UTX maintains the functional integrity of the murine hematopoietic system by globally regulating aging-associated genes
Open accessAbstract
Epigenetic regulation is essential for the maintenance of the hematopoietic system, and its deregulation is implicated in hematopoietic disorders. In this study, UTX, a demethylase for lysine 27 on histone H3 (H3K27) and a component of COMPASS-like and SWI/SNF complexes, played an essential role in the hematopoietic system by globally regulating aging-associated genes. Utx-deficient (UtxΔ/Δ) mice exhibited myeloid skewing with dysplasia, extramedullary hematopoiesis, impaired hematopoietic reconstituting ability, and increased susceptibility to leukemia, which are the hallmarks of hematopoietic aging. RNA-sequencing (RNA-seq) analysis revealed that Utx deficiency converted the gene expression profiles of young hematopoietic stem-progenitor cells (HSPCs) to those of aged HSPCs. Utx expression in hematopoietic stem cells declined with age, and UtxΔ/Δ HSPCs exhibited increased expression of an aging-associated marker, accumulation of reactive oxygen species, and impaired repair of DNA double-strand breaks. Pathway and chromatin immunoprecipitation analyses coupled with RNA-seq data indicated that UTX contributed to hematopoietic homeostasis mainly by maintaining the expression of genes downregulated with aging via demethylase-dependent and -independent epigenetic programming. Of note, comparison of pathway changes in UtxΔ/Δ HSPCs, aged muscle stem cells, aged fibroblasts, and aged induced neurons showed substantial overlap, strongly suggesting common aging mechanisms among different tissue stem cells.
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The H3K27me3 demethylase UTX helps maintain a youthful phenotype in HSCs, with UTX-deficient HSCs acquiring an early-ageing phenotype.
“Consistently, the H3K27me3 demethylase UTX helps maintain a youthful phenotype in HSCs, with UTX-deficient HSCs acquiring an early-ageing phenotype100.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [100]
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Drosophila UTX Coordinates with p53 to Regulate ku80 Expression in Response to DNA Damage
Zhang, C., Hong, Z., Ma, W., Ma, D., Qian, Y., Xie, W., Tie, F., & Fang, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078652 · Cited by 24 · see citing works
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Blood stem cells: from beginning to end
Bigas, A., & Waskow, C. (2016) · Development · doi:10.1242/dev.142828 · Cited by 11 · see citing works
Folate deficiency facilitates coordination of KDM6A with p53 in response to DNA damagePreprint
Gao, J., Zou, J., Li, J., Zhang, Y., Qiao, L., Wang, F., Bao, Y., Hu, J., Zhang, T., Xie, Q., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/591768 · Cited by 2 · see citing works
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1 of the 94 references couldn’t be matched to a known paper.
Cited by
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Ageing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
Cellular rejuvenation: molecular mechanisms and potential therapeutic interventions for diseases
Ji, S., Xiong, M., Chen, H., Liu, Y., Zhou, L., Hong, Y., Wang, M., Wang, C., Fu, X., & Sun, X. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01343-5 · Cited by 166 · see citing works
“found that the X-chromosomespecific enzyme, UTX, maintained the expression of downregulated genes during ageing via demethylase-dependent and -independent epigenetic modulation, contributing to hematopoietic homeostasis and inflammation regulation.(212) There are many phytochemicals and short-chain fatty acids regulat…”
BackgroundZhao, A., Zhou, H., Yang, J., Li, M., & Niu, T. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01342-6 · Cited by 143 · see citing works
“UTX deficiency was associated with the aggregation of reactive oxygen species, reduced DNA damage repair, and aging in HSPCs.(432) Regarding hematologic malignancies, UTX mutations were found in 8% of CMML patients.”
BackgroundInflammation, Aging and Hematopoiesis: A Complex Relationship
Bousounis, P., Bergo, V., & Trompouki, E. (2021) · Cells · doi:10.3390/cells10061386 · Cited by 55 · see citing works
“UTX-deficient mice further presented with trilineage dysplasia, a condition similar to myelodysplastic syndrome (MDS) in humans, which becomes more common with age [92].”
