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Animal secretory endolysosome channel discovery

Yun Zhang Qi-Quan Wang Zhong Zhao Cheng-Jie Deng

Yun Zhang, Qi-Quan Wang, Zhong Zhao, Cheng-Jie Deng. Animal secretory endolysosome channel discovery. Zoological Research, 2021, 42(2): 141-152. doi: 10.24272/j.issn.2095-8137.2020.358
Citation: Yun Zhang, Qi-Quan Wang, Zhong Zhao, Cheng-Jie Deng. Animal secretory endolysosome channel discovery. Zoological Research, 2021, 42(2): 141-152. doi: 10.24272/j.issn.2095-8137.2020.358


doi: 10.24272/j.issn.2095-8137.2020.358

Animal secretory endolysosome channel discovery

Funds: This work was supported by the National Natural Science Foundation of China (31572268, U1602225, 31872226) and Yunling Scholar Program to Y.Z.
More Information
  • 摘要: 分泌型孔道形成蛋白(pore-forming proteins, PFPs)广泛分布于自然界的各种生物物种中。我们以两栖动物大蹼铃蟾(Bombina maxima)为模型开展的研究发现:细菌孔道形成毒素家族(aerolysin family)蛋白(af-PFPs)和三叶因子(trefoil factors, TFFs)在大蹼铃蟾中广泛分布,而且它们之间存在相互作用网络。首先,大蹼铃蟾af-PFP蛋白BmALP1可被其同源蛋白BmALP3进行氧浓度依赖的负调控,造成 BmALP1蛋白可在其活性(单体)和非活性形式(同源二聚体或多聚体)之间进行可逆性的转变。其次,活性形式的BmALP1可与BmTFF3相互作用以形成具有细胞活性的复合物βγ-CAT。该孔道形成蛋白复合物的特性在于通过受体介导的内吞(endocytosis)进入细胞并在内吞溶酶体上(endolysosomes)形成物质通道调控内吞溶酶体的生化特性,包括刺激和参与细胞巨胞饮(macropinocytosis)的作用。βγ-CAT复合物还同时具有诱导和调节细胞胞吐(exocytosis)的作用。取决于细胞类型和状态以及细胞外环境,βγ-CAT的细胞作用和效应可促进大蹼铃蟾的物质(例如水、营养成分、代谢物和外来抗原等)吸收和囊泡化运输以及胞内物质交换与外排,同时维持粘膜屏障和免疫防御的功能。基于已有的实验证据,我们提出了分泌型内吞溶酶体通道(secretory endolysosome channel, SELC)的创新性慨念并提出了SELC细胞通路的特征框架,两栖动物大蹼铃蟾βγ-CAT是第一个被实验验证了的SELC蛋白实例。鉴于新发现的SELC蛋白以及相应细胞作用通路在细胞与环境相互作用和环境适应中发挥的基础作用,它们在生物体,特别是脊椎动物物种中,应该具有进化上的保守性。
    #Authors contributed equally to this work
  • Figure  1.  Proposed SELC pathway based on βγ-CAT evidence

    There are four main steps in the proposed SELC pathway. Related elements of βγ-CAT pathway are bracketed. (1) In extracellular surroundings, a SELC PFP can be reversibly converted between inactive or active forms by specific negative or positive regulators in response to variations in environmental conditions (like oxygen tension, water balance, pH, nutrients, metabolites, pathogens). Active form of SELC PFP may or may not be necessary to interact with a cofactor to form a cellular active complex. βγ-CAT is the former case. (2) Active PFP or the complex binds membrane receptor(s) and stimulates endocytosis, especially macropinocytosis. (3) PFP then oligomerizes and forms channels on endolysosomes to facilitate material exchange. (4) Actions result in distinct biological outcomes depending on cell contexts and environment, see text.

    Figure  2.  SELC proteins manipulate endocytosis and exocytosis

    Depending on distinct cell contexts and environments, cellular action of SELC proteins is well adapted for material uptake and exchange as well as vesicular transport either within a cell or across cells. (1) Macropinocytosis induced by SELC protein results in uptake of external material, including water and solutes (nutrients or antigens). Solutes may be processed and/or hydrolyzed in endolysosomes, and channels formed by SELC protein can mediate the release of resulting products from vesicles to cytoplasm. (2) Channels formed by SELC protein on endolysosomes can mediate material exchange, which results in biochemical property modulation of vesicles (e.g., pH and/or content), leading to specific cellular responses. (3) Furthermore, exocytosis can be induced and modulated in the presence of a SELC protein, which plays a role in transcytosis of cell surrounding materials (like lipids with a carrier), secretion of intracellular materials, and waste expulsion. (4) SELC proteins may participate in the recycling and re-distribution of membrane components, like functional proteins and lipid components.

    Figure  3.  Proposed direct action of SELC PFP on EVs

    EVs comprised of exosomes and microvesicles circulate in biological fluids. They bear cargo molecules, like proteins and metabolites. Membrane active secretory PFPs, like SELC protein βγ-CAT, can be tightly regulated by specific regulators relying on distinct micro-environmental conditions (Figure 1). Subsequent oligomerization and channel formation of PFPs in EVs may lead to release of EV cargo molecules in a temporal and spatial manner to fit specific cellular and biological requirements in situ. Alternatively, channels formed by PFP can also be used to take up specific substances in the surrounding environment, and cells can obtain these substances by fusing with vesicles containing PFP channels, functioning as an alternative way for cells to acquire extracellular material.

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  • 收稿日期:  2020-12-09
  • 录用日期:  2021-01-29
  • 网络出版日期:  2021-02-01
  • 刊出日期:  2021-03-18