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Mammalian Genomic Imprinting
Open accessAbstract
Normal mammalian development requires a maternal and paternal contribution, which is attributed to imprinted genes, or genes that are expressed from a single parental allele. Approximately 100 imprinted genes have been reported in mammals thus far. Imprinted genes are controlled by cis-acting regulatory elements, termed imprinting control regions (ICRs), which have parental-specific epigenetic modifications, including DNA methylation. ICRs are methylated by de novo DNA methyltransferases during germline development; these parental-specific modifications must be maintained following fertilization when the genome is extensively reprogrammed. Many imprinted genes reside in ∼1-megabase clusters, with two major mechanisms of imprinting regulation currently recognized, CTCF-dependent insulators and long noncoding RNAs. Unclustered imprinted genes are generally regulated by germline-derived differential promoter methylation. Here, we describe the identification and functions of imprinted genes, cis-acting control sequences, trans-acting factors, and imprinting mechanisms in clusters. Finally, we define questions that require more extensive research.
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“Genomic imprinting hypothetically evolved to control the dosage of developmentally important genes and occurs in about 100 mammalian genes.113”
From Pubertal development and regulation (2016) · cites this paper as [113]
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“INTRODUCTION The tight regulation of monoallelic gene expression based on gametic origin is termed genomic imprinting (Bartolomei and Ferguson-Smith, 2011).”
BackgroundImmunological Effects of Epigenetic Modifiers
Bezu, L., Chuang, A. W., Liu, P., Kroemer, G., & Kepp, O. (2019) · Cancers · doi:10.3390/cancers11121911 · Cited by 23
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Gore, A. V., & Weinstein, B. M. (2016) · Experimental Hematology · doi:10.1016/j.exphem.2016.04.013 · Cited by 26
“Subsequently several more genes were discovered whose regulation was dependent on DNA methylation based genomic imprinting (26, 30).”
BackgroundParental programming: How can we improve study design to discern the molecular mechanisms?
Lecomte, V., Youngson, N. A., Maloney, C., & Morris, M. J. (2013) · BioEssays · doi:10.1002/bies.201300051 · Cited by 21
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Balanced gene dosage control rather than parental origin underpins genomic imprinting
Weinberg‐Shukron, A., Ben-Yair, R., Takahashi, N., Dunjić, M., Shtrikman, A., Edwards, C. A., Ferguson‐Smith, A. C., & Stelzer, Y. (2022) · Nature Communications · doi:10.1038/s41467-022-32144-z · Cited by 21
22 Evolving insights on how cytosine methylation affects protein-DNA binding
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“genomic imprinting [3] and genome reprogramming”
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“Finally, the study of imprinting and allele-speci fi c methylation in humans was previously limited to few cell types, focusing on easily accessible blood DNA 15,28,30 – 32 .”
DAMEfinder: a method to detect differential allele-specific methylation
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“This methylation asymmetry is conferred during gametogenesis in the parental germlines, or during early embryogenesis after fertilization, and will remain during the lifetime of the offspring [10].”
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Weinberg‐Shukron, A., Youngson, N. A., Ferguson‐Smith, A. C., & Edwards, C. A. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1328806 · Cited by 20
“Paternal loss of the gene leads to partial neonatal lethality, and those animals that survive display post-natal growth retardation, increased adiposity, and skeletal defects (Moon et al., 2002).”
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“However, for imprinted regions of the genome, the parent-of-origin alters expression of genes and may lead to recognizable phenotypes (specifically for chromosomes 6, 7, 11, 14, 15, and 20).(21) On any chromosome, isodisomy for a region in which the parent carriers a deleterious single-gene mutation for an autosomal r…”
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“However, monoallelic expression of genes is common in phenomena such as genomic imprinting or X chromosome inactivation, where a single allele of a gene is expressed (Bartolomei and Ferguson-Smith, 2011; Gayen et al, 2015, 2016; Harris et al., 2019; Lyon, 1961; Mandal et al., 2020; Saiba et al., 2018; Sarkar et al., 2…”
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“Parental imprinting is an epigenetic process, where differentially methylated regions (DMRs) are induced at specific loci of parents’ gametocyte genomes, leading to the expression of only one copy of the target gene in a parent-specific way [250].”