Background20 years of histone lysine demethylases: From discovery to the clinic and beyond
Gray, Z. H., Honer, M. A., Ghatalia, P., Shi, Y., & Whetstine, J. R. (2025) · Cell · doi:10.1016/j.cell.2025.02.023 · Cited by 56 · see citing works
Macrophages at the Crossroad of Meta-Inflammation and Inflammaging
Qu, L., Matz, A., Karlinsey, K. S., Cao, Z., Vella, A. T., & Zhou, B. (2022) · Genes · doi:10.3390/genes13112074 · Cited by 38 · see citing works
“During the aging process, hematopoietic stem cells are skewed to produce more myeloid cells and the remaining lymphoid cells have decreased functionality and an increased propensity to undergo replicative senescence [26].”
BackgroundBoila, L. D., Ghosh, S., Bandyopadhyay, S. K., Jin, L., Murison, A., Zeng, A. G. X., Shaikh, W., Bhowmik, S., Muddineni, S. S. N. A., Biswas, M., et al. (2023) · Leukemia · doi:10.1038/s41375-023-01833-z · Cited by 28 · see citing works
Haematopoietic ageing in health and lifespan
Andersson, R., Mejía-Ramírez, E., & Florian, M. C. (2025) · Nature Cell Biology · doi:10.1038/s41556-025-01739-1 · Cited by 24 · see citing works
“…of epigenetic modulators, such as UTX (also known as KDM6A), which inhibits ageing-associated genes by controlling H3K27me3 and the SWI/SNF complex 42 , or KAT6B, whose expression is lower in aged HSCs, leading to loss of H3K27ac and H4K16ac, and provoking alterations in HSC differentiation 43 .”
Chen, L., Xu, X.-Y., Zhong, X.-D., Liu, Y., Zhu, M.-H., Tao, F., Li, C.-Y., She, Q. S., Yang, G.-J., & Chen, J. (2023) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2023.106409 · Cited by 21 · see citing works
Xie, Y., Luo, Z., Peng, W., Liu, Y., Yuan, F., Xu, J., Sun, Y. X., Lü, H., Wu, T., Jiang, L., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02936-1 · Cited by 21 · see citing works
Li, C., Qin, T., Zhao, J., Jin, Y., Qin, Y., He, R., Wu, T., Duan, C., Jiang, L., Yuan, F., et al. (2024) · Bone Research · doi:10.1038/s41413-024-00323-x · Cited by 16 · see citing works
“21 The H3K27 histone demethylase UTX was also found to be a direct sensor of oxygen, controlling cell fate.”
BackgroundBasta, M. D., Petruk, S., Summer, R., Rosenbloom, J., Wermuth, P. J., Macarak, E., Levin, A. V., Mazo, A., & Walker, J. L. (2023) · iScience · doi:10.1016/j.isci.2023.106570 · Cited by 14 · see citing works
“Similarly, in an aging study using hematopoietic stem-progenitor cells, UTX deficient mice resulted in a significant downregulation of the TGF-b signaling pathway gene set.(49) Moreover, knockdown of KDM6B in lung carcinoma epithelial cells impaired TGFb induced phosphorylation of downstream TFs, Mothers against decap…”
ResultCellular stress and epigenetic regulation in adult stem cells
Llewellyn, J., Baratam, R., Čulig, L., & Beerman, I. (2024) · Life Science Alliance · doi:10.26508/lsa.202302083 · Cited by 13 · see citing works
“This reduction leads to an aged gene expression pro fi le in HSCs, characterized by impaired DNA repair mechanisms and increased oxidative stress (94).”
BackgroundWalters, B. W., Rainsford, S. R., Heuer, R. A., Dias, N., Huang, X., de Rooij, D. G., & Lesch, B. J. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad141 · Cited by 12 · see citing works
“KDM6A has since been shown to play important roles in diverse cellular processes, including embryonic stem cell differentiation, aging, cellular reprogramming, development, and cancer [19–30].”
BackgroundGe, G., Zhang, P., Sui, P., Shi, C., Yang, H., Guo, Y., Rubalcava, I. P., Noor, A., Delma, C. R., Agosto-Peña, J., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci163964 · Cited by 10 · see citing works
“Kdm6b loss in mice has been shown to impair HSC self-renewal and enhance HSC differentiation (33), and Kdm6a -deficient mice have been shown to exhibit abnormal differentiation with myeloid skewing, impaired hematopoietic reconstituting ability, and increased susceptibility to leukemia (49).”
