Okochi Yoshifumi, Jinno Yuka, Okamura Yasushi
Integrative Physiology, Graduate School of Medicine, Osaka University, Suita, Japan.
Integrative Physiology, Graduate School of Medicine, Osaka University, Suita, Japan.
Biophys J. 2024 Dec 17;123(24):4221-4232. doi: 10.1016/j.bpj.2024.07.034. Epub 2024 Jul 31.
Multimerization of ion channels is essential for establishing the ion-selective pathway and tuning the gating regulated by membrane potential, second messengers, and temperature. Voltage-gated proton channel, Hv1, consists of voltage-sensor domain and coiled-coil domain. Hv1 forms dimer, whereas voltage-dependent channel activity is self-contained in monomer unlike many ion channels, which assemble to form ion-conductive pathways among multiple subunits. Dimerization of Hv1 is necessary for cooperative gating, but other roles of dimerization in physiological aspects are still largely unclear. In this study, we show that dimerization of Hv1 takes place in ER. Sea urchin Hv1 (Strongylocentrotus purpuratus Hv1: SpHv1) was glycosylated in the consensus sequence for N-linked glycosylation within the S1-S2 extracellular loop. However, glycosylation was not observed in the monomeric SpHv1 that lacks the coiled-coil domain. A version of mHv1 in which the S1-S2 loop was replaced by that of SpHv1 showed glycosylation and its monomeric form was not glycosylated. Tandem dimer of monomeric SpHv1 underwent glycosylation, suggesting that dimerization of Hv1 is required for glycosylation. Moreover, when monomeric Hv1 has a dilysine motif in the C-terminal end, which is known to act as a retrieval signal from Golgi to ER, prolonging the time of residency in ER, it was glycosylated. Overall, our results suggest that monomeric SpHv1 does not stay long in ER, thereby escaping glycosylation, while the dimerization causes the proteins to stay longer in ER. Thus, the findings highlight the novel significance of dimerization of Hv1: regulation of biogenesis and maturation of the proteins in intracellular compartments.
离子通道的多聚化对于建立离子选择性通道以及调节由膜电位、第二信使和温度控制的门控至关重要。电压门控质子通道Hv1由电压感受器结构域和卷曲螺旋结构域组成。Hv1形成二聚体,而与许多组装形成多个亚基间离子传导途径的离子通道不同,其电压依赖性通道活性在单体中是独立存在的。Hv1的二聚化对于协同门控是必要的,但二聚化在生理方面的其他作用仍 largely不清楚。在本研究中,我们表明Hv1的二聚化发生在内质网(ER)中。海胆Hv1(紫海胆Hv1:SpHv1)在S1 - S2细胞外环内的N - 连接糖基化共有序列中发生了糖基化。然而,在缺乏卷曲螺旋结构域的单体SpHv1中未观察到糖基化。一种将mHv1的S1 - S2环替换为SpHv1的S1 - S2环的变体显示出糖基化,且其单体形式未被糖基化。单体SpHv1的串联二聚体发生了糖基化,表明Hv1的二聚化是糖基化所必需的。此外,当单体Hv1在C末端具有双赖氨酸基序时,已知该基序作为从高尔基体到内质网的回收信号,延长在内质网中的驻留时间,它就会被糖基化。总体而言,我们的结果表明单体SpHv1在内质网中停留时间不长,从而逃避了糖基化,而二聚化导致蛋白质在内质网中停留更长时间。因此,这些发现突出了Hv1二聚化的新意义:调节细胞内区室中蛋白质的生物合成和成熟。