Laminar-flow immediate-overlay hepatocyte sandwich perfusion system for drug hepatotoxicity testing

Biomaterials

Volumn 30, Issue 30, 2009, Pages 5927-5936

  Xia, Lei ^a,b   Ng, Susanne ^a,c   Han, Rongbin ^a,d   Tuo, Xiaoye ^a,e,f   Xiao, Guangfa ^a,g,i   Leo, Hwa Liang ^a,e   Cheng, Tianming ^a,h,i   Yu, Hanry ^a,b,e,i,j  

^a INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d Texas AandM University   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f CHINESE PLA GENERAL HOSPITAL   (China)

^g Xiang Ya Hospital   (China)

^h SOUTHERN MEDICAL UNIVERSITY   (China)

ⁱ NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^j Massachusetts Institute of Technology Cambridge   (United States)

more..

Author keywords

Mass transfer; Perfusion bioreactor; Polarity; Sandwich culture; Shear stress; Stable functions

Indexed keywords

BILIARY EXCRETION; BIOTRANSFORMATION ENZYMES; COLLAGEN MATRICES; CULTURE PARAMETERS; DRUG TESTING; HEPATOCYTE CULTURE; HEPATOCYTES; HEPATOTOXICITY; IN-VITRO; INITIATION TIME; LIVER-SPECIFIC FUNCTIONS; OPTIMIZED SYSTEM; PERFUSION BIOREACTOR; PERFUSION CULTURES; PERFUSION SYSTEM; POLARITY; POROUS POLYMERIC MEMBRANE; SANDWICH CULTURE; STABLE FUNCTIONS; STATIC CULTURE;

BIOCONVERSION; BIOREACTORS; COLLAGEN; INDUSTRIAL CHEMICALS; LIVER; MASS TRANSFER; POLYMERIC MEMBRANES; SHEAR STRESS; STRENGTH OF MATERIALS; WINDOWS;

CELL CULTURE;

COLLAGEN; PARACETAMOL; POLYMER;

ANIMAL CELL; ARTICLE; BILIARY EXCRETION; BIOREACTOR; BIOTRANSFORMATION; CELL CULTURE; CELL POLARITY; CELL PROTECTION; CONTROLLED STUDY; CULTURE OPTIMIZATION; DRUG SCREENING; ENZYME ACTIVITY; FLOW RATE; IN VITRO STUDY; LAMINAR FLOW; LIVER CELL; LIVER FUNCTION; LIVER TOXICITY; MALE; NONHUMAN; PERFUSION; POROSITY; PRIORITY JOURNAL; PROCESS OPTIMIZATION; RAT; SENSITIVITY ANALYSIS; SHEAR STRESS; TOXICITY TESTING;

ANIMALS; BIOREACTORS; BIOTRANSFORMATION; CELL CULTURE TECHNIQUES; COLLAGEN; DRUG EVALUATION, PRECLINICAL; DRUG INDUSTRY; HEPATOCYTES; LIVER; MALE; POLYMERS; POROSITY; RATS; RATS, WISTAR; TECHNOLOGY, PHARMACEUTICAL;

EID: 69249206581     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.07.022     Document Type: Article

References (59)

