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Genomic Imprinting and Random Monoallelic Expression

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Abstract

The review discusses the mechanisms of monoallelic expression, such as genomic imprinting, in which gene transcription depends on the parental origin of the allele, and random monoallelic transcription. Data on the regulation of gene activity in the imprinted regions are summarized with a particular focus on the areas controlling imprinting and factors influencing the variability of the imprintome. The prospects of studies of the monoallelic expression are discussed.

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Abbreviations

DMR:

differentially methylated region

ICR:

imprinting control region

SNP:

single nucleotide polymorphism

References

  1. Crouse, H. V. (1960) The controlling element in sex chromosome behavior in sciara, Genetics, 45, 1429-1443, https://doi.org/10.1093/genetics/45.10.1429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bai, F., and Settles, A. M. (2014) Imprinting in plants as a mechanism to generate seed phenotypic diversity, Front. Plant Sci., 5, 780, https://doi.org/10.3389/fpls.2014.00780.

    Article  PubMed  Google Scholar 

  3. Patten, M. M., Ross, L., Curley, J. P., Queller, D. C., Bonduriansky, R., and Wolf, J. B. (2014) The evolution of genomic imprinting: theories, predictions and empirical tests, Heredity, 113, 119-128, https://doi.org/10.1038/hdy.2014.29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Constância, M., Angiolini, E., Sandovici, I., Smith, P., Smith, R., Kelsey, G., Dean, W., Ferguson-Smith, A., Sibley, C. P., Reik, W., and Fowden, A. (2005) Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems, Proc. Natl. Acad. Sci. USA, 102, 19219-19224, https://doi.org/10.1073/pnas.0504468103.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  5. Wang, T., Yang, L. J., Wu, M., and Ma, Q. (2021) The role of long non-coding RNAs in human imprinting disorders: prospective therapeutic targets, Front. Cell Dev. Biol., 9, 730014, https://doi.org/10.3389/fcell.2021.730014.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  6. Alazami, A. M., Awad, S. M., Coskun, S., Al-Hassan, S., Hijazi, H., and Abdulwahab, F. M. (2015) TLE6 mutation causes the earliest known human embryonic lethality, Genome Biol., 16, 240, https://doi.org/10.1186/s13059-015-0792-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Eggermann, T., Monk, D., de Nanclares, G. P., Kagami, M., Giabicani, E., and Riccio, A. (2023) Imprinting disorders, Nat. Rev. Dis. Primers, 9, 33, https://doi.org/10.1038/s41572-023-00443-4.

    Article  PubMed  Google Scholar 

  8. Borrás, C., Monleón, D., López-Grueso, R., Gambini, J., Orlando, L., Pallardó, F. V., Santos, E., Viña, J., and Font de Mora, J. (2011) RasGrf1 deficiency delays aging in mice, Aging, 3, 262-276, https://doi.org/10.18632/aging.100279.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kawahara, M., Wu, Q., Takahashi, N., Morita, S., Yamada, K., Ito, M., Ferguson-Smith, A. C., and Kono, T. (2007) High-frequency generation of viable mice from engineered bi-maternal embryos, Nat. Biotechnol., 25, 1045-1050, https://doi.org/10.1038/nbt1331.

    Article  CAS  PubMed  Google Scholar 

  10. Li, Z.-K., Wang, L.-Y., Wang, L.-B., Feng, G.-H., Yuan, X.-W., Liu, C., Xu, K., Li, Y.-H., Wan, H.-F., Zhang, Y., Li, Y.-F., Li, X., Li, W., Zhou, Q., and Hu, B.-Y. (2018) Generation of bimaternal and bipaternal mice from hypomethylated haploid ESCs with imprinting region deletions, Cell Stem Cell, 23, 665-676, https://doi.org/10.1016/j.stem.2018.09.004.

    Article  CAS  PubMed  Google Scholar 

  11. Monk, D. (2015) Genomic imprinting in the human placenta, Am. J. Obstet. Gynecol., 213, S152-S162, https://doi.org/10.1016/j.ajog.2015.06.032.

