Vitamin C–dependent lysine demethylase 6 (KDM6)-mediated demethylation promotes a chromatin state that supports the endothelial-to-hematopoietic transition
Open accessAbstract
Hematopoietic stem cells (HSCs)/progenitor cells (HPCs) are generated from hemogenic endothelial cells (HECs) during the endothelial-to-hematopoietic transition (EHT); however, the underlying mechanism remains poorly understood. Here, using an array of approaches, including CRSPR/Cas9 gene knockouts, RNA-Seq, ChIP-Seq, ATAC-Seq etc., we report that vitamin C (Vc) is essential in HPC generation during human pluripotent stem cell (hPSC) differentiation in defined culture conditions. Mechanistically, we found that the endothelial cells generated in the absence of Vc fail to undergo the EHT because of an apparent failure in opening up genomic loci essential for hematopoiesis. Under Vc deficiency, these loci exhibited abnormal accumulation of histone H3 trimethylation at Lys-27 (H3K27me3), a repressive histone modification that arose because of lower activities of demethylases that target H3K27me3. Consistently, deletion of the two H3K27me3 demethylases, Jumonji domain-containing 3 (JMJD3 or KDM6B) and histone demethylase UTX (UTX or KDM6A), impaired HPC generation even in the presence of Vc. Furthermore, we noted that Vc and jmjd3 are also important for HSC generation during zebrafish development. Together, our findings reveal an essential role for Vc in the EHT for hematopoiesis, and identify KDM6-mediated chromatin demethylation as an important regulatory mechanism in hematopoietic cell differentiation.
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Jumonji-C (JmjC) domain-containing proteins are responsible for hydroxylation of specific histone lysines leading to histone demethylation.
“One of the most known enzyme groups are Jumonji-C (JmjC) domain-containing proteins responsible for hydroxylation of specific histone lysines leading to histone demethylation (JmjC demethylases, e.g., JHDMs and KDMs families) [107,112,113,114].”
From Vitamin C-Sources, Physiological Role, Kinetics, Deficiency, Use, Toxicity, and Determination (2021) · cites this paper as [113]
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Zhang, C., Wei, Y., Zhang, Y., Zhang, J., Qi, X., Zhou, M., & Shan, Y. (2021) · Stem Cell Research · doi:10.1016/j.scr.2021.102234 · Cited by 2 · see citing works
Self-citationL-Ascorbic Acid in the Epigenetic Regulation of Cancer Development and Stem Cell Reprogramming
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Epigenetics, cell cycle and stem cell metabolism. Formation of insulin-producing cells
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Self-citationAutophagy is essential for human myelopoiesis
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Self-citationGeneration of a RGS18 gene knockout cell line from a human embryonic stem cell line by CRISPR/Cas9
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Self-citationIDH1 regulates human erythropoiesis by eliciting chromatin state reprogrammingPreprint
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Self-citation
- Authors
- Zhang, T., Huang, K., Zhu, Y., Wang, T., Shan, Y., Long, B., Li, Y., Chen, Q., Wang, P., Zhao, S., Li, D., Wu, C., Kang, B., Gu, J., Mai, Y., Wang, Q., Li, J., Zhang, Y., Liang, Z., Guo, L., Wu, F., Su, S., Wang, J., Gao, M., Zhong, X., Liao, B., Chen, J., Zhang, X., Shu, X., Pei, D., Nie, J., & Pan, G.
- Affiliations
- Chinese Academy of Sciences (CN)
- Sun Yat-sen University (CN)
- Corresponding author
- Pan, Guangjin
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 294
- Issue
- 37
- Pages
- 13657-13670
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC6746450
- OpenAlex
- W2963301787
- Cited by
- 47
- References
- 50
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 8 · 2023: 4 · 2022: 8 · 2021: 10 · 2020: 10
- FWCI
- 4.95
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Key Research and Development Program of China, Stem Cell and Translational Research (2017YFA0102601)
- Strategic Priority Research Program of Chinese Academy of Science (XDA16030504)
- Science and Technology Planning Project of Guangdong Province, China (2017B030314056, 2014B030301058)
- Frontier and Key Technology Innovation Special Grant from the Department of Science and Technology of Guangdong Province (2014B020225006, 2014B020225002, 2014B050504008, 2015B020228003, 2016B030230002, 2016B030229008)
- Natural Science Foundation of Guangdong Province, China (2016A030313167)
- National Basic Research Program of China, 973 Program of China (2015CB964900)
- International Science and Technology Cooperation Program of China (2014DFA30180)
- National Natural Science Foundation of China (31371514, 31421004, 31801225, 81571238, 81700149)
- Cooperation Grant of Natural Science Foundation of Guangdong Province (2014A030313801, 2014A030312012, 2015A030310229, 2015A030310254, 2017A030310376)
- Science and Information Technology of Guangzhou Key Project (201508020258, 201506010092)
- Guangzhou Science and Technology Program General Project (201804010339)
- Guangdong Province Special Program for Elite Scientists in Science and Technology Innovation (2015TX01R203)
- Innovative Team Program of Guangzhou Regenerative Medicine and Health Guangdong Laboratory (2018GZR110104005)
- Informationization Special Project of Chinese Academy of Sciences E-Science Application for Knowledge Discovery in Stem Cells (XXH13506–203)
- Open Research Funds of the State Key Laboratory of Ophthalmology (2019KF06)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- vitamin C, endothelial-to-hematopoietic transition, JMJD3, KDM6A, H3K27me3 demethylation, histone demethylase, hematopoietic stem cells, hematopoietic progenitor cells, hemogenic endothelial cells, chromatin regulation, H3K27me3
- MeSH terms
- Demethylation, Animals, Ascorbic Acid, Cell Differentiation, Chromatin, Hematopoietic Stem Cells, Histones, Humans, Lysine, Methylation, Zebrafish, Animals, Genetically Modified, Pluripotent Stem Cells, Endothelial Cells, Histone Demethylases, Jumonji Domain-Containing Histone Demethylases
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