Emerging Mechanisms in Initiating and Terminating Autophagy

Mizushima, 2011, Autophagy: renovation of cells and tissues, Cell, 147, 728, 10.1016/j.cell.2011.10.026 Choi, 2013, Autophagy in human health and disease, N. Engl. J. Med., 368, 1845, 10.1056/NEJMra1205406 Galluzzi, 2014, Metabolic control of autophagy, Cell, 159, 1263, 10.1016/j.cell.2014.11.006 Deretic, 2013, Autophagy in infection, inflammation and immunity, Nat. Rev. Immunol., 13, 722, 10.1038/nri3532 Sheng, 2015, The divergent roles of autophagy in ischemia and preconditioning, Acta Pharmacol. Sin., 36, 411, 10.1038/aps.2014.151 Xie, 2015, Posttranslational modification of autophagy-related proteins in macroautophagy, Autophagy, 11, 28, 10.4161/15548627.2014.984267 Lamb, 2013, The autophagosome: origins unknown, biogenesis complex, Nat. Rev. Mol. Cell Biol., 14, 759, 10.1038/nrm3696 Lin, 2016, Structure and function of the ULK1 complex in autophagy, Curr. Opin. Cell Biol., 39, 61, 10.1016/j.ceb.2016.02.010 Mizushima, 2010, The role of the Atg1/ULK1 complex in autophagy regulation, Curr. Opin. Cell Biol., 22, 132, 10.1016/j.ceb.2009.12.004 Levine, 2015, Beclin orthologs: integrative hubs of cell signaling, membrane trafficking, and physiology, Trends Cell Biol., 25, 533, 10.1016/j.tcb.2015.05.004 Baskaran, 2014, Architecture and dynamics of the autophagic phosphatidylinositol 3-kinase complex, Elife, 3, e05115, 10.7554/eLife.05115 Ktistakis, 2016, Digesting the expanding mechanisms of autophagy, Trends Cell Biol., 26, 624, 10.1016/j.tcb.2016.03.006 Hamasaki, 2013, Autophagosomes form at ER–mitochondria contact sites, Nature, 495, 389, 10.1038/nature11910 Ge, 2014, Phosphatidylinositol 3-kinase and COPII generate LC3 lipidation vesicles from the ER–Golgi intermediate compartment, Elife, 3, e04135, 10.7554/eLife.04135 Yamamoto, 2012, Atg9 vesicles are an important membrane source during early steps of autophagosome formation, J. Cell Biol., 198, 219, 10.1083/jcb.201202061 Mizushima, 2011, The role of Atg proteins in autophagosome formation, Annu. Rev. Cell Dev. Biol., 27, 107, 10.1146/annurev-cellbio-092910-154005 Dooley, 2014, WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1, Mol. Cell, 55, 238, 10.1016/j.molcel.2014.05.021 Nakatogawa, 2007, Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion, Cell, 130, 165, 10.1016/j.cell.2007.05.021 Rogov, 2014, Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy, Mol. Cell, 53, 167, 10.1016/j.molcel.2013.12.014 Amaya, 2015, Autophagy and proteins involved in vesicular trafficking, FEBS Lett., 589, 3343, 10.1016/j.febslet.2015.09.021 McEwan, 2015, PLEKHM1 regulates Salmonella-containing vacuole biogenesis and infection, Cell. Host Microbe, 17, 58, 10.1016/j.chom.2014.11.011 Itakura, 2012, The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes, Cell, 151, 1256, 10.1016/j.cell.2012.11.001 Liang, 2008, Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking, Nat. Cell Biol., 10, 776, 10.1038/ncb1740 Kim, 2015, mTORC1 phosphorylates UVRAG to negatively regulate autophagosome and endosome maturation, Mol. Cell, 57, 207, 10.1016/j.molcel.2014.11.013 Wong, 2013, The ULK1 complex: sensing nutrient signals for autophagy activation, Autophagy, 9, 124, 10.4161/auto.23323 Puente, 2016, Nutrient-regulated phosphorylation of ATG13 inhibits starvation-induced autophagy, J. Biol. Chem., 291, 6026, 10.1074/jbc.M115.689646 Saleiro, 2015, Central role of ULK1 in type I