    Article  PubMed  Google Scholar 

  12. Ho-Shing, O., and Dulac, C. (2019) Influences of genomic imprinting on brain function and behavior, Curr. Opin. Behav. Sci., 25, 66-76, https://doi.org/10.1016/j.cobeha.2018.08.008.

    Article  Google Scholar 

  13. Isles, A. R. (2022) The contribution of imprinted genes to neurodevelopmental and neuropsychiatric disorders, Transl. Psychiatry, 12, 210, https://doi.org/10.1038/s41398-022-01972-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bonthuis, P. J., Huang, W.-C., Stacher Hörndli, C. N., Ferris, E., Cheng, T., and Gregg, C. (2015) Noncanonical genomic imprinting effects in offspring, Cell Rep., 12, 979-991, https://doi.org/10.1016/j.celrep.2015.07.017.

    Article  CAS  PubMed  Google Scholar 

  15. Perez, J. D., Rubinstein, N. D., Fernandez, D. E., Santoro, S. W., Needleman, L. A., Ho-Shing, O., Choi, J. J., Zirlinger, M., Chen, S.-K., Liu, J. S., and Dulac, C. (2015) Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain, Elife, 4, e07860, https://doi.org/10.7554/eLife.07860.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Pinter, S. F., Colognori, D., Beliveau, B. J., Sadreyev, R. I., Payer, B., Yildirim, E., Wu, C.-T., and Lee, J. T. (2015) Allelic imbalance is a prevalent and tissue-specific feature of the mouse transcriptome, Genetics, 200, 537-549, https://doi.org/10.1534/genetics.115.176263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sazhenova, E. A., and Lebedev, I. N. (2021) Evolutionary aspects of genomic imprinting [in Russian], Mol. Biol., 55, 3-19, https://doi.org/10.31857/S0026898420060105.

    Article  CAS  Google Scholar 

  18. Goday, C., and Ruiz, M. F. (2002) Differential acetylation of histones H3 and H4 in paternal and maternal germline chromosomes during development of sciarid flies, J. Cell. Sci., 115, 4765-4775, https://doi.org/10.1242/jcs.00172.

    Article  CAS  PubMed  Google Scholar 

  19. Matsuura, K. (2020) Genomic imprinting and evolution of insect societies, Popul. Ecol., 62, 38-52, https://doi.org/10.1002/1438-390x.12026.

    Article  Google Scholar 

  20. Luo, M., Taylor, J. M., Spriggs, A., Zhang, H., Wu, X., and Russell, S. (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm, PLoS Genet., 7, e1002125, https://doi.org/10.1371/journal.pgen.1002125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wolff, P., Weinhofer, I., Seguin, J., Roszak, P., Beisel, C., and Donoghue, M. T. (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm, PLoS Genet., 7, e1002126, https://doi.org/10.1371/journal.pgen.1002126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ogunwuyi, O., Upadhyay, A., Adesina, S. K., Puri, R., Foreman, T. M., and Hauser, B. R. (2016) Genetic imprinting: comparative analysis between plants and mammals, Plant Tissue Cult. Biotechnol., 26, 267-284, https://doi.org/10.3329/ptcb.v26i2.30576.

    Article  Google Scholar 

  23. Xiao, W., Gehring, M., Choi, Y., Margossian, L., Pu, H., and Harada, J. J. (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase, Dev. Cell, 5, 891-901, https://doi.org/10.1016/s1534-5807(03)00361-7.

    Article  CAS  PubMed  Google Scholar 

  24. Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., and Jacobsen, S. E. (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation, Science, 303, 521-523, https://doi.org/10.1126/science.1089835.

    Article  CAS  PubMed  ADS  Google Scholar 

  25. Ferguson-Smith, A. C. (2011) Genomic imprinting: the emergence of an epigenetic paradigm, Nat Rev Genet., 12, 565-575, https://doi.org/10.1038/nrg3032.

