Human embryonic stem cell cultivation: Historical perspective and evolution of xeno-free culture systems

Reproductive Biology and Endocrinology

Volumn 13, Issue 1, 2015, Pages

  Desai, Nina ^a   Rambhia, Pooja ^a   Gishto, Arsela ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

3 D culture; Cell adhesion; Differentiation; ECM (extracellular matrix); Embryonic stem cells; Feeder layers; Human; Hydrogel; Pluripotent; Tissue regeneration

Indexed keywords

CELL ADHESION MOLECULE; GROWTH FACTOR; LAMININ; UVOMORULIN; VITRONECTIN; CULTURE MEDIUM;

AGE RELATED MACULAR DEGENERATION; BLOOD GROUP TYPING; CELL DIFFERENTIATION; COCULTURE; CULTURE MEDIUM; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; FEEDER CELL; HLA MATCHING; HUMAN; INNER CELL MASS; INSULIN DEPENDENT DIABETES MELLITUS; MONOLAYER CULTURE; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; RETINA PIGMENT CELL; REVIEW; SPINAL CORD INJURY; STARGARDT DISEASE; STEM CELL CULTURE; STEM CELL TRANSPLANTATION; XENO FREE CULTURE; ANIMAL; CELL CULTURE TECHNIQUE; CELL PROLIFERATION; HISTORY; HUMAN EMBRYONIC STEM CELL; MOUSE; STEM CELL RESEARCH; TRENDS;

ANIMALIA; BOVINAE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; COCULTURE TECHNIQUES; CULTURE MEDIA; FEEDER CELLS; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMAN EMBRYONIC STEM CELLS; HUMANS; MICE; STEM CELL RESEARCH;

EID: 84928235228     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/s12958-015-0005-4     Document Type: Review

References (148)

1. Baharvand H, Jafary H, Massumi M, Ashtiani SK. Generation of insulin-secreting cells from human embryonic stem cells. Dev Growth Differ. 2006;48(5):323-32. doi:10.1111/j.1440-169X.2006.00867.x.
2. Sundberg M, Andersson PH, Akesson E, Odeberg J, Holmberg L, Inzunza J, et al. Markers of pluripotency and differentiation in human neural precursor cells derived from embryonic stem cells and CNS tissue. Cell Transplant. 2011;20(2):177-91. doi:10.3727/096368910X527266.
3. Pal R, Mamidi MK, Das AK, Bhonde R. Comparative analysis of cardiomyocyte differentiation from human embryonic stem cells under 3-D and 2-D culture conditions. J Biosci Bioeng. 2013;115(2):200-6. doi:10.1016/j.jbiosc.2012.08.018.
4. Miki T, Ring A, Gerlach J. Hepatic differentiation of human embryonic stem cells is promoted by three-dimensional dynamic perfusion culture conditions. Tissue Eng Part C Methods. 2011;17(5):557-68. doi:10.1089/ten.TEC.2010.0437.
5. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282(5391):1145-7.
6. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol. 2001;19(10):971-4. doi:10.1038/nbt1001-971.
7. Marti M, Mulero L, Pardo C, Morera C, Carrio M, Laricchia-Robbio L, et al. Characterization of pluripotent stem cells. Nat Protoc. 2013;8(2):223-53. doi:10.1038/nprot.2012.154.
8. Loser P, Schirm J, Guhr A, Wobus AM, Kurtz A. Human embryonic stem cell lines and their use in international research. Stem Cells. 2010;28(2):240-6. doi:10.1002/stem.286.
9. Meng G, Liu S, Li X, Krawetz R, Rancourt DE. Derivation of human embryonic stem cell lines after blastocyst microsurgery. Biochem Cell Biol. 2010;88(3):479-90. doi:10.1139/o09-188.
10. Strom S, Inzunza J, Grinnemo KH, Holmberg K, Matilainen E, Stromberg AM, et al. Mechanical isolation of the inner cell mass is effective in derivation of new human embryonic stem cell lines. Hum Reprod. 2007;22(12):3051-8. doi:10.1093/humrep/dem335.
11. Tanaka N, Takeuchi T, Neri QV, Sills ES, Palermo GD. Laser-assisted blastocyst dissection and subsequent cultivation of embryonic stem cells in a serum/cell free culture system: applications and preliminary results in a murine model. J Transl Med. 2006;4:20. doi:10.1186/1479-5876-4-20.
12. Turetsky T, Aizenman E, Gil Y, Weinberg N, Shufaro Y, Revel A, et al. Laser-assisted derivation of human embryonic stem cell lines from IVF embryos after preimplantation genetic diagnosis. Hum Reprod. 2008;23(1):46-53. doi:10.1093/humrep/dem351.
13. Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, Zucker JP, et al. Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med. 2004;350(13):1353-6. doi:10.1056/NEJMsr040330.
14. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol. 2000;18(4):399-404. doi:10.1038/74447.
15. Tannenbaum SE, Turetsky TT, Singer O, Aizenman E, Kirshberg S, Ilouz N, et al. Derivation of xeno-free and GMP-grade human embryonic stem cells-platforms for future clinical applications. PLoS One. 2012;7(6):e35325. doi:10.1371/journal.pone.0035325.
16. Johnson MH. Human ES, cells and a blastocyst from one embryo: exciting science but conflicting ethics? Cell Stem Cell. 2008;2(2):103-4. doi:10.1016/j.stem.2008.01.021.
17. Chung Y, Klimanskaya I, Becker S, Li T, Maserati M, Lu SJ, et al. Human embryonic stem cell lines generated without embryo destruction. Cell Stem Cell. 2008;2(2):113-7. doi:10.1016/j.stem.2007.12.013.
18. Ilic D, Giritharan G, Zdravkovic T, Caceres E, Genbacev O, Fisher SJ, et al. Derivation of human embryonic stem cell lines from biopsied blastomeres on human feeders with minimal exposure to xenomaterials. Stem Cells Dev. 2009;18(9):1343-50. doi:10.1089/scd.2008.0416.
19. Klimanskaya I, Chung Y, Becker S, Lu SJ, Lanza R. Human embryonic stem cell lines derived from single blastomeres. Nature. 2006;444(7118):481-5. doi:10.1038/nature05142.
20. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol. 2000;227(2):271-8. doi:10.1006/dbio.2000.9912.
21. Klimanskaya I, Chung Y, Meisner L, Johnson J, West MD, Lanza R. Human embryonic stem cells derived without feeder cells. Lancet. 2005;365(9471):1636-41. doi:10.1016/S0140-6736(05)66473-2.
22. Galan A, Diaz-Gimeno P, Poo ME, Valbuena D, Sanchez E, Ruiz V, et al. Defining the genomic signature of totipotency and pluripotency during early human development. PLoS One. 2013;8(4):e62135. doi:10.1371/journal.pone.0062135.
23. Giritharan G, Ilic D, Gormley M, Krtolica A. Human embryonic stem cells derived from embryos at different stages of development share similar transcription profiles. PLoS One. 2011;6(10):e26570. doi:10.1371/journal.pone.0026570.
24. Cobo F, Navarro JM, Herrera MI, Vivo A, Porcel D, Hernandez C, et al. Electron microscopy reveals the presence of viruses in mouse embryonic fibroblasts but neither in human embryonic fibroblasts nor in human mesenchymal cells used for hESC maintenance: toward an implementation of microbiological quality assurance program in stem cell banks. Cloning Stem Cells. 2008;10(1):65-74. doi:10.1089/clo.2007.0020.
25. Llewelyn CA, Hewitt PE, Knight RS, Amar K, Cousens S, Mackenzie J, et al. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet. 2004;363(9407):417-21. doi:10.1016/S0140-6736(04)15486-X.
26. Kubikova I, Konecna H, Sedo O, Zdrahal Z, Rehulka P, Hribkova H, et al. Proteomic profiling of human embryonic stem cell-derived microvesicles reveals a risk of transfer of proteins of bovine and mouse origin. Cytotherapy. 2009;11(3):330-40. 1 p following 40. doi:10.1080/14653240802595531.
27. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20(5):847-56. doi:10.1038/sj.leu.2404132.
28. Martin MJ, Muotri A, Gage F, Varki A. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med. 2005;11(2):228-32. doi:10.1038/nm1181.
29. Bongso A, Fong CY, Ng SC, Ratnam S. Isolation and culture of inner cell mass cells from human blastocysts. Hum Reprod. 1994;9(11):2110-7.
30. Amit M, Margulets V, Segev H, Shariki K, Laevsky I, Coleman R, et al. Human feeder layers for human embryonic stem cells. Biol Reprod. 2003;68(6):2150-6. doi:10.1095/biolreprod.102.012583.
31. Richards M, Fong CY, Chan WK, Wong PC, Bongso A. Human feeders support prolonged undifferentiated growth of human inner cell masses and embryonic stem cells. Nat Biotechnol. 2002;20(9):933-6. doi:10.1038/nbt726.
