Das Jhuma, Aleksandrov Andrei A, Cui Liying, He Lihua, Riordan John R, Dokholyan Nikolay V
Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
Cystic Fibrosis Treatment and Research Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
PLoS Comput Biol. 2017 Jun 22;13(6):e1005594. doi: 10.1371/journal.pcbi.1005594. eCollection 2017 Jun.
Mutations in the Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) gene affect CFTR protein biogenesis or its function as a chloride channel, resulting in dysregulation of epithelial fluid transport in the lung, pancreas and other organs in cystic fibrosis (CF). Development of pharmaceutical strategies to treat CF requires understanding of the mechanisms underlying channel function. However, incomplete 3D structural information on the unique ABC ion channel, CFTR, hinders elucidation of its functional mechanism and correction of cystic fibrosis causing mutants. Several CFTR homology models have been developed using bacterial ABC transporters as templates but these have low sequence similarity to CFTR and are not ion channels. Here, we refine an earlier model in an outward (OWF) and develop an inward (IWF) facing model employing an integrated experimental-molecular dynamics simulation (200 ns) approach. Our IWF structure agrees well with a recently solved cryo-EM structure of a CFTR IWF state. We utilize cysteine cross-linking to verify positions and orientations of residues within trans-membrane helices (TMHs) of the OWF conformation and to reconstruct a physiologically relevant pore structure. Comparison of pore profiles of the two conformations reveal a radius sufficient to permit passage of hydrated Cl- ions in the OWF but not the IWF model. To identify structural determinants that distinguish the two conformations and possible rearrangements of TMHs within them responsible for channel gating, we perform cross-linking by bifunctional reagents of multiple predicted pairs of cysteines in TMH 6 and 12 and 6 and 9. To determine whether the effects of cross-linking on gating observed are the result of switching of the channel from open to close state, we also treat the same residue pairs with monofunctional reagents in separate experiments. Both types of reagents prevent ion currents indicating that pore blockage is primarily responsible.
囊性纤维化跨膜传导调节因子(CFTR)基因的突变会影响CFTR蛋白的生物合成或其作为氯离子通道的功能,导致囊性纤维化(CF)患者肺部、胰腺和其他器官的上皮液体运输失调。开发治疗CF的药物策略需要了解通道功能的潜在机制。然而,关于独特的ABC离子通道CFTR的不完整三维结构信息阻碍了对其功能机制的阐明以及对导致囊性纤维化的突变体的校正。已经使用细菌ABC转运蛋白作为模板开发了几种CFTR同源模型,但这些模型与CFTR的序列相似性较低,并且不是离子通道。在这里,我们改进了一个向外(OWF)的早期模型,并采用综合实验-分子动力学模拟(200 ns)方法开发了一个向内(IWF)的模型。我们的IWF结构与最近解析的CFTR IWF状态的冷冻电镜结构非常吻合。我们利用半胱氨酸交联来验证OWF构象跨膜螺旋(TMHs)内残基的位置和取向,并重建生理相关的孔结构。两种构象的孔轮廓比较显示,OWF模型中有一个足以允许水合氯离子通过的半径,而IWF模型中则没有。为了确定区分两种构象的结构决定因素以及其中TMHs可能的重排对通道门控的影响,我们对TMH 6和12以及6和9中多对预测的半胱氨酸进行双功能试剂交联。为了确定观察到的交联对门控的影响是否是通道从开放状态切换到关闭状态的结果,我们还在单独的实验中用单功能试剂处理相同的残基对。两种类型的试剂都能阻止离子电流,表明孔堵塞是主要原因。