Design of polymeric materials for culturing human pluripotent stem cells: Progress toward feeder-free and xeno-free culturing

Progress in Polymer Science

Volumn 39, Issue 7, 2014, Pages 1348-1374

  Higuchi, Akon ^a,b,c   Ling, Qing Dong ^a,c   Kumar, S Suresh ^a,d   Munusamy, Murugan ^e   Alarfajj, Abdullah A ^e   Umezawa, Akihiro ^b   Wu, Gwo Jang ^f  

^a NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^b NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^c CATHAY GENERAL HOSPITAL   (Taiwan)

^d Department of Medical Microbiology and Parasitology Universities Putra Malaysia   (Malaysia)

^e KING SAUD UNIVERSITY   (Saudi Arabia)

^f TRI SERVICE GENERAL HOSPITAL   (Taiwan)

Author keywords

Biomaterial; Cell culture; Embryonic stem cells; Extracellular matrix; Hydrogel; Microcapsule; Microcarrier

Indexed keywords

AMINO ACIDS; BIOMATERIALS; CELL CULTURE; ENCAPSULATION; FEEDING; HYDROGELS; NATURAL POLYMERS; RECOMBINANT PROTEINS; STEM CELLS;

CELL ADHESION MOLECULES; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRICES; HUMAN EMBRYONIC STEM CELLS; INDUCED PLURIPOTENT STEM CELLS; MICROCAPSULES; MICROCARRIERS; MOUSE EMBRYONIC FIBROBLASTS;

SCAFFOLDS (BIOLOGY);

EID: 84902177951     PISSN: 00796700     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.progpolymsci.2014.01.002     Document Type: Review

References (136)

1. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
2. K.A. D'Amour, A.G. Bang, S. Eliazer, O.G. Kelly, A.D. Agulnick, N.G. Smart, M.A. Moorman, E. Kroon, M.K. Carpenter, and E.E. Baetge Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells Nat Biotechnol 24 2006 1392 1401
3. E. Kroon, L.A. Martinson, K. Kadoya, A.G. Bang, O.G. Kelly, S. Eliazer, H. Young, M. Richardson, N.G. Smart, J. Cunningham, A.D. Agulnick, K.A. D'Amour, M.K. Carpenter, and E.E. Baetge Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo Nat Biotechnol 26 2008 443 452
4. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
5. 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, I.I. Slukvin, and J.A. Thomson Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
6. B.S. Mallon, K.Y. Park, K.G. Chen, R.S. Hamilton, and R.D. McKay Toward xeno-free culture of human embryonic stem cells Int J Biochem Cell Biol 38 2006 1063 1075
7. T. Lei, S. Jacob, I. Ajil-Zaraa, J.B. Dubuisson, O. Irion, M. Jaconi, and A. Feki Xeno-free derivation and culture of human embryonic stem cells: current status, problems and challenges Cell Res 17 2007 682 688
8. B.M. Rao, and P.W. Zandstra Culture development for human embryonic stem cell propagation: molecular aspects and challenges Curr Opin Biotech 16 2005 568 576
9. M. Prewitz, F.P. Seib, T. Pompe, and C. Werner Polymeric biomaterials for stem cell bioengineering Macromol Rapid Comm 33 2012 1420 1431
10. C. Chai, and K.W. Leong Biomaterials approach to expand and direct differentiation of stem cells Mol Ther 15 2007 467 480
11. S. Abraham, N. Eroshenko, and R.R. Rao Role of bioinspired polymers in determination of pluripotent stem cell fate Reg Med 4 2009 561 578
12. T. Vazin, and W.J. Freed Human embryonic stem cells: derivation, culture, and differentiation: a review Restor Neurol Neuros 28 2010 589 603
13. Y. Hwang, A. Phadke, and S. Varghese Engineered microenvironments for self-renewal and musculoskeletal differentiation of stem cells Reg Med 6 2011 505 524
14. J.M. Crook, T.T. Peura, L. Kravets, A.G. Bosman, J.J. Buzzard, R. Horne, H. Hentze, N.R. Dunn, R. Zweigerdt, F. Chua, A. Upshall, and A. Colman The generation of six clinical-grade human embryonic stem cell lines Cell Stem Cell 1 2007 490 494
15. K. Rajala, B. Lindroos, S.M. Hussein, R.S. Lappalainen, M. Pekkanen-Mattila, J. Inzunza, B. Rozell, S. Miettinen, S. Narkilahti, E. Kerkela, K. Aalto-Setala, T. Otonkoski, R. Suuronen, O. Hovatta, and H. Skottman A defined and xeno-free culture method enabling the establishment of clinical-grade human embryonic, induced pluripotent and adipose stem cells PLoS ONE 5 2010 e10246/1-14
16. S.T. Hwang, S.W. Kang, S.J. Lee, T.H. Lee, W. Suh, S.H. Shim, D.R. Lee, L.J. Taite, K.S. Kim, and S.H. Lee The expansion of human ES and iPS cells on porous membranes and proliferating human adipose-derived feeder cells Biomaterials 31 2010 8012 8021
17. P.C. Beltrao-Braga, G.C. Pignatari, P.C. Maiorka, N.A. Oliveira, N.F. Lizier, C.V. Wenceslau, M.A. Miglino, A.R. Muotri, and I. Kerkis Feeder-free derivation of induced pluripotent stem cells from human immature dental pulp stem cells Cell Transplant 20 2011 1707 1719
18. C. Xu, M.S. Inokuma, J. Denham, K. Golds, P. Kundu, J.D. Gold, and M.K. Carpenter Feeder-free growth of undifferentiated human embryonic stem cells Nat Biotechnol 19 2001 971 974
19. M.K. Carpenter, E.S. Rosler, G.J. Fisk, R. Brandenberger, X. Ares, T. Miura, M. Lucero, and M.S. Rao Properties of four human embryonic stem cell lines maintained in a feeder-free culture system Dev Dyn 229 2004 243 258
20. C. Xu, E. Rosler, J. Jiang, J.S. Lebkowski, J.D. Gold, C. O'Sullivan, K. Delavan-Boorsma, M. Mok, A. Bronstein, and M.K. Carpenter Basic fibroblast growth factor supports undifferentiated human embryonic stem cell growth without conditioned medium Stem Cells 23 2005 315 323
