Application of human mesenchymal and pluripotent stem cell microcarrier cultures in cellular therapy: Achievements and future direction

Biotechnology Advances

Volumn 31, Issue 7, 2013, Pages 1032-1046

  Chen, Allen Kuan Liang ^a   Reuveny, Shaul ^a   Oh, Steve Kah Weng ^a  

^a AGENCY FOR SCIENCE   (Singapore)

Author keywords

Aggregates; Cell harvesting; Cell therapy; Clinical trials; Differentiation; Expansion; Extracellular matrix; Human mesenchymal stem cells; Human pluripotent stem cells; Microcarrier

Indexed keywords

CELL THERAPY; CLINICAL TRIAL; EXTRACELLULAR MATRICES; HUMAN MESENCHYMAL STEM CELLS; MICROCARRIERS; PLURIPOTENT STEM CELLS;

AGGREGATES; DIFFERENTIATION (CALCULUS); EXPANSION; EXPERIMENTS; FLOWCHARTING; SHEAR FLOW; STEM CELLS; TISSUE CULTURE;

CYTOLOGY;

BIOENGINEERING; BONE; CELL ORGANELLE; PIGMENT; STEM; TRANSPLANTATION; VACCINE;

AGGREGATES; BIOLOGICAL THERAPY; BIOTECHNOLOGY; CELL HARVESTING; CELL THERAPY; CLINICAL TRIAL (TOPIC); CULTURE TECHNIQUE; DIFFERENTIATION; EQUIPMENT; EXPANSION; EXTRACELLULAR MATRIX; HUMAN; HUMAN MESENCHYMAL STEM CELLS; HUMAN PLURIPOTENT STEM CELLS; MESENCHYMAL STROMA CELL; METHODOLOGY; MICROCARRIER; PLURIPOTENT STEM CELL; REVIEW;

AGGREGATES; CELL HARVESTING; CELL THERAPY; CLINICAL TRIALS; DIFFERENTIATION; EXPANSION; EXTRACELLULAR MATRIX; HUMAN MESENCHYMAL STEM CELLS; HUMAN PLURIPOTENT STEM CELLS; MICROCARRIER;

BIOTECHNOLOGY; CELL CULTURE TECHNIQUES; CELL- AND TISSUE-BASED THERAPY; HUMANS; MESENCHYMAL STROMAL CELLS; PLURIPOTENT STEM CELLS;

EID: 84886786622     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2013.03.006     Document Type: Review

References (151)

