The microwell control of embryoid body size in order to regulate cardiac differentiation of human embryonic stem cells

Biomaterials

Volumn 31, Issue 7, 2010, Pages 1885-1893

  Mohr, Jeffrey C ^a,c   Zhang, Jianhua ^b,c   Azarin, Samira M ^a,c   Soerens, Andrew G ^b,c   de Pablo, Juan J ^a   Thomson, James A ^b,c   Lyons, Gary E ^b   Palecek, Sean P ^a,c   Kamp, Timothy J ^b,c  

^a University of Wisconsin Madison   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c WiCell Research Institute   (United States)

Author keywords

Cardiomyocytes; Differentiation; Embryoid body; Human embryonic stem cells; Microwells

Indexed keywords

CARDIAC DIFFERENTIATION; CARDIOGENESIS; CARDIOMYOCYTES; DISAGGREGATION TECHNIQUES; EMBRYOID BODY; HUMAN EMBRYONIC STEM CELLS; IMMUNOLABELING; LATERAL DIMENSION; MICROWELLS; MYOSIN LIGHT CHAINS; THERAPEUTIC APPLICATION; UNIFORM-SIZED;

CELL CULTURE; CELL GROWTH; FLOW CYTOMETRY; MICROCHANNELS;

STEM CELLS;

MYOSIN LIGHT CHAIN 2; MYOSIN LIGHT CHAIN 2A; UNCLASSIFIED DRUG;

ARTICLE; BIOENGINEERING; BODY SIZE; CELL CULTURE; CELL DIFFERENTIATION; CELL FRACTIONATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; HEART DEVELOPMENT; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; REPRODUCIBILITY;

CELL COUNT; CELL DIFFERENTIATION; CELL LINE; CELL SIZE; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MYOCYTES, CARDIAC; MYOSIN LIGHT CHAINS; ORGANOGENESIS; TIME FACTORS;

EID: 73249125581     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.11.033     Document Type: Article

References (45)