21. H. Hakala, K. Rajala, M. Ojala, S. Panula, S. Areva, M. Kellomaki, R. Suuronen, and H. Skottman Comparison of biomaterials and extracellular matrices as a culture platform for multiple, independently derived human embryonic stem cell lines Tissue Eng A 15 2009 1775 1785
22. V. Akopian, P.W. Andrews, S. Beil, N. Benvenisty, J. Brehm, M. Christie, A. Ford, V. Fox, P.J. Gokhale, L. Healy, F. Holm, O. Hovatta, B.B. Knowles, T.E. Ludwig, R.D. McKay, T. Miyazaki, N. Nakatsuji, S.K. Oh, M.F. Pera, J. Rossant, G.N. Stacey, and H. Suemori Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells In Vitro Cell Dev-An 46 2010 247 258
23. A. Swistowski, J. Peng, Y. Han, A.M. Swistowska, M.S. Rao, and X. Zeng Xeno-free defined conditions for culture of human embryonic stem cells, neural stem cells and dopaminergic neurons derived from them PLoS ONE 4 2009 e6233/1-11
24. A. Higuchi, Q.D. Ling, Y.A. Ko, Y. Chang, and A. Umezawa Biomaterials for the feeder-free culture of human embryonic stem cells and induced pluripotent stem cells Chem Rev 111 2011 3021 3035
25. M.J. Martin, A. Muotri, F. Gage, and A. Varki Human embryonic stem cells express an immunogenic nonhuman sialic acid Nat Med 11 2005 228 232
26. H. Nandivada, L.G. Villa-Diaz, K.S. O'Shea, G.D. Smith, P.H. Krebsbach, and J. Lahann Fabrication of synthetic polymer coatings and their use in feeder-free culture of human embryonic stem cells Nat Protocol 6 2011 1037 1043
27. D. Ilic, E. Stephenson, V. Wood, L. Jacquet, D. Stevenson, A. Petrova, N. Kadeva, S. Codognotto, H. Patel, M. Semple, G. Cornwell, C. Ogilvie, and P. Braude Derivation and feeder-free propagation of human embryonic stem cells under xeno-free conditions Cytotherapy 14 2012 122 128
28. A.G. Elefanty, and E.G. Stanley Defined substrates for pluripotent stem cells: are we there yet? Nat Methods 7 2010 967 968
29. R. Bergstrom, S. Strom, F. Holm, A. Feki, and O. Hovatta Xeno-free culture of human pluripotent stem cells Methods Mol Biol 767 2011 125 136
30. T. Sampsell-Barron Xeno-free adaptation and culture of human pluripotent stem cells Methods Mol Biol 1001 2013 81 97
31. A.J. Want, A.W. Nienow, C.J. Hewitt, and K. Coopman Large-scale expansion and exploitation of pluripotent stem cells for regenerative medicine purposes: beyond the T flask Reg Med 7 2012 71 84
32. X. Fu, and Y. Xu Self-renewal and scalability of human embryonic stem cells for human therapy Reg Med 6 2011 327 334
33. M. Serra, C. Brito, C. Correia, and P.M. Alves Process engineering of human pluripotent stem cells for clinical application Trends Biotechnol 30 2012 350 359
34. B. Valamehr, H. Tsutsui, C.M. Ho, and H. Wu Developing defined culture systems for human pluripotent stem cells Reg Med 6 2011 623 634
35. S. Abraham, S.D. Sheridan, B. Miller, and R.R. Rao Stable propagation of human embryonic and induced pluripotent stem cells on decellularized human substrates Biotechnol Prog 26 2010 1126 1134
36. N. Sato, L. Meijer, L. Skaltsounis, P. Greengard, and A.H. Brivanlou Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor Nat Med 10 2004 55 63
37. A. Ranga, and M.P. Lutolf High-throughput approaches for the analysis of extrinsic regulators of stem cell fate Curr Opin Cell Biol 24 2012 236 244
38. G.L. Meng, S.Y. Liu, and D.E. Rancourt Synergistic effect of medium, matrix, and exogenous factors on the adhesion and growth of human pluripotent stem cells under defined, xeno-free conditions Stem Cells Dev 21 2012 2036 2048
39. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, and D.R. Marshak Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
40. K. Alberti, R.E. Davey, K. Onishi, S. George, K. Salchert, F.P. Seib, M. Bornhauser, T. Pompe, A. Nagy, C. Werner, and P.W. Zandstra Functional immobilization of signaling proteins enables control of stem cell fate Nat Methods 5 2008 645 650
41. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689
42. A. Higuchi, Q.D. Ling, Y. Chang, S.T. Hsu, and A. Umezawa Physical cues of biomaterials guide stem cell differentiation fate Chem Rev 113 2013 3297 3328
