E-Cadherin – Fc Chimeric Protein-Based Biomaterial: Breaking the Barriers in Stem Cell Technology and Regenerative Medicine

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Abstract:

Chimeric proteins have been used for years for various purposes ranging from biomaterials to candidate drug molecules, and from bench to bulk. Regenerative medicine needs various kinds of proteins for providing essential factors for maintaining starting cells, like induced pluripotent stem cells (iPSC), and renewal, proliferation, targeted differentiation of these cells, and as extracellular matrix for the experimental cells. However, there are several challenges associated with making functional chimeric proteins for effective application as biomaterial in this field. Fc-chimeric protein technology could be an effective solution to overcome many of them. These tailored proteins are recently becoming superior choice of biomaterials in stem cell technology and regenerative medicine due to their specific advantageous biophysical and biochemical properties over other chimeric forms of same proteins. Recent advances in recombinant protein-related science and technology also expedited the popularity of this kind of engineered protein. Over the last decade our lab has been pioneering this field, and we and others have been successfully applied Fc-chimeric proteins to overcome many critical issues in stem cell technologies targeting regenerative medicine and tissue engineering. Fc-chimeric protein-based biomaterials, specifically, E-cad-Fc have been preferentially applied for coating of cell culture plates for establishing xenogeneic-agent free monolayer stem cell culture and their maintenance, enhanced directed differentiation of stem cells to specific lineages, and non-enzymatic on-site one-step purification of target cells. Here the technology, recent discoveries, and future direction related with the E-cad-Fc-chimeric protein in connection with regenerative medicine are described.

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[1] M. Nagaoka, H.L. Jiang, T. Hoshiba, T. Akaike, C.S. Cho, Application of recombinant fusion proteins for tissue engineering, Ann. Biomed. Eng. 38 (2010) 683-693.

DOI: 10.1007/s10439-010-9935-3

Google Scholar

[2] J.H. Collier, T. Segura, Evolving the use of peptides as components of biomaterials, Biomaterials 32 (2011) 4198-4204.

DOI: 10.1016/j.biomaterials.2011.02.030

Google Scholar

[3] S.H. Kim, J. Turnbull, S. Guimond, Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor, J. Endocrinol. 209 (2011) 139-151.

DOI: 10.1530/joe-10-0377

Google Scholar

[4] R. Assenberg, P.T. Wan, S. Geisse, L.M. Mayr, Advances in recombinant protein expression for use in pharmaceutical research, Curr. Opin. Struct. Biol. 23 (2013) 393-402.

DOI: 10.1016/j.sbi.2013.03.008

Google Scholar

[5] M. Yu, F. Du, H. Ise, W. Zhao, Y. Zhang, Y. Yu, F. Yao, J. Yang, T. Akaike, Preparation and characterization of a VEGF-Fc fusion protein matrix for enhancing HUVEC growth, Biotechnol. Lett. 34 (2012) 1765-1771.

DOI: 10.1007/s10529-012-0959-7

Google Scholar

[6] A. Haque, B. Hexig, Q. Meng, S. Hossain, M. Nagaoka, T. Akaike, The effect of recombinant E-cadherin substratum on the differentiation of endoderm-derived hepatocyte-like cells from embryonic stem cells, Biomaterials 32 (2011) 2032-2042.

DOI: 10.1016/j.biomaterials.2010.11.045

Google Scholar

[7] X.S. Yue, Y. Murakami, T. Tamai, M. Nagaoka, C.S. Cho, Y. Ito, T. Akaike, A fusion protein N-cadherin-Fc as an artificial extracellular matrix surface for maintenance of stem cell features, Biomaterials 31 (2010) 5287-5296.

DOI: 10.1016/j.biomaterials.2010.03.035

Google Scholar

[8] D.J. Capon, S.M. Chamow, J. Mordenti, S.A. Marsters, T. Gregory, H. Mitsuya, R.A. Byrn, C. Lucas, F.M. Wurm, J.E. Groopman, et al., Designing CD4 immunoadhesins for AIDS therapy, Nature 337 (1989) 525-531.

DOI: 10.1038/337525a0

Google Scholar

[9] A.L. Nelson, J.M. Reichert, Development trends for therapeutic antibody fragments, Nat. Biotechnol. 27 (2009) 331-337.