BackgroundRegulation of microRNA during cardiomyocyte maturation in sheep
Morrison, J. L., Zhang, S., Tellam, R. L., Brooks, D. A., McMillen, I. C., Porrello, E. R., & Botting, K. J. (2015) · BMC Genomics · doi:10.1186/s12864-015-1693-z · Cited by 19
“Maternally expressed genes typically limit aspects of offspring tissue growth and are often down-regulated after birth [54].”
BackgroundParental and sexual conflicts over the Peg3 imprinted domain
He, H., Perera, B. P. U., Ye, A., & Kim, J. (2016) · Scientific Reports · doi:10.1038/srep38136 · Cited by 19
Epigenomic landscape and epigenetic regulation in maize
Yu, J., Xu, F., Wei, Z., Zhang, X., Chen, T., & Pu, L. (2020) · Theoretical and Applied Genetics · doi:10.1007/s00122-020-03549-5 · Cited by 18
“It also plays important roles in gene imprinting and X chromosome inactivation (Bartolomei and Ferguson-Smith 2011; Chan et al. 2005; Wang et al. 2016a; Xie et al. 2013).”
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“Differential DNA methylation, histone modification, and regulatory noncoding RNA are the most important mechanisms driving monoallelic expression at imprinted loci (Bartolomei and Ferguson-Smith 2011).”
BackgroundDissection of gene function at clonal level using mosaic analysis with double markers
Hippenmeyer, S. (2013) · Frontiers in Biology · doi:10.1007/s11515-013-1279-6 · Cited by 17
The Dynamic Regulation of G-Quadruplex DNA Structures by Cytosine Methylation
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DNA methylation reprogramming of genomic imprints in the mammalian germline: A TET‐centric view
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Differential regulation of genomic imprinting by TET proteins in embryonic stem cells
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“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript (Barlow and Bartolomei, 2014; Bartolomei and Ferguson-Smith, 2011; Tilghman, 1999).”
BackgroundInfluentialInvolvement of parental imprinting in the antisense regulation of onco-miR-372-373
Stelzer, Y., Sagi, I., & Benvenisty, N. (2013) · Nature Communications · doi:10.1038/ncomms3724 · Cited by 18
Preclinical and Clinical Epigenetic-Based Reconsideration of Beckwith-Wiedemann Syndrome
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“For example, it is possible to mitigate CpG island methylation on maternal and/or paternal allele to restore the normal transcriptional activity in the imprinting control regions (Bartolomei and Ferguson-Smith, 2011).”
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“2, the DLK1-MEG3 locus, were found silence in several types of cancers [30], and loss of imprinting genes impairs various biological processes [31].”
BackgroundDNA methylation dynamics in the germline of the marsupial tammar wallaby, Macropus eugenii
Ishihara, T., Hickford, D. E., Shaw, G., Pask, A. J., & Renfree, M. B. (2018) · DNA Research · doi:10.1093/dnares/dsy040 · Cited by 18
“Gametogenesis requires global demethylation to ensure the erasure of parent-specific imprinting.(7,23) This allows resetting of sex-specific imprinting marks in the male and female germ cells.”
BackgroundCultural relativism: maintenance of genomic imprints in pluripotent stem cell culture systems
Greenberg, M., & Bourc’his, D. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.04.005 · Cited by 19
“However, the importance of genomic imprinting is underscored by embryonic lethality or severe developmental defects in mice harboring global and gene-specific imprint defects, not to mention a number of human diseases that are associated with imprinted gene misregulation [1].”
