Advances in cell culture: Anchorage dependence

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1661, 2015, Pages

  Merten, Otto Wilhelm ^a  

^a GÉNÉTHON   (France)

Author keywords

Adherent cells; Cell therapy; Engineering issues; Large scale expansion; Stem cells; Virus production

Indexed keywords

ADHESION; BIOTECHNOLOGY; GERM CELL; MEDICINE; VIRUS;

VIRUS VACCINE;

ANIMAL; CELL ADHESION; CELL CULTURE; IMMOBILIZED CELL; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

ANIMALS; CELL ADHESION; CELLS, CULTURED; CELLS, IMMOBILIZED; VIRAL VACCINES; VIRUS REPLICATION;

EID: 84919754098     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0040     Document Type: Review

References (165)

1. Griffiths JB, Riley PA. 1985 Cell biology: basic concepts. In Animal cell biotechnology, vol. 1 (eds RE Spier, JB Griffiths), pp. 17-48. London, UK: Academic Press.
2. Frisch SM, Screaton RA. 2001 Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555-562. doi: 10.1016/S0955-0674(00)00251-9
3. Castillo J, Egloff M, Collignon F, Goffinet J, Drugmand J. 2013 Transfer of hepatic progenitor stem cell culture process from multiple tray stacks to the Xpansion multiplate bioreactor. Cytotherapy 15, Suppl. S20. doi: 10.1016/j.jcyt.2013.01.074
4. Merten O-W, Manuguerra JC, Hannoun C, van der Werf S. 1999 Production of influenza virus in serum-free mammalian cell cultures. Dev. Biol. Stand. 98, 23-37; discussion 73-74.
5. Barrett PN, Mundt W, Kistner O, Howard MK. 2009 Vero cell platform in vaccine production: moving towards cell culture-based viral vaccine. Expert Rev. Vaccines 8, 607-618. doi: 10.1586/erv.09.19
6. Eaker S et al. 2013 Concise review: guidance in developing commercializable autologous/patient-specific cell therapy manufacturing. Stem Cells Transl. Med. 2, 871-883. doi: 10.5966/sctm.2013-0050
7. Malda J, Frondoza CG. 2006 Microcarriers in the engineering of cartilage and bone. Trends Biotechnol. 24, 299-304. doi: 10.1016/j.tibtech.2006.04.009
8. Panina GF. 1985 Monolayer growth systems: multiple processes. In Animal cell biotechnology, vol. 1 eds RE Spier, JB Griffiths), pp. 211-242. London, UK: Academic Press.
9. Kunitake R, Suzuki A, Ichihashi H, Matsuda S, Hirai O, Morimoto K. 1997 Fully-automated roller bottle handling system for large scale culture of mammalian cells. J. Biotechnol. 52, 289-294. doi: 10.1016/S0168-1656(96)01654-9
10. Pakos V, Johansson A. 1985 Large scale production of human fibroblast interferon in multitray battery systems. Dev. Biol. Stand. 60, 317-320.
11. van Wezel AL. 1967 Growth of cell-strains and primary cells on micro-carriers in homogeneous culture. Nature 216, 64-65. doi: 10.1038/216064a0
12. Levine DW, Wong JS, Wang DI, Thilly WG. 1977 Microcarrier cell culture: new methods for research-scale application. Somatic Cell Genet. 3, 149-155. doi: 10.1007/BF01551811
13. Levine DW, Wong JS, Wang DIC, Thilly WG. 1979 Optimization of growth surface parameters in microcarrier cell cultures. Biotechnol. Bioeng. 21, 821-846. doi: 10.1002/bit.260210507
14. Maroudas NG. 1972 Anchorage dependence correlation between amount of growth and diameter of bead, for single cells grown on individual glass beads. Exp. Cell Res. 74, 337-342. doi: 10.1016/0014-4827(72)90385-0
15. Chen AK-L, Reuveny S, Oh SKW. 2013 Application of human mesenchymal and pluripotent stem cell microcarrier cultures in cellular therapy: achievements and future direction. Biotechnol. Adv. 31, 1032-1046. doi: 10.1016/j.biotechadv.2013.03.006
16. Meignier B, Mougeot H, Favre H. 1980 Foot and mouth disease virus production on microcarrier-grown cells. Dev. Biol. Stand. 46, 249-256.
17. Montagnon BJ, Fanget B, Vincent-Falquet JC. 1984 Industrial scale production of inactivated poliovirus vaccine prepared by culture of Vero cells on microcarrier. Rev. Infect. Dis. 6, S341-S344. doi: 10.1093/clinids/6.Supplement_2.S341
18. Montagnon B, Vincent-Falquet JC, Fanget B. 1984 Thousand litre scale microcarrier culture of Vero cells for killed polio virus vaccine. Promising Results Dev. Biol. Stand. 55, 37-42.
19. Montagnon BJ, Vincent-Falquet JC, Saluzzo JF. 1999 Experience with vero cells at Pasteur Mérieux Connaught. Dev. Biol. Stand. 98, 137-140; discussion 167.
