Evaluation of seven drug metabolisms and clearances by cryopreserved human primary hepatocytes cultivated in microfluidic biochips

References

• Barter ZE, Bayliss MK, Beaune PH, Boobis AR, Carlile DJ, Edwards RJ, Houston JB, Lake BG, Lipscomb JC, Pelkonen OR, Tucker GT, Rostami-Hodjegan A. (2007). Scaling factors for the extrapolation of in vivo metabolic drug clearance from in vitro data: Reaching a consensus on values of human microsomal protein and hepatocellularity per gram of liver. Curr Drug Metab 8:33–45.
   PubMed Web of Science ®Google Scholar
• Benet LZ, Øie S, Schwartz JB. (1996). Goodman and Gilman’s: The pharmacological basis of therapeutics. Gilman AG, Hardman JG, Limbard LE, Molinoff PB, Ruddon RW, eds. 9th ed. New York: McGraw Hill Book Company.
   Google Scholar
• Barth CA, Schwarz LR. (1982). Transcellular transport of fluorescein in hepatocyte monolayers: Evidence for functional polarity of cells in culture. Proc Natl Acad Sci USA 79:4985–4987.
   PubMedGoogle Scholar
• Baudoin R, Griscom L, Prot JM, Legallais C, Leclerc E. (2011). Behavior of HepG2/C3A cell cultures in a microfluidic bioreactor. Biochem Eng J 53:172–181.
   Web of Science ®Google Scholar
• Baudoin R, Liberto G, Legallais C, Leclerc E. (in press). Development of a culture box for parallelized microfluidic biochips for xenobiotic toxicity applications. Sensors and Actuators B.
   Google Scholar
• Bhogal N, Grindon C, Combes R, Balls M. (2005). Toxicity testing: Creating a revolution based on new technologies. Trends Biotechnol 23:299–307.
   PubMed Web of Science ®Google Scholar
• Blaauboer BJ, Andersen ME. (2007). The need for a new toxicity testing and risk analysis paradigm to implement REACH or any other large scale testing initiative. Arch Toxicol 81:385–387.
   PubMed Web of Science ®Google Scholar
• Bois F, Maszle D. (1997). MCSim: A simulation program. J Stat Software 2:1–60.
   Google Scholar
• Brown HS, Griffin M, Houston JB. (2007). Evaluation of cryopreserved human hepatocytes as an alternative in vitro system to microsomes for the prediction of metabolic clearance. Drug Metab Dispos 35:293–301.
   PubMed Web of Science ®Google Scholar
• Chao P, Maguire T, Novik E, Cheng KC, Yarmush ML. (2009). Evaluation of a microfluidic based cell culture platform with primary human hepatocytes for the prediction of hepatic clearance in human. Biochem Pharmacol 78:625–632.
   PubMed Web of Science ®Google Scholar
• Cheng S, Prot JM, Leclerc E, Bois FY. (2012). Zonation-related pathways in human hepatocellular carcinoma cells in dynamic vs. static culture microenvironments. BMC Genomic 13:54.
   PubMedGoogle Scholar
• Greim H, Arand M, Autrup H, Bolt HM, Bridges J, Dybing E, Glomot R, Foa V, Schulte-Hermann R. (2006). Toxicological comments to the discussion about REACH. Arch Toxicol 80:121–124.
   PubMed Web of Science ®Google Scholar
• Griffin SJ, Houston JB. (2005). Prediction of in vitro intrinsic clearance from hepatocytes: Comparison of suspensions and monolayer cultures. Drug Metab Dispos 33:115–120.
   PubMed Web of Science ®Google Scholar
• Griffith LG, Naughton G. (2002). Tissue engineering–current challenges and expanding opportunities. Science 295:1009–1014.
   PubMed Web of Science ®Google Scholar
• Groothuis GM, Meijer DK. (1996). Drug traffic in the hepatobiliary system. J Hepatol 24 Suppl 1:3–28.