1. Allison M. Genzyme backs Osiris, despite Prochymal flop. Nat Biotech. 2009, 27:966-967.
2. Amit M., Itskovitz-Eldor J. Maintenance of human embryonic stem cells in animal serum- and feeder layer-free culture conditions. Methods Mol Biol 2006, 331:105-113.
3. 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, 6:572-579.
4. Anderson D., Self T., Mellor I.R., Goh G., Hill S.J., Denning C. Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol Ther 2007, 15:2027-2036.
5. Bardy J., Chen A., Lim Y.M., Wu S., Wei S., Weiping H., et al. Microcarrier suspension cultures produce high yields of neural progenitor cells from human pluripotent stem cells. Tissue Eng Part C Methods 2013, 19:166-180.
6. Bernardo M.E., Avanzini M.A., Perotti C., Cometa A.M., Moretta A., Lenta E., et al. Optimization of in vitro expansion of human multipotent mesenchymal stromal cells for cell-therapy approaches: further insights in the search for a fetal calf serum substitute. J Cell Physiol 2007, 211:121-130.
7. Billig D., Clark J.M., Ewell A.J., Carter C.M., Gebb C. The separation of harvested cells from microcarriers: a comparison of methods. Dev Biol Stand 1983, 55:67-75.
8. Blüml G. Microcarrier cell culture technology. Animal cell biotechnology 2007, 149-178. Humana Press. R. Pörtner (Ed.).
9. Boo L., Selvaratnam L., Tai C.C., Ahmad T.S., Kamarul T. Expansion and preservation of multipotentiality of rabbit bone-marrow derived mesenchymal stem cells in dextran-based microcarrier spin culture. J Mater Sci Mater Med 2011, 22:1343-1356.
10. Braam S.R., Zeinstra L., Litjens S., Oostwaard D.W., 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, 26:2257-2265.
11. Braam S.R., Nauw R., Ward-van Oostwaard D., Mummery C., Passier R. Inhibition of ROCK improves survival of human embryonic stem cell-derived cardiomyocytes after dissociation. Ann N Y Acad Sci 2010, 1188:52-57.
12. Brandenberger R., Burger S., Campbell A., Fong T., Lapinskas E., Rowley J.A. Cell therapy bioprocessing. BioProcess International. 2011, 9:30-37.
13. Bretzner F., Gilbert F., Baylis F., Brownstone R.M. Target populations for first-in-human embryonic stem cell research in spinal cord injury. Cell Stem Cell 2011, 8:468-475.
14. Butler M., Imamura T., Thomas J., Thilly W.G. High yields from microcarrier cultures by medium perfusion. J Cell Sci 1983, 61:351-363.
15. Cao F., Wagner R.A., Wilson K.D., Xie X., Fu J.-D., Drukker M., et al. Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes. PLoS One 2008, 3:e3474.
16. Cetinkaya G., Kahraman A.S., Gumusderelioglu M., Arat S., Onur M.A. Derivation, characterization and expansion of fetal chondrocytes on different microcarriers. Cytotechnology 2011, 63:633-643.
17. Chase L.G., Lakshmipathy U., Solchaga L.A., Rao M.S., Vemuri M.C. A novel serum-free medium for the expansion of human mesenchymal stem cells. Stem Cell Res Ther 2010, 1:8.
18. Chen A.K., Chen X., Choo A.B., Reuveny S., Oh S.K. Expansion of human embryonic stem cells on cellulose microcarriers 2010, John Wiley & Sons, Inc., [Chapter 1:Unit 1C 11].
19. Chen G., Hou Z., Gulbranson D.R., Thomson J.A. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 2010, 7:240-248.
20. Chen X., Chen A., Woo T.L., Choo A.B.H., Reuveny S., Oh S.K.W. Investigations into the metabolism of two-dimensional colony and suspended microcarrier cultures of human embryonic stem cells in serum-free media. Stem Cells Dev 2010, 19:1781-1792.
21. Chen A.K.-L., Chen X., Choo A.B.H., Reuveny S., Oh S.K.W. Critical microcarrier properties affecting the expansion of undifferentiated human embryonic stem cells. Stem Cell Res 2011, 7:97-111.