32. Xi J, Wang Y, Zhang P, He L, Nan X, Yue W, et al. Human fetal liver stromal cells that overexpress bFGF support growth and maintenance of human embryonic stem cells. PLoS One. 2010;5(12):e14457. doi:10.1371/journal.pone.0014457.
33. Cheng L, Hammond H, Ye Z, Zhan X, Dravid G. Human adult marrow cells support prolonged expansion of human embryonic stem cells in culture. Stem Cells. 2003;21(2):131-42. doi:10.1634/stemcells.21-2-131.
34. Cho M, Lee EJ, Nam H, Yang JH, Cho J, Lim JM, et al. Human feeder layer system derived from umbilical cord stromal cells for human embryonic stem cells. Fertil Steril. 2010;93(8):2525-31. doi:10.1016/j.fertnstert.2010.03.027.
35. Genbacev O, Krtolica A, Zdravkovic T, Brunette E, Powell S, Nath A, et al. Serum-free derivation of human embryonic stem cell lines on human placental fibroblast feeders. Fertil Steril. 2005;83(5):1517-29. doi:10.1016/j.fertnstert.2005.01.086.
36. Miyamoto K, Hayashi K, Suzuki T, Ichihara S, Yamada T, Kano Y, et al. Human placenta feeder layers support undifferentiated growth of primate embryonic stem cells. Stem Cells. 2004;22(4):433-40. doi:10.1634/stemcells.22-4-433.
37. Gao X, Yan J, Shen Y, Li M, Ma S, Wang J, et al. Human fetal trophonema matrix and uterine endometrium support better human embryonic stem cell growth and neural differentiation than mouse embryonic fibroblasts. Cell Reprogram. 2010;12(3):295-303. doi:10.1089/cell.2009.0071.
38. Lee JB, Lee JE, Park JH, Kim SJ, Kim MK, Roh SI, et al. Establishment and maintenance of human embryonic stem cell lines on human feeder cells derived from uterine endometrium under serum-free condition. Biol Reprod. 2005;72(1):42-9. doi:10.1095/biolreprod.104.033480.
39. Lee JB, Song JM, Lee JE, Park JH, Kim SJ, Kang SM, et al. Available human feeder cells for the maintenance of human embryonic stem cells. Reproduction. 2004;128(6):727-35. doi:10.1530/rep.1.00415.
40. Aguilar-Gallardo C, Poo M, Gomez E, Galan A, Sanchez E, Marques-Mari A, et al. Derivation, characterization, differentiation, and registration of seven human embryonic stem cell lines (VAL-3,-4,-5,-6 M,-7,-8, and-9) on human feeder. In Vitro Cell Dev Biol Anim. 2010;46(3-4):317-26. doi:10.1007/s11626-010-9285-3.
41. Rajala K, Lindroos B, Hussein SM, Lappalainen RS, Pekkanen-Mattila M, Inzunza J, et al. A defined and xeno-free culture method enabling the establishment of clinical-grade human embryonic, induced pluripotent and adipose stem cells. PLoS One. 2010;5(4):e10246. doi:10.1371/journal.pone.0010246.
42. Rajala K, Hakala H, Panula S, Aivio S, Pihlajamaki H, Suuronen R, et al. Testing of nine different xeno-free culture media for human embryonic stem cell cultures. Hum Reprod. 2007;22(5):1231-8. doi:10.1093/humrep/del523.
43. Desai N, Ludgin J, Goldberg J, Falcone T. Development of a xeno-free non-contact co-culture system for derivation and maintenance of embryonic stem cells using a novel human endometrial cell line. J Assist Reprod Genet. 2013;30(5):609-15. doi:10.1007/s10815-013-9977-1.
44. Chen HF, Chuang CY, Shieh YK, Chang HW, Ho HN, Kuo HC. Novel autogenic feeders derived from human embryonic stem cells (hESCs) support an undifferentiated status of hESCs in xeno-free culture conditions. Hum Reprod. 2009;24(5):1114-25. doi:10.1093/humrep/dep003.
45. Fu X, Toh WS, Liu H, Lu K, Li M, Hande MP, et al. Autologous feeder cells from embryoid body outgrowth support the long-term growth of human embryonic stem cells more effectively than those from direct differentiation. Tissue Eng Part C Methods. 2010;16(4):719-33. doi:10.1089/ten.tec.2009.0360.
46. Abraham S, Sheridan SD, Laurent LC, Albert K, Stubban C, Ulitsky I, et al. Propagation of human embryonic and induced pluripotent stem cells in an indirect co-culture system. Biochem Biophys Res Commun. 2010;393(2):211-6. doi:10.1016/j.bbrc.2010.01.101.
