Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo
Cells rely on autophagy to clear misfolded proteins and damaged organelles to maintain cellular homeostasis. In this study we use the new autophagy inhibitor PIK-III to screen for autophagy substrates. PIK-III is a selective inhibitor of VPS34 that binds a unique hydrophobic pocket not present in re...
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Published in | Nature cell biology Vol. 16; no. 11; pp. 1069 - 1079 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.11.2014
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Abstract | Cells rely on autophagy to clear misfolded proteins and damaged organelles to maintain cellular homeostasis. In this study we use the new autophagy inhibitor PIK-III to screen for autophagy substrates. PIK-III is a selective inhibitor of VPS34 that binds a unique hydrophobic pocket not present in related kinases such as PI(3)Kα. PIK-III acutely inhibits autophagy and
de novo
lipidation of LC3, and leads to the stabilization of autophagy substrates. By performing ubiquitin-affinity proteomics on PIK-III-treated cells we identified substrates including NCOA4, which accumulates in
ATG7
-deficient cells and co-localizes with autolysosomes. NCOA4 directly binds ferritin heavy chain-1 (FTH1) to target the iron-binding ferritin complex with a relative molecular mass of 450,000 to autolysosomes following starvation or iron depletion. Interestingly,
Ncoa4
−/−
mice exhibit a profound accumulation of iron in splenic macrophages, which are critical for the reutilization of iron from engulfed red blood cells. Taken together, the results of this study provide a new mechanism for selective autophagy of ferritin and reveal a previously unappreciated role for autophagy and NCOA4 in the control of iron homeostasis
in vivo
.
Murphy and colleagues generate an inhibitor of the lipid kinase VPS34, which they use to uncover autophagy substrates. One of their targets, NCOA4, regulates iron homeostasis by binding ferritin heavy chain-1 and targeting ferritin to autolysosomes. |
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AbstractList | Cells rely on autophagy to clear misfolded proteins and damaged organelles to maintain cellular homeostasis. In this study we use the new autophagy inhibitor PIK-III to screen for autophagy substrates. PIK-III is a selective inhibitor of VPS34 that binds a unique hydrophobic pocket not present in related kinases such as PI(3)Kα. PIK-III acutely inhibits autophagy and
de novo
lipidation of LC3, and leads to the stabilization of autophagy substrates. By performing ubiquitin-affinity proteomics on PIK-III-treated cells we identified substrates including NCOA4, which accumulates in
ATG7
-deficient cells and co-localizes with autolysosomes. NCOA4 directly binds ferritin heavy chain-1 (FTH1) to target the iron-binding ferritin complex with a relative molecular mass of 450,000 to autolysosomes following starvation or iron depletion. Interestingly,
Ncoa4
−/−
mice exhibit a profound accumulation of iron in splenic macrophages, which are critical for the reutilization of iron from engulfed red blood cells. Taken together, the results of this study provide a new mechanism for selective autophagy of ferritin and reveal a previously unappreciated role for autophagy and NCOA4 in the control of iron homeostasis
in vivo
.
Murphy and colleagues generate an inhibitor of the lipid kinase VPS34, which they use to uncover autophagy substrates. One of their targets, NCOA4, regulates iron homeostasis by binding ferritin heavy chain-1 and targeting ferritin to autolysosomes. Cells rely on autophagy to clear misfolded proteins and damaged organelles to maintain cellular homeostasis. In this study we use the new autophagy inhibitor PIK-III to screen for autophagy substrates. PIK-III is a selective inhibitor of VPS34 that binds a unique hydrophobic pocket not present in related kinases such as PI(3)Kα. PIK-III acutely inhibits autophagy and de novo lipidation of LC3, and leads to the stabilization of autophagy substrates. By performing ubiquitin-affinity proteomics on PIK-III-treated cells we identified substrates including NCOA4, which accumulates in ATG7-deficient cells and co-localizes with autolysosomes. NCOA4 directly binds ferritin heavy chain-1 (FTH1) to target the iron-binding ferritin complex with a relative molecular mass of 450,000 to autolysosomes following starvation or iron depletion. Interestingly, Ncoa4(-/-) mice exhibit a profound accumulation of iron in splenic macrophages, which are critical for the reutilization of iron from engulfed red blood cells. Taken together, the results of this study provide a new mechanism for selective autophagy of ferritin and reveal a previously