Klar Joakim, Piontek Jörg, Milatz Susanne, Tariq Muhammad, Jameel Muhammad, Breiderhoff Tilman, Schuster Jens, Fatima Ambrin, Asif Maria, Sher Muhammad, Mäbert Katrin, Fromm Anja, Baig Shahid M, Günzel Dorothee, Dahl Niklas
Department of Immunology, Genetics and Pathology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
Institute of Clinical Physiology, Charité-Universitätsmedizin Berlin, Charité, Berlin, Germany.
PLoS Genet. 2017 Jul 7;13(7):e1006897. doi: 10.1371/journal.pgen.1006897. eCollection 2017 Jul.
Claudins constitute the major component of tight junctions and regulate paracellular permeability of epithelia. Claudin-10 occurs in two major isoforms that form paracellular channels with ion selectivity. We report on two families segregating an autosomal recessive disorder characterized by generalized anhidrosis, severe heat intolerance and mild kidney failure. All affected individuals carry a rare homozygous missense mutation c.144C>G, p.(N48K) specific for the claudin-10b isoform. Immunostaining of sweat glands from patients suggested that the disease is associated with reduced levels of claudin-10b in the plasma membranes and in canaliculi of the secretory portion. Expression of claudin-10b N48K in a 3D cell model of sweat secretion indicated perturbed paracellular Na+ transport. Analysis of paracellular permeability revealed that claudin-10b N48K maintained cation over anion selectivity but with a reduced general ion conductance. Furthermore, freeze fracture electron microscopy showed that claudin-10b N48K was associated with impaired tight junction strand formation and altered cis-oligomer formation. These data suggest that claudin-10b N48K causes anhidrosis and our findings are consistent with a combined effect from perturbed TJ function and increased degradation of claudin-10b N48K in the sweat glands. Furthermore, affected individuals present with Mg2+ retention, secondary hyperparathyroidism and mild kidney failure that suggest a disturbed reabsorption of cations in the kidneys. These renal-derived features recapitulate several phenotypic aspects detected in mice with kidney specific loss of both claudin-10 isoforms. Our study adds to the spectrum of phenotypes caused by tight junction proteins and demonstrates a pivotal role for claudin-10b in maintaining paracellular Na+ permeability for sweat production and kidney function.
闭合蛋白是紧密连接的主要组成部分,可调节上皮细胞的细胞旁通透性。闭合蛋白-10有两种主要的异构体,它们形成具有离子选择性的细胞旁通道。我们报告了两个家系,其中分离出一种常染色体隐性疾病,其特征为全身性无汗、严重不耐热和轻度肾衰竭。所有受影响的个体都携带一种罕见的纯合错义突变c.144C>G,p.(N48K),该突变是闭合蛋白-10b异构体特有的。对患者汗腺的免疫染色表明,该疾病与分泌部质膜和小管中闭合蛋白-10b水平降低有关。在汗液分泌的三维细胞模型中表达闭合蛋白-10b N48K表明细胞旁Na+转运受到干扰。对细胞旁通透性的分析表明,闭合蛋白-10b N48K保持阳离子对阴离子的选择性,但总体离子电导率降低。此外,冷冻蚀刻电子显微镜显示,闭合蛋白-10b N48K与紧密连接链形成受损和顺式寡聚体形成改变有关。这些数据表明,闭合蛋白-10b N48K导致无汗,我们的发现与紧密连接功能紊乱和汗腺中闭合蛋白-10b N48K降解增加的综合作用一致。此外,受影响的个体出现Mg2+潴留、继发性甲状旁腺功能亢进和轻度肾衰竭,这表明肾脏中阳离子重吸收受到干扰。这些源自肾脏的特征概括了在两种闭合蛋白-10异构体均在肾脏中特异性缺失的小鼠中检测到的几个表型方面。我们的研究增加了由紧密连接蛋白引起的表型谱,并证明了闭合蛋白-10b在维持细胞旁Na+通透性以产生汗液和维持肾功能方面的关键作用。