Time-lapse analysis of human embryonic stem cells reveals multiple bottlenecks restricting colony formation and their relief upon culture adaptation

Stem Cell Reports

Volumn 3, Issue 1, 2014, Pages 142-155

  Barbaric, Ivana ^a   Biga, Veronica ^a   Gokhale, Paul J ^a   Jones, Mark ^a   Stavish, Dylan ^a   Glen, Adam ^a   Coca, Daniel ^a   Andrews, Peter W ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CONTACT; CELL DEATH; CELL DENSITY; CELL DIVISION; CELL EXPANSION; CELL FUNCTION; CELL MOTILITY; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; DAUGHTER CELL; EMBRYONIC STEM CELL; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC VARIABILITY; HUMAN; HUMAN CELL; KARYOTYPE; POPULATION GROWTH; PRIORITY JOURNAL; PROGENY; TIME-LAPSE VIDEO MICROSCOPY; CELL CYCLE; CONTROLLED STUDY; STEM CELL CULTURE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; PHYSIOLOGY; TIME LAPSE IMAGING;

CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; TIME-LAPSE IMAGING;

EID: 84904262196     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.05.006     Document Type: Article

References (27)

1. K. Amps, P.W. Andrews, G. Anyfantis, L. Armstrong, S. Avery, H. Baharvand, J. Baker, D. Baker, M.B. Munoz, S. Beil International Stem Cell Initiative Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage Nat. Biotechnol. 29 2011 1132 1144
2. P.W. Andrews, P.N. Goodfellow, L.H. Shevinsky, D.L. Bronson, and B.B. Knowles Cell-surface antigens of a clonal human embryonal carcinoma cell line: morphological and antigenic differentiation in culture Int. J. Cancer 29 1982 523 531 (Pubitemid 12114626)
3. S. Avery, A.J. Hirst, D. Baker, C.Y. Lim, S. Alagaratnam, R.I. Skotheim, R.A. Lothe, M.F. Pera, A. Colman, and P. Robson et al. BCL-XL mediates the strong selective advantage of a 20q11.21 amplification commonly found in human embryonic stem cell cultures Stem Cell Rep. 1 2013 379 386
4. D.E. Baker, N.J. Harrison, E. Maltby, K. Smith, H.D. Moore, P.J. Shaw, P.R. Heath, H. Holden, and P.W. Andrews Adaptation to culture of human embryonic stem cells and oncogenesis in vivo Nat. Biotechnol. 25 2007 207 215 (Pubitemid 46227120)
5. I. Barbaric, P.J. Gokhale, M. Jones, A. Glen, D. Baker, and P.W. Andrews Novel regulators of stem cell fates identified by a multivariate phenotype screen of small compounds on human embryonic stem cell colonies Stem Cell Res. (Amst.) 5 2010 104 119
6. K.A. Becker, P.N. Ghule, J.A. Therrien, J.B. Lian, J.L. Stein, A.J. van Wijnen, and G.S. Stein Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase J. Cell. Physiol. 209 2006 883 893 (Pubitemid 44665710)
7. V.M. Campa, R. Gutiérrez-Lanza, F. Cerignoli, R. Díaz-Trelles, B. Nelson, T. Tsuji, M. Barcova, W. Jiang, and M. Mercola Notch activates cell cycle reentry and progression in quiescent cardiomyocytes J. Cell Biol. 183 2008 129 141
8. G. Chen, Z. Hou, D.R. Gulbranson, and J.A. Thomson Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells Cell Stem Cell 7 2010 240 248
9. P. Dieterich, R. Klages, R. Preuss, and A. Schwab Anomalous dynamics of cell migration Proc. Natl. Acad. Sci. USA 105 2008 459 463 (Pubitemid 351171730)
10. J.S. Draper, C. Pigott, J.A. Thomson, and P.W. Andrews Surface antigens of human embryonic stem cells: changes upon differentiation in culture J. Anat. 200 2002 249 258 (Pubitemid 34467317)
11. J.S. Draper, K. Smith, P. Gokhale, H.D. Moore, E. Maltby, J. Johnson, L. Meisner, T.P. Zwaka, J.A. Thomson, and P.W. Andrews Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells Nat. Biotechnol. 22 2004 53 54 (Pubitemid 38057956)
