Controlling embryonic stem cell proliferation and pluripotency: The role of PI3K- and GSK-3-dependent signalling

Biochemical Society Transactions

Volumn 39, Issue 2, 2011, Pages 674-678

  Welham, Melanie J ^a   Kingham, Emmajayne ^a,b   Sanchez Ripoll, Yolanda ^a   Kumpfmueller, Benjamin ^a   Storm, Michael ^a   Bone, Heather ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Cell cycle; Embryonic stem cell; Glycogen synthase kinase 3 (GSK 3); Phosphoinositide 3 kinase (PI3K); Pluripotency; Proliferation; Self renewal

Indexed keywords

CYCLIN DEPENDENT KINASE 2; GLYCOGEN SYNTHASE KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA;

CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL FATE; CELL MATURATION; CELL METABOLISM; CELL PROLIFERATION; CELL RENEWAL; CYTOLOGY; EMBRYONIC STEM CELL; HUMAN; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL;

ADULT; ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOL 3-KINASES; PLURIPOTENT STEM CELLS;

HARNESS;

EID: 79953201225     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390674     Document Type: Review

References (48)

1. Smith, A.G. (2001) Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 17, 435-462
2. He, S.H., Nakada, D. and Morrison, S.J. (2009) Mechanisms of stem cell self-renewal. Annu. Rev. Cell Dev. Biol. 25, 377-406
3. Orford, K.W. and Scadden, D.T. (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9, 115-128
4. Boiani, M. and Schoeler, H.R. (2005) Regulatory networks in embryo-derived pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 6, 872-881
5. Niwa, H. (2007) How is pluripotency determined and maintained? Development 134, 635-646
6. Silva, J. and Smith, A. (2008) Capturing pluripotency. Cell 132, 532-536 (Pubitemid 351253697)
7. Canham, M., Sharov, A., Ko, M. and Brickman, J.M. (2010) Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379
8. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L. and Smith, A. (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1238
9. Van Den Berg, D.L.C., Zhang, W., Yates, A., Engelen, E., Takacs, K., Bezstarosti, K., Demmers, J., Chambers, I. and Poot, R.A. (2008) Estrogen-related receptor β interacts with Oct4 to positively regulate Nanog gene expression. Mol. Biol. Cell 28, 5986-5995
10. Toyooka, Y., Shimosato, D., Murakami, K., Takahashi, K. and Niwa, H. (2008) Identification and characterisation of subpopulations in undifferentiated ES cell culture. Development 135, 909-918 (Pubitemid 351524145)
11. Savatier, P., Huang, S., Szekely, L., Wiman, K.G. and Samarut, J. (1994) Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts. Oncogene 9, 809-818 (Pubitemid 24065919)
12. Stead, E., White, J., Faast, R., Conn, S., Goldstone, S., Rathjen, J., Dhingra, U., Rathjen, P., Walker, D. and Dalton, S. (2002) Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21, 8320-8333 (Pubitemid 35477872)
13. Savatier, P., Lapillonne, H., vanGrunsven, L.A., Rudkin, B. and Samarut, J. (1996) Withdrawal of differentiation inhibitory activity leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12, 309-322
14. Aladjem, M.I., Spike, B.T., Rodewald, L.W., Hope, T.J., Klemm, M., Jaenisch, R. and Wahl, G.M. (1998) ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8, 145-155
15. Neganova, I, Zhang, X, Atkinson, S and M, L. (2009) 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 28, 20-30
16. Card, D.A.G., Hebbar, P.B., Li, L., Trotter, K.W., Komatsu, Y., Mishina, Y. and Archer, T.K. (2008) Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol. Biol. Cell 28, 6426-6438
17. Wang, Y., Baskerville, S., Shenoy, A., Babiariz, J.E., Baehner, L. and Blelloch, R. (2008) Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 40, 1478-1483
18. Vanhaesebroeck, B., Ali, K., Bilancio, A., Geering, B. and Foukas, L.C. (2005) Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem. Sci. 30, 194-204
19. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. and Bilanges, B. (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11, 329-341
20. Cantley, L.C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
21. Bi, L., Okabe, I., Bernard, D.J. and Nussbaum, R.L. (2002) Early embryonic lethality in mice deficient in the p110β catalytic subunit of PI 3-kinase. Mamm. Genome 13, 169-172
22. Sun, H., Lesche, R., Li, D.M., Liliental, J., Zhang, H., Gao, J., Gavrilova, N., Mueller, B., Liu, X. and Wu, H. (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 6199-6204
23. 1/S transition in mouse embryonic stem cells. Oncogene 21, 5515-5528
24. Takahashi, K., Mitsui, K. and Yamanaka, S. (2003) Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. Nature 423, 541-545 (Pubitemid 36648578)
