Fukumoto Aono, Yamanaka Tomoki, Yanaizu Motoaki, Nakamori Masayuki, Hama Manami, Yasumizu Yoshiaki, Shiotsu Kana, Matsumura Tsuyoshi, Nutter Curtis A, Kubota Tomoya, Fujimura Harutoshi, Kino Yoshihiro, Swanson Maurice S, Inoue Kimiko, Takahashi Masanori P
Clinical Neurophysiology, Department of Clinical Laboratory and Biomedical Sciences, Graduate School of Medicine, The University of Osaka, 1-7 Yamadaoka, Suita, Osaka, 565-0871, Japan.
Department of RNA Pathobiology and Therapeutics, Meiji Pharmaceutical University, 2-522-1, Noshio, Kiyose, Tokyo 204-8588, Japan.
Hum Mol Genet. 2025 Aug 13. doi: 10.1093/hmg/ddaf124.
Myotonic dystrophy type 1 (DM1) is caused by expanded CTG repeats in the DMPK 3'-untranslated region, affecting multiple organs, including the skeletal muscles, eyes, heart, central nervous system, and endocrine system. A major pathogenic event in DM1 is the sequestration of muscleblind-like (MBNL) proteins by CUG repeat-containing RNAs transcribed from expanded repeats. Among the various symptoms of DM1, lipid abnormalities and liver dysfunction are frequent but remain understudied. Although abnormal splicing of insulin receptor RNA is implicated, it cannot fully explain these abnormalities. To investigate the molecular mechanisms, we performed transcriptome analysis of postmortem livers from patients with DM1 and Mbnl-knockout mice. RNA-sequencing revealed differentially expressed genes (DEGs) and aberrant splicing in DM1 livers. A comparison of Mbnl1- and Mbnl2-knockout mouse livers indicated that MBNL1 accounts for some of the transcriptomic changes observed in patients with DM1. The DEGs included those related to lipid metabolism and liver fibrosis. DM1-associated changes in the liver transcriptome partially resolved sexual dimorphism in gene expression and uncovered distinct sex-specific pathway alterations. Besides the known MBNL-regulated genes, those related to lipid and glucose metabolism were identified in the aberrant splicing clusters detected in DM1. A correlation between serum gamma-glutamyl transferase levels and overall splicing abnormalities was observed, linking splicing changes in the liver to clinical abnormalities. These findings provide new insights into the molecular basis of DM1-related metabolic and hepatic abnormalities, enhancing our understanding of the systemic effects of this disease.
1型强直性肌营养不良症(DM1)由DMPK 3'非翻译区的CTG重复序列扩增引起,会影响多个器官,包括骨骼肌、眼睛、心脏、中枢神经系统和内分泌系统。DM1的一个主要致病事件是含有CUG重复序列的RNA(由扩增的重复序列转录而来)隔离肌肉盲样(MBNL)蛋白。在DM1的各种症状中,脂质异常和肝功能障碍很常见,但仍未得到充分研究。尽管胰岛素受体RNA的异常剪接与之有关,但它不能完全解释这些异常。为了研究其分子机制,我们对DM1患者的死后肝脏和Mbnl基因敲除小鼠进行了转录组分析。RNA测序揭示了DM1肝脏中差异表达基因(DEG)和异常剪接。对Mbnl1和Mbnl2基因敲除小鼠肝脏的比较表明,MBNL1导致了DM1患者中观察到的一些转录组变化。差异表达基因包括与脂质代谢和肝纤维化相关的基因。DM1相关的肝脏转录组变化部分消除了基因表达中的性别二态性,并揭示了不同的性别特异性途径改变。除了已知的MBNL调节基因外,在DM1中检测到的异常剪接簇中还发现了与脂质和葡萄糖代谢相关的基因。观察到血清γ-谷氨酰转移酶水平与总体剪接异常之间存在相关性,将肝脏中的剪接变化与临床异常联系起来。这些发现为DM1相关代谢和肝脏异常的分子基础提供了新的见解,增进了我们对这种疾病全身影响的理解。