DOI: 10.1038/nbt0409-331

Google Scholar

[10] J. Zhang, J. Carter, S. Siu, J.W. O'Neill, A.H. Gates, J. Delaney, C. Mehlin, Fusion partners as a tool for the expression of difficult proteins in mammalian cells, Curr. Pharm. Biotechnol. 11 (2010) 241-245.

DOI: 10.2174/138920110791111898

Google Scholar

[11] A. Beck, J.M. Reichert, Therapeutic Fc-fusion proteins and peptides as successful alternatives to antibodies, MAbs 3 (2011) 415-416.

DOI: 10.4161/mabs.3.5.17334

Google Scholar

[12] D.M. Czajkowsky, J. Hu, Z. Shao, R.J. Pleass, Fc-fusion proteins: new developments and future perspectives, EMBO Mol. Med. 4 (2012) 1015-1028.

DOI: 10.1002/emmm.201201379

Google Scholar

[13] M. Nagaoka, Y. Hagiwara, K. Takemura, Y. Murakami, J. Li, S.A. Duncan, T. Akaike, Design of the artificial acellular feeder layer for the efficient propagation of mouse embryonic stem cells, J. Biol. Chem. 283 (2008) 26468-26476.

DOI: 10.1074/jbc.m805037200

Google Scholar

[14] D.C. Roopenian, S. Akilesh, FcRn: the neonatal Fc receptor comes of age, Nat. Rev. Immunol. 7 (2007) 715-725.

DOI: 10.1038/nri2155

Google Scholar

[15] R.E. Kontermann, Strategies for extended serum half-life of protein therapeutics, Curr. Opin. Biotechnol. 22 (2011) 868-876.

DOI: 10.1016/j.copbio.2011.06.012

Google Scholar

[16] F. Nimmerjahn, J.V. Ravetch, Fcgamma receptors as regulators of immune responses, Nat. Rev. Immunol. 8 (2008) 34-47.

DOI: 10.1038/nri2206

Google Scholar

[17] M. Nagaoka, T. Akaike, Single amino acid substitution in the mouse IgG1 Fc region induces drastic enhancement of the affinity to protein A, Protein. Eng. 16 (2003) 243-245.

DOI: 10.1093/proeng/gzg037

Google Scholar

[18] Y. Huang, G.B. Willars, Generation of epitope-tagged GPCRs, Methods Mol. Biol. 746 (2011) 53-84.

Google Scholar

[19] A. Bialkowska, X.Y. Zhang, J. Reiser, Improved tagging strategy for protein identification in mammalian cells, BMC Genomics 6 (2005) 113.

DOI: 10.1186/1471-2164-6-113

Google Scholar

[20] J.W. Jarvik, C.A. Telmer, Epitope tagging, Annu. Rev. Genet. 32 (1998) 601-618.

DOI: 10.1146/annurev.genet.32.1.601

Google Scholar

[21] S. Sakai, J. Kim, B. Hexig, Y. Okahata, C.S. Cho, T. Akaike, Adsorption behaviors of recombinant E-cadherin-IgG Fc fusion protein on polystyrene surface, Colloids Surf B Biointerfaces 94 (2012) 192-198.

DOI: 10.1016/j.colsurfb.2012.01.031

Google Scholar

[22] J. Turkova, Oriented immobilization of biologically active proteins as a tool for revealing protein interactions and function, J. Chromatogr. B Biomed. Sci. Appl. 722 (1999) 11-31.

Google Scholar

[23] H. Nagashima, K. Kaneko, A. Yamanoi, S. Motoi, S. Konakahara, J. Kohroki, Y. Masuho, TNF receptor II fusion protein with tandemly repeated Fc domains, J. Biochem. 149 (2011) 337-346.

DOI: 10.1093/jb/mvq149

Google Scholar

[24] D.N. Mekhaiel, D.M. Czajkowsky, J.T. Andersen, J. Shi, M. El-Faham, M. Doenhoff, R.S. McIntosh, I. Sandlie, J. He, J. Hu, Z. Shao, R.J. Pleass, Polymeric human Fc-fusion proteins with modified effector functions, Sci. Rep. 1 (2011) 124.