12. T. Enver, S. Soneji, C. Joshi, J. Brown, F. Iborra, T. Orntoft, T. Thykjaer, E. Maltby, K. Smith, and R. Abu Dawud et al. Cellular differentiation hierarchies in normal and culture-adapted human embryonic stem cells Hum. Mol. Genet. 14 2005 3129 3140 (Pubitemid 41631288)
13. V. Fox, P.J. Gokhale, J.R. Walsh, M. Matin, M. Jones, and P.W. Andrews Cell-cell signaling through NOTCH regulates human embryonic stem cell proliferation Stem Cells 26 2008 715 723
14. N.J. Harrison, D. Baker, and P.W. Andrews Culture adaptation of embryonic stem cells echoes germ cell malignancy Int. J. Androl. 30 2007 275 281 discussion 281 (Pubitemid 47254405)
15. I. Joshi, L.M. Minter, J. Telfer, R.M. Demarest, A.J. Capobianco, J.C. Aster, P. Sicinski, A. Fauq, T.E. Golde, and B.A. Osborne Notch signaling mediates G1/S cell-cycle progression in T cells via cyclin D3 and its dependent kinases Blood 113 2009 1689 1698
16. L.C. Laurent, I. Ulitsky, I. Slavin, H. Tran, A. Schork, R. Morey, C. Lynch, J.V. Harness, S. Lee, and M.J. Barrero et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture Cell Stem Cell 8 2011 106 118
17. L. Li, B.H. Wang, S. Wang, L. Moalim-Nour, K. Mohib, D. Lohnes, and L. Wang Individual cell movement, asymmetric colony expansion, rho-associated kinase, and E-cadherin impact the clonogenicity of human embryonic stem cells Biophys. J. 98 2010 2442 2451
18. R. Metzler, and J. Klafter The random walk's guide to anomalous diffusion: a fractional dynamics approach Phys. Rep. 339 2000 1 77
19. M. Ohgushi, M. Matsumura, M. Eiraku, K. Murakami, T. Aramaki, A. Nishiyama, K. Muguruma, T. Nakano, H. Suga, and M. Ueno et al. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells Cell Stem Cell 7 2010 225 239
20. V. Olariu, N.J. Harrison, D. Coca, P.J. Gokhale, D. Baker, S. Billings, V. Kadirkamanathan, and P.W. Andrews Modeling the evolution of culture-adapted human embryonic stem cells Stem Cell Res. (Amst.) 4 2010 50 56
21. M.D. Rand, L.M. Grimm, S. Artavanis-Tsakonas, V. Patriub, S.C. Blacklow, J. Sklar, and J.C. Aster Calcium depletion dissociates and activates heterodimeric notch receptors Mol. Cell. Biol. 20 2000 1825 1835 (Pubitemid 30100199)
22. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147 (Pubitemid 28516247)
23. A. Walker, H. Su, M.A. Conti, N. Harb, R.S. Adelstein, and N. Sato Non-muscle myosin II regulates survival threshold of pluripotent stem cells Nat. Commun. 1 2010 71
24. K. Watanabe, M. Ueno, D. Kamiya, A. Nishiyama, M. Matsumura, T. Wataya, J.B. Takahashi, S. Nishikawa, S. Nishikawa, K. Muguruma, and Y. Sasai A ROCK inhibitor permits survival of dissociated human embryonic stem cells Nat. Biotechnol. 25 2007 681 686 (Pubitemid 46897207)
25. T.E. Werbowetski-Ogilvie, M. Bossé, M. Stewart, A. Schnerch, V. Ramos-Mejia, A. Rouleau, T. Wynder, M.J. Smith, S. Dingwall, and T. Carter et al. Characterization of human embryonic stem cells with features of neoplastic progression Nat. Biotechnol. 27 2009 91 97
26. G. Xue, and B.A. Hemmings PKB/Akt-dependent regulation of cell motility J. Natl. Cancer Inst. 105 2013 393 404
27. T. Yugawa, K. Nishino, S. Ohno, T. Nakahara, M. Fujita, N. Goshima, A. Umezawa, and T. Kiyono Noncanonical NOTCH signaling limits self-renewal of human epithelial and induced pluripotent stem cells through ROCK activation Mol. Cell. Biol. 33 2013 4434 4447