Gro/TLE enables embryonic stem cell differentiation by repressing pluripotent gene expression

Developmental Biology

Volumn 397, Issue 1, 2015, Pages 56-66

  Laing, Adam F ^a   Lowell, Sally ^a   Brickman, Joshua M ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b University of Copenhagen   (Denmark)

Author keywords

Differentiation; Embryonic stem cells; Gro TLE; Pluripotency

Indexed keywords

MEMBRANE PROTEIN; PROTEIN TLE1; PROTEIN TLE2; PROTEIN TLE3; PROTEIN TLE4; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; COREPRESSOR PROTEIN; DNA BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; REPRESSOR PROTEIN; TLE1 PROTEIN, MOUSE; TLE3 PROTEIN, MOUSE; TLE4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; HETEROZYGOSITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; INTRON; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; UPREGULATION; ALLELE; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; ENDODERM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; PLURIPOTENT STEM CELL; TRANSGENIC MOUSE;

ALLELES; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CO-REPRESSOR PROTEINS; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; ENDODERM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MICE; MICE, TRANSGENIC; MODELS, GENETIC; PHENOTYPE; PLURIPOTENT STEM CELLS; REPRESSOR PROTEINS;

EID: 84915782769     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.10.007     Document Type: Article

References (48)

1. Beddington R., Robertson E. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 1989, 105:733-737.
2. Buscarlet M., Stifani S. The "Marx"of Groucho on development and disease. Trends Cell Biol. 2007, 17:353-361. 10.1016/j.tcb.2007.07.002.
3. Canham M., Sharov A., Ko M., Brickman J. Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 2010, 8:e1000379. 10.1371/journal.pbio.1000379.
4. Chambers I., Tomlinson S. The transcriptional foundation of pluripotency. Development 2009, 136:2311-2322.
5. Chazaud C., Yamanaka Y., Pawson T., Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 2006, 10:615-624.
6. Chen G., Fernandez J., Mische S., Courey A.J. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 1999, 13:2218-2230.
7. Cheng A.M., Saxton T.M., Sakai R., Kulkarni S., Mbamalu G., W, V., Tortorice C., Cardiff R.D., Cross J.C., Muller W.J., Pawson T. Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 1998, 95:793-803.
8. Chodaparambil J.V, Pate K.T., Hepler M.R., Tsai B.P., Muthurajan U.M., Luger K., Waterman M.L., Weis W.I. Molecular functions of the TLE tetramerization domain in Wnt target gene repression. EMBO J. 2014, 33:719-731.
9. Cloonan N., Forrest A.R., Kolle G., Gardiner B.B., Faulkner G.J., Brown M.K., Taylor D.F., Steptoe A.L., Wani S., Bethel G., Robertson A.J., Perkins A.C., Bruce S.J., Lee C.C., Ranade S.S., Peckham H.E., Manning J.M., McKernan K.J., Grimmond S.M. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat. Methods 2008, 5:613-619.
10. Cole M.F., Johnstone S.E., Newman J.J., Kagey M.H., Young R.A. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev. 2008, 22:746.
11. Davies O.R., Lin C.Y., Radzisheuskaya A., Zhou X., Taube J., Blin G., Waterhouse A., Smith A.J., Lowell S. Tcf15 primes pluripotent cells for differentiation. Cell Rep 2013, 3:472-484.
12. Friedel R., Plump A., Lu X., Spilker K., Jolicoeur C., Wong K., Venkatesh T., Yaron A., Hynes M., Chen B., Okada A., McConnel S., Rayburn H., Tessier-Lavigne M. Gene targeting using a promoterless gene trap vector is an efficient method. Proc. Natl. Acad. Sci 2005, 102:13188-13193.
13. Fujikura J., Yamato E., Yonemura S., Hosoda K., Masui S., Nakao K., Miyazaki J., Niwa H. Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 2002, 16:784.
14. Hamazaki T., Kehoe S.M., Nakano T., Terada N. The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Mol. Cell. Biol. 2006, 26:7539-7549.
15. Hamilton W.B., Kaji K., Kunath T. ERK2 suppresses self-renewal capacity of embryonic stem cells, but is not required for multi-lineage commitment. PLoS One 2013, 8:e60907.
16. Hayashi K., de Sousa Lopes S.M.C., Tang F., Surani M.A. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 2008, 3:391-401.
17. Huyer G., Liu S., Kelly J., Moffat J., Payette P., Kennedy B., Tsaprailis G., Gresser M.J., Ramachandran C. Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J. Biol. Chem. 1997, 272:843-851.
18. Jennings B.H., Ish-Horowicz D. The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 2008, 9:205. 10.1186/gb-2008-9-1-205.
19. Khar A., Ali A.M. Serum protects HeLa cells from antiestrogen effects in culture. Eur. J. Cancer Clin. Oncol 1987, 23:761-763.
20. Kobayashi T., Mizuno H., Imayoshi I., Furusawa C., Shirahige K., Kageyama R. The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 2009, 23:1870-1875. 10.1101/gad.1823109.