unappreciated role for autophagy and NCOA4 in the control of iron homeostasis in vivo. Cells rely on autophagy to clear misfolded proteins and damaged organelles to maintain cellular homeostasis. In this study we use the new autophagy inhibitor PIK-III to screen for autophagy substrates. PIK-III is a selective inhibitor of VPS34 that binds a unique hydrophobic pocket not present in related kinases such as PI(3)Kα. PIK-III acutely inhibits autophagy and de novo lipidation of LC3, and leads to the stabilization of autophagy substrates. By performing ubiquitin-affinity proteomics on PIK-III-treated cells we identified substrates including NCOA4, which accumulates in ATG7-deficient cells and co-localizes with autolysosomes. NCOA4 directly binds ferritin heavy chain-1 (FTH1) to target the iron-binding ferritin complex with a relative molecular mass of 450,000 to autolysosomes following starvation or iron depletion. Interestingly, [Ncoa4.sup.-/-] mice exhibit a profound accumulation of iron in splenic macrophages, which are critical for the reutilization of iron from engulfed red blood cells. Taken together, the results of this study provide a new mechanism for selective autophagy of ferritin and reveal a previously unappreciated role for autophagy and NCOA4 in the control of iron homeostasis in vivo. |
Audience | Academic |
Author | Harrington, Edmund Burdick, Debra Wiederschain, Dmitri Porter, Jeffery A. Labow, Mark A. Murphy, Leon O. D’Aquin, Simon Myer, Vic E. Kuerth, Jenny Lei, Hong Nyfeler, Beat Mao, Xiaohong Cantwell, John Thomas, Jason Hamann, Lawrence G. Ugwonali, Savuth Harbinski, Fred Helliwell, Stephen B. Fang, Qing Wilson, Christopher J. Elling, Robert A. Wang, Zuncai Pardee, Gwynn Nagel, Jane Honda, Ayako Wang, Henry Dowdle, William E. Liu, Shanming Schwalb, David Schirle, Markus Tallarico, John Cornella-Taracido, Ivan Digan, Mary Ellen Nicholson, Thomas Menon, Suchithra Powers, Andrew F. Bastien, Julie Finan, Peter M. Luu, Catherine Knapp, Mark S. Keaney, Erin P. Bergman, Philip Fekkes, Peter Manning, Brendan D. Valdez, Reginald A. Bussiere, Dirksen E. Triantafellow, Ellen |
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organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 25 givenname: Dmitri surname: Wiederschain fullname: Wiederschain, Dmitri organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 26 givenname: Jenny surname: Kuerth fullname: Kuerth, Jenny organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 27 givenname: Philip surname: Bergman fullname: Bergman, Philip organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 28 givenname: David surname: Schwalb fullname: Schwalb, David organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 29 givenname: Jason surname: Thomas fullname: Thomas, Jason organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 30 givenname: Savuth surname: Ugwonali fullname: Ugwonali, Savuth organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 31 givenname: Fred surname: Harbinski fullname: Harbinski, Fred organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 32 givenname: John surname: Tallarico fullname: Tallarico, John organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 33 givenname: Christopher J. surname: Wilson fullname: Wilson, Christopher J. organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 34 givenname: Vic E. surname: Myer fullname: Myer, Vic E. organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – sequence: 35 givenname: Jeffery A. surname: Porter fullname: Porter, Jeffery A. organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge – 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O. surname: Murphy fullname: Murphy, Leon O. email: leon.murphy@novartis.com organization: Novartis Institutes for BioMedical Research, 250 Massachusetts Avenue, Cambridge |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25327288$$D View this record in MEDLINE/PubMed |
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SubjectTerms | 13/106 13/109 13/95 14/1 14/19 14/63 631/80/39 64/60 82/58 Animals Automation Autophagy Autophagy (Cytology) Autophagy - drug effects Autophagy - physiology Biomedical research Cancer Research Cell Biology Cells, Cultured Class III Phosphatidylinositol 3-Kinases - antagonists & inhibitors Developmental Biology Erythrocytes Ferritin Ferritins - metabolism Genetic aspects Homeostasis Homeostasis - physiology Humans Huntingtons disease Iron Iron - metabolism Kinases Life Sciences Lysosomes - metabolism Mice Microscopy Nuclear Receptor Coactivators - metabolism Phagosomes - metabolism Properties Protein Binding Proteins Stem Cells Substrates |
Title | Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo |
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