Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas

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The placenta is vital for the proper development of the fetus, not only facilitating the exchange of nutrients, oxygen, and waste between the mother and the fetus but also acting as an interface to the maternal immune system and regulating fetal growth by excreting hormones and growth factors. DNA methylation is important for both placental and embryonic development as loss of proteins involved in DNA methylation can result in placental dysmorphology and early embryonic death. The human placenta has a unique DNA methylation landscape characterized by alternating regions of low methylation, covering silent genes with tissue-specific developmental functions, and high methylation, covering active genes. In order to better understand the significance of this DNA methylation landscape in the human placenta, we performed a cross-species comparison of DNA methylation in mammalian placentas, oocytes, and early embryos from this and other studies. Although the levels and extent of hypomethylation differed between mammalian placentas, what we found to be highly conserved was relatively higher methylation levels over active genes. These same genes also had high methylation in the opossum extraembryonic membrane, a primitive placenta, as well as oocytes and early embryos, suggesting that high methylation over these genes predated placental mammals and is established very early in development.

Vyšlo v časopise: Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005442
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005442

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1. Carter AM, Enders AC (2004) Comparative aspects of trophoblast development and placentation. Reproductive biology and endocrinology: RB&E 2: 46. 15236656

2. Turner (1876) Some General Observations on the Placenta, with especial reference to the Theory of Evolution. Journal of anatomy and physiology 11: 33–53. 17231137

3. Carter AM (2012) Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol Rev 92: 1543–1576. doi: 10.1152/physrev.00040.2011 23073626

4. Padykula HA, Taylor JM (1982) Marsupial placentation and its evolutionary significance. Journal of reproduction and fertility Supplement 31: 95–104. 6762435

5. Selwood L, Johnson MH (2006) Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins. BioEssays: news and reviews in molecular, cellular and developmental biology 28: 128–145.

6. Renfree MB (2010) Review: Marsupials: placental mammals with a difference. Placenta 31 Suppl: S21–26. doi: 10.1016/j.placenta.2009.12.023 20079531

7. Graves JA, Renfree MB (2013) Marsupials in the age of genomics. Annual review of genomics and human genetics 14: 393–420. doi: 10.1146/annurev-genom-091212-153452 23834319

8. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, et al. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429: 900–903. 15215868

9. Arima T, Hata K, Tanaka S, Kusumi M, Li E, et al. (2006) Loss of the maternal imprint in Dnmt3Lmat-/- mice leads to a differentiation defect in the extraembryonic tissue. Dev Biol 297: 361–373. 16920095

10. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536–2539. 11719692

11. Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129: 1983–1993. 11934864

12. Ding F, Patel C, Ratnam S, McCarrey JR, Chaillet JR (2003) Conservation of Dnmt1o cytosine methyltransferase in the marsupial Monodelphis domestica. Genesis 36: 209–213. 12929092

13. McGraw S, Oakes CC, Martel J, Cirio MC, de Zeeuw P, et al. (2013) Loss of DNMT1o disrupts imprinted X chromosome inactivation and accentuates placental defects in females. PLoS genetics 9: e1003873. doi: 10.1371/journal.pgen.1003873 24278026

14. Himes KP, Koppes E, Chaillet JR (2013) Generalized disruption of inherited genomic imprints leads to wide-ranging placental defects and dysregulated fetal growth. Developmental Biology 373: 72–82. doi: 10.1016/j.ydbio.2012.10.010 23085235

15. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC, et al. (1982) Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 10: 2709–2721. 7079182

16. Fuke C, Shimabukuro M, Petronis A, Sugimoto J, Oda T, et al. (2004) Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Annals of human genetics 68: 196–204. 15180700

17. Cotton AM, Avila L, Penaherrera MS, Affleck JG, Robinson WP, et al. (2009) Inactive X chromosome-specific reduction in placental DNA methylation. Hum Mol Genet 18: 3544–3552. doi: 10.1093/hmg/ddp299 19586922

18. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, et al. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463: 1101–1105. doi: 10.1038/nature08829 20098412

19. Hon GC, Rajagopal N, Shen Y, McCleary DF, Yue F, et al. (2013) Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nature Genetics 45: 1198–1206. doi: 10.1038/ng.2746 23995138

20. Chu T, Handley D, Bunce K, Surti U, Hogge WA, et al. (2011) Structural and regulatory characterization of the placental epigenome at its maternal interface. PLoS One 6: e14723. doi: 10.1371/journal.pone.0014723 21373191

21. Schroeder DI, Blair JD, Lott P, Yu HO, Hong D, et al. (2013) The human placenta methylome. Proceedings of the National Academy of Sciences of the United States of America 110: 6037–6042. doi: 10.1073/pnas.1215145110 23530188

22. Ng HK, Novakovic B, Hiendleder S, Craig JM, Roberts CT, et al. (2010) Distinct patterns of gene-specific methylation in mammalian placentas: implications for placental evolution and function. Placenta 31: 259–268. doi: 10.1016/j.placenta.2010.01.009 20167366

23. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, et al. (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS genetics 8: e1002440. doi: 10.1371/journal.pgen.1002440 22242016

24. Wang L, Zhang J, Duan J, Gao X, Zhu W, et al. (2014) Programming and inheritance of parental DNA methylomes in mammals. Cell 157: 979–991. doi: 10.1016/j.cell.2014.04.017 24813617

25. Guo H, Zhu P, Yan L, Li R, Hu B, et al. (2014) The DNA methylation landscape of human early embryos. Nature 511: 606–610. doi: 10.1038/nature13544 25079557

26. Lee HJ, Hore TA, Reik W (2014) Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 14: 710–719. doi: 10.1016/j.stem.2014.05.008 24905162