20. Elsdale T, Bard J. 1972 Cellular interactions in mass cultures of human diploid fibroblasts. Nature 236, 152-155. doi: 10.1038/236152a0
21. Kistner O, Barrett PN, Mundt W, Reiter M, Schober-Bendixen S, Eder G, Dorner F. 1999 Development of a Vero cell-derived influenza whole virus vaccine. Dev. Biol. Stand. 98, 101-110; discussion 111.
22. Moran E. 1999 A microcarrier-based cell culture process for the production of a bovine respiratory syncytial virus vaccine. Cytotechnology 29, 135-148. doi: 10.1023/A:1008022828736
23. Ng YC, Berry JM, Butler M. 1996 Optimization of physical parameters for cell attachment and growth on macroporous microcarriers. Biotechnol. Bioeng. 50, 627-635. doi: 10.1002/(SICI)1097-0290(19960620)50:6,627::AID-BIT3.3.0.CO;2-M
24. Hu WS, Meier J, Wang DI. 1985 A mechanistic analysis of the inoculum requirement for the cultivation of mammalian cells on microcarriers. Biotechnol. Bioeng. 27, 585-595. doi: 10.1002/bit.260270507
25. Butler M, Thilly WG. 1982 MDCK microcarrier cultured: seeding density effects and amino acid utilization. In Vitro 18, 213-219. doi: 10.1007/BF02618573
26. Cherry RS, Papoutsakis ET. 1990 Understanding and controlling fluid-mechanical injury of animal cells in bioreactors. In Animal cell biotechnology, vol. 4 (eds RE Spier, JB Griffiths), pp. 71-121. London, UK: Academic Press.
27. Croughan MS, Wang DIC. 1991 Hydrodynamic effects on animal cells in microcarrier bioreactors. In Animal cell bioreactors (eds CS Ho, DIC Wang), pp. 213-249. Stoneham, MA: Butterworth-Heinemann.
28. Nienow AW. 2014 Re ‘Development of a scale-down model of hydrodynamic stress to study the performance of an industrial CHO cell line under simulated production scale bioreactor conditions’ [Sieck JB, Cordes T, Budach WE, Rhiel MH, Suemeghy Z, Leist C, Villiger TK, Morbidelli M, Soos M. 2013 J. Biotechnol. 164, 41-49]. J. Biotechnol. 171, 82-84. doi: 10.1016/j.jbiotec.2013.12.002
29. Rushton JH, Costich EW, Everett HJ. 1950 Power characteristics of mixing impellers. Chem. Eng. Proc. 46, 467-471.
30. Paul EL, Atiemo-Obeng VA, Kresta SM. 2004 Handbook of industrial mixing. Hoboken, NJ: Wiley-Interscience.
31. Croughan MS, Hamel JF, Wang DIC. 1987 Hydrodynamic effects on animal cells grown in microcarrier cultures. Biotechnol. Bioeng. 29, 130-141. doi: 10.1002/bit.260290117
32. Sen A, Kallos MS, Behie LA. 2002 Expansion of mammalian neural stem cells in bioreactors: effect of power input and medium viscosity. Brain Res. Dev. Brain Res. 134, 103-113. doi: 10.1016/S0165-3806(01)00328-5
33. Moreira JL, Santana PC, Feliciano AS, Cruz PE, Racher AJ, Griffiths JB, Carrondo MJ. 1995 Effect of viscosity upon hydrodynamically controlled natural aggregates of animal cells grown in stirred vessels. Biotechnol. Prog. 11, 575-583. doi: 10.1021/bp00035a012
34. Cherry RS, Kwon KY. 1990 Transient shear stresses on a suspension cell in turbulence. Biotechnol. Bioeng. 36, 563-571. doi: 10.1002/bit.260360603
35. Geisler R, Krebs R, Forschner P. 1994 Local turbulent shear stress in stirred vessels and its significance for different mixing tasks. In Proc. 8th Eur. Conf. on Mixing, IChemE Symposium Series no. 136, pp. 241-251. London, UK: IChemE.
36. Croughan MS, Hamel JF, Wang DI. 1988 Effects of microcarrier concentration in animal cell culture. Biotechnol. Bioeng. 32, 975-982. doi: 10.1002/bit.260320805
37. Nienow AW. 1997 The mixer as a reactor—liquid/solid systems. In Mixing in the process industries (eds N Harnby, MF Edwards, AW Nienow), pp. 394-411. London, UK: Butterworth-Heinemann.
38. Cherry RS, Papoutsakis ET. 1989 Growth and death rates of bovine embryonic kidney cells in turbulent microcarrier bioreactors. Bioproc. Eng. 4, 81-89. doi: 10.1007/BF00373735
39. Hassanzadeh SM, Zavareh A, Shokrgozar MA, Ramezani A, Fayaz A. 2011 High vero cell density and rabies virus proliferation on fibracel disks versuscytodex-1 in spinner flask. Pak. J. Biol. Sci. 14, 441-448. doi: 10.3923/pjbs.2011.441.448
40. Croughan MS, Sayre ES, Wang DIC. 1989 Viscous reduction of turbulent damage in animal cell culture. Biotechnol. Bioeng. 33, 862-872. doi: 10.1002/bit.260330710
41. Stathopoulos NA, Hellums JD. 1985 Shear stress effects on human embryonic kidney cells in vitro. Biotechnol. Bioeng. 27, 1021-1026. doi: 10.1002/bit.260270713
42. Ma N, Chalmers JJ, Aunins JG, Zhou W, Xie L. 2004 Quantitative studies of cell-bubble interactions and cell damage at different pluronic F-68 and cell concentrations. Biotechnol. Prog. 20, 1183-1191. doi: 10.1021/bp0342405
43. Nienow AW. 2006 Reactor engineering in large scale animal cell culture. Cytotechnology 50, 9-33. doi: 10.1007/s10616-006-9005-8
44. Merten O-W. 2010 Cell detachment. In Encyclopedia of industrial biotechnology: bioprocess, bioseparation, and cell technology (ed. MC Flickinger), pp. 1-22. New York, NY: John Wiley & Sons Ltd.
