Placental imprinting: Emerging mechanisms and functions
Autoři:
Courtney W. Hanna aff001
Působiště autorů:
Centre for Trophoblast Research, Department of Physiology, Development, and Neuroscience, University of Cambridge, Cambridge, United Kingdom
aff001; Epigenetics Programme, Babraham Institute, Cambridge, United Kingdom
aff002
Vyšlo v časopise:
Placental imprinting: Emerging mechanisms and functions. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008709
Kategorie:
Review
doi:
https://doi.org/10.1371/journal.pgen.1008709
Souhrn
As the maternal–foetal interface, the placenta is essential for the establishment and progression of healthy pregnancy, regulating both foetal growth and maternal adaptation to pregnancy. The evolution and functional importance of genomic imprinting are inextricably linked to mammalian placentation. Recent technological advances in mapping and manipulating the epigenome in embryogenesis in mouse models have revealed novel mechanisms regulating genomic imprinting in placental trophoblast, the physiological implications of which are only just beginning to be explored. This review will highlight important recent discoveries and exciting new directions in the study of placental imprinting.
Klíčová slova:
DNA methylation – Epigenetics – Gene expression – Gene regulation – Genetic loci – Genomic imprinting – Mouse models – Trophoblasts
Zdroje
1. Liu Y, Fan X, Wang R, Lu X, Dang YL, Wang H, et al. Single-cell RNA-seq reveals the diversity of trophoblast subtypes and patterns of differentiation in the human placenta. Cell Res. 2018;28: 819–832. doi: 10.1038/s41422-018-0066-y 30042384
2. Suryawanshi H, Morozov P, Straus A, Sahasrabudhe N, Max KEA, Garzia A, et al. A single-cell survey of the human first-trimester placenta and decidua. Sci Adv. 2018;4: eaau4788. doi: 10.1126/sciadv.aau4788 30402542
3. Vento-Tormo R, Efremova M, Botting RA, Turco MY, Vento-Tormo M, Meyer KB, et al. Single-cell reconstruction of the early maternal-fetal interface in humans. Nature. 2018;563: 347–353. doi: 10.1038/s41586-018-0698-6 30429548
4. Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991;7: 45–49. doi: 10.1016/0168-9525(91)90230-N 2035190
5. Babak T, DeVeale B, Tsang EK, Zhou Y, Li X, Smith KS, et al. Genetic conflict reflected in tissue-specific maps of genomic imprinting in human and mouse. Nat Genet. 2015;47: 544–549. doi: 10.1038/ng.3274 25848752
6. Peters J. The role of genomic imprinting in biology and disease: an expanding view. Nat Rev Genet. 2014;15: 517–530. doi: 10.1038/nrg3766 24958438
7. White CR, MacDonald WA, Mann MR. Conservation of DNA Methylation Programming Between Mouse and Human Gametes and Preimplantation Embryos. Biol Reprod. 2016;95: 61. doi: 10.1095/biolreprod.116.140319 27465133
8. Latos PA, Pauler FM, Koerner MV, Senergin HB, Hudson QJ, Stocsits RR, et al. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Science. 2012;338: 1469–1472. doi: 10.1126/science.1228110 23239737
9. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature. 2000;405: 486–489. doi: 10.1038/35013106 10839547
10. Wood AJ, Schulz R, Woodfine K, Koltowska K, Beechey CV, Peters J, et al. Regulation of alternative polyadenylation by genomic imprinting. Genes Dev. 2008;22: 1141–1146. doi: 10.1101/gad.473408 18451104
11. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH, et al. Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell. 2008;15: 668–679. doi: 10.1016/j.devcel.2008.08.015 18848501
12. Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature. 1984;308: 548–550. doi: 10.1038/308548a0 6709062
13. McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell. 1984;37: 179–183. doi: 10.1016/0092-8674(84)90313-1 6722870
14. Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse H19 gene. Nature. 1991;351: 153–155. doi: 10.1038/351153a0 1709450
15. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science. 2001;294: 2536–2539. doi: 10.1126/science.1065848 11719692
16. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature. 2004;429: 900–903. doi: 10.1038/nature02633 15215868
17. Veselovska L, Smallwood SA, Saadeh H, Stewart KR, Krueger F, Maupetit-Mehouas S, et al. Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol. 2015;16: 209-015–0769-z.
18. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43: 811–814. doi: 10.1038/ng.864 21706000
19. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012;8: e1002440. doi: 10.1371/journal.pgen.1002440 22242016
20. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol. 2002;241: 172–182. doi: 10.1006/dbio.2001.0501 11784103
21. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, et al. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol Cell. 2011;44: 361–372. doi: 10.1016/j.molcel.2011.08.032 22055183
22. Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science. 2012;335: 1499–1502. doi: 10.1126/science.1216154 22442485
23. Takahashi N, Coluccio A, Thorball CW, Planet E, Shi H, Offner S, et al. ZNF445 is a primary regulator of genomic imprinting. Genes Dev. 2019;33: 49–54. doi: 10.1101/gad.320069.118 30602440
24. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99: 247–257. doi: 10.1016/s0092-8674(00)81656-6 10555141
25. Decato BE, Lopez-Tello J, Sferruzzi-Perri AN, Smith AD, Dean MD. DNA Methylation Divergence and Tissue Specialization in the Developing Mouse Placenta. Mol Biol Evol. 2017;34: 1702–1712. doi: 10.1093/molbev/msx112 28379409
26. Proudhon C, Duffie R, Ajjan S, Cowley M, Iranzo J, Carbajosa G, et al. Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol Cell. 2012;47: 909–920. doi: 10.1016/j.molcel.2012.07.010 22902559
27. Ferguson-Smith AC. Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet. 2011;12: 565–575. doi: 10.1038/nrg3032 21765458
28. Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L, Krebs AR, et al. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature. 2015;520: 243–247. doi: 10.1038/nature14176 25607372
29. Fan T, Hagan JP, Kozlov SV, Stewart CL, Muegge K. Lsh controls silencing of the imprinted Cdkn1c gene. Development. 2005;132: 635–644. doi: 10.1242/dev.01612 15647320
30. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, et al. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet. 2004;36: 1291–1295. doi: 10.1038/ng1468 15516931
31. Sato S, Yoshida W, Soejima H, Nakabayashi K, Hata K. Methylation dynamics of IG-DMR and Gtl2-DMR during murine embryonic and placental development. Genomics. 2011;98: 120–127. doi: 10.1016/j.ygeno.2011.05.003 21620950
32. Okae H, Matoba S, Nagashima T, Mizutani E, Inoue K, Ogonuki N, et al. RNA sequencing-based identification of aberrant imprinting in cloned mice. Hum Mol Genet. 2014;23: 992–1001. doi: 10.1093/hmg/ddt495 24105465
33. Inoue A, Jiang L, Lu F, Suzuki T, Zhang Y. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature. 2017;547: 419–424. doi: 10.1038/nature23262 28723896
34. Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013;152: 1308–1323. doi: 10.1016/j.cell.2013.02.016 23498939
35. Duffie R, Ajjan S, Greenberg MV, Zamudio N, Escamilla del Arenal M, Iranzo J, et al. The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals. Genes Dev. 2014;28: 463–478. doi: 10.1101/gad.232058.113 24589776
36. Andergassen D, Dotter CP, Wenzel D, Sigl V, Bammer PC, Muckenhuber M, et al. Mapping the mouse Allelome reveals tissue-specific regulation of allelic expression. Elife. 2017;6: doi: 10.7554/eLife.25125 28806168
37. Calabrese JM, Starmer J, Schertzer MD, Yee D, Magnuson T. A survey of imprinted gene expression in mouse trophoblast stem cells. G3 (Bethesda). 2015;5: 751–759.
