Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates

PLoS ONE

Volumn 3, Issue 2, 2008, Pages

  Ungrin, Mark D ^a   Joshi, Chirag ^a   Nica, Andra ^a   Bauwens, Céline ^a,b   Zandstra, Peter W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL FATE; CELL SUSPENSION; CENTRIFUGATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; HEART MUSCLE CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; MORPHOGENESIS; NERVE CELL; REPRODUCIBILITY; ULTRA HIGH THROUGHPUT CENTRIFUGAL FORCED AGGREGATION; CELL SEPARATION; CULTURE TECHNIQUE; CYTOLOGY; METHODOLOGY; MULTICELLULAR SPHEROID; TISSUE ENGINEERING;

CELL CULTURE TECHNIQUES; CELL SEPARATION; EMBRYONIC STEM CELLS; HUMANS; MORPHOGENESIS; SPHEROIDS, CELLULAR; TISSUE ENGINEERING;

EID: 45349084219     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001565     Document Type: Article

References (65)

1. Gilbert SF (2000) Early Mammalian Development. In: Gilbert SF. Developmental Biology. Sinauer Associates Inc. Available: http://www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=dbio.section.2609 Accessed 8 September, 2007.
2. Wells JM, Melton DA (2000) Early mouse endoderm is patterned by soluble factors from adjacent germ layers. Development 127: 1563-1572.
3. Ingber DE (2006) Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 50: 255-266.
4. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
5. Eakin GS, Behringer RR (2004) Diversity of germ layer and axis formation among mammals. Semin Cell Dev Biol 15: 619-629.
6. Langer R, Vacanti JP (1993) Tissue engineering. Science 260: 920-926.
7. Wang L, Menendez P, Shojaei F, Li L, Mazurier F, et al. (2005) Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 201: 1603-1614.
8. Raikwar SP, Mueller T, Zavazava N (2006) Strategies for developing therapeutic application of human embryonic stem cells. Physiology (Bethesda) 21: 19-28.
9. Ingber DE, Levin M (2007) What lies at the interface of regenerative medicine and developmental biology? Development 134: 2541-2547.
10. Blum B, Benvenisty N (2007) Clonal Analysis of Human Embryonic Stem Cell Differentiation into Teratomas. Stem Cells 25: 1924-1930.
11. Itskovitz-Eldor J, Schuldiner M, Karsenti D, Eden A, Yanuka O, et al. (2000) Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers, Mol Med 6: 88-95.
12. Keller GM (1995) In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol 7: 862-869.
13. Dang SM, Kyba M, Perlingeiro R, Daley GQ, Zandstra PW (2002) Efficiency of embryoid body formation and hematopoietic development from embryonic stem cells in different culture systems. Biotechnol Bioeng 78: 442-453.
14. Kurosawa H, Imamura T, Koike M, Sasaki K, Amano Y (2003) A simple method for furming embryoid body from mouse embryonic stem cells. J Biosci Bioeng 96: 409-411.
15. Fok EYL, Zandstra PW (2005) Shear-controlled single-step mouse embryonic stem cell expansion and embryoid body-based differentiation. Stem Cells 23: 1333-1342.
16. Koike M, Kurosawa H, Amano Y (2005) A round-bottom 96-well polystyrene plate coated with 2-methacryloyloxyethylphosphorylcholine as an effective tool for embryoid body formation. Cytotechnology 47: 3-10.
17. Weitzer G (2006) Embryonic stem cell-derived embryoid bodies: an in vitro model of eutherian pregastrulation development and early gastrulation. Handh Exp Pharmacol 174: 21-51.
18. Walters MJ, Wayman GA, Christian JL (2001) Bone morphogenetic protein function is required for terminal differentiation of the heart but not for early expression of cardiac marker genes. Mech Dev 100: 263-273.
19. Schohl A, Fagotto F (2003) A role for maternal beta-catenin in early mesoderm induction in Xenopus. EMBO J 22: 3303-3313.
20. Duboc V, Röttinger E, Besnardeau L, Lepage T (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6: 397-410.
21. Herzog W, Sonntag C, von der Hardt S, Roehl HH, Varga ZM, et al. (2004) Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis. Development 131: 3681-3692.
22. Chu J, Ding J, Jeays-Ward K, Price SM, Placzek M, et al. (2005) Non-cell-autonomous role for Cripto in axial midline formation during vertebrate embryogenesis. Development 132: 5539-5551.
23. Chen SS, Fitzgerald W, Zimmerberg J, Kleinman HK, Margolis L (2007) Cell-cell and cell-extracellular matrix interactions regulate embryonic stem cell differentiation. Stem Cells 25: 553-561.
24. Nussbaum J, Minami E, Laflamme MA, Virag JAI, Ware CB, et al. (2007) Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASER J 21: 1345-1357.
25. Dang SM, Gerecht-Nir S, Chen J, Itskovitz-Eldor J, Zandstra PW (2004) Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 22: 275-282.
26. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, et al. (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123: 917-929.
27. Coucouvanis E, Martin GR (1999) BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126: 535-546.
28. Li L, Arman E, Ekbbom P, Edgar D, Murray P, et al. (2004) Distinct GATA6- and laminin-dependent mechanisms regulate endodermal and ectodermal embryonic stem cell fates. Development 131: 5277-5286.
29. Conley BJ, Trounson AO, Mollard R (2004) Human embryonic stem cells form embryoid bodies containing visceral endoderm-like derivatives. Fetal Diagn Ther 19: 218-223.