47. Park Y, Kim JH, Lee SJ, Choi IY, Park SJ, Lee SR, et al. Human feeder cells can support the undifferentiated growth of human and mouse embryonic stem cells using their own basic fibroblast growth factors. Stem Cells Dev. 2011;20(11):1901-10. doi:10.1089/scd.2010.0496.
48. Liu CX, Zhang RL, Gao J, Li T, Ren Z, Zhou CQ, et al. Derivation. of human embryonic stem cell lines without any exogenous growth factors. Mol Reprod Dev. 2014; doi:10.1002/mrd.22312.
49. Vallier L, Alexander M, Pedersen RA. Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci. 2005;118(Pt 19):4495-509. doi:10.1242/jcs.02553.
50. Albano RM, Groome N, Smith JC. Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development. 1993;117(2):711-23.
51. Beattie GM, Lopez AD, Bucay N, Hinton A, Firpo MT, King CC, et al. Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells. 2005;23(4):489-95. doi:10.1634/stemcells. 2004-0279.
52. Chen S, Choo A, Chin A, Oh SK. TGF-beta2 allows pluripotent human embryonic stem cell proliferation on E6/E7 immortalized mouse embryonic fibroblasts. J Biotechnol. 2006;122(3):341-61. doi:10.1016/j.jbiotec.2005.11.022.
53. James D, Levine AJ, Besser D, Hemmati-Brivanlou A. TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development. 2005;132(6):1273-82. doi:10.1242/dev.01706.
54. Vallier L, Touboul T, Chng Z, Brimpari M, Hannan N, Millan E, et al. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways. PLoS One. 2009;4(6):e6082. doi:10.1371/journal.pone.0006082.
55. Hongisto H, Vuoristo S, Mikhailova A, Suuronen R, Virtanen I, Otonkoski T, et al. Laminin-511 expression is associated with the functionality of feeder cells in human embryonic stem cell culture. Stem Cell Res. 2012;8(1):97-108. doi:10.1016/j.scr.2011.08.005.
56. Kleinman HK. Preparation of basement membrane components from EHS tumors. Curr Protoc Cell Biol. 2001;Chapter 10:Unit 10 2. doi:10.1002/0471143030.cb1002s00.
57. Brimble SN, Zeng X, Weiler DA, Luo Y, Liu Y, Lyons IG, et al. Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev. 2004;13(6):585-97. doi:10.1089/scd.2004.13.585.
58. Hakala H, Rajala K, Ojala M, Panula S, Areva S, Kellomaki M, et al. 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(7):1775-85. doi:10.1089/ten.tea.2008.0316.
59. Levenstein ME, Ludwig TE, Xu RH, Llanas RA, VanDenHeuvel-Kramer K, Manning D, et al. Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells. 2006;24(3):568-74. doi:10.1634/stemcells. 2005-0247.
60. Montes R, Ligero G, Sanchez L, Catalina P, de la Cueva T, Nieto A, et al. Feeder-free maintenance of hESCs in mesenchymal stem cell-conditioned media: distinct requirements for TGF-beta and IGF-II. Cell Res. 2009;19(6):698-709. doi:10.1038/cr.2009.35.
61. Priddle H, Allegrucci C, Burridge P, Munoz M, Smith NM, Devlin L, et al. Derivation and characterisation of the human embryonic stem cell lines, NOTT1 and NOTT2. In Vitro Cell Dev Biol Anim. 2010;46(3-4):367-75. doi:10.1007/s11626-010-9290-6.
62. 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(3):185-90. doi:10.1038/nmeth744.
63. Yao S, Chen S, Clark J, Hao E, Beattie GM, Hayek A, et al. Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc Natl Acad Sci U S A. 2006;103(18):6907-12. doi:10.1073/pnas.0602280103.
64. Carlson Scholz JA, Garg R, Compton SR, Allore HG, Zeiss CJ, Uchio EM. Poliomyelitis in MuLV-infected ICR-SCID mice after injection of basement membrane matrix contaminated with lactate dehydrogenase-elevating virus. Comp Med. 2011;61(5):404-11.
65. 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 Methods. 2011;17(9):927-37. doi:10.1089/ten.TEC.2010.0735.
66. Ludwig T, AT J. Defined, feeder-independent medium for human embryonic stem cell culture. Curr Protoc Stem Cell Biol. 2007;Chapter 1:Unit 1C 2. doi:10.1002/9780470151808.sc01c02s2.
