Defining synthetic surfaces for human pluripotent stem cell culture

Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998, 282: 1145–1147. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131: 861–872. 10.1016/j.cell.2007.11.019 Kim SH, Turnbull J, Guimond S: Extracellular matrix and cell signalling: The dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 2011, 209: 139–151. 10.1530/JOE-10-0377 Li L, Bennett SAL, Wang L: Role of E-cadherin and other cell adhesion molecules in survival and differentiation of human pluripotent stem cells. Cell Adh Migr 2012, 6: 59–70. 10.4161/cam.19583 Shen B, Delaney MK, Du X: Inside-out, outside-in, and inside-outside-in: G protein signaling in integrin-mediated cell adhesion, spreading, and retraction. Curr Opin Cell Biol 2012, 24: 600–606. 10.1016/j.ceb.2012.08.011 Lu J, Hou R, Booth CJ, Yang SH, Snyder M: Defined culture conditions of human embryonic stem cells. Proc Natl Acad Sci USA 2006, 103: 5688–5693. 10.1073/pnas.0601383103 Braam SR, Zeinstra L, Litjens S, Ward-van Oostwaard D, van den Brink S, van Laake L, Lebrin F, Kats P, Hochstenbach R, Passier R, et al.: Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells 2008, 26: 2257–2265. 10.1634/stemcells.2008-0291 Klim JR, Li L, Wrighton PJ, Piekarczyk MS, Kiessling LL: A defined glycosaminoglycan-binding substratum for human pluripotent stem cells. Nat Methods 2010, 7: 989–994. 10.1038/nmeth.1532 Melkoumian Z, Weber JL, Weber DM, Fadeev AG, Zhou Y, Dolley-Sonneville P, Yang J, Qiu L, Priest CA, Shogbon C, et al.: Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat Biotechnol 2010, 28: 606–610. 10.1038/nbt.1629 Nagaoka M, Si Tayeb K, Akaike T, Duncan SA: Culture of human pluripotent stem cells using completely defined conditions on a recombinant E-cadherin substratum. BMC Dev Biol 2010, 10: 60. 10.1186/1471-213X-10-60 Rodin S, Domogatskaya A, Ström S, Hansson EM, Chien KR, Inzunza J, Hovatta O, Tryggvason K: Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat Biotechnol 2010, 28: 611–615. 10.1038/nbt.1620 Saha K, Mei Y, Reisterer CM, Pyzocha NK, Yang J, Muffat J, Davies MC, Alexander MR, Langer R, Anderson DG, Jaenisch R: Surface-engineered substrates for improved human pluripotent stem cell culture under fully defined conditions. Proc Natl Acad Sci 2011, 108: 18714–18719. 10.1073/pnas.1114854108 Miyazaki T, Futaki S, Suemori H, Taniguchi Y, Yamada M, Kawasaki M, Hayashi M, Kumagai H, Nakatsuji N, Sekiguchi K, Kawase E: Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nat Commun 2012, 3: 1236. Irwin EF, Gupta R, Dashti DC, Healy KE: Engineered polymer-media interfaces for the long-term self-renewal of human embryonic stem cells. Biomaterials 2011, 32: 6912–6919. 10.1016/j.biomaterials.2011.05.058 Brafman D, Shah K, Fellner T, Chien S, Willert K: Defining long-term maintenance conditions of human embryonic stem cells with arrayed cellular microenvironment technology. Stem cells dev 2009, 18: 1141–1154. 10.1089/scd.2008.0410 Hakala H, Rajala K, Ojala M, Panula S, Areva S, Kellomaki M, Suuronen R, Skottman H: Comparison of Biomaterials and Extracellular Matrices as a Culture Platform for Multiple, Independently Derived Human Embryonic Stem Cell Lines. Tissue Eng Part A 2009, 15: 1775–1785. 10.1089/ten.tea.2008.0316 Akopian V, Andrews PW, Beil S, Benvenisty N, Brehm J, Christie M, Ford A, Fox V, Gokhale PJ, Healy L, et al.: Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. Vitro Cell Dev Biol Animal 2010, 46: 247–258. 10.1007/s11626-010-9297-z Kleinsmith LJ, Pierce GB Jr: Multipotentiality of Single Embryonal Carcinoma Cells. Cancer research 1964, 24: 1544–1551. Greenow K, Clarke AR: Controlling the stem cell compartment and regeneration in vivo: The role of pluripotency pathways. Physiol Rev 2012, 92: 75–99. 