45. Van Wezel AL, van der Velden de Groot CAM, van Herwaarden JAM. 1980 The production of inactivated poliovaccine on serially cultivated kidney cells from captive-bred monkeys. Dev. Biol. Stand. 46, 151-158.
46. Shevitz J, LaPorte TL, Stinnett TE. 1990 Production of viral vaccines in stirred bioeactors. In Viral vaccines in the series of advances in biotechnological processes, vol. 14 (ed. A Mizrahi), pp. 1-35. New York, NY: Wiley-Liss.
47. Ohlson S, Branscomb J, Nilsson K. 1994 Bead-to-bead transfer of Chinese hamster ovary cells using macroporous microcarriers. Cytotechnology 14, 67-80. doi: 10.1007/BF00772197
48. Kong D, Chen M, Gentz R, Zhang J. 1999 Cell growth and protein formation on various microcarriers. Cytotechnology 29, 149-156.
49. Xiao C, Huang Z, Li W, Hu X, Qu W, Gao L, Liu G. 1999 High density and scale-up cultivation of recombinant CHO cell line and hybridomas with porous Cytopore. Cytotechnology 30, 143-147. doi: 10.1023/A:1008038609967
50. Wang Y, Ouyang F. 1999 Bead-to-bead transfer of Vero cells in microcarrier culture. Cytotechnology 31, 221-224. doi: 10.1023/A:1008079013375
51. Luo F, Sun H, Gang T, Qi N. 2008 Application of Taguchi’s method in the optimization of bridging efficiency between confluent and fresh microcarriers in bead-to-bead transfer of Vero cells. Biotechnol. Lett. 30, 645-649. doi: 10.1007/s10529-007-9604-2
52. Xiao C, Huang Z, Zhang Z, Ye L, Gao L, Guo Z, Cheng D, Zhou H, Kong W. 1994 High density cultivation of a recombinant CD-1 cell line producing prourokinase using a Biosilon microcarrier culture system. Chin. Med. Sci. J. 9, 203-208.
53. Genzel Y, Reichl U. 2009 Continuous cell lines as a production system for influenza vaccines. Expert. Rev. Vaccines 8, 1681-1692. doi: 10.1586/erv.09.128
54. Merten O-W, Bakker WAM, Vorlop J, Reiter M, Visnovsky G, Jäger V, Merabishvili M, Reichl U. 2014Virus production under suspension conditions. In Industrial scale suspension culture of living cells (eds H-P Meyer, D Schmidhalter), pp. 503-554. Weinheim, Germany: Wiley-VCH.
55. Yu P, Huang Y, Zhang Y, Tang Q, Liang G. 2012 Production and evaluation of a chromatographically purified Vero cell rabies vaccine (PVRV) in China using microcarrier technology. Hum. Vaccine Immunother. 8, 1230-1235. doi: 10.4161/hv.20985
56. Aunins JG et al. 1997 Reactor development for the hepatitis A vaccine VAQTA. In Animal cell technology: from vaccines to genetic medicins (eds MJT Carrondo, B Griffiths, JLP Moreira), pp. 175-183. Dordrecht, The Netherlands: Kluwer Academic Publishers.
57. Hagen A et al. 2000 Development, preparation, and testing of VAQTA, a highly purified hepatits A vaccine. Bioproc. Eng. 23, 439-449. doi: 10.1007/s004499900157
58. Junker BH et al. 1992 Evaluation of a microcarrier process for large-scale cultivation of attenuated hepatitis A. Cytotechnology 9, 173-187. doi: 10.1007/BF02521745
59. Domenici M et al. 2006 Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317. doi: 10.1080/14653240600855905
60. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. 2004 Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22, 675-682. doi: 10.1634/stemcells.22-5-675
61. da Silva Meirelles L, Fontes AM, Covas DT, Caplan AI. 2009 Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 20, 419-427. doi: 10.1016/j. cytogfr.2009.10.002
62. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998 Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147. doi: 10.1126/science.282.5391.1145
63. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007 Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. doi: 10.1016/j.cell.2007.11.019
64. Serra M, Correia C, Malpique R, Brito C, Jensen J, Bjorquist P, Carrondo MJ, Alves PM. 2011 Microencapsulation technology: a powerful tool for integrating expansion and cryopreservation of human embryonic stem cells. PLoS ONE 6, e23212. doi: 10.1371/journal.pone.0023212
65. Akins RE, Rockwood D, Robinson KG, Sandusky D, Rabolt J, Pizarro C. 2010 Three-dimensional culture alters primary cardiac cell phenotype. Tissue Eng. Part A 16, 629-641. doi: 10.1089/ten.tea.2009.0458
66. Chang TT, Hughes-Fulford M. 2009 Monolayer and spheroid culture of human liver hepatocellular carcinoma cell line cells demonstrate distinct global gene expression patterns and functional phenotypes. Tissue Eng. Part A 15, 559-567. doi: 10.1089/ten.tea.2007.0434
67. Dasgupta A, Hughey R, Lancin P, Larue L, Moghe PV. 2005 E-cadherin synergistically induces hepatospecific phenotype and maturation of embryonic stem cells in conjunction with hepatotrophic factors. Biotechnol. Bioeng. 92, 257-266. doi: 10.1002/bit.20676
68. Correia C et al. 2014 Combining hypoxia and bioreactor hydrodynamics boosts induced pluripotent stem cell differentiation towards cardiomyocytes. Stem Cell Rev. Rep. 10, 786-801.
