Different drug metabolism behavior between species in drug-induced hepatotoxicity: limitations and novel resolutions

References

• Adhikari, M. and Arora, R., 2016. The flavonolignan-silymarin protects enzymatic, hematological, and immune system against gamma-radiation-induced toxicity. Environmental toxicology, 31 (6), 641–654.
   PubMed Web of Science ®Google Scholar
• Arakawa, H., et al., 2017. Preliminary evaluation of three-dimensional primary human hepatocyte culture system for assay of drug-metabolizing enzyme-inducing potential. Biological and pharmaceutical bulletin, 40 (7), 967–974.
   PubMed Web of Science ®Google Scholar
• Ballet, F., 2015. Preventing drug-induced liver injury: how useful are animal models? Digestive diseases, 33 (4), 477–485.
   PubMed Web of Science ®Google Scholar
• Bell, C.C., et al., 2016. Characterization of primary human hepatocyte spheroids as a model system for drug-induced liver injury, liver function and disease. Scientific reports, 6, 25187.
   PubMed Web of Science ®Google Scholar
• Bhatia, S.N. and Ingber, D.E., 2014. Microfluidic organs-on-chips. Nature biotechnology, 32 (8), 760–772.
   PubMed Web of Science ®Google Scholar
• Chang, J.H., et al., 2013. Evaluating the in vitro inhibition of UGT1A1, OATP1B1, OATP1B3, MRP2, and BSEP in predicting drug-induced hyperbilirubinemia. Molecular pharmaceutics, 10 (8), 3067–3075.
   PubMed Web of Science ®Google Scholar
• Chiew, G.G.Y., et al., 2017. Bioengineered three-dimensional co-culture of cancer cells and endothelial cells: a model system for dual analysis of tumor growth and angiogenesis. Biotechnology and bioengineering, 114 (8), 1865–1877.
   PubMed Web of Science ®Google Scholar
• Choi, M.K., et al., 2011. Differential effect of genetic variants of Na(+)-taurocholate co-transporting polypeptide (NTCP) and organic anion-transporting polypeptide 1B1 (OATP1B1) on the uptake of HMG-CoA reductase inhibitors. Xenobiotica, 41 (1), 24–34.
   PubMed Web of Science ®Google Scholar
• Chu, N.H., et al., 2015. Role of bicyclol in preventing drug-induced liver injury in tuberculosis patients with liver disease. The international journal of tuberculosis and lung disease, 19 (4), 475–480.
   PubMed Web of Science ®Google Scholar
• Coll, M., et al., 2018. Generation of hepatic stellate cells from human pluripotent stem cells enables in vitro modeling of liver fibrosis. Cell Stem Cell, 23 (1), 101–113 e107.
   PubMed Web of Science ®Google Scholar
• Coronado, R.E., et al., 2017. Decellularization and solubilization of porcine liver for use as a substrate for porcine hepatocyte culture: method optimization and comparison. Cell Transplantation, 26 (12), 1840–1854.
   PubMed Web of Science ®Google Scholar
• Corsini, A. and Bortolini, M., 2013. Drug-induced liver injury: the role of drug metabolism and transport. Journal of clinical pharmacology, 53 (5), 463–474.
   PubMed Web of Science ®Google Scholar
• Crettol, S., Petrovic, N., and Murray, M., 2010. Pharmacogenetics of phase I and phase II drug metabolism. Current pharmaceutical design, 16 (2), 204–219.
   PubMed Web of Science ®Google Scholar
• Djomehri, S.I., et al., 2019. A reproducible scaffold-free 3D organoid model to study neoplastic progression in breast cancer. Journal of cell communication and signaling, 13 (1), 129–143.
   PubMed Web of Science ®Google Scholar
• Ford, A.J. and Rajagopalan, P., 2018. Extracellular matrix remodeling in 3D: implications in tissue homeostasis and disease progression. Wiley interdisciplinary reviews: nanomedicine and nanobiotechnology, 10 (4), e1503.
