398
Views
18
CrossRef citations to date
0
Altmetric
Reviews

A mouse with humanized liver as an animal model for predicting drug effects and for studying hepatic viral infection: where to next?

(Professor Emeritus, Academic Adviser) & (Professor Emeritus, Academic Adviser)
Pages 1419-1435 | Published online: 27 Aug 2013

Bibliography

  • Hyodo K, Yamamoto E, Suzuki T, et al. Development of liposomal anticancer drugs. Biol Pharm Bull 2013;36(5):703-7
  • Sun H, Xia M, Austin CP, Huang R. Paradigm shift in toxicity testing and modeling. AAPS J 2012;14(3):473-80
  • Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 2004;3:711-15
  • Dr. Sugai, S in personal communication
  • Renaud HJ, Cui JY, Khan M, Klaassen CD. Tissue distribution and gender-divergent expression of 78 cytochrome P450 mRNAs in mice. Toxicol Sci 2011;124:261-77
  • Wilkinson GR. Drug metabolism and variability among patients in drug response. N Engl J Med 2005;352:2211-21; Review
  • Jiang XL, Gonzalez FJ, Yu AM. Drug-metabolizing enzyme, transporter, and nuclear receptor genetically modified mouse models. Drug Metab Rev 2011;43:27-40
  • Liggett SB. Genetically modified mouse models for pharmacogenomic research. Nat Rev Genet 2004;5:657-63; Review
  • Muruganandan S, Sinal CJ. Mice as clinically relevant models for the study of cytochrome P450-dependent metabolism. Clin Pharmacol Ther 2008;83:818-28
  • Dandri M, Burda MR, Török E, et al. Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 2001;33:981-8
  • Mercer DF, Schiller DE, Elliott JF, et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001;7:927-33
  • Tateno C, Yoshizane Y, Saito N, et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol 2004;165:901-12
  • Yoshizato K, Tateno C. In vivo modeling of human liver for pharmacological study using humanized mouse. Expert Opin Drug Metab Toxicol 2009;5:1435-46; Review
  • Yoshizato K, Tateno C, Utoh R. The mechanism of liver size control in mammals: a novel animal study. Int J Des Nature Ecodynamics 2009;4:123-42
  • Yoshizato K, Tateno C. A human hepatocyte-bearing mouse: an animal model to predict drug metabolism and effectiveness in humans. PPAR Res 2009;2009:476217
  • 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(1):63-76
  • Sandgren EP, Degen JL, Palmiter RD, et al. Replacement of diseased mouse liver by hepatic cell transplantation. Science 1994;263:1149-52
  • Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983;301:527-30
  • Schatz DG. Antigen receptor genes and the evolution of a recombinase. Semin Immunol 2004;16:245-56
  • Azuma H, Paulk N, Ranade A, et al. Robust expansion of human hepatocytes in Fah(–/–)/Rag2(–/–)/Il2rg(–/–) mice. Nat Biotechnol 2007;25:903-10
  • Traggiai E, Chicha L, Mazzucchelli L, et al. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 2004;304:104-7
  • Gorantla S, Sneller H, Walters L, et al. Human immunodeficiency virus type 1 pathobiology studied in humanized BALB/c-Rag2-/-gammac-/- mice. J Virol 2007;81:2700-12
  • Shinkai Y, Rathbun G, Lam KP, et al. RAG-2–deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 1992;68:855-67
  • Perryman LE. Molecular pathology of severe combined immunodeficiency in mice, horses, and dogs. Vet Pathol 2004;41:95-100
  • Bosma MJ, Carroll AM. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol 1991;9:323-50; Review
  • Suemizu H, Hasegawa M, Kawai K, et al. Establishment of a humanized model of liver using NOD/Shi-scid IL2Rgnull mice. Biochem Biophys Res Commun 2008;377:248-52
  • Kikutani H, Makino S. The murine autoimmune diabetes model: NOD and related strains. Adv Immunol 1992;51:285-322