69. Abbasalizadeh S, Larijani MR, Samadian A, Baharvand H. 2012 Bioprocess development for mass production of size-controlled human pluripotent stem cell aggregates in stirred suspension bioreactor. Tissue Eng. Part C 18, 831-851. doi: 10.1089/ten.tec.2012.0161
70. Baptista RP, Fluri DA, Zandstra PW. 2012 High density continuous production of murine pluripotent cells in an acoustic perfused bioreactor at different oxygen concentrations. Biotechnol. Bioeng. 112, 648-655. doi: 10.1002/bit.24717
71. Coˆme J, Nissan X, Aubry L, Tournois J, Girard M, Perrier AL, Peschanski M, Cailleret M. 2008 Improvement of culture conditions of human embryoid bodies using a controlled perfused and dialyzed bioreactor system. Tissue Eng. Part C 14, 289-298. doi: 10.1089/ten.tec.2008.0029
72. Cameron CM, Hu WS, Kaufman DS. 2006 Improved development of human embryonic stem cell-derived embryoid bodies by stirred vessel cultivation. Biotechnol. Bioeng. 94, 938-948. doi: 10.1002/bit.20919
73. Carpenedo RL, Sargent CY, McDevitt TC. 2007 Rotary suspension culture enhances the efficiency, yield, and homogeneity of embryoid body differentiation. Stem Cells 25, 2224-2234. doi: 10.1634/stemcells.2006-0523
74. Yirme G, Amit M, Laevsky I, Osenberg S, Itskovitz-Eldor J. 2008 Establishing a dynamic process for the formation, propagation, and differentiation of human embryoid bodies. Stem Cells Dev. 17, 1227-1241. doi: 10.1089/scd.2007.0272
75. Gerecht-Nir S, Cohen S, Itskovitz-Eldor J. 2004 Bioreactor cultivation enhances the efficiency of human embryoid body (hEB) formation and differentiation. Biotechnol. Bioeng. 86, 493-502. doi: 10.1002/bit.20045
76. Schroeder M, Niebruegge S, Werner A, Willbold E, Burg M, Ruediger M, Field LJ, Lehmann J, Zweigerdt R. 2005 Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol. Bioeng. 92, 920-933. doi: 10.1002/bit.20668
77. Kinney MA, Sargent CY, McDevitt TC. 2011 The multiparametric effects of hydrodynamic environments on stem cell culture. Tissue Eng. Part B 17, 249-262. doi: 10.1089/ten.teb.2011.0040
78. Placzek MR et al. 2009 Stem cell bioprocessing: fundamentals and principles. J. R. Soc. Interface 6, 209-232. doi: 10.1098/rsif.2008.0442
79. Frith JE, Thomson B, Genever PG. 2010 Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng. Part C 16, 735-749. doi: 10.1089/ten.tec.2009.0432
80. Bartosh TJ, Ylöstalo JH, Mohammadipoor A, Bazhanov N, Coble K, Claypool K, Lee RH, Choi H, Prockop DJ. 2010 Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties. Proc. Natl Acad. Sci. USA 107, 13724-13729. doi: 10.1073/pnas.1008117107
81. Sart S, Tsai AC, Li Y, Ma T. 2013 Three-dimensional aggregates of mesenchymal stem cells: cellular mechanisms, biological properties, and applications. Tissue Eng. Part B 20, 365-380. doi: 10.1089/ten.teb.2013.0537
82. Zhang ZY, Teoh SH, Teo EY, Chong MSK, Shin CW, Tien FT, Choolani MA, Chan JK. 2010 A comparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 31, 8684-8695. doi: 10.1016/j.biomaterials.2010.07.097
83. Mukundakrishnan K, Ayyaswamy PS, Risbud M, Hu HH, Shapiro IM. 2004 Modeling of phosphate ion transfer to the surface of osteoblasts under normal gravity and simulated microgravity conditions. Ann. N Y Acad. Sci. 1027, 85-98. doi: 10.1196/annals.1324.009
84. Sikavitsas VI, Bancroft GN, Mikos AG. 2004 Formation of three-dimensional cell/polymer constructs for bone tissue engineering in a spinner flask and a rotating wall vessel bioreactor.J. Biomed. Mater. Res. 62, 136-148. doi: 10.1002/jbm.10150
85. Chun KW, Yoo HS, Yoon JJ, Park TG. 2004 Biodegradable PLGA microcarriers for injectable delivery of chondrocytes: effect of surface modification on cell attachment and function. Biotechnol. Prog. 20, 1797-1801. doi: 10.1021/bp0496981
86. Mercier NR, Costantino HR, Tracy MA, Bonassar LJ. 2005 Poly(lactide-co-glycolide) microspheres as a moldable scaffold for cartilage tissue engineering. Biomaterials 26, 1945-1952. doi: 10.1016/j.biomaterials.2004.06.030
87. Hong Y, Gao C, Xie Y, Gong Y, Shen J. 2005 Collagen-coated polylactide microspheres as chondrocyte microcarriers. Biomaterials 26, 6305-6313. doi: 10.1016/j.biomaterials.2005.03.038
88. Botchwey EA, Pollack SR, Levine EM, Laurencin CT. 2001 Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system. J. Biomed. Mater. Res. 55, 242-253. doi: 10.1002/1097-4636(200105)55:2,242::AID-JBM1011.3.0.CO;2-D
89. Rowley J, Abraham E, Campbell A, Brandwein H, Oh S. 2012 Meeting lot-size challenges of manufacturing adherent cells for therapy. BioProcess. Int. 103, 16-20.