67. Kidwai FK, Liu H, Toh WS, Fu X, Jokhun DS, Movahednia MM, et al. Differentiation of human embryonic stem cells into clinically amenable keratinocytes in an autogenic environment. J Invest Dermatol. 2013;133(3):618-28. doi:10.1038/jid.2012.384.
68. Wang Q, Mou X, Cao H, Meng Q, Ma Y, Han P, et al. A novel xeno-free and feeder-cell-free system for human pluripotent stem cell culture. Protein Cell. 2012;3(1):51-9. doi:10.1007/s13238-012-2002-0.
69. Amit M, Shariki C, Margulets V, Itskovitz-Eldor J. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod. 2004;70(3):837-45. doi:10.1095/biolreprod.103.021147.
70. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, Frane JL, et al. Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol. 2006;24(2):185-7. doi:10.1038/nbt1177.
71. Rodin S, Domogatskaya A, Strom S, Hansson EM, Chien KR, Inzunza J, et al. Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat Biotechnol. 2010;28(6):611-5. doi:10.1038/nbt.1620.
72. Miyazaki T, Futaki S, Hasegawa K, Kawasaki M, Sanzen N, Hayashi M, et al. Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem Biophys Res Commun. 2008;375(1):27-32. doi:10.1016/j.bbrc.2008.07.111.
73. Miyazaki T, Futaki S, Suemori H, Taniguchi Y, Yamada M, Kawasaki M, et al. Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nat Commun. 2012;3:1236. doi:10.1038/ncomms2231.
74. Nakagawa M, Taniguchi Y, Senda S, Takizawa N, Ichisaka T, Asano K, et al. A novel efficient feeder-free culture system for the derivation of human induced pluripotent stem cells. Sci Rep. 2014;4:3594. doi:10.1038/srep03594.
75. Whittard JD, Craig SE, Mould AP, Koch A, Pertz O, Engel J, et al. E-cadherin is a ligand for integrin alpha2beta1. Matrix Biol. 2002;21(6):525-32.
76. Li L, Bennett SA, 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(1):59-70. doi:10.4161/cam.19583.
77. Li L, Wang S, Jezierski A, Moalim-Nour L, Mohib K, Parks RJ, et al. A unique interplay between Rap1 and E-cadherin in the endocytic pathway regulates self-renewal of human embryonic stem cells. Stem Cells. 2010;28(2):247-57. doi:10.1002/stem.289.
78. Xu Y, Zhu X, Hahm HS, Wei W, Hao E, Hayek A, et al. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci U S A. 2010;107(18):8129-34. doi:10.1073/pnas.1002024107.
79. 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. doi:10.1186/1471-213X-10-60.
80. Rodin S, Antonsson L, Niaudet C, Simonson OE, Salmela E, Hansson EM, et al. Clonal culturing of human embryonic stem cells on laminin-521/E-cadherin matrix in defined and xeno-free environment. Nat Commun. 2014;5:3195. doi:10.1038/ncomms4195.
81. Tsutsui H, Valamehr B, Hindoyan A, Qiao R, Ding X, Guo S, et al. An optimized small molecule inhibitor cocktail supports long-term maintenance of human embryonic stem cells. Nat Commun. 2011;2:167. doi:10.1038/ncomms1165.
82. Braam SR, Zeinstra L, Litjens S, Ward-van Oostwaard D, van den Brink S, van Laake L, et al. Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells. 2008;26(9):2257-65. doi:10.1634/stemcells. 2008-0291.
83. Chen G, Gulbranson DR, Hou Z, Bolin JM, Ruotti V, Probasco MD, et al. Chemically defined conditions for human iPSC derivation and culture. Nat Methods. 2011;8(5):424-9. doi:10.1038/nmeth.1593.
84. Hasegawa K, Yasuda SY, Teo JL, Nguyen C, McMillan M, Hsieh CL, et al. Wnt signaling orchestration with a small molecule DYRK inhibitor provides long-term xeno-free human pluripotent cell expansion. Stem Cells Transl Med. 2012;1(1):18-28. doi:10.5966/sctm. 2011-0033.
85. Wang Y, Chou BK, Dowey S, He C, Gerecht S, Cheng L. Scalable expansion of human induced pluripotent stem cells in the defined xeno-free E8 medium under adherent and suspension culture conditions. Stem Cell Res. 2013;11(3):1103-16. doi:10.1016/j.scr.2013.07.011.
86. Cai L, Ye Z, Zhou BY, Mali P, Zhou C, Cheng L. Promoting human embryonic stem cell renewal or differentiation by modulating Wnt signal and culture conditions. Cell Res. 2007;17(1):62-72. doi:10.1038/sj.cr.7310138.
