Biased Expression of Parental Alleles in the Human Placenta
- Authors: Sazhenova E.A.1, Vasilev S.A.1, Lebedev I.N.1
-
Affiliations:
- Research Institute of Medical Genetics, Tomsk National Research Medical Center of the Russian Academy of Sciences
- Issue: Vol 59, No 3 (2023)
- Pages: 249-265
- Section: ОБЗОРНЫЕ И ТЕОРЕТИЧЕСКИЕ СТАТЬИ
- URL: https://journals.rcsi.science/0016-6758/article/view/134563
- DOI: https://doi.org/10.31857/S001667582302011X
- EDN: https://elibrary.ru/KYGICR
- ID: 134563
Cite item
Abstract
The biased expression of parental alleles plays a fundamental role in the formation of the placenta as a multifunctional organ necessary for the development and survival of the fetus. First of all, this is expressed in the phenomenon of imprinting, when only the maternal or paternal allele is expressed in placental cells. The placenta uses an extended range of imprinting mechanisms compared to the embryo – histone modifications that suppress or, conversely, activate the expression of nearby genes, regulatory sequences and genes derived from retroviruses or retrotransposons, microRNAs that function as antisense RNAs and participate in transcriptional and post-transcriptional regulation of gene expression. In addition, incomplete suppression of the activity of one of the parental alleles is detected in the placenta, leading to a biased imprinted expression of some genes. This review shows the role of biased expression of parental alleles in the development of placental structures of an embryo, discusses the mechanisms of epigenetic control of parental alleles, mainly expressed in the placenta.
About the authors
E. A. Sazhenova
Research Institute of Medical Genetics, Tomsk National Research MedicalCenter of the Russian Academy of Sciences
Author for correspondence.
Email: elena.sazhenova@medgenetics.ru
Russia, 634050, Tomsk
S. A. Vasilev
Research Institute of Medical Genetics, Tomsk National Research MedicalCenter of the Russian Academy of Sciences
Email: elena.sazhenova@medgenetics.ru
Russia, 634050, Tomsk
I. N. Lebedev
Research Institute of Medical Genetics, Tomsk National Research MedicalCenter of the Russian Academy of Sciences
Email: elena.sazhenova@medgenetics.ru
Russia, 634050, Tomsk
References
- Gui B., Slone J., Huang T. Perspective: Is random monoallelic expression a contributor to phenotypic variability of autosomal dominant disorders? // Front. Genet. 2017. V. 29(8). P. e191. https://doi.org/10.3389/fgene.2017.00191
- Pilvar D., Reiman M., Pilvar A., Laan M. Parent-of-origin-specific allelic expression in the human placenta is limited to established imprinted loci and it is stably maintained across pregnancy // Clin. Epigenet. 2019. V. 11. P. e94. https://doi.org/10.1186/s13148-019-0692-3
- Tucci V., Isles A.R., Kelsey G. et al. Genomic imprinting and physiological processes in mammals // Cell. 2019. V. 176. P. 952–965. https://doi.org/10.1016/j.cell.2019.01.043
- Bogutz A.B., Brind A.J., Kobayashi H. et al. Evolution of imprinting via lineage-specific insertion of retroviral promoters // Nat. Commun. 2019. V. 10. P. e5674. https://doi.org/10.1038/s41467-019-13662-9
- Raas M.W., Zijlmans D.W., Vermeulen M. et al. There is another: H3K27me3-mediated genomic imprinting // Trends Genet. 2022. V. 38(1). P. 82–96. https://doi.org/10.1016/j.tig.2021.06.017
- Cierna Z., Varga I., Danihel L.J. et al. Intermediate trophoblast-A distinctive, unique and often unrecognized population of trophoblastic cells // Ann. Anat. 2016. V. 204. P. 45–50. https://doi.org/10.1016/j.aanat.2015.10.003
- Norwitz E.R. Defective implantation and placentation: Laying the blueprint for pregnancy complications // Reprod. Biomed. Online. 2006. V. 13(4). P. 591–599. https://doi.org/10.1016/s1472-6483(10)60649-9
- Thamban T., Agarwaal V., Khosla S. Role of genomic imprinting in mammalian development // J. Biosci. 2020. V. 45. P. e20.