    Article  CAS  PubMed  Google Scholar 

  26. Andergassen, D., Dotter, C. P., Wenzel, D., Sigl, V., Bammer, P. C., Muckenhuber, M., Mayer, D., Kulinski, T. M., Theussl, H.-C., Penninger, J. M., Bock, C., Barlow, D. P., Pauler, F. M., and Hudson, Q. J. (2017) Mapping the mouse Allelome reveals tissue-specific regulation of allelic expression, Elife, 6, e25125, https://doi.org/10.7554/eLife.25125.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Zhang, Y., Guan, D.-G., Yang, J.-H., Shao, P., Zhou, H., and Qu, L.-H. (2010) ncRNAimprint: a comprehensive database of mammalian imprinted noncoding RNAs, RNA, 16, 1889-1901, https://doi.org/10.1261/rna.2226910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Doe, C. M., Relkovic, D., Garfield, A. S., Dalley, J. W., Theobald, D. E. H., Humby, T., Wilkinson, L. S., and Isles, A. R. (2009) Loss of the imprinted snoRNA mbii-52 leads to increased 5htr2c pre-RNA editing and altered 5HT2CR-mediated behaviour, Hum. Mol. Genet., 18, 2140-2148, https://doi.org/10.1093/hmg/ddp137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Edwards, C. A., Mungall, A. J., Matthews, L., Ryder, E., Gray, D. J., Pask, A. J., Shaw, G., Graves, J. A. M., and Rogers, J., SAVOIR Consortium, Dunham, I., Renfree, M. B., Ferguson-Smith, A. C. (2008) The evolution of the DLK1-DIO3 imprinted domain in mammals, PLoS Biol., 6, e135, https://doi.org/10.1371/journal.pbio.0060135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Hanna, C. W., and Kelsey, G. (2017) Genomic imprinting beyond DNA methylation: a role for maternal histones, Genome Biol., 18, 177, https://doi.org/10.1186/s13059-017-1317-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Umlauf, D., Goto, Y., Cao, R., Cerqueira, F., Wagschal, A., Zhang, Y., and Feil, R. (2004) Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes, Nat. Genet., 36, 1296-1300, https://doi.org/10.1038/ng1467.

    Article  CAS  PubMed  Google Scholar 

  32. Mager, J., Montgomery, N. D., de Villena, F. P.-M., and Magnuson, T. (2003) Genome imprinting regulated by the mouse Polycomb group protein Eed, Nat. Genet., 33, 502-507, https://doi.org/10.1038/ng1125.

    Article  CAS  PubMed  Google Scholar 

  33. Yang, H., Bai, D., Li, Y., Yu, Z., Wang, C., Sheng, Y., Liu, W., Gao, S., and Zhang, Y. (2022) Allele-specific H3K9me3 and DNA methylation co-marked CpG-rich regions serve as potential imprinting control regions in pre-implantation embryo, Nat. Cell Biol., 24, 783-792, https://doi.org/10.1038/s41556-022-00900-4.

    Article  CAS  PubMed  Google Scholar 

  34. Hao, N., Palmer, A. C., Dodd, I. B., and Shearwin, K. E. (2017) Directing traffic on DNA-How transcription factors relieve or induce transcriptional interference, Transcription, 8, 120-125, https://doi.org/10.1080/21541264.2017.1285851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Latos, P. A., Pauler, F. M., Koerner, M. V., Şenergin, H. B., Hudson, Q. J., Stocsits, R. R., Allhoff, W., Stricker, S. H., Klement, R. M., Warczok, K. E., Aumayr, K., Pasierbek, P., and Barlow, D. P. (2012) Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing, Science, 338, 1469-1472, https://doi.org/10.1126/science.1228110.

