Lysine-specific demethylase 1 regulates differentiation onset and migration of trophoblast stem cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhu, Dongmei ^a   Hölz, Stefanie ^a   Metzger, Eric ^a   Pavlovic, Mihael ^a   Jandausch, Anett ^a   Jilg, Cordula ^a   Galgoczy, Petra ^a   Herz, Corinna ^a   Moser, Markus ^b   Metzger, Daniel ^c   Günther, Thomas ^a   Arnold, Sebastian J ^a,d   Schüle, Roland ^a,d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE SPECIFIC DEMETHYLASE 1; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OVOL2; UNCLASSIFIED DRUG; AOF2 PROTEIN, MOUSE; HISTONE DEMETHYLASE;

CYTOLOGY; ENZYME ACTIVITY; RODENT;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL INVASION; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; EPIGENETIC REPRESSION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; TROPHOBLAST STEM CELL; ANIMAL; CELL MOTION; CYTOLOGY; FEMALE; PHYSIOLOGY; PREGNANCY; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; HISTONE DEMETHYLASES; MICE; PREGNANCY; STEM CELLS; TROPHOBLASTS;

EID: 84893006653     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4174     Document Type: Article

References (45)

1. Guzman-Ayala, M., Ben-Haim, N., Beck, S. & Constam, D. B. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc. Natl Acad. Sci. USA 101, 15656-15660 (2004). (Pubitemid 39473543)
2. Simmons, D. G. & Cross, J. C. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 284, 12-24 (2005). (Pubitemid 41096720)
3. Arnold, S. J. & Robertson, E. J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91-103 (2009).
4. Niwa, H. et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917-929 (2005). (Pubitemid 41721036)
5. 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). (Pubitemid 40744469)
6. Russ, A. P. et al. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404, 95-99 (2000). (Pubitemid 30143140)
7. Hemberger, M., Hughes, M. & Cross, J. C. Trophoblast stem cells differentiate in vitro into invasive trophoblast giant cells. Dev. Biol. 271, 362-371 (2004). (Pubitemid 38833667)
8. Li, M., Liu, G. H. & Izpisua Belmonte, J. C. Navigating the epigenetic landscape of pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 13, 524-535 (2012).
9. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007). (Pubitemid 46273577)
10. Hemberger, M., Dean,W. & Reik, W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 10, 526-537 (2009).
11. Hemberger, M. Epigenetic landscape required for placental development. Cell. Mol. Life Sci. 64, 2422-2436 (2007). (Pubitemid 47402578)
12. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000). (Pubitemid 30038513)
13. Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953 (2004). (Pubitemid 40037608)
14. Metzger, E. et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437, 436-439 (2005). (Pubitemid 41613508)
15. Metzger, E. et al. Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 464, 792-796 (2010).
16. Lee, M. G., Wynder, C., Cooch, N. & Shiekhattar, R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432-435 (2005). (Pubitemid 41613507)
17. Wang, Y. et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660-672 (2009).
18. Garcia-Bassets, I. et al. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128, 505-518 (2007). (Pubitemid 46198894)
19. Wang, J. et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat. Genet. 41, 125-129 (2009).
20. Macfarlan, T. S. et al. Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev. 25, 594-607 (2011).
21. Foster, C. T. et al. Lysine-specific demethylase 1 regulates the embryonic transcriptome and CoREST stability. Mol. Cell Biol. 30, 4851-4863 (2010).
22. Wang, J. et al. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 446, 882-887 (2007). (Pubitemid 46633160)
23. Adamo, A. et al. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat. Cell Biol. 13, 652-659 (2011).
24. Whyte, W. A. et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482, 221-225 (2012).
25. Hayashi, S., Lewis, P., Pevny, L. & McMahon, A. P. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 119(Suppl 1): S97-S101 (2002). (Pubitemid 39658693)
26. Costello, I. et al. The T-box transcription factor Eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat. Cell Biol. 13, 1084-1091 (2011).
27. Nichols, J. et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391 (1998). (Pubitemid 28507326)
28. Arnold, S. J., Sugnaseelan, J., Groszer, M., Srinivas, S. & Robertson, E. J. Generation and analysis of a mouse line harboring GFP in the Eomes/Tbr2 locus. Genesis 47, 775-781 (2009).
29. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. & Rossant, J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998). (Pubitemid 29001261)
30. Lee, M. G. et al. Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell Biol. 26, 6395-6402 (2006). (Pubitemid 44277880)
31. Harris, W. J. et al. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 21, 473-487 (2012).
32. Ueda, R. et al. Identification of cell-active lysine specific demethylase 1-selective inhibitors. J. Am. Chem. Soc. 131, 17536-17537 (2009).
33. Unezaki, S., Horai, R., Sudo, K., Iwakura, Y. & Ito, S. Ovol2/Movo, a homologue of Drosophila ovo, is required for angiogenesis, heart formation and placental development in mice. Genes Cells 12, 773-785 (2007). (Pubitemid 46952550)
34. Mackay, D. R., Hu, M., Li, B., Rheaume, C. & Dai, X. The mouse Ovol2 gene is required for cranial neural tube development. Dev. Biol. 291, 38-52 (2006). (Pubitemid 43343925)
35. Abell, A. N. et al. MAP3K4/CBP-regulated H2B acetylation controls epithelialmesenchymal transition in trophoblast stem cells. Cell Stem Cell 8, 525-537 (2011).
36. Lin, T., Ponn, A., Hu, X., Law, B. K. & Lu, J. Requirement of the histone demethylase LSD1 in Snai1-mediated transcriptional repression during epithelial-mesenchymal transition. Oncogene 29, 4896-4904 (2010).
37. Lin, Y. et al. The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J. 29, 1803-1816 (2010).
38. McDonald, O. G., Wu, H., Timp, W., Doi, A. & Feinberg, A. P. Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition. Nat. Struct. Mol. Biol. 18, 867-874 (2011).
39. Seibler, J. et al. Single copy shRNA configuration for ubiquitous gene knockdown in mice. Nucleic Acids Res. 33, e67 (2005).
40. Quinn, J., Kunath, T. & Rossant, J. Mouse trophoblast stem cells. Methods Mol. Med. 121, 125-148 (2006).
41. Nagy, A., Gertsenstein, M., Vintersten, K & Behringer, R. Manipulating the Mouse Embryo: A Laboratory Manual Manipulating the Mouse Embryo: A Laboratory Manual 3rd edn (CSH Press, 2002).
42. Müller, J. M. et al. FHL2, a novel tissue-specific coactivator of the androgen receptor. EMBO J. 19, 359-369 (2000). (Pubitemid 30072606)
43. Hölzel, M. et al. Rapid conditional knock-down-knock-in system for mammalian cells. Nucleic Acids Res. 35, e17 (2007).
44. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
45. Huang da, W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).