22. Chen M., Wang X., Ye Z., Zhang Y., Tan W.-S. A modular approach to the engineering of a centimeter-sized bone tissue construct with human amniotic mesenchymal stem cells-laden microcarrier. Biomaterials 2011, 32:7532-7542.
23. Chen V.C., Couture S.M., Ye J., Lin Z., Hua G., Huang H.I., et al. Scalable GMP compliant suspension culture system for human ES cells. Stem Cell Res 2012, 8:388-402.
24. Chen A.K.-L., Chen X., Lim Y.M., Reuveny S., Oh S.K. Inhibition of ROCK-Myosin II Signaling pathway enables culturing of human pluripotent stem cells on microcarriers without extracellular matrix coating. Tissue Eng Part C 2013, [Submitted for publication].
25. Choo A., Padmanabhan J., Chin A., Fong W.J., Oh S.K.W. Immortalized feeders for the scale-up of human embryonic stem cells in feeder and feeder-free conditions. J Biotechnol 2006, 122:130-141.
26. Choo A.B., Tan H.L., Ang S.N., Fong W.J., Chin A., Lo J., et al. Selection against undifferentiated human embryonic stem cells by a cytotoxic antibody recognizing podocalyxin-like protein-1. Stem Cells 2008, 26:1454-1463.
27. Chung H.J., Kim I.K., Kim T.G., Park T.G. Highly open porous biodegradable microcarriers: in vitro cultivation of chondrocytes for injectable delivery. Tissue Eng Part A 2008, 14:607-615.
28. Colman A., Dreesen O. Pluripotent stem cells and disease modeling. Cell Stem Cell 2009, 5:244-247.
29. Consortium T.I., Akopian V., Andrews P., Beil S., Benvenisty N., Brehm J., et al. Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. In Vitro Cell Dev Biol Anim 2010, 46:247-258.
30. Covello K.L., Kehler J., Yu H., Gordan J.D., Arsham A.M., Hu C.-J., et al. HIF-2α regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 2006, 20:557-570.
31. da Cruz L., Chen F.K., Ahmado A., Greenwood J., Coffey P. RPE transplantation and its role in retinal disease. Prog Retin Eye Res 2007, 26:598-635.
32. D'Amour K.A., Agulnick A.D., Eliazer S., Kelly O.G., Kroon E., Baetge E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotech. 2005, 23:1534-1541.
33. Davie N.L., Brindley D.A., Culme-Seymour E.J., Mason C. Streamlining cell therapy manufacture. Bioprocess Int 2012, 10:24-27.
34. Doetschman T.C., Eistetter H., Katz M., Schmidt W., Kemler R. 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.
35. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
36. Dubois N.C., Craft A.M., Sharma P., Elliott D.A., Stanley E.G., Elefanty A.G., et al. SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotech. 2011, 29:1011-1018.
37. Duijvestein M., Vos A.C.W., Roelofs H., Wildenberg M.E., Wendrich B.B., Verspaget H.W., et al. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 2010, 59:1662-1669.
38. Eibes G., dos Santos F., Andrade P.Z., Boura J.S., Abecasis M.M.A., da Silva C.L., et al. Maximizing the ex vivo expansion of human mesenchymal stem cells using a microcarrier-based stirred culture system. J Biotechnol 2010, 146:194-197.
39. Elseberg C.L., Leber J., Salzig D., Wallrapp C., Kassem M., Kraume M., et al. Microcarrier-based expansion process for hMSCs with high vitality and undifferentiated characteristics. Int J Artif Organs 2012, 35:93-107.
40. Fernandes A.M., Marinho P.A.N., Sartore R.C., Paulsen B.S., Mariante R.M., Castilho L.R., et al. Successful scale-up of human embryonic stem cell production in a stirred microcarrier culture system. Braz J Med Biol Res 2009, 42:515-522.
41. Ferrari C., Balandras F., Guedon E., Olmos E., Chevalot I., Marc A. Limiting cell aggregation during mesenchymal stem cell expansion on microcarriers. Biotechnol Prog 2012, 28:780-787.
42. Forristal C.E., Wright K.L., Hanley N.A., Oreffo R.O.C., Houghton F.D. Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 2010, 139:85-97.