90. Goh TW-P, Zhang Z-Y, Chen AK-L, Reuveny S, Choolani M, Chan JKY, Oh SK-W. 2013 Microcarrier culture for efficient expansion and osteogenic differentiation of human fetal mesenchymal stem cells. BioResearch Open Access 2, 84-97. doi: 10.1089/biores.2013.0001
91. Bardy J, Chen AK, Lim YM, Wu S, Wei S, Weiping H, Chan K, Reuveny S, Oh SK. 2013 Microcarrier suspension cultures for high-density expansion and differentiation of human pluripotent stem cells to neural progenitor cells. Tissue Eng. Part C 19, 166-180. doi: 10.1089/ten.tec.2012.0146
92. Simaria AS, Hassan S, Varadaraju H, Rowley J, Warren K, Vanek P, Farid SS. 2013 Allogeneic cell therapy bioprocess economics and optimization: single-use cell expansion technologies. Biotechnol. Bioeng. 111, 69-83. doi: 10.1002/bit.25008
93. Sart S, Schneider YJ, Agathos SN. 2010 Influence of culture parameters on ear mesenchymal stem cells expanded on microcarriers. J. Biotechnol. 150, 149-160. doi: 10.1016/j.jbiotec.2010.08.003
94. Want AJ, Nienow AW, Hewitt CJ, Coopman K. 2012 Large-scale expansion and exploitation of pluripotent stem cells for regenerative medicine purposes: beyond the T flask. Regen. Med. 7, 71-84. doi: 10.2217/rme.11.101
95. Kehoe D, Schnitzler A, Simler J, DiLeo A, Ball A. 2012 Scale-up of human mesenchymal stem cells on microcarriers in suspension in a single-use bioreactor. BioPharm. Int. 25, 28-38.
96. Sart S, Agathos SN, Li Y. 2013 Engineering stem cell fate with biochemical and biomechanical properties of microcarriers. Biotechnol. Prog. 29, 1354-1366. doi: 10.1002/btpr.1825
97. dos Santos F et al. 2011 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 17, 1201-1210. doi: 10.1089/ten.tec.2011.0255
98. Hughes CS, Radan L, Betts D, Postovit LM, Lajoie GA. 2011 Proteomic analysis of extracellular matrices used in stem cell culture. Proteomics 11, 3983-3991. doi: 10.1002/pmic.201100030
99. Roubelakis MG, Pappa KI, Bitsika V, Zagoura D, Vlahou A, Papadaki HA, Antsaklis A, Anagnou NP. 2007 Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells. Stem Cells Dev. 16, 931-952. doi: 10.1089/scd.2007.0036
100. Maijenburg MW, Noort WA, Kleijer M, Kompier CJ, Weijer K, van Buul JD, van der Schoot CE, Voermans C. 2010 Cell cycle and tissue of origin contribute to the migratory behaviour of human fetal and adult mesenchymal stromal cells. Br. J. Haematol. 148, 428-440. doi: 10.1111/j.1365-2141.2009.07960.x
101. Zhang ZY, Teoh SH, Chong MS, Schantz JT, Fisk NM, Choolani MA, Chan J. 2009 Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells. Stem Cells 27, 126-137. doi: 10.1634/stemcells.2008-0456
102. Sart S, Errachid A, Schneider YJ, Agathos SN. 2013 Modulation of mesenchymal stem cell actin organization on conventional microcarriers for proliferation and differentiation in stirred bioreactors. J. Tissue Eng. Regen. Med. 7, 537-551. doi: 10.1002/term.545
103. Weber C, Pohl S, PÖrtner R, Wallrapp C, Kassem M, Geigle P, Czermak P. 2007 Expansion and harvesting of hMSC-TERT. Open Biomed. Eng. J. 1, 38-46. doi: 10.2174/1874120700701010038
104. Yang Y, Rossi FM, Putnins EE. 2007 Ex vivo expansion of rat bone marrow mesenchymal stromal cells on microcarrier beads in spin culture. Biomaterials 28, 3110-3120. doi: 10.1016/j.biomaterials.2007.03.015
105. Chen AK-L, Chen X, Choo AB, Reuveny S, Oh SK. 2011 Critical microcarrier properties affecting the expansion of undifferentiated human embryonic stem cells. Stem Cell Res. 7, 97-111. doi: 10.1016/j.scr.2011.04.007
106. Nie Y, Walsh P, Clarke DL, Rowley JA, Fellner T. 2014 Scalable passaging of adherent human pluripotent stem cells. PLoS ONE 9, e88012. doi: 10.1371/journal.pone.0088012
107. Heng BC, Li J, Chen AK, Reuveny S, Cool SM, Birch WR, Oh SK. 2012 Translating human embryonic stem cells from 2-dimensional to 3-dimensional cultures in a defined medium on laminin- and vitronectin-coated surfaces. Stem Cells Dev. 21, 1701-1715. doi: 10.1089/scd.2011.0509