87. Hasegawa K, Pomeroy JE, Pera MF. Current technology for the derivation of pluripotent stem cell lines from human embryos. Cell Stem Cell. 2010;6(6):521-31. doi:10.1016/j.stem.2010.05.010.
88. Miki T, Yasuda SY, Kahn M. Wnt/beta-catenin signaling in embryonic stem cell self-renewal and somatic cell reprogramming. Stem Cell Rev. 2011;7(4):836-46. doi:10.1007/s12015-011-9275-1.
89. Melkoumian Z, Weber JL, Weber DM, Fadeev AG, Zhou Y, Dolley-Sonneville P, et al. Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat Biotechnol. 2010;28(6):606-10. doi:10.1038/nbt.1629.
90. Jin S, Yao H, Weber JL, Melkoumian ZK, Ye K. A synthetic, xeno-free peptide surface for expansion and directed differentiation of human induced pluripotent stem cells. PLoS One. 2012;7(11):e50880. doi:10.1371/journal.pone.0050880.
91. Kawase E. Efficient. Expansion of Dissociated Human Pluripotent Stem Cells Using a Synthetic Substrate. Methods Mol Biol. 2014; May30 Epub, doi:10.1007/7651_2014_82.
92. Klim JR, Li L, Wrighton PJ, Piekarczyk MS, Kiessling LL. A defined glycosaminoglycan-binding substratum for human pluripotent stem cells. Nat Methods. 2010;7(12):989-94. doi:10.1038/nmeth.1532.
93. Wu S, Johansson J, Damdimopoulou P, Shahsavani M, Falk A, Hovatta O, et al. Spider silk for xeno-free long-term self-renewal and differentiation of human pluripotent stem cells. Biomaterials. 2014;35(30):8496-502. doi:10.1016/j.biomaterials.2014.06.039.
94. 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(34):9135-44. doi:10.1016/j.biomaterials.2010.08.007.
95. 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(29):6912-9. doi:10.1016/j.biomaterials.2011.05.058.
96. Mei Y, Saha K, Bogatyrev SR, Yang J, Hook AL, Kalcioglu ZI, et al. Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat Mater. 2010;9(9):768-78. doi:10.1038/nmat2812.
97. 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(7):1037-43. doi:10.1038/nprot.2011.342.
98. Villa-Diaz LG, Nandivada H, Ding J, Nogueira-de-Souza NC, Krebsbach PH, O'Shea KS, et al. Synthetic polymer coatings for long-term growth of human embryonic stem cells. Nat Biotechnol. 2010;28(6):581-3. doi:10.1038/nbt.1631.
99. Villa-Diaz LG, Ross AM, Lahann J, Krebsbach PH. Concise review: the evolution of human pluripotent stem cell culture: from feeder cells to synthetic coatings. Stem Cells. 2013;31(1):1-7. doi:10.1002/stem.1260.
100. Furue MK, Na J, Jackson JP, Okamoto T, Jones M, Baker D, et al. Heparin promotes the growth of human embryonic stem cells in a defined serum-free medium. Proc Natl Acad Sci U S A. 2008;105(36):13409-14. doi:10.1073/pnas.0806136105.
101. 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(6):688-98. doi:10.1002/bit.20536.
102. Frank S, Zhang M, Scholer HR, Greber B. Small molecule-assisted, line-independent maintenance of human pluripotent stem cells in defined conditions. PLoS One. 2012;7(7):e41958. doi:10.1371/journal.pone.0041958.
103. van der Valk J, Brunner D, De Smet K, Fex Svenningsen A, Honegger P, Knudsen LE, et al. Optimization of chemically defined cell culture media-replacing fetal bovine serum in mammalian in vitro methods. Toxicol In Vitro. 2010;24(4):1053-63. doi:10.1016/j.tiv.2010.03.016.
104. Wang Y, Cheng L, Gerecht S. Efficient and scalable expansion of human pluripotent stem cells under clinically compliant settings: a view in 2013. Ann Biomed Eng. 2014;42(7):1357-72. doi:10.1007/s10439-013-0921-4.
105. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol. 2004;166(6):877-87. doi:10.1083/jcb.200405004.
106. Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J. 2000;79(1):144-52. doi:10.1016/S0006-3495(00)76279-5.
107. Yeung T, Georges P, Flanagan L, Marg B, Ortiz M, Funaki M, et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton. 2005;60(1):24-34.
108. Kraehenbuehl TP, Langer R, Ferreira LS. Three-dimensional biomaterials for the study of human pluripotent stem cells. Nat Methods. 2011;8(9):731-6. doi:10.1038/nmeth.1671.
