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, where only a 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, which are 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.
REFERENCES
Gui, B., Slone, J., and Huang, T., Perspective: is random monoallelic expression a contributor to phenotypic variability of autosomal dominant disorders?, Front. Genet., 2017, vol. 29, no. 8. e191. https://doi.org/10.3389/fgene.2017.00191
Pilvar, D., Reiman, M., Pilvar, A., and 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, vol. 11. 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, vol. 176, pp. 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, vol. 10. 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, vol. 38, no. 1, pp. 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, vol. 204, pp. 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, vol. 13, no. 4, pp. 591—599. https://doi.org/10.1016/s1472-6483(10)60649-9
Thamban, T., Agarwaal, V., and Khosla, S., Role of genomic imprinting in mammalian development, J. Biosci., 2020, vol. 45. 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, Nucleic Acids Res., 2017, vol. 45, no. 18, pp. 10466—10480. https://doi.org/10.1093/nar/gkx672
Hanna, C.W., Placental imprinting: emerging mechanisms and functions, PLoS Genet., 2020, vol. 16, no. 4. e1008709. https://doi.org/10.1371/journal.pgen.1008709
Starks, R.R., Kaur, H., and Tuteja, G., Mapping cis-regulatory elements in the midgestation mouse placenta, Sci. Rep., 2021, vol. 11. e22331. https://doi.org/10.1038/s41598-021-01664-x
Woods, L., Perez-Garcia, V., and Hemberger, M., Regulation of placental development and its impact on fetal growth-new insights from mouse models, Front. Endocrinol. (Lausanne), 2018, vol. 9. 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, vol. 140, pp. 4480—4489. https://doi.org/10.1242/dev.096511
Tang, P., Miri, K., and Varmuza, S., Unique trophoblast chromatin environment mediated by the PcG protein SFMBT2, Biol. Open, 2019, vol. 8, no. 8. 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, vol. 6. 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, vol. 75, no. 3, pp. 523—537. https://doi.org/10.1016/j.molcel.2019.05.028
Bartel, D.P., Metazoan microRNAs, Cell, 2018, vol. 173, pp. 20—51. https://doi.org/10.1016/j.cell.2018.03.006
Hayder, H., O’Brien, J., Nadeem, U., and Peng, C., MicroRNAs: crucial regulators of placental development, Reproduction, 2018, vol. 155, no. 6, pp. R259—R271. https://doi.org/10.1530/REP-17-0603
Malnou, E.C., Umlauf, D., Mouysset, M., and Cavaille, J., Imprinted microRNA gene clusters in the evolution, development, and functions of mammalian placenta, Front. Genet., 2019, vol. 9. e706. https://doi.org/10.3389/fgene.2018.00706
Inno, R., Kikas, T., Lillepea, K., and Laan, M., Coordinated expressional landscape of the human placental miRNome and transcriptome, Front. Cell Dev. Biol., 2021, vol. 9, p. e697947. https://doi.org/10.3389/fcell.2021.697947
Kaneko-Ishino, T. and Ishino, F., Retrotransposon silencing by DNA methylation contributed to the evolution of placentation and genomic imprinting in mammals, Dev. Growth Differ., 2010, vol. 52, no. 6, pp. 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, vol. 142, no. 14, pp. 2425—2430. https://doi.org/10.1242/dev.121996
Bentwich, I., Prediction and validation of microRNAs and their targets, FEBS Lett., 2005, vol. 579, no. 26, pp. 5904—5910. https://doi.org/10.1016/j.febslet.2005.09.040
Haig, D. and Mainieri, A., The evolution of imprinted microRNAs and their RNA targets, Genes (Basel), 2020, vol. 11, no. 9. 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, vol. 19, no. 18, pp. 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, vol. 258, no. 1, pp. 209—218. https://doi.org/10.1007/s00709-020-01548
