Differentiation of liver progenitor cell line to functional organotypic cultures in 3D nanofibrillar cellulose and hyaluronan-gelatin hydrogels

Biomaterials

Volumn 35, Issue 19, 2014, Pages 5110-5121

  Malinen, Melina M ^a   Kanninen, Liisa K ^a   Corlu, Anne ^b   Isoniemi, Helena M ^c   Lou, Yan Ru ^a   Yliperttula, Marjo L ^a   Urtti, Arto O ^a,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Univ Rennes   (France)

^c HOSPITAL DISTRICT OF HELSINKI AND UUSIMAA   (Finland)

^d UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

3D Cell culture; Cell differentiation; Hepatocyte; Multicellular spheroids; Nanocellulose; Organotypic

Indexed keywords

CELL CULTURE; CELLS; CELLULOSE; HYALURONIC ACID; METABOLISM; MORPHOLOGY; PHYSIOLOGICAL MODELS; THREE DIMENSIONAL; TISSUE ENGINEERING; WOOD;

3-D CELL CULTURE; CELL DIFFERENTIATION; HEPATOCYTES; MULTICELLULAR SPHEROID; NANO-CELLULOSE; ORGANOTYPIC;

HYDROGELS;

ALBUMIN; CELLULOSE; CYTOCHROME P450 3A4; CYTOKERATIN 19; F ACTIN; GELATIN; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HYALURONIC ACID; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 1; NANOFIBRILLAR CELLULOSE; NANOMATERIAL; UNCLASSIFIED DRUG; HYDROGEL; NANOFIBER;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYDROGEL; INTRAHEPATIC BILE DUCT; LIVER CELL; LIVER CELL CULTURE; MALE; MULTICELLULAR SPHEROID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STEM CELL; ADOLESCENT; CELL LINE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; IN VITRO STUDY; LIVER; MIDDLE AGED; PHARMACOLOGY; PHYSIOLOGY; PRESCHOOL CHILD;

HYALURONIC ACID; METABOLISM; PHYSIOLOGY; SPHERES; THREE DIMENSIONAL DESIGN; TISSUE CULTURE; WOOD;

ADOLESCENT; ADULT; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CELLULOSE; CHILD, PRESCHOOL; FEMALE; GELATIN; HUMANS; HYALURONIC ACID; HYDROGEL; IN VITRO TECHNIQUES; LIVER; MALE; MIDDLE AGED; NANOFIBERS; STEM CELLS;

EID: 84898460722     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.020     Document Type: Article

References (41)

