Acetaminophen cytotoxicity is ameliorated in a human liver organotypic co-culture model

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Nelson, Leonard J ^a   Navarro, Maria ^a   Treskes, Philipp ^a   Samuel, Kay ^a   Tura Ceide, Olga ^b   Morley, Steven D ^a   Hayes, Peter C ^a   Plevris, John N ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LACTIC ACID DERIVATIVE; PARACETAMOL; PYRUVIC ACID;

CELL SURVIVAL; COCULTURE; CYTOLOGY; DRUG EFFECTS; HUMAN; LIVER; METABOLISM; MITOCHONDRION; PROCEDURES; TOXICITY TESTING; UMBILICAL VEIN ENDOTHELIAL CELL;

ACETAMINOPHEN; CELL SURVIVAL; COCULTURE TECHNIQUES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LACTATES; LIVER; MITOCHONDRIA; PYRUVIC ACID; TOXICITY TESTS;

EID: 84949186976     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17455     Document Type: Article

References (59)

1. O'Brien, P. J. et al. High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cellbased model using high content screening. Arch Toxicol 80, 580-604, doi: 10.1007/s00204-006-0091-3 (2006).
2. Gomez-Lechon, M. J., Tolosa, L., Conde, I. and Donato, M. T. Competency of different cell models to predict human hepatotoxic drugs. Expert Opin Drug Metab Toxicol 10, 1553-1568, doi: 10.1517/17425255.2014.967680 (2014).
3. Aninat, C. et al. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab Dispos 34, 75-83, doi: 10.1124/dmd.105.006759 (2006).
4. Hewitt, N. J. et al. Primary hepatocytes: current understanding of the regulation of metabolic enzymes and transporter proteins, and pharmaceutical practice for the use of hepatocytes in metabolism, enzyme induction, transporter, clearance, and hepatotoxicity studies. Drug Metab Rev 39, 159-234, doi: 10.1080/03602530601093489 (2007).
5. Nipic, D., Pirc, A., Banic, B., Suput, D. and Milisav, I. Preapoptotic cell stress response of primary hepatocytes. Hepatology 51, 2140-2151, doi: 10.1002/hep.23598 (2010).
6. Khetani, S. R. and Bhatia, S. N. Microscale culture of human liver cells for drug development. Nat Biotechnol 26, 120-126, doi: 10.1038/nbt1361 (2008).
7. Guillouzo, A. and Guguen-Guillouzo, C. Evolving concepts in liver tissue modeling and implications for in vitro toxicology. Expert Opin Drug Metab Toxicol 4, 1279-1294, doi: 10.1517/17425255.4.10.1279 (2008).
8. Park, B. K. et al. Managing the challenge of chemically reactive metabolites in drug development. Nat Rev Drug Discov 10, 292-306, doi: 10.1038/nrd3408 (2011).
9. Cheng, J., Ma, X., Krausz, K. W., Idle, J. R. and Gonzalez, F. J. Rifampicin-activated human pregnane X receptor and CYP3A4 induction enhance acetaminophen-induced toxicity. Drug Metabolism and Disposition 37, 1611-1621 (2009).
10. Laine, J., Auriola, S., Pasanen, M. and Juvonen, R. Acetaminophen bioactivation by human cytochrome P450 enzymes and animal microsomes. Xenobiotica 39, 11-21 (2009).
11. Thummel, K. E., Lee, C. A., Kunze, K. L., Nelson, S. D. and Slattery, J. T. Oxidation of acetaminophen to N-acetyl-paminobenzoquinone imine by human CYP3A4. Biochemical pharmacology 45, 1563-1569 (1993).
12. Filippi, C. et al. Improvement of C3A cell metabolism for usage in bioartificial liver support systems. J Hepatol 41, 599-605, doi: 10.1016/j.jhep.2004.06.012 (2004).