Gu, Y., Sun, J., Groome, L.J., and Wang, Y., Differential miRNA expression profiles between the first and third trimester human placentas, Am. J. Physiol.: Endocrinol. Metab., 2013, vol. 304, no. 8, pp. 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, vol. 22, no. 19. 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. U.S.A., 2013, vol. 110, pp. 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, vol. 35, pp. 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, vol. 19, pp. 949—956. https://doi.org/10.1016/j.celrep.2017.04.018
Farhadova, S., Gomez-Velazquez, M., and Feil, R., Stability and lability of parental methylation imprints in development and disease, Genes (Basel), 2019, vol. 10, no. 12. e999. https://doi.org/10.3390/genes10120999
Zeng, Y. and Chen, T., DNA methylation reprogramming during mammalian development, Genes (Basel), 2019, vol. 10, no. 4. 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, vol. 17, no. 6, pp. 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, vol. 33, pp. 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, vol. 34, pp. 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, vol. 28, pp. 463—478. https://doi.org/10.1101/gad.232058.113
Chen, Z., Djekidel, M.N., and Zhang, Y., Distinct dynamics and functions of H2AK119ub1 and H3K27me3 in mouse preimplantation embryos, Nat. Genet., 2021, vol. 53, no. 4, pp. 551—563. https://doi.org/10.1038/s41588-021-00821-2
Jambhekar, A., Dhall, A., and Shi, Y., Roles and regulation of histone methylation in animal development, Nat. Rev. Mol. Cell Biol., 2019, vol. 20, no. 10, pp. 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, vol. 76, no. 3, pp. 437—452. https://doi.org/10.1016/j.molcel.2019.08.012
Cheutin, T. and Cavalli, G., The multiscale effects of polycomb mechanisms on 3D chromatin folding, Crit. Rev. Biochem. Mol. Biol., 2019, vol. 54, no. 5, pp. 399—417. https://doi.org/10.1080/10409238.2019.1679082
Yang, P., Wang, Y., and Macfarlan, T.S., The role of KRAB-ZFPs in transposable element repression and mammalian evolution, Trends Genet., 2017, vol. 33, no. 11, pp. 871—881. https://doi.org/10.1016/j.tig.2017.08.006
Xu, Q. and Xie, W., Epigenome in early mammalian development: inheritance, reprogramming and establishment, Trends Cell Biol., 2018, vol. 28, pp. 237—253.
Prokopuk, L., Stringer, J.M., White, C.R., et al., Loss of maternal EED results in postnatal overgrowth, Clin. Epigenet., 2018, vol. 10, no. 1. e95. https://doi.org/10.1186/s13148-018-0526-8
Hanna, C.W. and Gavin, K., Features and mechanisms of canonical and noncanonical genomic imprinting, Genes Dev., 2021, vol. 35, nos. 11—12, pp. 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, vol. 20. 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, vol. 5, no. 12. 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, vol. 33, nos. 7—8, pp. 382—387. https://doi.org/10.1101/gad.323105.118
Enriquez-Gasca, R., Gould, P.A., and Rowe, H.M., Host gene regulation by transposable elements: the new, the old and the ugly, Viruses, 2020, vol. 12, no. 10. e1089. https://doi.org/10.3390/v12101089
Senft, A.D. and Macfarlan, T.S., Transposable elements shape the evolution of mammalian development, Nat. Rev. Genet., 2021, vol. 22, no. 11, pp. 691—711. https://doi.org/10.1038/s41576-021-00385-1
Zhang, X. and Muglia, L.J., Baby’s best Foe-riend: endogenous retroviruses and the evolution of eutherian reproduction, Placenta, 2021, vol. 15, no. 113, pp. 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, vol. 2, no. 4. 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, vol. 3. 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, vol. 113, pp. 8—14. https://doi.org/10.1016/j.placenta.2021.01.006
Catalog of imprinted genes. http://igc.otago.ac.nz.