30. Coucouvanis E, Martin GR (1995) Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83: 279-287.
31. Li X, Chen Y, Schéele S, Arman E, Haffner-Krausz R, et al. (2001) Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J Cell Biol 153: 811-822.
32. Conley B, Ellis S, Gulluyan L, Mollard R (2007) BMPs regulate differentiation of a putative visceral endoderm layer within human embryonic stem-cell-derived embryoid bodies. Biochem Cell Biol 85: 121-132.
33. Yoon BS, Yoo SJ, Lee JE, You S, Lee HT, et al. (2006) Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation 74: 149-159.
34. Ng ES, Davis RP, Azzola L, Stanley EG, Elefanty AG (2005) Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106: 1601-1603.
35. Peerani R, Rao BM, Bauwens C, Yin T, Wood GA, et al. (2007) Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J 26: 4744-4755.
36. Burridge PW, Anderson D, Priddle H, Barbadillo-Muñoz MD, Chamberlain S, et al. (2007) Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte diffierentiation from a novel V-96 plate aggregation system highlights inter-line variability. Stem Cells 25: 929-938.
37. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, et al. (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25: 681-686.
38. Bauwens C, Yin T, Dang S, Peerani R, Zandstra PW (2005) Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: oxygen-mediated enhancement of cardiomyocyte output. Biotechnol Bioeng 90: 452-461.
39. Hirashima M, Bernstein A, Stanford WL, Rossant J (2004) Gene-trap expression screening to identify endothelial-specific genes. Blood 104: 711-718.
40. Seiler A, Visan A, Buesen R, Genschow E, Spielmann H (2004) Improvement of an in vitro stem cell assay for developmental toxicity: the use of molecular endpoints in the embryonic stem cell test. Reprod Toxicol 18: 231-240.
41. Sohn SK, Kim JG, Kim DH, Lee NY, Suh JS, et al. (2003) Impact of transplanted CD34+ cell dose in allogeneic unmanipulated peripheral blood stem cell transplantation. Bone Marrow Transplant 31: 967-972.
42. Laflamme MA, Murry CE (2005) Regenerating the heart. Nat Biotechnol 23: 845-856.
43. Bruder JM, Monu NC, Harrison MW, Hoffman-Kim D (2006) Fabrication of polymeric replicas of cell surfaces with nanoscale resolution. Langmuir 22: 8266-8270.
44. Mohr JC, de Pablo JJ, Palecek SP (2006) 3-D microwell culture of human embryonic stem cells. Biomaterials 27: 6032-6042.
45. Khademhosseini A, Ferreira L, Blumling J, Yeh J, Karp JM, et al. (2006) Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials 27: 5968-5977.
46. Kovacs GTA, Maluf NI, Petersen KE (1998) Bulk micromachining of silicon. Proceedings of the IEEE 86: 1536-1551.
47. Vallier L, Alexander M, Pedersen RA (2005) Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118: 4495-4509.
48. Rossant J, Chazaud C, Yamanaka Y (2003) Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 358: 1341-8.
49. Chazaud C, Yamanaka Y, Pawson T, Rossant J (2006) Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 10: 615-624.
50. Mesnard D, Guzman-Ayala M, Constam DB (2006) Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133: 2497-2505.
51. Lazarevich NL (2000) Molecular mechanisms of alpba-fetoprotein gene expression. Biochemistry (Mosc) 65: 117-133.
52. Perea-Gómez A, Shawlot W, Sasaki H, Behringer RR, Ang S (1999) HNF3beta and Lim1 interact in the visceral endoderm to regulate primitive streak formation and anterior-posterior polarity in the mouse embryo. Development 126: 4499-4511.
53. Kimura-Yoshida C, Tian E, Nakano H, Amazaki S, Shimokawa K, et al. (2007) Crucial roles of Foxa2 in mouse anterior-posterior axis polarization via regulation of anterior visceral endoderm-specific genes. Proc Natl Acad Sci U S A 104: 5919-5924.
54. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, et al. (2002) Depletion of definitive gut endoderm in Sox17-null mutant riiice. Development 129: 2367-2379.
55. Goldflirb M, Bates B, Drucker B, Hardin J, Haub O (1991) Expression and possible functions of the FGF-5 gene. Ann N Y Acad Sci 638: 38-52.
56. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, et al. (2005) Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23: 1534-1541.
57. Joannides AJ, Fiore-Hériché C, Battersby AA, Athauda-Arachchi P, Boubon IA, et al. (2007) A scaleable and defined system for generating neural stem cells from human embryonic stem cells. Stem Cells 25: 731-737.
58. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
59. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JI, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
60. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, et al. (2001) Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19: 971-974.
61. 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.
62. Ungrin M, O'Connor M, Eaves C, Zandstra PW (2007) Phenotypic analysis of human embryonic stem cells. Curr Protoc Stem Cell Biol 2: 1B.3.1-1B.3.25.
63. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, et al. (2003) Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915.
64. Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29: e45.
65. Wang X, Seed B (2003) A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 31: e154.