BackgroundInfluentialDNA methylation dynamics of a maternally methylated DMR in the mouse Dlk1–Dio3 domain
Zeng, T.-B., He, H., Han, Z., Zhang, F., Huang, Z., Liu, Q., Cui, W., & Wu, Q. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.10.038 · Cited by 18
“Allele-specific DNA methylation can be established either in the germline or post-fertilization (defined as germline and somatic DMRs, respectively) [4].”
BackgroundHanin, G., & Ferguson‐Smith, A. C. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1476 · Cited by 17
“About 150 imprinted genes have been identified and validated in the mouse and most of them are arranged in clusters of different sizes containing between 2 and 15 genes (Figure 1) (Barlow, 2011; Bartolomei & Ferguson-Smith, 2011).”
BackgroundDynamics of paternal contributions to early embryo development in large animals
Daigneault, B. W. (2020) · Biology of Reproduction · doi:10.1093/biolre/ioaa182 · Cited by 19
“Eutherians have evolved unique methods of regulating allele-specific gene expression during embryogenesis and placentation through epigenetic mechanisms that depart from Mendelian inheritance known as genomic imprinting [5, 6].”
MethodH3K9 Methyltransferase EHMT2/G9a Controls ERVK-Driven Noncanonical Imprinted Genes
Zeng, T.-B., Pierce, N., Liao, J., & Szabó, P. E. (2021) · Epigenomics · doi:10.2217/epi-2021-0168 · Cited by 17
Measurements of DNA Methylation at Seven Loci in Various Tissues of CD1 Mice
Daugela, L., Nüsgen, N., Walier, M., Oldenburg, J., Schwaab, R., & El‐Maarri, O. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044585 · Cited by 17
“Deviation from normal levels of methylation are associated with disease and include hyper- or hypomethylation of CpG islands and hypomethylation of repeats found in most tumors in addition to differentially methylated regions associated with imprinting disorders [7,8].”
BackgroundLoss of Imprinting in Human Placentas Is Widespread, Coordinated, and Predicts Birth Phenotypes
Vincenz, C., Lovett, J. L., Wu, W.-S., Shedden, K., & Strassmann, B. I. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz226 · Cited by 16
Meg3-DMR, not the Meg3 gene, regulates imprinting of the Dlk1-Dio3 locus
Zhu, W., Botticelli, E. M., Kery, R. E., Mao, Y., Wang, X., Yang, A., Wang, X., Zhou, J., Zhang, X., Soberman, R. J., et al. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.07.005 · Cited by 16
“The cis-elements controlling genomic imprinting are differentially methylated regions (DMRs) (11).”
BackgroundKrefft, M., Frydecka, D., Adamowski, T., & Misiak, B. (2014) · Epigenomics · doi:10.2217/epi.14.52 · Cited by 16
Ratajczak, M. Z. (2012) · Journal of Stem Cell Research & Therapy · doi:10.4172/2157-7633.1000e108 · Cited by 16
“In contrast, the presence of a methylated DMR on the paternal chromosome prevents binding of CTCF, and in this situation, the 3’ distal enhancer promotes transcription of mRNA from the Igf2 locus.”
BackgroundInfluentialKnown unknowns for allele-specific expression and genomic imprinting effects
Gregg, C. J. (2014) · F1000Prime Reports · doi:10.12703/p6-75 · Cited by 16
“marks in the embryo have been defined and recently reviewed [26,27].”
BackgroundSwanzey, E., & Stadtfeld, M. (2016) · Development · doi:10.1242/dev.138255 · Cited by 15
“More than 100 mammalian genes are expressed in a predominantly monoallelic fashion in a paradigmatic epigenetic event referred to as genomic imprinting (Bartolomei and Ferguson-Smith, 2011).”
Differential susceptibility to endocrine disruptor-induced epimutagenesis
Lehle, J. D., & McCarrey, J. R. (2020) · Current Zoology · doi:10.1093/eep/dvaa016 · Cited by 17
“ECRs are believed to epigenetically regulate gene clusters ranging from 2 to 5 megabases in size and function in a manner similar to imprinting control regions (ICRs) [185].”
