Cited by 296Genetic Syndromes and ImprintingHematopoietic Stem Cell TransplantationEpigenetics and DNA Methylation

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Maternal imprinting at the H19-Igf2 locus maintains adult haematopoietic stem cell quiescence

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Venkatraman, Aparna, He, Xi C., Thorvaldsen, Joanne L., Sugimura, Ryohichi, Perry, John M., Tao, Fang, Zhao, Meng, Christenson, Matthew K., Sanchez, Rebeca, Yu, Jaclyn Y., Peng, Lai, Haug, Jeffrey S., Paulson, Ariel, Li, Hua, Zhong, Xiao-bo, Clemens, Thomas L., Bartolomei, Marisa S., Li, Linheng·2013·Nature

DOI 10.1038/nature12303PMC PMC3896866

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Abstract

The epigenetic regulation of imprinted genes by monoallelic DNA methylation of either maternal or paternal alleles is critical for embryonic growth and development. Imprinted genes were recently shown to be expressed in mammalian adult stem cells to support self-renewal of neural and lung stem cells; however, a role for imprinting per se in adult stem cells remains elusive. Here we show upregulation of growth-restricting imprinted genes, including in the H19-Igf2 locus, in long-term haematopoietic stem cells and their downregulation upon haematopoietic stem cell activation and proliferation. A differentially methylated region upstream of H19 (H19-DMR), serving as the imprinting control region, determines the reciprocal expression of H19 from the maternal allele and Igf2 from the paternal allele. In addition, H19 serves as a source of miR-675, which restricts Igf1r expression. We demonstrate that conditional deletion of the maternal but not the paternal H19-DMR reduces adult haematopoietic stem cell quiescence, a state required for long-term maintenance of haematopoietic stem cells, and compromises haematopoietic stem cell function. Maternal-specific H19-DMR deletion results in activation of the Igf2-Igfr1 pathway, as shown by the translocation of phosphorylated FoxO3 (an inactive form) from nucleus to cytoplasm and the release of FoxO3-mediated cell cycle arrest, thus leading to increased activation, proliferation and eventual exhaustion of haematopoietic stem cells. Mechanistically, maternal-specific H19-DMR deletion leads to Igf2 upregulation and increased translation of Igf1r, which is normally suppressed by H19-derived miR-675. Similarly, genetic inactivation of Igf1r partly rescues the H19-DMR deletion phenotype. Our work establishes a new role for this unique form of epigenetic control at the H19-Igf2 locus in maintaining adult stem cells.

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Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., & Pachter, L. (2010) · Nature Biotechnology · doi:10.1038/nbt.1621 · Cited by 15,556
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,682
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
Irizarry, R. A. (2003) · Biostatistics · doi:10.1093/biostatistics/4.2.249 · Cited by 10,603
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.185 · Cited by 8,328
Summaries of Affymetrix GeneChip probe level data
Irizarry, R. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gng015 · Cited by 4,837
Identification of the haematopoietic stem cell niche and control of the niche size
Zhang, J., Niu, C. S., Ye, L., Huang, H., He, X. C., Tong, W.-G., Ross, J., Haug, J., Johnson, T. J., Feng, J. Q., et al. (2003) · Nature · doi:10.1038/nature02041 · Cited by 2,948
Self-citation
Parental imprinting of the mouse insulin-like growth factor II gene
DeChiara, T. M., Robertson, E. J., & Efstratiadis, A. (1991) · Cell · doi:10.1016/0092-8674(91)90513-x · Cited by 1,804
FoxOs Are Critical Mediators of Hematopoietic Stem Cell Resistance to Physiologic Oxidative Stress
Tothova, Z., Kollipara, R., Huntly, B. J., Lee, B. H., Castrillon, D. H., Cullen, D. E., McDowell, E. P., Lazo-Kallanian, S., Williams, I. R., Sears, C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.01.003 · Cited by 1,562

Show all 44 references

Research works printed but not linked: 2

Thorvaldsen, J. L., Fedoriw, A. M., Nguyen, S. & Bartolomei, M. S. Developmental profile of H19 differentially methylated domain (DMD) deletion alleles reveals multiple roles of the DMD in regulating allelic expression and DNA methylation at the imprinted H19/Igf2 locus. Mol. Cell. Biol. 26, 1245–1258 (2006) · DOI
Haug, J. S. et al. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2, 367–379 (2008) · DOI

