FBXL4 suppresses mitophagy by restricting the accumulation of NIX and BNIP3 mitophagy receptors.

TitleFBXL4 suppresses mitophagy by restricting the accumulation of NIX and BNIP3 mitophagy receptors.
Publication TypeJournal Article
Year of Publication2023
AuthorsNguyen-Dien GThanh, Kozul K-L, Cui Y, Townsend B, Kulkarni PGosavi, Ooi SSiang, Marzio A, Carrodus N, Zuryn S, Pagano M, Parton RG, Lazarou M, S Millard S, Taylor RW, Collins BM, Jones MJk, Pagan JK
JournalEMBO J
Volume42
Issue13
Paginatione112767
Date Published2023 Jul 03
ISSN1460-2075
KeywordsAnimals, Autophagy, DNA, Mitochondrial, Humans, Mice, Mitochondria, Mitochondrial Proteins, Mitophagy, Phagocytosis
Abstract

To maintain both mitochondrial quality and quantity, cells selectively remove damaged or excessive mitochondria through mitophagy, which is a specialised form of autophagy. Mitophagy is induced in response to diverse conditions, including hypoxia, cellular differentiation and mitochondrial damage. However, the mechanisms that govern the removal of specific dysfunctional mitochondria under steady-state conditions to fine-tune mitochondrial content are not well understood. Here, we report that SCFFBXL4 , an SKP1/CUL1/F-box protein ubiquitin ligase complex, localises to the mitochondrial outer membrane in unstressed cells and mediates the constitutive ubiquitylation and degradation of the mitophagy receptors NIX and BNIP3 to suppress basal levels of mitophagy. We demonstrate that the pathogenic variants of FBXL4 that cause encephalopathic mtDNA depletion syndrome (MTDPS13) do not efficiently interact with the core SCF ubiquitin ligase machinery or mediate the degradation of NIX and BNIP3. Thus, we reveal a molecular mechanism whereby FBXL4 actively suppresses mitophagy by preventing NIX and BNIP3 accumulation. We propose that the dysregulation of NIX and BNIP3 turnover causes excessive basal mitophagy in FBXL4-associated mtDNA depletion syndrome.

DOI10.15252/embj.2022112767
Alternate JournalEMBO J
PubMed ID37161784
PubMed Central IDPMC10308361
Grant ListT32 CA009161 / CA / NCI NIH HHS / United States
/ DH_ / Department of Health / United Kingdom
MR/W019027/1 / MRC_ / Medical Research Council / United Kingdom
MR/S005021/1 / MRC_ / Medical Research Council / United Kingdom
203105/Z/16/Z / WT_ / Wellcome Trust / United Kingdom
R35 GM136250 / GM / NIGMS NIH HHS / United States
T32CA009161 / CA / NCI NIH HHS / United States
/ WT_ / Wellcome Trust / United Kingdom
Related Faculty: 
Antonio Marzio, Ph.D.

Pathology & Laboratory Medicine 1300 York Avenue New York, NY 10065 Phone: (212) 746-6464
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