Kirby Tyler J, Zahr Hind C, Fong Ern Hwei Hannah, Lammerding Jan
Department of Physiology, Amsterdam Cardiovascular Sciences, Amsterdam Movement Sciences, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, Netherlands.
Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY, USA.
Cell Death Discov. 2024 May 22;10(1):245. doi: 10.1038/s41420-024-01998-1.
Lamins A and C, encoded by the LMNA gene, are nuclear intermediate filaments that provide structural support to the nucleus and contribute to chromatin organization and transcriptional regulation. LMNA mutations cause muscular dystrophies, dilated cardiomyopathy, and other diseases. The mechanisms by which many LMNA mutations result in muscle-specific diseases have remained elusive, presenting a major hurdle in the development of effective treatments. Previous studies using striated muscle laminopathy mouse models found that cytoskeletal forces acting on mechanically fragile Lmna-mutant nuclei led to transient nuclear envelope rupture, extensive DNA damage, and activation of DNA damage response (DDR) pathways in skeletal muscle cells in vitro and in vivo. Furthermore, hearts of Lmna mutant mice have elevated activation of the tumor suppressor protein p53, a central regulator of DDR signaling. We hypothesized that elevated p53 activation could present a pathogenic mechanism in striated muscle laminopathies, and that eliminating p53 activation could improve muscle function and survival in laminopathy mouse models. Supporting a pathogenic function of p53 activation in muscle, stabilization of p53 was sufficient to reduce contractility and viability in wild-type muscle cells in vitro. Using three laminopathy models, we found that increased p53 activity in Lmna-mutant muscle cells primarily resulted from mechanically induced damage to the myonuclei, and not from altered transcriptional regulation due to loss of lamin A/C expression. However, global deletion of p53 in a severe muscle laminopathy model did not reduce the disease phenotype or increase survival, indicating that additional drivers of disease must contribute to the disease pathogenesis.
由LMNA基因编码的核纤层蛋白A和C是核中间丝,为细胞核提供结构支持,并有助于染色质组织和转录调控。LMNA突变会导致肌肉萎缩症、扩张型心肌病和其他疾病。许多LMNA突变导致肌肉特异性疾病的机制仍然难以捉摸,这是有效治疗方法开发中的一个主要障碍。先前使用横纹肌核纤层病小鼠模型的研究发现,作用于机械脆弱的Lmna突变核的细胞骨架力会导致核膜瞬时破裂、广泛的DNA损伤以及体外和体内骨骼肌细胞中DNA损伤反应(DDR)途径的激活。此外,Lmna突变小鼠的心脏中肿瘤抑制蛋白p53的激活增加,p53是DDR信号传导的核心调节因子。我们假设p53激活增加可能是横纹肌核纤层病的一种致病机制,消除p53激活可能会改善核纤层病小鼠模型的肌肉功能和存活率。支持p53激活在肌肉中的致病作用的是,p53的稳定足以降低体外野生型肌肉细胞的收缩力和活力。使用三种核纤层病模型,我们发现Lmna突变肌肉细胞中p53活性增加主要是由机械诱导的肌核损伤引起的,而不是由于核纤层蛋白A/C表达缺失导致的转录调控改变。然而,在严重的肌肉核纤层病模型中全局删除p53并没有减轻疾病表型或提高存活率,这表明疾病的其他驱动因素必定促成了疾病的发病机制。