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Li, F., Ma, N., Zhao, R., Wu, G., Zhang, Y., Qiao, Y., Han, D. H., Xu, Y. F., Xiang, Y., Yan, B., et al. (2014) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12293 · Cited by 60
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Zaro, B. W., Noh, J. J., Mascetti, V. L., Demeter, J., George, B. M., Żukowska, M., Gulati, G. S., Sinha, R., Flynn, R. A., Banuelos, A. M., et al. (2020) · eLife · doi:10.7554/elife.62210 · Cited by 59
IGF-1 facilitates thrombopoiesis primarily through Akt activation
Chen, S., Hu, M., Shen, M., Wang, S., Wang, C., Chen, F., Tang, Y., Wang, X., Zeng, H., Chen, M., et al. (2018) · Blood · doi:10.1182/blood-2018-01-825927 · Cited by 59
Age-dependent effects of Igf2bp2 on gene regulation, function, and aging of hematopoietic stem cells in mice
Suo, M., Rommelfanger, M. K., Chen, Y., Amro, E. M., Han, B., Chen, Z., Szafranski, K., Chakkarappan, S. R., Boehm, B. O., MacLean, A. L., et al. (2022) · Blood · doi:10.1182/blood.2021012197 · Cited by 57
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Shaikh, A., Bhartiya, D., Kapoor, S., & Nimkar, H. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0311-6 · Cited by 56
Transcriptome sequencing to detect the potential role of long non-coding RNAs in bovine mammary gland during the dry and lactation period
Yang, B., Jiao, B., Ge, W., Zhang, X., Wang, S., Zhao, H., & Wang, X. (2018) · BMC Genomics · doi:10.1186/s12864-018-4974-5 · Cited by 58
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Goyal, N., Sivadas, A., Vellarikkal, S. K., Jayarajan, R., Verma, A., Sivasubbu, S., Scaria, V., & Datta, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-08281-7 · Cited by 56
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Suszyńska, M., Zuba‐Surma, E. K., Maj, M. A., Mierzejewska, K., Ratajczak, J., Kucia, M., & Ratajczak, M. Z. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0472 · Cited by 54
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Yang, X., Wang, H., & Jiao, B. (2016) · Oncotarget · doi:10.18632/oncotarget.12893 · Cited by 60
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Haig, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0178 · Cited by 53
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Wang, F., He, J., Liu, S., Gao, A., Yang, L., Sun, G., Ding, W., Li, C., Gou, F., He, M., et al. (2021) · Blood · doi:10.1182/blood.2021011314 · Cited by 51
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Chen, Z., Guo, Q., Song, G., & Hou, Y. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04200-w · Cited by 56
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Li, C., Lei, B., Huang, S., Zheng, M., Liu, Z., Li, Z., & Deng, Y. (2015) · Europe PMC (PubMed Central) · Cited by 48
Genome-wide analysis of aberrantly expressed lncRNAs and miRNAs with associated co-expression and ceRNA networks in β-thalassemia and hereditary persistence of fetal hemoglobin
Lai, K., Jia, S., Yu, S., Luo, J., & He, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.18263 · Cited by 45
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Pio, L., O'Neill, A. F., Woodley, H., Murphy, A. J., Tiao, G. M., Franchi‐Abella, S., Fresneau, B. C., Watanabe, K., Alaggio, R., Lopez-Terrada, D. H., et al. (2025) · Nature Reviews Disease Primers · doi:10.1038/s41572-025-00620-7 · Cited by 48
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Lai, R. W., Lu, R. J., Danthi, P. S., Bravo, J. I., Goumba, A., Sampathkumar, N. K., & Benayoun, B. A. (2019) · BMB Reports · doi:10.5483/bmbrep.2019.52.1.296 · Cited by 45
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Espinoza, D. A., Fan, X., Yang, D., Cordes, S., Truitt, L. L., Calvo, K. R., Yabe, I. M., Demirci, S., Hope, K. J., Hong, S. G., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.04.003 · Cited by 41
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Pivotal functions and impact of long con-coding RNAs on cellular processes and genome integrity
Sharma, S., Houfani, A. A., & Foster, L. J. (2024) · Journal of Biomedical Science · doi:10.1186/s12929-024-01038-1 · Cited by 42
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Ratajczak, M. Z., Bartke, A., & Darżynkiewicz, Z. (2017) · Stem Cell Reviews and Reports · doi:10.1007/s12015-017-9728-2 · Cited by 42
Down-regulation of long non-coding RNA GAS5-AS1 and its prognostic and diagnostic significance in hepatocellular carcinoma
Wang, Y., Wei, J., Ma, W., Liang, C., Chai, H., & Tu, J. (2018) · Cancer Biomarkers · doi:10.3233/cbm-170781 · Cited by 40
Long noncoding RNAs: emerging regulators of normal and malignant hematopoiesis
Qiu, Y., Xu, M., & Huang, S. (2021) · Blood · doi:10.1182/blood.2021011992 · Cited by 40
Somatic mutations and epigenetic abnormalities in myelodysplastic syndromes
Itzykson, R., Kosmider, O., & Fenaux, P. (2013) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2014.01.001 · Cited by 40
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Hu, M., Lu, Y., Wang, S., Zhang, Z., Qi, Y., Chen, N., Shen, M., Chen, F., Chen, M., Yang, L., et al. (2021) · Cell Death and Differentiation · doi:10.1038/s41418-021-00848-2 · Cited by 40
Long non-coding RNA H19 inhibition promotes hyperglycemia in mice by upregulating hepatic FoxO1 levels and promoting gluconeogenesis
Goyal, N., Tiwary, S., Kesharwani, D., & Datta, M. (2018) · Journal of Molecular Medicine · doi:10.1007/s00109-018-1718-6 · Cited by 38
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Klimmeck, D., Cabezas‐Wallscheid, N., Reyes, A., von Paleske, L., Renders, S., Hansson, J., Krijgsveld, J., Huber, W. K., & Trumpp, A. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.08.012 · Cited by 33
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Zhang, Y., Cruickshanks, N. A., Pahuski, M., Yuan, F., Dutta, A., Schiff, D., Purow, B. W., & Abounader, R. (2017) · Codon Publications eBooks · doi:10.15586/codon.glioblastoma.2017.ch6 · Cited by 38
Is There a Histone Code for Cellular Quiescence?
Bonitto, K., Sarathy, K., Atai, K., Mitra, M., & Coller, H. A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.739780 · Cited by 39