43. Frauenschuh S., Reichmann E., Ibold Y., Goetz P.M., Sittinger M., Ringe J. A microcarrier-based cultivation system for expansion of primary mesenchymal stem cells. Biotechnol Prog 2007, 23:187-193.
44. Gepstein L. Derivation and potential applications of human embryonic stem cells. Circ Res 2002, 91:866-876.
45. Goh T.K.-P., Zhang Z.-Y., Chen A.K.-L., Reuveny S., Choolani M., Chan J.K.Y., et al. Microcarrier culture for efficient expansion and osteogenic differentiation of human fetal mesenchymal stem cells. BioResearch Open Access 2013, 2(2):84-97. 10.1089/biores.2013.0001.
46. Govindasamy V., Ronald V.S., Abdullah A.N., Ganesan Nathan K.R., Aziz Z.A., Abdullah M., et al. Human platelet lysate permits scale-up of dental pulp stromal cells for clinical applications. Cytotherapy 2011, 13:1221-1233.
47. Hare J.M., Traverse J.H., Henry T.D., Dib N., Strumpf R.K., Schulman S.P., et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009, 54:2277-2286.
48. Hendrick V., Muniz E., Geuskens G., Wérenne J. Adhesion, growth and detachment of cells on modified polystyrene surface. Cytotechnology 2001, 36:49-53.
49. Heng B.C., Li J., Chen A.K.-L., Reuveny S., Cool S.M., Birch W.R., et al. 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.
50. Herrmann R., Sturm M., Shaw K., Purtill D., Cooney J., Wright M., et al. Mesenchymal stromal cell therapy for steroid-refractory acute and chronic graft versus host disease: a phase 1 study. Int J Hematol 2012, 95:182-188.
51. Hewitt C., Lee K., Nienow A., Thomas R., Smith M., Thomas C. Expansion of human mesenchymal stem cells on microcarriers. Biotechnol Lett 2011, 33:2325-2335.
52. Himes V.B., Hu W.-S. Attachment and growth of mammalian cells on microcarriers with different ion exchange capacities. Biotechnol Bioeng 1987, 29:1155-1163.
53. Horwitz E.M., Prockop D.J., Fitzpatrick L.A., Koo W.W.K., Gordon P.L., Neel M., et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999, 5:309-313.
54. Horwitz E.M., Gordon P.L., Koo W.K.K., Marx J.C., Neel M.D., McNall R.Y., et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 2002, 99:8932-8937.
55. Huber I., Itzhaki I., Caspi O., Arbel G., Tzukerman M., Gepstein A., et al. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J 2007, 21:2551-2563.
56. Itskovitz-Eldor J., Schuldiner M., Karsenti D., Eden A., Yanuka O., Amit M., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 2000, 6:88-95.
57. Jang J., Yoo J.E., Lee J.A., Lee D.R., Kim J.Y., Huh Y.J., et al. Disease-specific induced pluripotent stem cells: a platform for human disease modeling and drug discovery. Exp Mol Med 2012, 44:202-213.
58. Kebriaei P., Isola L., Bahceci E., Holland K., Rowley S., McGuirk J., et al. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 2009, 15:804-811.
59. Kehat I., Gepstein L. Derivation and properties of human embryonic stem cell-derived cardiomyocytes. Gene Ther Regul 2001, 1:387-398.
60. Kehoe D.E., Jing D., Lock L.T., Tzanakakis E.S. Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng Part A 2010, 16:405-421.
61. Keirstead H.S., 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, 25:4694-4705.
62. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 2005, 19:1129-1155.
63. Kim M.R., Jeong J.H., Park T.G. Swelling induced detachment of chondrocytes using RGD-modified poly(N-isopropylacrylamide) hydrogel beads. Biotechnol Prog 2002, 18:495-500.
64. Koç O.N., Day J., Nieder M., Gerson S.L., Lazarus H.M., Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of Metachromatic Leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant 2002, 30:215-222.
