Cytomimetic engineering of hepatocyte morphogenesis and function by substrate-based presentation of acellular E-cadherin

Tissue Engineering

Volumn 11, Issue 5-6, 2005, Pages 734-750

  Semler, Eric J ^a   Dasgupta, Anouska ^a   Moghe, Prabhas V ^a,b,c  

^a The State University of New Jersey   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c C230 Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; CELLS; CYTOLOGY; LIGAMENTS; PROTEINS; TWO DIMENSIONAL; UREA;

CYTOMIMETIC PROCESS; E-CADHERIN; HEPATOCELLULAR PHENOTYPES; HEPATOCYTE MORPHOGENESIS;

BIOMEDICAL ENGINEERING;

CADHERIN; IMMUNOGLOBULIN FC FRAGMENT; LIGAND; PROTEIN A; UVOMORULIN;

ARTICLE; CELL AGGREGATION; CELL DENSITY; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CHIMERA; CYTOMIMETIC ENGINEERING; IN VITRO STUDY; INTRACELLULAR TRANSPORT; LIGAND BINDING; LIVER CELL; LIVER FUNCTION; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RAT; SIGNAL TRANSDUCTION; SPATIAL DISCRIMINATION; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING; TISSUE SPECIFICITY;

ANIMALS; BIOCOMPATIBLE MATERIALS; CADHERINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HEPATOCYTES; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; RATS; RATS, INBRED F344; TIME FACTORS; TISSUE ENGINEERING;

EID: 21844459207     PISSN: 10763279     EISSN: None     Source Type: Journal    
DOI: 10.1089/ten.2005.11.734     Document Type: Article

References (91)

