Li Mengjia, Zhang Hengchao, Wu Xiuyun, Yu Mengqi, Yang Qianqian, Sun Lei, Li Wei, Jiang Zhongxing, Xue Fumin, Wang Ting, An Xuili, Chen Lixiang
State Key Laboratory of Metabolic Dysregulation and Prevention and Treatment of Esophageal Cancer; School of Life Sciences, Zhengzhou University, Zhengzhou, China.
Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China.
Elife. 2025 Apr 29;13:RP100406. doi: 10.7554/eLife.100406.
Isocitrate dehydrogenase 1 (IDH1) is the key enzyme that can modulate cellular metabolism, epigenetic modification, and redox homeostasis. Gain-of-function mutations and decreased expression of IDH1 have been demonstrated to be associated with pathogenesis of various myeloid malignancies characterized by ineffective erythropoiesis, such as acute myeloid leukemia (AML) and myelodysplastic syndrome (MDS). However, the function and mechanism of IDH1 in human erythropoiesis still remains unclear. Here, utilizing the human erythropoiesis system, we present an evidence of IDH1-mediated chromatin state reprogramming besides its well-characterized metabolism effects. We found that knockdown IDH1 induced chromatin reorganization and subsequently led to abnormalities biological events in erythroid precursors, which could not be rescued by addition of reactive oxygen species (ROS) scavengers or supplementation of α-ketoglutarate (α-KG).We further revealed that knockdown IDH1 induces genome-wide changes in distribution and intensity of multiple histone marks, among which H3K79me3 was identified as a critical factor in chromatin state reprogramming. Integrated analysis of ChIP-seq, ATAC-seq, and RNA-seq recognized that SIRT1 was the key gene affected by IDH1 deficiency. Thus, our current work provided novel insights for further clarifying fundamental biological function of IDH1 which has substantial implications for an in-depth understanding of pathogenesis of diseases with IDH1 dysfunction and accordingly development of therapeutic strategies.
异柠檬酸脱氢酶1(IDH1)是一种关键酶,可调节细胞代谢、表观遗传修饰和氧化还原稳态。功能获得性突变和IDH1表达降低已被证明与各种以无效红细胞生成特征的髓系恶性肿瘤的发病机制有关,如急性髓系白血病(AML)和骨髓增生异常综合征(MDS)。然而,IDH1在人类红细胞生成中的功能和机制仍不清楚。在这里,利用人类红细胞生成系统,我们除了展示其已被充分表征的代谢效应外,还提供了IDH1介导的染色质状态重编程的证据。我们发现敲低IDH1会诱导染色质重组,随后导致红系前体细胞出现异常生物学事件,而添加活性氧(ROS)清除剂或补充α-酮戊二酸(α-KG)并不能挽救这些事件。我们进一步揭示,敲低IDH1会诱导全基因组范围内多种组蛋白标记的分布和强度发生变化,其中H3K79me3被确定为染色质状态重编程中的关键因素。ChIP-seq、ATAC-seq和RNA-seq的综合分析表明,SIRT1是受IDH1缺乏影响的关键基因。因此,我们目前的工作为进一步阐明IDH1的基本生物学功能提供了新的见解,这对于深入理解IDH1功能障碍相关疾病的发病机制以及相应治疗策略的开发具有重要意义。