10.1152/physrev.00040.2010 Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, Bello PA, Benvenisty N, Berry LS, Bevan S, et al.: Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 2007, 25: 803–816. 10.1038/nbt1318 Hough SR, Laslett AL, Grimmond SB, Kolle G, Pera MF: A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells. PLoS ONE 2009, 4: e7708. 10.1371/journal.pone.0007708 Nichols J, Smith A: Naive and Primed Pluripotent States. Cell Stem Cell 2009, 4: 487–492. 10.1016/j.stem.2009.05.015 Xu Y, Zhu X, Hahm HS, Wei W, Hao E, Hayek A, Ding S: Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci USA 2010, 107: 8129–8134. 10.1073/pnas.1002024107 Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A: Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95: 379–391. 10.1016/S0092-8674(00)81769-9 Martin GR, Evans MJ: Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 1975, 72: 1441–1445. 10.1073/pnas.72.4.1441 Solter D, Knowles BB: Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 1978, 75: 5565–5569. 10.1073/pnas.75.11.5565 Clark AT, Rodriguez RT, Bodnar MS, Abeyta MJ, Cedars MI, Turek PJ, Firpo MT, Pera RAR: Human STELLAR, NANOG, and GDF3 Genes Are Expressed in Pluripotent Cells and Map to Chromosome 12p13, a Hotspot for Teratocarcinoma. Stem Cells 2004, 22: 169–179. 10.1634/stemcells.22-2-169 Spencer H, Keramari M, Ward CM: Using cadherin to assess spontaneous differentiation of embryonic stem cells. Methods Mol Biol 2011, 690: 81–94. Boyes J, Bird A: Repression of genes by DNA methylation depends on CpG density and promoter strength: Evidence for involvement of a methyl-CpG binding protein. EMBO Journal 1992, 11: 327–333. Baker-Andresen D, Ratnu VS, Bredy TW: Dynamic DNA methylation: A prime candidate for genomic metaplasticity and behavioral adaptation. Trends Neurosci 2013, 36: 3–13. 10.1016/j.tins.2012.09.003 Bock C, Kiskinis E, Verstappen G, Gu H, Boulting G, Smith ZD, Ziller M, Croft GF, Amoroso MW, Oakley DH, et al.: Reference maps of human es and ips cell variation enable high-throughput characterization of pluripotent cell lines. Cell 2011, 144: 439–452. 10.1016/j.cell.2010.12.032 Doetschman TC, Eistetter H, Katz M: The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 1985, 87: 27–45. Keller GM: In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol 1995, 7: 862–869. 10.1016/0955-0674(95)80071-9 Jones-Villeneuve EMV, McBurney MW, Rogers KA, Kalnins VI: Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol 1982, 94: 253–262. 10.1083/jcb.94.2.253 Laurent LC, Ulitsky I, Slavin I, Tran H, Schork A, Morey R, Lynch C, Harness JV, Lee S, Barrero MJ, et al.: Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 2011, 8: 106–118. 10.1016/j.stem.2010.12.003 Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK: Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001, 19: 971–974. 10.1038/nbt1001-971 Fu X, Toh WS, Liu H, Lu K, Li M, Cao T: Establishment of clinically compliant human embryonic stem cells in an autologous feeder-free system. Tissue Eng Part C Meth 2011, 17: 927–937. 10.1089/ten.tec.2010.0735 Prathalingam N, Ferguson L, Young L, Lietz G, Oldershaw R, Healy L, Craig A, Lister H, Binaykia R, Sheth R, et al.: Production and validation of a good manufacturing practice grade human fibroblast line for supporting human embryonic stem cell derivation and culture. Stem Cell Res Ther 2012, 3: 12. 10.1186/scrt103 Wang Q, Mou X, Cao H, Meng Q, Ma Y, Han P, Jiang J, Zhang H: A novel xeno-free and feeder-cell-free system for human pluripotent stem cell culture. Protein and Cell 2012, 3: 51–59. 