   PubMedGoogle Scholar
• Guillouzo A. (1998). Liver cell models in in vitro toxicology. Environ Health Perspect 106 Suppl 2:511–532.
   PubMed Web of Science ®Google Scholar
• Guillouzo A, Morel F, Langouët S, Maheo K, Rissel M. (1997). Use of hepatocyte cultures for the study of hepatotoxic compounds. J Hepatol 26 Suppl 2:73–80.
   PubMedGoogle Scholar
• Hallifax D, Rawden H, Hakooz N, Houston B. (2004). Prediction of metabolic clearance using cryopreserved human hepatocytes: Kinetic characteristic for five benzodiazepines. Drug Metab Dispos 33:115–120.
   Google Scholar
• Hartung T, Rovida C. (2009). Chemical regulators have overreached. Nature 460:1080–1081.
   PubMed Web of Science ®Google Scholar
• Hewitt NJ, Bühring KU, Dasenbrock J, Haunschild J, Ladstetter B, Utesch D. (2001). Studies comparing in vivo:in vitro metabolism of three pharmaceutical compounds in rat, dog, monkey, and human using cryopreserved hepatocytes, microsomes, and collagen gel immobilized hepatocyte cultures. Drug Metab Dispos 29:1042–1050.
   PubMed Web of Science ®Google Scholar
• Hewitt NJ, Lechón MJ, Houston JB, Hallifax D, Brown HS, Maurel P, Kenna JG, Gustavsson L, Lohmann C, Skonberg C, Guillouzo A, Tuschl G, Li AP, LeCluyse E, Groothuis GM, Hengstler JG. (2007). 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.
   PubMed Web of Science ®Google Scholar
• Jones H, Barton H, Lai Y, Bi Y, Kimoto E, Kempshall S, Tate S, El-Kattan A, Houston B, Galetin A, Fenner K. (2012). Mechanistic pharmacokinetic modeling for the prediction of transporter-mediated disposition in human from sandwich culture human hepatocyte data. doi:10.1124/dmd.111.042994
   Google Scholar
• Lau YY, Sapidou E, Cui X, White RE, Cheng KC. (2002). Development of a novel in vitro model to predict hepatic clearance using fresh, cryopreserved, and sandwich-cultured hepatocytes. Drug Metab Dispos 30:1446–1454.
   PubMed Web of Science ®Google Scholar
• McGinnity DF, Soars MG, Urbanowicz RA, Riley RJ. (2004). Evaluation of fresh and cryopreserved hepatocytes as in vitro drug metabolism tools for the prediction of metabolic clearance. Drug Metab Dispos 32:1247–1253.
   PubMed Web of Science ®Google Scholar
• Novik E, Maguire TJ, Chao P, Cheng KC, Yarmush ML. (2010). A microfluidic hepatic coculture platform for cell-based drug metabolism studies. Biochem Pharmacol 79:1036–1044.
   PubMed Web of Science ®Google Scholar
• Ouattara DA, Prot JM, Bunescu A, Dumas ME, Elena-Herrmann B, Leclerc E, Brochot C. (2012). Metabolomics-on-a-chip and metabolic flux analysis for label-free modeling of the internal metabolism of HepG2/C3A cells. Mol Biosyst 8:1908–1920.
   PubMed Web of Science ®Google Scholar
• Paine SW, Parker AJ, Gardiner P, Webborn PJ, Riley RJ. (2008). Prediction of the pharmacokinetics of atorvastatin, cerivastatin, and indomethacin using kinetic models applied to isolated rat hepatocytes. Drug Metab Dispos 36:1365–1374.
   PubMed Web of Science ®Google Scholar
• Park J, Berthiaume F, Toner M, Yarmush ML, Tilles AW. (2005). Microfabricated grooved substrates as platforms for bioartificial liver reactors. Biotechnol Bioeng 90:632–644.