- Varrault A., Dantec C., Le Digarcher A. et al. Identification of Plagl1/Zac1 binding sites and target genes establishes its role in the regulation of extracellular matrix genes and the imprinted gene network // Nucl. Acids Res. 2017. V. 45(18). P. 10466–10480. https://doi.org/10.1093/nar/gkx672
- Hanna C.W. Placental imprinting: Emerging mechanisms and functions // PLoS Genet. 2020. V. 16(4). P. e1008709. https://doi.org/10.1371/journal.pgen.1008709
- Starks R.R., Kaur H., Tuteja G. Mapping cis-regulatory elements in the midgestation mouse placenta // Sci. Rep. 2021. V. 11. P. e22331. https://doi.org/10.1038/s41598-021-01664-x
- 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. V. 9. P. e570. https://doi.org/10.3389/fendo.2018.00570
- Miri K., Latham K., Panning B. et al. The imprinted polycomb group gene Sfmbt2 is required for trophoblast maintenance and placenta development // Development. 2013. V. 140. P. 4480–4489. https://doi.org/10.1242/dev.096511
- Tang P., Miri K., Varmuza S. Unique trophoblast chromatin environment mediated by the PcG protein SFMBT2 // Biol. Open. 2019. V. 8(8). P. e043638. https://doi.org/10.1242/bio.043638
- Andergassen D., Dotter C.P., Wenzel D. et al. Mapping the mouse Allelome reveals tissue-specific regulation of allelic expression // Elife. 2017. V. 6. P. e25125. https://doi.org/10.7554/eLife.25125
- Schertzer M.D., Braceros K.C., Starmer J. et al. lncRNA‑induced spread of Polycomb controlled by genome architecture, RNA abundance, and CpG island DNA // Mol. Cell. 2019. V. 75(3). P. 523–537. https://doi.org/10.1016/j.molcel.2019.05.028
- Bartel D.P. Metazoan MicroRNAs // Cell. 2018. V. 173. P. 20–51. https://doi.org/10.1016/j.cell.2018.03.006
- Hayder H., O’Brien J., Nadeem U., Peng C. Micro-RNAs: Crucial regulators of placental development // Reproduction. 2018. V. 155(6). P. R259–R271. https://doi.org/10.1530/REP-17-0603
- Malnou E.C., Umlauf D., Mouysset M., Cavaille J. Imprinted microRNA gene clusters in the evolution, development, and functions of mammalian placenta // Front. Genet. 2019. V. 9. P. e706. https://doi.org/10.3389/fgene.2018.00706
- Inno R., Kikas T., Lillepea K., Laan M. Coordinated expressional landscape of the human placental miRNome and transcriptome // Front. Cell Dev. Biol. 2021. V. 9. P. e697947. https://doi.org/10.3389/fcell.2021.697947
- Kaneko-Ishino T., Ishino F. Retrotransposon silencing by DNA methylation contributed to the evolution of placentation and genomic imprinting in mammals // Dev. Growth Differ. 2010. V. 52(6). P. 533–543. https://doi.org/10.1111/j.1440-169X.2010.01194.x
- Ito M., Sferruzzi-Perri A.N., Edwards C.A. et al. A trans-homologue interaction between reciprocally imprinted miR-127 and Rtl1 regulates placenta development // Development. 2015. V. 142(14). P. 2425–2430. https://doi.org/10.1242/dev.121996
- Bentwich I. Prediction and validation of microRNAs and their targets // FEBS Lett. 2005. V. 579(26). P. 5904–5910. https://doi.org/10.1016/j.febslet.2005.09.040
- Haig D., Mainieri A. The evolution of imprinted microRNAs and their RNA targets // Genes (Basel). 2020. V. 11(9). P. e1038. https://doi.org/10.3390/genes11091038
- Noguer-Dance M., Abu-Amero S., Al-Khtib M. et al. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta // Hum. Mol. Genet. 2010. V. 19(18). P. 3566–3582. https://doi.org/10.1093/hmg/ddq272
- Gottlieb A., Flor I., Nimzyk R. et al. The expression of miRNA encoded by C19MC and miR-371-3 strongly varies among individual placentas but does not differ between spontaneous and induced abortions // Protoplasma. 2021. V. 258(1). P. 209–218. https://doi.org/10.1007/s00709-020-01548
