Ding Xi-Qin, Thapa Arjun, Ma Hongwei, Xu Jianhua, Elliott Michael H, Rodgers Karla K, Smith Marci L, Wang Jin-Shan, Pittler Steven J, Kefalov Vladimir J
From the Departments of Cell Biology and
From the Departments of Cell Biology and.
J Biol Chem. 2016 Apr 15;291(16):8721-34. doi: 10.1074/jbc.M115.696138. Epub 2016 Feb 18.
Cone photoreceptor cyclic nucleotide-gated (CNG) channels play a pivotal role in cone phototransduction, which is a process essential for daylight vision, color vision, and visual acuity. Mutations in the cone channel subunits CNGA3 and CNGB3 are associated with human cone diseases, including achromatopsia, cone dystrophies, and early onset macular degeneration. Mutations in CNGB3 alone account for 50% of reported cases of achromatopsia. This work investigated the role of CNGB3 in cone light response and cone channel structural stability. As cones comprise only 2-3% of the total photoreceptor population in the wild-type mouse retina, we used Cngb3(-/-)/Nrl(-/-) mice with CNGB3 deficiency on a cone-dominant background in our study. We found that, in the absence of CNGB3, CNGA3 was able to travel to the outer segments, co-localize with cone opsin, and form tetrameric complexes. Electroretinogram analyses revealed reduced cone light response amplitude/sensitivity and slower response recovery in Cngb3(-/-)/Nrl(-/-) mice compared with Nrl(-/-) mice. Absence of CNGB3 expression altered the adaptation capacity of cones and severely compromised function in bright light. Biochemical analysis demonstrated that CNGA3 channels lacking CNGB3 were more resilient to proteolysis than CNGA3/CNGB3 channels, suggesting a hindered structural flexibility. Thus, CNGB3 regulates cone light response kinetics and the channel structural flexibility. This work advances our understanding of the biochemical and functional role of CNGB3 in cone photoreceptors.
视锥光感受器环核苷酸门控(CNG)通道在视锥光转导过程中起关键作用,而视锥光转导是明视觉、色觉和视敏度所必需的过程。视锥通道亚基CNGA3和CNGB3的突变与人类视锥疾病相关,包括全色盲、视锥营养不良和早发性黄斑变性。仅CNGB3的突变就占已报道全色盲病例的50%。这项工作研究了CNGB3在视锥光反应和视锥通道结构稳定性中的作用。由于视锥细胞仅占野生型小鼠视网膜中光感受器总数的2-3%,我们在研究中使用了在视锥细胞占主导的背景下缺乏CNGB3的Cngb3(-/-)/Nrl(-/-)小鼠。我们发现,在没有CNGB3的情况下,CNGA3能够迁移到外段,与视锥视蛋白共定位,并形成四聚体复合物。视网膜电图分析显示,与Nrl(-/-)小鼠相比,Cngb3(-/-)/Nrl(-/-)小鼠的视锥光反应幅度/敏感性降低,反应恢复较慢。CNGB3表达的缺失改变了视锥细胞的适应能力,并严重损害了强光下的功能。生化分析表明,缺乏CNGB3的CNGA3通道比CNGA3/CNGB3通道对蛋白水解更具弹性,这表明其结构灵活性受到阻碍。因此,CNGB3调节视锥光反应动力学和通道结构灵活性。这项工作推进了我们对CNGB3在视锥光感受器中的生化和功能作用的理解。