43. F. Guilak, D.M. Cohen, B.T. Estes, J.M. Gimble, W. Liedtke, and C.S. Chen Control of stem cell fate by physical interactions with the extracellular matrix Cell Stem Cell 5 2009 17 26
44. A.S. Rowlands, P.A. George, and J.J. Cooper-White Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation Am J Physiol - Cell Physiol 295 2008 C1037 C1044
45. W.Q. Chen, L.G. Villa-Diaz, Y.B. Sun, S.N. Weng, J.K. Kim, R.H.W. Lam, L. Han, R. Fan, P.H. Krebsbach, and J.P. Fu Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells ACS Nano 6 2012 4094 4103
46. F. Chowdhury, S. Na, D. Li, Y.C. Poh, T.S. Tanaka, F. Wang, and N. Wang Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells Nat Mater 9 2010 82 88
47. F. Chowdhury, Y. Li, Y.C. Poh, T. Yokohama-Tamaki, N. Wang, and T.S. Tanaka Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions PLoS ONE 5 2010 e15655/1-10
48. Y. Sun, L.G. Villa-Diaz, R.H. Lam, W. Chen, P.H. Krebsbach, and J. Fu Mechanics regulates fate decisions of human embryonic stem cells PLoS ONE 7 2012 e37178/1-7
49. J. Li, J. Bardy, L.Y. Yap, A. Chen, V. Nurcombe, S.M. Cool, S.K. Oh, and W.R. Birch Impact of vitronectin concentration and surface properties on the stable propagation of human embryonic stem cells Biointerphases 5 2010 FA132-42
50. Y. Mei, K. Saha, S.R. Bogatyrev, J. Yang, A.L. Hook, Z.I. Kalcioglu, S.W. Cho, M. Mitalipova, N. Pyzocha, F. Rojas, K.J. Van Vliet, M.C. Davies, M.R. Alexander, R. Langer, R. Jaenisch, and D.G. Anderson Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells Nat Mater 9 2010 768 778
51. A. Higuchi, S. Tamiya, T. Tsubomura, A. Katoh, C.S. Cho, T. Akaike, and M. Hara Growth of L929 cells on polymeric films prepared by Langmuir-Blodgett and casting methods J Biomat Sci - Polym Ed 11 2000 149 168
52. X. Fu, W.S. Toh, H. Liu, K. Lu, M. Li, and T. Cao Establishment of clinically compliant human embryonic stem cells in an autologous feeder-free system Tissue Eng C 17 2011 927 937
53. G. Meng, S. Liu, X. Li, R. Krawetz, and D.E. Rancourt Extracellular matrix isolated from foreskin fibroblasts supports long-term xeno-free human embryonic stem cell culture Stem Cells Dev 19 2010 547 556
54. M.P. Stelling, Y.M. Lages, A.M. Tovar, P.A. Mourao, and S.K. Rehen Matrix-bound heparan sulfate is essential for the growth and pluripotency of human embryonic stem cells Glycobiology 23 2013 337 345
55. K. Rajala, H. Hakala, S. Panula, S. Aivio, H. Pihlajamaki, R. Suuronen, O. Hovatta, and H. Skottman Testing of nine different xeno-free culture media for human embryonic stem cell cultures Hum Reprod 22 2007 1231 1238
56. K.J. Manton, S. Richards, D. Van Lonkhuyzen, L. Cormack, D. Leavesley, and Z. Upton A chimeric vitronectin: IGF-I protein supports feeder-cell-free and serum-free culture of human embryonic stem cells Stem Cells Dev 19 2010 1297 1305
57. M.R. Zonca Jr., P.S. Yune, C.L. Heldt, G. Belfort, and Y. Xie High-throughput screening of substrate chemistry for embryonic stem cell attachment, expansion, and maintaining pluripotency Macromol Biosci 13 2013 177 190
58. A. Higuchi, Q.D. Ling, S.T. Hsu, and A. Umezawa Biomimetic cell culture proteins as extracellular matrices for stem cell differentiation Chem Rev 112 2012 4507 4540
59. D. Hernandez, L. Ruban, and C. Mason Feeder-free culture of human embryonic stem cells for scalable expansion in a reproducible manner Stem Cells Dev 20 2011 1089 1098
60. M. Amit, C. Shariki, V. Margulets, and J. Itskovitz-Eldor Feeder layer- and serum-free culture of human embryonic stem cells Biol Reprod 70 2004 837 845
61. C.S. Hughes, L. Radan, D. Betts, L.M. Postovit, and G.A. Lajoie Proteomic analysis of extracellular matrices used in stem cell culture Proteomics 11 2011 3983 3991
62. S. Sugii, Y. Kida, W.T. Berggren, and R.M. Evans Feeder-dependent and feeder-independent iPS cell derivation from human and mouse adipose stem cells Nat Protocol 6 2011 346 358
63. S. Sugii, Y. Kida, T. Kawamura, J. Suzuki, R. Vassena, Y.Q. Yin, M.K. Lutz, W.T. Berggren, J.C. Izpisua Belmonte, and R.M. Evans Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells Proc Natl Acad Sci U S A 107 2010 3558 3563