DOI: 10.1038/srep00124

Google Scholar

[25] M. Nagaoka, H. Ise, T. Akaike, Immobilized E-cadherin model can enhance cell attachment and differentiation of primary hepatocytes but not proliferation, Biotechnol. Lett. 24 (2002) 1857-1862.

Google Scholar

[26] K. Ogiwara, M. Nagaoka, C.S. Cho, T. Akaike, Construction of a novel extracellular matrix using a new genetically engineered epidermal growth factor fused to IgG-Fc, Biotechnol. Lett. 27 (2005) 1633-1637.

DOI: 10.1007/s10529-005-2605-0

Google Scholar

[27] K. Azuma, M. Nagaoka, C.S. Cho, T. Akaike, An artificial extracellular matrix created by hepatocyte growth factor fused to IgG-Fc, Biomaterials 31 (2010) 802-809.

DOI: 10.1016/j.biomaterials.2009.09.105

Google Scholar

[28] H. Oda, M. Takeichi, Evolution: structural and functional diversity of cadherin at the adherens junction, J. Cell. Biol. 193 (2011) 1137-1146.

DOI: 10.1083/jcb.201008173

Google Scholar

[29] C.M. Niessen, D. Leckband, A.S. Yap, Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation, Physiol. Rev. 91 (2011) 691-731.

DOI: 10.1152/physrev.00004.2010

Google Scholar

[30] D. Vestweber, R. Kemler, Rabbit antiserum against a purified surface glycoprotein decompacts mouse preimplantation embryos and reacts with specific adult tissues, Exp. Cell. Res. 152 (1984) 169-178.

DOI: 10.1016/0014-4827(84)90241-6

Google Scholar

[31] Y. Shirayoshi, T.S. Okada, M. Takeichi, The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development, Cell 35 (1983) 631-638.

DOI: 10.1016/0092-8674(83)90095-8

Google Scholar

[32] F. Hyafil, C. Babinet, F. Jacob, Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium, Cell 26 (1981) 447-454.

DOI: 10.1016/0092-8674(81)90214-2

Google Scholar

[33] M. Takeichi, Functional correlation between cell adhesive properties and some cell surface proteins, J. Cell. Biol. 75 (1977) 464-474.

DOI: 10.1083/jcb.75.2.464

Google Scholar

[34] M. Horie, A. Ito, T. Kiyohara, Y. Kawabe, M. Kamihira, E-cadherin gene-engineered feeder systems for supporting undifferentiated growth of mouse embryonic stem cells, J. Biosci. Bioeng. 110 (2010) 582-587.

DOI: 10.1016/j.jbiosc.2010.06.002

Google Scholar

[35] T. Chen, D. Yuan, B. Wei, J. Jiang, J. Kang, K. Ling, Y. Gu, J. Li, L. Xiao, G. Pei, E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation, Stem Cells 28 (2010) 1315-1325.

DOI: 10.1002/stem.456

Google Scholar

[36] L. Larue, C. Antos, S. Butz, O. Huber, V. Delmas, M. Dominis, R. Kemler, A role for cadherins in tissue formation, Development 122 (1996) 3185-3194.

DOI: 10.1242/dev.122.10.3185

Google Scholar

[37] D. Riethmacher, V. Brinkmann, C. Birchmeier, A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development, Proc. Natl. Acad. Sci. USA 92 (1995) 855-859.

DOI: 10.1073/pnas.92.3.855

Google Scholar

[38] L. Larue, M. Ohsugi, J. Hirchenhain, R. Kemler, E-cadherin null mutant embryos fail to form a trophectoderm epithelium, Proc. Natl. Acad. Sci. USA 91 (1994) 8263-8267.

DOI: 10.1073/pnas.91.17.8263

Google Scholar

[39] L. Li, S.A. Bennett, L. Wang, Role of E-cadherin and other cell adhesion molecules in survival and differentiation of human pluripotent stem cells, Cell Adh. Migr. 6 (2012) 59-70.

DOI: 10.4161/cam.19583

Google Scholar

[40] F. Balzac, M. Avolio, S. Degani, I. Kaverina, M. Torti, L. Silengo, J.V. Small, S.F. Retta, E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function, J. Cell Sci. 118 (2005) 4765-4783.

DOI: 10.1242/jcs.02584

Google Scholar

[41] K. Xiao, D.F. Allison, K.M. Buckley, M.D. Kottke, P.A. Vincent, V. Faundez, A.P. Kowalczyk, Cellular levels of p.120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells, J. Cell Biol. 163 (2003) 535-545.

