Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: Oxygen-mediated enhancement of cardiomyocyte output

Biotechnology and Bioengineering

Volumn 90, Issue 4, 2005, Pages 452-461

  Bauwens, Céline ^a,b   Yin, Ting ^b   Dang, Stephen ^a,b   Peerani, Raheem ^b   Zandstra, Peter W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bioreactor design; Cardiomyocytes; Oxygen; Stem cells; Tissue engineering

Indexed keywords

BIOLOGICAL ORGANS; BIOREACTORS; CARDIOLOGY; CELLS; DISEASES; HYDROGELS; MATHEMATICAL MODELS; MEDICAL APPLICATIONS;

CARDIOMYOCYTES; CELL TRANSPLANTATION; EMBRYONIC STEM (ES) CELLS; MYOCARDIUM;

TRANSPLANTATION (SURGICAL);

DISSOLVED OXYGEN;

ANIMAL TESTING REFINEMENT; ARTICLE; BIOREACTOR; CELL AGGREGATION; CELL POPULATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENETIC SELECTION; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPOXIA; MUSCLE DEVELOPMENT; OXYGEN TENSION; PERFUSION FED BIOREACTOR; PROCESS OPTIMIZATION; PRODUCTIVITY;

ANIMALS; BIOREACTORS; CELL DIFFERENTIATION; EMBRYO; MICE; MYOCYTES, CARDIAC; OXYGEN; PERFUSION; STEM CELLS;

ANIMALIA;

EID: 20344382984     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20445     Document Type: Article

References (43)