64. A. Kaupisch, L. Kennedy, V. Stelmanis, B. Tye, N.M. Kane, J.C. Mountford, A. Courtney, and A.H. Baker Derivation of vascular endothelial cells from human embryonic stem cells under GMP-compliant conditions: towards clinical studies in ischaemic disease J Cardiovasc Transl Res 5 2012 605 617
65. H. Tsutsui, B. Valamehr, A. Hindoyan, R. Qiao, X. Ding, S. Guo, O.N. Witte, X. Liu, C.M. Ho, and H. Wu An optimized small molecule inhibitor cocktail supports long-term maintenance of human embryonic stem cells Nat Commun 2 2011 167/1-18
66. T.M. Yoon, B. Chang, H.T. Kim, J.H. Jee, D.W. Kim, and D.Y. Hwang Human embryonic stem cells (hESCs) cultured under distinctive feeder-free culture conditions display global gene expression patterns similar to hESCs from feeder-dependent culture conditions Stem Cell Rev 6 2010 425 437
67. S.R. Braam, L. Zeinstra, S. Litjens, D. Ward-van Oostwaard, S. van den Brink, L. van Laake, F. Lebrin, P. Kats, R. Hochstenbach, R. Passier, A. Sonnenberg, and C.L. Mummery Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin Stem Cells 26 2008 2257 2265
68. A. Swistowski, J. Peng, Q. Liu, P. Mali, M.S. Rao, L. Cheng, and X. Zeng Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions Stem Cells 28 2010 1893 1904
69. Y. Hayashi, T. Chan, M. Warashina, M. Fukuda, T. Ariizumi, K. Okabayashi, N. Takayama, M. Otsu, K. Eto, M.K. Furue, T. Michiue, K. Ohnuma, H. Nakauchi, and M. Asashima Reduction of N-glycolylneuraminic acid in human induced pluripotent stem cells generated or cultured under feeder- and serum-free defined conditions PLoS ONE 5 2010 e14099/1-11
70. S. Rodin, A. Domogatskaya, S. Strom, E.M. Hansson, K.R. Chien, J. Inzunza, O. Hovatta, and K. Tryggvason Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511 Nat Biotechnol 28 2010 611 615
71. T. Miyazaki, S. Futaki, K. Hasegawa, M. Kawasaki, N. Sanzen, M. Hayashi, E. Kawase, K. Sekiguchi, N. Nakatsuji, and H. Suemori Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells Biochem Bioph Res Commun 375 2008 27 32
72. H. Hongisto, S. Vuoristo, A. Mikhailova, R. Suuronen, I. Virtanen, T. Otonkoski, and H. Skottman Laminin-511 expression is associated with the functionality of feeder cells in human embryonic stem cell culture Stem Cell Res 8 2012 97 108
73. A.K. Chen, X. Chen, A.B. Choo, S. Reuveny, and S.K. Oh Critical microcarrier properties affecting the expansion of undifferentiated human embryonic stem cells Stem Cell Res 7 2011 97 111
74. D. Evseenko, K. Schenke-Layland, G. Dravid, Y. Zhu, Q.L. Hao, J. Scholes, X.C. Wang, W.R. Maclellan, and G.M. Crooks Identification of the critical extracellular matrix proteins that promote human embryonic stem cell assembly Stem Cells Dev 18 2009 919 928
75. I. Schvartz, D. Seger, and S. Shaltiel Vitronectin Int J Biochem Cell B 31 1999 539 544
76. A.B. Prowse, M.R. Doran, J.J. Cooper-White, F. Chong, T.P. Munro, J. Fitzpatrick, T.L. Chung, D.N. Haylock, P.P. Gray, and E.J. Wolvetang Long term culture of human embryonic stem cells on recombinant vitronectin in ascorbate free media Biomaterials 31 2010 8281 8288
77. L.Y. Yap, J. Li, I.Y. Phang, L.T. Ong, J.Z. Ow, J.C. Goh, V. Nurcombe, J. Hobley, A.B. Choo, S.K. Oh, S.M. Cool, and W.R. Birch Defining a threshold surface density of vitronectin for the stable expansion of human embryonic stem cells Tissue Eng C 17 2011 193 207
78. N. Nishishita, M. Shikamura, C. Takenaka, N. Takada, N. Fusaki, and S. Kawamata Generation of virus-free induced pluripotent stem cell clones on a synthetic matrix via a single cell subcloning in the naive state PLoS ONE 7 2012 e38389/1-9
79. B.S. Kim, I.K. Park, T. Hoshiba, H.L. Jiang, Y.J. Choi, T. Akaike, and C.S. Cho Design of artificial extracellular matrices for tissue engineering Prog Polym Sci 36 2011 238 268
80. Z. Melkoumian, J.L. Weber, D.M. Weber, A.G. Fadeev, Y. Zhou, P. Dolley-Sonneville, J. Yang, L. Qiu, C.A. Priest, C. Shogbon, A.W. Martin, J. Nelson, P. West, J.P. Beltzer, S. Pal, and R. Brandenberger Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells Nat Biotechnol 28 2010 606 610