1. Abe K., Bridges A.S., Brouwer K.L. Use of sandwich-cultured human hepatocytes to predict biliary clearance of angiotensin II receptor blockers and HMG-CoA reductase inhibitors. Drug Metab Dispos 2009, 37:447-452.
2. Pedersen J.M., Matsson P., Bergstrom C.A., Hoogstraate J., Noren A., Lecluyse E.L., et al. Early identification of clinically relevant drug interactions with the human bile salt export pump (BSEP/ABCB11). Toxicol Sci 2013, 136:328-343.
3. Noor F., Niklas J., Muller-Vieira U., Heinzle E. An integrated approach to improved toxicity prediction for the safety assessment during preclinical drug development using Hep G2 cells. Toxicol Appl Pharmacol 2009, 237:221-231.
4. Josse R., Aninat C., Glaise D., Dumont J., Fessard V., Morel F., et al. Long-term functional stability of human HepaRG hepatocytes and use for chronic toxicity and genotoxicity studies. Drug Metab Dispos 2008, 36:1111-1118.
5. Antherieu S., Chesne C., Li R.Y., Camus S., Lahoz A., Picazo L., et al. Stable expression, activity, and inducibility of cytochromes P450 in differentiated HepaRG cells. Drug Metab Dispos 2010, 38:516-525.
6. Lubberstedt M., Muller-Vieira U., Mayer M., Biemel K.M., Knospel F., Knobeloch D., et al. HepaRG human hepatic cell line utility as a surrogate for primary human hepatocytes in drug metabolism assessment in vitro. J Pharmacol Toxicol 2011, 63:59-68.
7. Kanebratt K.P., Andersson T.B. HepaRG cells as an in vitro model for evaluation of cytochrome P450 induction in humans. Drug Metab Dispos 2008, 36:137-145.
8. Darnell M., Schreiter T., Zeilinger K., Urbaniak T., Soderdahl T., Rossberg I., et al. Cytochrome P450-Dependent metabolism in HepaRG cells cultured in a dynamic three-dimensional bioreactor. Drug Metab Dispos 2011, 39:1131-1138.
9. Salerno S., Campana C., Morelli S., Drioli E., De Bartolo L. Human hepatocytes and endothelial cells in organotypic membrane systems. Biomaterials 2011, 32:8848-8859.
10. Skardal A., Smith L., Bharadwaj S., Atala A., Soker S., Zhang Y. Tissue specific synthetic ECM hydrogels for 3-D in vitro maintenance of hepatocyte function. Biomaterials 2012, 33:4565-4575.
11. Meli L., Jordan E.T., Clark D.S., Linhardt R.J., Dordick J.S. Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems. Biomaterials 2012, 33:9087-9096.
12. Bhattacharya M., Malinen M.M., Lauren P., Lou Y.R., Kuisma S.W., Kanninen L., et al. Nanofibrillar cellulose hydrogel promotes three-dimensional liver cell culture. J Control Release 2012, 164:291-298.
13. Lou Y.R., Kanninen L., Kuisma T., Niklander J., Noon L.A., Burks D., et al. The use of nanofibrillar cellulose hydrogel as a flexible three-dimensional model to culture human pluripotent stem cells. Stem Cells Devel 2014, 23:380-392.
14. Klemm D., Kramer F., Moritz S., Lindstrom T., Ankerfors M., Gray D., et al. Nanocelluloses: a new family of nature-based materials. Angew Chem Int Ed 2011, 50:5438-5466.
15. Prestwich G.D., Liu Y., Yu B., Shu X.Z., Scott A. 3-D culture in synthetic extracellular matrices: new tissue models for drug toxicology and cancer drug discovery. Adv Enzyme Regul 2007, 47:196-207.
16. Vanderhooft J.L., Alcoutlabi M., Magda J.J., Prestwich G.D. Rheological properties of cross-linked hyaluronan-gelatin hydrogels for tissue engineering. Macromol Biosci 2009, 9:20-28.
17. Gripon P., Rumin S., Urban S., Le Seyec J., Glaise D., Cannie I., et al. Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci 2002, 99:15655-15660.
18. Cerec V., Glaise D., Garnier D., Morosan S., Turlin B., Drenou B., et al. Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology 2007, 45:957-967.
19. Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012, 13.
20. Toivonen S., Ojala M., Hyysalo A., Ilmarinen T., Rajala K., Pekkanen-Mattila M., et al. Comparative analysis of targeted differentiation of human induced pluripotent stem cells (hiPSCs) and human embryonic stem cells reveals variability associated with incomplete transgene silencing in retrovirally derived hiPSC lines. Stem Cells Transl Med 2013, 2:83-93.
21. Mikkola M., Olsson C., Palgi J., Ustinov J., Palomaki T., Horelli-Kuitunen N., et al. Distinct differentiation characteristics of individual human embryonic stem cell lines. BMC Dev Biol 2006, 6:40.