   PubMed Web of Science ®Google Scholar
• Friedman, S.L., 2008. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiological reviews, 88 (1), 125–172.
   PubMed Web of Science ®Google Scholar
• Fukumitsu, K., Yagi, H., and Soto-Gutierrez, A., 2011. Bioengineering in organ transplantation: targeting the liver. Transplantation proceedings, 43, 2137–2138.
   PubMed Web of Science ®Google Scholar
• Godoy, P., et al., 2013. Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Archives of toxicology, 87 (8), 1315–1530.
   PubMed Web of Science ®Google Scholar
• Gomez-Lechon, M.J., Tolosa, L., and Donato, M.T., 2017. Upgrading HepG2 cells with adenoviral vectors that encode drug-metabolizing enzymes: application for drug hepatotoxicity testing. Expert opinion on drug metabolism & toxicology, 13, 137–148.
   PubMed Web of Science ®Google Scholar
• Gritsenko, P.G., Ilina, O., and Friedl, P., 2012. Interstitial guidance of cancer invasion. The journal of pathology, 226 (2), 185–199.
   PubMed Web of Science ®Google Scholar
• Gu, J., et al., 2015. An open-label, randomized and multi-center clinical trial to evaluate the efficacy of silibinin in preventing drug-induced liver injury. International journal of clinical and experimental medicine, 8 (3), 4320–4327.
   PubMed Web of Science ®Google Scholar
• Han, W., et al., 2019. Innovation for hepatotoxicity in vitro research models: a review. Journal of applied toxicology, 39 (1), 146–162.
   PubMed Web of Science ®Google Scholar
• Hasanain, A.F.A., et al., 2017. Cholecalciferol for prophylaxis against antituberculosis therapy-induced liver disorders among naive patients with pulmonary tuberculosis: a randomized, comparative study. International journal of mycobacteriology, 6 (2), 149–155.
   PubMed Web of Science ®Google Scholar
• Hediger, M.A., et al., 2004. The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteinsIntroduction. Pflugers archives, 447 (5), 465–468.
   PubMed Web of Science ®Google Scholar
• Hendriks, D.F., et al., 2016. Hepatic 3D spheroid models for the detection and study of compounds with cholestatic liability. Scientific reports, 6, 35434.
   PubMed Web of Science ®Google Scholar
• Heo, E., et al., 2017. Effect of prophylactic use of silymarin on anti-tuberculosis drugs induced hepatotoxicity. Tuberculosis and respiratory diseases, 80 (3), 265–269.
   PubMed Web of Science ®Google Scholar
• Hong, J.W., Song, S., and Shin, J.H., 2013. A novel microfluidic co-culture system for investigation of bacterial cancer targeting. Lab on a chip, 13 (15), 3033–3040.
   PubMed Web of Science ®Google Scholar
• Hussein, K.H., et al., 2016. Three dimensional culture of HepG2 liver cells on a rat decellularized liver matrix for pharmacological studies. Journal of biomedical materials research part B: applied biomaterials, 104 (2), 263–273.
   PubMed Web of Science ®Google Scholar
• Hynes, R.O., 2002. Integrins: bidirectional, allosteric signaling machines. Cell, 110 (6), 673–687.
   PubMed Web of Science ®Google Scholar
• International Transporter, et al., 2010. Membrane transporters in drug development. Nature reviews drug discovery, 9, 215–236.
   PubMed Web of Science ®Google Scholar
• Jigorel, E., et al., 2006. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug metabolism and disposition, 34 (10), 1756–1763.
   PubMed Web of Science ®Google Scholar
• Johnson, V.J., et al., 2003. Physiological responses of a natural antioxidant flavonoid mixture, silymarin, in BALB/c mice: III. Silymarin inhibits T-lymphocyte function at low doses but stimulates inflammatory processes at high doses. Planta medica, 69 (1), 44–49.