38. Okae H, Hiura H, Nishida Y, Funayama R, Tanaka S, Chiba H, et al. Re-investigation and RNA sequencing-based identification of genes with placenta-specific imprinted expression. Hum Mol Genet. 2012;21: 548–558. doi: 10.1093/hmg/ddr488 22025075
39. Hanna CW, Pérez-Palacios R, Gahurova L, Schubert M, Krueger F, Biggins L, et al. Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues. Genome Biol. 2019;20(1): 225. doi: 10.1186/s13059-019-1833-x 31665063
40. Hudson QJ, Seidl CI, Kulinski TM, Huang R, Warczok KE, Bittner R, et al. Extra-embryonic-specific imprinted expression is restricted to defined lineages in the post-implantation embryo. Dev Biol. 2011;353: 420–431. doi: 10.1016/j.ydbio.2011.02.017 21354127
41. Kobayashi H, Yamada K, Morita S, Hiura H, Fukuda A, Kagami M, et al. Identification of the mouse paternally expressed imprinted gene Zdbf2 on chromosome 1 and its imprinted human homolog ZDBF2 on chromosome 2. Genomics. 2009;93: 461–472. doi: 10.1016/j.ygeno.2008.12.012 19200453
42. Greenberg MV, Glaser J, Borsos M, Marjou FE, Walter M, Teissandier A, et al. Transient transcription in the early embryo sets an epigenetic state that programs postnatal growth. Nat Genet. 2017;49: 110–118. doi: 10.1038/ng.3718 27841881
43. Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature. 2002;415: 810–813. doi: 10.1038/415810a 11845212
44. Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet. 2002;32: 426–431. doi: 10.1038/ng988 12410230
45. Andergassen D, Muckenhuber M, Bammer PC, Kulinski TM, Theussl HC, Shimizu T, et al. The Airn lncRNA does not require any DNA elements within its locus to silence distant imprinted genes. PLoS Genet. 2019;15: e1008268. doi: 10.1371/journal.pgen.1008268 31329595
46. Mager J, Montgomery ND, de Villena FP, Magnuson T. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat Genet. 2003;33: 502–507. doi: 10.1038/ng1125 12627233
47. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science. 2008;322: 1717–1720. doi: 10.1126/science.1163802 18988810
48. Wagschal A, Sutherland HG, Woodfine K, Henckel A, Chebli K, Schulz R, et al. G9a histone methyltransferase contributes to imprinting in the mouse placenta. Mol Cell Biol. 2008;28: 1104–1113. doi: 10.1128/MCB.01111-07 18039842
49. Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, et al. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet. 2004;36: 1296–1300. doi: 10.1038/ng1467 15516932
50. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, et al. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell. 2008;32: 232–246. doi: 10.1016/j.molcel.2008.08.022 18951091
51. Schertzer MD, Braceros KCA, Starmer J, Cherney RE, Lee DM, Salazar G, et al. lncRNA-Induced Spread of Polycomb Controlled by Genome Architecture, RNA Abundance, and CpG Island DNA. Mol Cell. 2019;75(3): 523–537. doi: 10.1016/j.molcel.2019.05.028 31256989
52. Inoue A, Chen Z, Yin Q, Zhang Y. Maternal Eed knockout causes loss of H3K27me3 imprinting and random X inactivation in the extraembryonic cells. Genes Dev. 2018;32: 1525–1536. doi: 10.1101/gad.318675.118 30463900
53. Zheng H, Huang B, Zhang B, Xiang Y, Du Z, Xu Q, et al. Resetting Epigenetic Memory by Reprogramming of Histone Modifications in Mammals. Mol Cell. 2016;63: 1066–1079. doi: 10.1016/j.molcel.2016.08.032 27635762
54. Kaneko-Ishino T, Ishino F. Mammalian-specific genomic functions: Newly acquired traits generated by genomic imprinting and LTR retrotransposon-derived genes in mammals. Proc Jpn Acad Ser B Phys Biol Sci. 2015;91: 511–538. doi: 10.2183/pjab.91.511 26666304
55. Brind'Amour J, Kobayashi H, Richard Albert J, Shirane K, Sakashita A, Kamio A, et al. LTR retrotransposons transcribed in oocytes drive species-specific and heritable changes in DNA methylation. Nat Commun. 2018;9: 3331. doi: 10.1038/s41467-018-05841-x 30127397
56. Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science. 2011;332: 848–852. doi: 10.1126/science.1203919 21566194
57. Bogutz AB, Brind'Amour J, Kobayashi H, Jensen KN, Nakabayashi K, Imai H, et al. Evolution of imprinting via lineage-specific insertion of retroviral promoters. Nat Commun. 2019;10: 5674. doi: 10.1038/s41467-019-13662-9 31831741