The Hippo Signaling Pathway Manipulates Cellular Senescence
Miyajima, C., Nagasaka, M., Aoki, H., Toriuchi, K., Yamanaka, S., Hashiguchi, S., Morishita, D., Aoyama, M., Hayashi, H., & Inoue, Y. (2024) · Cells · doi:10.3390/cells14010013 · Cited by 9 · see citing works
“Histone demethylases have also been shown to inhibit Hematopoietic stem cell senescence in a methylation activity-dependent manner [90].”
Tian, L., Chavez, M., Chang, G. S., Helton, N., Katerndahl, C. D. S., Miller, C. A., & Wartman, L. D. (2021) · PLoS ONE · doi:10.1371/journal.pone.0255706 · Cited by 8 · see citing works
Epidermal growth factor augments the self-renewal capacity of aged hematopoietic stem cells
Chang, V. Y., He, Y., Grohe, S., Brady, M. R., Chan, A., Kadam, R., Fang, T., Pang, A., Pohl, K. A., Tran, E., et al. (2024) · iScience · doi:10.1016/j.isci.2024.110306 · Cited by 8 · see citing works
“EGF treatment also had no effect on levels of SA-b -galactosidase, a marker of cell senescence, 42 or reactive oxygen species, 43 which characteristically accumulate in aged HSCs (Figures S2D and S2E).”
Hematopoietic aging: Cellular, molecular, and related mechanisms
Ye, L., Tian, C., Li, Y., Pan, H., Hu, J., Shu, L., & Pan, X. (2023) · Chinese Medical Journal · doi:10.1097/cm9.0000000000002871 · Cited by 7 · see citing works
“[28] Sera et al [29] reported that the demethylase ubiquitously transcribed tetratricopeptide repeat on chromosome X (UTX) maintains the integrity and stability of the hematopoietic system by promoting the expression of antiaging genes.”
BackgroundEpigenetic Mechanisms in Hematologic Aging and Premalignant Conditions
Yan, B., Yuan, Q., & Guryanova, O. A. (2023) · Epigenomes · doi:10.3390/epigenomes7040032 · Cited by 8 · see citing works
“Thus, UTX-deficient HSCs acquire an early aging phenotype characterized by myeloid skewing, impaired hematopoietic reconstitution, and increased susceptibility to leukemia [44].”
BackgroundDiscovery and structural studies of histone demethylases
Peng, L., Li, X., Yang, H., Chen, H., Yue, Y., & Peng, S. (2025) · Frontiers in Epigenetics and Epigenomics · doi:10.3389/freae.2025.1594400 · Cited by 6 · see citing works
“KDM6A can also be used as a component of COMPASS complex to regulate aging genes in mice (Sera et al., 2021).”
Koizumi, M., Eto, H., Saeki, M., Seki, M., Fukushima, T., Mukai, S., Ide, H., Sera, Y., 岩崎, 正., Suzuki, Y., et al. (2022) · The FASEB Journal · doi:10.1096/fj.202201002rr · Cited by 6 · see citing works
Self-citationPTIP epigenetically regulates DNA damage-induced cell cycle arrest by upregulating PRDM1
Nakata, Y., Nagasawa, S., Sera, Y., Yamasaki, N., Kanai, A., Kobatake, K., Ueda, T., Koizumi, M., Manabe, I., Kaminuma, O., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-68295-w · Cited by 6 · see citing works
Self-citationOdaira, K., Yasuda, T., Okada, K., Shimooka, T., Kojima, Y., Noura, M., Tamura, S., Kurahashi, S., Iwamoto, E., Sanada, M., et al. (2022) · Cancer Science · doi:10.1111/cas.15641 · Cited by 5 · see citing works
Jia, H., Zhang, H., Mo, D., Xie, B., Qiao, H., Chen, T., Song, H., Xu, X., & Yang, S. L. (2025) · Advanced Science · doi:10.1002/advs.202505723 · Cited by 5 · see citing works
JMJD3-mediated senescence is required to overcome stress-induced hematopoietic defects
Nakata, Y., Ueda, T., Sera, Y., Koizumi, M., Imamura, K., Kanai, A., Ikeda, K., Yamasaki, N., Nagamachi, A., Kobatake, K., et al. (2025) · EMBO Reports · doi:10.1038/s44319-025-00502-9 · Cited by 5 · see citing works
“To address this possibility, we compared RNA-seq data from Jmjd3 Δ / Δ and Utx Δ / Δ LSK cells (Sera et al, 2021) and analyzed genes that were more than 2-fold upregulated or downregulated following Jmjd3 or Utx de fi ciency.”