    Article  CAS  PubMed  ADS  Google Scholar 

  36. Schertzer, M. D., Braceros, K. C. A., Starmer, J., Cherney, R. E., Lee, D. M., Salazar, G., Justice, M., Bischoff, S. R., Cowley, D. O., Ariel, P., Zylka, M. J., Dowen, J. M., Magnuson, T., and Calabrese, J. M. (2019) lncRNA-induced spread of polycomb controlled by genome architecture, RNA abundance, and CpG island DNA, Mol. Cell, 75, 523-537, https://doi.org/10.1016/j.molcel.2019.05.028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nagano, T., Mitchell, J. A., Sanz, L. A., Pauler, F. M., Ferguson-Smith, A. C., Feil, R., and Fraser, P. (2008) The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin, Science, 322, 1717-1720, https://doi.org/10.1126/science.1163802.

    Article  CAS  PubMed  ADS  Google Scholar 

  38. Kinoshita, T., Yadegari, R., Harada, J. J., Goldberg, R. B., and Fischer, R. L. (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm, Plant Cell, 11, 1945-1952, https://doi.org/10.1105/tpc.11.10.1945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kaplun, D. S., Kaluzhny, D. N., Prokhortchouk, E. B., and Zhenilo, S. V. (2022) DNA methylation: genomewide distribution, regulatory mechanism and therapy target, Acta Naturae, 14, 4-19, https://doi.org/10.32607/actanaturae.11822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Butz, S., Schmolka, N., Karemaker, I. D., Villaseñor, R., Schwarz, I., Domcke, S., Uijttewaal, E. C. H., Jude, J., Lienert, F., Krebs, A. R., de Wagenaar, N. P., Bao, X., Zuber, J., Elling, U., Schübeler, D., and Baubec, T. (2022) DNA sequence and chromatin modifiers cooperate to confer epigenetic bistability at imprinting control regions, Nat. Genet., 54, 1702-1710, https://doi.org/10.1038/s41588-022-01210-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Krebs, A. R., Dessus-Babus, S., Burger, L., and Schübeler, D. (2014) High-throughput engineering of a mammalian genome reveals building principles of methylation states at CG rich regions, Elife, 3, e04094, https://doi.org/10.7554/eLife.04094.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Matsuzaki, H., Okamura, E., Kuramochi, D., Ushiki, A., Hirakawa, K., Fukamizu, A., and Tanimoto, K. (2018) Synthetic DNA fragments bearing ICR cis elements become differentially methylated and recapitulate genomic imprinting in transgenic mice, Epigenetics Chromatin, 11, 36, https://doi.org/10.1186/s13072-018-0207-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Taylor, D. H., McLean, C. M., Wu, W. L., Wang, A. B., and Soloway, P. D. (2016) Imprinted DNA methylation reconstituted at a non-imprinted locus, Epigenetics Chromatin, 9, 41, https://doi.org/10.1186/s13072-016-0094-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Anvar, Z., Cammisa, M., Riso, V., Baglivo, I., Kukreja, H., Sparago, A., Girardot, M., Lad, S., De Feis, I., Cerrato, F., et al. (2016) ZFP57 recognizes multiple and closely spaced sequence motif variants to maintain repressive epigenetic marks in mouse embryonic stem cells, Nucleic Acids Res., 44, 1118-1132, https://doi.org/10.1093/nar/gkv1059.

    Article  CAS  PubMed  Google Scholar 

  45. Zuo, X., Sheng, J., Lau, H.-T., McDonald, C. M., Andrade, M., Cullen, D. E., Bell, F. T., Iacovino, M., Kyba, M., Xu, G., and Li, X. (2012) Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain, J. Biol. Chem., 287, 2107-2118, https://doi.org/10.1074/jbc.M111.322644.

    Article  CAS  PubMed  Google Scholar 

  46. Imbeault, M., Helleboid, P.-Y., and Trono, D. (2017) KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks, Nature, 543, 550-554, https://doi.org/10.1038/nature21683.