  • Ohbo K, Suda T, Hashiyama M, et al. Modulation of hematopoiesis in mice with a truncated mutant of the interleukin-2 receptor gamma chain. Blood 1996;87:956-67
  • Heckel JL, Sandgren EP, Dege JL, et al. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 1990;62:447-56
  • Mohammed FF, Pennington CJ, Kassiri Z, et al. Metalloproteinase inhibitor TIMP-1 affects hepatocyte cell cycle via HGF activation in murine liver regeneration. Hepatology 2005;41:857-67
  • Bissig KD, Le TT, Woods NB, Verma IM. Repopulation of adult and neonatal mice with human hepatocytes: a chimeric animal model. Proc Natl Acad Sci USA 2007;104:20507-11
  • Grompe M, et al. Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev 1993;7:2298-307
  • Brezillon NM, DaSilva L, L'Hôte D, et al. Rescue of fertility in homozygous mice for the urokinase plasminogen activator transgene by the transplantation of mouse hepatocytes. Cell Transplant 2008;17:803-12
  • Sandgren EP, Palmiter RD, Heckel JL, et al. Complete hepatic regeneration after somatic deletion of an albumin-plasminogen activator transgene. Cell 1991;66:245-56
  • Okamura K, Asahina K, Fujimori H, et al. Generation of hybrid hepatocytes by cell fusion from monkey embryoid body cells in the injured mouse liver. Histochem Cell Biol 2006;125:247-57
  • Tateno C, Miya F, Wake K, et al. Morphological and microarray analyses of human hepatocytes from xenogeneic host livers. Lab Invest 2013;93(1):54-71
  • Lootens L, Meuleman P, Pozo OJ, et al. uPA+/+-SCID mouse with humanized liver as a model for in vivo metabolism of exogenous steroids: methandienone as a case study. Clin Chem 2009;55:1783-93
  • Okumura H, Katoh M, Sawada T, et al. Humanization of excretory pathway in chimeric mice with humanized liver. Toxicol Sci 2007;97:533-8
  • Botrè F. Humanized animal models to study drug metabolism: no longer a “chimera”? Clin Chem 2009;55(10):1763-4
  • Lootens L, Van Eenoo P, Meuleman P, et al. The uPA(+/+)-SCID mouse with humanized liver as a model for in vivo metabolism of 4-androstene-3,17-dione. Drug Metab Dispos 2009;37:2367-74
  • Dai Y, Su W, Ding Z, et al. Mehta JL. Regulation of MSR-1 and CD36 in macrophages by LOX-1 mediated through PPAR-γ. Biochem Biophys Res Commun 2013; [Epub ahead of print]
  • Schulz-Utermoehl T, Sarda S, Foster JR, et al. Evaluation of the pharmacokinetics, biotransformation and hepatic transporter effects of troglitazone in mice with humanized livers. Xenobiotica 2012;42(6):503-17
  • Sanoh S, Horiguchi A, Sugihara K, et al. Predictability of metabolism of ibuprofen and naproxen using chimeric mice with human hepatocytes. Drug Metab Dispos 2012;40(12):2267-72
  • Sanoh S, Horiguchi A, Sugihara K, et al. Prediction of in vivo hepatic clearance and half-life of drug candidates in human using chimeric mice with humanized liver. Drug Metab Dispos 2012;40(2):322-8
  • Garattini E, Mendel R, Romão MJ, et al. Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology. Biochem J 2003;372(Pt 1):15-32; Review
  • Sanoh S, Nozaki K, Murai H, et al. Prediction of human metabolism of FK3453 by aldehyde oxidase using chimeric mice transplanted with human or rat hepatocytes. Drug Metab Dispos 2012;40(1):76-82
  • Pryde DC, Dalvie D, Hu Q, et al. Aldehyde oxidase: an enzyme of emerging importance in drug discovery. J Med Chem 2010;53:8441-60
  • Garattini E, Terao M. Increasing recognition of the importance of aldehyde oxidase in drug development and discovery. Drug Metab Rev 2011;43:374-86
  • Akabane T, Tanaka K, Irie M, et al. Case report of extensive metabolism by aldehyde oxidase in humans: pharmacokinetics and metabolite profile of FK3453 in rats, dogs, and humans. Xenobiotica 2011;41:372-84