21. Kunath T., Saba-El-Leil M.K., Almousailleakh M., Wray J., Meloche S., Smith A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007, 134:2895-2902. 10.1242/dev.02880.
22. Levasseur D.N., Wang J., Dorschner M.O., Stamatoyannopoulos J.A., Orkin S.H. Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes Dev. 2008, 22:575-580.
23. Lien W.H., Polak L., Lin M., Lay K., Zheng D., Fuchs E. In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators. Nat. Cell Biol. 2014, 16:179-190.
24. Liu Y., Labosky P. Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells 2008, 26:2475-2484. 10.1634/stemcells.2008-0269.
25. Marson A., Levine S.S., Cole M.F., Frampton G.M., Brambrink T., Johnstone S., Guenther M.G., Johnston W.K., Wernig M., Newman J., Calabrese J.M., Dennis L.M., Volkert T.L., Gupta S., Love J., Hannett N., Sharp P.A., Bartel D.P., Jaenisch R., Young R.A. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134:521-533.
26. Martello G., Sugimoto T., Diamanti E., Joshi A., Hannah R., Ohtsuka S., Göttgens B., Niwa H., Smith A. Esrrb is a pivotal target of the gsk3/tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 2012, 11:491-504.
27. Martinez Arias A., Brickman J.M. Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr. Opin. Cell Biol. 2011, 23:650-656.
28. Morgani S.M., Canham M.A., Nichols J., Sharov A.A., Migueles R.P., Ko M.S., Brickman J.M. Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep 2013, 3:1945-1957.
29. Nichols J., Silva J., Roode M., Smith A. Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 2009, 136:3215-3222.
30. Pereira L., Yi F., Merrill B.J. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol. Cell. Biol. 2006, 26:7479-7491. 10.1128/MCB.00368-06.
31. Ramahlo-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., Melton D.A. " Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002, (80-):597-600.
32. Sekiya T., Zaret K. Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol. Cell 2007, 28:291-303. 10.1016/j.molcel.2007.10.002.
33. Sekkai D., Gruel G., Herry M., Moucadel V., Constantinescu S., Albagli O., Roux D., Vainchenker W., Bennaceur-Griscelli A. Microarray analysis of LIF/Stat3 transcriptional targets in embryonic stem cells. Stem Cells 2005, 23:1634. 10.1634/stemcells.2005-0182.
34. Shy B.R., Wu C.I., Khramtsova G.F., Zhang J.Y., Olopade O.I., Goss K.H., Merrill B.J. Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt/β-catenin signaling. Cell Rep 2013, 4:1-9.
35. Singh A.M., Hamazaki T., Hankowski K.E., Terada N. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 2007, 25:2534-2542. 10.1634/stemcells.2007-0126.
36. Swingler T.E., Bess K.L., Yao J., Stifani S., Jayaraman P.-S. The proline-rich homeodomain protein recruits members of the Groucho/Transducin-like enhancer of split protein family to co-repress transcription in hematopoietic cells. J. Biol. Chem. 2004, 279:34938-34947. 10.1074/jbc.M404488200.
37. Tam W., Lim C.Y., Han J., Zhang J., Ang Y.S., Ng H.H., Yang H., Lim B. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008, 26:2019-2031.
38. Ten Berge D., Kurek D., Blauwkamp T., Koole W., Maas A., Eroglu E., Siu R.K., Nusse R. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat. Cell Biol. 2011, 13:1070-1075.
39. Wray J., Kalkan T., Gomez-Lopez S., Eckardt D., Cook A., Kemler R., Smith A. 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, 13:838-845.
40. Wu C.I., Hoffman J.A., Shy B.R., Ford E.M., Fuchs E., Nguyen H., Merrill B. Function of Wnt/β-catenin in Counteracting Tcf3 Repression Through the Tcf3-β-Catenin Interaction.... 2012, 2118-2129.
41. Yao J., Liu Y., Lo R., Tretjakoff I., Peterson A., Stifani S. development of the cerebral hemispheres in transgenic mice expressing the mammalian Groucho homologue transducin-like-enhancer of split 1 in postmitotic. Dev 2000, 93:105-115.
42. Yi F., Pereira L., Hoffman J.A., Shy B.R., Yuen C.M., Liu D.R., Merrill B.J. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 2011, 13:762-770.
43. Yi F., Pereira L., Merrill B.J. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008, 26:1951-1960.
44. Ying Q., Stavridis M., Griffiths D., Li M., Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 2003, 21:183-186.
45. Ying Q.-L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523. 10.1038/nature06968.
46. Zamparini A.L., Watts T., Gardner C.E., Tomlinson S.R., Johnston G.I., Brickman J.M. Hex acts with {beta}-catenin to regulate anteroposterior patterning via a Groucho-related co-repressor and Nodal. Development 2006, 133:3709-3722.
47. Zhou X., Smith A., Waterhouse A., Blin G., Malguti M., Lin C.Y., Osorno R., Chambers I., Lowell S. Hes1 Desynchronizes differentiation of pluripotent cells by modulating STAT3 activity. Stem Cells 2013, 31:1511-1522.
48. Ziemer A., Tietze K., Knust E., Campos-Ortega J.A. Genetic analysis of enhancer of split, a locus involved in neurogenesis in Drosophila melanogaster. Genetics 1988, 119:63.