Simple suspension culture system of human iPS cells maintaining their pluripotency for cardiac cell sheet engineering

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 12, 2015, Pages 1363-1375

  Haraguchi, Yuji ^a   Matsuura, Katsuhisa ^a   Shimizu, Tatsuya ^a   Yamato, Masayuki ^a   Okano, Teruo ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Agitation rate; Cardiac differentiation; Cell sheet engineering; Embryoid body; Human iPS cells; Suspension culture

Indexed keywords

BOTTLES; CELL CULTURE; CELL ENGINEERING; GENE EXPRESSION; HEART; STEM CELLS; SUSPENSIONS (COMPONENTS); SUSPENSIONS (FLUIDS); TISSUE; TISSUE ENGINEERING;

AGITATION RATES; CARDIAC DIFFERENTIATION; CELL SHEET ENGINEERING; CELL-BE; CELL/B.E; EMBRYOID BODY; HUMAN IPS CELL; HUMAN-INDUCED PLURIPOTENT STEM CELLS; IPS CELLS; SUSPENSION CULTURES;

AGGREGATES;

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2;

ARTICLE; BEATING CARDIOMYOCYTE; CELL AGGREGATION; CELL COUNT; CELL DIFFERENTIATION; CELL ENGINEERING; CELL EXPANSION; CELL SHEET ENGINEERING; CELL SUSPENSION; CELL VIABILITY; CELLULAR PARAMETERS; CONTROLLED STUDY; CULTURE TECHNIQUE; ECTODERM; ENDODERM; FLOW CYTOMETRY; GENE; GENE EXPRESSION; HCN4 GENE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN INDUCED PLURIPOTENT STEM CELL; IMMUNOCYTOCHEMISTRY; MCL 2V GENE; MESODERM; MLC 2 ALPHA GENE; MOLECULAR DYNAMICS; PLURIPOTENCY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REGENERATIVE MEDICINE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; SIMPLE THREE DIMENSIONAL SUSPENSION CULTURE SYSTEM; SINGLE CELL SUSPENSION; TISSUE ENGINEERING; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL LINE; CYTOLOGY; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PROCEDURES;

CELL DIFFERENTIATION; CELL LINE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCARDIUM; MYOCYTES, CARDIAC; TISSUE ENGINEERING;

EID: 84952873506     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1761     Document Type: Article

References (50)