  • Brunner C, Muller B, Wirth T. Bruton's tyrosine kinase is involved in innate and adaptive immunity. Histol Histopathol 2005;20:945-55
  • Pan Z. Bruton's tyrosine kinase as a drug discovery target. Drug News Perspect 2008;21:357-62
  • Liu L, Di Paolo J, Barbosa J, et al. Antiarthritis effect of a novel Bruton's tyrosine kinase (BTK) inhibitor in rat collagen-induced arthritis and mechanism based pharmacokinetic/pharmacodynamic modeling: relationships between inhibition of BTK phosphorylation and efficacy. J Pharmacol Exp Ther 2011;338:154-63
  • Liu L, Halladay JS, Shin Y, et al. Significant species difference in amide hydrolysis of GDC-0834, a novel potent and selective Bruton's tyrosine kinase inhibitor. Drug Metab Dispos 2011;39(10):1840-9
  • Ploss A, Rice CM. Towards a small animal model for hepatitis C. EMBO Rep 2009;10:1220-7
  • Uprichard SL, Chung J, Chisari FV, Wakita T. Replication of a hepatitis C virus replicon clone in mouse cells. Virol J 2006;3:89
  • Wakita T, Pietschmann T, Kato T, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005;11:791-6
  • Bissig KD, Wieland SF, Tran P, et al. Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment. J Clin Invest 2010;120:924-30
  • Tsuge M, Hiraga N, Takaishi H, et al. Yoshizato K. nfection of human hepatocyte chimeric mouse with genetically engineered hepatitis B virus. Hepatology 2005;42(5):1046-54
  • Kimura T, Imamura M, Hiraga N, et al. Establishment of an infectious genotype 1b hepatitis C virus clone in human hepatocyte chimeric mice. J Gen Virol 2008;89(Pt 9):2108-13
  • Kamiya N, Iwao E, Hiraga N, et al. Practical evaluation of a mouse with chimeric human liver model for hepatitis C virus infection using an NS3-4A protease inhibitor. J Gen Virol 2010;91(Pt 7):1668-77
  • Ohara E, Hiraga N, Imamura M, et al. Elimination of hepatitis C virus by short term NS3-4A and NS5B inhibitor combination therapy in human hepatocyte chimeric mice. J Hepatol 2011;54(5):872-8
  • Abe H, Imamura M, Hiraga N, et al. ME3738 enhances the effect of interferon and inhibits hepatitis C virus replication both in vitro and in vivo. J Hepatol 2011;55(1):11-18
  • Perni RB, Almquist SJ, Byrn RA, et al. Preclinical profile of VX-950, a potent, selective, and orally bioavailable inhibitor of hepatitis C virus NS3-4A serine protease. Antimicrob Agents Chemother 2006;50:899-909
  • Hiraga N, Imamura M, Abe H, et al. Rapid emergence of telaprevir resistant hepatitis C virus strain from wildtype clone in vivo. Hepatology 2011;54(3):781-8
  • Song X, Guo Y, Duo S, et al. A mouse model of inducible liver injury caused by tet-on regulated urokinase for studies of hepatocyte transplantation. Am J Pathol 2009;175:1975-83
  • Held WA, Mullins JJ, Kuhn NJ, et al. T antigen expression and tumorigenesis in transgenic mice containing a mouse major urinary protein/SV40 T antigen hybrid gene. EMBO J 1989;8:183-91
  • Weglarz TC, Degen JL, Sandgren EP. Hepatocyte transplantation into diseased mouse liver. Kinetics of parenchymal repopulation and identification of the proliferative capacity of tetraploid and octaploid hepatocytes. Am J Pathol 2000;157:1963-74
  • He Z, Zhang H, Zhang X, et al. Liver xeno-repopulation with human hepatocytes in Fah-/-Rag2-/- mice after pharmacological immunosuppression. Am J Pathol 2010;177:1311-19
  • Escribano O, Fernández-Moreno MD, Piña MJ, et al. Pretreatment with FK506 up-regulates insulin receptors in regenerating rat liver. Hepatology 2002;36:555-61