81. L.M. Hoffman, and M.K. Carpenter Characterization and culture of human embryonic stem cells Nat Biotechnol 23 2005 699 708
82. P. Kolhar, V.R. Kotamraju, S.T. Hikita, D.O. Clegg, and E. Ruoslahti Synthetic surfaces for human embryonic stem cell culture J Biotechnol 146 2010 143 146
83. J.R. Klim, L. Li, P.J. Wrighton, M.S. Piekarczyk, and L.L. Kiessling A defined glycosaminoglycan-binding substratum for human pluripotent stem cells Nat Methods 7 2010 989 994
84. B.M. Gumbiner Regulation of cadherin-mediated adhesion in morphogenesis Nat Rev Mol Cell Biol 6 2005 622 634
85. U. Ullmann, P. In't Veld, C. Gilles, K. Sermon, M. De Rycke, H. Van de Velde, A. Van Steirteghem, and I. Liebaers Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions Mol Hum Reprod 13 2007 21 32
86. M. Nagaoka, K. Si-Tayeb, T. Akaike, and S.A. Duncan Culture of human pluripotent stem cells using completely defined conditions on a recombinant E-cadherin substratum BMC Dev Biol 10 2010 60/1-12
87. S. Dedhar Cell-substrate interactions and signaling through ILK Curr Opin Cell Biol 12 2000 250 256
88. E.T. Pashuck, and M.M. Stevens Designing regenerative biomaterial therapies for the clinic Sci Transl Med 4 2012 160 164
89. L. Armstrong, O. Hughes, S. Yung, L. Hyslop, R. Stewart, I. Wappler, H. Peters, T. Walter, P. Stojkovic, J. Evans, M. Stojkovic, and M. Lako The role of PI3K/AKT, MAPK/ERK and NFkappabeta signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis Hum Mol Genet 15 2006 1894 1913
90. E. Stephenson, L. Jacquet, C. Miere, V. Wood, N. Kadeva, G. Cornwell, S. Codognotto, Y. Dajani, P. Braude, and D. Ilic Derivation and propagation of human embryonic stem cell lines from frozen embryos in an animal product-free environment Nat Protocol 7 2012 1366 1381
91. Y.X. Liu, L.F. Charles, T.I. Zarembinski, K.I. Johnson, S.K. Atzet, R.L. Wesselschmidt, M.E. Wight, and L.T. Kuhn Modified hyaluronan hydrogels support the maintenance of mouse embryonic stem cells and human induced pluripotent stem cells Macromol Biosci 12 2012 1034 1042
92. H.F. Lu, K. Narayanan, S.X. Lim, S. Gao, M.F. Leong, and A.C. Wan A 3D microfibrous scaffold for long-term human pluripotent stem cell self-renewal under chemically defined conditions Biomaterials 33 2012 2419 2430
93. Z. Li, M. Leung, R. Hopper, R. Ellenbogen, and M. Zhang Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds Biomaterials 31 2010 404 412
94. N. Siti-Ismail, A.E. Bishop, J.M. Polak, and A. Mantalaris The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance Biomaterials 29 2008 3946 3952
95. S. Gerecht, J.A. Burdick, L.S. Ferreira, S.A. Townsend, R. Langer, and G. Vunjak-Novakovic Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells Proc Natl Acad Sci U S A 104 2007 11298 11303
96. M.M. Mahlstedt, D. Anderson, J.S. Sharp, R. McGilvray, M.D. Munoz, L.D. Buttery, M.R. Alexander, F.R. Rose, and C. Denning Maintenance of pluripotency in human embryonic stem cells cultured on a synthetic substrate in conditioned medium Biotechnol Bioeng 105 2010 130 140
97. Y. Nie, V. Bergendahl, D.J. Hei, J.M. Jones, and S.P. Palecek Scalable culture and cryopreservation of human embryonic stem cells on microcarriers Biotechnol Prog 25 2009 20 31
98. S. Kim, S.E. Ahn, J.H. Lee, D.S. Lim, K.S. Kim, H.M. Chung, and S.H. Lee A novel culture technique for human embryonic stem cells using porous membranes Stem Cells 25 2007 2601 2609
99. N. Bigdeli, M. Andersson, R. Strehl, K. Emanuelsson, E. Kilmare, J. Hyllner, and A. Lindahl Adaptation of human embryonic stem cells to feeder-free and matrix-free culture conditions directly on plastic surfaces J Biotechnol 133 2008 146 153
100. L.G. Villa-Diaz, H. Nandivada, J. Ding, N.C. Nogueira-de-Souza, P.H. Krebsbach, K.S. O'Shea, J. Lahann, and G.D. Smith Synthetic polymer coatings for long-term growth of human embryonic stem cells Nat Biotechnol 28 2010 581 583
