Department of General Physiology, St. Petersburg State University, St. Petersburg 199034, Russia.
J Biol Chem. 2010 Sep 10;285(37):28614-26. doi: 10.1074/jbc.M110.150961. Epub 2010 Jul 1.
The nicotinic acetylcholine receptor (nAChR) and the Na,K-ATPase functionally interact in skeletal muscle (Krivoi, I. I., Drabkina, T. M., Kravtsova, V. V., Vasiliev, A. N., Eaton, M. J., Skatchkov, S. N., and Mandel, F. (2006) Pflugers Arch. 452, 756-765; Krivoi, I., Vasiliev, A., Kravtsova, V., Dobretsov, M., and Mandel, F. (2003) Ann. N.Y. Acad. Sci. 986, 639-641). In this interaction, the specific binding of nanomolar concentrations of nicotinic agonists to the nAChR stimulates electrogenic transport by the Na,K-ATPase alpha2 isozyme, causing membrane hyperpolarization. This study examines the molecular nature and membrane localization of this interaction. Stimulation of Na,K-ATPase activity by the nAChR does not require ion flow through open nAChRs. It can be induced by nAChR desensitization alone, in the absence of nicotinic agonist, and saturates when the nAChR is fully desensitized. It is enhanced by noncompetitive blockers of the nAChR (proadifen, QX-222), which promote non-conducting or desensitized states; and retarded by tetracaine, which stabilizes the resting nAChR conformation. The interaction operates at the neuromuscular junction as well as on extrajunctional sarcolemma. The Na,K-ATPase alpha2 isozyme is enriched at the postsynaptic neuromuscular junction and co-localizes with nAChRs. The nAChR and Na,K-ATPase alpha subunits specifically coimmunoprecipitate with each other, phospholemman, and caveolin-3. In a purified membrane preparation from Torpedo californica enriched in nAChRs and the Na,K-ATPase, a ouabain-induced conformational change of the Na,K-ATPase enhances a conformational transition of the nAChR to a desensitized state. These results suggest a mechanism by which the nAChR in a desensitized state with high apparent affinity for agonist interacts with the Na,K-ATPase to stimulate active transport. The interaction utilizes a membrane-delimited complex involving protein-protein interactions, either directly or through additional protein partners. This interaction is expected to enhance neuromuscular transmission and muscle excitation.
烟碱型乙酰胆碱受体 (nAChR) 和 Na,K-ATP 酶在骨骼肌中具有功能相互作用 (Krivoi, I. I., Drabkina, T. M., Kravtsova, V. V., Vasiliev, A. N., Eaton, M. J., Skatchkov, S. N., and Mandel, F. (2006) Pflugers Arch. 452, 756-765; Krivoi, I., Vasiliev, A., Kravtsova, V., Dobretsov, M., and Mandel, F. (2003) Ann. N.Y. Acad. Sci. 986, 639-641)。在此相互作用中,烟碱激动剂的纳摩尔浓度的特异性结合刺激 Na,K-ATP 酶 alpha2 同工酶的电致运动,导致膜超极化。本研究检查了这种相互作用的分子性质和膜定位。nAChR 对 Na,K-ATP 酶活性的刺激不需要通过开放的 nAChR 进行离子流动。它可以仅通过 nAChR 脱敏诱导,在没有烟碱激动剂的情况下,并且当 nAChR 完全脱敏时达到饱和。它被 nAChR 的非竞争性阻滞剂 (proadifen, QX-222) 增强,其促进非传导或脱敏状态; 并被稳定静息 nAChR 构象的四卡因延迟。该相互作用在神经肌肉接头以及在连接肌膜上起作用。Na,K-ATP 酶 alpha2 同工酶在突触后神经肌肉接头处富集,并与 nAChRs 共定位。nAChR 和 Na,K-ATP 酶 alpha 亚基与彼此、磷蛋白和 caveolin-3 特异性地共免疫沉淀。在从富含 nAChR 和 Na,K-ATP 酶的加利福尼亚扁尾魟纯化的膜制剂中,哇巴因诱导的 Na,K-ATP 酶构象变化增强 nAChR 向脱敏状态的构象转变。这些结果表明了一种机制,其中具有高亲和力的烟碱型乙酰胆碱受体处于脱敏状态,与 Na,K-ATP 酶相互作用以刺激主动转运。该相互作用利用涉及蛋白-蛋白相互作用的膜限定复合物,直接或通过其他蛋白伴侣进行。这种相互作用预计会增强神经肌肉传递和肌肉兴奋。