- Gu Y., Sun J., Groome L.J., Wang Y. Differential miRNA expression profiles between the first and third trimester human placentas // Am. J. Physiol. Endocrinol. Metab. 2013. V. 304(8). P. 836–843. https://doi.org/10.1152/ajpendo.00660.2012
- Munjas J., Sopic M., Stefanovic A. et al. Non-coding RNAs in preeclampsia-molecular mechanisms and diagnostic potential // Int. J. Mol. Sci. 2021. V. 22(19). P. e10652. https://doi.org/10.3390/ijms221910652
- Delorme-Axford E., Donker R.B., Mouillet J.F. et al. Human placental trophoblasts confer viral resistance to recipient cells // Proc. Natl Acad. Sci. USA. 2013. V. 110. P. 12048–12053. https://doi.org/10.1073/pnas.1304718110
- Ishida Y., Zhao D., Ohkuchi A. et al. Maternal peripheral blood natural killer cells incorporate placenta-associated microRNAs during pregnancy // Int. J. Mol. Med. 2015. V. 35. P. 1511–1524. https://doi.org/10.3892/ijmm.2015.2157
- Inoue K., Hirose M., Inoue H. et al. The rodent-specific microRNA cluster within the Sfmbt2 gene is imprinted and essential for placental development // Cell Rep. 2017. V. 19. P. 949–956. https://doi.org/10.1016/j.celrep.2017.04.018
- Farhadova S., Gomez-Velazquez M., Feil R. Stability and lability of parental methylation imprints in development and disease // Genes (Basel). 2019. V. 10(12). P. e999. https://doi.org/10.3390/genes10120999
- Zeng Y., Chen T. DNA methylation reprogramming during mammalian development // Genes (Basel). 2019. V. 10(4). P. e257. https://doi.org/10.3390/genes10040257
- Huang Y., Liu H., Du H. et al. Developmental features of DNA methylation in CpG islands of human gametes and preimplantation embryos // Exp. Ther. Med. 2019. V. 17(6). P. 4447–4456. https://doi.org/10.3892/etm.2019.7523
- Takahashi N., Coluccio A., Thorball C.W. et al. ZNF445 is a primary regulator of genomic imprinting // Genes Dev. 2019. V. 33. P. 49–54. https://doi.org/10.1101/gad.320069.118
- Decato B.E., Lopez-Tello J., Sferruzzi-Perri A.N. et al. DNA methylation divergence and tissue specialization in the developing mouse placenta // Mol. Biol. Evol. 2017. V. 34. P. 1702–1712. https://doi.org/10.1093/molbev/msx112
- Duffie R., Ajjan S., Greenberg M.V. et al. The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals // Genes Dev. 2014. V. 28. P. 463–478. https://doi.org/10.1101/gad.232058.113
- Chen Z., Djekidel M.N., Zhang Y. Distinct dynamics and functions of H2AK119ub1 and H3K27me3 in mouse preimplantation embryos // Nat. Genet. 2021. V. 53(4). P. 551–563. https://doi.org/10.1038/s41588-021-00821-2
- Jambhekar A., Dhall A., Shi Y. Roles and regulation of histone methylation in animal development // Nat. Rev. Mol. Cell Biol. 2019. V. 20(10). P. 625–641. https://doi.org/10.1038/s41580-019-0151-1
- Healy E., Mucha M., Glancy E. et al. PRC2.1 and PRC2.2 synergize to coordinate H3K27 trimethylation // Mol. Cell. 2019. V. 76(3). P. 437–452. https://doi.org/10.1016/j.molcel.2019.08.012
- Cheutin T., Cavalli G. The multiscale effects of polycomb mechanisms on 3D chromatin folding // Crit. Rev. Biochem. Mol. Biol. 2019. V. 54(5). P. 399–417. https://doi.org/10.1080/10409238.2019.1679082
- Yang P., Wang Y., Macfarlan T.S. The role of KRAB-ZFPs in transposable element repression and mammalian evolution // Trends Genet. 2017. V. 33(11). P. 871–881. https://doi.org/10.1016/j.tig.2017.08.006
- Xu Q., Xie W. Epigenome in early mammalian development: inheritance, reprogramming and establishment // Trends Cell Biol. 2018. V. 28. P. 237–253.