DOI: 10.1083/jcb.200306001

Google Scholar

[42] R.C. Ireton, M.A. Davis, J. van Hengel, D.J. Mariner, K. Barnes, M.A. Thoreson, P.Z. Anastasiadis, L. Matrisian, L.M. Bundy, L. Sealy, B. Gilbert, F. van Roy, A.B. Reynolds, A novel role for p.120 catenin in E-cadherin function, J. Cell Biol. 159 (2002) 465-476.

DOI: 10.1083/jcb.200205115

Google Scholar

[43] M.A. Thoreson, P.Z. Anastasiadis, J.M. Daniel, R.C. Ireton, M.J. Wheelock, K.R. Johnson, D.K. Hummingbird, A.B. Reynolds, Selective uncoupling of p.120(ctn) from E-cadherin disrupts strong adhesion, J. Cell Biol. 148 (2000) 189-202.

DOI: 10.1083/jcb.148.1.189

Google Scholar

[44] M. Cavey, M. Rauzi, P.F. Lenne, T. Lecuit, A two-tiered mechanism for stabilization and immobilization of E-cadherin, Nature 453 (2008) 751-756.

DOI: 10.1038/nature06953

Google Scholar

[45] S. Yamada, S. Pokutta, F. Drees, W.I. Weis, W.J. Nelson, Deconstructing the cadherin-catenin-actin complex, Cell 123 (2005) 889-901.

DOI: 10.1016/j.cell.2005.09.020

Google Scholar

[46] F. Palacios, J.S. Tushir, Y. Fujita, C. D'Souza-Schorey, Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions, Mol. Cell Biol. 25 (2005) 389-402.

DOI: 10.1128/mcb.25.1.389-402.2005

Google Scholar

[47] A. Kobielak, H.A. Pasolli, E. Fuchs, Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables, Nat. Cell Biol. 6 (2004) 21-30.

DOI: 10.1038/ncb1075

Google Scholar

[48] J. Xu, C. Zhu, Y. Zhang, N. Jiang, S. Li, Z. Su, T. Akaike, J. Yang, hE-cadherin-Fc fusion protein coated surface enhances the adhesion and proliferation of human mesenchymal stem cells, Colloids Surf B Biointerfaces 109 (2013) 97-102.

DOI: 10.1016/j.colsurfb.2013.03.042

Google Scholar

[49] T. Redmer, S. Diecke, T. Grigoryan, A. Quiroga-Negreira, W. Birchmeier, D. Besser, E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming, EMBO Rep 12 (2011) 720-726.

DOI: 10.1038/embor.2011.88

Google Scholar

[50] R. Awata, H. Sawai, K. Imai, K. Terada, H. Senoo, T. Sugiyama, Morphological comparison and functional reconstitution of rat hepatic parenchymal cells on various matrices, J. Gastroenterol Hepatol. 13 Suppl (1998) S55-61.

DOI: 10.1111/jgh.1998.13.s1.55

Google Scholar

[51] X. Zhang, W. Wharton, M. Donovan, D. Coppola, R. Croxton, W.D. Cress, W.J. Pledger, Density-dependent growth inhibition of fibroblasts ectopically expressing p.27(kip1), Mol. Biol. Cell 11 (2000) 2117-2130.

DOI: 10.1091/mbc.11.6.2117

Google Scholar

[52] N. Kojima, T. Kinoshita, A. Kamiya, K. Nakamura, K. Nakashima, T. Taga, A. Miyajima, Cell density-dependent regulation of hepatic development by a gp130-independent pathway, Biochem. Biophys. Res. Commun. 277 (2000) 152-158.

DOI: 10.1006/bbrc.2000.3635

Google Scholar

[53] A. Haque, X.S. Yue, A. Motazedian, Y. Tagawa, T. Akaike, Characterization and neural differentiation of mouse embryonic and induced pluripotent stem cells on cadherin-based substrata, Biomaterials 33 (2012) 5094-5106.

DOI: 10.1016/j.biomaterials.2012.04.003

Google Scholar

[54] M. Nagaoka, K. Si-Tayeb, T. Akaike, S.A. Duncan, Culture of human pluripotent stem cells using completely defined conditions on a recombinant E-cadherin substratum, BMC Dev. Biol. 10 (2010) 60.