   PubMed Web of Science ®Google Scholar
• Pelkonen O, Turpeinen M, Hakkola J, Honkakoski P, Hukkanen J, Raunio H. (2008). Inhibition and induction of human cytochrome P450 enzymes: Current status. Arch Toxicol 82:667–715.
   PubMed Web of Science ®Google Scholar
• Powers MJ, Janigian DM, Wack KE, Baker CS, Beer Stolz D, Griffith LG. (2002). Functional behavior of primary rat liver cells in a three-dimensional perfused microarray bioreactor. Tissue Eng 8:499–513.
   PubMedGoogle Scholar
• Prot JM, Aninat C, Griscom L, Razan F, Brochot C, Guillouzo CG, Legallais C, Corlu A, Leclerc E. (2011a). Improvement of HepG2/C3a cell functions in a microfluidic biochip. Biotechnol Bioeng 108:1704–1715.
   PubMed Web of Science ®Google Scholar
• Prot JM, Briffaut AS, Letourneur F, Chafey P, Merlier F, Grandvalet Y, Legallais C, Leclerc E. (2011b). Integrated proteomic and transcriptomic investigation of the acetaminophen toxicity in liver microfluidic biochip. PLoS ONE 6:e21268.
   Google Scholar
• Prot JM, Videau O, Brochot C, Legallais C, Bénech H, Leclerc E. (2011c). A cocktail of metabolic probes demonstrates the relevance of primary human hepatocyte cultures in a microfluidic biochip for pharmaceutical drug screening. Int J Pharm 408:67–75.
   PubMed Web of Science ®Google Scholar
• Sivaraman A, Leach JK, Townsend S, Iida T, Hogan BJ, Stolz DB, Fry R, Samson LD, Tannenbaum SR, Griffith LG. (2005). A microscale in vitro physiological model of the liver: Predictive screens for drug metabolism and enzyme induction. Curr Drug Metab 6:569–591.
   PubMed Web of Science ®Google Scholar
• Shintu L, Baudoin R, Navratil V, Prot JM, Pontoizeau C, Defernez M, Blaise BJ, Domange C, Péry AR, Toulhoat P, Legallais C, Brochot C, Leclerc E, Dumas ME. (2012). Metabolomics-on-a-chip and predictive systems toxicology in microfluidic bioartificial organs. Anal Chem 84:1840–1848.
   PubMed Web of Science ®Google Scholar
• Tilles AW, Baskaran H, Roy P, Yarmush ML, Toner M. (2001). Effects of oxygenation and flow on the viability and function of rat hepatocytes cocultured in a microchannel flat-plate bioreactor. Biotechnol Bioeng 73:379–389.
   PubMed Web of Science ®Google Scholar
• Tompkins LM, Wallace AD. (2007). Mechanisms of cytochrome P450 induction. J Biochem Mol Toxicol 21:176–181.
   PubMed Web of Science ®Google Scholar
• Videau O, Delaforge M, Levi M, Thevenot E, Gal O, Becquemont L, Beaune P, Benech H. (2010). Biochemical and analytical development of the CIME cocktail for drug fate assessment in humans. Rapid Commun Mass Spectrom 24:2407–2419. Available at: http://dx.doi.org/10.1002/rcm.4641.
   PubMed Web of Science ®Google Scholar
• Zhang S, Tong W, Zheng B, Susanto TA, Xia L, Zhang C, Ananthanarayanan A, Tuo X, Sakban RB, Jia R, Iliescu C, Chai KH, McMillian M, Shen S, Leo H, Yu H. (2011). A robust high-throughput sandwich cell-based drug screening platform. Biomaterials 32:1229–1241.
   PubMedGoogle Scholar
• Zuegge J, Schneider G, Coassolo P, Lavé T. (2001). Prediction of hepatic metabolic clearance: Comparison and assessment of prediction models. Clin Pharmacokinet 40:553–563.
   PubMed Web of Science ®Google Scholar