Self-citationRomhányi, D., Bessenyei, Á., Szabó, K., Kemény, L. V., Gyulai, R., & Groma, G. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26136329 · Cited by 5 · see citing works
“Additionally, KDM6A is vital for lineage-specific differentiation and hematopoietic balance [142–144] and contributes to age-related keratinocyte proliferation/differentiation imbalances [88,98,99] that may be important in the late-onset of the disease [145].”
Rizq, O., Mimura, N., Oshima, M., Momose, S., Takayama, N., Itokawa, N., Koide, S., Shibamiya, A., Miyamoto-Nagai, Y., Rizk, M., et al. (2023) · Leukemia · doi:10.1038/s41375-023-01928-7 · Cited by 5 · see citing works
“RESULTS Utx loss cooperates with Braf to induce B-cell neoplasms To conditionally delete Utx in GC B cells, we crossed Utx mice, in which exons 11 and 12 were floxed [22], with Cγ1-Cre mice, which express Cre recombinase in GC B cells, class switched memory B cells, and plasma cells in response to immunization [23].”
BackgroundSelf-citationMBTD1 preserves adult hematopoietic stem cell pool size and function
Takubo, K., Htun, P. W., Ueda, T., Sera, Y., 岩崎, 正., Koizumi, M., Shiroshita, K., Kobayashi, H., Haraguchi, M., Watanuki, S., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2206860120 · Cited by 4 · see citing works
“We assessed the tolerance of cKO HSCs after hematological stresses by performing 5-fluorouracil (5-FU) treatment (22) and BM transplant (BMT) assays (23).”
Self-citationProgress of genome editing technology and developmental biology useful for radiation research
Miura, K., Ogura, A., Kobatake, K., Honda, H., & Kaminuma, O. (2020) · Journal of Radiation Research · doi:10.1093/jrr/rraa127 · Cited by 4 · see citing works
“We also used this system for investigating a role of Kdm6a in the regulation of aging-associated gene expression in a murine hematopoietic system by achieving tamoxifen-inducible KO of the Kdm6a gene [80].”
MethodSelf-citationHistone modifications in the regulation of erythropoiesis
Wu, X., Xu, H., Xia, E., Gao, L., Hou, Y., Sun, L., Zhang, H., & Cheng, Y. (2025) · Annals of Medicine · doi:10.1080/07853890.2025.2490824 · Cited by 3 · see citing works
“Interestingly, UTX can maintain hematopoietic homeostasis with or without demethylase activity by removing deposition of H3K27me3 at transcriptional initiation sites and protecting the function of HSCs [61].”
Chen, H., Wang, S., Dong, R., Yu, P., Li, T., Hu, L., Wang, M., Qian, Z., Zhou, H., Yue, X., et al. (2025) · Advanced Science · doi:10.1002/advs.202413091 · Cited by 3 · see citing works
Bashir, K., Ghafar, S. A., Rehman, A. T., Waris, T., Farooq, F., & Alamin, A. A. (2024) · Molecular Carcinogenesis · doi:10.1002/mc.23846 · Cited by 2 · see citing works
“In a recent study, it was observed that IDH1 SNP rs11554137 is 11% in pediatric and adult types of AML patients [41].”
Animal models of Kabuki syndrome and their applicability to novel drug discovery
Mertens, M., Khalife, L., Ma, X., & Bodamer, O. A. (2025) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2025.2457624 · Cited by 2 · see citing works
“The following will describe several Mouse models using this approach [90].”
Zhao, J., Sheng, X., Ding, Y., Wen, H., Zheng, L., Sun, Y. X., He, R., Li, C., Qin, T., Wu, T., et al. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.10.019 · Cited by 2 · see citing works
“In line with our discovery, previous research has identified UTX as a regulator of cellular senescence in various non-traumatic scenarios, including osteoarthritis [73], age-related hematopoietic diseases [74], and cancer stem cell formation [75].”
KDM6A loss sensitizes human acute myeloid leukemia to PARP and BCL2 inhibitionPreprint
Boila, L. D., Ghosh, S., Bandyopadhyay, S. K., Jin, L., Murison, A., Zeng, A. G. X., Shaikh, W., Bhowmik, S., Muddineni, S. S. N. A., Biswas, M., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.12.498585 · Cited by 1 · see citing works
“KDM6A escapes X chromosome inactivation, and Utx null homozygous female mice spontaneously develop aging associated myeloid leukemia (9, 13).”
