubMed Web of Science ®Google Scholar
• Tsukada A, Suemizu H, Murayama N, et al. (2013). Plasma concentrations of melengestrol acetate in humans extrapolated from the pharmacokinetics established in in vivo experiments with rats and chimeric mice with humanized liver and physiologically based pharmacokinetic modeling. Regul Toxicol Pharmacol 65:316–24
   PubMed Web of Science ®Google Scholar
• Van Buskirk KM, O'Neill MT, De La Vega P, et al. (2009). Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc Natl Acad Sci USA 106:13004–9
   PubMed Web of Science ®Google Scholar
• van den Brink MR, Hunt LE, Hiserodt JC. (1990). In vivo treatment with monoclonal antibody 3.2.3 selectively eliminates natural killer cells in rat. J Exp Med 171:197–210
   PubMed Web of Science ®Google Scholar
• van Rooijen N, Sanders A. (1994). Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83–93
   PubMed Web of Science ®Google Scholar
• Vaughan AM, Mikolajczak SA, Wilson EM, et al. (2012). Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J Clin Invest 122:3618–28
   PubMed Web of Science ®Google Scholar
• Volz T, Lütgehetmann M, Allweiss L, et al. (2012). Strong antiviral activity of the new L-hydroxycytidine derivative, L-Hyd4FC, in HBV-infected human chimeric uPA/SCID mice. Antivir Ther 17:623–31
   PubMed Web of Science ®Google Scholar
• Volz T, Allweiss LM, ḾBarek MB, et al. (2013). The entry inhibitor Myrcludex-B efficiently blocks intrahepatic virus spreading in humanized mice previously infected with hepatitis B virus. J Hepatol 58:861–7
   PubMed Web of Science ®Google Scholar
• Wakita T, Pietschmann T, Kato T, et al. (2005). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791–6
   PubMed Web of Science ®Google Scholar
• Walczak H, Miller RE, Ariail K, et al. (1999). Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5:157–63
   PubMed Web of Science ®Google Scholar
• Washburn ML, Bility MT, Zhang L, et al. (2011). A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 140:1334–44
   PubMed Web of Science ®Google Scholar
• Willmann S, Schmitt W, Keldenich J, et al. (2004). A physiological model for the estimation of the fraction dose absorbed in humans. J Med Chem 47:4022–31
   PubMed Web of Science ®Google Scholar
• Wong H, Grossman SJ, Bai SA, et al. (2004). The chimpanzee (Pan troglodytes) as a pharmacokinetic model for selection of drug candidates: model characterization and application. Drug Metab Dispos 32:1359–69
   PubMed Web of Science ®Google Scholar
• Wu CH, Ouyang EC, Walton C, et al. (2001). Human hepatocytes transplanted into genetically immunocompetent rats are susceptible to infection by hepatitis B virus in situ. J Viral Hepat 8:111–19
   PubMed Web of Science ®Google Scholar
• Wu GY, Konishi M, Walton CM, et al. (2005). A novel immunocompetent rat model of HCV infection and hepatitis. Gastroenterology 128:1416–23
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Suemizu H, Murayama N, et al. (2013). In vivo drug interactions of the teratogen thalidomide with midazolam: heterotropic cooperativity of human cytochrome P450 in humanized TK-NOG mice. Chem Res Toxicol 26:486–9
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Suemizu H, Igaya S, et al. (2012). In vivo formation of a glutathione conjugate derived from thalidomide in humanized uPA-NOG mice. Chem Res Toxicol 24:287–9
   Web of Science ®Google Scholar
• Yoshizato K, Tateno C. (2009). A human hepatocyte-bearing mouse: an animal model to predict drug metabolism and effectiveness in humans. PPAR Res 2009:476217
   Google Scholar
• Zülke U, Weinbauer G. (2003). The common marmoset (Callithrix jacchus) as a model in toxicology. Toxicol Pathol 31:123–7
   PubMedGoogle Scholar