13. Lockman, K. A. et al. Oxidative stress rather than triglyceride accumulation is a determinant of mitochondrial dysfunction in in vitro models of hepatic cellular steatosis. Liver Int 32, 1079-1092, doi: 10.1111/j.1478-3231.2012.02775.x (2012).
14. Du, C., Narayanan, K., Leong, M. F. and Wan, A. C. Induced pluripotent stem cell-derived hepatocytes and endothelial cells in multi-component hydrogel fibers for liver tissue engineering. Biomaterials 35, 6006-6014, doi: 10.1016/j.biomaterials.2014.04.011 (2014).
15. Ohno, M., Motojima, K., Okano, T. and Taniguchi, A. Induction of drug-metabolizing enzymes by phenobarbital in layered coculture of a human liver cell line and endothelial cells. Biol Pharm Bull 32, 813-817 (2009).
16. Toyoda, Y. et al. Acetaminophen-induced hepatotoxicity in a liver tissue model consisting of primary hepatocytes assembling around an endothelial cell network. Drug Metab Dispos 40, 169-177, doi: 10.1124/dmd.111.041137 (2012).
17. Nahmias, Y., Schwartz, R. E., Hu, W. S., Verfaillie, C. M. and Odde, D. J. Endothelium-mediated hepatocyte recruitment in the establishment of liver-like tissue in vitro. Tissue Eng 12, 1627-1638, doi: 10.1089/ten.2006.12.1627 (2006).
18. Soto-Gutierrez, A. et al. Engineering of an hepatic organoid to develop liver assist devices. Cell Transplant 19, 815-822, doi: 10.3727/096368910x508933 (2010).
19. Bhatia, S. N., Underhill, G. H., Zaret, K. S. and Fox, I. J. Cell and tissue engineering for liver disease. Sci Transl Med 6, 245sr242, doi: 10.1126/scitranslmed.3005975 (2014).
20. DeLeve, L. D., Wang, X., Hu, L., McCuskey, M. K. and McCuskey, R. S. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol 287, G757-763, doi: 10.1152/ajpgi.00017.2004 (2004).
21. Salerno, S., Campana, C., Morelli, S., Drioli, E. and De Bartolo, L. Human hepatocytes and endothelial cells in organotypic membrane systems. Biomaterials 32, 8848-8859, doi: 10.1016/j.biomaterials.2011.08.004 (2011).
22. Elvevold, K., Smedsrod, B. and Martinez, I. The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity. Am J Physiol Gastrointest Liver Physiol 294, G391-400, doi: 10.1152/ajpgi.00167.2007 (2008).
23. Fomin, M. E. et al. Production of factor VIII by human liver sinusoidal endothelial cells transplanted in immunodeficient uPA mice. PLoS One 8, e77255, doi: 10.1371/journal.pone.0077255 (2013).
24. Takayama, G., Taniguchi, A. and Okano, T. Identification of differentially expressed genes in hepatocyte/endothelial cell co-culture system. Tissue Eng 13, 159-166, doi: 10.1089/ten.2006.0143 (2007).
25. Harimoto, M. et al. Novel approach for achieving double-layered cell sheets co-culture: overlaying endothelial cell sheets onto monolayer hepatocytes utilizing temperature-responsive culture dishes. J Biomed Mater Res 62, 464-470, doi: 10.1002/jbm.10228 (2002).
26. Chiew, G. G., Fu, A., Low, K. P. and Luo, K. Q. Physical supports from liver cancer cells are essential for differentiation and remodeling of endothelial cells in a HepG2-HUVEC co-culture model. Sci Rep 5, 10801, doi: 10.1038/srep10801 (2015).
27. Prill, S. et al. Real-time monitoring of oxygen uptake in hepatic bioreactor shows CYP450-independent mitochondrial toxicity of acetaminophen and amiodarone. Arch Toxicol, doi: 10.1007/s00204-015-1537-2 (2015).
28. Badmann, A. et al. TRAIL enhances paracetamol-induced liver sinusoidal endothelial cell death in a Bim- and Bid-dependent manner. Cell Death Dis 3, e447, doi: 10.1038/cddis.2012.185 (2012).