BackgroundThe Key Lnc (RNA)s in Cardiac and Skeletal Muscle Development, Regeneration, and Disease
Pinheiro, A., & Naya, F. J. (2021) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd8080084 · Cited by 16
Wyder, S., Raissig, M. T., & Grossniklaus, U. (2017) · Scientific Reports · doi:10.1038/s41598-018-36768-4 · Cited by 15
“…their sequence but rather carry parent-specific, epigenetic imprints that allow the cell to distinguish the two alleles (Reik and Walter, 2001; Grossniklaus, 2007; Bartolomei and Ferguson-Smith, 2011; Ferguson-Smith, 2011; Barlow, 2011; Raissig et al., 2011; Jiang and Köhler, 2012; Gehring, 2013).”
Is imprinting the result of “friendly fire” by the host defense system?
Ondičová, M., Oakey, R. J., & Walsh, C. P. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008599 · Cited by 18
“In other cases, selective pressure may not have been sufficiently large to either fix or remove the control mechanism, which might go some way to explaining why it is hard to fit all imprinted genes into any clear functional group and why there is such variation among tissues, stages, and populations in imprinting sta…”
BackgroundPan, Y., Wang, M., Baloch, A. R., Zhang, Q., Wang, J., Ma, R., Xu, G., Kashif, J., Wang, L., Fan, J., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28394 · Cited by 15
Deyssenroth, M. A., Marsit, C. J., Chen, J., & Lambertini, L. (2019) · Epigenetics · doi:10.1080/15592294.2019.1647945 · Cited by 15
“Genomic imprinting, a process through which a subset of genes are monoallelically expressed based on parent-of-origin, is an epigenetically-determined phenomenon that coevolved with placentation and is recognized as an important conveyor of placental function [3].”
BackgroundAnalysis of DNA methylation acquisition at the imprinted Dlk1 locus reveals asymmetry at CpG dyads
Gagne, A. L., Hochman, A., Rahim, M. Q., Tong, C., Arbon, J., McDaniel, K., & Davis, T. L. (2014) · Epigenetics & Chromatin · doi:10.1186/1756-8935-7-9 · Cited by 15
“cluster, either directly or indirectly [3].”
BackgroundInfluentialTranscription-driven DNA methylation setting on the mouse Peg3 locus
Bretz, C. L., & Kim, J. (2017) · Epigenetics · doi:10.1080/15592294.2017.1377869 · Cited by 14
“First, in previous genetic studies on genomic imprinting, genomic regions of the ICRs have been deleted to test their predicted functions.(16,17) In this situation, it was difficult to determine whether genomic sequences or allelespecific DNA methylation were more critical for the functions of ICRs.”
BackgroundImprinted X chromosome inactivation at the gamete-to-embryo transition
Wei, C., Kesner, B., Yin, H., & Lee, J. T. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.02.013 · Cited by 13
Effect of DNMT inhibitor on bovine parthenogenetic embryo development
Zhang, S., Tang, B., Fan, C., Shi, L., Zhang, X., Sun, L., & Li, Z. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.09.060 · Cited by 14
Epigenesis and plasticity of mouse trophoblast stem cells
Prudhomme, J., & Morey, C. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2086-9 · Cited by 15
Xing, Y., Liu, H., Cui, Y.-P., Wang, X., & Tong, X. (2019) · PLoS ONE · doi:10.1371/journal.pone.0218278 · Cited by 14
Nikolova, E. N., Stanfield, R. L., Dyson, H. J., & Wright, P. E. (2020) · Biochemistry · doi:10.1021/acs.biochem.0c00253 · Cited by 16
The Igf2as Transcript is Exported into Cytoplasm and Associated with Polysomes
Duart-Garcia, C., & Braunschweig, M. (2012) · Biochemical Genetics · doi:10.1007/s10528-012-9547-8 · Cited by 14
“Imprinted genes are controlled by imprinting control regions (ICRs) as well as cis-acting long noncoding RNA such as Xist, Kcnq1ot1, and Air (Bartolomei and Ferguson-Smith 2011; Mohammad et al. 2009).”
