VPS34 Acetylation Controls Its Lipid Kinase Activity and the Initiation of Canonical and Non-canonical Autophagy

Asara, 2008, A label-free quantification method by MS/MS TIC compared to SILAC and spectral counting in a proteomics screen, Proteomics, 8, 994, 10.1002/pmic.200700426 Axe, 2008, Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum, J. Cell Biol., 182, 685, 10.1083/jcb.200803137 Backer, 2008, The regulation and function of Class III PI3Ks: novel roles for Vps34, Biochem. J., 410, 1, 10.1042/BJ20071427 Bánréti, 2013, The emerging role of acetylation in the regulation of autophagy, Autophagy, 9, 819, 10.4161/auto.23908 Bordoli, 2001, Functional analysis of the p300 acetyltransferase domain: the PHD finger of p300 but not of CBP is dispensable for enzymatic activity, Nucleic Acids Res., 29, 4462, 10.1093/nar/29.21.4462 Burke, 2012, Oncogenic mutations mimic and enhance dynamic events in the natural activation of phosphoinositide 3-kinase p110α (PIK3CA), Proc. Natl. Acad. Sci. USA, 109, 15259, 10.1073/pnas.1205508109 Cantó, 2009, AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity, Nature, 458, 1056, 10.1038/nature07813 Chang, 2015, AMPK-dependent phosphorylation of GAPDH triggers Sirt1 activation and is necessary for autophagy upon glucose starvation, Mol. Cell, 60, 930, 10.1016/j.molcel.2015.10.037 Cheng, 2017, Pacer mediates the function of Class III PI3K and HOPS complexes in autophagosome maturation by engaging Stx17, Mol. Cell, 65, 1029, 10.1016/j.molcel.2017.02.010 Cheong, 2011, Ammonia-induced autophagy is independent of ULK1/ULK2 kinases, Proc. Natl. Acad. Sci. USA, 108, 11121, 10.1073/pnas.1107969108 Codogno, 2011, Canonical and non-canonical autophagy: variations on a common theme of self-eating?, Nat. Rev. Mol. Cell Biol., 13, 7, 10.1038/nrm3249 Eng, 2010, Ammonia derived from glutaminolysis is a diffusible regulator of autophagy, Sci. Signal., 3, ra31, 10.1126/scisignal.2000911 Fujita, 2008, The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy, Mol. Biol. Cell, 19, 2092, 10.1091/mbc.e07-12-1257 Grotemeier, 2010, AMPK-independent induction of autophagy by cytosolic Ca2+ increase, Cell. Signal., 22, 914, 10.1016/j.cellsig.2010.01.015 Huang, 2015, Deacetylation of nuclear LC3 drives autophagy initiation under starvation, Mol. Cell, 57, 456, 10.1016/j.molcel.2014.12.013 Ichimura, 2000, A ubiquitin-like system mediates protein lipidation, Nature, 408, 488, 10.1038/35044114 Itakura, 2008, Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG, Mol. Biol. Cell, 19, 5360, 10.1091/mbc.e08-01-0080 Kabeya, 2004, LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation, J. Cell Sci., 117, 2805, 10.1242/jcs.01131 Karanam, 2006, Kinetic and mass spectrometric analysis of p300 histone acetyltransferase domain autoacetylation, J. Biol. Chem., 281, 40292, 10.1074/jbc.M608813200 Kihara, 2001, Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae, J. Cell Biol., 152, 519, 10.1083/jcb.152.3.519 Kim, 2011, AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1, Nat. Cell Biol., 13, 132, 10.1038/ncb2152 Kim, 2013, Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy, Cell, 152, 290, 10.1016/j.cell.2012.12.016 Lee, 2009, Regulation of autophagy by the p300 acetyltransferase, J. Biol. Chem., 284, 6322, 10.1074/jbc.M807135200 Lee, 2008, A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy, Proc. Natl. Acad. Sci. USA, 105, 3374, 10.1073/pnas.0712145105 Liang, 2006, Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG, Nat. Cell Biol., 8, 688, 10.1038/ncb1426 Lin, 2012, GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy, Science, 336, 477, 10.1126/science.1217032 Lipinski, 2010, A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions, Dev. Cell, 18, 1041, 10.1016/j.devcel.2010.05.005 Luhr, 2017, A simple cargo sequestration assay for quantitative measurement of nonselective autophagy in cultured cells, Methods Enzymol., 587, 351, 10.1016/bs.mie.2016.09.064 Mariño, 