1. Odorico J.S., Kaufman D.S., and Thomson J.A. Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19 (2001) 193-204
2. Watt F.M., and Hogan B.L. Out of Eden: stem cells and their niches. Science 287 (2000) 1427-1430
3. Spradling A., Drummond-Barbosa D., and Kai T. Stem cells find their niche. Nature 414 (2001) 98-104
4. Streuli C. Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol 11 (1999) 634-640
5. Mummery C., Ward-van Oostwaard D., Doevendans P., Spijker R., van den B.S., Hassink R., et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107 (2003) 2733-2740
6. Laflamme M.A., Chen K.Y., Naumova A.V., Muskheli V., Fugate J.A., Dupras S.K., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25 (2007) 1015-1024
7. Schuldiner M., Yanuka O., Itskovitz-Eldor J., Melton D.A., and Benvenisty N. From the cover: effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 97 (2000) 11307-11312
8. Itskovitz-Eldor J., Schuldiner M., Karsenti D., Eden A., Yanuka O., Amit M., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 6 (2000) 88-95
9. Dvash T., and Benvenisty N. Human embryonic stem cells as a model for early human development. Best Pract Res Clin Obstet Gynaecol 18 (2004) 929-940
10. Tian X., Morris J.K., Linehan J.L., and Kaufman D.S. Cytokine requirements differ for stroma and embryoid body-mediated hematopoiesis from human embryonic stem cells. Exp Hematol 32 (2004) 1000-1009
11. Wang L., Li L., Shojaei F., Levac K., Cerdan C., Menendez P., et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21 (2004) 31-41
12. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453 (2008) 524-528
13. Doetschman T.C., Eistetter H., Katz M., Schmidt W., and Kemler R. 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 (1985) 27-45
14. Boheler K.R., Czyz J., Tweedie D., Yang H.T., Anisimov S.V., and Wobus A.M. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91 (2002) 189-201
15. Singla D.K., Jayaraman S., Zhang J., and Kamp T.J. Cardiomyocyte derivation from human embryonic stem cells. In: Master J.R., Palsson B.O., and Thomson J.A. (Eds). Human cell culture 6: embryonic stem cells (2007), Springer-Verlag, New York 211-234
16. Xu C., Police S., Rao N., and Carpenter M.K. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91 (2002) 501-508
17. He J.-Q., January C.T., Thomson J., and Kamp T.J. Human embryonic stem cell-derived cardiomyocytes: drug discovery and safety pharmacology. Expert Opin Drug Discov 2 (2007) 39-753
18. Segev H., Kenyagin-Karsenti D., Fishman B., Gerecht-Nir S., Ziskind A., Amit M., et al. Molecular analysis of cardiomyocytes derived from human embryonic stem cells. Dev Growth Differ 47 (2005) 295-306
19. Burridge P.W., Anderson D., Priddle H., Barbadillo M., Chamberlain S., Allegrucci C., et al. Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells 25 (2007) 929-938
20. Reubinoff B.E., Pera M.F., Fong C.Y., Trounson A., and Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18 (2000) 399-404
21. Ng E.S., Davis R.P., Azzola L., Stanley E.G., and Elefanty A.G. Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106 (2005) 1601-1603
22. Bauwnes C.L., Peerani R., Niebruegge S., Woodhouse K.A., Kumacheva E., Husain M., et al. Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26 (2008) 2300-2310
23. Peerani R., Rao B.M., Bauwens C., Yin T., Wood G.A., Nagy A., et al. Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J 26 (2007) 4744-4755
24. Ungrin M.D., Joshi C., Nica A., Bauwens C., and Zandstra P.W. Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS ONE 3 (2008) e1565
25. Mohr J.C., de Pablo J.J., and Palecek S.P. 3-D microwell culture of human embryonic stem cells. Biomaterials 27 (2006) 6032-6042
26. Khademhosseini A., Ferreira L., Blumling III J., Yeh J., Karp J.M., Fukuda J., et al. Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials 27 (2006) 5968-5977
27. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001) 402-408
28. Kubalak S.W., Miller-Hance W.C., O'Brien T.X., Dyson E., and Chien K.R. Chamber specification of atrial myosin light chain-2 expression precedes septation during murine cardiogenesis. J Biol Chem 269 (1994) 16961-16970
29. Kehat I., Kenyagin-Karsenti D., Snir M., Segev H., Amit M., Gepstein A., et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108 (2001) 407-414
30. He J.Q., Ma Y., Lee Y., Thomson J.A., and Kamp T.J. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res 93 (2003) 32-39
31. Osafune K., Caron L., Borowiak M., Martinez R.J., Fitz-Gerald C.S., Sato Y., et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26 (2008) 313-315
32. Tomescot A., Leschik J., Bellamy V., Dubois G., Messas E., Bruneval P., et al. Differentiation in vivo of cardiac committed human embryonic stem cells in postmyocardial infarcted rats. Stem Cells 25 (2007) 2200-2205
33. Rudy-Reil D., and Lough J. Avian precardiac endoderm/mesoderm induces cardiac myocyte differentiation in murine embryonic stem cells. Circ Res 94 (2004) e107-e116
34. Schultheiss T.M., Burch J.B., and Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev 11 (1997) 451-462
35. Sugi Y., and Lough J. Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev Dyn 200 (1994) 155-162
36. Climent S., Sarasa M., Villar J.M., and Murillo-Ferrol N.L. Neurogenic cells inhibit the differentiation of cardiogenic cells. Dev Biol 171 (1995) 130-148
37. Cohen E.D., Tian Y., and Morrisey E.E. Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development 135 (2008) 789-798
38. Wagner M., and Siddiqui M.A. Signal transduction in early heart development (I): cardiogenic induction and heart tube formation. Exp Biol Med (Maywood) 232 (2007) 852-865
39. Conley B.J., Trounson A.O., and Mollard R. Human embryonic stem cells form embryoid bodies containing visceral endoderm-like derivatives. Fetal Diagn Ther 19 (2004) 218-223
40. Coucouvanis E., and Martin G.R. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83 (1995) 279-287
41. Li X., Chen Y., Scheele S., Arman E., Haffner-Krausz R., Ekblom P., et al. Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J Cell Biol 153 (2001) 811-822
42. Conley B.J., Ellis S., Gulluyan L., and Mollard R. BMPs regulate differentiation of a putative visceral endoderm layer within human embryonic stem-cell-derived embryoid bodies. Biochem Cell Biol 85 (2007) 121-132
43. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318 (2007) 1917-1920
44. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131 (2007) 861-872
45. Zhang J., Wilson G.F., Soerens A.G., Koonce C.H., Yu J., Palecek S.P., et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104 (2009) e30-e41