Regulation of self-renewal and reprogramming by TCF factors

Cell Cycle

Volumn 11, Issue 1, 2012, Pages 39-47

  Ombrato, Luigi ^a   Lluis, Frederic ^a   Cosma, Maria Pia ^a,b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Cell reprogramming; Self renewal; T cell factor; Tcf1; Tcf3; Tcf7; Tcf7l1; Wnt pathway; catenin

Indexed keywords

6 BROMOINDIRUBIN 3' OXIME; ALPHA CATENIN; BETA CATENIN; CADHERIN; CHIR 99021; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; KRUPPEL LIKE FACTOR 4; LEUKEMIA INHIBITORY FACTOR; LITHIUM CHLORIDE; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; OCTAMER TRANSCRIPTION FACTOR 4; PLAKOGLOBIN; STAT3 PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN;

BINDING SITE; CELL ADHESION; CELL CULTURE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FUSION; CELL JUNCTION; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; EMBRYONIC STEM CELL; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; TRANSCRIPTION REGULATION;

EID: 84855696042     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.1.18759     Document Type: Review

References (67)

1. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20:781-810; PMID:15473860; http://dx.doi.org/10. 1146/annurev.cellbio.20.010403.113126.
2. Miller JR. The Wnts. Genome Biol 2002; 3:3001; PMID:11806834.
3. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms and diseases. Dev Cell 2009; 17:9-26; PMID:19619488; http://dx.doi.org/10.1016/j.devcel.2009.06.016.
4. Wu D, Pan W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem Sci 2010; 35:161-8; PMID:19884009; http://dx.doi.org/10.1016/j.tibs.2009.10. 002.
5. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 2008; 22:746-55; PMID:18347094; http://dx.doi.org/10.1101/gad.1642408.
6. Willert K, Jones KA. Wnt signaling: is the party in the nucleus? Genes Dev 2006; 20:1394-404; PMID:16751178; http://dx.doi.org/10.1101/gad.1424006.
7. Hoppler S, Kavanagh CL. Wnt signalling: variety at the core. J Cell Sci 2007; 120:385-93; PMID:17251379; http://dx.doi.org/10.1242/jcs.03363.
8. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004; 10:55-63; PMID:14702635; http://dx.doi.org/10.1038/nm979.
9. Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, Smith A. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol 2008; 6:253; PMID:18942890; http://dx.doi.org/10.1371/journal.pbio. 0060253.
10. Sineva GS, Pospelov VA. Inhibition of GSK3beta enhances both adhesive and signalling activities of beta-catenin in mouse embryonic stem cells. Biol Cell 2010; 102:549-60; PMID:20626347; http://dx.doi.org/10.1042/BC20100016.
11. Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, Leost M, et al. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 2003; 10:1255-66; PMID:14700633; http://dx.doi.org/10. 1016/j.chembiol.2003.11.010.
12. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, et al. The ground state of embryonic stem cell self-renewal. Nature 2008; 453:519-23; PMID:18497825; http://dx.doi.org/10.1038/nature06968.
13. Niwa H, Burdon T, Chambers I, Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998; 12:2048-60; PMID:9649508; http://dx.doi.org/10.1101/gad.12.13.2048.
14. Smith AG. Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 2001; 17:435-62; PMID:11687496; http://dx.doi.org/10.1146/annurev.cellbio. 17.1.435.
15. Sato N, Sanjuan IM, Heke M, Uchida M, Naef F, Brivanlou AH. Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev Biol 2003; 260:404-13; PMID:12921741; http://dx.doi.org/10.1016/S0012-1606(03) 00256-2.
16. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, et al. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 2011; 13:762-70; PMID:21685894; http://dx.doi.org/ 10.1038/ncb2283.
17. Aubert J, Dunstan H, Chambers I, Smith A. Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat Biotechnol 2002; 20:1240-5; PMID:12447396; http://dx.doi.org/10.1038/nbt763.
18. ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, Eroglu E, et al. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 2011; 13:1070-5; PMID:21841791; http://dx.doi.org/10. 1038/ncb2314.
19. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR. Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 2007; 12:957-71; PMID:17543867; http://dx.doi.org/10.1016/j.devcel.2007.04.001.
20. Kelly KF, Ng DY, Jayakumaran G, Wood GA, Koide H, Doble BW. beta-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 2011; 8:214-27; PMID:21295277; http://dx.doi.org/10. 1016/j.stem.2010.12.010.