1. Guillouzo A. Liver cell models in in vitro toxicology. Environ Health Perspect 106 Suppl. 2 (1998) 511-532
2. Groneberg D.A., Grosse-Siestrup C., and Fischer A. In vitro models to study hepatotoxicity. Toxicol Pathol 30 3 (2002) 394-399
3. Ilan Y. Towards a bank of cryopreserved hepatocytes: which cell to freeze?. J Hepatol 37 1 (2002) 145-146
4. Hengstler J.G., Utesch D., Steinberg P., Platt K.L., Diener B., Ringel M., et al. Cryopreserved primary hepatocytes as a constantly available in vitro model for the evaluation of human and animal drug metabolism and enzyme induction. Drug Metab Rev 32 1 (2000) 81-118
5. Li A.P., Lu C., Brent J.A., Pham C., Fackett A., Ruegg C.E., et al. Cryopreserved human hepatocytes: characterization of drug-metabolizing enzyme activities and applications in higher throughput screening assays for hepatotoxicity, metabolic stability, and drug-drug interaction potential. Chem Biol Interact 121 1 (1999) 17-35
6. Li A.P. Human hepatocytes: isolation, cryopreservation and applications in drug development. Chem Biol Interact 168 1 (2007) 16-29
7. Xu J.J., Diaz D., and O'Brien P.J. Applications of cytotoxicity assays and pre-lethal mechanistic assays for assessment of human hepatotoxicity potential. Chem Biol Interact 150 1 (2004) 115-128
8. Landry J., Bernier D., Ouellet C., Goyette R., and Marceau N. Spheroidal aggregate culture of rat liver cells: histotypic reorganization, biomatrix deposition, and maintenance of functional activities. J Cell Biol 101 3 (1985) 914-923
9. Abu-Absi S.F., Friend J.R., Hansen L.K., and Hu W.S. Structural polarity and functional bile canaliculi in rat hepatocyte spheroids. Exp Cell Res 274 1 (2002) 56-67
10. Dunn J.C., Tompkins R.G., and Yarmush M.L. Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol Prog 7 3 (1991) 237-245
11. LeCluyse E.L., Audus K.L., and Hochman J.H. Formation of extensive canalicular networks by rat hepatocytes cultured in collagen-sandwich configuration. Am J Physiol 266 6 Pt 1 (1994) C1764-C1774
12. Glicklis R., Merchuk J.C., and Cohen S. Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol Bioeng 86 6 (2004) 672-680
13. Kern A., Bader A., Pichlmayr R., and Sewing K.F. Drug metabolism in hepatocyte sandwich cultures of rats and humans. Biochem Pharmacol 54 7 (1997) 761-772
14. Ghibellini G., Leslie E.M., and Brouwer K.L. Methods to evaluate biliary excretion of drugs in humans: an updated review. Mol Pharmacol 3 3 (2006) 198-211
15. Toritsuka N., Nonogaki Y., Hori Y., Sawada S., Shoun H., and Motooka S. Well maintained expression of CYP genes in sandwich-culturing hepatocytes: quantitative analysis using real-time PCR method. Res Commun Mol Pathol Pharmacol 110 5-6 (2001) 311-318
16. Liu X., LeCluyse E.L., Brouwer K.R., Gan L.S., Lemasters J.J., Stieger B., et al. Biliary excretion in primary rat hepatocytes cultured in a collagen-sandwich configuration. Am J Physiol 277 1 Pt 1 (1999) G12-G21
17. Farghali H., Kamenikova L., and Hynie S. The concept of application of immobilized and perfused mammalian cells (a bioreactor model) in biomedical research. Physiol Res 43 2 (1994) 117-120
18. Langsch A., and Bader A. Longterm stability of phase I and phase II enzymes of porcine liver cells in flat membrane bioreactors. Biotechnol Bioeng 76 2 (2001) 115-125
19. De Bartolo L., Jarosch-Von Schweder G., Haverich A., and Bader A. A novel full-scale flat membrane bioreactor utilizing porcine hepatocytes: cell viability and tissue-specific functions. Biotechnol Prog 16 1 (2000) 102-108
20. Taguchi K., Matsushita M., Takahashi M., and Uchino J. Development of a bioartificial liver with sandwiched-cultured hepatocytes between two collagen gel layers. Artif Organs 20 2 (1996) 178-185