101. A.M. Ross, H. Nandivada, A.L. Ryan, and J. Lahann Synthetic substrates for long-term stem cell culture Polymer 53 2012 2533 2539
102. E.F. Irwin, R. Gupta, D.C. Dashti, and K.E. Healy Engineered polymer-media interfaces for the long-term self-renewal of human embryonic stem cells Biomaterials 32 2011 6912 6919
103. D.A. Brafman, C.W. Chang, A. Fernandez, K. Willert, S. Varghese, and S. Chien Long-term human pluripotent stem cell self-renewal on synthetic polymer surfaces Biomaterials 31 2010 9135 9144
104. R. Zhang, H.K. Mjoseng, M.A. Hoeve, N.G. Bauer, S. Pells, R. Besseling, S. Velugotla, G. Tourniaire, R.E. Kishen, Y. Tsenkina, C. Armit, C.R. Duffy, M. Helfen, F. Edenhofer, P.A. de Sousa, and M. Bradley A thermoresponsive and chemically defined hydrogel for long-term culture of human embryonic stem cells Nat Commun 4 2013 1335/1-10
105. A. Higuchi, A. Hamamura, Y. Shindo, H. Kitamura, B.O. Yoon, T. Mori, T. Uyama, and A. Umezawa Photon-modulated changes of cell attachments on poly(spiropyran-co-methyl methacrylate) membranes Biomacromolecules 5 2004 1770 1774
106. A. Higuchi, T. Yamamoto, K. Sugiyama, S. Hayashi, T.M. Tak, and T. Nakagawa Temperature-dependent cell detachment on Pluronic gels Biomacromolecules 6 2005 691 696
107. A. Tamura, J. Kobayashi, M. Yamato, and T. Okano Temperature-responsive poly(N-isopropylacrylamide)-grafted microcarriers for large-scale non-invasive harvest of anchorage-dependent cells Biomaterials 33 2012 3803 3812
108. T. Saito, K. Ohashi, R. Utoh, H. Shimizu, K. Ise, H. Suzuki, M. Yamato, T. Okano, and M. Gotoh Reversal of diabetes by the creation of neo-islet tissues into a subcutaneous site using islet cell sheets Transplantation 92 2011 1231 1236
109. H. Wei, S.X. Cheng, X.Z. Zhang, and R.X. Zhuo Thermo-sensitive polymeric micelles based on poly(N-isopropylacrylamide) as drug carriers Prog Polym Sci 34 2009 893 910
110. T.P. Kraehenbuehl, R. Langer, and L.S. Ferreira Three-dimensional biomaterials for the study of human pluripotent stem cells Nat Methods 8 2011 731 736
111. A.L. Carlson, C.A. Florek, J.J. Kim, T. Neubauer, J.C. Moore, R.I. Cohen, J. Kohn, M. Grumet, and P.V. Moghe Microfibrous substrate geometry as a critical trigger for organization, self-renewal, and differentiation of human embryonic stem cells within synthetic 3-dimensional microenvironments FASEB J 26 2012 3240 3251
112. B.W. Phillips, R. Horne, T.S. Lay, W.L. Rust, T.T. Teck, and J.M. Crook Attachment and growth of human embryonic stem cells on microcarriers J Biotechnol 138 2008 24 32
113. S. Janssens, C. Dubois, J. Bogaert, K theunissen, C. Deroose, W. Desmet, M. Kalantzi, L. Herbots, P. Sinnaeve, J. Dens, J. Maertens, F. Rademakers, S. Dymarkowski, O. Gheysens, J. Van Cleemput, G. Bormans, J. Nuyts, A. Belmans, L. Mortelmans, M. Boogaerts, and F. Van de Werf Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial Lancet 367 2006 113 121
114. K. Lunde, S. Solheim, S. Aakhus, H. Arnesen, M. Abdelnoor, T. Egeland, K. Endresen, A. Ilebekk, A. Mangschau, J.G. Fjeld, H.J. Smith, E. Taraldsrud, H.K. Grogaard, R. Bjornerheim, M. Brekke, C. Muller, E. Hopp, A. Ragnarsson, J.E. Brinchmann, and K. Forfang Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction New Engl J Med 355 2006 1199 1209
115. M. Serra, C. Correia, R. Malpique, C. Brito, J. Jensen, P. Bjorquist, M.J. Carrondo, and P.M. Alves Microencapsulation technology: a powerful tool for integrating expansion and cryopreservation of human embryonic stem cells PLoS ONE 6 2011 e23212/1-13
116. D. Steiner, H. Khaner, M. Cohen, S. Even-Ram, Y. Gil, P. Itsykson, T. Turetsky, M. Idelson, E. Aizenman, R. Ram, Y. Berman-Zaken, and B. Reubinoff Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension Nat Biotechnol 28 2010 361 364
117. M. Amit, J. Chebath, V. Margulets, I. Laevsky, Y. Miropolsky, K. Shariki, M. Peri, I. Blais, G. Slutsky, M. Revel, and J. Itskovitz-Eldor Suspension culture of undifferentiated human embryonic and induced pluripotent stem cells Stem Cell Rev 6 2010 248 259
