The AAA-ATPase Yta4/ATAD1 interacts with the mitochondrial divisome to inhibit mitochondrial fission

被引:7
|
作者
He, Jiajia [1 ,2 ,3 ,4 ]
Liu, Ke [1 ,2 ,3 ,4 ]
Wu, Yifan [1 ,2 ]
Zhao, Chenhui [1 ,2 ]
Yan, Shuaijie [1 ,2 ]
Chen, Jia-Hui [1 ,2 ,5 ]
Hu, Lizhu [2 ,6 ]
Wang, Dongmei [1 ,2 ]
Zheng, Fan [1 ,2 ]
Wei, Wenfan [1 ,2 ]
Xu, Chao [1 ,2 ,3 ,4 ]
Huang, Chengdong [1 ,2 ,3 ,4 ]
Liu, Xing [1 ,2 ,3 ,4 ]
Yao, Xuebiao [1 ,2 ,3 ,4 ]
Ding, Lijun [7 ]
Fang, Zhiyou [6 ]
Tang, Ai-Hui [1 ,2 ,5 ]
Fu, Chuanhai [1 ,2 ,3 ,4 ]
机构
[1] Univ Sci & Technol China, MOE Key Lab Cellular Dynam, Hefei, Peoples R China
[2] Univ Sci & Technol China, Ctr Adv Interdisciplinary Sci & Biomed IHM, Div Life Sci & Med, Hefei, Peoples R China
[3] Univ Sci & Technol China, Sch Life Sci, Anhui Key Lab Cellular Dynam & Chem Biol, Hefei, Peoples R China
[4] Univ Sci & Technol China, Hefei Natl Res Ctr Interdisciplinary Sci Microscal, Sch Life Sci, Hefei, Peoples R China
[5] Hefei Comprehens Natl Sci Ctr, Inst Artificial Intelligence, Hefei, Peoples R China
[6] Chinese Acad Sci, Inst Hlth & Med Technol, Hefei Inst Phys Sci, Anhui Prov Key Lab Med Phys & Technol, Hefei, Peoples R China
[7] Nanjing Univ, Affiliated Drum Tower Hosp, Ctr Reprod Med, Dept Obstet & Gynecol,Med Sch, Nanjing, Peoples R China
基金
中国国家自然科学基金;
关键词
PROTEIN; YEAST; FIS1P; DNM1P; MSP1;
D O I
10.1371/journal.pbio.3002247
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Mitochondria are in a constant balance of fusion and fission. Excessive fission or deficient fusion leads to mitochondrial fragmentation, causing mitochondrial dysfunction and physiological disorders. How the cell prevents excessive fission of mitochondria is not well understood. Here, we report that the fission yeast AAA-ATPase Yta4, which is the homolog of budding yeast Msp1 responsible for clearing mistargeted tail-anchored (TA) proteins on mitochondria, plays a critical role in preventing excessive mitochondrial fission. The absence of Yta4 leads to mild mitochondrial fragmentation in a Dnm1-dependent manner but severe mitochondrial fragmentation upon induction of mitochondrial depolarization. Overexpression of Yta4 delocalizes the receptor proteins of Dnm1, i.e., Fis1 (a TA protein) and Mdv1 (the bridging protein between Fis1 and Dnm1), from mitochondria and reduces the localization of Dnm1 to mitochondria. The effect of Yta4 overexpression on Fis1 and Mdv1, but not Dnm1, depends on the ATPase and translocase activities of Yta4. Moreover, Yta4 interacts with Dnm1, Mdv1, and Fis1. In addition, Yta4 competes with Dnm1 for binding Mdv1 and decreases the affinity of Dnm1 for GTP and inhibits Dnm1 assembly in vitro. These findings suggest a model, in which Yta4 inhibits mitochondrial fission by inhibiting the function of the mitochondrial divisome composed of Fis1, Mdv1, and Dnm1. Therefore, the present work reveals an uncharacterized molecular mechanism underlying the inhibition of mitochondrial fission.
引用
收藏
页数:34
相关论文
共 6 条
  • [1] Collateral deletion of the mitochondrial AAA plus ATPase ATAD1 sensitizes cancer cells to proteasome dysfunction
    Winter, Jacob M.
    Fresenius, Heidi L.
    Cunningham, Corey N.
    Wei, Peng
    Keys, Heather R.
    Berg, Jordan
    Bott, Alex
    Yadav, Tarun
    Ryan, Jeremy
    Sirohi, Deepika
    Tripp, Sheryl R.
    Barta, Paige
    Agarwal, Neeraj
    Letai, Anthony
    Sabatini, David M.
    Wohlever, Matthew L.
    Rutter, Jared
    ELIFE, 2022, 11
  • [2] The AAA-ATPase ATAD1 and its partners promote degradation of desmin intermediate filaments in muscle
    Aweida, Dina
    Cohen, Shenhav
    EMBO REPORTS, 2022, 23 (12)
  • [3] Characterization of the mitochondrial protein LETM1, which maintains the mitochondrial tubular shapes and interacts with the AAA-ATPase BCS1L
    Tamai, Shoko
    Iida, Hiroshi
    Yokota, Sadaki
    Sayano, Tomoko
    Kiguchiya, Shoko
    Ishihara, Naotada
    Hayashi, Jun-Ichi
    Mihara, Katsuyoshi
    Oka, Toshihiko
    JOURNAL OF CELL SCIENCE, 2008, 121 (15) : 2588 - 2600
  • [4] Proofreading of protein localization mediated by a mitochondrial AAA-ATPase Msp1
    Matsumoto, Shunsuke
    Endo, Toshiya
    JOURNAL OF BIOCHEMISTRY, 2023, 173 (04): : 265 - 271
  • [5] Mitochondrial nucleoid trafficking regulated by the inner-membrane AAA-ATPase ATAD3A modulates respiratory complex formation
    Ishihara, Takaya
    Ban-Ishihara, Reiko
    Ota, Azusa
    Ishihara, Naotada
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2022, 119 (47)
  • [6] Mitochondrial AAA-ATPase Msp1 detects mislocalized tail-anchored proteins through a dual-recognition mechanism
    Li, Lanlan
    Zheng, Jing
    Wu, Xi
    Jiang, Hui
    EMBO REPORTS, 2019, 20 (04)