58. Chuong EB, Rumi MA, Soares MJ, Baker JC. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet. 2013;45: 325–329. doi: 10.1038/ng.2553 23396136
59. Todd CD, Deniz O, Taylor D, Branco MR. Functional evaluation of transposable elements as enhancers in mouse embryonic and trophoblast stem cells. Elife. 2019;8. doi: 10.7554/eLife.44344 31012843
60. Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature. 2000;403: 785–789. doi: 10.1038/35001608 10693809
61. Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, et al. Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet. 2008;40: 243–248. doi: 10.1038/ng.2007.51 18176565
62. Cohen CJ, Rebollo R, Babovic S, Dai EL, Robinson WP, Mager DL. Placenta-specific expression of the interleukin-2 (IL-2) receptor beta subunit from an endogenous retroviral promoter. J Biol Chem. 2011;286: 35543–35552. doi: 10.1074/jbc.M111.227637 21865161
63. Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol. 2014;6. doi: 10.1101/cshperspect.a018382 24492710
64. Hu D, Cross JC. Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010;54: 341–354. doi: 10.1387/ijdb.082768dh 19876834
65. Itoh M, Yoshida Y, Nishida K, Narimatsu M, Hibi M, Hirano T. Role of Gab1 in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol Cell Biol. 2000;20: 3695–3704. doi: 10.1128/mcb.20.10.3695-3704.2000 10779359
66. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature. 2002;417: 945–948. doi: 10.1038/nature00819 12087403
67. Sibley CP, Coan PM, Ferguson-Smith AC, Dean W, Hughes J, Smith P, et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci U S A. 2004;101: 8204–8208. doi: 10.1073/pnas.0402508101 15150410
68. Woods L, Perez-Garcia V, Hemberger M. Regulation of Placental Development and Its Impact on Fetal Growth-New Insights From Mouse Models. Front Endocrinol (Lausanne). 2018;9: 570.
69. Miri K, Latham K, Panning B, Zhong Z, Andersen A, Varmuza S. The imprinted polycomb group gene Sfmbt2 is required for trophoblast maintenance and placenta development. Development. 2013;140: 4480–4489. doi: 10.1242/dev.096511 24154523
70. Tang P, Miri K, Varmuza S. Unique trophoblast chromatin environment mediated by the PcG protein SFMBT2. Biol Open. 2019;8. doi: 10.1242/bio.043638 31391163
71. Senner CE, Krueger F, Oxley D, Andrews S, Hemberger M. DNA methylation profiles define stem cell identity and reveal a tight embryonic-extraembryonic lineage boundary. Stem Cells. 2012;30: 2732–2745. doi: 10.1002/stem.1249 23034951
72. Inoue K, Hirose M, Inoue H, Hatanaka Y, Honda A, Hasegawa A, et al. The Rodent-Specific MicroRNA Cluster within the Sfmbt2 Gene Is Imprinted and Essential for Placental Development. Cell Rep. 2017;19: 949–956. doi: 10.1016/j.celrep.2017.04.018 28467908
73. Bogutz AB, Oh-McGinnis R, Jacob KJ, Ho-Lau R, Gu T, Gertsenstein M, et al. Transcription factor ASCL2 is required for development of the glycogen trophoblast cell lineage. PLoS Genet. 2018;14: e1007587. doi: 10.1371/journal.pgen.1007587 30096149
74. Oh-McGinnis R, Bogutz AB, Lefebvre L. Partial loss of Ascl2 function affects all three layers of the mature placenta and causes intrauterine growth restriction. Dev Biol. 2011;351: 277–286. doi: 10.1016/j.ydbio.2011.01.008 21238448
75. Tunster SJ, McNamara GI, Creeth HDJ, John RM. Increased dosage of the imprinted Ascl2 gene restrains two key endocrine lineages of the mouse Placenta. Dev Biol. 2016;418: 55–65. doi: 10.1016/j.ydbio.2016.08.014 27542691
76. Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC. Origin and characteristics of glycogen cells in the developing murine placenta. Dev Dyn. 2006;235: 3280–3294. doi: 10.1002/dvdy.20981 17039549
77. Tunster SJ, Creeth HDJ, John RM. The imprinted Phlda2 gene modulates a major endocrine compartment of the placenta to regulate placental demands for maternal resources. Dev Biol. 2016;409: 251–260. doi: 10.1016/j.ydbio.2015.10.015 26476147
78. Salas M, John R, Saxena A, Barton S, Frank D, Fitzpatrick G, et al. Placental growth retardation due to loss of imprinting of Phlda2. Mech Dev. 2004;121: 1199–1210. doi: 10.1016/j.mod.2004.05.017 15327781
