Single-Cell Profiling of Epigenetic Modifiers Identifies PRDM14 as an Inducer of Cell Fate in the Mammalian Embryo

Cell Reports

Volumn 5, Issue 3, 2013, Pages 687-701

  Burton, Adam ^a   Muller, Julius ^b   Tu, Shengjiang ^d   Padilla Longoria, Pablo ^c   Guccione, Ernesto ^b,e   Torres Padilla, Maria Elena ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c Ciudad Universitaria   (Mexico)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HISTONE H3; PROTEIN PRDM14; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CHROMATIN; PRDM14 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DEVELOPMENTAL STAGE; DNA MODIFICATION; ECTODERM; EMBRYO; EMBRYO CELL; EPIGENETICS; MAMMAL CELL; MICROFLUIDICS; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; ANIMAL; ANIMAL EMBRYO; BIOSYNTHESIS; BLASTOMA; CELL LINEAGE; CHROMATIN; CYTOLOGY; DNA METHYLATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; PHYSIOLOGY; PROCEDURES; SINGLE CELL ANALYSIS;

MAMMALIA;

ANIMALS; BLASTOMERES; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; SINGLE-CELL ANALYSIS; TRANSCRIPTION FACTORS;

EID: 84887617702     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.09.044     Document Type: Article

References (44)