1. Harrington, K.J., Syrigos, K.N., and Harington, K.J. The role of E-cadherin-catenin complex: More than an intercellular glue? Ann. Surg. Oncol. 7, 783, 2000.
2. Gumbiner, B.M. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84, 345, 1996.
3. Kemler, R. Classical cadherins. Semin. Cell Biol. 3, 149, 1992.
4. Takeichi, M. Cadherins: A molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59, 237, 1990.
5. Vleminckx, K., and Kemler, R. Cadherins and tissue formation: Integrating adhesion and signaling. Bioessays 21, 211, 1999.
6. Huber, O., Bierkamp, C., and Kemler, R. Cadherins and catenins in development. Curr. Opin. Cell Biol. 8, 685, 1996.
7. Takeichi, M. Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7, 619, 1995.
8. Steinberg, M.S., and Takeichi, M. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl. Acad. Sci. U.S.A. 91, 206, 1994.
9. Ivanov, D.B., Philippova, M.P., and Tkachuk, V.A. Structure and functions of classical cadherins. Biochemistry (Mosc) 66, 1174, 2001.
10. Owens, D.W., Brunton, V.G., Parkinson, E.K., and Frame, M.C. E-cadherin at the cell periphery is a determinant of keratinocyte differentiation in vitro. Biochem. Biophys. Res. Commun. 269, 369, 2000.
11. Hines, M.D., Jin, H.C., Wheelock, M.J., and Jensen, P.J. Inhibition of cadherin function differentially affects markers of terminal differentiation in cultured human keratinocytes. J. Cell Sci. 112, 4569, 1999.
12. Redfield, A., Nieman, M.T., and Knudsen, K.A. Cadherins promote skeletal muscle differentiation in three-dimensional cultures. J. Cell Biol. 138, 1323, 1997.
13. Cavallaro, U., Schaffhauser, B., and Christofori, G. Cadherins and the tumour progression: Is it all in a switch? Cancer Lett. 176, 123, 2002.
14. Van Aken, E., De Wever, O., Correia da Rocha, A.S., and Mareel, M. Defective E-cadherin/catenin complexes in human cancer. Virchows Arch. 439, 725, 2001.
15. Wijnhoven, B.P., Dinjens, W.N., and Pignatelli, M. E-cadherin-catenin cell-cell adhesion complex and human cancer. Br. J. Surg. 87, 992, 2000.
16. Mareel, M., Vleminckx, K., Vermeulen, S., Van, G., Bracke, M., and van Roy, F. Downregulation in vivo of the invasion-suppressor molecule E-cadherin in experimental and clinical cancer. Princess Takamatsu Symp. 24, 63, 1994.
17. Steinberg, M.S., and McNutt, P.M. Cadherins and their: connections: Adhesion junctions have broader functions. Curr. Opin. Cell Biol. 11, 554, 1999.
18. Potter, E., Bergwitz, C., and Brabant, G. The cadherin-catenin system: Implications for growth and differentiation of endocrine tissues. Endocr. Rev. 20, 207, 1999.
19. El-Bahrawy, M.A., and Pignatelli, M. E-cadherin and catenins: Molecules with versatile roles in normal and neoplastic epithelial cell biology. Microsc. Res. Tech. 43, 224, 1998.
20. Marrs, J.A., and Nelson, W.J. Cadherin cell adhesion molecules in differentiation and embryogenesis. Int. Rev. Cytol. 165, 159, 1996.
21. Brieva, T.A., and Moghe, P.V. Engineering the hepatocyte differentiation/proliferation balance by acellular cadherin micropresentation. Tissue Eng. 10, 553, 2004.
22. Brieva, T.A., and Moghe, P.V. Exogenous cadherin microdisplay can interfere with endogenous signaling and reprogram gene expression in cultured hepatocytes. Biotechnol. Bioeng. 85, 283, 2004.
23. Tomschy, A., Fauser, C., Landwehr, R., and Engel, J. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 15, 3507, 1996.
24. Takeda, H., Shimoyama, Y., Nagafuchi, A., and Hirohashi, S. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat. Struct. Biol. 6, 310, 1999.
25. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18, 1738, 1999.
26. Koch, A.W., Pokutta, S., Lustig, A., and Engel, J. Calcium binding and homoassociation of E-cadherin domains. Biochemistry 36, 7697, 1997.
27. Zhu, B., Chappuis-Flament, S., Wong, E., Jensen, I.E., Gumbiner, B.M., and Leckband, D. Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys. J. 84, 4033, 2003.
