State Key Laboratory of Cellular Stress Biology, School of Pharmaceutical Sciences, Faculty of Medicine and Life Sciences, Xiamen University, Xiang'an South Road, Xiamen, Fujian 361102, China.
Fujian Provincial Key Laboratory of Innovative Drug Target Research, School of Pharmaceutical Sciences, Faculty of Medicine and Life Sciences, Xiamen University, Xiang'an South Road, Xiamen, Fujian 361102, China.
Nucleic Acids Res. 2024 Jul 8;52(12):6811-6829. doi: 10.1093/nar/gkae329.
Protein arginine methyltransferase CARM1 has been shown to methylate a large number of non-histone proteins, and play important roles in gene transcriptional activation, cell cycle progress, and tumorigenesis. However, the critical substrates through which CARM1 exerts its functions remain to be fully characterized. Here, we reported that CARM1 directly interacts with the GATAD2A/2B subunit in the nucleosome remodeling and deacetylase (NuRD) complex, expanding the activities of NuRD to include protein arginine methylation. CARM1 and NuRD bind and activate a large cohort of genes with implications in cell cycle control to facilitate the G1 to S phase transition. This gene activation process requires CARM1 to hypermethylate GATAD2A/2B at a cluster of arginines, which is critical for the recruitment of the NuRD complex. The clinical significance of this gene activation mechanism is underscored by the high expression of CARM1 and NuRD in breast cancers, and the fact that knockdown CARM1 and NuRD inhibits cancer cell growth in vitro and tumorigenesis in vivo. Targeting CARM1-mediated GATAD2A/2B methylation with CARM1 specific inhibitors potently inhibit breast cancer cell growth in vitro and tumorigenesis in vivo. These findings reveal a gene activation program that requires arginine methylation established by CARM1 on a key chromatin remodeler, and targeting such methylation might represent a promising therapeutic avenue in the clinic.
精氨酸甲基转移酶 CARM1 已被证明可以甲基化大量非组蛋白,并且在基因转录激活、细胞周期进展和肿瘤发生中发挥重要作用。然而,CARM1 发挥其功能的关键底物仍有待充分表征。在这里,我们报道 CARM1 直接与核小体重塑和去乙酰化酶(NuRD)复合物中的 GATAD2A/2B 亚基相互作用,将 NuRD 的活性扩展到包括蛋白质精氨酸甲基化。CARM1 和 NuRD 结合并激活了一大群与细胞周期控制有关的基因,以促进 G1 到 S 期的转变。这个基因激活过程需要 CARM1 在一组精氨酸上高度甲基化 GATAD2A/2B,这对于 NuRD 复合物的招募至关重要。CARM1 和 NuRD 在乳腺癌中的高表达,以及敲低 CARM1 和 NuRD 抑制体外癌细胞生长和体内肿瘤发生的事实,强调了这种基因激活机制的临床意义。用 CARM1 特异性抑制剂靶向 CARM1 介导的 GATAD2A/2B 甲基化,可在体外强烈抑制乳腺癌细胞生长和体内肿瘤发生。这些发现揭示了一种需要 CARM1 在关键染色质重塑剂上建立的精氨酸甲基化的基因激活程序,靶向这种甲基化可能代表临床有前途的治疗途径。