1. Agger K., Cloos P.A., Christensen J., Pasini D., Rose S., Rappsilber J., Issaeva I., Canaani E., Salcini A.E., Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007, 449:731-734.
2. Ahmed K., Dehghani H., Rugg-Gunn P., Fussner E., Rossant J., Bazett-Jones D.P. Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS ONE 2010, 5:e10531.
3. Alder O., Lavial F., Helness A., Brookes E., Pinho S., Chandrashekran A., Arnaud P., Pombo A., O'Neill L., Azuara V. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development 2010, 137:2483-2492.
4. Bhattacharya S., Zhang Q., Andersen M.E. A deterministic map of Waddington's epigenetic landscape for cell fate specification. BMC Syst. Biol. 2011, 5:85.
5. Borgel J., Guibert S., Li Y., Chiba H., Schübeler D., Sasaki H., Forné T., Weber M. Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 2010, 42:1093-1100.
6. Bultman S.J., Gebuhr T.C., Pan H., Svoboda P., Schultz R.M., Magnuson T. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 2006, 20:1744-1754.
7. Burton A., Torres-Padilla M.E. Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief Funct Genomics 2010, 9:444-454.
8. 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.
9. Chen D., Ma H., Hong H., Koh S.S., Huang S.M., Schurter B.T., Aswad D.W., Stallcup M.R. Regulation of transcription by a protein methyltransferase. Science 1999, 284:2174-2177.
10. Dietrich J.E., Hiiragi T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007, 134:4219-4231.
11. Erhardt S., Su I.H., Schneider R., Barton S., Bannister A.J., Perez-Burgos L., Jenuwein T., Kouzarides T., Tarakhovsky A., Surani M.A. Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 2003, 130:4235-4248.
12. Gillich A., Bao S., Grabole N., Hayashi K., Trotter M.W., Pasque V., Magnúsdóttir E., Surani M.A. Epiblast stem cell-based system reveals reprogramming synergy of germline factors. Cell Stem Cell 2012, 10:425-439.
13. Guo G., Huss M., Tong G.Q., Wang C., Li Sun L., Clarke N.D., Robson P. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 2010, 18:675-685.
14. Hamatani T., Carter M.G., Sharov A.A., Ko M.S. Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 2004, 6:117-131.
15. Hemberger M., Dean W., Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 2009, 10:526-537.
16. Hirasawa R., Sasaki H. Dynamic transition of Dnmt3b expression in mouse pre- and early post-implantation embryos. Gene Expr. Patterns 2009, 9:27-30.
17. Hirasawa R., Chiba H., Kaneda M., Tajima S., Li E., Jaenisch R., Sasaki H. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 2008, 22:1607-1616.
18. Johnson M.H. From mouse egg to mouse embryo: polarities, axes, and tissues. Annu. Rev. Cell Dev. Biol. 2009, 25:483-512.
19. Johnson M.H., McConnell J.M. Lineage allocation and cell polarity during mouse embryogenesis. Semin. Cell Dev. Biol. 2004, 15:583-597.
20. Kang M., Piliszek A., Artus J., Hadjantonakis A.K. FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 2013, 140:267-279.
21. Lan F., Bayliss P.E., Rinn J.L., Whetstine J.R., Wang J.K., Chen S., Iwase S., Alpatov R., Issaeva I., Canaani E., et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007, 449:689-694.
22. Lopez-Bigas N., Kisiel T.A., Dewaal D.C., Holmes K.B., Volkert T.L., Gupta S., Love J., Murray H.L., Young R.A., Benevolenskaya E.V. Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Mol. Cell 2008, 31:520-530.
23. Lorthongpanich C., Doris T.P., Limviphuvadh V., Knowles B.B., Solter D. Developmental fate and lineage commitment of singled mouse blastomeres. Development 2012, 139:3722-3731.
24. Ma Z., Swigut T., Valouev A., Rada-Iglesias A., Wysocka J. Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 2011, 18:120-127.
25. Magnúsdóttir E., Dietmann S., Murakami K., Günesdogan U., Tang F., Bao S., Diamanti E., Lao K., Gottgens B., Azim Surani M. A tripartite transcription factor network regulates primordial germ cell specification in mice. Nat. Cell Biol. 2013, 15:905-915.
26. Meshorer E., Yellajoshula D., George E., Scambler P.J., Brown D.T., Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 2006, 10:105-116.
27. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
28. Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Schöler H., Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391.
29. Ohinata Y., Payer B., O'Carroll D., Ancelin K., Ono Y., Sano M., Barton S.C., Obukhanych T., Nussenzweig M., Tarakhovsky A., et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 2005, 436:207-213.
30. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
31. Parfitt D.E., Zernicka-Goetz M. Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol. Biol. Cell 2010, 21:2649-2660.
32. Puschendorf M., Terranova R., Boutsma E., Mao X., Isono K., Brykczynska U., Kolb C., Otte A.P., Koseki H., Orkin S.H., et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 2008, 40:411-420.
33. Ratnam S., Mertineit C., Ding F., Howell C.Y., Clarke H.J., Bestor T.H., Chaillet J.R., Trasler J.M. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev. Biol. 2002, 245:304-314.
34. Rossant J., Tam P.P. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 2009, 136:701-713.
35. Sakaue M., Ohta H., Kumaki Y., Oda M., Sakaide Y., Matsuoka C., Yamagiwa A., Niwa H., Wakayama T., Okano M. DNA methylation is dispensable for the growth and survival of the extraembryonic lineages. Curr. Biol. 2010, 20:1452-1457.
36. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
37. Tabansky I., Lenarcic A., Draft R.W., Loulier K., Keskin D.B., Rosains J., Rivera-Feliciano J., Lichtman J.W., Livet J., Stern J.N., et al. Developmental bias in cleavage-stage mouse blastomeres. Curr. Biol. 2013, 23:21-31.
38. Tang F., Barbacioru C., Nordman E., Bao S., Lee C., Wang X., Tuch B.B., Heard E., Lao K., Surani M.A. Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS ONE 2011, 6:e21208.
39. Torres-Padilla M.E., Bannister A.J., Hurd P.J., Kouzarides T., Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 2006, 50:455-461.
40. Torres-Padilla M.E., Parfitt D.E., Kouzarides T., Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007, 445:214-218.
41. Wang Q.T., Piotrowska K., Ciemerych M.A., Milenkovic L., Scott M.P., Davis R.W., Zernicka-Goetz M. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 2004, 6:133-144.
42. Yamaji M., Seki Y., Kurimoto K., Yabuta Y., Yuasa M., Shigeta M., Yamanaka K., Ohinata Y., Saitou M. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 2008, 40:1016-1022.
43. Yamaji M., Ueda J., Hayashi K., Ohta H., Yabuta Y., Kurimoto K., Nakato R., Yamada Y., Shirahige K., Saitou M. PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 2013, 12:368-382.
44. Ziomek C.A., Johnson M.H. Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 1980, 21:935-942.