21. Anton R, Kestler HA, Kuhl M. beta-Catenin signaling contributes to stemness and regulates early differentiation in murine embryonic stem cells. FEBS Lett 2007; 581:5247-54; PMID:17950287; http://dx.doi.org/10.1016/j.febslet. 2007.10.012.
22. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, et al. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat Cell Biol 2011; 13:838-45; PMID:21685889; http://dx.doi.org/10.1038/ncb2267.
23. Lyashenko N, Winter M, Migliorini D, Biechele T, Moon RT, Hartmann C. Differential requirement for the dual functions of beta-catenin in embryonic stem cell self-renewal and germ layer formation. Nat Cell Biol 2011; 13:753-61; PMID:21685890; http://dx.doi.org/10.1038/ncb2260.
24. Lluis F, Cosma MP. Somatic cell reprogramming control: signaling pathway modulation versus transcription factor activities. Cell Cycle 2009; 8:1138-44; PMID:19305152; http://dx.doi.org/10.4161/cc.8.8.8206.
25. Lluis F, Pedone E, Pepe S, Cosma MP. Periodic activation of Wnt/beta-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 2008; 3:493-507; PMID:18983965; http://dx.doi.org/10. 1016/j.stem.2008.08.017.
26. Lluis F, Pedone E, Pepe S, Cosma MP. The Wnt/beta-catenin signaling pathway tips the balance between apoptosis and reprograming of cell fusion hybrids. Stem Cells 2010; 28:1940-9; PMID:20827748; http://dx.doi.org/10.1002/ stem.515.
27. Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA, et al. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 2008; 3:132-5; PMID:18682236; http://dx.doi.org/10.1016/j.stem.2008.06. 019.
28. Li W, Zhou H, Abujarour R, Zhu S, Young Joo J, Lin T, et al. Generation of human-induced pluripotent stem cells in the absence of exogenous Sox2. Stem Cells 2009; 27:2992-3000; PMID:19839055.
29. Zhu S, Ma T, Li J, Ding S. Recent advances in chemically induced reprogramming. Cell Cycle 2011; 10:871-2; PMID:21368574; http://dx.doi.org/10. 4161/cc.10.6.15035.
30. Banito A, Rashid ST, Acosta JC, Li S, Pereira CF, Geti I, et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009; 23:2134-9; PMID:19696146; http://dx.doi.org/10.1101/gad.1811609.
31. Hong H, Takahashi K, Ichisaka T, Aoi T, Kanagawa O, Nakagawa M, et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009; 460:1132-5; PMID:19668191; http://dx.doi.org/10.1038/nature08235. org/10.1038/nature08311.
32. Li H, Collado M, Villasante A, Strati K, Ortega S, Canamero M, et al. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009; 460:1136-9; PMID:19668188; http://dx.doi.org/10.1038/nature08290.
33. Marión RM, Strati K, Li H, Murga M, Blanco R, Ortega S, et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009; 460:1149-53; PMID:19668189; http://dx.doi.org/10.1038/ nature08287.
34. Utikal J, Polo JM, Stadtfeld M, Maherali N, Kulalert W, Walsh RM, et al. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009; 460:1145-8; PMID:19668190; http://dx.doi.org/10.1038/ nature08285.
35. Menendez S, Camus S, Izpisua Belmonte JC. p53: guardian of reprogramming. Cell Cycle 2010; 9:3887-91; PMID:20948296; http://dx.doi.org/10.4161/cc.9.19. 13301.
36. Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 1993; 9:317-21; PMID:8236461; http://dx.doi.org/10.1016/0168-9525(93)90250-L.
37. Larue L, Ohsugi M, Hirchenhain J, Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 1994; 91:8263-7; PMID:8058792; http://dx.doi.org/10.1073/pnas.91.17.8263.
38. Dang SM, Gerecht-Nir S, Chen J, Itskovitz-Eldor J, Zandstra PW. Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 2004; 22:275-82; PMID:15153605; http://dx.doi.org/10.1634/stemcells.22-3-275.
39. Fukunaga Y, Liu H, Shimizu M, Komiya S, Kawasuji M, Nagafuchi A. Defining the roles of beta-catenin and plakoglobin in cell-cell adhesion: isolation of beta-catenin/plakoglobin-deficient F9 cells. Cell Struct Funct 2005; 30:25-34; PMID:16357441; http://dx.doi.org/10.1247/csf.30.25.
40. Soncin F, Mohamet L, Eckardt D, Ritson S, Eastham AM, Bobola N, et al. Abrogation of E-cadherin-mediated cell-cell contact in mouse embryonic stem cells results in reversible LIF-independent self-renewal. Stem Cells 2009; 27:2069-80; PMID:19544408; http://dx.doi.org/10.1002/stem.134.
41. Redmer T, Diecke S, Grigoryan T, Quiroga-Negreira A, Birchmeier W, Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep 2011; 12:720-6; PMID:21617704; http://dx.doi.org/10.1038/embor.2011.88.
42. Li R, Liang J, Ni S, Zhou T, Qing X, Li H, et al. A mesenchymal-to- epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010; 7:51-63; PMID:20621050; http://dx.doi.org/10.1016/j.stem.2010.04.014.
