Maintenance of human hepatocyte function in vitro by liver-derived extracellular matrix gels

Tissue Engineering - Part A

Volumn 16, Issue 3, 2010, Pages 1075-1082

  Sellaro, Tiffany L ^a   Ranade, Aarati ^b   Faulk, Denver M ^c   McCabe, George P ^d   Dorko, Kenneth ^b   Badylak, Stephen F ^a,e   Strom, Stephen C ^b,e  

^a Department of Bioengineering ^*  (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; ENZYME ACTIVITY; GENE EXPRESSION; METABOLISM; PHYSIOLOGY; SUBSTRATES; TISSUE ENGINEERING;

ALBUMIN SECRETION; AMMONIA METABOLISM; ASSIST DEVICE; EXTRACELLULAR MATRICES; HEPATIC TRANSPORTS; HEPATOCYTE CULTURE; HEPATOCYTE FUNCTIONS; HEPATOCYTES; HUMAN HEPATOCYTES; IN-VITRO; IN-VIVO; LIVER DISEASE; MATRIX; MICROENVIRONMENTS; RATE-LIMITING STEPS; REGENERATIVE MEDICINE; TEMPORARY SUPPORT; THERAPEUTIC STRATEGY; TRANSPORTER EXPRESSION; TWO LAYERS;

LIVER;

SUS;

ABC TRANSPORTER; ABCB11 PROTEIN, HUMAN; ALBUMINOID; AMMONIA; COTRANSPORTER; DNA; MESSENGER RNA; ORGANIC ANION TRANSPORTER; SODIUM BILE ACID COTRANSPORTER; SODIUM-BILE ACID COTRANSPORTER;

ADULT; AGED; ANIMAL; ARTICLE; CELL CULTURE; CELL SHAPE; CYTOLOGY; EXTRACELLULAR MATRIX; FEMALE; GEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER; LIVER CELL; MALE; METABOLISM; MIDDLE AGED; SECRETION; SWINE; TRANSPORT AT THE CELLULAR LEVEL;

AGED; ALBUMINS; AMMONIA; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL SHAPE; CELLS, CULTURED; DNA; EXTRACELLULAR MATRIX; FEMALE; GELS; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; LIVER; MALE; MIDDLE AGED; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; RNA, MESSENGER; SUS SCROFA; SYMPORTERS; YOUNG ADULT;

EID: 77649262057     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0587     Document Type: Article

References (45)