- Prokopuk L., Stringer J.M., White C.R. et al. Loss of maternal EED results in postnatal overgrowth // Clin. Epigenetics. 2018. V. 10(1) P. e95. https://doi.org/10.1186/s13148-018-0526-8
- Hanna C.W., Gavin K. Features and mechanisms of canonical and noncanonical genomic imprinting // Genes Dev. 2021. V. 35(11–12). P. 821–834. https://doi.org/10.1101/gad.348422.121
- Hanna C.W. Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues // Genome Biol. 2019. V. 20. P. e225. https://doi.org/10.1186/s13059-019-1833-x
- Chen Z., Yin Q., Inoue A. et al. Allelic H3K27me3 to allelic DNA methylation switch maintains noncanonical imprinting in extraembryonic cells // Sci. Adv. 2019. V. 5(12). P. e7246. https://doi.org/10.1126/sciadv.aay7246
- Zhang W., Chen Z., Yin Q. et al. Maternal-biased H3K27me3 correlates with paternal-specific gene expression in the human morula // Genes Dev. 2019. V. 33(7–8). P. 382–387. https://doi.org/10.1101/gad.323105.118
- Enriquez-Gasca R., Gould P.A., Rowe H.M. Host gene regulation by transposable elements: the new, the old and the ugly // Viruses. 2020. V. 12(10). P. e1089. https://doi.org/10.3390/v12101089
- Senft A.D., Macfarlan T.S. Transposable elements shape the evolution of mammalian development // Nat. Rev. Genet. 2021. V. 22(11). P. 691–711. https://doi.org/10.1038/s41576-021-00385-1
- Zhang X., Muglia L.J. Baby’s best Foe-riend: Endogenous retroviruses and the evolution of eutherian reproduction // Placenta. 2021. V. 15(113). P. 1–7. https://doi.org/10.1016/j.placenta.2021.02.011
- Schust D.J., Bonney E.A., Sugimoto J. et al. The immunology of syncytialized trophoblast // Int. J. Mol. Sci. 2021. V. 2(4). P. e1767. https://doi.org/10.3390/ijms22041767
- Sugimoto J., Sugimoto M., Bernstein H. et al. A novel human endogenous retroviral protein inhibits cell-cell fusion // Sci. Rep. 2013. V. 3. P. e1462. https://doi.org/10.1038/srep01462
- Roberts R.M., Ezashi T., Schulz L.C. et al. Syncytins expressed in human placental trophoblast // Placenta. 2021. V. 113. P. 8–14. https://doi.org/10.1016/j.placenta.2021.01.006
- Каталог импринтированных генов. http://igc.otago.ac.nz.
