Expansion of embryonic stem cells in suspension and fibrous bed bioreactors

Journal of Biotechnology

Volumn 178, Issue 1, 2014, Pages 54-64

  Liu, Ning ^a,c   Li, Yan ^b   Yang, Shang Tian ^a  

^a The Ohio State University   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c Irvine Scientific   (United States)

Author keywords

Embryonic stem cells; Expansion; Fibrous bed bioreactor; Suspension culture; Three dimensional culture

Indexed keywords

BIOCONVERSION; BIOREACTORS; CELL CULTURE; CELL PROLIFERATION; EXPANSION; QUALITY CONTROL; STEM CELLS; TISSUE ENGINEERING; CELL GROWTH; CELLS; CYTOLOGY; MOBILE SECURITY;

CELL CULTURE PROCESS; DIFFERENTIATION MARKERS; EMBRYONIC STEM CELLS; EXPRESSION LEVELS; FIBROUS BED BIOREACTOR; MASS PRODUCTION; SUSPENSION CULTURES; THREE-DIMENSIONAL CULTURE;

CELL ENGINEERING;

CELL MARKER; OCTAMER TRANSCRIPTION FACTOR 4; STAGE SPECIFIC EMBRYO ANTIGEN 1; GLUCOSE; LACTIC ACID;

ANIMAL CELL; ARTICLE; BIOREACTOR; CELL AGGREGATION; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL GROWTH; CELL SUSPENSION; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; FIBROUS BED BIOREACTOR; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL CULTURE; STEM CELL EXPANSION; SUSPENSION CELL CULTURE; CELL PROLIFERATION; DOWN REGULATION; GLUCOSE INTAKE; HYDRODYNAMICS; MONOLAYER CULTURE; MOUSE; REAL TIME POLYMERASE CHAIN REACTION; SCALE UP; ANIMAL; CELL SURVIVAL; CULTURE TECHNIQUE; CYTOLOGY; DEVICES; KINETICS; METABOLISM; PHYSIOLOGY; PROCEDURES;

MURINAE;

ANIMALS; BIOREACTORS; CELL CULTURE TECHNIQUES; CELL SURVIVAL; EMBRYOID BODIES; EMBRYONIC STEM CELLS; GLUCOSE; KINETICS; LACTIC ACID; MICE;

EID: 84896965671     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.03.007     Document Type: Article

References (65)