28. Leckband, D., and Sivasankar, S. Mechanism of homophilic cadherin adhesion. Curr. Opin. Cell Biol. 12, 587, 2000.
29. Kusumi, A., Suzuki, K., and Koyasako, K. Mobility and cytoskeletal interactions of cell adhesion receptors. Curr. Opin. Cell Biol. 11, 582, 1999.
30. Troyanovsky, S.M. Mechanism of cell-cell adhesion complex assembly. Curr. Opin. Cell Biol. 11, 561, 1999.
31. Ben-Ze'ev, A. The dual role of cytoskeletal anchor proteins in cell adhesion and signal transduction. Ann. N.Y. Acad. Sci. 886, 37, 1999.
32. Nieset, J.E., Redfield, A.R., Jin, F., Knudsen, K.A., Johnson, K.R., and Wheelock, M.J. Characterization of the interactions of α-catenin with α-actinin and β-catenin/plakoglobin. J. Cell Sci. 110, 1013, 1997.
33. Omelchenko, T., Fetisova, E., Ivanova, O., Bonder, E.M., Feder, H., Vasiliev, J.M., and Gelfand, I.M. Contact interactions between epitheliocytes and fibroblasts: Formation of heterotypic cadherin-containing adhesion sites is accompanied by local cytoskeletal reorganization. Proc. Natl. Acad. Sci. U.S.A. 98, 8632, 2001.
34. Nachtigal, P., Gojova, A., and Semecky, V. The role of epithelial and vascular-endothelial cadherin in the differentiation and maintenance of tissue integrity. Acta Medica (Hradec Kralove) 44, 83, 2001.
35. Goichberg, P., Shtutman, M., Ben-Ze'ev, A., and Geiger, B. Recruitment of β-catenin to cadherin-mediated intercellular adhesions is involved in myogenic induction. J. Cell Sci. 114, 1309, 2001.
36. Orsulic, S., Huber, O., Aberle, H., Arnold, S., and Kemler, R. E-cadherin binding prevents β-catenin nuclear localization and β-catenin/LEF-1- mediated transactivation. J. Cell Sci. 112, 1237, 1999.
37. Novak, A., and Dedhar, S. Signaling through β-catenin and Lef/Tcf. Cell. Mol. Life Sci. 56, 523, 1999.
38. Knudsen, K.A., Frankowski, C., Johnson, K.R., and Wheelock, M.J. A role for cadherins in cellular signaling and differentiation. J. Cell Biochem. Suppl. 31, 168, 1998.
39. Davis, M.W., and Vacanti, J.P. Toward development of an implantable tissue engineered liver. Biomaterials 17, 365, 1996.
40. Yarmush, M.L., Toner, M., Dunn, J.C., Rotem, A., Rubel, A., and Tompkins, R.G. Hepatic tissue engineering: Development of critical technologies. Ann. N.Y. Acad. Sci. 665, 238, 1992.
41. Sundback, C.A., and Vacanti, J.P. Alternatives to liver transplantation: From hepatocyte transplantation to tissue-engineered organs. Gastroenterology 118, 438, 2000.
42. Arkadopoulos, N., Detry, O., Rozga, J., and Demetriou, A.A. Liver assist systems: State of the art. Int. J. Artif. Organs 21, 781, 1998.
43. Semler, E.J., and Moghe, P.V. Engineering hepatocyte functional fate through growth factor dynamics: The role of cell morphologic priming. Biotechnol. Bioeng. 75, 510, 2001.
44. Semler, E.J., Ranucci, C.S., and Moghe, P.V. Mechanochemical manipulation of hepatocyte aggregation can selectively induce or repress liver-specific function. Biotechnol. Bioeng. 69, 359, 2000.
45. Ranucci, C.S., Kumar, A., Batra, S.P., and Moghe, P.V. Control of hepatocyte function on collagen foams: Sizing matrix pores toward selective induction of 2-D and 3-D cellular morphogenesis. Biomaterials 21, 783, 2000.
46. Hansen, L.K., Hsiao, C., Friend, J.R., Wu, F.J., Bridge, G.A., Remmel, R.P., Cerra, F.B., and Hu, W. Enhanced morphology and function in hepatocyte spheroids: A model of tissue self-assembly. Tissue Eng. 4, 65, 1998.
47. Lindblad, W.J., Schuetz, E.G., Redford, K.S., and Guzelian, P.S. Hepatocellular phenotype in vitro is influenced by biophysical features of the collagenous substratum. Hepatology 13, 282, 1991.
48. 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.
49. Bucher, N.L.R., Robinson, G.S., and Farmer, S.R. Effects of extracellular matrix on hepatocyte growth and gene expression: Implications for hepatic regeneration and the repair of liver injury. Semin. Liver Dis. 10, 11, 1990.