DOI: 10.1186/1471-213x-10-60

Google Scholar

[55] M. Nagaoka, U. Koshimizu, S. Yuasa, F. Hattori, H. Chen, T. Tanaka, M. Okabe, K. Fukuda, T. Akaike, E-cadherin-coated plates maintain pluripotent ES cells without colony formation, PLoS One 1 (2006) e15.

DOI: 10.1371/journal.pone.0000015

Google Scholar

[56] C. Xu, J. Jiang, V. Sottile, J. McWhir, J. Lebkowski, M.K. Carpenter, Immortalized fibroblast-like cells derived from human embryonic stem cells support undifferentiated cell growth, Stem Cells 22 (2004) 972-980.

DOI: 10.1634/stemcells.22-6-972

Google Scholar

[57] C.V. Alvarez, M. Garcia-Lavandeira, M.E. Garcia-Rendueles, E. Diaz-Rodriguez, A.R. Garcia-Rendueles, S. Perez-Romero, T.V. Vila, J.S. Rodrigues, P.V. Lear, S.B. Bravo, Defining stem cell types: understanding the therapeutic potential of ESCs, ASCs, and iPS cells, J. Mol. Endocrinol. 49 (2012) R89-111.

DOI: 10.1530/jme-12-0072

Google Scholar

[58] A. Dar, H. Domev, O. Ben-Yosef, M. Tzukerman, N. Zeevi-Levin, A. Novak, I. Germanguz, M. Amit, J. Itskovitz-Eldor, Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb, Circulation 125 (2012) 87-99.

DOI: 10.1161/circulationaha.111.048264

Google Scholar

[59] E. Szabo, S. Rampalli, R.M. Risueno, A. Schnerch, R. Mitchell, A. Fiebig-Comyn, M. Levadoux-Martin, M. Bhatia, Direct conversion of human fibroblasts to multilineage blood progenitors, Nature 468 (2010) 521-526.

DOI: 10.1038/nature09591

Google Scholar

[60] G. Lee, S.M. Chambers, M.J. Tomishima, L. Studer, Derivation of neural crest cells from human pluripotent stem cells, Nat Protoc. 5 (2010) 688-701.

DOI: 10.1038/nprot.2010.35

Google Scholar

[61] A.E. Grigoriadis, M. Kennedy, A. Bozec, F. Brunton, G. Stenbeck, I.H. Park, E.F. Wagner, G.M. Keller, Directed differentiation of hematopoietic precursors and functional osteoclasts from human ES and iPS cells, Blood 115 (2010) 2769-2776.

DOI: 10.1182/blood-2009-07-234690

Google Scholar

[62] S. Yao, S. Chen, J. Clark, E. Hao, G.M. Beattie, A. Hayek, S. Ding, Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions, Proc. Natl. Acad. Sci. USA 103 (2006) 6907-6912.

DOI: 10.1073/pnas.0602280103

Google Scholar

[63] K.A. D'Amour, A.D. Agulnick, S. Eliazer, O.G. Kelly, E. Kroon, E.E. Baetge, Efficient differentiation of human embryonic stem cells to definitive endoderm, Nat. Biotechnol. 23 (2005) 1534-1541.

DOI: 10.1038/nbt1163

Google Scholar

[64] K. Takahashi, S. Yamanaka, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell 126 (2006) 663-676.

DOI: 10.1016/j.cell.2006.07.024

Google Scholar

[65] J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, J.M. Jones, Embryonic stem cell lines derived from human blastocysts, Science 282 (1998) 1145-1147.

DOI: 10.1126/science.282.5391.1145

Google Scholar

[66] T.E. Ludwig, V. Bergendahl, M.E. Levenstein, J. Yu, M.D. Probasco, J.A. Thomson, Feeder-independent culture of human embryonic stem cells, Nat. Methods 3 (2006) 637-646.

DOI: 10.1038/nmeth902

Google Scholar

[67] M.E. Levenstein, T.E. Ludwig, R.H. Xu, R.A. Llanas, K. VanDenHeuvel-Kramer, D. Manning, J.A. Thomson, Basic fibroblast growth factor support of human embryonic stem cell self-renewal, Stem Cells 24 (2006) 568-574.