79. Burton GJ, Jauniaux E. What is the placenta? Am J Obstet Gynecol. 2015;213: S6.e1, S6–8.
80. Creeth HDJ, McNamara GI, Tunster SJ, Boque-Sastre R, Allen B, Sumption L, et al. Maternal care boosted by paternal imprinting in mammals. PLoS Biol. 2018;16: e2006599. doi: 10.1371/journal.pbio.2006599 30063711
81. Monteagudo-Sanchez A, Sanchez-Delgado M, Mora JRH, Santamaria NT, Gratacos E, Esteller M, et al. Differences in expression rather than methylation at placenta-specific imprinted loci is associated with intrauterine growth restriction. Clin Epigenetics. 2019;11: 35-019-0630–4.
82. Okae H, Toh H, Sato T, Hiura H, Takahashi S, Shirane K, et al. Derivation of Human Trophoblast Stem Cells. Cell Stem Cell. 2018;22: 50–63.e6. doi: 10.1016/j.stem.2017.11.004 29249463
83. Haider S, Meinhardt G, Saleh L, Kunihs V, Gamperl M, Kaindl U, et al. Self-Renewing Trophoblast Organoids Recapitulate the Developmental Program of the Early Human Placenta. Stem Cell Reports. 2018;11: 537–551. doi: 10.1016/j.stemcr.2018.07.004 30078556
84. Turco MY, Gardner L, Kay RG, Hamilton RS, Prater M, Hollinshead MS, et al. Trophoblast organoids as a model for maternal-fetal interactions during human placentation. Nature. 2018;564: 263–267. doi: 10.1038/s41586-018-0753-3 30487605
85. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell. 2013;154: 442–451. doi: 10.1016/j.cell.2013.06.044 23849981
86. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell. 2013;152: 1173–1183. doi: 10.1016/j.cell.2013.02.022 23452860
87. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, et al. Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation. Cell. 2014;159: 647–661. doi: 10.1016/j.cell.2014.09.029 25307932
88. Cheng AW, Wang H, Yang H, Shi L, Katz Y, Theunissen TW, et al. Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res. 2013;23: 1163–1171. doi: 10.1038/cr.2013.122 23979020
89. Hanna CW, Penaherrera MS, Saadeh H, Andrews S, McFadden DE, Kelsey G, et al. Pervasive polymorphic imprinted methylation in the human placenta. Genome Res. 2016;26: 756–767. doi: 10.1101/gr.196139.115 26769960
90. Hamada H, Okae H, Toh H, Chiba H, Hiura H, Shirane K, et al. Allele-Specific Methylome and Transcriptome Analysis Reveals Widespread Imprinting in the Human Placenta. Am J Hum Genet. 2016;99: 1045–1058. doi: 10.1016/j.ajhg.2016.08.021 27843122
91. Sanchez-Delgado M, Court F, Vidal E, Medrano J, Monteagudo-Sanchez A, Martin-Trujillo A, et al. Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting. PLoS Genet. 2016;12: e1006427. doi: 10.1371/journal.pgen.1006427 27835649
92. Xia W, Xu J, Yu G, Yao G, Xu K, Ma X, et al. Resetting histone modifications during human parental-to-zygotic transition. Science. 2019;365: 353–360. doi: 10.1126/science.aaw5118 31273069
93. Zhang W, Chen Z, Yin Q, Zhang D, Racowsky C, Zhang Y. Maternal-biased H3K27me3 correlates with paternal-specific gene expression in the human morula. Genes Dev. 2019;33: 382–387. doi: 10.1101/gad.323105.118 30808660
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 4
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- Analysis of genes within the schizophrenia-linked 22q11.2 deletion identifies interaction of night owl/LZTR1 and NF1 in GABAergic sleep control
- High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements
- Molecular genetics of maternally-controlled cell divisions
- Spastin mutations impair coordination between lipid droplet dispersion and reticulum