1. Organ Procurement and Transplantation Network (OPTN). Available at www.optn.org/data/.
2. The Organ Procurement and Transplantation Network. 2008. Available at www.optn.org/latestData/rptData.asp.
3. Allen, J.W., and Bhatia, S.N. Engineering liver therapies for the future. Tissue Eng 8, 725, 2002.
4. Fiegel, H.C., Kaufmann, P.M., Bruns, H., Kluth, D., Horch, R.E., Vacanti, J.P., and Kneser, U. Hepatic tissue engineering: from transplantation to customized cell-based liver directed therapies from the laboratory. J Cell Mol Med 12, 56, 2008.
5. Borenstein, J.T., Weinberg, E.J., Orrick, B.K., Sundback, C, Kaazempur-Mofrad, M.R., and Vacanti, J.P. Microfabrication of three-dimensional engineered scaffolds. Tissue Eng 13, 1837, 2007.
6. Ohashi, K., Yokoyama, T., Yamato, M., Kuge, H., Kanehiro, H., Tsutsumi, M., Amanuma, T., Iwata, H., Yang, J., Okano, T., and Nakajima, Y. Engineering functional two-and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med 13, 880, 2007.
7. Schuetz, E.G., Li, D., Omiecinski, C.J., Muller-Eberhard, U., Kleinman, H.K., Elswick, B., and Guzelian, P.S. Regulation of gene expression in adult rat hepatocytes cultured on a basement membrane matrix. J Cell Physiol 134, 309, 1988.
8. Michalopoulos, G., Sattler, G., Sattler, C, and Pitot, H.C. Interaction of chemical carcinogens and drug-metabolizing enzymes in primary cultures of hepatic cells from the rat. Am J Pathol 85, 755, 1976.
9. Hamilton, G.A., Jolley, S.L., Gilbert, D., Coon, D.J., Barros, S., and LeCluyse, E.L. Regulation of cell morphology and cytochrome P450 expression in human hepatocytes by extracellular matrix and cell-cell interactions. Cell Tissue Res 306, 85, 2001.
10. Reid, L.M., Gaitmaitan, Z., Arias, I., Ponce, P., and Rojkind, M. Long-term cultures of normal rat hepatocytes on liver biomatrix. Ann NY Acad Sci 349, 70, 1980.
11. Watt, F.M. Cell culture models of differentiation. FASEB J 5, 287, 1991.
12. Lin, P., Chan, W.C., Badylak, S.F., and Bhatia, S.N. Assessing porcine liver-derived biomatrix for hepatic tissue engineering. Tissue Eng 10, 1046, 2004.
13. Gross-Steinmeyer, K., Stapleton, P.L., Tracy, J.H., Bammler, T.K., Lehman, T., Strom, S.C., and Eaton, D.L. Influence of Matrigel-overlay on constitutive and inducible expression of nine genes encoding drug-metabolizing enzymes in primary human hepatocytes. Xenobiotica 35, 419, 2005.
14. LeCluyse, E.L., Fix, J.A., Audus, K.L., and Hochman, J.H. Regeneration and maintenance of bile canalicular networks in collagen-sandwiched hepatocytes. Toxicol In Vitro 14, 117, 2000.
15. 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, 237, 1991.
16. Sidhu, J.S., Farin, F.M., and Omiecinski, C.J. Influence of extracellular matrix overlay on phenobarbital-mediated induction of CYP2B1, 2B2, and 3A1 genes in primary adult rat hepatocyte culture. Arch Biochem Biophys 301, 103, 1993.
17. 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), C1764, 1994.
18. Moghe, P.V., Berthiaume, F., Ezzell, R.M., Toner, M, Tompkins, R.G., and Yarmush, M.L. Culture matrix configuration and composition in the maintenance of hepatocyte polarity and function. Biomaterials 17, 373, 1996.
19. Zeisberg, M., Kramer, K., Sindhi, N., Sarkar, P., Upton, M., and Kalluri, R. De-differentiation of primary human hepa-tocytes depends on the composition of specialized liver basement membrane. Mol Cell Biochem 283, 181, 2006.
20. LeCluyse, E., Madan, A., Hamilton, G., Carroll, K., DeHann, R., and Parkinson, A. Expression and regulation of cytochrome P450 enzymes in primary cultures of human hepa-tocytes. J Biochem Mol Toxicol 14, 177, 2000.
21. Silva, J.M., Morin, P.E., Day, S.H., Kennedy, B.P., Payette, P., Rushmore, T., Yergey, J.A., and Nicoll-Griffith, D.A. Refinement of an in vitro cell model for cytochrome P450 induction. Drug Metab Dispos 26, 490,1998.
22. Kern, A., Bader, A., Pichlmayr, R., and Sewing, K.F. Drug metabolism in hepatocyte sandwich cultures of rats and humans. Biochem Pharmacol 54, 761,1997.
23. Jasmund, I., Schwientek, S., Acikgoz, A., Langsch, A., Ma-chens, H.G., and Bader, A. The influence of medium composition and matrix on long-term cultivation of primary porcine and human hepatocytes. Biomol Eng 24, 59, 2007.