109. Dellatore SM, Garcia AS, Miller WM. Mimicking stem cell niches to increase stem cell expansion. Curr Opin Biotechnol. 2008;19(5):534-40. doi:10.1016/j.copbio.2008.07.010.
110. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126(4):677-89. doi:10.1016/j.cell.2006.06.044.
111. Lutolf MP, Blau HM. Artificial stem cell niches. Adv Mater. 2009;21(32-33):3255-68. doi:10.1002/adma.200802582.
112. Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature. 2009;462(7272):433-41. doi:10.1038/nature08602.
113. 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 U S A. 2007;104(27):11298-303. doi:10.1073/pnas.0703723104.
114. Li Z, Leung M, Hopper R, Ellenbogen R, Zhang M. Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds. Biomaterials. 2010;31(3):404-12. doi:10.1016/j.biomaterials.2009.09.070.
115. Lu HF, Narayanan K, Lim SX, Gao S, Leong MF, Wan AC. A 3D microfibrous scaffold for long-term human pluripotent stem cell self-renewal under chemically defined conditions. Biomaterials. 2012;33(8):2419-30. doi:10.1016/j.biomaterials.2011.11.077.
116. Siti-Ismail N, Bishop AE, Polak JM, Mantalaris A. The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance. Biomaterials. 2008;29(29):3946-52. doi:10.1016/j.biomaterials.2008.04.027.
117. Lou YR, Kanninen L, Kuisma T, Niklander J, Noon LA, Burks D, et al. The use of nanofibrillar cellulose hydrogel as a flexible three-dimensional model to culture human pluripotent stem cells. Stem Cells Dev. 2014;23(4):380-92. doi:10.1089/scd.2013.0314.
118. Jang M, Lee ST, Kim JW, Yang JH, Yoon JK, Park JC, et al. A feeder-free, defined three-dimensional polyethylene glycol-based extracellular matrix niche for culture of human embryonic stem cells. Biomaterials. 2013;34(14):3571-80. doi:10.1016/j.biomaterials.2013.01.073.
119. Lee ST, Yun JI, Jo YS, Mochizuki M, van der Vlies AJ, Kontos S, et al. Engineering integrin signaling for promoting embryonic stem cell self-renewal in a precisely defined niche. Biomaterials. 2010;31(6):1219-26. doi:10.1016/j.biomaterials.2009.10.054.
120. Badenes SM, Fernandes TG, Rodrigues CA, Diogo MM, Cabral JM. Scalable expansion of human-induced pluripotent stem cells in xeno-free microcarriers. Methods Mol Biol. 2015;1283:23-9. doi:10.1007/7651_2014_106.
121. Chen AK, Chen X, Choo AB, Reuveny S, Oh SK. Expansion of human embryonic stem cells on cellulose microcarriers. Curr Protoc Stem Cell Biol. 2010;Chapter 1:Unit 1C 11. doi:10.1002/9780470151808.sc01c11s14.
122. Chen AK, Chen X, Choo AB, Reuveny S, Oh SK. Critical microcarrier properties affecting the expansion of undifferentiated human embryonic stem cells. Stem Cell Res. 2011;7(2):97-111. doi:10.1016/j.scr.2011.04.007.
123. Marinho PA, Vareschini DT, Gomes IC, Paulsen Bda S, Furtado DR, Castilho Ldos R, et al. Xeno-free production of human embryonic stem cells in stirred microcarrier systems using a novel animal/human-component-free medium. Tissue Eng Part C Methods. 2013;19(2):146-55. doi:10.1089/ten.TEC.2012.0141.
124. Nie Y, Bergendahl V, Hei DJ, Jones JM, Palecek SP. Scalable culture and cryopreservation of human embryonic stem cells on microcarriers. Biotechnol Prog. 2009;25(1):20-31. doi:10.1002/btpr.110.
125. Oh SK, Chen AK, Mok Y, Chen X, Lim UM, Chin A, et al. Long-term microcarrier suspension cultures of human embryonic stem cells. Stem Cell Res. 2009;2(3):219-30. doi:10.1016/j.scr.2009.02.005.
126. Serra M, Correia C, Malpique R, Brito C, Jensen J, Bjorquist P, et al. Microencapsulation technology: a powerful tool for integrating expansion and cryopreservation of human embryonic stem cells. PLoS One. 2011;6(8):e23212. doi:10.1371/journal.pone.0023212.
127. 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(1):71-84. doi:10.2217/rme.11.101.
128. Steiner D, Khaner H, Cohen M, Even-Ram S, Gil Y, Itsykson P, et al. Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat Biotechnol. 2010;28(4):361-4. doi:10.1038/nbt.1616.