    Article  CAS  PubMed  ADS  Google Scholar 

  47. Monteagudo-Sánchez, A., Mora, J. R. H., Simon, C., Burton, A., Tenorio, J., Lapunzina, P., Clark, S., Esteller, M., Kelsey, G., López-Siguero, J. P., et al. (2020) The role of ZFP57 and additional KRAB-zinc finger proteins in the maintenance of human imprinted methylation and multi-locus imprinting disturbances, Nucleic Acids Res., 48, 11394-11407, https://doi.org/10.1093/nar/gkaa837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Menafra, R., and Stunnenberg, H. G. (2014) MBD2 and MBD3: elusive functions and mechanisms, Front. Genet., 5, 428, https://doi.org/10.3389/fgene.2014.00428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kaplun, D. S., Fok, R. E., Korostina, V. S., Prokhortchouk, E. B., and Zhenilo, S. V. (2019) Kaiso gene knockout promotes somatic cell reprogramming, Biochemistry (Moscow), 84, 283-290, https://doi.org/10.1134/S0006297919030106.

    Article  CAS  PubMed  Google Scholar 

  50. Barrett, C. W., Smith, J. J., Lu, L. C., Markham, N., Stengel, K. R., and Short, S. P. (2012) Kaiso directs the transcriptional corepressor MTG16 to the Kaiso binding site in target promoters, PLoS One, 7, e51205, https://doi.org/10.1371/journal.pone.0051205.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  51. Michalak, P. (2014) Evidence for maternal imprinting of 45S ribosomal RNA genes in Xenopus hybrids, Dev. Genes Evol., 224, 125-128, https://doi.org/10.1007/s00427-014-0464-1.

    Article  CAS  PubMed  Google Scholar 

  52. Ruzov, A., Dunican, D. S., Prokhortchouk, A., Pennings, S., Stancheva, I., Prokhortchouk, E., and Meehan, R. R. (2004) Kaiso is a genome-wide repressor of transcription that is essential for amphibian development, Development, 131, 6185-6194, https://doi.org/10.1242/dev.01549.

    Article  CAS  PubMed  Google Scholar 

  53. Lobanova, Y., Filonova, G., Kaplun, D., Zhigalova, N., Prokhortchouk, E., and Zhenilo, S. (2023) TRIM28 regulates transcriptional activity of methyl-DNA binding protein Kaiso by SUMOylation, Biochimie, 206, 73-80, https://doi.org/10.1016/j.biochi.2022.10.006.

    Article  CAS  PubMed  Google Scholar 

  54. Kulikov, A. V., Korostina, V. S., Kulikova, E. A., Fursenko, D. V., Akulov, A. E., Moshkin, M. P., and Prokhortchouk, E. B. (2016) Knockout Zbtb33 gene results in an increased locomotion, exploration and pre-pulse inhibition in mice, Behav. Brain Res., 297, 76-83, https://doi.org/10.1016/j.bbr.2015.10.003.

    Article  CAS  PubMed  Google Scholar 

  55. Kravitz, S. N., Ferris, E., Love, M. I., Thomas, A., Quinlan, A. R., and Gregg, C. (2023) Random allelic expression in the adult human body, Cell Rep., 42, 111945, https://doi.org/10.1016/j.celrep.2022.111945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Phung, T. N., Olney, K. C., Pinto, B. J., Silasi, M., Perley, L., and O’Bryan, J. (2022) X chromosome inactivation in the human placenta is patchy and distinct from adult tissues, HGG Adv., 3, 100-121, https://doi.org/10.1016/j.xhgg.2022.100121.

    Article  CAS  Google Scholar 

  57. Deng, Q., Ramsköld, D., Reinius, B., and Sandberg, R. (2014) Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells, Science, 343, 193-196, https://doi.org/10.1126/science.1245316.

    Article  CAS  PubMed  ADS  Google Scholar 

  58. Chess, A. (2016) Monoallelic gene expression in mammals, Annu. Rev. Genet., 50, 317-327, https://doi.org/10.1146/annurev-genet-120215-035120.