43. Samavarchi-Tehrani P, Golipour A, David L, Sung HK, Beyer TA, Datti A, et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010; 7:64-77; PMID:20621051; http://dx.doi.org/10.1016/j.stem.2010.04.015.
44. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000; 24:372-6; PMID:10742100; http://dx.doi.org/10.1038/74199.
45. Niwa H. How is pluripotency determined and maintained? Development 2007; 134:635-46; PMID:17215298; http://dx.doi.org/10.1242/dev.02787.
46. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, et al. Nanog is the gateway to the pluripotent ground state. Cell 2009; 138:722-37; PMID:19703398; http://dx.doi.org/10.1016/j.cell.2009.07.039.
47. Boyer LA, Mathur D, Jaenisch R. Molecular control of pluripotency. Curr Opin Genet Dev 2006; 16:455-62; PMID:16920351; http://dx.doi.org/10.1016/j.gde. 2006.08.009.
48. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006; 38:431-40; PMID:16518401; http://dx.doi.org/10.1038/ ng1760.
49. 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 2007; 131:861-72; PMID:18035408; http://dx.doi.org/10.1016/j.cell. 2007.11.019.
50. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-76; PMID:16904174; http://dx.doi.org/10.1016/j.cell.2006.07.024.
51. Yamanaka S, Blau HM. Nuclear reprogramming to a pluripotent state by three approaches. Nature 2010; 465:704-12; PMID:20535199; http://dx.doi.org/10. 1038/nature09229.
52. Brannon M, Brown JD, Bates R, Kimelman D, Moon RT. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 1999; 126:3159-70; PMID:10375506.
53. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, et al. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 1996; 86:391-9; PMID:8756721; http://dx.doi.org/10.1016/S0092-8674(00)80112-9.
54. Lluis F, Ombrato L, Pedone E, Pepe S, Merrill BJ, Cosma MP. T-cell factor 3 (Tcf3) deletion increases somatic cell reprogramming by inducing epigenome modifications. Proc Natl Acad Sci USA 2011; 108:11912-7; PMID:21730189; http://dx.doi.org/10.1073/pnas.1017402108.
55. Pereira L, Yi F, Merrill BJ. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 2006; 26:7479-91; PMID:16894029; http://dx.doi.org/10.1128/MCB.00368-06.
56. Salomonis N, Conklin BR. Stem cell pluripotency: alternative modes of transcription regulation. Cell Cycle 2010; 9:3133-4; PMID:20814242; http://dx.doi.org/10.4161/cc.9.16.12888.
57. Salomonis N, Schlieve CR, Pereira L, Wahlquist C, Colas A, Zambon AC, et al. Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc Natl Acad Sci USA 2010; 107:10514-9; PMID:20498046; http://dx.doi.org/10.1073/pnas.0912260107.
58. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008; 134:521-33; PMID:18692474; http://dx.doi.org/10.1016/j.cell.2008.07.020.
59. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH, et al. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008; 26:2019-31; PMID:18467660; http://dx.doi.org/10.1634/stemcells.2007-1115.
60. Guo G, Huang Y, Humphreys P, Wang X, Smith A. A PiggyBac-based recessive screening method to identify pluripotency regulators. PLoS ONE 2011; 6:18189; PMID:21533166; http://dx.doi.org/10.1371/journal.pone.0018189.
61. Yi F, Pereira L, Merrill BJ. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008; 26:1951-60; PMID:18483421; http://dx.doi.org/10.1634/stemcells.2008-0229.
62. Han J, Yuan P, Yang H, Zhang J, Soh BS, Li P, et al. Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature 2010; 463:1096-100; PMID:20139965; http://dx.doi.org/10.1038/nature08735.
63. Meshorer E, Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol 2006; 7:540-6; PMID:16723974; http://dx.doi.org/10.1038/nrm1938.
64. Sokol SY. Maintaining embryonic stem cell pluripotency with Wnt signaling. Development 2011; 138:4341-50; PMID:21903672; http://dx.doi.org/10. 1242/dev.066209.
65. Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY. Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 2010; 19:521-32; PMID:20951344; http://dx.doi.org/10.1016/j.devcel.2010.09. 005.
66. Hikasa H, Sokol SY. Phosphorylation of TCF Proteins by Homeodomain-interacting Protein Kinase 2. J Biol Chem 2011; 286:12093-100; PMID:21285352; http://dx.doi.org/10.1074/jbc.M110.185280.
67. Takao Y, Yokota T, Koide H. Beta-catenin upregulates Nanog expression through interaction with Oct-3/4 in embryonic stem cells. Biochem Biophys Res Commun 2007; 353:699-705; PMID:17196549; http://dx.doi.org/10.1016/j.bbrc.2006. 12.072.