2014, Regulation of autophagy by cytosolic acetyl-coenzyme A, Mol. Cell, 53, 710, 10.1016/j.molcel.2014.01.016 Matsunaga, 2009, Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages, Nat. Cell Biol., 11, 385, 10.1038/ncb1846 Matsunaga, 2010, Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L, J. Cell Biol., 190, 511, 10.1083/jcb.200911141 McKnight, 2014, Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG-VPS34 complex, PLoS Genet., 10, e1004626, 10.1371/journal.pgen.1004626 Miller, 2010, Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34, Science, 327, 1638, 10.1126/science.1184429 Mizushima, 2004, In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker, Mol. Biol. Cell, 15, 1101, 10.1091/mbc.e03-09-0704 Nishimura, 2013, FIP200 regulates targeting of Atg16L1 to the isolation membrane, EMBO Rep., 14, 284, 10.1038/embor.2013.6 Pietrocola, 2015, Spermidine induces autophagy by inhibiting the acetyltransferase EP300, Cell Death Differ., 22, 509, 10.1038/cdd.2014.215 Pietrocola, 2015, Acetyl coenzyme A: a central metabolite and second messenger, Cell Metab., 21, 805, 10.1016/j.cmet.2015.05.014 Rudge, 2004, Vacuole size control: regulation of PtdIns(3,5)P2 levels by the vacuole-associated Vac14-Fig4 complex, a PtdIns(3,5)P2-specific phosphatase, Mol. Biol. Cell, 15, 24, 10.1091/mbc.e03-05-0297 Russell, 2013, ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase, Nat. Cell Biol., 15, 741, 10.1038/ncb2757 Scarlatti, 2008, Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells, Cell Death Differ., 15, 1318, 10.1038/cdd.2008.51 Sebti, 2014, BAT3 modulates p300-dependent acetylation of p53 and autophagy-related protein 7 (ATG7) during autophagy, Proc. Natl. Acad. Sci. USA, 111, 4115, 10.1073/pnas.1313618111 Shi, 2009, CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53, Proc. Natl. Acad. Sci. USA, 106, 16275, 10.1073/pnas.0904305106 Smith, 2010, Arsenic trioxide induces a beclin-1-independent autophagic pathway via modulation of SnoN/SkiL expression in ovarian carcinoma cells, Cell Death Differ., 17, 1867, 10.1038/cdd.2010.53 Sun, 2011, The RUN domain of rubicon is important for hVps34 binding, lipid kinase inhibition, and autophagy suppression, J. Biol. Chem., 286, 185, 10.1074/jbc.M110.126425 Sun, 2015, Acetylation of Beclin 1 inhibits autophagosome maturation and promotes tumour growth, Nat. Commun., 6, 7215, 10.1038/ncomms8215 Taguchi-Atarashi, 2010, Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy, Traffic, 11, 468, 10.1111/j.1600-0854.2010.01034.x Thompson, 2004, Regulation of the p300 HAT domain via a novel activation loop, Nat. Struct. Mol. Biol., 11, 308, 10.1038/nsmb740 Tian, 2010, Beclin 1-independent autophagy induced by a Bcl-XL/Bcl-2 targeting compound, Z18, Autophagy, 6, 1032, 10.4161/auto.6.8.13336 Vicinanza, 2015, PI(5)P regulates autophagosome biogenesis, Mol. Cell, 57, 219, 10.1016/j.molcel.2014.12.007 Yamamoto, 2006, Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway, J. Cell Biol., 172, 719, 10.1083/jcb.200510065 Yang, 2001, Regulation of transcription by AMP-activated protein kinase: phosphorylation of p300 blocks its interaction with nuclear receptors, J. Biol. Chem., 276, 38341, 10.1074/jbc.C100316200 Yang, 2013, Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy, Proc. Natl. Acad. Sci. USA, 110, 6841, 10.1073/pnas.1217692110 Zhang, 2011, AMP-activated protein kinase suppresses endothelial cell inflammation through phosphorylation of transcriptional coactivator p300, Arterioscler. Thromb. Vasc. Biol., 31, 2897, 10.1161/ATVBAHA.111.237453 Zhang, 2015, G-protein-coupled receptors regulate autophagy by ZBTB16-mediated ubiquitination and proteasomal degradation of Atg14L, eLife, 4, e06734, 10.7554/eLife.06734 Zhong, 2009, Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex, Nat. Cell Biol., 11, 468, 10.1038/ncb1854 Zhu, 2007, Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death, Am. J. Pathol., 170, 75, 10.2353/ajpath.2007.060524