BackgroundEffects of maternal nutrition on the expression of genomic imprinted genes in ovine fetuses
Duan, J. E., Zhang, M., Flock, K., Seesi, S. A., Măndoiu, I., Jones, A. K., Johnson, E., Pillai, S. M., Hoffman, M. L., McFadden, K. K., et al. (2018) · Epigenetics · doi:10.1080/15592294.2018.1503489 · Cited by 14
“Most of imprinted genes were found to reside in clusters of approximately one megabase [1]; therefore, discovery of novel imprinted genes often uses the already established clusters as a guide [11].”
BackgroundMaternal regulation of chromosomal imprinting in animals
Singh, P. B., Shloma, V. V., & Belyakin, S. N. (2019) · Chromosoma · doi:10.1007/s00412-018-00690-5 · Cited by 14
Kaneko-Ishino, T., & Ishino, F. (2023) · Biomolecules · doi:10.3390/biom13101436 · Cited by 15
Imprinted Long Non-Coding RNAs in Mammalian Development and Disease
Michele, F. D., Chillón, I., & Feil, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713647 · Cited by 13
“Interestingly, almost all the methylation-controlled imprinted domains express one or more lncRNAs [6,12].”
BackgroundCzamara, D., Dieckmann, L., Lahti‐Pulkkinen, M., Cruceanu, C., Henrich, W., Plagemann, A., Räikkönen, K., Braun, T., Binder, E. B., Lahti, J. M. T., et al. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05208-0 · Cited by 15
“Genomic imprinting is a form of epigenetic modification in which gene expression differs in an allele-specific manner depending on parent of origin [71, 72].”
BackgroundMendel’s laws of heredity on his 200th birthday: What have we learned by considering exceptions?
Wolf, J. B., Ferguson‐Smith, A. C., & Lorenz, A. (2022) · Heredity · doi:10.1038/s41437-022-00552-y · Cited by 13
“in such genes being expressed according to parental origin (Bartolomei and Ferguson-Smith, 2011).”
BackgroundGenomic responses to hepatitis B virus (HBV) infection in primary human hepatocytes
Ancey, P., Testoni, B., Gruffaz, M., Cros, M., Durand, G., Calvez‐Kelm, F. L., Durantel, D., Herceg, Z., & Hernández‐Vargas, H. (2015) · Oncotarget · doi:10.18632/oncotarget.6270 · Cited by 13
“com/oncotarget Imprinted genes are mono-allelically expressed in a parent-of-origin manner, a process tightly controlled by DNA methylation [17].”
Besson, V., Kyryachenko, S., Janich, P., Benitah, S. A., Marazzi, G., & Sassoon, D. A. (2016) · Stem Cells · doi:10.1002/stem.2540 · Cited by 13
CpG Islands: A Historical Perspective
Antequera, F., & Bird, A. P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7768-0_1 · Cited by 14
“in X chromosome inactivation, DNA methylation is also functionally relevant for the monoallelic expression of imprinted genes (reviewed in [58]) and in the silencing of endogenous retrotransposons [59].”
BackgroundLoss of TSC complex enhances gluconeogenesis via upregulation of Dlk1-Dio3 locus miRNAs
Liko, D., Rzepiela, A. J., Vukojević, V., Zavolan, M., & Hall, M. N. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918931117 · Cited by 13
“miRNAs are encoded throughout the genome, including at imprinted loci from which expression is regulated by CpG methylation and heterochromatin maintenance in an allele-specific manner (19).”
BackgroundEpigenetic memories and the evolution of infectious diseases
McLeod, D. V., Wild, G., & Úbeda, F. (2021) · Nature Communications · doi:10.1038/s41467-021-24580-0 · Cited by 12
Matsuzaki, H., Sugihara, S., & Tanimoto, K. (2023) · Epigenetics & Chromatin · doi:10.1186/s13072-023-00482-x · Cited by 12
Aberrant methylation of multiple imprinted genes in embryos of tamoxifen-treated male rats
Kedia-Mokashi, N., Kadam, L., Ankolkar, M., Dumasia, K., & Balasinor, N. (2013) · Reproduction · doi:10.1530/rep-12-0439 · Cited by 12
“Approximately 100 imprinted genes are known in mammals, and most of them have been implicated in embryo growth and development (Bartolomei & Ferguson-Smith 2011).”