108. Lam AT-L, Li J, Chen AK, Reuveny S, Oh SK, Birch WR. 2014 Cationic surface charge combined with either vitronectin or laminin dictates the evolution of hESC/microcarrier aggregates and cell growth in agitated cultures. Stem Cells Dev. 23, 1688-1703. doi: 10.1089/scd.2013.0645
109. Miyazaki T et al. 2008 Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem. Biophys. Res. Commun. 375, 27-32. doi: 10.1016/j.bbrc.2008.07.111
110. Rodin S, Domogatskaya A, StrÖm S, Hansson EM, Chien KR, Inzunza J, Hovatta O, Tryggvason K. 2010 Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat. Biotechnol. 28, 611-615. doi: 10.1038/nbt.1620
111. Melkoumian Z et al. 2010 Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat. Biotechnol. 28, 606-610. doi: 10.1038/nbt.1629
112. Kolhar P, Kotamraju VR, Hikita ST, Clegg DO, Ruoslahti E. 2010 Synthetic surfaces for human embryonic stem cell culture. J. Biotechnol. 146, 143-146. doi: 10.1016/j.jbiotec.2010.01.016
113. Villa-Diaz LG, Nandivada H, Ding J, Nogueira-de-Souza NC, Krebsbach PH, O’Shea KS, Lahann J, Smith GD. 2010 Synthetic polymer coatings for long-term growth of human embryonic stem cells. Nat. Biotechnol. 28, 581-583. doi: 10.1038/nbt.1631
114. Villa-Diaz LG, Ross AM, Lahann J, Krebsbach PH. 2013 Concise review: The evolution of human pluripotent stem cell culture: from feeder cells to synthetic coatings. Stem Cells 31, 1-7. doi: 10.1002/stem.1260
115. Huebsch N, Arany PR, Mao AS, Shvartsman D, Ali OA, Bencherif SA, Rivera-Feliciano J, Mooney DJ. 2010 Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518-526. doi: 10.1038/nmat2732
116. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006 Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. doi: 10.1016/j.cell.2006.06.044
117. Lanniel M, Huq E, Allen S, Buttery L, Williams PM, Alexander MR. 2011 Substrate induced differentiation of human mesenchymal stem cells on hydrogels with modified surface chemistry and controlled modulus. Soft Matter 7, 6501-6514. doi: 10.1039/c1sm05167a
118. Shih YR, Tseng KF, Lai HY, Lin CH, Lee OK. 2011 Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells. J. Bone Miner. Res. 26, 730-738. doi: 10.1002/jbmr.278
119. Zoldan J, Karagiannis ED, Lee CY, Anderson DG, Langer R, Levenberg S. 2011 The influence of scaffold elasticity on germ layer specification of human embryonic stem cells. Biomaterials 32, 9612-9621. doi: 10.1016/j.biomaterials.2011.09.012
120. Kehoe DE, Jing D, Lock LT, Tzanakakis ES. 2010 Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng. Part A 16, 405-421. doi: 10.1089/ten.tea.2009.0454
121. Hunt MM, Meng G, Rancourt DE, Gates ID, Kallos MS. 2014 Factorial experimental design for the culture of human embryonic stem cells as aggregates in stirred suspension bioreactors reveals the potential for interaction effects between bioprocess parameters. Tissue Eng. Part C 20, 76-89. doi: 10.1089/ten.tec.2013.0040
122. Cormier JT, zur Nieden NI, Rancourt DE, Kallos MS. 2006 Expansion of undifferentiated murine embryonic stem cells as aggregates in suspension culture bioreactors. Tissue Eng. 12, 3233-3245. doi: 10.1089/ten.2006.12.3233
123. Wolfe RP, Ahsan T. 2013 Shear stress during early embryonic stem cell differentiation promotes hematopoietic and endothelial phenotypes. Biotechnol. Bioeng. 110, 1231-1242. doi: 10.1002/bit.24782
124. Przybyla LM, Voldman J. 2012 Probing embryonic stem cell autocrine and paracrine signaling using microfluidics. Ann. Rev. Anal. Chem. 5, 293-315. doi: 10.1146/annurev-anchem-062011-143122
125. Przybyla LM, Voldman J. 2012 Attenuation of extrinsic signaling reveals the importance of matrix remodeling on maintenance of embryonic stem cell self-renewal. Proc. Natl Acad. Sci. USA 109, 835-840. doi: 10.1073/pnas.1103100109
126. Toh Y-C, Voldman J. 2011 Fluid shear stress primes mouse embryonic stem cells for differentiation in a self-renewing environment via heparan sulfate proteoglycans transduction. FASEB J. 25, 1208-1217. doi: 10.1096/fj.10-168971