65. Kolhar P., Kotamraju V.R., Hikita S.T., Clegg D.O., Ruoslahti E. Synthetic surfaces for human embryonic stem cell culture. J Biotechnol 2010, 146:143-146.
66. Krawetz R., Taiani J.T., Liu S., Meng G., Li X., Kallos M., et al. Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. Tissue Eng Part C Methods 2010, 16:573-582.
67. Kroon E., Martinson L.A., Kadoya K., Bang A.G., Kelly O.G., Eliazer S., et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008, 26:443-452.
68. Kuzmina L.A., Petinati N.A., Parovichnikova E.N., Lubimova L.S., Gribanova E.O., Gaponova T.V., et al. Multipotent mesenchymal stromal cells for the prophylaxis of acute graft-versus-host disease-a phase II study. Stem Cells Int 2012, 2012:8.
69. Laflamme M.A., Chen K.Y., Naumova A.V., Muskheli V., Fugate J.A., Dupras S.K., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 2007, 25:1015-1024.
70. Lakshmipathy U., Verfaillie C. Stem cell plasticity. Blood Rev 2005, 19:29-38.
71. Larijani M.R., Seifinejad A., Pournasr B., Hajihoseini V., Hassani S.N., Totonchi M., et al. Long-term maintenance of undifferentiated human embryonic and induced pluripotent stem cells in suspension. Stem Cells Dev 2011, 20:1911-1923.
72. Le Blanc K., Götherström C., Ringdén O., Hassan M., McMahon R., Horwitz E., et al. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005, 79:1607-1614.
73. Lecina M., Ting S., Choo A., Reuveny S., Oh S. Scalable platform for hESC differentiation to cardiomyocytes in suspended microcarrier cultures. Tissue Eng Part C Methods 2010, 16:1609-1619.
74. Leung H.W., Chen A., Choo A., Reuveny S., Oh S. Agitation can induce differentiation of human pluripotent stem cells in microcarrier cultures. Tissue Eng Part C Methods 2010, 17:165-172.
75. Levenberg S., Golub J.S., Amit M., Itskovitz-Eldor J., Langer R. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2002, 99:4391-4396.
76. Lian Q., Lye E., Suan Yeo K., Khia Way Tan E., Salto-Tellez M., Liu T.M., et al. Derivation of clinically compliant MSCs from CD105+, CD24- differentiated human ESCs. Stem Cells 2007, 25:425-436.
77. Lindskog U., Lundgren B., Billig D., Lindner E. Alternatives for harvesting cells grown on microcarriers: effects on subsequent attachment and growth. Dev Biol Stand 1987, 66:307-313.
78. Lock L.T., Tzanakakis E.S. Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture. Tissue Eng Part A 2009, 15:2051-2063.
79. Lu B., Malcuit C., Wang S., Girman S., Francis P., Lemieux L., et al. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 2009, 27:2126-2135.
80. Ludwig T.E., Levenstein M.E., Jones J.M., Berggren W.T., Mitchen E.R., Frane J.L., et al. Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 2006, 24:185-187.
81. Marinho P.A., Vareschini D.T., Gomes I.C., Paulsen Bda S., Furtado D.R., 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, 19:146-155.
82. Markvicheva E., Grandfils C.H. Microcarriers for animal cell culture. Fundamentals of cell immobilisation biotechnology, series focus on biotechnology 2004, 441-461. Kluwer Academic Publishers. R. Willaert, V. Nedovich (Eds.).
83. Martin Y., Eldardiri M., Lawrence-Watt D.J., Sharpe J.R. Microcarriers and their potential in tissue regeneration. Tissue Eng Part B 2011, 17:71-80.
84. Melkoumian Z., Weber J.L., Weber D.M., Fadeev A.G., 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, 28:606-610.
85. 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, 375:27-32.
86. Newman R.E., Yoo D., LeRoux M.A., Danilkovitch-Miagkova A. Treatment of inflammatory diseases with mesenchymal stem cells. Inflamm Allergy Drug Targets 2009, 8:110-123.