- Roberts R.M., Green J.A., Schulz L.C. The evolution of the placenta // Reproduction. 2016. V. 152. P. 179–189. https://doi.org/10.1530/REP-16-0325
- Henke C., Strissel P.L., Schubert M.T. Selective expression of sense and antisense transcripts of the sushi-ichi-related retrotransposon-derived family during mouse placentogenesis // Retrovirology. 2015. V. 12. P. e9. https://doi.org/10.1186/s12977-015-0138-8
- Miao J., Zhu Y., Xu L. et al. MiR‑181b‑5Pinhibits trophoblast cell migration and invasion through targeting S1PR1 in multiple abnormal trophoblast invasion‑related events // Mol. Med. Rep. 2020. V. 22(5). P. 4442–4451. https://doi.org/10.3892/mmr.2020.11515
- Barlow D.P. Methylation and imprinting: From host defense to gene regulation? // Science. 1993. V. 260. P. 309–310. https://doi.org/10.1126/science.8469984
- Ondicova M., Oakey R.J., Walsh C.P. Is imprinting the result of “friendly fire” by the host defense system? // PLoS Genet. 2020. V. 16. P. e1008599. https://doi.org/10.1126/science.8469984
- Jahner D., Stuhlmann H., Stewart C.L. et al. De novo methylation and expression of retroviral genomes during mouse embryogenesis // Nature. 1982. V. 298. P. 623–628. https://doi.org/10.1038/298623a0
- Chaillet J., Vogt T., Beier D., Leder P. Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogenesis // Cell. 1991. V. 66. P. 77–83. https://doi.org/10.1016/0092-8674(91)90140-t
- Walter J., Hutter B., Khare T., Paulsen M. Repetitive elements in imprinted genes // Cytogenet. Genome Res. 2006. V. 113. P. 109–115. https://doi.org/10.1159/000090821
- Cowley M., de Burca A., McCole R.B. et al. Short Interspersed Element (SINE) depletion and Long Interspersed Element (LINE) abundance are not features universally required for imprinting // PLoS One. 2011. V. 6. P. e18953. https://doi.org/10.1371/journal.pone.0018953
- Wood A.J., Bourc’his D., Bestor T.H., Oakey R.J. Allele-specific demethylation at an imprinted mammalian promoter // Nucl. Acids Res. 2007. V. 35. P. 7031–7039. https://doi.org/10.1093/nar/gkm742
- Wood A.J., Roberts R.G., Monk D. et al. A screen for retrotransposed imprinted genes reveals an association between X chromosome homology and maternal germ-line methylation // PLoS Genet. 2007. V. 3. P. e20. https://doi.org/10.1371/journal.pgen.0030020
- Youngson N.A., Kocialkowski S., Peel N., Ferguson-Smith A.C. A small family of sushi-class retrotransposon-derived genes in mammals and their relation to genomic imprinting // J. Mol. Evol. 2005. V. 61. P. 481–490. https://doi.org/10.1007/s00239-004-0332-0
- Cowley M., Oakey R.J. Retrotransposition and genomic imprinting // Brief. Funct. Genomics. 2010. V. 9. P. 340–346. https://doi.org/10.1093/bfgp/elq015
- Thomas J.H., Schneider S. Coevolution of retroelements and tandem zinc finger genes // Genome Res. 2011. V. 21. P. 1800–1812. https://doi.org/10.1101/gr.121749.111
- Yang P., Wang Y., Hoang D. et al. A placental growth factor is silenced in mouse embryos by the zinc finger protein ZFP568 // Science. 2017. V. 356. P. 757–759. https://doi.org/10.1126/science.aah6895
- Helleboid P., Heusel M., Duc J. et al. The interactome of KRAB zinc finger proteins reveals the evolutionary history of their functional diversification // EMBO J. 2019. V. 38. P. e101220. https://doi.org/10.15252/embj.2018101220
- Jacobs F.M., Greenberg D., Nguyen N. et al. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons // Nature. 2014. V. 516. P. 242–245.