127. Bliem R, Katinger H. 1988 Scale-up engineering in animal-cell technology. Parts I and II. Trends Biotechnol. 6, 190-195, 224-230. doi: 10.1016/0167-7799(88)90045-5
128. Sen A, Kallos MS, Behie LA. 2001 Effects of hydrodynamics on cultures of mammalian neural stem cell aggregates in suspension bioreactors. Ind. Eng. Chem. Res. 40, 5350-5357. doi: 10.1021/ie001107y
129. Wu J, Rostami MR, Cadavid Olaya DP, Tzanakakis ES. 2014 Oxygen transport and stem cell aggregation in stirred-suspension bioreactor cultures. PLoS ONE 9, e102486. doi: 10.1371/journal.pone.0102486
130. Prado-Lopez S et al. 2010 Hypoxia promotes efficient differentiation of human embryonic stem cells to functional endothelium. Stem Cells 28, 407-418. doi: 10.1002/stem.295
131. Koay EJ, Athanasiou KA. 2008 Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. Osteoarthrit. Cartilage 16, 1450-1456. doi: 10.1016/j.joca.2008.04.007
132. Ezashi T, Das P, Roberts RM. 2005 Low O2 tensions and the prevention of differentiation of hES cells. Proc. Natl Acad. Sci. USA 102, 4783-4788. doi: 10.1073/pnas.0501283102
133. Forsyth NR, Musio A, Vezzoni P, Simpson AH, Noble BS, McWhir J. 2006 Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cells 8, 16-23. doi: 10.1089/clo.2006.8.16
134. Martin Y, Vermette P. 2005 Bioreactors for tissue mass culture: design, characterization, and recent advances. Biomaterials 26, 7481-7503. doi: 10.1016/j.biomaterials.2005.05.057
135. Singh H, Mok P, Balakrishnan T, Rahmat SN, Zweigerdt R. 2010 Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. Stem Cell Res. 4, 165-179. doi: 10.1016/j.scr.2010.03.001
136. Olmer R, Lange A, Selzer S, Kasper C, Haverich A, Martin U, Zweigerdt R. 2012 Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors. Tissue Eng. Part C 18, 772-784. doi: 10.1089/ten.tec.2011.0717
137. Leung HW, Chen A, Choo AB, Reuveny S, Oh SK. 2011 Agitation can induce differentiation of human pluripotent stem cells in microcarrier cultures. Tissue Eng. Part C 17, 165-172. doi: 10.1089/ten.tec.2010.0320
138. Mitalipova MM, Rao RR, Hoyer DM, Johnson JA, Meisner LF, Jones KL, Dalton S, Stice SL. 2005 Preserving the genetic integrity of human embryonic stem cells. Nat. Biotechnol. 23, 19-20. doi: 10.1038/nbt0105-19
139. Canavan HE, Cheng X, Graham DJ, Ratner BD, Castner DG. 2005 Cell sheet detachment affects the extracellular matrix: a surface science study comparing thermal liftoff, enzymatic, and mechanical methods. J. Biomed. Mater. Res. Part A 75, 1-13. doi: 10.1002/jbm.a.30297
140. Potapova IA, Brink PR, Cohen IS, Doronin SV. 2008 Culturing of human mesenchymal stem cells as three-dimensional aggregates induces functional expression of CXCR4 that regulates adhesion to endothelial cells. J. Biol. Chem. 283, 13 100-13 107. doi: 10.1074/jbc.M800184200
141. Nienow AW, Rafiq QA, Coopman K, Hewitt CJ. 2014 A potentially scalable method for the harvesting of hMSCs from microcarriers. Biochem. Eng. J. 85, 79-88. doi: 10.1016/j.bej.2014.02.005
142. Watanabe K et al. 2007 A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686. doi: 10.1038/nbt1310
143. Oh SKW, Chen AK, Mok Y, Chen X, Lim UM, Chin A, Choo AB, Reuveny S. 2009 Long-term microcarrier suspension cultures of human embryonic stem cells. Stem Cell Res. 2, 219-230. doi: 10.1016/j.scr.2009.02.005
144. Yang J, Yamato M, Nishida K, Ohki T, Kanzaki M, Sekine H, Shimizu T, Okano T. 2006 Cell delivery in regenerative medicine: the cell sheet engineering approach. J. Control. Release 116, 193-203. doi: 10.1016/j.jconrel.2006.06.022
145. Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y. 1995 Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials 16, 297-303. doi: 10.1016/0142-9612(95)93257-E
146. Arisaka Y, Kobayashi J, Yamato M, Akiyama Y, Okano T. 2013 Switching of cell growth/detachment on heparin-functionalized thermoresponsive surface for rapid cell sheet fabrication and manipulation. Biomaterials 34, 4214-4222. doi: 10.1016/j.biomaterials.2013.02.056
147. Higuchi A et al. 2006 Temperature-induced cell detachment on immobilized pluronic surface. J. Biomed Mater. Res. A 79, 380-392. doi: 10.1002/jbm.a.30773