10.1007/s13238-012-2002-0 Jones MB, Chu CH, Pendleton JC, Betenbaugh MJ, Shiloach J, Baljinnyam B, Rubin JS, Shamblott MJ: Proliferation and pluripotency of human embryonic stem cells maintained on type i collagen. Stem cells dev 2010, 19: 1923–1935. 10.1089/scd.2009.0326 Yue XS, Fujishiro M, Nishioka C, Arai T, Takahashi E, Gong JS, Akaike T, Ito Y: Feeder cells support the culture of induced pluripotent stem cells even after chemical fixation. PLoS ONE 2012, 7: e32707. 10.1371/journal.pone.0032707 Mei Y, Saha K, Bogatyrev SR, Yang J, Hook AL, Kalcioglu ZI, Cho SW, Mitalipova M, Pyzocha N, Rojas F, et al.: Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat Mater 2010, 9: 768–778. 10.1038/nmat2812 Stephenson E, Jacquet L, Miere C, Wood V, Kadeva N, Cornwell G, Codognotto S, Dajani Y, Braude P, Ilic D: Derivation and propagation of human embryonic stem cell lines from frozen embryos in an animal product-free environment. Nat Protoc 2012, 7: 1366–1381. 10.1038/nprot.2012.080 Villa-Diaz LG, Brown SE, Liu Y, Ross AM, Lahann J, Parent JM, Krebsbach PH: Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells 2012, 30: 1174–1181. 10.1002/stem.1084 Hu P, Luo BH: Integrin bi-directional signaling across the plasma membrane. J Cell Physiol 2013, 228: 306–312. 10.1002/jcp.24154 Kolle G, Ho M, Zhou Q, Chy HS, Krishnan K, Cloonan N, Bertoncello I, Laslett AL, Grimmond SM: Identification of human embryonic stem cell surface markers by combined membrane-polysome translation state array analysis and immunotranscriptional profiling. Stem Cells 2009, 27: 2446–2456. 10.1002/stem.182 Adjaye J, Huntriss J, Herwig R, Benkahla A, Brink TC, Wierling C, Hultschig C, Groth D, Yaspo ML, Picton HM, et al.: Primary differentiation in the human blastocyst: Comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 2005, 23: 1514–1525. 10.1634/stemcells.2005-0113 Baxter MA, Camarasa MV, Bates N, Small F, Murray P, Edgar D, Kimber SJ: Analysis of the distinct functions of growth factors and tissue culture substrates necessary for the long-term self-renewal of human embryonic stem cell lines. Stem Cell Res 2009, 3: 28–38. 10.1016/j.scr.2009.03.002 Eastham AM, Spencer H, Soncin F, Ritson S, Merry CLR, Stern PL, Ward CM: Epithelial-mesenchymal transition events during human embryonic stem cell differentiation. Cancer Res 2007, 67: 11254–11262. 10.1158/0008-5472.CAN-07-2253 Chen W, Villa-Diaz LG, Sun Y, Weng S, Kim JK, Lam RHW, Han L, Fan R, Krebsbach PH, Fu J: Nanotopography influences adhesion, spreading, and self-renewal of Human embryonic stem cells. ACS Nano 2012, 6: 4094–4103. 10.1021/nn3004923 Horák V, Fléchon JE: Immunocytochemical characterisation of rabbit and mouse embryonic fibroblasts. Reprod Nutr Dev 1998, 38: 683–695. 10.1051/rnd:19980610 Hughes CS, Postovit LM, Lajoie GA: Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 2010, 10: 1886–1890. 10.1002/pmic.200900758 Kadler KE, Hill A, Canty-Laird EG: Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 2008, 20: 495–501. 10.1016/j.ceb.2008.06.008 Heino J: The collagen family members as cell adhesion proteins. Bioessays 2007, 29: 1001–1010. 10.1002/bies.20636 Graf J, Iwamoto Y, Sasaki M, Martin GR, Kleinman HK, Robey FA, Yamada Y: Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell 1987, 48: 989–996. 10.1016/0092-8674(87)90707-0 Nomizu M, Kuratomi Y, Song SY, Ponce ML, Hoffman MP, Powell SK, Miyoshi K, Otaka A, Kleinman HK, Yamada Y: Identification of cell binding sequences in mouse laminin chain by systematic peptide screening. J Biol Chem 1997, 272: 32198–32205. 