    Article  CAS  PubMed  Google Scholar 

  59. Gimelbrant, A., Hutchinson, J. N., Thompson, B. R., and Chess, A. (2007) Widespread monoallelic expression on human autosomes, Science, 318, 1136-1140, https://doi.org/10.1126/science.1148910.

    Article  CAS  PubMed  ADS  Google Scholar 

  60. Walker, E. J., Zhang, C., Castelo-Branco, P., Hawkins, C., Wilson, W., Zhukova, N., Alon, N., Novokmet, A., Baskin, B., Ray, P., Knobbe, C., Dirks, P., Taylor, M. D., Croul, S., Malkin, D., and Tabori, U. (2012) Monoallelic expression determines oncogenic progression and outcome in benign and malignant brain tumors, Cancer Res., 72, 636-644, https://doi.org/10.1158/0008-5472.CAN-11-2266.

    Article  CAS  PubMed  Google Scholar 

  61. Huang, W.-C., Ferris, E., Cheng, T., Hörndli, C. S., Gleason, K., Tamminga, C., Wagner, J. D., Boucher, K. M., Christian, J. L., and Gregg, C. (2017) Diverse non-genetic, allele-specific expression effects shape genetic architecture at the cellular level in the mammalian brain, Neuron, 93, 1094-1109.e7, https://doi.org/10.1016/j.neuron.2017.01.033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhenilo, S., Khrameeva, E., Tsygankova, S., Zhigalova, N., Mazur, A., and Prokhortchouk, E. (2015) Individual genome sequencing identified a novel enhancer element in exon 7 of the CSFR1 gene by shift of expressed allele ratios, Gene, 566, 223-228, https://doi.org/10.1016/j.gene.2015.04.053.

    Article  CAS  PubMed  Google Scholar 

  63. Rv, P., Sundaresh, A., Karunyaa, M., Arun, A., and Gayen, S. (2021) Autosomal clonal monoallelic expression: natural or artifactual? Trends Genet., 37, 206-211, https://doi.org/10.1016/j.tig.2020.10.011.

    Article  CAS  PubMed  Google Scholar 

  64. Gupta, S., Lafontaine, D. L., Vigneau, S., Vinogradova, S., Mendelevich, A., Igarashi, K. J., Bortvin, A., Alves-Pereira, C. F., Clement, K., Pinello, L., Gnirke, A., Long, H., Gusev, A., Nag, A., and Gimelbrant, A. A. (2020) DNA methylation is a key mechanism for maintaining monoallelic expression on autosomes, bioRxiv, https://doi.org/10.1101/2020.02.20.954834.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Gendrel, A.-V., Attia, M., Chen, C.-J., Diabangouaya, P., Servant, N., Barillot, E., and Heard, E. (2014) Developmental dynamics and disease potential of random monoallelic gene expression, Dev. Cell, 28, 366-380, https://doi.org/10.1016/j.devcel.2014.01.016.