- Rowe H.M., Friedli M., Offner S. et al. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET // Development. 2013. V. 140. P. 519–529. https://doi.org/10.1242/dev.087585
- Imbeault M., Helleboid P.Y., Trono D. KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks // Nature. 2017. V. 543. P. 550–554. https://doi.org/10.1038/nature21683
- Strogantsev R., Krueger F., Yamazawa K. et al. Allele-specific binding of ZFP57 in the epigenetic regulation of imprinted and non-imprinted monoallelic expression // Genome Biol. 2015. V. 16. P. e112. https://doi.org/10.1186/s13059-015-0672-7
- Moore T., Haig D. Genomic imprinting in mammalian development: A parental tug-of-war // TIG. 1991. V. 7. P. 45–49. https://doi.org/10.1016/0168-9525(91)90230-N
- Quenneville S., Verde G., Corsinotti A. 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. V. 44. P. 361–372. https://doi.org/10.1016/j.molcel.2011.08.032
- Li X., Ito M., Zhou F. et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints // Dev. Cell. 2008. V. 15. P. 547–557. https://doi.org/10.1016/j.devcel.2008.08.014
- Criscione S.W., Theodosakis N., Micevic G. et al. Genome-wide characterization of human L1 antisense promoter-driven transcripts // BMC Genomics. 2016. V. 17. P. e463. https://doi.org/10.1186/s12864-016-2800-5
- Castro-Diaz N., Ecco G., Coluccio A. et al. Evolutionally dynamic L1 regulation in embryonic stem cells // Genes Dev. 2014. V. 28(13). P. 397–409. https://doi.org/10.1101/gad.241661.114
- Vincenz C., Lovett J.L., Wu W. et al. Loss of imprinting in human placentas is widespread, coordinated, and predicts birth phenotypes // Mol. Biol. Evol. 2020. V. 37(2). P. 429–441. https://doi.org/10.1093/molbev/msz226
- Wang X.X., Miller D.C., Harman R. et al. Paternal expressed genes predominate in the placenta // Proc. Natl Acad. Sci. USA. 2013. V. 110. P. 10705–10710. https://doi.org/10.1073/pnas.1308998110
- Monteagudo-Sánchez A., Sánchez-Delgado M., Hernandez J.R. et al. Differences in expression rather than methylation at placenta-specific imprinted loci is associated with intrauterine growth restriction // Clin. Epigenetics. 2019. V. 11(1). P. e35. https://doi.org/10.1186/s13148-019-0630-4
- Kappil M.A., Green B.B., Armstrong D.A. et al. Placental expression profile of imprinted genes impacts birth weight // Epigenetics. 2015. V. 10(9). P. 842–849. https://doi.org/10.1080/15592294.2015.1073881
- Court F., Tayama C., Romanelli V. et al. Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment // Genome Res. 2014. V. 24(4). P. 554–569. https://doi.org/10.1101/gr.164913.113
- Hanna C.W., Penaherrera M.S., Saadeh H. et al. Pervasive polymorphic imprinted methylation in the human // Genome Res. 2016. V. 26(6). P. 756–767. https://doi.org/10.1101/gr.196139.115
- Sanchez-Delgado M., Riccio A., Eggermann T. et al. Causes and consequences of multi-locus imprinting disturbances in humans // Trends Genet. 2016. V. 32(7). P. 444–455. https://doi.org/10.1016/j.tig.2016.05.001
- Xu D., Zhang C., Li J. et al. Polymorphic imprinting of SLC38A4 gene in bovine placenta // Biochem. Genet. 2018. V. 56(6). P. 639–649. https://doi.org/10.1007/s10528-018-9866-5
- Sanli I., Feil R. Chromatin mechanisms in the developmental control of imprinted gene expression // Int. J. Biochem. Cell Biol. 2015. V. 67. P. 139–147. https://doi.org/10.1016/j.biocel.2015.04.004
- Саженова Е.А., Никитина Т.В., Скрябин Н.А. и др. Эпигенетический статус импринтированных генов в плаценте при привычном невынашивании беременности // Генетика. 2017. Т. 53. № 3. С. 364–377. https://doi.org/10.7868/s0016675817020096
- Sazhenova E.A., Nikitina T.V., Vasilyev S.A. et al. NLRP7 variants in spontaneous abortions with multilocus imprinting disturbances from women with recurrent pregnancy loss // J. Assisted Reprod. Genet. 2021. V. 38(11). P. 2893–2908. https://doi.org/10.1007/s10815-021-02312-z
- Hirasawa R., Chiba H., Kaneda M. et al. Maternal and zygotic dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development // Genes Dev. 2008. V. 22. P. 1607–1616. https://doi.org/10.1101/gad.1667008
- Wyns C., De Geyter C., Calhaz-Jorge C. et al. ART in Europe, 2017: Results generated from European registries by ESHRE. European IVF-Monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE) // Hum. Reprod. Open. 2021. V. 2021(3). P. e026. https://doi.org/10.1093/hropen/hoab026
- Kobayashi H. Canonical and non-canonical genomic imprinting in rodents // Front. Cell Dev. Biol. 2021. V. 9. P. e713878. https://doi.org/10.3389/fcell.2021.713878
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