Cited by 232Autophagy in Disease and TherapyMitochondrial Function and PathologyParkinson's Disease Mechanisms and Treatments

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The ADP/ATP translocase drives mitophagy independent of nucleotide exchange

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Hoshino, Atsushi, Wang, Wei-jia, Wada, Shogo, McDermott-Roe, Chris, Evans, Chantell S., Gosis, Bridget, Morley, Michael P., Rathi, Komal S., Li, Jian, Li, Kristina, Yang, Steven, McManus, Meagan J., Bowman, Caitlyn, Potluri, Prasanth, Levin, Michael, Damrauer, Scott, Wallace, Douglas C., Holzbaur, Erika L. F., Arany, Zoltan·2019·Nature

DOI 10.1038/s41586-019-1667-4PMC PMC6858570

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Abstract

Mitochondrial homeostasis depends on mitophagy, the programmed degradation of mitochondria. Only a few proteins are known to participate in mitophagy. Here we develop a multidimensional CRISPR-Cas9 genetic screen, using multiple mitophagy reporter systems and pro-mitophagy triggers, and identify numerous components of parkin-dependent mitophagy 1. Unexpectedly, we find that the adenine nucleotide translocator (ANT) complex is required for mitophagy in several cell types. Whereas pharmacological inhibition of ANT-mediated ADP/ATP exchange promotes mitophagy, genetic ablation of ANT paradoxically suppresses mitophagy. Notably, ANT promotes mitophagy independently of its nucleotide translocase catalytic activity. Instead, the ANT complex is required for inhibition of the presequence translocase TIM23, which leads to stabilization of PINK1, in response to bioenergetic collapse. ANT modulates TIM23 indirectly via interaction with TIM44, which regulates peptide import through TIM23 2. Mice that lack ANT1 show blunted mitophagy and consequent profound accumulation of aberrant mitochondria. Disease-causing human mutations in ANT1 abrogate binding to TIM44 and TIM23 and inhibit mitophagy. Together, our findings show that ANT is an essential and fundamental mediator of mitophagy in health and disease.

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STAR: ultrafast universal RNA-seq aligner
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Additional file 13 of Down-regulation of BCL2L13 renders poor prognosis in clear cell and papillary renal cell carcinoma
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Additional file 14 of Down-regulation of BCL2L13 renders poor prognosis in clear cell and papillary renal cell carcinoma
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Additional file 11 of Down-regulation of BCL2L13 renders poor prognosis in clear cell and papillary renal cell carcinoma
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Additional file 12 of Down-regulation of BCL2L13 renders poor prognosis in clear cell and papillary renal cell carcinoma
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Mitochondria mitophagy and autophagy
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Authors: Hoshino, A., Wang, W.-J., Wada, S., McDermott-Roe, C., Evans, C. S., Gosis, B., Morley, M. P., Rathi, K. S., Li, J., Li, K., Yang, S., McManus, M. J., Bowman, C., Potluri, P., Levin, M., Damrauer, S., Wallace, D. C., Holzbaur, E. L. F., & Arany, Z.
Affiliations: Kyoto Prefectural University of Medicine (JP)
University of Pennsylvania (US)
Children's Hospital of Philadelphia (US)
Corresponding author: Arany, Zoltan
ORCID: Hoshino, Atsushi
Wada, Shogo
Evans, Chantell S.
Gosis, Bridget
Morley, Michael P.
Rathi, Komal S.
Li, Kristina
Yang, Steven
McManus, Meagan J.
Bowman, Caitlyn
Potluri, Prasanth
Levin, Michael
Damrauer, Scott
Wallace, Douglas C.
Holzbaur, Erika L. F.
Arany, Zoltan
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2019-10-16
Volume: 575
Issue: 7782
Pages: 375-379
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1667-4
PMC: PMC6858570
OpenAlex: W2980489405
Cited by: 228
References: 44
Citations by year: 2026: 16 · 2025: 30 · 2024: 39 · 2023: 27 · 2022: 44 · 2021: 43 · 2020: 29
FWCI: 22.84
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health (R01OD010944)
Japan Society for the Promotion of Science (19H03658)
National Heart, Lung, and Blood Institute (R01HL094499, R01HL126797, T32HL007843)
National Institute of Mental Health (R01MH110185, R01MH108592)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK107667, R01DK114103)
National Institute of Neurological Disorders and Stroke (R37NS060698, R01NS021328)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Keywords: mitophagy, adenine nucleotide translocase, ANT1, Tim23, Tim44, mitochondrial homeostasis, nucleotide exchange
MeSH terms: Mitochondrial Precursor Protein Import Complex Proteins, PTEN-Induced Putative Kinase, Animals, Cell Line, Nucleotides, Protein Binding, Protein Kinases, Mitochondrial Membrane Transport Proteins, Mice, Mitophagy

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The ADP/ATP translocase drives mitophagy independent of nucleotide exchange

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