87. Ng Y.-C., Berry J.M., Butler M. Optimization of physical parameters for cell attachment and growth on macroporous microcarriers. Biotechnol Bioeng 1996, 50:627-635.
88. Nie Y., Bergendahl V., Hei D.J., Jones J.M., Palecek S.P. Scalable culture and cryopreservation of human embryonic stem cells on microcarriers. Biotechnol Prog 2009, 25:20-31.
89. O'Brien C., Laslett A.L. Suspended in culture-human pluripotent cells for scalable technologies. Stem Cell Res 2012, 9:167-170.
90. Odorico J.S., Kaufman D.S., Thomson J.A. Multilineage differentiation from human embryonic stem cell lines. Stem Cells 2001, 19:193-204.
91. Oh S.K.W., Choo A.B.H. 1.25-stem cells. Comprehensive biotechnology 2011, 341-365. Academic Press, Burlington. 2nd ed. M.-Y. Murray (Ed.).
92. Oh S.K.W., Chen A.K., Mok Y., Chen X., Lim U.-M., Chin A., et al. Long-term microcarrier suspension cultures of human embryonic stem cells. Stem Cell Res 2009, 2:219-230.
93. Olivier E.N., Rybicki A.C., Bouhassira E.E. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 2006, 24:1914-1922.
94. Olmer R., Haase A., Merkert S., Cui W., Paleček J., Ran C., et al. Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res 2010, 5:51-64.
95. Olson M.F. Applications for ROCK kinase inhibition. Curr Opin Cell Biol 2008, 20:242-248.
96. Pera M.F., Trounson A.O. Human embryonic stem cells: prospects for development. Development 2004, 131:5515-5525.
97. Phillips B.W., Horne R., Lay T.S., Rust W.L., Teck T.T., Crook J.M. Attachment and growth of human embryonic stem cells on microcarriers. J Biotechnol 2008, 138:24-32.
98. Pruszak J., Sonntag K.C., Aung M.H., Sanchez-Pernaute R., Isacson O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 2007, 25:2257-2268.
99. Reuveny S., Silberstein L., Shahar A., Freeman E., Mizrahi A. Cell and virus propagation on cylindrical cellulose based microcarriers. Dev Biol Stand 1981, 50:115-123.
100. Reuveny S., Silberstein L., Shahar A. DE-52 and DE-53 cellulose microcarriers. I. Growth of primary and established anchorage-dependent cells. In Vitro 1982, 18:92-98.
101. Reuveny S., Mizrahi A., Kotler M., Freeman A. Factors affecting cell attachment, spreading, and growth on derivatized microcarriers. I. Establishment of working system and effect of the type of the amino-charged groups. Biotechnol Bioeng 1983, 25:469-480.
102. Robinton D.A., Daley G.Q. The promise of induced pluripotent stem cells in research and therapy. Nature 2012, 481:295-305.
103. Rodin S., Domogatskaya A., Ström S., Hansson E.M., Chien K.R., Inzunza J., et al. Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat Biotechnol 2010, 28:611-615.
104. Rowley J., Abraham E., Campbell A., Brandwein H., Oh S. Meeting lot-size challenges of manufacturing adherent cells for therapy. BioProcess Int 2012, 10:16-22.
105. Santos F., Andrade P.Z., Abecasis M.M., Gimble J.M., Chase L.G., Campbell A.M., et al. Toward a clinical-grade expansion of mesenchymal stem cells from human sources: a microcarrier-based culture system under xeno-free conditions. Tissue Eng Part C Methods 2011, 17:1201-1210.
106. Sart S., Schneider Y.-J., Agathos S.N. Ear mesenchymal stem cell: an efficient adult multipotent cell population fit for rapid and scalable expansion. J Biotechnol 2009, 139:291-299.
107. Sart S., Schneider Y.-J., Agathos S.N. Influence of culture parameters on ear mesenchymal stem cells expanded on microcarriers. J Biotechnol 2010, 150:149-160.
108. Sart S., Errachid A., Schneider Y.-J., Agathos S.N. Modulation of mesenchymal stem cell actin organization on conventional microcarriers for proliferation and differentiation in stirred bioreactors. J Tissue Eng Regen Med 2012, 10.1002/term.545.
