Cited by 265Pluripotent Stem Cells ResearchFluid Dynamics and MixingMesenchymal stem cell research

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Scalable Stirred-Suspension Bioreactor Culture of Human Pluripotent Stem Cells

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Kehoe, Daniel E., Jing, Donghui, Lock, Lye T., Tzanakakis, Emmanuel S.·2010·Tissue Engineering Part A

DOI 10.1089/ten.tea.2009.0454PMC PMC2813185

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Abstract

Advances in stem cell biology have afforded promising results for the generation of various cell types for therapies against devastating diseases. However, a prerequisite for realizing the therapeutic potential of stem cells is the development of bioprocesses for the production of stem cell progeny in quantities that satisfy clinical demands. Recent reports on the expansion and directed differentiation of human embryonic stem cells (hESCs) in scalable stirred-suspension bioreactors (SSBs) demonstrated that large-scale production of therapeutically useful hESC progeny is feasible with current state-of-the-art culture technologies. Stem cells have been cultured in SSBs as aggregates, in microcarrier suspension and after encapsulation. The various modes in which SSBs can be employed for the cultivation of hESCs and human induced pluripotent stem cells (hiPSCs) are described. To that end, this is the first account of hiPSC cultivation in a microcarrier stirred-suspension system. Given that cultured stem cells and their differentiated progeny are the actual products used in tissue engineering and cell therapies, the impact of bioreactor's operating conditions on stem cell self-renewal and commitment should be considered. The effects of variables specific to SSB operation on stem cell physiology are discussed. Finally, major challenges are presented which remain to be addressed before the mainstream use of SSBs for the large-scale culture of hESCs and hiPSCs.

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Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., & Yamanaka, S. (2007) · Cell · doi:10.1016/j.cell.2007.11.019 · Cited by 20,221
Embryonic Stem Cell Lines Derived from Human Blastocysts
Thomson, J. A., Itskovitz‐Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., & Jones, J. M. (1998) · Science · doi:10.1126/science.282.5391.1145 · Cited by 15,947
Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells
Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., et al. (2007) · Science · doi:10.1126/science.1151526 · Cited by 10,310
Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering
Lutolf, M. P., & Hubbell, J. A. (2005) · Nature Biotechnology · doi:10.1038/nbt1055 · Cited by 4,551
Mathematical Theory of the Kinetics of the Coagulation of Colloidal Solutions
Smoluchowski, M. (1917) · Zeitschrift für Physikalische Chemie · Cited by 2,792
Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor
Sato, N., Meijer, L., Skaltsounis, A., Greengard, P., & Brivanlou, A. H. (2003) · Nature Medicine · doi:10.1038/nm979 · Cited by 2,139
A ROCK inhibitor permits survival of dissociated human embryonic stem cells
Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J. B., Nishikawa, S., Nishikawa, S.-I., Muguruma, K., et al. (2007) · Nature Biotechnology · doi:10.1038/nbt1310 · Cited by 2,055
Production of pancreatic hormone–expressing endocrine cells from human embryonic stem cells
D’Amour, K. A., Bang, A. G., Eliazer, S., Kelly, O., Agulnick, A. D., Smart, N. G., Moorman, M. A., KROON, E. J., Carpenter, M. K., & Baetge, E. E. (2006) · Nature Biotechnology · doi:10.1038/nbt1259 · Cited by 1,913
Synthetic Matrix Metalloproteinase-Sensitive Hydrogels for the Conduction of Tissue Regeneration: Engineering Cell-Invasion Characteristics
Lutolf, M. P., Lauer-Fields, J. L., Schmoekel, H. G., Metters, A. T., Weber, F. E., Fields, G. B., & Hubbell, J. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737381100 · Cited by 1,508
Population Balances: Theory and Applications to Particulate Systems in Engineering
Ramkrishna, D. (2000) · Cited by 1,434

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Show all 179 references

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Research works printed but not linked: 6

Palsson B.O., 2004, Tissue Engineering
Lock L.T., 2008, Med J Malaysia, 63, 5
Billig D., 1983, Dev Biol Stand, 55, 67
Hinze J.O., 1975, Turbulence
Daoutidis P., 2002, AIChE Symp Ser, 326, 274
von Smoluchowski M., 1917, Z Phys Chem, 92, 129

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Authors: Kehoe, D. E., Jing, D., Lock, L. T., & Tzanakakis, E. S.
Affiliations: University at Buffalo, State University of New York (US)
Corresponding author: Tzanakakis, Emmanuel S.
ORCID: Tzanakakis, Emmanuel S.
Venue: Tissue Engineering Part A
Publisher: SAGE Publications
Published: 2010-02
Volume: 16
Issue: 2
Pages: 405-421
ISSN: 1937-3341 (ISSN-L)
1937-335X
DOI: 10.1089/ten.tea.2009.0454
PMC: PMC2813185
OpenAlex: W1983810137
Cited by: 264
References: 179
Citations by year: 2026: 3 · 2025: 5 · 2024: 11 · 2023: 14 · 2022: 3 · 2021: 17 · 2020: 9 · 2019: 10 · 2018: 17 · 2017: 16 · 2016: 19 · 2015: 18 · 2014: 27 · 2013: 33 · 2012: 27
FWCI: 1.56
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.liebertpub.com/nv/resources-tools/text-and-data-mining-policy/121/ (tdm)
Locations: Tissue Engineering Part A (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Harvard University
Amrita Vishwa Vidyapeetham University
National Institutes of Health
Office of Science
Harvard Stem Cell Institute
National Heart, Lung, and Blood Institute (R21HL092398, HL092398)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Physical Sciences › Chemical Engineering › Fluid Flow and Transfer Processes › Fluid Dynamics and Mixing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Keywords: stirred suspension bioreactors, human pluripotent stem cells, human embryonic stem cells, human induced pluripotent stem cells, large-scale cell culture, microcarrier culture, encapsulation, stem cell self-renewal, directed differentiation, bioprocess scale-up, cell therapy
MeSH terms: Cells, Cultured, Humans, Cell Culture Techniques, Bioreactors, Pluripotent Stem Cells

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Scalable Stirred-Suspension Bioreactor Culture of Human Pluripotent Stem Cells

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