29. Bessems, J. G. and Vermeulen, N. P. Paracetamol (acetaminophen)-induced toxicity: molecular and biochemical mechanisms, analogues and protective approaches. Crit Rev Toxicol 31, 55-138, doi: 10.1080/20014091111677 (2001).
30. Willett, C. et al. Building shared experience to advance practical application of pathway-based toxicology: liver toxicity modeof- action. Altex 31, 500-519, doi: 10.14573/altex.1401281 (2014).
31. Nelson, L. J. et al. Profiling the impact of medium formulation on morphology and functionality of primary hepatocytes in vitro. Sci Rep 3, 2735, doi: 10.1038/srep02735 (2013).
32. Limonciel, A. et al. Lactate is an ideal non-invasive marker for evaluating temporal alterations in cell stress and toxicity in repeat dose testing regimes. Toxicol In Vitro 25, 1855-1862, doi: 10.1016/j.tiv.2011.05.018 (2011).
33. Burcham, P. C. and Harman, A. W. Mitochondrial dysfunction in paracetamol hepatotoxicity: in vitro studies in isolated mouse hepatocytes. Toxicol Lett 50, 37-48 (1990).
34. Walker, R. M., Racz, W. J. and McElligott, T. F. Acetaminophen-induced hepatotoxic congestion in mice. Hepatology 5, 233-240 (1985).
35. Ito, Y., Bethea, N. W., Abril, E. R. and McCuskey, R. S. Early hepatic microvascular injury in response to acetaminophen toxicity. Microcirculation 10, 391-400, doi: 10.1038/sj.mn.7800204 (2003).
36. McCuskey, R. S. Sinusoidal endothelial cells as an early target for hepatic toxicants. Clin Hemorheol Microcirc 34, 5-10 (2006).
37. Jemnitz, K., Veres, Z., Monostory, K., Kobori, L. and Vereczkey, L. Interspecies differences in acetaminophen sensitivity of human, rat, and mouse primary hepatocytes. Toxicol In Vitro 22, 961-967, doi: 10.1016/j.tiv.2008.02.001 (2008).
38. Sjogren, A. K. et al. Critical differences in toxicity mechanisms in induced pluripotent stem cell-derived hepatocytes, hepatic cell lines and primary hepatocytes. Arch Toxicol 88, 1427-1437, doi: 10.1007/s00204-014-1265-z (2014).
39. LeCluyse, E. L., Witek, R. P., Andersen, M. E. and Powers, M. J. Organotypic liver culture models: meeting current challenges in toxicity testing. Crit Rev Toxicol 42, 501-548, doi: 10.3109/10408444.2012.682115 (2012).
40. Berger, D. R., Ware, B. R., Davidson, M. D., Allsup, S. R. and Khetani, S. R. Enhancing the functional maturity of induced pluripotent stem cell-derived human hepatocytes by controlled presentation of cell-cell interactions in vitro. Hepatology 61, 1370-1381, doi: 10.1002/hep.27621 (2015).
41. Kaplowitz, N. and DeLeve, L. D. Drug-induced liver disease. (Academic Press, 2013).
42. Atlante, A. et al. An increase in the ATP levels occurs in cerebellar granule cells en route to apoptosis in which ATP derives from both oxidative phosphorylation and anaerobic glycolysis. Biochim Biophys Acta 1708, 50-62, doi: 10.1016/j.bbabio.2005.01.009 (2005).
43. Liu, Y., Li, H., Yan, S., Wei, J. and Li, X. Hepatocyte cocultures with endothelial cells and fibroblasts on micropatterned fibrous mats to promote liver-specific functions and capillary formation capabilities. Biomacromolecules 15, 1044-1054, doi: 10.1021/ bm401926k (2014).
