Human embryonic stem cells exhibit increased propensity to differentiate during the G1 phase prior to phosphorylation of retinoblastoma protein

Stem Cells

Volumn 30, Issue 6, 2012, Pages 1097-1108

  Sela, Yogev ^a,b   Molotski, Natali ^b   Golan, Saar ^b   Itskovitz Eldor, Joseph ^a,c   Soen, Yoav ^b  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c Rambam Health Care Campus ^*  (Israel)

Author keywords

Cell cycle phase; Cell density; Centrifugal elutriation; Differentiation; Human embryonic stem cells; Restriction point

Indexed keywords

RETINOBLASTOMA PROTEIN;

ARTICLE; CELL CONTACT; CELL CULTURE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL DENSITY; CELL DIFFERENTIATION; CELL ISOLATION; CELL RENEWAL; CENTRIFUGATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; RETINOBLASTOMA;

CELL CULTURE TECHNIQUES; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; G1 PHASE; HUMANS; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN;

EID: 84861889707     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1078     Document Type: Article

References (34)

1. Pardee AB. A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci USA 1974;71:1286-1290.
2. Zetterberg A, Larsson O. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc Natl Acad Sci USA 1985;82:5365-5369. (Pubitemid 15012107)
3. Blomen VA, Boonstra J. Cell fate determination during G1 phase progression. Cell Mol Life Sci 2007;64:3084-3104. (Pubitemid 351152236)
4. Hui EK, Yung BY. Cell cycle phase-dependent effect of retinoic acid on the induction of granulocytic differentiation in HL-60 promyelocytic leukemia cells. Evidence for sphinganine potentiation of retinoic acid-induced differentiation. FEBS Lett 1993;318:193-199. (Pubitemid 23065952)
5. Clegg CH, Linkhart TA, Olwin BB et al. Growth factor control of skeletal muscle differentiation: Commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J Cell Biol 1987;105:949-956. (Pubitemid 18043854)
6. Mummery CL, van den Brink CE, de Laat SW. Commitment to differentiation induced by retinoic acid in P19 embryonal carcinoma cells is cell cycle dependent. Dev Biol 1987;121:10-19. (Pubitemid 17076825)
7. Stead E, White J, Faast R et al. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 2002;21:8320-8333. (Pubitemid 35477872)
8. Becker KA, Ghule PN, Therrien JA et al. Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J Cell Physiol 2006;209:883-893. (Pubitemid 44665710)
9. Barta T, Vinarsky V, Holubcova Z et al. Human embryonic stem cells are capable of executing G1/S checkpoint activation. Stem Cells 2010; 28:1143-1152.
10. Filipczyk AA, Laslett AL, Mummery C et al. Differentiation is coupled to changes in the cell cycle regulatory apparatus of human embryonic stem cells. Stem Cell Res 2007;1:45-60. (Pubitemid 350251946)
11. Neganova I, Zhang X, Atkinson S et al. Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells. Oncogene 2009;28:20-30.
12. Koledova Z, Kafkova LR, Calabkova L et al. Cdk2 inhibition prolongs G1 phase progression in mouse embryonic stem cells. Stem Cells Dev 2010;19:181-194.
13. Maimets T, Neganova I, Armstrong L et al. Activation of p53 by nutlin leads to rapid differentiation of human embryonic stem cells. Oncogene 2008;27:5277-5287.
14. Wang Y, Baskerville S, Shenoy A et al. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 2008;40:1478-1483.
15. Menchon C, Edel MJ, Izpisua Belmonte JC. The cell cycle inhibitor p27 (Kip1) controls self-renewal and pluripotency of human embryonic stem cells by regulating the cell cycle, Brachyury and Twist. Cell Cycle 2011;10:1435-1447.
16. Yang C, Przyborski S, Cooke MJ et al. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 2008;26:850-863.
17. Conklin JF, Sage J. Keeping an eye on retinoblastoma control of human embryonic stem cells. J Cell Biochem 2009;108:1023-1030.
18. Kallas A, Pook M, Maimets M et al. Nocodazole treatment decreases expression of pluripotency markers Nanog and Oct4 in human embryonic stem cells. PLoS One 2011;6:e19114.
19. Amit M, Itskovitz-Eldor J. Sources, derivation, and culture of human embryonic stem cells. Semin Reprod Med 2006;24:298-303. (Pubitemid 44877572)
20. Dean P, Jett J. Mathematical analysis of DNA distribution derived from flow micro-fluorimetry. Cell Biol 1974;60:523.
21. McEwen CR, Stallard RW, Juhos ET. Separation of biological particles by centrifugal elutriation. Anal Biochem 1968;23:369-377.
22. Banfalvi G. Synchronization of mammalian cells and nuclei by centrifugal elutriation. Methods Mol Biol 2011;761:25-45.
23. Cooper S. Rethinking synchronization of mammalian cells for cell cycle analysis. Cell Mol Life Sci 2003;60:1099-1106. (Pubitemid 36791914)
24. Darr H, Mayshar Y, Benvenisty N. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 2006;133:1193-1201.
25. Becker KA, Stein JL, Lian JB et al. Human embryonic stem cells are pre-mitotically committed to self-renewal and acquire a lengthened G1 phase upon lineage programming. J Cell Physiol 2010;222: 103-110.
26. Heng BC, Liu H, Rufaihah AJ et al. Human embryonic stem cell (hES) colonies display a higher degree of spontaneous differentiation when passaged at lower densities. In Vitro Cell Dev Biol Anim 2006; 42:54-57. (Pubitemid 44264506)
27. Levenstein ME, Ludwig TE, Xu RH et al. Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 2006;24:568-574. (Pubitemid 44464760)
28. Becker KA, Stein JL, Lian JB et al. Establishment of histone gene regulation and cell cycle checkpoint control in human embryonic stem cells. J Cell Physiol 2007;210:517-526. (Pubitemid 44956897)
29. Chambers I, Silva J, Colby D et al. Nanog safeguards pluripotency and mediates germline development. Nature 2007;450:1230-1234.
30. Niwa H. How is pluripotency determined and maintained? Development 2007;134:635-646. (Pubitemid 46437906)
31. Silva J, Smith A. Capturing pluripotency. Cell 2008;132:532-536. (Pubitemid 351253697)
32. Glauche I, Herberg M, Roeder I. Nanog variability and pluripotency regulation of embryonic stem cells - Insights from a mathematical model analysis. PLoS One 2010;5:e11238.
33. Zhang X, Neganova I, Przyborski S et al. A role for NANOG in G1 to S transition in human embryonic stem cells through direct binding of CDK6 and CDC25A. J Cell Biol 2009;184:67-82.
34. Hough SR, Laslett AL, Grimmond SB et al. A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells. PLoS One 2009;4:e7708.