DOI: 10.1634/stemcells.2005-0247

Google Scholar

[68] L. Wang, L. Li, P. Menendez, C. Cerdan, M. Bhatia, Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development, Blood 105 (2005) 4598-4603.

DOI: 10.1182/blood-2004-10-4065

Google Scholar

[69] M.H. Stewart, S.C. Bendall, M. Bhatia, Deconstructing human embryonic stem cell cultures: niche regulation of self-renewal and pluripotency, J. Mol. Med. (Berl) 86 (2008) 875-886.

DOI: 10.1007/s00109-008-0356-9

Google Scholar

[70] C. Xu, M.S. Inokuma, J. Denham, K. Golds, P. Kundu, J.D. Gold, M.K. Carpenter, Feeder-free growth of undifferentiated human embryonic stem cells, Nat. Biotechnol. 19 (2001) 971-974.

DOI: 10.1038/nbt1001-971

Google Scholar

[71] S. Vukicevic, H.K. Kleinman, F.P. Luyten, A.B. Roberts, N.S. Roche, A.H. Reddi, Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components, Exp. Cell. Res. 202 (1992) 1-8.

DOI: 10.1016/0014-4827(92)90397-q

Google Scholar

[72] H.K. Kleinman, M.L. McGarvey, L.A. Liotta, P.G. Robey, K. Tryggvason, G.R. Martin, Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma, Biochemistry 21 (1982) 6188-6193.

DOI: 10.1021/bi00267a025

Google Scholar

[73] H.K. Kleinman, M.L. McGarvey, J.R. Hassell, V.L. Star, F.B. Cannon, G.W. Laurie, G.R. Martin, Basement membrane complexes with biological activity, Biochemistry 25 (1986) 312-318.

DOI: 10.1021/bi00350a005

Google Scholar

[74] H.K. Kleinman, G.R. Martin, Matrigel: basement membrane matrix with biological activity, Semin. Cancer Biol. 15 (2005) 378-386.

DOI: 10.1016/j.semcancer.2005.05.004

Google Scholar

[75] J. Carlson, R. Garg, S.R. Compton, C. Zeiss, E. Uchio, Poliomyelitis in SCID Mice Following Injection of Basement Membrane Matrix Contaminated with Lactate Dehydrogenase-elevating Virus, J. Am. Assoc. Lab. Anim. Sci. 47 (2008) 80-81.

Google Scholar

[76] T. Miyazaki, S. Futaki, K. Hasegawa, M. Kawasaki, N. Sanzen, M. Hayashi, E. Kawase, K. Sekiguchi, N. Nakatsuji, H. Suemori, Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells, Biochem. Biophys. Res. Commun. 375 (2008) 27-32.

DOI: 10.1016/j.bbrc.2008.07.111

Google Scholar

[77] H. Ido, S. Ito, Y. Taniguchi, M. Hayashi, R. Sato-Nishiuchi, N. Sanzen, Y. Hayashi, S. Futaki, K. Sekiguchi, Laminin isoforms containing the gamma3 chain are unable to bind to integrins due to the absence of the glutamic acid residue conserved in the C-terminal regions of the gamma1 and gamma2 chains, J. Biol. Chem. 283 (2008) 28149-28157.

DOI: 10.1074/jbc.m803553200

Google Scholar

[78] A. Domogatskaya, S. Rodin, A. Boutaud, K. Tryggvason, Laminin-511 but not -332, -111, or -411 enables mouse embryonic stem cell self-renewal in vitro, Stem Cells 26 (2008) 2800-2809.

DOI: 10.1634/stemcells.2007-0389

Google Scholar

[79] Y. Hayashi, M.K. Furue, T. Okamoto, K. Ohnuma, Y. Myoishi, Y. Fukuhara, T. Abe, J.D. Sato, R. Hata, M. Asashima, Integrins regulate mouse embryonic stem cell self-renewal, Stem Cells 25 (2007) 3005-3015.

DOI: 10.1634/stemcells.2007-0103

Google Scholar

[80] T.E. Ludwig, M.E. Levenstein, J.M. Jones, W.T. Berggren, E.R. Mitchen, J.L. Frane, L.J. Crandall, C.A. Daigh, K.R. Conard, M.S. Piekarczyk, R.A. Llanas, J.A. Thomson, Derivation of human embryonic stem cells in defined conditions, Nat. Biotechnol. 24 (2006) 185-187.