10.1074/jbc.272.51.32198 Meng Y, Eshghi S, Li YJ, Schmidt R, Schaffer DV, Healy KE: Characterization of integrin engagement during defined human embryonic stem cell culture. FASEB J 2010, 24: 1056–1065. 10.1096/fj.08-126821 Li Y, Powell S, Brunette E, Lebkowski J, Mandalam R: Expansion of human embryonic stem cells in defined serum-free medium devoid of animal-derived products. Biotechnol Bioeng 2005, 91: 688–698. 10.1002/bit.20536 Fletcher JM, Ferrier PM, Gardner JO, Harkness L, Dhanjal S, Serhal P, Harper J, Delhanty J, Brownstein DG, Prasad YR, et al.: Variations in humanized and defined culture conditions supporting derivation of new human embryonic stem cell lines. Cloning Stem Cells 2006, 8: 319–334. 10.1089/clo.2006.8.319 Miyazaki T, Futaki S, Hasegawa K, Kawasaki M, Sanzen N, Hayashi M, Kawase E, Sekiguchi K, Nakatsuji N, Suemori H: Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem Biophys Res Commun 2008, 375: 27–32. 10.1016/j.bbrc.2008.07.111 Manton KJ, Richards S, Van Lonkhuyzen D, Cormack L, Leavesley D, Upton Z: A chimeric vitronectin: IGF-I protein supports feeder-cell-free and serum-free culture of human embryonic stem cells. Stem Cells Dev 2010, 19: 1297–1305. 10.1089/scd.2009.0504 Derda R, Li L, Orner BP, Lewis RL, Thomson JA, Kiessling L: Defined substrates for human embryonic stem cell growth identified from surface arrays. ACS Chem Biol 2007, 2: 347–355. 10.1021/cb700032u Deutzmann R, Aumailley M, Wiedemann H, Pysny W, Timpl R, Edgar D: Cell adhesion, spreading and neurite stimulation by laminin fragment E8 depends on maintenance of secondary and tertiary structure in its rod and globular domain. Eur J Biochem 1990, 191: 513–522. 10.1111/j.1432-1033.1990.tb19151.x Keski Oja J: Polymerization of a major surface associated glycoprotein, fibronectin, in cultured fibroblasts. FEBS Lett 1976, 71: 325–329. 10.1016/0014-5793(76)80962-3 Singh P, Carraher C, Schwarzbauer JE: Assembly of fibronectin extracellular marix. Annu Rev Cell Dev Biol 2010, 26: 397–419. 10.1146/annurev-cellbio-100109-104020 Tsutsui H, Valamehr B, Hindoyan A, Qiao R, Ding X, Guo S, Witte ON, Liu X, Ho C-M, Wu H: An optimized small molecule inhibitor cocktail supports long-term maintenance of human embryonic stem cells. Nat Commun 2011, 2: 167. Liu Y, Charles LF, Zarembinski TI, Johnson KI, Atzet SK, Wesselschmidt RL, Wight ME, Kuhn LT: Modified Hyaluronan Hydrogels Support the Maintenance of Mouse Embryonic Stem Cells and Human Induced Pluripotent Stem Cells. Macromol Biosci 2012, 12: 1034–1042. 10.1002/mabi.201200043 Hughes CS, Radan L, Betts D, Postovit LM, Lajoie GA: Proteomic analysis of extracellular matrices used in stem cell culture. Proteomics 2011, 11: 3983–3991. 10.1002/pmic.201100030 Hautanen A, Gailit J, Mann DM, Ruoslahti E: Effects of modifications of the RGD sequence and its context on recognition by the fibronectin receptor. J Biol Chem 1989, 264: 1437–1442. Mardilovich A, Craig JA, McCammon MQ, Garg A, Kokkoli E: Design of a novel fibronectin-mimetic peptide-amphiphile for functionalized biomaterials. Langmuir 2006, 22: 3259–3264. 10.1021/la052756n Schvartz I, Seger D, Shaltiel S: Vitronectin. Int J Biochem Cell Biol 1999, 31: 539–544. 10.1016/S1357-2725(99)00005-9 Suzuki S, Oldberg A, Hayman EG, Pierschbacher MD, Ruoslahti E: Complete amino acid sequence of human vitronectin deduced from cDNA. Similarity of cell attachment sites in vitronectin and fibronectin. EMBO Journal 1985, 4: 2519–2524. Yap LYW, Li J, Phang IY, Ong LT, Ow JZE, Goh JCH, Nurcombe V, Hobley J, Choo ABH, Oh SKW, et al.: Defining a threshold surface density of vitronectin for the stable expansion of human embryonic stem cells. Tissue Eng Part C Meth 2011, 17: 193–207. 