22. Malinen M.M., Palokangas H., Yliperttula M., Urtti A. Peptide nanofiber hydrogel induces formation of bile canaliculi structures in three-dimensional hepatic cell culture. Tissue Engn Part A 2012, 18:2418-2425.
23. Meisenheimer P.L., Uyeda H.T., Ma D.P., Sobol M., McDougall M.G., Corona C., et al. Proluciferin acetals as bioluminogenic substrates for cytochrome P450 activity and probes for CYP3A inhibition. Drug Metab Dispos 2011, 39:2403-2410.
24. Aninat C., Piton A., Glaise D., Le Charpentier T., Langouet S., Morel F., et al. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab Dispos 2006, 34:75-83.
25. Chen Y.T., Sonnaert M., Roberts S.J., Luyten F.P., Schrooten J. Validation of a pico green-based DNA quantification integrated in an RNA extraction method for two-dimensional and three-dimensional cell cultures. Tissue Engn Part C 2012, 18:444-452.
26. Barth C.A., Schwarz L.R. Transcellular transport of fluorescein in hepatocyte monolayers: evidence for functional polarity of cells in culture. Proc Natl Acad Sci 1982, 79:4985-4987.
27. Bravo P., Bender V., Cassio D. Efficient in vitro vectorial transport of a fluorescent conjugated bile acid analogue by polarized hepatic hybrid WIF-B and WIF-B9 cells. Hepatology 1998, 27:576-583.
28. Lai Y., Xing L., Poda G.I., Hu Y. Structure-activity relationships for interaction with multidrug resistance protein 2 (ABCC2/MRP2): the role of torsion angle for a series of biphenyl-substituted heterocycles. Drug Metab Dispos 2007, 35:937-945.
29. Godoy P., Hewitt N.J., Albrecht U., Andersen M.E., Ansari N., Bhattacharya S., et al. 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. Arch Toxicol 2013, 87:1315-1530.
30. Hart S.N., Li Y., Nakamoto K., Subileau E.A., Steen D., Zhong X.B. A comparison of whole genome gene expression profiles of HepaRG cells and HepG2 cells to primary human hepatocytes and human liver tissues. Drug Metab Dispos 2010, 38:988-994.
31. Gunness P., Mueller D., Shevchenko V., Heinzle E., Ingelman-Sundberg M., Noor F. 3D Organotypic cultures of human HepaRG cells: a tool for in vitro toxicity studies. Toxicol Sci 2013, 133:67-78.
32. Vartiainen J., Pohler T., Sirola K., Pylkkanen L., Alenius H., Hokkinen J., et al. Health and environmental safety aspects of friction grinding and spray drying of microfibrillated cellulose. Cellulose 2011, 18:775-786.
33. Ghosh K., Pan Z., Guan E., Ge S., Liu Y., Nakamura T., et al. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 2007, 28:671-679.
34. Liu Y., Shu X.Z., Gray S.D., Prestwich G.D. Disulfide-crosslinked hyaluronan-gelatin sponge: growth of fibrous tissue in vivo. J Biomed Mater Res A 2004, 68:142-149.
35. Karppinen A., Saarinen T., Salmela J., Laukkanen A., Nuopponen M., Seppala J. Flocculation of microfibrillated cellulose in shear flow. Cellulose 2012, 19:1807-1819.
36. Paakko M., Ankerfors M., Kosonen H., Nykanen A., Ahola S., Osterberg M., et al. Enzymatic hydrolysis combined with mechanical shearing and high-pressure homogenization for nanoscale cellulose fibrils and strong gels. Biomacromolecules 2007, 8:1934-1941.
37. Lambert C.B., Spire C., Claude N., Guillouzo A. Dose- and time-dependent effects of phenobarbital on gene expression profiling in human hepatoma HepaRG cells. Toxicol Appl Pharmacol 2009, 234:345-360.
38. Le Vee M., Jigorel E., Glaise D., Gripon P., Guguen-Guillouzo C., Fardel O. Functional expression of sinusoidal and canalicular hepatic drug transporters in the differentiated human hepatoma HepaRG cell line. Eur J Pharm Sci 2006, 28:109-117.
39. Wang E.J., Casciano C.N., Clement R.P., Johnson W.W. Fluorescent substrates of sister-P-glycoprotein (BSEP) evaluated as markers of active transport and inhibition: evidence for contingent unequal binding sites. Pharm Res 2003, 20:537-544.
40. Feller N., Broxterman H.J., Wahrer D.C.R., Pinedo H.M. Atp-dependent efflux of calcein by the multidrug-resistance protein (MRP) - no inhibition by intracellular glutathione depletion. FEBS Lett 1995, 368:385-388.
41. Litman T., Brangi M., Hudson E., Fetsch P., Abati A., Ross D.D., et al. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J Cell Sci 2000, 113(Pt 11):2011-2021.