DOI: 10.1038/nbt1177

Google Scholar

[81] D.P. Gearing, N.M. Gough, J.A. King, D.J. Hilton, N.A. Nicola, R.J. Simpson, E.C. Nice, A. Kelso, D. Metcalf, Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF), EMBO J 6 (1987) 3995-4002.

DOI: 10.1002/j.1460-2075.1987.tb02742.x

Google Scholar

[82] H. Baumann, G.G. Wong, Hepatocyte-stimulating factor III shares structural and functional identity with leukemia-inhibitory factor, J. Immunol. 143 (1989) 1163-1167.

DOI: 10.4049/jimmunol.143.4.1163

Google Scholar

[83] N. Ferrara, J. Winer, W.J. Henzel, Pituitary follicular cells secrete an inhibitor of aortic endothelial cell growth: identification as leukemia inhibitory factor, Proc. Natl. Acad. Sci. USA 89 (1992) 698-702.

DOI: 10.1073/pnas.89.2.698

Google Scholar

[84] M. Nagaoka, H. Ise, I. Harada, U. Koshimizu, A. Maruyama, T. Akaike, Embryonic undifferentiated cells show scattering activity on a surface coated with immobilized E-cadherin, J. Cell Biochem. 103 (2008) 296-310.

DOI: 10.1002/jcb.21406

Google Scholar

[85] N. Harb, T.K. Archer, N. Sato, The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells, PLoS One 3 (2008) e3001.

DOI: 10.1371/journal.pone.0003001

Google Scholar

[86] K.F. Kelly, D.Y. Ng, G. Jayakumaran, G.A. Wood, H. Koide, B.W. Doble, beta-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism, Cell Stem Cell 8 (2011) 214-227.

DOI: 10.1016/j.stem.2010.12.010

Google Scholar

[87] R.N. Moore, J.F. Cherry, V. Mathur, R. Cohen, M. Grumet, P.V. Moghe, E-cadherin-expressing feeder cells promote neural lineage restriction of human embryonic stem cells, Stem Cells Dev. 21 (2012) 30-41.

DOI: 10.1089/scd.2010.0434

Google Scholar

[88] Z. Zhang, Y. Gao, A. Gordon, Z.Z. Wang, Z. Qian, W.S. Wu, Efficient generation of fully reprogrammed human iPS cells via polycistronic retroviral vector and a new cocktail of chemical compounds, PLoS One 6 (2011) e26592.

DOI: 10.1371/journal.pone.0026592

Google Scholar

[89] B. Liao, X. Bao, L. Liu, S. Feng, A. Zovoilis, W. Liu, Y. Xue, J. Cai, X. Guo, B. Qin, R. Zhang, J. Wu, L. Lai, M. Teng, L. Niu, B. Zhang, M.A. Esteban, D. Pei, MicroRNA cluster 302-367 enhances somatic cell reprogramming by accelerating a mesenchymal-to-epithelial transition, J. Biol. Chem. 286 (2011) 17359-17364.

DOI: 10.1074/jbc.c111.235960

Google Scholar

[90] H. Kim, G. Lee, Y. Ganat, E.P. Papapetrou, I. Lipchina, N.D. Socci, M. Sadelain, L. Studer, miR-371-3 expression predicts neural differentiation propensity in human pluripotent stem cells, Cell Stem Cell 8 (2011) 695-706.

DOI: 10.1016/j.stem.2011.04.002

Google Scholar

[91] N. Xu, T. Papagiannakopoulos, G. Pan, J.A. Thomson, K.S. Kosik, MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells, Cell 137 (2009) 647-658.

DOI: 10.1016/j.cell.2009.02.038

Google Scholar

[92] I.H. Park, R. Zhao, J.A. West, A. Yabuuchi, H. Huo, T.A. Ince, P.H. Lerou, M.W. Lensch, G.Q. Daley, Reprogramming of human somatic cells to pluripotency with defined factors, Nature 451 (2008) 141-146.

