Department of Anatomy and Cell Biology, The Jared Grantham Kidney Institute, University of Kansas Medical Center, Kansas City, Kansas, USA.
Department of Pathology and Laboratory Medicine, The Jared Grantham Kidney Institute, University of Kansas Medical Center, Kansas City, Kansas, USA.
Kidney Int. 2022 Sep;102(3):577-591. doi: 10.1016/j.kint.2022.04.034. Epub 2022 May 27.
Primary cilia are sensory organelles built and maintained by intraflagellar transport (IFT) multiprotein complexes. Deletion of several IFT-B genes attenuates polycystic kidney disease (PKD) severity in juvenile and adult autosomal dominant polycystic kidney disease (ADPKD) mouse models. However, deletion of an IFT-A adaptor, Tulp3, attenuates PKD severity in adult mice only. These studies indicate that dysfunction of specific cilia components has potential therapeutic value. To broaden our understanding of cilia dysfunction and its therapeutic potential, we investigate the role of global deletion of an IFT-A gene, Ttc21b, in juvenile and adult mouse models of ADPKD. Both juvenile (postnatal day 21) and adult (six months of age) ADPKD mice exhibited kidney cysts, increased kidney weight/body weight ratios, lengthened kidney cilia, inflammation, and increased levels of the nutrient sensor, O-linked β-N-acetylglucosamine (O-GlcNAc). Deletion of Ttc21b in juvenile ADPKD mice reduced cortical collecting duct cystogenesis and kidney weight/body weight ratios, increased proximal tubular and glomerular dilations, but did not reduce cilia length, inflammation, nor O-GlcNAc levels. In contrast, Ttc21b deletion in adult ADPKD mice markedly attenuated kidney cystogenesis and reduced cilia length, inflammation, and O-GlcNAc levels. Thus, unlike IFT-B, the effect of Ttc21b deletion in mouse models of ADPKD is development-specific. Unlike an IFT-A adaptor, deleting Ttc21b in juvenile ADPKD mice is partially ameliorative. Thus, our studies suggest that different microenvironmental factors, found in distinct nephron segments and in developing versus mature stages, modify ciliary homeostasis and ADPKD pathobiology. Further, elevated levels of O-GlcNAc, which regulates cellular metabolism and ciliogenesis, may be a pathological feature of ADPKD.
原发性纤毛是由鞭毛内运输(IFT)多蛋白复合物构建和维持的感觉细胞器。几种 IFT-B 基因的缺失可减弱青少年和成年常染色体显性多囊肾病(ADPKD)小鼠模型的多囊肾病(PKD)严重程度。然而,IFT-A 接头蛋白 Tulp3 的缺失仅在成年小鼠中减轻 PKD 的严重程度。这些研究表明,特定纤毛成分的功能障碍具有潜在的治疗价值。为了扩大我们对纤毛功能障碍及其治疗潜力的理解,我们研究了 IFT-A 基因,Ttc21b 的全局缺失在青少年和成年 ADPKD 小鼠模型中的作用。在青少年(出生后第 21 天)和成年(六个月大)ADPKD 小鼠中均观察到肾脏囊肿、肾脏重量/体重比增加、肾脏纤毛延长、炎症和营养传感器 O-连接的β-N-乙酰氨基葡萄糖(O-GlcNAc)水平升高。在青少年 ADPKD 小鼠中,Ttc21b 的缺失减少了皮质集合管囊肿的形成和肾脏重量/体重比,增加了近端小管和肾小球的扩张,但并未减少纤毛长度、炎症或 O-GlcNAc 水平。相比之下,在成年 ADPKD 小鼠中,Ttc21b 的缺失明显减轻了肾脏囊肿的形成,并降低了纤毛长度、炎症和 O-GlcNAc 水平。因此,与 IFT-B 不同,Ttc21b 在 ADPKD 小鼠模型中的缺失的影响是发育特异性的。与 IFT-A 接头蛋白不同,在青少年 ADPKD 小鼠中缺失 Ttc21b 部分改善了病情。因此,我们的研究表明,不同的微环境因素,存在于不同的肾单位节段和发育与成熟阶段,会改变纤毛的内稳态和 ADPKD 的病理生物学。此外,细胞代谢和纤毛发生的调节物 O-GlcNAc 的水平升高可能是 ADPKD 的一个病理特征。