Fgf and Esrrb integrate epigenetic and transcriptional networks that regulate self-renewal of trophoblast stem cells

Nature Communications

Volumn 6, Issue , 2015, Pages

  Latos, Paulina A ^a,b   Goncalves, Angela ^c   Oxley, David ^a   Mohammed, Hisham ^a   Turro, Ernest ^d,e   Hemberger, Myriam ^a,b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR BETA; ESTROGEN RELATED RECEPTOR BETA; FIBROBLAST GROWTH FACTOR; HISTONE DEMETHYLASE; RNA POLYMERASE II; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 5; TRANSCRIPTION FACTORS EOMES; UNCLASSIFIED DRUG; AOF2 PROTEIN, MOUSE; ESRRB PROTEIN, MOUSE; ESTROGEN RECEPTOR;

CELLS AND CELL COMPONENTS; COLLAGEN; GENE EXPRESSION; GENETIC STRUCTURE; GERMPLASM; GROWTH RATE; RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL RENEWAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EARLY RESPONSE GENE; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION; GIANT CELL; HIGH THROUGHPUT SEQUENCING; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TROPHOBLAST; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HISTONE DEMETHYLASES; MAP KINASE SIGNALING SYSTEM; MICE; PROTEIN INTERACTION MAPPING; RECEPTORS, ESTROGEN; RNA POLYMERASE II; TROPHOBLASTS;

EID: 84937820049     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8776     Document Type: Article

References (54)