1. Abbasalizadeh S., Baharvand H. Technological progress and challenges towards cGMP manufacturing of human pluripotent stem cells based therapeutic products for allogeneic and autologous cell therapies. Biotechnol. Adv. 2013, 31:1600-1623.
2. Abbasalizadeh S., Larijani M.R., Samadian A., Baharvand H. Bioprocess development for mass production of size-controlled human pluripotent stem cell aggregates in stirred suspension bioreactor. Tissue Eng. C Methods 2012, 18:831-851.
3. Abranches E., Bekman E., Henrique D., Cabral J.M.S. Expansion of mouse embryonic stem cells on microcarriers. Biotechnol. Bioeng. 2007, 96:1211-1221.
4. Alfred R., Gareau T., Krawetz R., Rancourt D., Kallos M.S. Serum-free scaled up expansion and differentiation of murine embryonic stem cells to osteoblasts in suspension bioreactors. Biotechnol. Bioeng. 2010, 106:829-840.
5. Alfred R., Radford J., Fan J., Boon K., Krawetz R., Rancourt D., Kallos M.S. Efficient suspension bioreactor expansion of murine embryonic stem cells on microcarriers in serum-free medium. Biotechnol. Prog. 2011, 27:811-823.
6. Amit M., Itskovitz-Eldor J. Embryonic stem cells: isolation, characterization and culture. Adv. Biochem. Eng. Biotechnol. 2009, 114:173-184.
7. 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. Protocol 2011, 6:572-579.
8. Chaudhry M.A., Bowen B.D., Piret J.M. Culture pH and osmolality influence proliferation and embryoid body yields of murine embryonic stem cells. Biochem. Eng. J. 2009, 45:126-135.
9. Chen A., Reuveny S., Oh S. Application of human mesenchymal and pluripotent stem cell microcarrier cultures in cellular therapy: achievements and future direction. Biotechnol. Adv. 2013, 31:1032-1046.
10. Chen C., Huang Y.L., Yang S.T. A fibrous-bed bioreactor for continuous production of developmental endothelial locus-1 by osteosarcoma cells. J. Biotechnol. 2002, 97:23-39.
11. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276:1425-1428.
12. Chen X., Chen A., Woo T.L., Choo A.B., Reuveny S., Oh S.K. Investigations into the metabolism of two-dimensional colony and suspended microcarrier cultures of human embryonic stem cells in serum-free media. Stem Cell Dev. 2010, 19:1781-1792.
13. Cormier J.T., zur Nieden N.I., Rancourt D.E., Kallos M.S. Expansion of undifferentiated murine embryonic stem cells as aggregates in suspension culture bioreactors. Tissue Eng. 2006, 12:3233-3245.
14. Engle S.J., Puppala D. Integrating human pluripotent stem cells into drug development. Cell Stem Cell 2013, 12:669-677.
15. Fan Y., Hsiung M., Cheng C., Tzanakakis E.S. Facile engineering of xeno-free microcarriers for the scalable cultivation of human pluripotent stem cells in stirred suspension. Tissue Eng. A 2013, (in press). 10.1089/ten.tea.2013.0219.
16. Fernandes A.M., Fernandes T.G., Diogo M.M., da Silva C.L., Henrique D., Cabral J.M.S. Mouse embryonic stem cell expansion in a microcarrier-based stirred culture system. J. Biotechnol. 2007, 132:227-236.
17. Fernandes-Platzgummer A., Diogo M.M., Baptista R.P., da Silva C.L., Cabral J.M.S. Scale-up of mouse embryonic stem cell expansion in stirred bioreactors. Biotechnol. Prog. 2011, 27:1421-1432.
18. Fluri D.A., Tonge P.D., Song H., Baptista R.P., Shakiba N., Shukla S., Clarke G., Nagy A., Zandstra P.W. Derivation, expansion and differentiation of induced pluripotent stem cells in continuous suspension cultures. Nat. Methods 2012, 9:509-516.
19. Fok E.Y.L., Zandstra P.W. Shear-controlled single-step mouse embryonic stem cell expansion and embryoid body-based differentiation. Stem Cell 2005, 23:1333-1342.
20. Giebel L.B. Stem cells: a hard sell to investors. Nat. Biotechnol. 2005, 23:798-800.
21. Gilbertson J.A., Sen A., Behie L.A., Kallos M.S. Scaled-up production of mammalian neural precursor cell aggregates in computer-controlled suspension bioreactors. Biotechnol. Bioeng. 2006, 94:783-792.