21. Rotem A., Toner M., Tompkins R.G., and Yarmush M.L. Oxygen uptake rates in cultured rat hepatocytes. Biotechnol Bioeng 40 10 (1992) 1286-1291
22. Koebe H.G., Deglmann C.J., Metzger R., Hoerrlein S., and Schildberg F.W. In vitro toxicology in hepatocyte bioreactors-extracellular acidification rate (EAR) in a target cell line indicates hepato-activated transformation of substrates. Toxicology 154 1-3 (2000) 31-44
23. Tilles A.W., Baskaran H., Roy P., Yarmush M.L., and Toner M. Effects of oxygenation and flow on the viability and function of rat hepatocytes cocultured in a microchannel flat-plate bioreactor. Biotechnol Bioeng 73 5 (2001) 379-389
24. Roy P., Washizu J., Tilles A.W., Yarmush M.L., and Toner M. Effect of flow on the detoxification function of rat hepatocytes in a bioartificial liver reactor. Cell Transplant 10 7 (2001) 609-614
25. Ng S., Han R., Chang S., Ni J., Hunziker W., Goryachev A.B., et al. Improved hepatocyte excretory function by immediate presentation of polarity cues. Tissue Eng 12 8 (2006) 2181-2191
26. Seglen P.O. Preparation of isolated rat liver cells. Methods Cell Biol 13 (1976) 29-83
27. Kim S.S., Sundback C.A., Kaihara S., Benvenuto M.S., Kim B.S., Mooney D.J., et al. Dynamic seeding and in vitro culture of hepatocytes in a flow perfusion system. Tissue Eng 6 1 (2000) 39-44
28. Cereijido M., Shoshani L., and Contreras R.G. Molecular physiology and pathophysiology of tight junctions. I. Biogenesis of tight junctions and epithelial polarity. Am J Physiol Gastrointest Liver Physiol 279 3 (2000) G477-G482
29. Wang L., and Boyer J.L. The maintenance and generation of membrane polarity in hepatocytes. Hepatology 39 4 (2004) 892-899
30. Karecla P.I., Green S.J., Bowden S.J., Coadwell J., and Kilshaw P.J. Identification of a binding site for integrin alphaEbeta7 in the N-terminal domain of E-cadherin. J Biol Chem 271 48 (1996) 30909-30915
31. Brieva T.A., and Moghe P.V. Functional engineering of hepatocytes via heterocellular presentation of a homoadhesive molecule, E-cadherin. Biotechnol Bioeng 76 4 (2001) 295-302
32. Danjo Y., and Gipson I.K. Actin 'purse string' filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement. J Cell Sci 111 Pt 22 (1998) 3323-3332
33. Kawahara H., Marceau N., and French S.W. Effect of agents which rearrange the cytoskeleton in vitro on the structure and function of hepatocytic canaliculi. Lab Invest 60 5 (1989) 692-704
34. Kacich R.L., Renston R.H., and Jones A.L. Effects of cytochalasin D and colchicine on the uptake, translocation, and biliary secretion of horseradish peroxidase and [14C]sodium taurocholate in the rat. Gastroenterology 85 2 (1983) 385-394
35. Durand-Schneider A.M., Bouanga J.C., Feldmann G., and Maurice M. Microtubule disruption interferes with the structural and functional integrity of the apical pole in primary cultures of rat hepatocytes. Eur J Cell Biol 56 2 (1991) 260-268
36. Margolis R.L., and Wilson L. Addition of colchicine-tubulin complex to microtubule ends: the mechanism of substoichiometric colchicine poisoning. Proc Natl Acad Sci U S A 74 8 (1977) 3466-3470
37. Wilson L., Panda D., and Jordan M.A. Modulation of microtubule dynamics by drugs: a paradigm for the actions of cellular regulators. Cell Struct Funct 24 5 (1999) 329-335
38. Hemery I., Durand-Schneider A.M., Feldmann G., Vaerman J.P., and Maurice M. The transcytotic pathway of an apical plasma membrane protein (B10) in hepatocytes is similar to that of IgA and occurs via a tubular pericentriolar compartment. J Cell Sci 109 Pt 6 (1996) 1215-1227