109. Schmidt J.J., Jeong J., Kong H. The interplay between cell adhesion cues and curvature of cell adherent alginate microgels in multipotent stem cell culture. Tissue Eng Part A 2011, 17:2687-2694.
110. Schop D., van Dijkhuizen-Radersma R., Borgart E., Janssen F.W., Rozemuller H., Prins H.J., et al. Expansion of human mesenchymal stromal cells on microcarriers: growth and metabolism. J Tissue Eng Regen Med 2010, 4:131-140.
111. Schriebl K., Lim S., Choo A., Tscheliessnig A., Jungbauer A. Stem cell separation: a bottleneck in stem cell therapy. Biotechnol J 2010, 5:50-61.
112. Schriebl K., Satianegara G., Hwang A., Tan H.L., Fong W.J., Yang H.H., et al. Selective removal of undifferentiated human embryonic stem cells using magnetic activated cell sorting followed by a cytotoxic antibody. Tissue Eng Part A 2012, 18:899-909.
113. Schwartz S.D., Hubschman J.-P., Heilwell G., Franco-Cardenas V., Pan C.K., Ostrick R.M., et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012, 379:713-720.
114. Selvaggi T.A., Walker R.E., Fleisher T.A. Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 1997, 89:776-779.
115. Serra M., Brito C., Costa E., Sousa M., Alves P. Integrating human stem cell expansion and neuronal differentiation in bioreactors. BMC Biotechnol 2009, 9:82.
116. Serra M., Brito C., Sousa M.F.Q., Jensen J., Tostões R., Clemente J., et al. Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. J Biotechnol 2010, 148:208-215.
117. Shahdadfar A., Fronsdal K., Haug T., Reinholt F.P., Brinchmann J.E. In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells 2005, 23:1357-1366.
118. Singh H., Mok P., Balakrishnan T., Rahmat S.N.B., Zweigerdt R. Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. Stem Cell Res 2010, 4:165-179.
119. Strauer B.E., Brehm M., Zeus T., Köstering M., Hernandez A., Sorg R.V., et al. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 2002, 106:1913-1918.
120. Sun L.Y., Hsieh D.K., Syu W.S., Li Y.S., Chiu H.T., Chiou T.W. Cell proliferation of human bone marrow mesenchymal stem cells on biodegradable microcarriers enhances in vitro differentiation potential. Cell Prolif 2010, 43:445-456.
121. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
122. Tamura A., Kobayashi J., Yamato M., Okano T. Temperature-responsive poly(N-isopropylacrylamide)-grafted microcarriers for large-scale non-invasive harvest of anchorage-dependent cells. Biomaterials 2012, 33:3803-3812.
123. Thiel A., Scheffold A., Radbruch A. Immunomagnetic cell sorting-pushing the limits. Immunotechnology 1998, 4:89-96.
124. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
125. Thomson H.A., Treharne A.J., Backholer L.S., Cuda F., Grossel M.C., Lotery A.J. Biodegradable poly(α-hydroxy ester) blended microspheres as suitable carriers for retinal pigment epithelium cell transplantation. J Biomed Mater Res A 2010, 95A:1233-1243.
126. Timmins N.E., Kiel M., Günther M., Heazlewood C., Doran M.R., Brooke G., et al. Closed system isolation and scalable expansion of human placental mesenchymal stem cells. Biotechnol Bioeng 2012, 109:1817-1826.
127. Ting S., Lecina M., Reuveny S., Oh S. Differentiation of human embryonic stem cells to cardiomyocytes on microcarrier cultures 2012, John Wiley & Sons, Inc., [Chapter 1:Unit 1D 7].
128. Tree J.A., Richardson C., Fooks A.R., Clegg J.C., Looby D. Comparison of large-scale mammalian cell culture systems with egg culture for the production of influenza virus A vaccine strains. Vaccine 2001, 19:3444-3450.
129. Trounson A., Thakar R., Lomax G., Gibbons D. Clinical trials for stem cell therapies. BMC Med 2011, 9:52.