    Article  CAS  PubMed  Google Scholar 

  66. Eckersley-Maslin, M. A., Thybert, D., Bergmann, J. H., Marioni, J. C., Flicek, P., and Spector, D. L. (2014) Random monoallelic gene expression increases upon embryonic stem cell differentiation, Dev. Cell, 28, 351-365, https://doi.org/10.1016/j.devcel.2014.01.017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kissiov, D. U., Ethell, A., Chen, S., Wolf, N. K., Zhang, C., Dang, S. M., Jo, Y., Madsen, K. N., Paranjpe, I., Lee, A. Y., Chim, B., Muljo, S. A., and Raulet, D. H. (2022) Binary outcomes of enhancer activity underlie stable random monoallelic expression, Elife, 11, e74204, https://doi.org/10.7554/eLife.74204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Sands, B., Yun, S., and Mendenhall, A. R. (2021) Introns control stochastic allele expression bias, Nat. Commun., 12, 6527, https://doi.org/10.1038/s41467-021-26798-4.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  69. Kim, J. K., Kolodziejczyk, A. A., Ilicic, T., Teichmann, S. A., and Marioni, J. C. (2015) Characterizing noise structure in single-cell RNA-seq distinguishes genuine from technical stochastic allelic expression, Nat. Commun., 6, 8687, https://doi.org/10.1038/ncomms9687.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  70. Mendelevich, A., Gupta, S., Pakharev, A., Teodosiadis, A., Mironov, A. A., and Gimelbrant, A. A. (2023) Foreign RNA spike-ins enable accurate allele-specific expression analysis at scale, Bioinformatics, 39, i431-i439, https://doi.org/10.1093/bioinformatics/btad254.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Reinius, B., Mold, J. E., Ramsköld, D., Deng, Q., Johnsson, P., Michaëlsson, J., Frisén, J., and Sandberg, R. (2016) Analysis of allelic expression patterns in clonal somatic cells by single-cell RNA-seq, Nat. Genet., 48, 1430-1435, https://doi.org/10.1038/ng.3678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Naik, H. C., Hari, K., Chandel, D., Mandal, S., Jolly, M. K., and Gayen, S. (2021) Semicoordinated allelic-bursting shape dynamic random monoallelic expression in pregastrulation embryos, iScience, 24, 102954, https://doi.org/10.1016/j.isci.2021.102954.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  73. Tunnacliffe, E., and Chubb, J. R. (2020) What is a transcriptional burst? Trends Genet., 36, 288-297, https://doi.org/10.1016/j.tig.2020.01.003.

    Article  CAS  PubMed  Google Scholar 

  74. Garber, K. (2015) RIKEN suspends first clinical trial involving induced pluripotent stem cells, Nat. Biotechnol., 33, 890-891, https://doi.org/10.1038/nbt0915-890.

    Article  CAS  PubMed  Google Scholar 

  75. Perrera, V., and Martello, G. (2019) How does reprogramming to pluripotency affect genomic imprinting? Front. Cell Dev. Biol., 7, 76, https://doi.org/10.3389/fcell.2019.00076.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Anguera, M. C., Sadreyev, R., Zhang, Z., Szanto, A., Payer, B., and Sheridan, S. D. (2012) Molecular signatures of human induced pluripotent stem cells highlight sex differences and cancer genes, Cell Stem Cell, 11, 75-90, https://doi.org/10.1016/j.stem.2012.03.008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Patel, S., Bonora, G., Sahakyan, A., Kim, R., Chronis, C., and Langerman, J. (2017) Human embryonic stem cells do not change their X inactivation status during differentiation, Cell Rep., 18, 54-67, https://doi.org/10.1016/j.celrep.2016.11.054.

    Article  CAS  PubMed  Google Scholar 

  78. Arez, M., Eckersley-Maslin, M., Klobučar, T., von Gilsa Lopes, J., Krueger, F., and Mupo, A. (2022) Imprinting fidelity in mouse iPSCs depends on sex of donor cell and medium formulation, Nat. Commun., 13, 5432, https://doi.org/10.1038/s41467-022-33013-5.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  79. Bar, S., Schachter, M., Eldar-Geva, T., and Benvenisty, N. (2017) Large-scale analysis of loss of imprinting in human pluripotent stem cells, Cell Rep., 19, 957-968, https://doi.org/10.1016/j.celrep.2017.04.020.

    Article  CAS  PubMed  Google Scholar 

  80. Uyar, A., and Seli, E. (2014) The impact of assisted reproductive technologies on genomic imprinting and imprinting disorders, Curr. Opin. Obstet. Gynecol., 26, 210-221, https://doi.org/10.1097/GCO.0000000000000071.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Russian Science Foundation (project no. 19-74-30026-P; genomic imprinting) and Ministry of Science and Higher Education of the Russian Federation (122041100149-7; random monoallelic expression).

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Correspondence to Svetlana V. Zhenilo.

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Lobanova, Y.V., Zhenilo, S.V. Genomic Imprinting and Random Monoallelic Expression. Biochemistry Moscow 89, 84–96 (2024). https://doi.org/10.1134/S000629792401005X

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