1. Adelman DM, Maltepe E, Simon MC. 1999. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes Dev 13:2478-2483.
2. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM. 2002. Differentiation of plurjpotent embryonic stem cells into cardiomyocytes. Circ Res 91:189-201.
3. Caldwell J, Palsson BO, Locey B, Emerson SG. 1991. Culture perfusion schedules influence the metabolic activity and granulocyte-macrophage colony-stimulating factor production rates of human bone marrow stromal cells. J Cell Physiol 147:344-353.
4. Czyz J, Wobus A. 2001. Embryonic stem cell differentiation: the role of extracellular factors. Differentiation 68:167-174.
5. Dang S, Kyba M, Perlingeiro R, Daley G, Zandstra P. 2002. Efficiency of embryoid body formation and hematopoietic development from embryonic stem cells in different culture systems. Biotechnol Bioeng 78: 442-453.
6. Dang SM, Gerecht-Nir S, Chen J, Itskovitz-Eldor J, Zandstra P. 2004. Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 22:275-282.
7. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. 1985. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87:27-45.
8. Doevendans PA, Kubalak SW, An RH, Becker DK, Chien KR, Kass RS. 2000. Differentiation of cardiomyocytes in floating embryoid bodies is comparable to fetal cardiomyocytes. J Mol Cell Cardiol 32:839-851.
9. Erdo F, Buhrle C, Blunk J, Hoehn M, Xia Y, Fleischmann B, Focking M, Kustermann E, Kolossov E, Hescheler J, et al. 2003. Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J Cereb Blood Flow Metab 23:780-785.
10. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156.
11. Gassmann M, Fandrey J, Bichet S, Wartenberg M, Marti HH, Bauer C, Wenger RH, Acker H. 1996. Oxygen supply and oxygen-dependent gene expression in differentiating embryonic stem cells. Proc Natl Acad Sci U S A 93:2867-2872.
12. Gulbins H, Meiser BM, Reichenspurner H, Reichart B. 2002. Cell transplantation - a potential therapy for cardiac repair in the future? Heart Surg Forum 5:E28-34.
13. Hescheler J, Fleischmann BK, Wartenberg M, Bloch W, Kolossov E, Ji G, Addicks K, Sauer H. 1999. Establishment of ionic channels and signalling cascades in the embryonic stem cell-derived primitive endoderm and cardiovascular system. Cells Tissues Organs 165:153-164.
14. Hilberg F, Wagner EF. 1992. Embryonic stem (ES) cells lacking functional c-jun: consequences for growth and differentiation, AP-1 activity and tumorigenicity. Oncogene 7:2371-2380.
15. Johkura K, Cui L, Suzuki A, Teng R, Kamiyoshi A, Okamura S, Kubota S, Zhao X, Asanuma K, Okouchi Y, et al. 2003. Survival and function of mouse embryonic stem cell-derived cardiomyocytes in ectopic transplants. Cardiovasc Res 58:435-443.
16. Kehat I, Gepstein L. 2003. Human embryonic stem cells for myocardial regeneration. Heart Fail Rev 8:229-236.
17. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Itskovitz-Eldor J, Gepstein L. 2001. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108:407-414.
18. Klug MG, Soonpaa MH, Field LJ. 1995. DNA synthesis and multinucleation in embryonic stem cell-derived cardiomyocytes. Am J Physiol 269:H1913-1921.
19. Klug MG, Soonpaa MH, Koh GY, Field LJ. 1996. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J Clin Invest 98:216-224.
20. Koller MR, Bender JG, Miller WM, Papoutsakis ET. 1993a. Expansion of primitive human hematopoietic progenitors in a perfusion bioreactor system with IL-3, IL-6, and stem cell factor. Biotechnology (NY) 11:358-363.
21. Koller MR, Emerson SG, Palsson BO. 1993b. Large-scale expansion of human stem and progenitor cells from bone marrow mononuclear cells in continuous perfusion cultures. Blood 82:378-384.
22. Koller MR, Bradley MS, Palsson BO. 1995. Growth factor consumption and production in perfusion cultures of human bone marrow correlate with specific cell production. Exp Hematol 23:1275-1283.
23. Li M, Pevny L, Lovell-Badge R, Smith A. 1998. Generation of purified neural precursors from embryonic stem cells by lineage selection. Curr Biol 8:971-974.
24. Lopez-Sanchez C, Climent V, Schoenwolf GC, Alvarez IS, Garcia-Martinez V. 2002. Induction of cardiogenesis by Hensen's node and fibroblast growth factors. Cell Tissue Res 309:237-249.
25. Lough J, Barron M, Brogley M, Sugi Y, Bolender DL, Zhu X. 1996. Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. Dev Biol 178:198-202.
26. Magyar JP, Nemir M, Ehler E, Suter N, Perriard JC, Eppenberger HM. 2001. Mass production of embryoid bodies in microbeads. Ann N Y Acad Sci 944:135-143.
27. Maltsev VA, Rohwedel J, Hescheler J, Wobus AM. 1993. Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44:41-50.
28. Marchetti S, Gimond C, Iljin K, Bourcier C, Alitalo K, Pouyssegur J, Pages G. 2002. Endothelial cells genetically selected from differentiating mouse embryonic stem cells incorporate at sites of neovascularization in vivo. J Cell Sci 115:2075-2085.
29. Nakayama N, Lee J, Chiu L. 2000. Vascular endothelial growth factor synergistically enhances bone morphogenetic protein-4-dependent lymphohematopoietic cell generation from embryonic stem cells in vitro. Blood 95:2275-2283.
30. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P. 2001a. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938:221-229; discussion 229-230.
31. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM and others. 2001b. Bone marrow cells regenerate infarcted myocardium. Nature 410:701-705.
32. Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, Huard J. 2002. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 110:751-759.
33. Ramirez-Bergeron DL, Simon MC. 2001. Hypoxia-inducible factor and the development of stem cells of the cardiovascular system. Stem Cells 19:279-286.
34. Ryan C, Nguyen BT, Sullivan SJ. 1995. Rapid assay for mycobacterial growth and antibiotic susceptibility using gel microdrop encapsulation. J Clin Microbiol 33:1720-1726.
35. Sachinidis A, Kolossov E, Fleischmann BK, Hescheler J. 2002. Generation of cardiomyocytes from embryonic stem cells experimental studies. Herz 27:589-597.
36. Sachinidis A, Fleischmann BK, Kolossov E, Wartenberg M, Sauer H, Hescheler J. 2003. Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc Res 58:278-291.
37. Semenza GL. 2001. Regulation of hypoxia-induced angiogenesis: a chaperone escorts VEGF to the dance. J Clin Invest 108:39-40.
38. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. 1996. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271:H2183-189.
39. Taylor DA, Atkins BZ, Hungspreugs P, Jones TR, Reedy MC, Hutcheson KA, Glower DD, Kraus WE. 1998. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 4:929-933.
40. Van Zant G, Rummel SA, Koller MR, Larson DB, Drubachevsky I, Palsson M, Emerson SG. 1994. Expansion in bioreactors of human progenitor populations from cord blood and mobilized peripheral blood. Blood Cells 20:482-490; discussion 491.
41. Xu C, Police S, Rao N, Carpenter MK. 2002. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91:501-508.
42. Zandstra PW, Bauwens C, Yin T, Liu Q, Schiller H, Zweigerdt R, Pasumarthi KBS, Field LJ. 2003. Scalable production of embryonic stem cell-derived cardiomyocytes. Tissue Eng 9:767-778.
43. Zweigerdt R, Burg M, Willbold E, Abts H, Ruediger M. 2003. Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy 5:399-413.