Emory University School of Medicine, Atlanta, Georgia, USA.
Institute for Biochemistry & Molecular Biology, University of Hamburg, Hamburg, Germany.
J Clin Invest. 2019 Dec 2;129(12):5236-5253. doi: 10.1172/JCI124282.
Cystic fibrosis (CF) is caused by mutations in the CF transmembrane conductance regulator (CFTR), with approximately 90% of patients harboring at least one copy of the disease-associated variant F508del. We utilized a yeast phenomic system to identify genetic modifiers of F508del-CFTR biogenesis, from which ribosomal protein L12 (RPL12/uL11) emerged as a molecular target. In the present study, we investigated mechanism(s) by which suppression of RPL12 rescues F508del protein synthesis and activity. Using ribosome profiling, we found that rates of translation initiation and elongation were markedly slowed by RPL12 silencing. However, proteolytic stability and patch-clamp assays revealed RPL12 depletion significantly increased F508del-CFTR steady-state expression, interdomain assembly, and baseline open-channel probability. We next evaluated whether Rpl12-corrected F508del-CFTR could be further enhanced with concomitant pharmacologic repair (e.g., using clinically approved modulators lumacaftor and tezacaftor) and demonstrated additivity of these treatments. Rpl12 knockdown also partially restored maturation of specific CFTR variants in addition to F508del, and WT Cftr biogenesis was enhanced in the pancreas, colon, and ileum of Rpl12 haplosufficient mice. Modulation of ribosome velocity therefore represents a robust method for understanding both CF pathogenesis and therapeutic response.
囊性纤维化 (CF) 是由 CF 跨膜电导调节因子 (CFTR) 的突变引起的,大约 90%的患者至少携带一个与疾病相关的变体 F508del。我们利用酵母表型系统来鉴定 F508del-CFTR 生物发生的遗传修饰因子,其中核糖体蛋白 L12 (RPL12/uL11) 作为一个分子靶标脱颖而出。在本研究中,我们研究了抑制 RPL12 可挽救 F508del 蛋白合成和活性的机制。通过核糖体谱分析,我们发现 RPL12 沉默显著减缓了翻译起始和延伸的速度。然而,蛋白酶体稳定性和膜片钳检测显示 RPL12 耗竭显著增加了 F508del-CFTR 的稳定表达、域间组装和基础开放通道概率。我们接下来评估了 Rpl12 校正的 F508del-CFTR 是否可以通过同时进行药理学修复 (例如,使用临床批准的调节剂 lumacaftor 和 tezacaftor) 进一步增强,并证明这些治疗方法具有相加性。Rpl12 敲低还部分恢复了除 F508del 以外的特定 CFTR 变体的成熟,并且 Rpl12 杂合子小鼠的胰腺、结肠和回肠中的 WT Cftr 生物发生也得到了增强。因此,调节核糖体速度是理解 CF 发病机制和治疗反应的一种有效方法。