10.1089/ten.tec.2010.0328 Meng G, Liu S, Rancourt DE: 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 2012, 21: 2036–2048. 10.1089/scd.2011.0489 Chen G, Gulbranson DR, Hou Z, Bolin JM, Ruotti V, Probasco MD, Smuga-Otto K, Howden SE, Diol NR, Propson NE, et al.: Chemically defined conditions for human iPSC derivation and culture. Nat Methods 2011, 8: 424–429. 10.1038/nmeth.1593 Kim HT, Lee KI, Kim DW, Hwang DY: An ECM-based culture system for the generation and maintenance of xeno-free human iPS cells. Biomaterials 2013, 34: 1041–1050. 10.1016/j.biomaterials.2012.10.064 Abraham S, Riggs MJ, Nelson K, Lee V, Rao RR: Characterization of human fibroblast-derived extracellular matrix components for human pluripotent stem cell propagation. Acta Biomater 2010, 6: 4622–4633. 10.1016/j.actbio.2010.07.029 Prowse ABJ, Doran MR, Cooper-White JJ, Chong F, Munro TP, Fitzpatrick J, Chung TL, Haylock DN, Gray PP, Wolvetang EJ: Long term culture of human embryonic stem cells on recombinant vitronectin in ascorbate free media. Biomaterials 2010, 31: 8281–8288. 10.1016/j.biomaterials.2010.07.037 Klim JR, Fowler AJ, Courtney AH, Wrighton PJ, Sheridan RTC, Wong ML, Kiessling LL: Small-molecule-modified surfaces engage cells through the α vβ 3 integrin. ACS Chem Biol 2012, 7: 518–525. 10.1021/cb2004725 Ludwig TE, Bergendahl V, Levenstein ME, Yu J, Probasco MD, Thomson JA: Feeder-independent culture of human embryonic stem cells. Nat meth 2006, 3: 637–646. 10.1038/nmeth902 Lu HF, Narayanan K, Lim SX, Gao S, Leong MF, Wan ACA: A 3D microfibrous scaffold for long-term human pluripotent stem cell self-renewal under chemically defined conditions. Biomaterials 2012, 33: 2419–2430. 10.1016/j.biomaterials.2011.11.077 Mahlstedt MM, Anderson D, Sharp JS, McGilvray R: Barbadillo Muñoz MD, Buttery LD, Alexander MR, Rose FRAJ, Denning C: Maintenance of pluripotency in human embryonic stem cells cultured on a synthetic substrate in conditioned medium. Biotechnol Bioeng 2010, 105: 130–140. 10.1002/bit.22520 Bigdeli N, Andersson M, Strehl R, Emanuelsson K, Kilmare E, Hyllner J, Lindahl A: Adaptation of human embryonic stem cells to feeder-free and matrix-free culture conditions directly on plastic surfaces. J Biotechnol 2008, 133: 146–153. 10.1016/j.jbiotec.2007.08.045 Nandivada H, Villa-Diaz LG, O'Shea KS, Smith GD, Krebsbach PH, Lahann J: Fabrication of synthetic polymer coatings and their use in feeder-free culture of human embryonic stem cells. Nat Protoc 2011, 6: 1037–1043. 10.1038/nprot.2011.342 Chowdhury F, Li Y, Poh YC, Yokohama-Tamaki T, Wang N, Tanaka TS: Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS ONE 2010, 5: e15655. 10.1371/journal.pone.0015655 Kolhar P, Kotamraju VR, Hikita ST, Clegg DO, Ruoslahti E: Synthetic surfaces for human embryonic stem cell culture. J Biotechnol 2010, 146: 143–146. 10.1016/j.jbiotec.2010.01.016 Tamada Y, Ikada Y: Effect of Preadsorbed Proteins on Cell Adhesion to Polymer Surfaces. J Colloid Interface Sci 1993, 155: 334–339. 10.1006/jcis.1993.1044 Love JC, Estroff LA, Kriebel JK, Nuzzo RG, Whitesides GM: Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev 2005, 105: 1103–1169. 10.1021/cr0300789 Jonas SJ, Alva JA, Richardson W, Sherman SP, Galic Z, Pyle AD, Dunn B: A spatially and chemically defined platform for the uniform growth of human pluripotent stem cells. Mater Sci Eng C 2013, 33: 234–241. 10.1016/j.msec.2012.08.035 Flynn NT, Tran TNT, Cima MJ, Langer R: Long-term stability of self-assembled monolayers in biological media. Langmuir 2003, 19: 10909–10915. 