1. Amit M, Laevsky I, Miropolsky Y, et al. 2011; Dynamic suspension culture for scalable expansion of undifferentiated human pluripotent stem cells. Nat Protoc 6: 572-579.
2. Bauwens CL, Peerani R, Niebruegge S, et al. 2008; Control of human embryonic stem cell colony and aggregatesize heterogeneity influences differentiation trajectories. Stem Cells 26: 2300-2310.
3. Boheler KR, Czyz J, Tweedie D, et al. 2002; Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91: 189-201.
4. 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.
5. Chen VC, Couture SM, Ye J, et al. 2012; Scalable GMP compliant suspension culture system for human ES cells. Stem Cell Res 8: 388-402.
6. Fluri DA, Tonge PD, Song H, et al. 2012; Derivation, expansion and differentiation of induced pluripotent stem cells in continuous suspension cultures. Nat Methods 9: 509-516.
7. 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.
8. Graichen R, Xu X, Braam SR, et al. 2008; Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 76: 357-370.
9. Haraguchi Y, Shimizu T, Sasagawa T, et al. 2012a; Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro. Nat Protoc 7: 850-858.
10. Haraguchi Y, Shimizu T, Yamato M, et al. 2012b; Cell therapy and tissue engineering for cardiovascular disease. Stem Cells Trans Med 1: 136-141.
11. Haraguchi Y, Shimizu T, Yamato M, et al. 2006; Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27: 4765-4774.
12. Ishii TM, Takano M, Xie L-H, et al. 1999; Molecular characterization of the hyperpolarization-activated cation channel in rabbit heart sinoatrial node. J Biol Chem 274: 12835-12839.
13. Kehat I, Kenyagin-Karsenti D, Snir M, et al. 2001; Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108: 407-414.
14. Kehoe DE, Jing D, Lock LT, et al. 2010; Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng Part A 16: 405-421.
15. Kelly WJ. 2008; Using computational fluid dynamics to characterize and improve bioreactor performance. Biotechnol Appl Biochem 49: 225-238.
16. Khademhosseini A, Ferreira L, Blumling J, et al. 2006; Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials 27: 5968-5977.
17. Lin B, Kim J, Li Y, et al. 2012; High-purity enrichment of functional cardiovascular cells from human iPS cells. Cardiovasc Res 95: 327-335.
18. Lock LT, Tzanakakis ES. 2009; Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture. Tissue Eng Part A 15: 2051-2063.
19. Ludwig TE, Levenstein ME, Jones JM, et al. 2006; Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24, 185-187.
20. Masumoto H, Matsuo T, Yamamizu K, et al. 2012; Pluripotent stem cell-engineered cells sheets reassembled with defined cardiovascular populations ameliorates reduction in infarct heart function through cardiomyocyte-mediated neovascularization. Stem Cell 30: 1196-1205.
21. Matsuura K, Honda T, Nagai T, et al. 2009; Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest 119: 2204-2217.
22. Matsuura K, Masuda S, Haraguchi Y, et al. 2011; Creation of mouse embryonic stem cell-derived cardiac cell sheets. Biomaterials 32: 7355-7362.
23. Matsuura K, Wada M, Shimizu T, et al. 2012; Creation of human cardiac cell sheets using pluripotent stem cells. Biochem Biophys Res Commun 425: 321-327.
24. Mohr JC, de Pablo JJ, Palecek SP. 2006; 3D microwell culture of human embryonic stem cells. Biomaterials 27: 6032-6042.
25. Mummery C, Ward-van Oostwaard D, Doevendans P, et al. 2003; Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107: 2733-2740.
26. Nakagawa M, Koyanagi M, Tanabe K, et al. 2008; Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26: 101-106.
27. Ng ES, Davis RP, Azzola L, et al. 2005; Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106: 1601-1603.
28. O'Brien C, Laslett AL. 2012; Suspended in culture - human pluripotent cells for scalable technologies. Stem Cell Res 9: 167-170.
29. Okano T, Yamada H, Sakai H, et al. 1993; A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly(N-isopropylacrylamide). J Biomed Mater Res 27: 1243-1251.
30. Olivetti G, Melissari M, Capasso JM, et al. 1991; Cardiomyopathy for the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circ Res 68: 1560-1568.
31. Paige SL, Osugi T, Afanasiev OK, et al. 2010; Endogenous Wnt/β-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 5: e11134.
32. Rungarunlert S, Techakumphu M, Pirity MK, et al. 2009; Embryoid body formation from embryonic and induced pluripotent stem cells: benefits of bioreactors. World J Stem Cells 1: 11-21.
33. Sasaki D, Shimizu T, Masuda S, et al. 2009; Mass preparation of size-controlled mouse embryonic stem cell aggregates and induction of cardiac differentiation by cell patterning method. Biomaterials 30: 4384-4389.
34. Sawa Y, Miyagawa S, Sakaguchi T, et al. 2012; Tissue engineered myoblast sheets improved cardiac function sufficiently to discontinue LVAS in a patient with DCM: report of a case. Surg Today 42: 181-184.
35. Sekine H, Shimizu T, Sakaguchi K, et al. 2013; In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat Commun 4: 1399.
36. Sekine W, Haraguchi Y, Shimizu T, et al. 2011; Thickness limitation and cell viability of multi-layered cell sheets and overcoming the diffusion limit by a porous-membrane culture insert. J Biochip Tissue Chip S1: 007.
37. Shimizu T, Yamato M, Isoi Y, et al. 2002; Fabrication of pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90, e40-48.
38. Shimizu T, Sekine H, Yamato M, et al. 2009; Cell sheet-based myocardial tissue engineering: new hope for damaged heart rescue. Curr Pharm Des 15: 2807-2814.
39. Singh H, Mok P, Balakrishnan T, et al. 2010; Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. Stem Cell Res 4: 165-179.
40. Takahashi K, Tanabe K, Ohnuki M, et al. 2007; Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
41. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. 1998; Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
42. Ungrin MD, Joshi C, Nica A, et al. 2008; Reproducible, ultra-high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS One 3: e1565.
43. Want AJ, Nienow AW, Hewitt CJ, et al. 2012; Large-scale expansion and exploitation of pluripotent stem cells for regenerative medicine purposes: beyond the T flask. Regen Med 7: 71-84.
44. Watanabe K, Ueno M, Kamiya D, et al. 2007; A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25: 681-686.
45. 2+ channel blockers. Differentiation 48: 173-182.
46. Yamada N, Okano T, Sakai H, et al. 1990; Thermo-responsive polymeric surface: control of attachment and detachment of cultured cells. Makromol Chem Rapid Commun 11: 571-576.
47. + embryonic stem cell-derived population. Nature 453: 524-528.
48. Yu J, Vodyanik MA, Smuga-Otto K, et al. 2007; Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
49. Zweigerdt R. 2009; Large scale production of stem cells and their derivatives. Adv Biochem Eng Biotechnol 114: 201-235.
50. Zweigerdt R, Olmer R, Singh H, et al. 2011; Scalable expansion of human pluripotent stem cells in suspension culture. Nat Protoc 6: 689-700.