Authors: Venkatraman, A., He, X. C., Thorvaldsen, J. L., Sugimura, R., Perry, J. M., Tao, F., Zhao, M., Christenson, M. K., Sanchez, R., Yu, J. Y., Peng, L., Haug, J. S., Paulson, A., Li, H., Zhong, X.-B., Clemens, T. L., Bartolomei, M. S., & Li, L.
Affiliations: Stowers Institute for Medical Research (US)
University of Pennsylvania (US)
University of Kansas Medical Center (US)
Johns Hopkins University (US)
Corresponding author: Li, Linheng
ORCID: Venkatraman, Aparna
He, Xi C.
Sugimura, Ryohichi
Perry, John M.
Zhao, Meng
Haug, Jeffrey S.
Paulson, Ariel
Li, Hua
Zhong, Xiao-bo
Bartolomei, Marisa S.
Li, Linheng
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2013-07-17
Volume: 500
Issue: 7462
Pages: 345-349
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature12303
PMC: PMC3896866
OpenAlex: W2081038378
Cited by: 296
References: 44
Citations by year: 2026: 9 · 2025: 7 · 2024: 21 · 2023: 19 · 2022: 21 · 2021: 15 · 2020: 21 · 2019: 31 · 2018: 25 · 2017: 39 · 2016: 27 · 2015: 34 · 2014: 22 · 2013: 5
FWCI: 19.41
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institute of General Medical Sciences (R01GM087376, GM-51279, R01GM051279, R37GM051279)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: genomic imprinting, hematopoietic stem cells, stem cell quiescence, H19 differentially methylated region, H19, insulin-like growth factor II, miR-675, IGF-1 receptor, FOXO3, DNA methylation
MeSH terms: Animals, Insulin-Like Growth Factor II, Signal Transduction, Transcriptional Activation, Receptor, IGF Type 1, Genomic Imprinting, Gene Expression Regulation, Developmental, Epigenesis, Genetic, Mice, Adult Stem Cells, RNA, Long Noncoding

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Maternal imprinting at the H19-Igf2 locus maintains adult haematopoietic stem cell quiescence

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