10.1021/la035331e Gasimli L, Linhardt RJ, Dordick JS: Proteoglycans in stem cells. Biotechnol Appl Biochem 2012, 59: 65–76. 10.1002/bab.1002 Musah S, Morin SA, Wrighton PJ, Zwick DB, Jin S, Kiessling LL: Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS Nano 2012, 6: 10168–10177. 10.1021/nn3039148 Ballut L, Sapay N, Chautard É, Imberty A, Ricard-Blum S: Mapping of heparin/heparan sulfate binding sites on αvβ3 integrin by molecular docking. J Mol Recognit 2013, 26: 76–85. 10.1002/jmr.2250 Ford-Perriss M, Guimond SE, Greferath U, Kita M, Grobe K, Habuchi H, Kimata K, Esko JD, Murphy M, Turnbull JE: Variant heparan sulfates synthesized in developing mouse brain differentially regulate FGF signaling. Glycobiology 2002, 12: 721–727. 10.1093/glycob/cwf072 Levenstein ME, Ludwig TE, Xu RH, Llanas RA, VanDenHeuvel-Kramer K, Manning D, Thomson JA: Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 2006, 24: 568–574. 10.1634/stemcells.2005-0247 Kraushaar DC, Yamaguchi Y, Wang L: Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J Biol Chem 2010, 285: 5907–5916. 10.1074/jbc.M109.066837 Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA: Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005, 2: 185–190. 10.1038/nmeth744 Villa-Diaz LG, Nandivada H, Ding J, Nogueira-De-Souza NC, Krebsbach PH, O'Shea KS, Lahann J, Smith GD: Synthetic polymer coatings for long-term growth of human embryonic stem cells. Nat Biotechnol 2010, 28: 581–583. 10.1038/nbt.1631 Ross AM, Nandivada H, Ryan AL, Lahann J: Synthetic substrates for long-term stem cell culture. Polymer (United Kingdom) 2012, 53: 2533–2539. Brafman DA, Chang CW, Fernandez A, Willert K, Varghese S, Chien S: Long-term human pluripotent stem cell self-renewal on synthetic polymer surfaces. Biomaterials 2010, 31: 9135–9144. 10.1016/j.biomaterials.2010.08.007 Zhang L, Cao Z, Bai T, Carr L, Ella-Menye JR, Irvin C, Ratner BD, Jiang S: Zwitterionic hydrogels implanted in mice resist the foreign-body reaction. Nat Biotechnol 2013,31(6):553–556. 10.1038/nbt.2580 Chang CW, Hwang Y, Brafman D, Hagan T, Phung C, Varghese S: Engineering cell-material interfaces for long-term expansion of human pluripotent stem cells. Biomaterials 2013, 34: 912–921. 10.1016/j.biomaterials.2012.10.020 Gao SY, Lees JG, Wong JCY, Croll TI, George P, Cooper-White JJ, Tuch BE: Modeling the adhesion of human embryonic stem cells to poly(lactic-co- glycolic acid) surfaces in a 3D environment. J Biomed Materials Res Part A 2010, 92: 683–692. Lib J, Bardy J, Yap LYW, Chen A, Nurcombe V, Cool SM, Oh SKW, Birch WR: Impact of vitronectin concentration and surface properties on the stable propagation of human embryonic stem cells. Biointerphases 2010, 5: 132–142. Barbey R, Lavanant L, Paripovic D, Schüwer N, Sugnaux C, Tugulu S, Klok HA: Polymer brushes via surface-initiated controlled radical polymerization: synthesis, characterization, properties, and applications. Chem Rev 2009, 109: 5437–5527. 10.1021/cr900045a Coad BR, Lu Y, Glattauer V, Meagher L: Substrate-independent method for growing and modulating the density of polymer brushes from surfaces by atrp. ACS Appl Materials Interfaces 2012, 4: 2811–2823. 10.1021/am300463q Ameringer T, Fransen P, Bean P, Johnson G, Pereira S, Evans RA, Thissen H, Meagher L: Polymer coatings that display specific biological signals while preventing nonspecific interactions. J Biomed Mater Res A 2012, 100 A: 370–379. Jing D, Parikh A, Canty JM Jr, Tzanakakis ES: Stem cells for heart cell therapies. Tissue Eng Part B Rev 2008, 14: 393–406. 