  • Legrand N, Ploss A, Balling R, et al. Humanized mice for modeling human infectious disease: challenges, progress, and outlook. Cell Host Microbe 2009;6:5-9; Review
  • Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005;436:946-52; Review
  • Washburn ML, Bility MT, Zhang L, et al. A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 2011;140:1334-44
  • Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 2011;365(18):1673-83
  • Pajvani UB, Trujillo ME, Combs TP, et al. Fat apoptosis through targeted activation of caspase 8: a new mouse model of inducible and reversible lipoatrophy. Nat Med 2005;11:797-803
  • Robinet E, Baumert TF. A first step towards a mouse model for hepatitis C virus infection containing a human immune system. J Hepatol 2011;55:718-20
  • Bataller R, Paik YH, Lindquist JN, et al. Hepatitis C virus core and nonstructural proteins induce fibrogenic effects in hepatic stellate cells. Gastroenterology 2004;126:529-40
  • Utoh R, Tateno C, Kataoka M, et al. Hepatic hyperplasia associated with discordant xenogeneic parenchymal-nonparenchymal interactions in human hepatocyte-repopulated mice. Am J Pathol 2010;177:654-65
  • Tsuge M, Fujimoto Y, Hiraga N, et al. Hepatitis C virus infection suppresses the interferon response in the liver of the human hepatocyte chimeric mouse. PLoS ONE 2011;6(8):e23856
  • Okazaki A, Hiraga N, Imamura M, et al. Severe necroinflammatory reaction caused by natural killer cell-mediated Fas/Fas ligand interaction and dendritic cells in human hepatocyte chimeric mouse. Hepatology 2012;56:555-66
  • Turrini P, Monego G, Gonzalez J, et al. Human hepatocytes in mice receiving]g pre-immune injection with human cord blood cells. Biochem Biophys Res Commun 2005;326(1):66-73
  • Cruse JM, Lewis RE Jr. The immune system victorious: selective preservation of self. Immunol Res 1993;12(2):101-14; Review
  • Porteus MH, Carroll D. Gene targeting using zinc finger nucleases. Nat Biotechnol 2005;23(8):967-73
  • Geurts AM, Cost GJ, Freyvert Y, et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 2009;325(5939):433
  • Mashimo T, Takizawa A, Kobayashi J, et al. Generation and characterization of severe combined immunodeficiency rats. Cell Rep 2012;2(3):685-94
  • Katayama S, Tateno C, Asahara T, Yoshizato K. Size-dependent in vivo growth potential of adult rat hepatocytes. Am J Pathol 2001;158(1):97-105
  • Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126(4):663-76
  • Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318(5858):1917-20
  • Si-Tayeb K, Noto FK, Nagaoka M, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010;51(1):297-305
  • Takayama K, Inamura M, Kawabata K, et al. Generation of metabolically functioning hepatocytes from human pluripotent stem cells by FOXA2 and HNF1alpha transduction. J Hepatol 2012;57(3):628-36
  • Schwartz RE, Trehan K, Andrus L, et al. Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci USA 2012;109(7):2544-8
  • Wu X, Robotham JM, Lee E, et al. Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog 2012;8(4):e1002617
  • Marukian S, Andrus L, Sheahan TP, et al. Hepatitis C virus induces interferon-λ and interferon-stimulated genes in primary liver cultures. Hepatology 2011;54(6):1913-23
  • Espejel S, Roll GR, McLaughlin KJ, et al. Induced pluripotent stem cell-derived hepatocytes have the functional and proliferative capabilities needed for liver regeneration in mice. J Clin Invest 2010;120(9):3120-6
  • Grompe M, Lindstedt S, al-Dhalimy M, et al. Pharmacological correction of neonatal lethal hepatic dysfunction in a murine model of hereditary tyrosinaemia type I. Nat Genet 1995;10(4):453-60

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.