50. Moghe, P.V., Coger, R.N., Toner, M., and Yarmush, M.L. Cell-cell interactions are essential for maintenance of hepatocyte function in collagen gel but not on matrigel. Biotechnol. Bioeng. 56, 706, 1997.
51. Mizuno, K., Higuchi, O., Tajima, H., Yonemasu, T., and Nakamura, T. Cell density-dependent regulation of hepatocyte growth factor receptor on adult rat hepatocytes in primary culture. J. Biochem. 114, 96, 1993.
52. Takehara, T., Matsumoto, K., and Nakamura, T. Cell density-dependent regulation of albumin synthesis and DNA synthesis in rat hepatocytes by hepatocyte growth factor. J. Biochem. 112, 330, 1992.
53. Nakamura, T., Nakayama, Y., and Ichihara, A. Reciprocal modulation of growth and liver functions of mature rat hepatocytes in primary culture by an extract of hepatic plasma membranes. J. Biol. Chem. 259, 8056, 1984.
54. Nakamura, T., Yoshimoto, K., Nakayama, Y., Tomita, Y., and Ichihara, A. Reciprocal modulation of growth and differentiated functions of mature rat hepatocytes in primary culture by cell-cell contact and cell membranes. Proc. Natl. Acad. Sci. U.S.A. 80, 7229, 1983.
55. 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.
56. Hou, D.X., Arimura, M., Fukuda, M., Oka, T., and Fujii, M. Expression of cell adhesion molecule and albumin genes in primary culture of rat hepatocytes. Cell Biol. Int. 25, 239, 2001.
57. Kim, T.H., Bowen, W.C., Stolz, D.B., Runge, D., Mars, W.M., and Michalopoulos, G.K. Differential expression and distribution of focal adhesion and cell adhesion molecules in rat hepatocyte differentiation. Exp. Cell Res. 244, 93, 1998.
58. Brieva, T.A., and Moghe, P.V. Functional engineering of hepatocytes via heterocellular presentation of a homoadhesive molecule, E-cadherin. Biotechnol. Bioeng. 76, 295, 2001.
59. Utton, M.A., Eickholt, B., Howell, F.V., Wallis, J., and Doherty, P. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J. Neurochem. 76, 1421, 2001.
60. Bixby, J.L., and Zhang, R. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J. Cell Biol. 110, 1253, 1990.
61. Schnadelbach, O., Blaschuk, O.W., Symonds, M., Gour, B.J., Doherty, P., and Fawcett, J.W. N-cadherin influences migration of oligodendrocytes on astrocyte monolayers. Mol. Cell. Neurosci. 15, 288, 2000.
62. Rubinek, T., Yu, R., Hadani, M., Barkai, G., Nass, D., Melmed, S., and Shimon, I. The cell adhesion molecules N-cadherin and neural cell adhesion molecule regulate human growth hormone: A novel mechanism for regulating pituitary hormone secretion. J. Clin. Endocrinol. Metab. 88, 3724, 2003.
63. Lambert, M., Choquet, D., and Mege, R.M. Dynamics of ligand-induced, Rac1-dependent anchoring of cadherins to the actin cytoskeleton. J. Cell Biol. 157, 469, 2002.
64. Goichberg, P., and Geiger, B. Direct involvement of N-cadherin-mediated signaling in muscle differentiation. Mol. Biol. Cell 9, 3119, 1998.
65. Lambert, M., Padilla, F., and Mege, R.M. Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: Contribution of both outside-in and inside-out signals. J. Cell Sci. 113, 2207, 2000.
66. Levenberg, S., Katz, B.Z., Yamada, K.M., and Geiger, B. Long-range and selective autoregulation of cell-cell or cell-matrix adhesions by cadherin or integrin ligands. J. Cell Sci. 111, 347, 1998.
67. Kovacs, E.M., Ali, R.G., McCormack, A.J., and Yap, A.S. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708, 2002.
68. Kovacs, E.M., Goodwin, M., Ali, R.G., Paterson, A.D., and Yap, A.S. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr. Biol. 12, 379, 2002.
69. Chappuis-Flament, S., Wong, E., Hicks, L.D., Kay, C.M., and Gumbiner, B.M. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154, 231, 2001.
70. Eliasson, M., Olsson, A., Palmcrantz, E., Wiberg, K., Inganas, M., Guss, B., Lindberg, M., and Uhlen, M. Chimeric IgG-binding receptors engineered from staphylococcal protein A and streptococcal protein G. J. Biol. Chem. 263, 4323, 1988.