25. Murakami, M., Ichisaka, T., Maeda, M., Oshiro, N., Hara, K., Edenhofer, F., Kiyama, H., Yonezawa, K. and Yamanaka, S. (2004) mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol. Cell. Biol. 24, 6710-6718
26. Paling, N.R., Wheadon, H., Bone, H.K. and Welham, M.J. (2004) Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling. J. Biol. Chem. 279, 48063-48070
27. Watanabe, S., Umehara, H., Murayama, K., Okabe, M., Kimura, T. and Nakano, T. (2006) Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene 25, 2697-2707
28. Pritsker, M., Ford, N.R., Jenq, H.T. and Lemischka, I.R. (2006) Genomewide gain-of-function genetic screen identifies functionally active genes in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 103, 6946-6951
29. Pyle, A., Lock, L. and Donovan, P. (2006) Neurotrophins mediate human embryonic stem cell survival. Nat. Biotechnol. 24, 344-350
30. Armstrong, L., Hughes, O., Yung, S., Hyslop, L., Stewart, R., Wappler, I., Peters, H., Walter, T., Stojkovic, P., Evans, J. et al. (2006) The role of PI3K/AKT, MAPK/ERK and NFκB signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Hum. Mol. Genet. 15, 1894-1913
31. Storm, M.P., Bone, H.K., Beck, C.G., Bourillot, P.Y., Schreiber, V., Damiano, T., Nelson, A., Savatier, P. and Welham, M.J. (2007) Regulation of Nanog expression by phosphoinositide 3-kinase-dependent signaling in murine embryonic stem cells. J. Biol. Chem. 282, 6265-6273
32. Storm, M.P., Kumpfmueller, B., Thompson, B., Kolde, R., Vilo, J., Hummel, O., Schulz, H. and Welham, M.J. (2009) Characterisation of the PI3K-dependent transcriptome in murine ES cells: identification of novel regulators of pluripotency. Stem Cells 27, 764-775
33. Niwa, H., Ogawa, K., Shimosato, D. and Adachi, K. (2009) A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460, 118-122
34. Zalzman, M., Falco, G., Sharova, L.V., Nishiyama, A., Thomas, M., Lee, S.-L., Stagg, C.A., Hoang, G.H., Yang, H.-T., Indig, F.E. et al. (2010) Zscan4 regulates telomere elongation and genomic stability in ES cells. Nature 464, 858-863
35. Kingham, E. and Welham, M.J. (2009) Distinct roles for class IA PI3K catalytic subunit isoforms in the regulation of murine embryonic stem cell behaviour. J. Cell Sci. 122, 2311-2321
36. Doble, B.W. and Woodgett, J.R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186 (Pubitemid 36410657)
37. Hoeflich, K.P., Luo, J., Rubie, E.A., Tsao, M.-S., Jin, O. and Woodgett, J.R. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406, 86-90
38. Ding, S., Wu, T.Y., Brinker, A., Peters, E.C., Hur, W., Gray, N.S. and Schultz, P.G. (2003) Synthetic small molecules that control stem cell fate. Proc. Natl. Acad. Sci. U.S.A. 100, 7632-7637
39. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. and Brivanlou, A.H. (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63
40. Wray, J., Kalkan, T. and Smith, A.G. (2010) The ground state of pluripotency. Biochem. Soc. Trans. 38, 1027-1032
41. Bone, H.K., Damiano, T., Bartlett, S., Perry, A., Letchford, J., Sanchez Ripoll, Y., Nelson, A.S. and Welham, M.J. (2009) Involvement of glycogen synthase kinase-3 in regulation of murine embryonic stem cell self-renewal revealed by a series of bisindolylmaleimides. Chem. Biol. 16, 15-27
42. Doble, B., Patel, S., Wood, G., Kockeritz, L. and Woodgett, J. (2007) Functional redundancy of GSK-3α and GSK-3β in Wnt/β-catenin signalling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12, 957-971
43. Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P. and Smith, A. (2008) The ground state of embryonic stem cell self-renewal. Nature 453, 519-523 (Pubitemid 351733324)
44. Kunath, T., Saba-El-Leil, M.K., Almousailleakh, M., Wray, J., Meloche, S. and Smith, A. (2007) FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895-2902 (Pubitemid 47386902)
45. Stavridis, M., Lunn, J.S., Collins, B.J. and Storey, K.G. (2007) A discrete period of FGF-induced Erk1/2 signalling is required fro vertebrate neural specification. Development 134, 2889-2894
46. D'Amour, K.A., Bang, A.G., Eliazer, S., Kelly, O.G., Agulnick, A.D., Smart, N.G., Moorman, M.A., Kroon, E., Carpenter, M.K. and Baetge, E.E. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24, 1392-1401
47. Hay, D.C., Fletcher, J., Payne, C., Terrace, J.D., Gallagher, R.C., Snoeys, J., Black, J.R., Wojtacha, D., Samuel, K., Hannoun, Z. et al. (2008) Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 12301-12306
48. Sumi, T., Tsuneyoshi, N., Nakatsuji, N. and Suemori, H. (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/β-catenin, Activin/Nodal and BMP signaling. Development 135, 2969-2979