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Exocytosis and endocytosis are tightly coupled. In addition to initiating exocytosis, Ca2+ plays critical roles in exocytosisendocytosis coupling in neurons and nonneuronal cells. Both positive and negative roles of Ca2+ in endocytosis have been reported; however, Ca2+ inhibition in endocytosis remains debatable with unknown mechanisms. Here, we show that synaptotagmin-1 (Syt1), the primary Ca2+ sensor initiating exocytosis, plays bidirectional and opposite roles in exocytosisendocytosis coupling by promoting slow, small-sized clathrin-mediated endocytosis but inhibiting fast, large-sized bulk endocytosis. Ca2+-binding ability is required for Syt1 to regulate both types of endocytic pathways, the disruption of which leads to inefficient vesicle recycling under mild stimulation and excessive membrane retrieval following intense stimulation. Ca2+-dependent membrane tubulation may explain the opposite endocytic roles of Syt1 and provides a general membrane-remodeling working model for endocytosis determination. Thus, Syt1 is a primary bidirectional Ca2+ sensor facilitating clathrin-mediated endocytosis but clamping bulk endocytosis, probably by manipulating membrane curvature to ensure both efficient and precise coupling of endocytosis to exocytosis.

Citation

Yang Chen, Shaoqin Hu, Xuanang Wu, Zhenli Xie, Yuan Wang, Bianbian Wang, Xiaopeng Li, Yingmei Pei, Yuhao Gu, Kai Huang, Jingxiao Huo, Anqi Wei, Cheng Bi, Zhe Lu, Qian Song, Huadong Xu, Xinjiang Kang, Shuli Shao, Jiangang Long, Jiankang Liu, Zhuan Zhou, Rong Huang, Zuying Chai, Changhe Wang. Synaptotagmin-1 is a bidirectional Ca2+ sensor for neuronal endocytosis. Proceedings of the National Academy of Sciences of the United States of America. 2022 May 17;119(20):e2111051119

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PMID: 35537054

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