71. Seglen, P.O. Preparation of isolated rat liver cells. Methods Cell Biol. 13, 29, 1976.
72. Sharma, R.I., Kohn, J., and Moghe, P.V. PEG accelerates cell motility on protein-based PEG-polycarbonate substrates: A mechanism for cell-guided ligand remodeling. J. Biomed. Mater. Res. 69, 114, 2004.
73. Garcia, A.J., Vega, M.D., and Boettiger, D. Modulation of cell proliferation and differentiation through substrate-dependent changes in fibronectin conformation. Mol. Biol. Cell 10, 785, 1999.
74. Baumgartner, W., Hinterdorfer, P., Ness, W., Raab, A., Vestweber, D., Schindler, H., and Drenckhahn, D. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 97, 4005, 2000.
75. Lehenkari, P.P., and Horton, M.A. Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy. Biochem. Biophys. Res. Commun. 259, 645, 1999.
76. Ryan, P.L., Foty, R.A., Kohn, J., and Steinberg, M.S. Tissue spreading on implantable substrates is a competitive outcome of cell-cell vs. cell-substratum adhesivity. Proc. Natl. Acad. Sci. U.S.A. 98, 4323, 2001.
77. Singhvi, R., Stephanopoulos, G., and Wang, D.I.C. Review: Effects of substratum morphology on cell physiology. Biotechnol. Bioeng. 43, 764, 1994.
78. Sawamoto, K., and Takahashi, N. Modulation of hepatocyte function by changing the cell shape in primary culture. In Vitro Cell. Dev. Biol. Anim. 33, 569, 1997.
79. Mooney, D.J., Langer, R., and Ingber, D.E. Cytoskeletal filament assembly and the control of cell spreading and function by extracellular matrix. J. Cell Sci. 108, 2311, 1995.
80. Singhvi, R., Kumar, A., Lopez, G.P., Stephanopoulos, G.N., Wang, D.I.C., Whitesides, G.M., and Ingber, D.E. Engineering cell shape and function. Science 264, 696, 1994.
81. Hamamoto, R., Yamada, K., Kamihira, M., and Iijima, S. Differentiation and proliferation of primary rat hepatocytes cultured as spheroids. J. Biochem. (Tokyo) 124, 972, 1998.
82. Hamada, T., Kato, Y., Terasaki, T., and Sugiyama, Y. Cell density-dependent mitogenic effect and independent cellular handling of epidermal growth factor in primary cultured rat hepatocytes. J. Hepatol. 26, 353, 1997.
83. Gumbiner, B.M. Signal transduction of β-catenin. Curr. Opin. Cell Biol. 7, 634, 1995.
84. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R., and Ben-Ze'ev, A. The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 5522, 1999.
85. He, T.C., Sparks, A.B., Rago, C., Hermeking, H., Zawel, L., da Costa, L.T., Morin, P.J., Vogelstein, B., and Kinzler, K.W. Identification of c-MYC as a target of the APC pathway. Science 281, 1509, 1998.
86. Rana, B., Mischoulon, D., Xie, Y., Bucher, N.L., and Farmer, S.R. Cell-extracellular matrix interactions can regulate the switch between growth and differentiation in rat hepatocytes: Reciprocal expression of C/EBP α and immediate-early growth response transcription factors. Mol. Cell. Biol. 14, 5858, 1994.
87. Parsons-Wingerter, P.A., and Saltzman, W.M. Growth versus function in the three-dimensional culture of single and aggregated hepatocytes within collagen gels. Biotechnol. Prog. 9, 600, 1993.
88. Bissell, D.M., Arenson, D.M., Maher, J.J., and Roll, F.J. Support of cultured hepatocytes by a laminin-rich gel: Evidence for a functionally significant subendothelial matrix in normal rat liver. J. Clin. Invest. 79, 801, 1987.
89. 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.
90. Fagman, H., Grande, M., Edsbagge, J., Semb, H., and Nilsson, M. Expression of classical cadherins in thyroid development: Maintenance of an epithelial phenotype throughout organogenesis. Endocrinology 144, 3618, 2003.
91. Nitou, M., Sugiyama, Y., Ishikawa, K., and Shiojiri, N. Purification of fetal mouse hepatoblasts by magnetic beads coated with monoclonal anti-E-cadherin antibodies and their in vitro culture. Exp. Cell Res. 279, 330, 2002.