22. Itskovitz-Eldor J., Schuldiner M., Karsenti D., Eden A., Yanuka O., Amit M., Soreq H., Benvenisty N. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol. Med. 2000, 6:88-95.
23. Kehoe D.E., Lock L.T., Parikh A., Tzanakakis E.S. Propagation of embryonic stem cells in stirred suspension without serum. Biotechnol. Prog. 2008, 24:1342-1352.
24. Kehoe D.E., Jing D., Lock L.T., Tzanakakis E.M. Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng. A 2010, 16:405-421.
25. King J.A., Miller W.M. Bioreactor development for stem cell expansion and controlled differentiation. Curr. Opin. Chem. Biol. 2007, 11:394-398.
26. Kinney M.A., Sargent C.Y., McDevitt T.C. The multiparametric effects of hydrodynamic environments on stem cell culture. Tissue Eng. B Rev. 2011, 17:249-262.
27. Krawetz R., Taiani J.T., Liu S., Meng G., Li X., Kallos M.S., et al. Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. Tissue Eng. C Methods 2010, 16:573-582.
28. Lei Y., Schaffer D.V. A fully defined and scalable 3D culture system for human pluripotent stem cell expansion and differentiation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E5039-E5048.
29. Li D., Isherwood S., Motz A., Zang R., Yang S.T., Wang J., Wang X. Cell-based screening of traditional chinese medicines for proliferation enhancers of mouse embryonic stem cells. Biotechnol. Progr. 2013, 29:738-744.
30. Li Y., Ma T., Kniss D.A., Yang S.T., Lasky L.C. Human cord cell hematopoiesis in three-dimensional nonwoven fibrous matrices: in vitro stimulation of the marrow microenvironment. J. Hematother. Stem Cell Res. 2001, 10:355-368.
31. Li Y., Kniss D.A., Lasky L.C., Yang S.T. Culturing and differentiation of murine embryonic stem cells in three-dimensional fibrous matrix. Cytotechnology 2003, 41:23-35.
32. Liu M., Li Y., Yang S.T. Expansion of human amniotic fluid stem cells in 3-dimensional fibrous scaffolds in stirred bioreactors. Biochem. Eng. J. 2014, 82:71-80.
33. Liu N., Li Y., Yang S.T. Microfibrous carriers for integrated expansion and neural differentiation of embryonic stem cells in suspension bioreactor. Biochem. Eng. J. 2013, 75:55-63.
34. Liu N., Ouyang A., Li Y., Yang S.T. Three-dimensional neural differentiation of embryonic stem cells with ACM induction in microfibrous matrices in bioreactors. Biotechnol. Prog. 2013, 29:1013-1022.
35. Lock D., Parikh A. Propagation of embryonic stem cells in stirred suspension without serum. Biotechnol. Prog. 2008, 24:1342-1352.
36. 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. A 2009, 15:2051-2063.
37. Marinho P.A., Vareschini D.T., Gomes I.C., Paulsen Bda S., Furtado D.R., Castilho Ldos R., Rehen S.K. Xeno-free production of human embryonic stem cells in stirred microcarrier systems using a novel animal/human-component-free medium. Tissue Eng. C Methods 2013, 19:146-155.
38. Murry C.E., Field L.J., Menasche P. Cell-based cardiac repair: reflections at the 10-year point. Circulation 2005, 112:3174-3183.
39. Oh S.K., Fong W.J., Teo Y., Tan H.L., Padmanabhan J., Chin A.C., Choo A.B. High density cultures of embryonic stem cells. Biotechnol. Bioeng. 2005, 91:523-533.
40. Oh S.K., Chen A.K., Mok Y., Chen X., et al. Long-term microcarrier suspension cultures of human embryonic stem cells. Stem Cell Res. 2009, 2:219-230.
41. Olmer R., Lange A., Selzer S., Kasper C., et al. Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors. Tissue Eng. C Methods 2012, 18:772-784.
42. Ouyang A., Yang S.T. A two-stage perfusion fibrous bed bioreactor system for mass production of embryonic stem cells. Expert Opin. Biol. Ther. 2008, 8:895-909.
43. Ouyang A., Ng R., Yang S.T. Long-term culturing of undifferentiated embryonic stem cells in conditioned media and three-dimensional fibrous matrices without extracellular matrix coating. Stem Cell 2007, 25:447-454.