44. Shah, A. D., Wood, D. M. and Dargan, P. I. Understanding lactic acidosis in paracetamol (acetaminophen) poisoning. Br J Clin Pharmacol 71, 20-28, doi: 10.1111/j.1365-2125.2010.03765.x (2011).
45. Kim, P. K., Zamora, R., Petrosko, P. and Billiar, T. R. The regulatory role of nitric oxide in apoptosis. Int Immunopharmacol 1, 1421-1441 (2001).
46. Jaeschke, H. et al. Mechanisms of hepatotoxicity. Toxicol Sci 65, 166-176 (2002).
47. Reliene, R., Fischer, E. and Schiestl, R. H. Effect of N-acetyl cysteine on oxidative DNA damage and the frequency of DNA deletions in atm-deficient mice. Cancer Res 64, 5148-5153, doi: 10.1158/0008-5472.can-04-0442 (2004).
48. Jaeschke, H., McGill, M. R. and Ramachandran, A. Oxidant stress, mitochondria, and cell death mechanisms in drug-induced liver injury: lessons learned from acetaminophen hepatotoxicity. Drug Metab Rev 44, 88-106, doi: 10.3109/03602532.2011.602688 (2012).
49. Saito, C., Zwingmann, C. and Jaeschke, H. Novel mechanisms of protection against acetaminophen hepatotoxicity in mice by glutathione and N-acetylcysteine. Hepatology 51, 246-254, doi: 10.1002/hep.23267 (2010).
50. Sappington, P. L., Han, X., Yang, R., Delude, R. L. and Fink, M. P. Ethyl pyruvate ameliorates intestinal epithelial barrier dysfunction in endotoxemic mice and immunostimulated caco-2 enterocytic monolayers. J Pharmacol Exp Ther 304, 464-476, doi: 10.1124/ jpet.102.043182 (2003).
51. Vanhaecke, T., Vercruysse, A. and Rogiers, V. Effect of pyruvate on glutathione s-transferase expression in primary cultures of rat hepatocytes. Toxicol In Vitro 11, 435-441 (1997).
52. Farin, F. Expression of Cytochrome P450s and Microsomal Epoxide Hydrolase in Primary Cultures of Human Umbilical Vein Endothelial Cells. Toxicol Appl Pharmacol 124, 1-9, doi: 10.1006/taap.1994.1001 (1994).
53. Moellering, D. et al. Nitric oxide-dependent induction of glutathione synthesis through increased expression of gammaglutamylcysteine synthetase. Arch Biochem Biophys 358, 74-82, doi: 10.1006/abbi.1998.0854 (1998).
54. Alva, N. et al. Nitric oxide as a mediator of fructose 1,6-bisphosphate protection in galactosamine-induced hepatotoxicity in rats. Nitric Oxide 28, 17-23, doi: 10.1016/j.niox.2012.09.004 (2013).
55. Bartberger, M. D. et al. The reduction potential of nitric oxide (NO) and its importance to NO biochemistry. Proc Natl Acad Sci USA 99, 10958-10963, doi: 10.1073/pnas.162095599 (2002).
56. Aharoni-Simon, M., Anavi, S., Beifuss, U., Madar, Z. and Tirosh, O. Nitric oxide, can it be only good? Increasing the antioxidant properties of nitric oxide in hepatocytes by YC-1 compound. Nitric Oxide 27, 248-256, doi: 10.1016/j.niox.2012.08.076 (2012).
57. Hinson, J. A., Roberts, D. W. and James, L. P. Mechanisms of acetaminophen-induced liver necrosis. Handb Exp Pharmacol, 369-405, doi: 10.1007/978-3-642-00663-0-12 (2010).
58. Kuo, P. C. and Slivka, A. Nitric oxide decreases oxidant-mediated hepatocyte injury. J Surg Res 56, 594-600, doi: 10.1006/ jsre.1994.1094 (1994).
59. McGill, M. R. et al. HepaRG cells: a human model to study mechanisms of acetaminophen hepatotoxicity. Hepatology 53, 974-982, doi: 10.1002/hep.24132 (2011).