BackgroundWalters, B. W., Rainsford, S. R., Dias, N., Huang, X., de Rooij, D. G., & Lesch, B. J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.27.513976
The pathogenetic significance of exhausted T cells in a mouse model of mature B cell neoplasms
Shibamiya, A., Miyamoto‐Nagai, Y., Koide, S., Oshima, M., Rizq, O., Aoyama, K., Nakajima‐Takagi, Y., Kato, R., Kayamori, K., Isshiki, Y., et al. (2023) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-023-03447-x
“Mice with the conditional expression of BrafV600E or Utx conditional knockout mice were previously reported [17, 18].”
BackgroundSelf-citationyang, Y., Chen, L., zhao, Q., zheng, Q., tang, J., Zhou, D., Li, L., peng, Z., Tan, X., guo, W., et al. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4829198
Xie, Y., Luo, Z., Peng, W., Liu, Y., Yuan, F., Xu, J., Sun, Y., Lu, H., Wu, T., Jiang, L., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26638668
Unlocking the HOX: Homeobox Genes as Regulators of Hematopoietic Development
Moyer, D. L., Henning, A. M., & Medina, K. L. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27073285
“Utx has emerged as a promising HOX regulator given that experiments which alter its expression lead to HOX-like phenotypes [121].”
MLL3 and MLL4 sustain hematopoietic stem cell multipotency by opposing a B-cell default state
Wang, H. C., Chen, R., Yang, W., Muthukumar, R., Hu, T., Patel, R. M., Casey, E. B., Denby, E., Zhang, R., Xie, G., et al. (2026) · Blood · doi:10.1182/blood.2025032969
- Authors
- Sera, Y., Nakata, Y., Ueda, T., Yamasaki, N., Koide, S., Kobayashi, H., Ikeda, K.-I., Kobatake, K., Iwasaki, M., Oda, H., Wolff, L., Kanai, A., Nagamachi, A., Inaba, T., Sotomaru, Y., Ichinohe, T., Koizumi, M., Miyakawa, Y., Honda, Z.-I., Iwama, A., Suda, T., Takubo, K., & Honda, H.
- Affiliations
- Tokyo Women's Medical University (JP)
- University of Miami (US)
- Kindai University (JP)
- Hiroshima University (JP)
- Institute of Medical Science, The University of Tokyo (JP)
- National Center for Global Health and Medicine (JP)
- Department of Disease Models, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan;
- Human Disease Models, Institute of Laboratory Animals, Tokyo Women’s Medical University, Tokyo, Japan;
- National Cancer Institute (US)
- Research Institute for Radiation Biology and Medicine, Hiroshima University (JP)
- Natural Science Center for Basic Research and Development, Hiroshima University (JP)
- Ochanomizu University (JP)
- National University of Singapore (SG)
- Corresponding author
- Sera, Yasuyuki
- Nakata, Yuichiro
- Ueda, Takeshi
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2021-02-18
- Volume
- 137
- Issue
- 7
- Pages
- 908-922
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC7918186
- OpenAlex
- W3105315244
- Cited by
- 42
- References
- 94
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 8 · 2023: 13 · 2022: 6 · 2021: 2 · 2020: 1
- FWCI
- 3.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (19H05653, 19H03693, 18H02845, 19K22546, 19H01056, 19K17918, 18K18196, 19K17847, 18K08357, 20K07346, 21K08395, 21K08378, 18H05284)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- KDM6A, H3K27 demethylase, hematopoietic aging, hematopoietic stem cells, hematopoietic stem and progenitor cells, epigenetic regulation, myeloid skewing, extramedullary hematopoiesis, leukemia susceptibility, DNA double-strand break repair, reactive oxygen species, SWI/SNF complex
- MeSH terms
- Immune Reconstitution, Aging, Animals, DNA Repair, Female, Gene Expression Regulation, Hematopoiesis, Hematopoiesis, Extramedullary, Hematopoietic System, Leukemia, Experimental, Male, Moloney murine leukemia virus, Radiation Chimera, Recombinant Proteins, Transcription Factors, Virus Integration, Cellular Senescence, Reactive Oxygen Species, Mice, Knockout, Genetic Predisposition to Disease, Myeloid Cells, Histone Code, Mice, DNA Breaks, Double-Stranded, Histone Demethylases, Jumonji Domain-Containing Histone Demethylases
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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