   PubMed Web of Science ®Google Scholar
• Jun, Y., et al., 2013. 3D co-culturing model of primary pancreatic islets and hepatocytes in hybrid spheroid to overcome pancreatic cell shortage. Biomaterials, 34 (15), 3784–3794.
   PubMed Web of Science ®Google Scholar
• Kang, Y.B., et al., 2013. Layered long-term co-culture of hepatocytes and endothelial cells on a transwell membrane: toward engineering the liver sinusoid. Biofabrication, 5 (4), 045008.
   PubMed Web of Science ®Google Scholar
• Khan, A.A., et al., 2009. The effect of continuous culture on the growth and structure of tissue-engineered cartilage. Biotechnology progress, 25 (2), 508–515.
   PubMed Web of Science ®Google Scholar
• Kim, J.Y., et al., 2015. 3D spherical microtissues and microfluidic technology for multi-tissue experiments and analysis. Journal of biotechnology, 205, 24–35.
   PubMed Web of Science ®Google Scholar
• Kolrep, F., et al., 2016. Differences in metabolism of the marine biotoxin okadaic acid by human and rat cytochrome P450 monooxygenases. Archives of toxicology, 90 (8), 2025–2036.
   PubMed Web of Science ®Google Scholar
• Kondo, T., et al., 2017. Uridine diphosphate-glucuronosyl transferase (UGT) 2B subfamily interspecies differences in carnivores. Toxicological sciences: an official journal of the society of toxicology, 158 (1), 90–100.
   PubMed Web of Science ®Google Scholar
• Kostadinova, R., et al., 2013. A long-term three dimensional liver co-culture system for improved prediction of clinically relevant drug-induced hepatotoxicity. Toxicology and applied pharmacology, 268 (1), 1–16.
   PubMed Web of Science ®Google Scholar
• Kubow, K.E., et al., 2015. Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix. Nature communications, 6 (1), 8026.
   PubMedGoogle Scholar
• Lee, J., Cuddihy, M.J., and Kotov, N.A., 2008. Three-dimensional cell culture matrices: state of the art. Tissue engineering. Part B, reviews, 14 (1), 61–86.
   PubMed Web of Science ®Google Scholar
• Lee, S.A., et al., 2013. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab on a chip, 13 (18), 3529–3537.
   PubMed Web of Science ®Google Scholar
• Lewis, P.L., Green, R.M., and Shah, R.N., 2018. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta biomaterialia, 69, 63–70.
   PubMed Web of Science ®Google Scholar
• Li, J., et al., 2010. Protective effect of silibinin on liver injury induced by antituberculosis drugs. Zhonghua gan zang bing za zhi [Chinese journal of hepatology], 18 (5), 385–386.
   Google Scholar
• Li, N., et al., 2009. LC-MS/MS mediated absolute quantification and comparison of bile salt export pump and breast cancer resistance protein in livers and hepatocytes across species. Analytical chemistry, 81 (6), 2251–2259.
   PubMed Web of Science ®Google Scholar
• Li, Y., et al., 2017. Construction of bioengineered hepatic tissue derived from human umbilical cord mesenchymal stem cells via aggregation culture in porcine decellularized liver scaffolds. Xenotransplantation, 24, e 12285.
   Web of Science ®Google Scholar
• Liu, G.T., et al., 2005. Mechanism of protective action of bicyclol against CCl-induced liver injury in mice. Liver international: official journal of the international association for the study of the liver, 25 (4), 872–879.
   PubMed Web of Science ®Google Scholar
• Lu, L., et al., 2000. In vitro and in vivo degradation of porous poly(DL-lactic-co-glycolic acid) foams. Biomaterials, 21, 1837–1845.
   PubMed Web of Science ®Google Scholar
• Luangchosiri, C., et al., 2015. A double-blinded randomized controlled trial of silymarin for the prevention of antituberculosis drug-induced liver injury. BMC complementary and alternative medicine, 15, 334.
