From the Department of Anatomy, Charité-Universitätsmedizin Berlin, 10115 Berlin.
J Biol Chem. 2014 Apr 4;289(14):9983-97. doi: 10.1074/jbc.M113.540948. Epub 2014 Feb 13.
The furosemide-sensitive Na(+)-K(+)-2Cl(-) cotransporter (NKCC2) is responsible for urine concentration and helps maintain systemic salt homeostasis. Its activity depends on trafficking to, and insertion into, the apical membrane, as well as on phosphorylation of conserved N-terminal serine and threonine residues. Vasopressin (AVP) signaling via PKA and other kinases activates NKCC2. Association of NKCC2 with lipid rafts facilitates its AVP-induced apical translocation and activation at the surface. Lipid raft microdomains typically serve as platforms for membrane proteins to facilitate their interactions with other proteins, but little is known about partners that interact with NKCC2. Yeast two-hybrid screening identified an interaction between NKCC2 and the cytosolic protein, annexin A2 (AnxA2). Annexins mediate lipid raft-dependent trafficking of transmembrane proteins, including the AVP-regulated water channel, aquaporin 2. Here, we demonstrate that AnxA2, which binds to phospholipids in a Ca(2+)-dependent manner and may organize microdomains, is codistributed with NKCC2 to promote its apical translocation in response to AVP stimulation and low chloride hypotonic stress. NKCC2 and AnxA2 interact in a phosphorylation-dependent manner. Phosphomimetic AnxA2 carrying a mutant phosphoacceptor (AnxA2-Y24D-GFP) enhanced surface expression and raft association of NKCC2 by 5-fold upon low chloride hypotonic stimulation, whereas AnxA2-Y24A-GFP and PKC-dependent AnxA2-S26D-GFP did not. As the AnxA2 effect involved only nonphosphorylated NKCC2, it appears to affect NKCC2 trafficking. Overexpression or knockdown experiments further supported the role of AnxA2 in the apical translocation and surface expression of NKCC2. In summary, this study identifies AnxA2 as a lipid raft-associated trafficking factor for NKCC2 and provides mechanistic insight into the regulation of this essential cotransporter.
速尿敏感的钠钾 2 氯共转运体(NKCC2)负责尿液浓缩,并有助于维持全身盐平衡。其活性取决于向顶端膜的运输和插入,以及保守的 N 端丝氨酸和苏氨酸残基的磷酸化。血管加压素(AVP)通过 PKA 和其他激酶的信号转导激活 NKCC2。NKCC2 与脂筏的关联促进了 AVP 诱导的顶端转位和激活。脂筏微区通常作为膜蛋白相互作用的平台,促进它们与其他蛋白质的相互作用,但关于与 NKCC2 相互作用的伙伴知之甚少。酵母双杂交筛选鉴定出 NKCC2 与细胞质蛋白 annexin A2(AnxA2)之间的相互作用。膜联蛋白介导包括 AVP 调节的水通道 aquaporin 2 在内的跨膜蛋白的脂筏依赖性转运。在这里,我们证明了以 Ca2+依赖性方式结合磷脂并可能组织微区的 AnxA2 与 NKCC2 共定位,以促进其在 AVP 刺激和低氯低渗应激下的顶端转位。NKCC2 和 AnxA2 以磷酸化依赖的方式相互作用。携带突变磷酸受体(AnxA2-Y24D-GFP)的磷酸模拟 AnxA2 在低氯低渗刺激下使 NKCC2 的表面表达和筏关联增加了 5 倍,而 AnxA2-Y24A-GFP 和 PKC 依赖性 AnxA2-S26D-GFP 则没有。由于 AnxA2 的作用仅涉及非磷酸化的 NKCC2,因此它似乎影响 NKCC2 的运输。过表达或敲低实验进一步支持了 AnxA2 在 NKCC2 顶端转位和表面表达中的作用。总之,这项研究将 AnxA2 鉴定为 NKCC2 的脂筏相关转运因子,并为这种重要的共转运体的调节提供了机制上的见解。