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Control of autophagy initiation by phosphoinositide 3‐phosphatase jumpy
Open accessAbstract
The majority of studies on autophagy, a cytoplasmic homeostasis pathway of broad biological and medical significance, have been hitherto focused on the phosphatidylinositol 3-kinases as the regulators of autophagy. Here, we addressed the reverse process driven by phosphoinositide phosphatases and uncovered a key negative regulatory role in autophagy of a phosphatidylinositol 3-phosphate (PI3P) phosphatase Jumpy (MTMR14). Jumpy associated with autophagic isolation membranes and early autophagosomes, defined by the key factor Atg16 necessary for proper localization and development of autophagic organelles. Jumpy orchestrated orderly succession of Atg factors by controlling recruitment to autophagic membranes of the sole mammalian Atg factor that interacts with PI3P, WIPI-1 (Atg18), and by affecting the distribution of Atg9 and LC3, the two Atg factors controlling organization and growth of autophagic membranes. A catalytically inactive Jumpy mutant, R336Q, found in congenital disease centronuclear myopathy, lost the ability to negatively regulate autophagy. This work reports for the first time that initiation of autophagy is controlled not only by the forward reaction of generating PI3P through a lipid kinase but that its levels are controlled by a specific PI3P phosphatase, which when defective can lead to human disease.
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“Furthermore, mounting evidence shows that autophagy is regulated by distinct mechanisms in different cell types [11–26], and these cell type-specific mechanisms underlie the differential vulnerability of separate tissues to autophagy mutations, resulting in heterogenous manifestations of disease.”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [20]
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“For instance, centronuclear myopathy is caused by mutations in the genes encoding MTM1 (myotubularin1) or MTMR14/Jumpy (myotubularin related protein 14) [17,20].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [20]
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“These loss-of-function mutations prevent these enzymes from metabolizing phosphoinositides required for autophagy, thereby disinhibiting autophagy flux and muscle atrophy [17,20].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [20]
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Metadata
- Authors
- Vergne, I., Roberts, E., Elmaoued, R. A., Tosch, V., Delgado, M. A., Proikas‐Cezanne, T., Laporte, J., & Deretic, V.
- Affiliations
- University of New Mexico (US)
- Centre National de la Recherche Scientifique (FR)
- University of Tübingen (DE)
- Corresponding author
- Vergne, Isabelle
- Deretic, Vojo
- Venue
- The EMBO Journal
- Published
- 2009-07-09
- Volume
- 28
- Issue
- 15
- Pages
- 2244-2258
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC2726690
- OpenAlex
- W2103545941
- Cited by
- 270
- References
- 55
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 8 · 2023: 7 · 2022: 5 · 2021: 12 · 2020: 6 · 2019: 12 · 2018: 11 · 2017: 13 · 2016: 23 · 2015: 22 · 2014: 25 · 2013: 22 · 2012: 29
- FWCI
- 20.69
- Type
- journal article
- Language
- en
- Update notices
- erratum (2009-09-10)
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 773)
- Agence Nationale de la Recherche
- Institut National de la Santé et de la Recherche Médicale
- Centre National de la Recherche Scientifique
- National Institutes of Health
- School of Medicine, University of New Mexico
- National Institute of Allergy and Infectious Diseases (R01AI042999, AI 45148, R01AI045148, R37AI042999)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- autophagy initiation, Atg16, Atg9, LC3, autophagosome formation, centronuclear myopathy, phosphatidylinositol 3-phosphate
- MeSH terms
- Animals, Autophagy, Cell Line, Humans, Molecular Sequence Data, Phosphoric Monoester Hydrolases, Sequence Analysis, DNA, Amino Acid Substitution, Mutation, Missense, Myopathies, Structural, Congenital, Mice
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