   PubMed Web of Science ®Google Scholar
• Ma, X., et al., 2013. Fibers in the extracellular matrix enable long-range stress transmission between cells. Biophysical journal, 104 (7), 1410–1418.
   PubMed Web of Science ®Google Scholar
• Ma, X., et al., 2016. Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proceedings of the national academy of sciencesU S A, 113 (8), 2206–2211.
   PubMed Web of Science ®Google Scholar
• Ma, X., et al., 2018. 3D bioprinting of functional tissue models for personalized drug screening and in vitro disease modeling. Advanced drug delivery reviews, 132, 235–251.
   PubMed Web of Science ®Google Scholar
• Ma, X.C., et al., 2011. Comparative metabolism of cinobufagin in liver microsomes from mouse, rat, dog, minipig, monkey, and human. Drug metabolism and disposition, 39 (4), 675–682.
   PubMed Web of Science ®Google Scholar
• Marjani, M., et al., 2016. Evaluation of hepatoprotective effect of silymarin among under treatment tuberculosis patients: a randomized clinical trial. Iranian journal of pharmaceutical research, 15 (1), 247–252.
   PubMed Web of Science ®Google Scholar
• McCuskey, R.S., 2006. Sinusoidal endothelial cells as an early target for hepatic toxicants. Clinical hemorheology and microcirculation, 34, 5–10.
   PubMed Web of Science ®Google Scholar
• Murtomaa-Hautala, M., et al., 2012. Significant interspecies differences in induction profiles of hepatic CYP enzymes by TCDD in bank and field voles. Environmental toxicology and chemistry 31 (3), 663–671.
   PubMed Web of Science ®Google Scholar
• Nakano, T., et al., 2011. Impact of artificial sunlight therapy on the progress of non-alcoholic fatty liver disease in rats. Journal of hepatology, 55 (2), 415–425.
   PubMed Web of Science ®Google Scholar
• Nguyen, D.G., et al., 2016. Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS One, 11 (7), e0158674.
   PubMed Web of Science ®Google Scholar
• Nguyen, D.G. and Pentoney, S.L., Jr. 2017. Bioprinted three dimensional human tissues for toxicology and disease modeling. Drug discovery today technologies, 23, 37–44.
   PubMedGoogle Scholar
• Nishimuta, H., et al., 2013. Species differences in hepatic and intestinal metabolic activities for 43 human cytochrome P450 substrates between humans and rats or dogs. Xenobiotica, 43 (11), 948–955.
   PubMed Web of Science ®Google Scholar
• Norona, L.M., et al., 2016. Editor’s highlight: modeling compound-induced fibrogenesis in vitro using three-dimensional bioprinted human liver tissues. Toxicological sciences, 154 (2), 354–367.
   PubMed Web of Science ®Google Scholar
• Oshiro, Y. and Ohkohchi, N., 2017. Three-dimensional liver surgery simulation: computer-assisted surgical planning with three-dimensional simulation software and three-dimensional printing. Tissue engineering part A, 23 (11–12), 474–480.
   PubMed Web of Science ®Google Scholar
• Poisson, J., et al., 2017. Liver sinusoidal endothelial cells: physiology and role in liver diseases. Journal of hepatology, 66 (1), 212–227.
   PubMed Web of Science ®Google Scholar
• Potter, B.M., et al., 2015. Differential CYP 2D6 metabolism alters primaquine pharmacokinetics. Antimicrobial agents and chemotherapy, 59 (4), 2380–2387.
   PubMed Web of Science ®Google Scholar
• Qiu, X., et al., 2013. Absolute measurement of species differences in sodium taurocholate cotransporting polypeptide (NTCP/Ntcp) and its modulation in cultured hepatocytes. Journal of pharmaceutical science, 102 (9), 3252–3263.
   PubMed Web of Science ®Google Scholar
• Rajaram, S., Vemuri, V.D., and Natham, R., 2014. Ascorbic acid improves stability and pharmacokinetics of rifampicin in the presence of isoniazid. Journal of pharmaceutical and biomedical analysis, 100, 103–108.
