Trophoblast-specific dna methylation occurs after the segregation of the trophectoderm and inner cell mass in the mouse periimplantation embryo

Epigenetics

Volumn 7, Issue 2, 2012, Pages 173-182

  Nakanishi, Momo O ^a   Hayakawa, Koji ^a   Nakabayashi, Kazuhiko ^b   Hata, Kenichiro ^b   Shiota, Kunio ^a   Tanaka, Satoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

Author keywords

Blastocyst; Dna methylation; Placenta; Trophectoderm; Trophoblast

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF5; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL ISOLATION; CELL LINEAGE; DNA METHYLATION; ECTODERM; EMBRYO; EMBRYONAL TISSUE; EMBRYONIC STEM CELL; FEMALE; GENE LOCUS; GENE SEQUENCE; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INNER CELL MASS; MOUSE; NIDATION; NONHUMAN; PLACENTA VILLUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST;

EID: 84857160311     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.7.2.18962     Document Type: Article

References (63)

1. Imamura T, Ohgane J, Ito S, Ogawa T, Hattori N, Tanaka S, et al. CpG island of rat sphingosine kinase-1 gene: tissue-dependent DNA methylation status and multiple alternative first exons. Genomics 2001; 76:117-25;PMID:11560121; http://dx.doi.org/10.1006/geno.2001.6607.
2. De Bustos C, Ramos E, Young JM, Tran RK, Menzel U, Langford CF, et al. Tissue-specific variation in DNA methylation levels along human chromosome 1. Epigenetics Chromatin 2009; 2:7;PMID:19505295; http://dx.doi.org/10.1186/1756-8935-2-7.
3. Shiota K, Kogo Y, Ohgane J, Imamura T, Urano A, Nishino K, et al. Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 2002; 7:961-9;PMID:12296826; http://dx.doi.org/10.1046/j.1365-2443.2002.00574.x.
4. Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994; 266:1508-18;PMID:7985020; http://dx.doi.org/10.1126/science.7985020.
5. Manes C, Menzel P. Demethylation of CpG sites in DNA of early rabbit trophoblast. Nature 1981; 293:589-90;PMID:6270567; http://dx.doi.org/10.1038/293589a0.
6. Chapman V, Forrester L, Sanford J, Hastie N, Rossant J. Cell lineage-specific undermethylation of mouse repetitive DNA. Nature 1984; 307:284-6;PMID:6694730; http://dx.doi.org/10.1038/307284a0.
7. Razin A, Webb C, Szyf M, Yisraeli J, Rosenthal A, Naveh-Many T, et al. Variations in DNA meth-ylation during mouse cell differentiation in vivo and in vitro. Proc Natl Acad Sci USA 1984; 81:2275-9;PMID:6585800; http://dx.doi.org/10.1073/pnas.81.8.2275.
8. Sanford JP, Clark HJ, Chapman VM, Rossant J. Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev 1987; 1:1039-46;PMID:3428592; http://dx.doi.org/10.1101/gad.1.10.1039.
9. Santos F, Hendrich B, Reik W, Dean W Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002; 241:172-82;PMID:11784103;http://dx.doi.org/10.1006/dbio.2001.0501.
10. Dean W, Santos F, Reik W Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Semin Cell Dev Biol 2003; 14:93-100;PMID:12524012; http://dx.doi.org/10.1016/S1084-9521(02)00141-6.
11. Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction 2004; 127:643-51;PMID:15175501; http://dx.doi.org/10.1530/rep.1.00221.
12. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet 2005; 14:47-58;PMID:15809273; http://dx.doi.org/10.1093/hmg/ddi114.
13. Howlett SK, Reik W. Methylation levels of maternal and paternal genomes during preimplantation development. Development 1991; 113:119-27;PMID:1764989.
14. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003; 35:88-93;PMID:12533790; http://dx.doi.org/10.1002/gene.10168.
15. Ko YG, Nishino K, Hattori N, Arai Y, Tanaka S, Shiota K. Stage-by-stage change in DNA methylation status of Dnmt1 locus during mouse early development. J Biol Chem 2005; 280:9627-34;PMID:15634679; http://dx.doi.org/10.1074/jbc.M413822200.
16. Yamagata K, Yamazaki T, Miki H, Ogonuki N, Inoue K, Ogura A, et al. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev Biol 2007; 312:419-26;PMID:17964565; http://dx.doi.org/10.1016/j.ydbio.2007.09.041.
17. Iqbal K, Jin SG, Pfeifer GP, Szabó PE. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 2011; 108:3642-7;PMID:21321204; http://dx.doi.org/10.1073/pnas.1014033108.
18. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2011; 2:241;PMID:21407207; http://dx.doi.org/10.1038/ncomms1240.
19. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998; 282:2072-5;PMID:9851926; http://dx.doi.org/10.1126/science.282.5396.2072.
20. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292:154-6;PMID:7242681; http://dx.doi.org/10.1038/292154a0.
21. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78:7634-8;PMID:6950406; http://dx.doi.org/10.1073/pnas.78.12.7634.
22. Donnison M, Beaton A, Davey HW, Broadhurst R, L'Huillier P, Pfeffer PL. Loss of the extraembry-onic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 2005; 132:2299-308;PMID:15829518; http://dx.doi.org/10.1242/dev.01819.
23. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, et al. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 2008; 10:1280-90;PMID:18836439; http://dx.doi.org/10.1038/ncb1786.
24. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998; 95:379-91;PMID:9814708; http://dx.doi.org/10.1016/S0092-8674(00)81769-9.
25. 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.
26. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113:643-55;PMID:12787505; http://dx.doi.org/10.1016/S0092-8674(03)00392-1.
27. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113:631-42;PMID:12787504; http://dx.doi.org/10.1016/S0092-8674(03)00393-3.
28. Hattori N, Nishino K, Ko YG, Hattori N, Ohgane J, Tanaka S, et al. Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J Biol Chem 2004; 279:17063-9;PMID: 14761969; http://dx.doi.org/10.1074/jbc.M309002200.
29. Hattori N, Imao Y, Nishino K, Hattori N, Ohgane J, Yagi S, et al. Epigenetic regulation of Nanog gene in embryonic stem and trophoblast stem cells. Genes Cells 2007; 12:387-96;PMID:17352742; http://dx.doi.org/10.1111/j.1365-2443.2007.01058.x.
30. Gidekel S, Bergman Y. A unique developmental pattern of Oct-3/4 DNA methylation is controlled by a cis-demodification element. J Biol Chem 2002; 277:34521-30;PMID:12110668; http://dx.doi.org/10.1074/jbc.M203338200.
31. Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S, Dean W, et al. Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet 2008; 4:1000116;PMID:18584034; http://dx.doi.org/10.1371/journal.pgen.1000116.
32. Yagi S, Hirabayashi K, Sato S, Li W, Takahashi Y, Hirakawa T, et al. DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Genome Res 2008; 18:1969-78;PMID:18971312; http://dx.doi.org/10.1101/gr.074070.107.
33. Takasugi M, Yagi S, Hirabayashi K, Shiota K DNA methylation status of nuclear-encoded mitochondrial genes underlies the tissue-dependent mitochondrial functions. BMC Genomics 2010; 11:481;PMID:20723256; http://dx.doi.org/10.1186/1471-2164-11-481.
34. Sakamoto H, Suzuki M, Abe T, Hosoyama T, Himeno E, Tanaka S, et al. Cell type-specific methylation profiles occurring disproportionately in CpG-less regions that delineate developmental similarity. Genes Cells 2007; 12:1123-32;PMID:17903172; http://dx.doi.org/10.1111/j.1365-2443.2007.01120.x.
35. Wakayama S, Jakt ML, Suzuki M, Araki R, Hikichi T, Kishigami S, et al. Equivalency of nuclear transfer-derived embryonic stem cells to those derived from fertilized mouse blastocysts. Stem Cells 2006; 24:2023-33;PMID:16690779; http://dx.doi.org/10.1634/stemcells.2005-0537.
36. Oda M, Tanaka S, Yamazaki Y, Ohta H, Iwatani M, Suzuki M, et al. Establishment of trophoblast stem cell lines from somatic cell nuclear-transferred embryos. Proc Natl Acad Sci USA 2009; 106:16293-7;PMID:19706390; http://dx.doi.org/10.1073/pnas.0908009106.
37. Uy GD, Downs KM, Gardner RL. Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 2002; 129:3913-24;PMID:12135928.
38. Tomikawa J, Fukatsu K, Tanaka S, Shiota K DNA methylation-dependent epigenetic regulation of dimethylarginine dimethylaminohydrolase 2 gene in trophoblast cell lineage. J Biol Chem 2006; 281:12163-9;PMID: 16520373; http://dx.doi.org/10.1074/jbc.M513782200.
39. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, Jaenisch R, et al. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 2008; 22:1607-16;PMID:18559477; http://dx.doi.org/10.1101/gad.1667008.
40. Borgel J, Guibert S, Li Y, Chiba H, Schübeler D, Sasaki H, et al. Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 2010; 42:1093-100;PMID:21057502; http://dx.doi.org/10.1038/ng.708.
41. Dietrich JE, Hiiragi T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007; 134:4219-31;PMID:17978007; http://dx.doi.org/10.1242/dev.003798.