24. Brown, B., Lindberg, K., Reing, J., Stolz, D.B., and Badylak, S.F. The basement membrane component of biologic scaffolds derived from extracellular matrix. Tissue Eng 12, 519, 2006.
25. Gilbert, T.W., Sellaro, T.L., and Badylak, S.F. Decellulariza-tion of tissues and organs. Biomaterials 27, 3675, 2006.
26. Freytes, D.O., Martin, J., Velankar, S.S., Lee, A.S., and Badylak, S.F. Preparation and rheological characterization of a gel form of the porcine urinary bladder matrix. Biomaterials 29, 1630, 2008.
27. Strom, S.C., Pisarov, L.A., Dorko, K., Thompson, M.T., Schuetz, J.D., and Schuetz, E.G. Use of human hepatocytes to study P450 gene induction. Methods Enzymol 272, 388, 1996.
28. Kostrubsky, V.E., Strom, S.C., Hanson, J., Urda, E., Rose, K., Burliegh, J., Zocharski, P., Cai, H., Sinclair, J.F., and Sahi, J. Evaluation of hepatotoxic potential of drugs by inhibition of bile-acid transport in cultured primary human hepatocytes and intact rats. Toxicol Sci 76, 220, 2003.
29. Cepko, C.L. The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr Opin Neurobiol 9, 37, 1999.
30. Jadhav, A.P., Mason, H.A., and Cepko, C.L. Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133, 913, 2006.
31. Sellaro, T.L., Ravindra, A.K., Stolz, D.B., and Badylak, S.F. Maintenance of hepatic sinusoidal endothelial cell pheno-type in vitro using organ-specific extracellular matrix scaffolds. Tissue Eng 13, 2301, 2007.
32. Hodde, J.P., Badylak, S.F., Brightman, A.O., and Voytik-Harbin, S.L. Glycosaminoglycan content of small intestinal submucosa: a bioscaffold for tissue replacement. Tissue Eng 2, 209, 1996.
33. Voytik-Harbin, S.L., Brightman, A.O., Kraine, M.R., Wais-ner, B., and Badylak, S.F. Identification of extractable growth factors from small intestinal submucosa. J Cell Biochem 67, 478, 1997.
34. Kleinman, H.K., McGarvey, M.L., Liotta, L.A., Robey, P.G., Tryggvason, K., and Martin, G.R. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21, 6188, 1982.
35. Futaki, S., Hayashi, Y., Yamashita, M., Yagi, K., Bono, H., Hayashizaki, Y., Okazaki, Y., and Sekiguchi, K. Molecular basis of constitutive production of basement membrane components. Gene expression profiles of Engelbreth-Holm-Swarm tumor and F9 embryonal carcinoma cells. J Biol Chem 278, 50691, 2003.
36. Couchman, J.R., Kapoor, R., Sthanam, M., and Wu, R.R. Per-lecan and basement membrane-chondroitin sulfate proteoglycan (bamacan) are two basement membrane chondroitin/ dermatan sulfate proteoglycans in the Engelbreth-Holm- Swarm tumor matrix. J Biol Chem 271, 9595, 1996.
37. Kato, S., Otsu, K., Ohtake, K., Kimura, Y., Yashiro, T., Suzuki, T., and Akamatsu, N. Concurrent changes in sinusoidal expression of laminin and affinity of hepatocytes to laminin during rat liver regeneration. Exp Cell Res 198, 59, 1992.
38. Reid, L.M., Fiorino, A.S., Sigal, S.H., Brill, S., and Hoist, P.A. Extracellular matrix gradients in the space of Disse: relevance to liver biology. Hepatology 15, 1198, 1992.
39. Hubbell, J.A. Materials as morphogenetic guides in tissue engineering. Curr Opin Biotechnol 14, 551, 2003.
40. Dow, J.A., Clark, P., Connolly, P., Curtis, A.S., and Wilkinson, CD. Novel methods for the guidance and monitoring of single cells and simple networks in culture. J Cell Sci Suppl 8, 55, 1987.
41. Clark, P., Connolly, P., Curtis, A.S., Dow, J.A., and Wilkinson, CD. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108, 635, 1990.
42. Clark, P., Connolly, P., Curtis, A.S., Dow, J.A., and Wilkinson, CD. Topographical control of cell behaviour. I. Simple step cues. Development 99, 439, 1987.
43. den Braber, E.T., de Ruijter, J.E., Smits, H.T., Ginsel, L.A., von Recum, A.F., and Jansen, J.A. Quantitative analysis of cell proliferation and orientation on substrata with uniform parallel surface micro-grooves. Biomaterials 17, 1093, 1996.
44. Chehroudi, B., Soorany, E., Black, N., Weston, L., and Brunette, D.M. Computer-assisted three-dimensional reconstruction of epithelial cells attached to percutaneous implants. J Biomed Mater Res 29, 371, 1995.
45. Zeltinger, J., Sherwood, J.K., Graham, D.A., Mueller, R., and Griffith, L.G. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng 7, 557, 2001