   PubMed Web of Science ®Google Scholar
• Rennert, K., et al., 2015. A microfluidically perfused three dimensional human liver model. Biomaterials, 71, 119–131.
   PubMed Web of Science ®Google Scholar
• Rushmore, T.H. and Kong, A.N., 2002. Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Current drug metabolism, 3, 481–490.
   PubMed Web of Science ®Google Scholar
• Saengtienchai, A., et al., 2018. Comparison of xenobiotic metabolism in phase I oxidation and phase II conjugation between rats and bird species. Comparative biochemistry and pysiology toxicology & pharmacology, 214, 28–35.
   PubMed Web of Science ®Google Scholar
• Sarkar, J., et al., 2017. Enhanced hepatic functions of genetically modified mouse hepatoma cells by spheroid culture for drug toxicity screening. Biotechnol journal, 12 (10), e201700274.
   PubMed Web of Science ®Google Scholar
• Schinkel, A.H. and Jonker, J.W., 2003. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Advanced drug delivery reviews, 55 (1), 3–29.
   PubMed Web of Science ®Google Scholar
• Schwartz, M.A., 2010. Integrins and extracellular matrix in mechanotransduction. Cold spring harbor perspectives in biology, 2 (12), a005066
   PubMed Web of Science ®Google Scholar
• Shi, X., et al., 2016. The different metabolism of morusin in various species and its potent inhibition against UDP-glucuronosyltransferase (UGT) and cytochrome p450 (CYP450) enzymes. Xenobiotica, 46 (5), 467–476.
   PubMed Web of Science ®Google Scholar
• Song, X., et al., 2013. Mechanistic insights into isoform-dependent and species-specific regulation of bile salt export pump by farnesoid X receptor. Journal of lipid research, 54 (11), 3030–3044.
   PubMed Web of Science ®Google Scholar
• Soto-Gutierrez, A., et al., 2011. A whole-organ regenerative medicine approach for liver replacement. Tissue engineering part C methods, 17 (6), 677–686.
   PubMed Web of Science ®Google Scholar
• Terelius, Y., et al., 2016. Transcriptional profiling suggests that Nevirapine and Ritonavir cause drug induced liver injury through distinct mechanisms in primary human hepatocytes. Chemico biological interactions, 255, 31–44.
   PubMed Web of Science ®Google Scholar
• Turpeinen, M., et al., 2007. Predictive value of animal models for human cytochrome P450 (CYP)-mediated metabolism: a comparative study in vitro. Xenobiotica, 37 (12), 1367–1377.
   PubMed Web of Science ®Google Scholar
• Uyama, N., et al., 2002. Regulation of cultured rat hepatocyte proliferation by stellate cells. Journal of hepatology, 36 (5), 590–599.
   PubMed Web of Science ®Google Scholar
• Wang, H., et al., 2014. Long-range force transmission in fibrous matrices enabled by tension-driven alignment of fibers. Biophysical journal, 107 (11), 2592–2603.
   PubMed Web of Science ®Google Scholar
• Wang, J.Z., et al., 2018. Review fantastic medical implications of 3D-printing in liver surgeries, liver regeneration, liver transplantation and drug hepatotoxicity testing: a review. International journal of surgery, 56, 1–6.
   PubMed Web of Science ®Google Scholar
• Wang, L., et al., 2015. Interspecies variability in expression of hepatobiliary transporters across human, dog, monkey, and rat as determined by quantitative proteomics. Drug metabolism & disposition, 43 (3), 367–374.
   PubMed Web of Science ®Google Scholar
• Ware, B.R., Berger, D.R., and Khetani, S.R., 2015. Prediction of drug-induced liver injury in micropatterned co-cultures containing iPSC-derived human hepatocytes. Toxicological sciences, 145 (2), 252–262.
   PubMed Web of Science ®Google Scholar
• Winer, J.P., Oake, S., and Janmey, P.A., 2009. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS One, 4 (7), e6382.
