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

PLoS Biol. 2023 Aug 17;21(8):e3002247. doi: 10.1371/journal.pbio.3002247. eCollection 2023 Aug.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATPases Associated with Diverse Cellular Activities / genetics
  • Adenosine Triphosphatases
  • Frontotemporal Dementia*
  • Humans
  • Mitochondria
  • Mitochondrial Dynamics
  • Schizosaccharomyces* / genetics

Substances

  • ATPases Associated with Diverse Cellular Activities
  • Adenosine Triphosphatases

Grants and funding

This work is supported by grants from the National Key Research and Development Program of China (https://service.most.gov.cn/) (2022YFA1303100 to X.Y.), the National Natural Science Foundation of China (https://www.nsfc.gov.cn/) (91754106, 32070707, and 31621002 to C.F. and 31872759 to A.T.), the Center for Advanced Interdisciplinary Science and Biomedicine of IHM (QYPY20220003 to C.F.), and the Fundamental Research Funds from University of Science and Technology of China (WK9110000141 to A.T.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.