1. Cross, J. C., Werb, Z. & Fisher, S. J. Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508-1518 (1994).
2. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. & Rossant, J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998).
3. Latos, P. A. & Hemberger, M. Review: the transcriptional and signalling networks of mouse trophoblast stem cells. Placenta 35(Suppl): S81-S85 (2014).
4. Rossant, J. Stem cells and early lineage development. Cell 132, 527-531 (2008).
5. Erlebacher, A., Price, K. A. & Glimcher, L. H. Maintenance of mouse trophoblast stem cell proliferation by TGF-beta/activin. Dev. Biol. 275, 158-169 (2004).
6. Natale, D. R., Hemberger, M., Hughes, M. & Cross, J. C. Activin promotes differentiation of cultured mouse trophoblast stem cells towards a labyrinth cell fate. Dev. Biol. 335, 120-131 (2009).
7. Kubaczka, C. et al. Derivation and maintenance of murine trophoblast stem cells under defined conditions. Stem Cell Rep. 2, 232-242 (2014).
8. Kunath, T., Strumpf, D. & Rossant, J. Early trophoblast determination and stem cell maintenance in the mouse-a review. Placenta 25(Suppl A): S32-S38 (2004).
9. Krueger, F. et al. Down-regulation of Cdx2 in colorectal carcinoma cells by the Raf-MEK-ERK 1/2 pathway. Cell Signal. 21, 1846-1856 (2009).
10. Russ, A. P. et al. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404, 95-99 (2000).
11. Strumpf, D. et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102 (2005).
12. Luo, J. et al. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 388, 778-782 (1997).
13. Donnison, M. et al. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132, 2299-2308 (2005).
14. Avilion, A. A. et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126-140 (2003).
15. Auman, H. J. et al. Transcription factor AP-2gamma is essential in the extraembryonic lineages for early postimplantation development. Development 129, 2733-2747 (2002).
16. Martello, G. et al. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 11, 491-504 (2012).
17. Masui, S. et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat. Cell Biol. 9, 625-635 (2007).
18. Adachi, K. et al. Context-dependent wiring of Sox2 regulatory networks for self-renewal of embryonic and trophoblast stem cells. Mol. Cell 52, 380-392 (2013).
19. Tremblay, G. B. et al. Diethylstilbestrol regulates trophoblast stem cell differentiation as a ligand of orphan nuclear receptor ERR beta. Genes Dev. 15, 833-838 (2001).
20. Percharde, M. et al. Ncoa3 functions as an essential Esrrb coactivator to sustain embryonic stem cell self-renewal and reprogramming. Genes Dev. 26, 2286-2298 (2012).
21. Festuccia, N. et al. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell 11, 477-490 (2012).
22. van den Berg, D. L. et al. Estrogen-related receptor beta interacts with Oct4 to positively regulate Nanog gene expression. Mol. Cell Biol. 28, 5986-5995 (2008).
23. van den Berg, D. L. et al. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6, 369-381 (2010).
24. Abell, A. N. et al. Trophoblast stem cell maintenance by fibroblast growth factor 4 requires MEKK4 activation of Jun N-terminal kinase. Mol. Cell Biol. 29, 2748-2761 (2009).
25. Saba-El-Leil, M. K. et al. An essential function of the mitogen-activated protein kinase Erk2 in mouse trophoblast development. EMBO Rep. 4, 964-968 (2003).
26. Yang, W. et al. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev. Cell 10, 317-327 (2006).
27. Bissonauth, V., Roy, S., Gravel, M., Guillemette, S. & Charron, J. Requirement for Map2k1 (Mek1) in extra-embryonic ectoderm during placentogenesis. Development 133, 3429-3440 (2006).
28. Ralston, A. & Rossant, J. How signaling promotes stem cell survival: trophoblast stem cells and Shp2. Dev. Cell 10, 275-276 (2006).
29. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008).
30. Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208 (2009).
31. Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L. & Noble, W. S. Quantifying similarity between motifs. Genome Biol. 8, R24 (2007).
32. Bailey, T. L. & Machanick, P. Inferring direct DNA binding from ChIP-seq. Nucleic Acids Res. 40, e128 (2012).
33. Chuong, E. B., Rumi, M. A., Soares, M. J. & Baker, J. C. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45, 325-329 (2013).
34. Yaniv, M. Chromatin remodeling: from transcription to cancer. Cancer Genet. 207, 352-357 (2014).
35. Amente, S., Lania, L. & Majello, B. The histone LSD1 demethylase in stemness and cancer transcription programs. Biochim. Biophys. Acta 1829, 981-986 (2013).
36. Zhu, D. et al. Lysine-specific demethylase 1 regulates differentiation onset and migration of trophoblast stem cells. Nat. Commun. 5, 3174 (2014).
37. Mohammed, H. et al. Endogenous purification reveals GREB1 as a key estrogen receptor regulatory factor. Cell Rep. 3, 342-349 (2013).
38. Baillat, D. et al. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123, 265-276 (2005).
39. Gardini, A. et al. Integrator regulates transcriptional initiation and pause release following activation. Mol. Cell 56, 128-139 (2014).
40. Whyte, W. A. et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482, 221-225 (2012).
41. Uranishi, K., Akagi, T., Sun, C., Koide, H. & Yokota, T. Dax1 associates with Esrrb and regulates its function in embryonic stem cells. Mol. Cell Biol. 33, 2056-2066 (2013).
42. Kim, J., Chu, J., Shen, X., Wang, J. & Orkin, S. H. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132, 1049-1061 (2008).
43. Malik, S. & Roeder, R. G. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 11, 761-772 (2010).
44. Himeno, E., Tanaka, S. & Kunath, T. Isolation and manipulation of mouse trophoblast stem cells. Curr. Protoc. Stem Cell Biol. Chapter 1, Unit 1E 4 (2008).
45. Tavares, L. et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148, 664-678 (2012).
46. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
47. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
48. Li, Q., Brown, J. B., Huang, H. & Bickel, P. J. Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat. 5, 1752-1779 (2011).
49. Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696-1697 (2011).
50. McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
51. Webster, J. O. D. & Oxley, D. in The Protein Protocols Handbook (edWalker, J. M.) 1117-1129 (Humana Press, 2009).
52. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
53. Turro, E. et al. Haplotype and isoform specific expression estimation using multi-mapping RNA-seq reads. Genome Biol. 12, R13 (2011).
54. Turro, E., Astle, W. J. & Tavare, S. Flexible analysis of RNA-seq data using mixed effects models. Bioinformatics 30, 180-188 (2014).