   PubMed Web of Science ®Google Scholar
• Wirz, W., et al., 2008. Hepatic stellate cells display a functional vascular smooth muscle cell phenotype in a three-dimensional co-culture model with endothelial cells. Differentiation, 76 (7), 784–794.
   PubMed Web of Science ®Google Scholar
• Woolbright, B.L. and Jaeschke, H., 2018. Mechanisms of inflammatory liver injury and drug-induced hepatotoxicity. Current pharmacology reports, 4 (5), 346–357.
   PubMedGoogle Scholar
• Wu, H., et al., 2017a. Efficacy of silibinin capsules in the prevention of liver injury induced by anti-tuberculosis drugs. Chinese journal of antituberculosis, 39, 757–760.
   Google Scholar
• Wu, Y., et al., 2017b. Ascorbic acid promotes extracellular matrix deposition while preserving valve interstitial cell quiescence within 3D hydrogel scaffolds. Journal of tissue engineering and regenerative medicine, 11 (7), 1963–1973.
   PubMed Web of Science ®Google Scholar
• Xie, J., et al., 2018. Solute carrier transporters: potential targets for digestive system neoplasms. Cancer Management and research, 10, 153–166.
   PubMed Web of Science ®Google Scholar
• Xu, X., et al., 2006. Influence of perfusion on metabolism and matrix production by bovine articular chondrocytes in hydrogel scaffolds. Biotechnology and bioengineering, 93 (6), 1103–1111.
   PubMed Web of Science ®Google Scholar
• Xu, Z., et al., 2013. Application of a microfluidic chip-based 3D co-culture to test drug sensitivity for individualized treatment of lung cancer. Biomaterials, 34 (16), 4109–4117.
   PubMed Web of Science ®Google Scholar
• Yokoyama, Y., et al., 2018. Comparison of drug metabolism and its related hepatotoxic effects in HepaRG, cryopreserved human hepatocytes, and HepG2 cell cultures. Biological & pharmaceutical bulletin, 41 (5), 722–732.
   PubMed Web of Science ®Google Scholar
• Zhang, J., et al., 2015. An in vitro liver model on microfluidic device for analysis of capecitabine metabolite using mass spectrometer as detector. Biosensors and bioelectronics, 68, 322–328.
   PubMed Web of Science ®Google Scholar
• Zhang, J., et al., 2016a. Inhibition of bile salt transport by drugs associated with liver injury in primary hepatocytes from human, monkey, dog, rat, and mouse. Chemico-biological interactions, 255, 45–54.
   PubMed Web of Science ®Google Scholar
• Zhang, S., et al., 2016b. Preventive use of a hepatoprotectant against anti-tuberculosis drug-induced liver injury: a randomized controlled trial. Journal of gastroenterology and hepatology, 31 (2), 409–416.
   PubMed Web of Science ®Google Scholar
• Zhang, X., Ouyang, J., and Thung, S.N., 2013. Histopathologic manifestations of drug-induced hepatotoxicity. Clinical liver disease, 17 (4), 547–564. vii–viii.
   PubMed Web of Science ®Google Scholar
• Zhang, Y.S., et al., 2017. Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proceedings of the national academy of sciences of the United States of America, 114 (12), E2293–E2302.
   PubMed Web of Science ®Google Scholar
• Zhao, J., Chen, H., and Li, Y., 2008. Protective effect of bicyclol on acute alcohol-induced liver injury in mice. European journal of pharmacology, 586 (1–3), 322–331.
   PubMed Web of Science ®Google Scholar
• Zhou, Q., et al., 2015. Liver injury-on-a-chip: microfluidic co-cultures with integrated biosensors for monitoring liver cell signaling during injury. Lab on a chip, 15 (23), 4467–4478.
   PubMed Web of Science ®Google Scholar
• Zhu, W., et al., 2017. Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials, 124, 106–115.
   PubMed Web of Science ®Google Scholar