148. Ebara M, Yamato M, Aoyagi T, Kikuchi A, Sakai K, Okano T. 2004 Immobilization of cell-adhesive peptides to temperature-responsive surfaces facilitates both serum-free cell adhesion and noninvasive cell harvest. Tissue Eng. 10, 1125-1135. doi: 10.1089/1076327041887691
149. Kenda-Ropson N, Lenglois S, Miller AO. 2002 Microsupport with two-dimensional geometry 2D-MS. 4. Temperature-induced detachment of anchorage-dependent CHO-K1 cells from cryoresponsive MicroHex((R)) (CryoHex). Cytotechnology 39, 163-170. doi: 10.1023/A:1023949716842
150. Tamura A, Kobayashi J, Yamato M, Okano T. 2012 Temperature-responsive poly(N-isopropylacrylamide)-grafted microcarriers for large-scale non-invasive harvest of anchorage-dependent cells. Biomaterials 33, 3803-3812. doi: 10.1016/j.biomaterials.2012.01.060
151. Yang HS, Jeon O, Bhang SH, Lee SH, Kim BS. 2010 Suspension culture of mammalian cells using thermosensitive microcarrier that allows cell detachment without proteolytic enzyme treatment.Cell Transplant. 19, 1123-1132. doi: 10.3727/096368910X516664
152. Gümüşderelioğlu M, Çakmak S, Timuçin HÖ, Çakmak AS. 2013 Thermosensitive PHEMA microcarriers: ATRP synthesis, characterization, and usabilities in cell cultures. J. Biomater. Sci. Polym. Ed. 24, 2110-2125. doi: 10.1080/09205063.2013.827104
153. Heng BC, Vinoth KJ, Liu H, Hande MP, Cao T. 2006 Low temperature tolerance of human embryonic stem cells. Int. J. Med. Sci. 3, 124-129. doi: 10.7150/ijms.3.124
154. Brun-Graeppi AK, Richard C, Bessodes M, Scherman D, Merten OW. 2011 Cell microcarriers and microcapsules of stimuli-responsive polymers. J. Control. Release 149, 209-224. doi: 10.1016/j.jconrel.2010.09.023
155. Dubois NC, Craft AM, Sharma P, Elliott DA, Stanley EG, Elefanty AG, Gramolini A, Keller G. 2011 SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat. Biotechnol. 29, 1011-1018. doi: 10.1038/nbt.2005
156. Pruszak J, Sonntag KC, Aung MH, Sanchez-Pernaute R, Isacson O. 2007 Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25, 2257-2268. doi: 10.1634/stemcells.2006-0744
157. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. 2002 Endothelial cells derived from human embryonic stem cells. Proc. Natl Acad. Sci. USA 99, 4391-4396. doi: 10.1073/pnas.032074999
158. Schriebl K, Satianegara G, Hwang A, Tan HL, Fong WJ, Yang HH, Jungbauer A, Choo A. 2012 Selective removal of undifferentiated human embryonic stem cells using magnetic activated cell sorting followed by a cytotoxic antibody. Tissue Eng. Part A 18, 899-909. doi: 10.1089/ten.tea.2011.0311
159. Tan HL, Fong WJ, Lee EH, Yap M, Choo A. 2009 mAb 84, a cytotoxic antibody that kills undifferentiated human embryonic stem cells via oncosis. Stem Cells 27, 1792-1801. doi: 10.1002/stem.109
160. Tohyama S et al. 2013 Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 12, 127-137. doi: 10.1016/j.stem.2012.09.013
161. Abbasalizadeh S, Baharvand H. 2013 Technological progress and challenges towards cGMP manufacturing of human pluripotent stem cells based therapeutic products for allogeneic and autologous cell therapies. Biotechnol. Adv. 31, 1600-1623. doi: 10.1016/j.biotechadv.2013.08.009
162. Diogo MM, da Silva CL, Cabral JM. 2012 Separation technologies for stem cell bioprocessing. Biotechnol. Bioeng. 109, 2699-2709. doi: 10.1002/bit.24706
163. Gupta P, Ismadi M-Z, Verma PJ, Fouras A, Jadhav S, Bellare J, Hourigan K. In press. Optimization of agitation speed in spinner flask for microcarrier structural integrity and expansion of induced plutipotent stem cells. Cytotechnology. doi: 10.1007/s10616-014-9750-z
164. Rafiq QA, Brosnan KM, Coopman K, Nienow AW, Hewitt CJ. 2013 Culture of human mesenchymal stem cells on microcarriers in a 5 l stirred-tank bioreactor. Biotechnol. Lett. 35, 1233-1245. doi: 10.1007/s10529-013-1211-9
165. Serra M et al. 2010 Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. J. Biotechnol. 148, 208-215. doi: 10.1016/j.jbiotec.2010.06.015