Department of Medicine, Division of Cardiovascular Medicine, University of Wisconsin-Madison, Madison, Wisconsin 53705, United States.
Department of Cell and Regenerative Biology, Human Proteomics Program, University of Wisconsin-Madison, Madison, Wisconsin 53705, United States.
J Proteome Res. 2024 Jun 7;23(6):1970-1982. doi: 10.1021/acs.jproteome.3c00853. Epub 2024 May 8.
Lamin A/C (LMNA) is an important component of nuclear lamina. Mutations cause arrhythmia, heart failure, and sudden cardiac death. While LMNA-associated cardiomyopathy typically has an aggressive course that responds poorly to conventional heart failure therapies, there is variability in severity and age of penetrance between and even within specific mutations, which is poorly understood at the cellular level. Further, this heterogeneity has not previously been captured to mimic the heterozygous state, nor have the hundreds of clinical LMNA mutations been represented. Herein, we have overexpressed cardiopathic LMNA variants in HEK cells and utilized state-of-the-art quantitative proteomics to compare the global proteomic profiles of (1) aggregating Q353 K alone, (2) Q353 K coexpressed with WT, (3) aggregating N195 K coexpressed with WT, and (4) nonaggregating E317 K coexpressed with WT to help capture some of the heterogeneity between mutations. We analyzed each data set to obtain the differentially expressed proteins (DEPs) and applied gene ontology (GO) and KEGG pathway analyses. We found a range of 162 to 324 DEPs from over 6000 total protein IDs with differences in GO terms, KEGG pathways, and DEPs important in cardiac function, further highlighting the complexity of cardiac laminopathies. Pathways disrupted by LMNA mutations were validated with redox, autophagy, and apoptosis functional assays in both HEK 293 cells and in induced pluripotent stem cell derived cardiomyocytes (iPSC-CMs) for LMNA N195 K. These proteomic profiles expand our repertoire for mutation-specific downstream cellular effects that may become useful as druggable targets for personalized medicine approach for cardiac laminopathies.
核纤层蛋白 A/C(LMNA)是核纤层的重要组成部分。突变会导致心律失常、心力衰竭和心源性猝死。虽然 LMNA 相关心肌病通常具有侵袭性病程,对传统心力衰竭治疗反应不佳,但特定突变之间甚至同一突变内的严重程度和发病年龄存在变异性,这在细胞水平上理解甚少。此外,这种异质性以前没有被捕获来模拟杂合状态,也没有代表数百种临床 LMNA 突变。在此,我们在 HEK 细胞中过表达了致病变异的 LMNA,并利用最先进的定量蛋白质组学技术,比较了(1)单独聚集的 Q353 K,(2)与 WT 共表达的 Q353 K,(3)与 WT 共表达的聚集的 N195 K,和(4)与 WT 共表达的非聚集的 E317 K 的全局蛋白质组谱,以帮助捕捉突变之间的一些异质性。我们分析了每个数据集以获得差异表达蛋白(DEPs),并应用基因本体论(GO)和 KEGG 途径分析。我们从超过 6000 个总蛋白质 ID 中获得了范围为 162 到 324 个 DEPs,GO 术语、KEGG 途径和对心脏功能重要的 DEPs 存在差异,进一步突出了心脏层粘连蛋白病的复杂性。通过在 HEK 293 细胞和诱导多能干细胞衍生的心肌细胞(iPSC-CMs)中针对 LMNA N195 K 进行的氧化还原、自噬和细胞凋亡功能测定,验证了由 LMNA 突变破坏的途径。这些蛋白质组谱扩展了我们对突变特异性下游细胞效应的了解,这可能成为心脏层粘连蛋白病个性化医学方法的有价值的药物靶点。