129. Baharvand H, Larijani MR, Yousefi M. Protocol for expansion of undifferentiated human embryonic and pluripotent stem cells in suspension. Methods Mol Biol. 2012;873:217-26. doi:10.1007/978-1-61779-794-1_13.
130. Amit M, Laevsky I, Miropolsky Y, Shariki K, Peri M, Itskovitz-Eldor J. Dynamic suspension culture for scalable expansion of undifferentiated human pluripotent stem cells. Nat Protoc. 2011;6(5):572-9. doi:10.1038/nprot.2011.325.
131. Otsuji TG, Bin J, Yoshimura A, Tomura M, Tateyama D, Minami I, et al. A 3D sphere culture system containing functional polymers for large-scale human pluripotent stem cell production. Stem Cell Rep. 2014;2(5):734-45. doi:10.1016/j.stemcr.2014.03.012.
132. Hyun I, Lindvall O, Ahrlund-Richter L, Cattaneo E, Cavazzana-Calvo M, Cossu G, et al. New ISSCR guidelines underscore major principles for responsible translational stem cell research. Cell Stem Cell. 2008;3(6):607-9. doi:10.1016/j.stem.2008.11.009.
133. Crook JM, Peura TT, Kravets L, Bosman AG, Buzzard JJ, Horne R, et al. The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell. 2007;1(5):490-4. doi:10.1016/j.stem.2007.10.004.
134. Unger C, Skottman H, Blomberg P, Dilber MS, Hovatta O. Good manufacturing practice and clinical-grade human embryonic stem cell lines. Hum Mol Genet. 2008;17(R1):R48-53. doi:10.1093/hmg/ddn079.
135. Couture LA. Scalable pluripotent stem cell culture. Nat Biotechnol. 2010;28(6):562-3. doi:10.1038/nbt0610-562.
136. Geron C. World's first clinical trial of human embryonic stem cell therapy cleared. Regen Med. 2009;4(2):161.
137. Strauss S. Geron trial resumes, but standards for stem cell trials remain elusive. Nat Biotechnol. 2010;28(10):989-90. doi:10.1038/nbt1010-989.
138. Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet. 2012;379(9817):713-20. doi:10.1016/S0140-6736(12)60028-2.
139. Ratcliffe E, Glen KE, Naing MW, Williams DJ. Current status and perspectives on stem cell-based therapies undergoing clinical trials for regenerative medicine: case studies. Br Med Bull. 2013;108:73-94. doi:10.1093/bmb/ldt034.
140. Alper J. Geron gets green light for human trial of ES cell-derived product. Nat Biotechnol. 2009;27(3):213-4. doi:10.1038/nbt0309-213a.
141. Trounson A, Thakar RG, Lomax G, Gibbons D. Clinical trials for stem cell therapies. BMC Med. 2011;9:52. doi:10.1186/1741-7015-9-52.
142. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci. 2005;25(19):4694-705. doi:10.1523/JNEUROSCI. 0311-05.2005.
143. Laikind P. ViaCyte, Inc. Announces FDA Acceptance of IND to Commence Clinical Trial of VC-01™ Candidate Cell Replacement Therapy for Type 1 Diabetes. August 19,2014 http://viacyte.com/press-releases/viacyte-inc-announces-fda-acceptance-of-ind-to-commence-clinical-trial-of-vc-01-candidate-cell-replacement-therapy-for-type-1-diabetes/ .
144. Fox C. Embryonic stem cells in trial for diabetes. Bioscience Technology. 2014. http://www.biosciencetechnology.com/articles/2014/10/embryonic-stem-cells-trial-diabetes .
145. Menendez P, Bueno C, Wang L, Bhatia M. Human embryonic stem cells: potential tool for achieving immunotolerance? Stem Cell Rev. 2005;1(2):151-8. doi:10.1385/SCR:1:2:151.
146. Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA. Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet. 2005;366(9502):2019-25. doi:10.1016/S0140-6736(05)67813-0.
147. Hentze H, Graichen R, Colman A. Cell therapy and the safety of embryonic stem cell-derived grafts. Trends Biotechnol. 2007;25(1):24-32. doi:10.1016/j.tibtech.2006.10.010.
148. Desai N, Xu J, Tsulaia T, Szeptycki-Lawson J, AbdelHafez F, Goldfarb J, et al. Vitrification of mouse embryo-derived ICM cells: a tool for preserving embryonic stem cell potential? J Assist Reprod Genet. 2011;28(2):93-9. doi:10.1007/s10815-010-9500-x.