39. Dumont M., D'Hont C., Durand-Schneider A.M., Legrand-Defretin V.L., Feldmann G., and Erlinger S. Inhibition by colchicine of biliary secretion of diethylmaleate in the rat: evidence for microtubule-dependent vesicular transport. Hepatology 14 1 (1991) 10-15
40. Torok N., Marks D., Hsiao K., Oswald B.J., and McNiven M.A. Vesicle movement in rat hepatocytes is reduced by ethanol exposure: alterations in microtubule-based motor enzymes. Gastroenterology 113 6 (1997) 1938-1948
41. Boyle M., Kurtovic J., Bihari D., Riordan S., and Steiner C. Equipment review: the molecular adsorbents recirculating system (MARS). Crit Care 8 4 (2004) 280-286
42. Meier P.J. Molecular mechanisms of hepatic bile salt transport from sinusoidal blood into bile. Am J Physiol 269 6 Pt 1 (1995) G801-G812
43. Zucker S.D., Goessling W., and Hoppin A.G. Unconjugated bilirubin exhibits spontaneous diffusion through model lipid bilayers and native hepatocyte membranes. J Biol Chem 274 16 (1999) 10852-10862
44. Yeaman C., Grindstaff K.K., and Nelson W.J. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79 1 (1999) 73-98
45. Kullak-Ublick G.A., Beuers U., and Paumgartner G. Hepatobiliary transport. J Hepatol 32 Suppl. 1 (2000) 3-18
46. Pauli-Magnus C., and Meier P.J. Hepatobiliary transporters and drug-induced cholestasis. Hepatology 44 4 (2006) 778-787
47. Tsukada N., and Phillips M.J. Bile canalicular contraction is coincident with reorganization of pericanalicular filaments and co-localization of actin and myosin-II. J Histochem Cytochem 41 3 (1993) 353-363
48. Amato M. Mechanisms of bilirubin toxicity. Eur J Pediatr 154 9 Suppl. 4 (1995) S54-S59
49. Palmeira C.M., and Rolo A.P. Mitochondrially-mediated toxicity of bile acids. Toxicology 203 1-3 (2004) 1-15
50. Stieger B., Fattinger K., Madon J., Kullak-Ublick G.A., and Meier P.J. Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118 2 (2000) 422-430
51. Jaeschke H., Gores G.J., Cederbaum A.I., Hinson J.A., Pessayre D., and Lemasters J.J. Mechanisms of hepatotoxicity. Toxicol Sci 65 2 (2002) 166-176
52. Powers M.J., Domansky K., Kaazempur-Mofrad M.R., Kalezi A., Capitano A., Upadhyaya A., et al. A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol Bioeng 78 3 (2002) 257-269
53. Powers M.J., Janigian D.M., Wack K.E., Baker C.S., Beer Stolz D., and Griffith L.G. Functional behavior of primary rat liver cells in a three-dimensional perfused microarray bioreactor. Tissue Eng 8 3 (2002) 499-513
54. Rumack B.H. Acetaminophen misconceptions. Hepatology 40 1 (2004) 10-15
55. Wang K., Shindoh H., Inoue T., and Horii I. Advantages of in vitro cytotoxicity testing by using primary rat hepatocytes in comparison with established cell lines. J Toxicol Sci 27 3 (2002) 229-237
56. Mingoia R.T., Nabb D.L., Yang C.H., and Han X. Primary culture of rat hepatocytes in 96-well plates: effects of extracellular matrix configuration on cytochrome P450 enzyme activity and inducibility, and its application in in vitro cytotoxicity screening. Toxicol In Vitro 21 1 (2007) 165-173
57. Kienhuis A.S., Wortelboer H.M., Hoflack J.C., Moonen E.J., Kleinjans J.C., van Ommen B., et al. Comparison of coumarin-induced toxicity between sandwich-cultured primary rat hepatocytes and rats in vivo: a toxicogenomics approach. Drug Metab Dispos 34 12 (2006) 2083-2090
58. Kostrubsky V.E., Strom S.C., Hanson J., Urda E., Rose K., Burliegh J., et al. Evaluation of hepatotoxic potential of drugs by inhibition of bile-acid transport in cultured primary human hepatocytes and intact rats. Toxicol Sci 76 1 (2003) 220-228
59. Kemp D.C., Zamek-Gliszczynski M.J., and Brouwer K.L. Xenobiotics inhibit hepatic uptake and biliary excretion of taurocholate in rat hepatocytes. Toxicol Sci 83 2 (2005) 207-214