27. Okae H, Chiba H, Hiura H, Hamada H, Sato A, et al. (2014) Genome-Wide Analysis of DNA Methylation Dynamics during Early Human Development. PLoS genetics 10: e1004868. doi: 10.1371/journal.pgen.1004868 25501653

28. Rugg-Gunn PJ (2012) Epigenetic features of the mouse trophoblast. Reproductive biomedicine online 25: 21–30. doi: 10.1016/j.rbmo.2012.01.012 22578826

29. Court F, Tayama C, Romanelli V, Martin-Trujillo A, Iglesias-Platas I, et al. (2014) Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Research 24: 554–569. doi: 10.1101/gr.164913.113 24402520

30. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, et al. (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505: 635–640. doi: 10.1038/nature12943 24463510

31. Wang X, Miller DC, Harman R, Antczak DF, Clark AG (2013) Paternally expressed genes predominate in the placenta. Proceedings of the National Academy of Sciences of the United States of America 110: 10705–10710. doi: 10.1073/pnas.1308998110 23754418

32. Sarkar AA, Nuwayhid SJ, Maynard T, Ghandchi F, Hill JT, et al. (2014) Hectd1 is required for development of the junctional zone of the placenta. Developmental Biology 392: 368–380. doi: 10.1016/j.ydbio.2014.05.007 24855001

33. Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, et al. (2014) Fine mapping of genome activation in bovine embryos by RNA sequencing. Proceedings of the National Academy of Sciences of the United States of America 111: 4139–4144. doi: 10.1073/pnas.1321569111 24591639

34. Reich A, Klatsky P, Carson S, Wessel G (2011) The transcriptome of a human polar body accurately reflects its sibling oocyte. The Journal of biological chemistry 286: 40743–40749. doi: 10.1074/jbc.M111.289868 21953461

35. Ziller MJ, Hansen KD, Meissner A, Aryee MJ (2015) Coverage recommendations for methylation analysis by whole-genome bisulfite sequencing. Nat Methods 12: 230–232, 231 p following 232. doi: 10.1038/nmeth.3152 25362363

36. Gaidatzis D, Burger L, Murr R, Lerch A, Dessus-Babus S, et al. (2014) DNA sequence explains seemingly disordered methylation levels in partially methylated domains of Mammalian genomes. PLoS genetics 10: e1004143. doi: 10.1371/journal.pgen.1004143 24550741

37. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, et al. (2011) Increased methylation variation in epigenetic domains across cancer types. Nature Genetics 43: 768–775. doi: 10.1038/ng.865 21706001

38. Hon GC, Hawkins RD, Caballero OL, Lo C, Lister R, et al. (2012) Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Research 22: 246–258. doi: 10.1101/gr.125872.111 22156296

39. Berman BP, Weisenberger DJ, Aman JF, Hinoue T, Ramjan Z, et al. (2012) Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nature Genetics 44: 40–46.

40. Timp W, Bravo HC, McDonald OG, Goggins M, Umbricht C, et al. (2014) Large hypomethylated blocks as a universal defining epigenetic alteration in human solid tumors. Genome medicine 6: 61. doi: 10.1186/s13073-014-0061-y 25191524

41. Hansen KD, Sabunciyan S, Langmead B, Nagy N, Curley R, et al. (2014) Large-scale hypomethylated blocks associated with Epstein-Barr virus-induced B-cell immortalization. Genome Research 24: 177–184. doi: 10.1101/gr.157743.113 24068705

42. Marzese DM, Scolyer RA, Huynh JL, Huang SK, Hirose H, et al. (2014) Epigenome-wide DNA methylation landscape of melanoma progression to brain metastasis reveals aberrations on homeobox D cluster associated with prognosis. Human Molecular Genetics 23: 226–238. doi: 10.1093/hmg/ddt420 24014427

43. van Dijk M, Visser A, Posthuma J, Poutsma A, Oudejans CB (2012) Naturally occurring variation in trophoblast invasion as a source of novel (epigenetic) biomarkers. Frontiers in genetics 3: 22. doi: 10.3389/fgene.2012.00022 22363344

44. Rousseaux S, Debernardi A, Jacquiau B, Vitte AL, Vesin A, et al. (2013) Ectopic activation of germline and placental genes identifies aggressive metastasis-prone lung cancers. Science translational medicine 5: 186ra166.

45. Novakovic B, Saffery R (2013) Placental pseudo-malignancy from a DNA methylation perspective: unanswered questions and future directions. Frontiers in genetics 4: 285. doi: 10.3389/fgene.2013.00285 24368911

46. Wang X, Douglas KC, Vandeberg JL, Clark AG, Samollow PB (2014) Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica. Genome Research 24: 70–83. doi: 10.1101/gr.161919.113 24065774

47. Douglas GC, King BF (1990) Isolation and morphologic differentiation in vitro of villous cytotrophoblast cells from rhesus monkey placenta. In Vitro Cell Dev Biol 26: 754–758. 2394671

48. Soghomonians A, Barakat AI, Thirkill TL, Blankenship TN, Douglas GC (2002) Effect of shear stress on migration and integrin expression in macaque trophoblast cells. Biochimica et biophysica acta 1589: 233–246. 12031791

49. Kumar P, Lindberg L, Thirkill TL, Ji JW, Martsching L, et al. (2012) The MUC1 extracellular domain subunit is found in nuclear speckles and associates with spliceosomes. PloS one 7: e42712. doi: 10.1371/journal.pone.0042712 22905162

50. Chen PY, Cokus SJ, Pellegrini M (2010) BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 11: 203. doi: 10.1186/1471-2105-11-203 20416082

51. Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Research 42: D764–770. doi: 10.1093/nar/gkt1168 24270787