BackgroundGenomic imprinting and genetic effects on muscle traits in mice
Kärst, S., Vahdati, A. R., Brockmann, G. A., & Hager, R. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-408 · Cited by 12
“Genomic imprinting is increasingly seen as an important epigenetic source of phenotypic variation that may act in addition to or in conjunction with genetic sources of variation [1-3].”
Thakur, A., Mackin, S.-J., Irwin, R. E., O’Neill, K. M., Pollin, G., & Walsh, C. P. (2016) · Epigenetics & Chromatin · doi:10.1186/s13072-016-0104-2 · Cited by 12
“This supports other evidence, suggesting that mechanism of imprinting and response to methylation loss and recovery can vary among imprinted genes [52].”
ResultDeyssenroth, M. A., Li, Q., Escudero, C., Myatt, L., Chen, J., & Roberts, J. M. (2020) · Genes · doi:10.3390/genes11101146 · Cited by 12
“Placental genomic patterns are also of interest, particularly imprinted genes, a subset of genes that are mono-allelically expressed on the basis of parent of origin [22,23].”
BackgroundGene‐environment interaction influences attachment‐like style in mice
Lassi, G., & Tucci, V. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12385 · Cited by 12
“Genomic imprinting is an epigenetic phenomenon in which maternal and paternal alleles are not functionally equivalent (Bartolomei & Ferguson-Smith 2011).”
BackgroundGenomic imprinted genes in reciprocal hybrid endosperm of Brassica napus
Rong, H., Yang, W., Zhu, H., Jiang, B., Jiang, J., & Wang, Y. (2021) · BMC Plant Biology · doi:10.1186/s12870-021-02908-8 · Cited by 12
“In mammals, most of the imprinted genes are clustered on the chromosome [32, 33, 48].”
BackgroundRivera, R. M., Donnelly, C. G., Patel, B. N., Li, Y., & Soto‐Moreno, E. J. (2021) · Wiley eBooks · doi:10.1002/9781119602484.ch71 · Cited by 12
Metadata
- Authors
- Bartolomei, M. S., & Ferguson-Smith, A. C.
- Affiliations
- University of Pennsylvania (US)
- ORCID
- Bartolomei, M. S.
- Venue
- Cold Spring Harbor Perspectives in Biology
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-05-16
- Volume
- 3
- Issue
- 7
- Pages
- a002592-a002592
- ISSN
- 1943-0264 (ISSN-L)
- PMC
- PMC3119911
- OpenAlex
- W2129246334
- Cited by
- 518
- References
- 109
- Citations by year
- 2026: 14 · 2025: 17 · 2024: 23 · 2023: 21 · 2022: 22 · 2021: 34 · 2020: 32 · 2019: 47 · 2018: 42 · 2017: 44 · 2016: 47 · 2015: 44 · 2014: 36 · 2013: 49 · 2012: 41
- Type
- posted content
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Cold Spring Harbor Perspectives in Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- U.S. Public Health Service
- Medical Research Council
- Biotechnology and Biological Sciences Research Council
- National Institute of General Medical Sciences (GM-51279, R01GM051279, R37GM051279)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD42026, R01HD042026)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- genomic imprinting, imprinted genes, imprinting control regions, DNA methylation, cis-regulatory elements, long non-coding RNA, imprinted gene clusters, germ cell development, trans-acting factors
- MeSH terms
- Animals, Female, Humans, Male, Mammals, Models, Genetic, Genomic Imprinting, Gene Expression Regulation, Developmental, DNA Methylation, RNA, Untranslated, Genetic Diseases, Inborn, Mice
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