118. R. Olmer, A. Haase, S. Merkert, W. Cui, J. Palecek, C. Ran, A. Kirschning, T. Scheper, S. Glage, K. Miller, E.C. Curnow, E.S. Hayes, and U. Martin Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium Stem Cell Res 5 2010 51 64
119. R. Zweigerdt, R. Olmer, H. Singh, A. Haverich, and U. Martin Scalable expansion of human pluripotent stem cells in suspension culture Nat Protocol 6 2011 689 700
120. M. Amit, I. Laevsky, Y. Miropolsky, K. Shariki, M. Peri, and J. Itskovitz-Eldor Dynamic suspension culture for scalable expansion of undifferentiated human pluripotent stem cells Nat Protocol 6 2011 572 579
121. M.R. Larijani, A. Seifinejad, B. Pournasr, V. Hajihoseini, S.N. Hassani, M. Totonchi, M. Yousefi, F. Shamsi, G.H. Salekdeh, and H. Baharvand Long-term maintenance of undifferentiated human embryonic and induced pluripotent stem cells in suspension Stem Cells Dev 20 2011 1911 1923
122. P.A. Marinho, D.T. Vareschini, I.C. Gomes, S. Paulsen Bda, D.R. Furtado, R. Castilho Ldos, and S.K. Rehen Xeno-free production of human embryonic stem cells in stirred microcarrier systems using a novel animal/human-component-free medium Tissue Eng C 19 2013 146 155
123. A.M. Fernandes, P.A. Marinho, R.C. Sartore, B.S. Paulsen, R.M. Mariante, L.R. Castilho, and S.K. Rehen Successful scale-up of human embryonic stem cell production in a stirred microcarrier culture system Braz J Med Biol Res 42 2009 515 522
124. M. Serra, C. Brito, M.F. Sousa, J. Jensen, R. Tostoes, J. Clemente, R. Strehl, J. Hyllner, M.J. Carrondo, and P.M. Alves Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control J Biotechnol 148 2010 208 215
125. S.K. Oh, A.K. Chen, Y. Mok, X. Chen, U.M. Lim, A. Chin, A.B. Choo, and S. Reuveny Long-term microcarrier suspension cultures of human embryonic stem cells Stem Cell Res 2 2009 219 230
126. J. Bardy, A.K. Chen, Y.M. Lim, S. Wu, S. Wei, H. Weiping, K. Chan, S. Reuveny, and S.K. Oh Microcarrier suspension cultures for high-density expansion and differentiation of human pluripotent stem cells to neural progenitor cells Tissue Eng C 19 2013 166 180
127. B.C. Heng, J. Li, A.K. Chen, S. Reuveny, S.M. Cool, W.R. Birch, and S.K. Oh Translating human embryonic stem cells from 2-dimensional to 3-dimensional cultures in a defined medium on laminin- and vitronectin-coated surfaces Stem Cells Dev 21 2012 1701 1715
128. M.P. Storm, C.B. Orchard, H.K. Bone, J.B. Chaudhuri, and M.J. Welham Three-dimensional culture systems for the expansion of pluripotent embryonic stem cells Biotechnol Bioeng 107 2010 683 695
129. L.T. Lock, and E.S. Tzanakakis Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture Tissue Eng A 15 2009 2051 2063
130. J.L. Wilson, and T.C. McDevitt Stem cell microencapsulation for phenotypic control, bioprocessing, and transplantation Biotechnol Bioeng 110 2013 667 682
131. K.Y. Lee, D.J. Mooney, and Alginate: properties and biomedical applications Prog Polym Sci 37 2012 106 126
132. D.Y. Ko, U.P. Shinde, B. Yeon, and B. Jeong Recent progress of in situ formed gels for biomedical applications Prog Polym Sci 38 2013 672 701
133. X. Huang, X. Zhang, X. Wang, C. Wang, and B. Tang Microenvironment of alginate-based microcapsules for cell culture and tissue engineering J Biosci Bioeng 114 2012 1 8
134. M. Jang, S.T. Lee, J.W. Kim, J.H. Yang, J.K. Yoon, J.C. Park, H.M. Ryoo, A.J. van der Vlies, J.Y. Ahn, J.A. Hubbell, Y.S. Song, G. Lee, and J.M. Lim A feeder-free, defined three-dimensional polyethylene glycol-based extracellular matrix niche for culture of human embryonic stem cells Biomaterials 34 2013 3571 3580
135. M.P. Lutolf, F.E. Weber, H.G. Schmoekel, J.C. Schense, T. Kohler, R. Muller, and J.A. Hubbell Repair of bone defects using synthetic mimetics of collagenous extracellular matrices Nat Biotechnol 21 2003 513 518
136. N. Harb, T.K. Archer, and N. Sato The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells PLoS ONE 3 2008 e3001/1-13