130. Tseng P.-C., Young T.-H., Wang T.-M., Peng H.-W., Hou S.-M., Yen M.-L. Spontaneous osteogenesis of MSCs cultured on 3D microcarriers through alteration of cytoskeletal tension. Biomaterials 2012, 33:556-564.
131. Turner A.E., Flynn L.E. Design and characterization of tissue-specific extracellular matrix-derived microcarriers. Tissue Eng Part C Methods 2012, 18:186-197.
132. Turner A.E.B., Yu C., Bianco J., Watkins J.F., Flynn L.E. The performance of decellularized adipose tissue microcarriers as an inductive substrate for human adipose-derived stem cells. Biomaterials 2012, 33:4490-4499.
133. Tuschong L., Soenen S.L., Blaese R.M., Candotti F., Muul L.M. Immune response to fetal calf serum by two adenosine deaminase-deficient patients after T cell gene therapy. Hum Gene Ther 2002, 13:1605-1610.
134. Uosaki H., Fukushima H., Takeuchi A., Matsuoka S., Nakatsuji N., Yamanaka S., et al. Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 2011, 6:e23657.
135. van Wezel A.L. Growth of cell-strains and primary cells on microcarriers in homogeneous culture. Nature 1967, 216:64-65.
136. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002, 10:199-206.
137. Wang Y., Ouyang F. Bead-to-bead transfer of Vero cells in microcarrier culture. Cytotechnology 1999, 31:221-224.
138. Watanabe K., Ueno M., Kamiya D., Nishiyama A., Matsumura M., Wataya T., et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 2007, 25:681-686.
139. Wohn D.Y. Korea okays stem cell therapies despite limited peer-reviewed data. Nat Med 2012, 18:329.
140. Wolfe M., Pochampally R., Swaney W., Reger R.L. Isolation and culture of bone marrow-derived human multipotent stromal cells (hMSCs). Methods Mol Biol 2008, 449:3-25.
141. Xu C. Differentiation and enrichment of cardiomyocytes from human pluripotent stem cells. J Mol Cell Cardiol 2012, 52:1203-1212.
142. Xu C., Police S., Rao N., Carpenter M.K. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 2002, 91:501-508.
143. Yang Y., Rossi F.M.V., Putnins E.E. Ex vivo expansion of rat bone marrow mesenchymal stromal cells on microcarrier beads in spin culture. Biomaterials 2007, 28:3110-3120.
144. Yang H.S., Jeon O., Bhang S.H., Lee S.-H., Kim B.-S. Suspension culture of mammalian cells using thermosensitive microcarrier that allows cell detachment without proteolytic enzyme treatment. Cell Transplant 2010, 19:1123-1132.
145. Yap L.Y.W., Li J., Ong I.Y.P.L.T., JaZ-E Ow, Goh J.C.H., Nurcombe V., et al. Defining a threshold surface density of vitronectin for the stable expansion of human embryonic stem cells. Tissue Eng Part C Methods 2010, 17:193-207.
146. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
147. Yuan Y., Kallos M.S., Hunter C., Sen A. Improved expansion of human bone marrow-derived mesenchymal stem cells in microcarrier-based suspension culture. J Tissue Eng Regen Med. 2012, [in press]. 10.1002/term.1515.
148. Zeevi-Levin N., Itskovitz-Eldor J., Binah O. Cardiomyocytes derived from human pluripotent stem cells for drug screening. Pharmacol Ther 2012, 134:180-188.
149. Zhang S.-C., Wernig M., Duncan I.D., Brustle O., Thomson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001, 19:1129-1133.
150. Zhang B., Yang S., Sun Z., Zhang Y., Xia T., Xu W., et al. Human mesenchymal stem cells induced by growth differentiation factor 5: an improved self-assembly tissue engineering method for cartilage repair. Tissue Eng Part C Methods 2011, 17:1189-1199.
151. Zhou Y., Yan Z., Zhang H., Lu W., Liu S., Huang X., et al. Expansion and delivery of adipose-derived mesenchymal stem cells on three microcarriers for soft tissue regeneration. Tissue Eng Part A 2011, 17:2981-2997.