42. Pearton DJ, Broadhurst R, Donnison M, Pfeffer PL. Elf5 regulation in the trophectoderm. Dev Biol 2011; 360:343-50;PMID:22020251; http://dx.doi.org/10.1016/j.ydbio.2011.10.007.
43. Sakaue M, Ohta H, Kumaki Y, Oda M, Sakaide Y, Matsuoka C, et al. DNA methylation is dispensable for the growth and survival of the extraembryonic lineages. Curr Biol 2010; 20:1452-7;PMID:20637626; http://dx.doi.org/10.1016/j.cub.2010.06.050.
44. O'Neill LP, VerMilyea MD, Turner BM. Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nat Genet 2006; 38:835-41;PMID:16767102; http://dx.doi.org/10.1038/ng1820.
45. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007; 445:214-8;PMID:17215844; http://dx.doi.org/10.1038/nature05458.
46. Ikegami K, Ohgane J, Tanaka S, Yagi S, Shiota K. Interplay between DNA methylation, histone modification and chromatin remodeling in stem cells and during development. Int J Dev Biol 2009; 53:203-14;PMID:19412882; http://dx.doi.org/10.1387/ijdb.082741ki.
47. Murr R. Interplay between different epigenetic modifications and mechanisms. Adv Genet 2010; 70:101-41;PMID:20920747; http://dx.doi.org/10.1016/B978-0-12-380866-0.60005-8.
48. Reijo Pera RA, DeJonge C, Bossert N, Yao M, Hwa Yang JY, Asadi NB, et al. Gene expression profiles of human inner cell mass cells and embryonic stem cells. Differentiation 2009; 78:18-23;PMID:19398262; http://dx.doi.org/10.1016/j.diff.2009.03.004.
49. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010; 6:468-78;PMID:20452321; http://dx.doi.org/10.1016/j.stem.2010.03.015.
50. Wongtawan T, Taylor JE, Lawson KA, Wilmut I, Pennings S. Histone H4K20me3 and HP1a are late heterochromatin markers in development, but present in undifferentiated embryonic stem cells. J Cell Sci 2011; 124:1878-90;PMID:21576353; http://dx.doi.org/10.1242/jcs.080721.
51. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, et al. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 2001; 98:13734-8;PMID:11717434; http://dx.doi.org/10.1073/pnas.241522698.
52. Bonk AJ, Li R, Lai L, Hao Y, Liu Z, Samuel M, et al. Aberrant DNA methylation in porcine in vitro-, parthenogenetic- and somatic cell nuclear transfer-produced blastocysts. Mol Reprod Dev 2008; 75:250-64;PMID:17595009; http://dx.doi.org/10.1002/mrd.20786.
53. Abell AN, Granger DA, Johnson NL, Vincent-Jordan N, Dibble C F, Johnson GL. Trophoblast stem cell maintenance by fibroblast growth factor 4 requires MEKK4 activation of Jun N-terminal kinase. Mol Cell Biol 2009; 29:2748-61;PMID:19289495; http://dx.doi.org/10.1128/MCB.01391-08.
54. Fazzari MJ, Greally JM. Epigenomics: beyond CpG islands. Nat Rev Genet 2004; 5:446-55;PMID:15153997; http://dx.doi.org/10.1038/nrg1349.
55. Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. Molecular basis of base substitution hotspots in Escherichia coli. Nature 1978; 274:775-80;PMID:355893; http://dx.doi.org/10.1038/274775a0.
56. Rossant J, Sanford J P, Chapman VM, Andrews GK. Undermethylation of structural gene sequences in extraembryonic lineages of the mouse. Dev Biol 1986; 117:567-73;PMID:2428685; http://dx.doi.org/10.1016/0012-1606(86)90325-8.
57. Ohgane J, Hattori N, Oda M, Tanaka S, Shiota K. Differentiation of trophoblast lineage is associated with DNA methylation and demethylation. Biochem Biophys Res Commun 2002; 290:701-6;PMID:11785956; http://dx.doi.org/10.1006/bbrc.2001.6258.
58. Fulka H, Mrazek M, Tepla O, Fulka J. DNA methyl-ation pattern in human zygotes and developing embryos. Reproduction 2004; 128:703-8;PMID:15579587; http://dx.doi.org/10.1530/rep.1.00217.
59. Nagy A, Gertstensen M, Vintersten K, Behringer R. Manipulating the Mouse Embryo. New York: Cold Spring Harbor Laboratory Press 2003.
60. Kawase E, Suemori H, Takahashi N, Okazaki K, Hashimoto K, Nakatsuji N. Strain difference in establishment of mouse embryonic stem (ES) cell lines. Int J Dev Biol 1994; 38:385-90;PMID:7981049.
61. Oda M, Shiota K, Tanaka S. Trophoblast stem cells. Methods Enzymol 2006; 419:387-400;PMID:17141063; http://dx.doi.org/10.1016/S0076-6879(06)19015-1.
62. Matise M P, Auerbach W, Joyner AL. Gene targeting: A Practical Approach Second Edition. New York: Oxford University Press 2000.
63. Kumaki Y, Oda M, Okano M. QUMA: quantification tool for methylation analysis. Nucleic Acids Res 2008; 36:170-5;PMID:18487274; http://dx.doi.org/10.1093/nar/gkn294.