10.1089/ten.teb.2008.0262 Want AJ, Nienow AW, Hewitt CJ, Coopman K: Large-scale expansion and exploitation of pluripotent stem cells for regenerative medicine purposes: Beyond the T flask. Regen Med 2012, 7: 71–84. Bardy J, Chen AK, Lim YM, Wu S, Wei S, Weiping H, Chan K, Reuveny S, Oh SKW: Microcarrier suspension cultures for high-density expansion and differentiation of human pluripotent stem cells to neural progenitor cells. Tissue Eng Part C Methods 2013, 19: 166–180. 10.1089/ten.tec.2012.0146 Abbasalizadeh S, Larijani MR, Samadian A, Baharvand H: Bioprocess development for mass production of size-controlled human pluripotent stem cell aggregates in stirred suspension bioreactor. Tissue Eng Part C Meth 2012, 18: 831–851. 10.1089/ten.tec.2012.0161 Domogatskaya A, Rodin S, Boutaud A, Tryggvason K: Laminin-511 but Not-332,-111, or-411 Enables Mouse Embryonic Stem Cell Self-Renewal In Vitro. Stem Cells 2008, 26: 2800–2809. 10.1634/stemcells.2007-0389 Kalaskar DM, Downes JE, Murray P, Edgar DH, Williams RL: Characterization of the interface between adsorbed fibronectin and human embryonic stem cells. J R Soc Interface 2013, 10: 20130139. 10.1098/rsif.2013.0139 Collins MN, Birkinshaw C: Hyaluronic acid based scaffolds for tissue engineering-A review. Carbohydr Polym 2012, 92: 1262–1279. Gerecht S, Burdick JA, Ferreira LS, Townsend SA, Langer R, Vunjak-Novakovic G: Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci USA 2007, 104: 11298–11303. 10.1073/pnas.0703723104 Li YJ, Chung EH, Rodriguez RT, Firpo MT, Healy KE: Hydrogels as artificial matrices for human embryonic stem cell self-renewal. J Biomed Mater Res A 2006, 79: 1–5. Chen AKL, Chen X, Choo ABH, Reuveny S, Oh SKW: Critical microcarrier properties affecting the expansion of undifferentiated human embryonic stem cells. Stem Cell Res 2011, 7: 97–111. 10.1016/j.scr.2011.04.007 Serra M, Brito C, Correia C, Alves PM: Process engineering of human pluripotent stem cells for clinical application. Trends Biotechnol 2012, 30: 350–359. 10.1016/j.tibtech.2012.03.003 O'Brien C, Laslett AL: Suspended in culture - Human pluripotent cells for scalable technologies. Stem Cell Res 2012, 9: 167–170. 10.1016/j.scr.2012.06.001 Heng BC, Li J, Chen AKL, Reuveny S, Cool SM, Birch WR, Oh SKW: 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 2012, 21: 1701–1715. 10.1089/scd.2011.0509 Ramos-Mejia V, Bueno C, Roldan M, Sanchez L, Ligero G, Menendez P, Martin M: The adaptation of human embryonic stem cells to different feeder-free culture conditions is accompanied by a mitochondrial response. Stem Cells Dev 2012, 21: 1145–1155. 10.1089/scd.2011.0248 Tompkins JD, Hall C, Chen VCY, Li AX, Wu X, Hsu D, Couture LA, Riggs AD: Epigenetic stability, adaptability, and reversibility in human embryonic stem cells. Proc Natl Acad Sci USA 2012, 109: 12544–12549. 10.1073/pnas.1209620109 Chen T, Yuan D, Wei B, Jiang J, Kang J, Ling K, Gu Y, Li J, Xiao L, Pei G: E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation. Stem Cells 2010, 28: 1315–1325. 10.1002/stem.456 Higuchi A, Ling QD, Chang Y, Hsu ST, Umezawa A: Physical cues of biomaterials guide stem cell differentiation fate. Chem Rev 2013, 113: 3297–3328. 10.1021/cr300426x Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, Frane JL, Crandall LJ, Daigh CA, Conard KR, Piekarczyk MS, et al.: Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 2006, 24: 185–187. 10.1038/nbt1177 Harb N, Archer TK, Sato N: The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells. PLoS ONE 2008, 3: e3001. 10.1371/journal.pone.0003001 Derda R, Musah S, Orner BP, Klim JR, Li N, Kiessling LL: High-throughput discovery of synthetic surfaces that support proliferation of pluripotent cells. J Am Chem Soc 2010, 132: 1289–1295. 10.1021/ja906089g