DOI: 10.1038/nature06534

Google Scholar

[93] T. Aasen, A. Raya, M.J. Barrero, E. Garreta, A. Consiglio, F. Gonzalez, R. Vassena, J. Bilic, V. Pekarik, G. Tiscornia, M. Edel, S. Boue, J.C. Izpisua Belmonte, Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes, Nat. Biotechnol. 26 (2008) 1276-1284.

DOI: 10.1038/nbt.1503

Google Scholar

[94] J. Yu, M.A. Vodyanik, K. Smuga-Otto, J. Antosiewicz-Bourget, J.L. Frane, S. Tian, J. Nie, G.A. Jonsdottir, V. Ruotti, R. Stewart, Slukvin, II, J.A. Thomson, Induced pluripotent stem cell lines derived from human somatic cells, Science 318 (2007) 1917-1920.

DOI: 10.1126/science.1151526

Google Scholar

[95] K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, S. Yamanaka, Induction of pluripotent stem cells from adult human fibroblasts by defined factors, Cell 131 (2007) 861-872.

DOI: 10.1016/j.cell.2007.11.019

Google Scholar

[96] R. Li, J. Liang, S. Ni, T. Zhou, X. Qing, H. Li, W. He, J. Chen, F. Li, Q. Zhuang, B. Qin, J. Xu, W. Li, J. Yang, Y. Gan, D. Qin, S. Feng, H. Song, D. Yang, B. Zhang, L. Zeng, L. Lai, M.A. Esteban, D. Pei, A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts, Cell Stem Cell 7 (2010) 51-63.

DOI: 10.1016/j.stem.2010.04.014

Google Scholar

[97] A.M. Eastham, H. Spencer, F. Soncin, S. Ritson, C.L. Merry, P.L. Stern, C.M. Ward, Epithelial-mesenchymal transition events during human embryonic stem cell differentiation, Cancer Res. 67 (2007) 11254-11262.

DOI: 10.1158/0008-5472.can-07-2253

Google Scholar

[98] C. Hogan, N. Serpente, P. Cogram, C.R. Hosking, C.U. Bialucha, S.M. Feller, V.M. Braga, W. Birchmeier, Y. Fujita, Rap1 regulates the formation of E-cadherin-based cell-cell contacts, Mol. Cell Biol. 24 (2004) 6690-6700.

DOI: 10.1128/mcb.24.15.6690-6700.2004

Google Scholar

[99] Y.H. Loh, Q. Wu, J.L. Chew, V.B. Vega, W. Zhang, X. Chen, G. Bourque, J. George, B. Leong, J. Liu, K.Y. Wong, K.W. Sung, C.W. Lee, X.D. Zhao, K.P. Chiu, L. Lipovich, V.A. Kuznetsov, P. Robson, L.W. Stanton, C.L. Wei, Y. Ruan, B. Lim, H.H. Ng, The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells, Nat. Genet. 38 (2006) 431-440.

DOI: 10.1038/ng1760

Google Scholar

[100] A. Singh, S. Suri, T. Lee, J.M. Chilton, M.T. Cooke, W. Chen, J. Fu, S.L. Stice, H. Lu, T.C. McDevitt, A.J. Garcia, Adhesion strength-based, label-free isolation of human pluripotent stem cells, Nat. Methods 10 (2013) 438-444.

DOI: 10.1038/nmeth.2437

Google Scholar

[101] L.G. Villa-Diaz, A.M. Ross, J. Lahann, P.H. Krebsbach, Concise review: The evolution of human pluripotent stem cell culture: from feeder cells to synthetic coatings, Stem Cells 31 (2013) 1-7.

DOI: 10.1002/stem.1260

Google Scholar

[102] M. Sundberg, L. Jansson, J. Ketolainen, H. Pihlajamaki, R. Suuronen, H. Skottman, J. Inzunza, O. Hovatta, S. Narkilahti, CD marker expression profiles of human embryonic stem cells and their neural derivatives, determined using flow-cytometric analysis, reveal a novel CD marker for exclusion of pluripotent stem cells, Stem Cell Res. 2 (2009) 113-124.

DOI: 10.1016/j.scr.2008.08.001

Google Scholar

[103] J. Pruszak, K.C. Sonntag, M.H. Aung, R. Sanchez-Pernaute, O. Isacson, Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations, Stem Cells 25 (2007) 2257-2268.

DOI: 10.1634/stemcells.2006-0744

Google Scholar