Roberts, R.M., Green, J.A., and Schulz, L.C., The evolution of the placenta, Reproduction, 2016, vol. 152, pp. 179—189. https://doi.org/10.1530/REP-16-0325
Henke, C., Strissel, P.L., and Schubert, M.T., Selective expression of sense and antisense transcripts of the sushi-ichi-related retrotransposon-derived family during mouse placentogenesis, Retrovirology, 2015, vol. 12. e9. https://doi.org/10.1186/s12977-015-0138-8
Miao, J., Zhu, Y., Xu, L., et al., MiR‑181b‑5p inhibits trophoblast cell migration and invasion through targeting S1PR1 in multiple abnormal trophoblast invasion‑related events, Mol. Med. Rep., 2020, vol. 22, no. 5, pp. 4442—4451. https://doi.org/10.3892/mmr.2020.11515
Barlow, D.P., Methylation and imprinting: from host defense to gene regulation?, Science, 1993, vol. 260, pp. 309—310. https://doi.org/10.1126/science.8469984
Ondicova, M., Oakey, R.J., and Walsh, C.P., Is imprinting the result of “friendly fire” by the host defense system?, PLoS Genet., 2020, vol. 16. 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, vol. 298, pp. 623—628. https://doi.org/10.1038/298623a0
Chaillet, J., Vogt, T., Beier, D., and Leder, P., Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogenesis, Cell, 1991, vol. 66, pp. 77—83. https://doi.org/10.1016/0092-8674(91)90140-t
Walter, J., Hutter, B., Khare, T., and Paulsen, M., Repetitive elements in imprinted genes, Cytogenet. Genome Res., 2006, vol. 113, pp. 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, vol. 6. e18953. https://doi.org/10.1371/journal.pone.0018953
Wood, A.J., Bourc’his, D., Bestor, T.H., and Oakey, R.J., Allele-specific demethylation at an imprinted mammalian promoter, Nucleic Acids Res., 2007, vol. 35, pp. 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, vol. 3. e20. https://doi.org/10.1371/journal.pgen.0030020
Youngson, N.A., Kocialkowski, S., Peel, N., and 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, vol. 61, pp. 481—490. https://doi.org/10.1007/s00239-004-0332-0
Cowley, M. and Oakey, R.J., Retrotransposition and genomic imprinting, Brief. Funct. Genomics, 2010, vol. 9, pp. 340—346. https://doi.org/10.1093/bfgp/elq015
Thomas, J.H. and Schneider, S., Coevolution of retroelements and tandem zinc finger genes, Genome Res., 2011, vol. 21, pp. 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, vol. 356, pp. 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, vol. 38. 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, vol. 516, pp. 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, vol. 140, pp. 519—529. https://doi.org/10.1242/dev.087585
Imbeault, M., Helleboid, P.Y., and Trono, D., KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks, Nature, 2017, vol. 543, pp. 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, vol. 16. e112. https://doi.org/10.1186/s13059-015-0672-7
Moore, T. and Haig, D., Genomic imprinting in mammalian development: a parental tug-of-war, TIG, 1991, vol. 7, pp. 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, vol. 44, pp. 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, vol. 15, pp. 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, vol. 17. 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, vol. 28, no. 13, pp. 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, vol. 37, no. 2, pp. 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. U.S.A., 2013, vol. 110, pp. 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. Epigenet., 2019, vol. 11, no. 1. 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, vol. 10, no. 9, pp. 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, vol. 24, no. 4, pp. 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, vol. 26, no. 6, pp. 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, vol. 32, no. 7, pp. 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, vol. 56, no. 6, pp. 639—649. https://doi.org/10.1007/s10528-018-9866-5
Sanli, I. and Feil, R., Chromatin mechanisms in the developmental control of imprinted gene expression, Int. J. Biochem. Cell Biol., 2015, vol. 67, pp. 139—147. https://doi.org/10.1016/j.biocel.2015.04.004
Sazhenova, E.A., Nikitina, T.V., Skryabin, N.A., et al., Epigenetic status of imprinted genes in placenta during recurrent pregnancy loss, Russ. J. Genet., 2017, vol. 53, no. 3, pp. 376—387. https://doi.org/10.1134/S1022795417020090
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, vol. 38, no. 11, pp. 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, vol. 22, pp. 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, vol. 2021, no. 3. e026. https://doi.org/10.1093/hropen/hoab026
Kobayashi, H., Canonical and non-canonical genomic imprinting in rodents, Front. Cell Dev. Biol., 2021, vol. 9. e713878. https://doi.org/10.3389/fcell.2021.713878
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Sazhenova, E.A., Vasilev, S.A. & Lebedev, I.N. Biased Expression of Parental Alleles in the Human Placenta. Russ J Genet 59, 211–225 (2023). https://doi.org/10.1134/S1022795423020114
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DOI: https://doi.org/10.1134/S1022795423020114