RUNDC1 inhibits autolysosome formation and survival of zebrafish via clasping ATG14-STX17-SNAP29 complex

Zhang, Rui, Yang, Yuyan, He, Chao, Zhang, Xin, Torraca, Vincenzo, Wang, Shen, Liu, Nan, Yang, Jiaren, Liu, Shicheng, Yuan, Jinglei, Gou, Dongzhi, Li, Shi, Dong, Xueying, Xie, Yufei, He, Junling, Bai, Hua, Hu, Mengyu, Liao, Zhiquan, Huang, Yuan, Lyu, Hao, Xiao, Shuai, Guo, Dong, Ali, Declan William, Michalak, M., Ma, C., Chen, X., Tang, J. and Zhou, C. 2023. RUNDC1 inhibits autolysosome formation and survival of zebrafish via clasping ATG14-STX17-SNAP29 complex. Cell Death and Differentiation. 30, p. 2231–2248. https://doi.org/10.1038/s41418-023-01215-z

TitleRUNDC1 inhibits autolysosome formation and survival of zebrafish via clasping ATG14-STX17-SNAP29 complex
TypeJournal article
AuthorsZhang, Rui, Yang, Yuyan, He, Chao, Zhang, Xin, Torraca, Vincenzo, Wang, Shen, Liu, Nan, Yang, Jiaren, Liu, Shicheng, Yuan, Jinglei, Gou, Dongzhi, Li, Shi, Dong, Xueying, Xie, Yufei, He, Junling, Bai, Hua, Hu, Mengyu, Liao, Zhiquan, Huang, Yuan, Lyu, Hao, Xiao, Shuai, Guo, Dong, Ali, Declan William, Michalak, M., Ma, C., Chen, X., Tang, J. and Zhou, C.
AbstractAutophagy serves as a pro-survival mechanism for a cell or a whole organism to cope with nutrient stress. Our understanding of the molecular regulation of this fusion event remains incomplete. Here, we identified RUNDC1 as a novel ATG14-interacting protein, which is highly conserved across vertebrates, including zebrafish and humans. By gain and loss of function studies, we demonstrate that RUNDC1 negatively modulates autophagy by blocking fusion between autophagosomes and lysosomes via inhibiting the assembly of the STX17-SNAP29-VAMP8 complex both in human cells and the zebrafish model. Moreover, RUNDC1 clasps the ATG14-STX17-SNAP29 complex via stimulating ATG14 homo-oligomerization to inhibit ATG14 dissociation. This also prevents VAMP8 from binding to STX17-SNAP29. We further identified that phosphorylation of RUNDC1 Ser is crucial to inhibit the assembly of the STX17-SNAP29-VAMP8 complex via promoting ATG14 homo-oligomerization. In line with our findings, RunDC1 is crucial for zebrafish in their response to nutrient-deficient conditions. Taken together, our findings demonstrate that RUNDC1 is a negative regulator of autophagy that restricts autophagosome fusion with lysosomes by clasping the ATG14-STX17-SNAP29 complex to hinder VAMP8 binding. [Abstract copyright: © 2023. The Author(s), under exclusive licence to ADMC Associazione Differenziamento e Morte Cellulare.]
JournalCell Death and Differentiation
Journal citation30, p. 2231–2248
ISSN1476-5403
Year2023
PublisherNature Publishing Group
Digital Object Identifier (DOI)https://doi.org/10.1038/s41418-023-01215-z
PubMed ID37684417
Publication dates
Published online08 Sep 2023
Project51808392
FunderNational Natural Science Foundation of China (National Science Foundation of China)
Page range10.1038/s41418-023-01215-z

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