44. Patel S.D., Papoutsakis E.T., Winter J.N., Miller W.M. The lactate issue revisited: novel feeding protocols to examine inhibition of cell proliferation and glucose metabolism in hematopoietic cell cultures. Biotechnol. Prog. 2000, 16:885-892.
45. Phillips B.W., Horne R., Lay T.S., Rust W.L., et al. Attachment and growth of human embryonic stem cells on microcarriers. J. Biotechnol. 2008, 138:24-32.
46. Rajamohan D., Matsa E., Kalra S., Crutchley J., Patel A., George V., Denning C. Current status of drug screening and disease modelling in human pluripotent stem cells. Bioessays 2013, 35:281-298.
47. Schroeder M., Niebruegge S., Werner A., Willbold E., Burg M., Ruediger M., Field L.J., Lehmann J., Zweigerdt R. Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol. Bioeng. 2005, 92:920-933.
48. Sen A., Kallos M.S., Behie L.A. Effects of hydrodynamics on cultures of mammalian neural stem cell aggregates in suspension bioreactors. Ind. Eng. Chem. Res. 2001, 40:5350-5357.
49. Serra M., Brito C., Sousa M.F., Jensen J., Tostoes R., Clemente J., Strehl R., Hyllner J., Carrondo M.J., Alves P.M. Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. J. Biotechnol. 2010, 148:208-215.
50. Serra M., Brito C., Correia C., Alves P.M. Process engineering of human pluripotent stem cells for clinical application. Trends Biotechnol. 2012, 30:350-359.
51. Shafa M., Sjonnesen K., Yamashita A., Liu S., Michalak M., Kallos M.S., Rancourt D.E. Expansion and long-term maintenance of induced pluripotent stem cells in stirred suspension bioreactors. J. Tissue Eng. Regen. Med. 2012, 6:462-472.
52. Sharma S., Raju R., Sui S., Hu W.S. Stem cell culture engineering - process scale up and beyond. Biotechnol. J. 2011, 6:1317-1329.
53. 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.
54. Steiner D., Khaner H., Cohen M., Even-Ram S., Gil Y., Itsykson P., Turetsky T., Idelson M., Aizenman E., Ram R., Berman-Zaken Y., Reubinoff B. Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat. Biotechnol. 2010, 28:361-364.
55. Storm M.P., Orchard C.B., Bone H.K., Chaudhuri J.B., Welham M.J. Three-dimensional culture systems for the expansion of pluripotent embryonic stem cells. Biotechnol. Bioeng. 2010, 107:683-695.
56. Subranmanian K., Park Y., Verfaillie C.M., Hu W.S. Scalable expansion of multipotent adult progenitor cells as three-dimensional cell aggregates. Biotechnol. Bioeng. 2010, 108:364-375.
57. Ungrin M.D., Clarke G., Yin T., Niebrugge S., Nostro M.C., Sarangi F., Wood G., Keller G., Zandstra P.W. Rational bioprocess design for human pluripotent stem cell expansion and endoderm differentiation based on cellular dynamics. Biotechnol. Bioeng. 2012, 109:853-866.
58. Want A.J., Nienow A.W., Hewitt C.J., Coopman K. Large-scale expansion and exploitation of pluripotent stem cells for regenerative medicine purposes: beyond the T flask. Regen. Med. 2012, 7:71-84.
59. Wang Y., Chou B.K., 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, 11:1103-1116.
60. Wen Y., Yang S.T. Microfibrous carriers for cell culture: a comparative study. Biotechnol. Prog. 2011, 27:1126-1136.
61. Wu S.M., Hochedlinger K. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat. Cell Biol. 2011, 13:497-505.
62. Yang S.T., Luo J., Chen C. A fibrous-bed bioreactor for continuous production of monoclonal antibody by hybridoma. Adv. Biochem. Eng. Biotechnol. 2004, 87:61-96.
63. zur Nieden N.I., Cormier J.T., Rancourt D.E., Kallos M.S. Embryonic stem cells remain highly pluripotent following long term expansion as aggregates in suspension bioreactors. J. Biotechnol. 2007, 129:421-432.
64. Zweigerdt R. Large scale production of stem cells and their derivatives. Adv. Biochem. Eng. Biotechnol. 2009, 114:201-235.
65. Zweigerdt R., Olmer R., Singh H., Haverich A., Martin U. Scalable expansion of human pluripotent stem cells in suspension culture. Nat. Protocol 2011, 6:689-700.