interferon signaling, Cell. Rep., 11, 605, 10.1016/j.celrep.2015.03.056 Russell, 2013, ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase, Nat. Cell Biol., 15, 741, 10.1038/ncb2757 Egan, 2015, Small molecule inhibition of the autophagy kinase ULK1 and identification of ULK1 substrates, Mol. Cell, 59, 285, 10.1016/j.molcel.2015.05.031 Park, 2016, The ULK1 complex mediates MTORC1 signaling to the autophagy initiation machinery via binding and phosphorylating ATG14, Autophagy, 12, 547, 10.1080/15548627.2016.1140293 Di Bartolomeo, 2010, The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy, J. Cell Biol., 191, 155, 10.1083/jcb.201002100 Antonioli, 2014, AMBRA1 interplay with cullin E3 ubiquitin ligases regulates autophagy dynamics, Dev. Cell., 31, 734, 10.1016/j.devcel.2014.11.013 Nazio, 2013, mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6, Nat. Cell Biol., 15, 406, 10.1038/ncb2708 Wang, 2012, Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation, Science, 338, 956, 10.1126/science.1225967 Wei, 2013, EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance, Cell, 154, 1269, 10.1016/j.cell.2013.08.015 Tan, 2015, A kinase-independent role for EGF receptor in autophagy initiation, Cell, 160, 145, 10.1016/j.cell.2014.12.006 Hardie, 2014, AMPK--sensing energy while talking to other signaling pathways, Cell. Metab., 20, 939, 10.1016/j.cmet.2014.09.013 Egan, 2011, Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy, Science, 331, 456, 10.1126/science.1196371 Kim, 2011, AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1, Nat. Cell Biol., 13, 132, 10.1038/ncb2152 Zhao, 2015, RACK1 promotes autophagy by enhancing the Atg14L–Beclin 1–Vps34–Vps15 complex formation upon phosphorylation by AMPK, Cell. Rep., 13, 1407, 10.1016/j.celrep.2015.10.011 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 Moller, 2015, Physical exercise increases autophagic signaling through ULK1 in human skeletal muscle, J. Appl. Physiol., 118, 971, 10.1152/japplphysiol.01116.2014 Hoyer-Hansen, 2007, Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2, Mol. Cell, 25, 193, 10.1016/j.molcel.2006.12.009 Levine, 2008, Bcl-2 family members: dual regulators of apoptosis and autophagy, Autophagy, 4, 600, 10.4161/auto.6260 Luo, 2012, Bim inhibits autophagy by recruiting Beclin 1 to microtubules, Mol. Cell, 47, 359, 10.1016/j.molcel.2012.05.040 Wei, 2008, JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy, Mol. Cell, 30, 678, 10.1016/j.molcel.2008.06.001 Geeraert, 2010, Starvation-induced hyperacetylation of tubulin is required for the stimulation of autophagy by nutrient deprivation, J. Biol. Chem., 285, 24184, 10.1074/jbc.M109.091553 Gurkar, 2013, Identification of ROCK1 kinase as a critical regulator of Beclin1-mediated autophagy during metabolic stress, Nat. Commun., 4, 2189, 10.1038/ncomms3189 Rashid, 2015, ER stress: autophagy induction, inhibition and selection, Autophagy, 11, 1956, 10.1080/15548627.2015.1091141 Cinque, 2015, FGF signalling regulates bone growth through autophagy, Nature, 528, 272, 10.1038/nature16063 Gomez-Sanchez, 2015, Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves, J. Cell Biol., 210, 153, 10.1083/jcb.201503019 Zalckvar, 2009, DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy, EMBO Rep., 10, 285, 10.1038/embor.2008.246 Eisenberg-Lerner, 2012, PKD is a kinase of Vps34 that mediates ROS-induced autophagy downstream of DAPk, Cell Death Differ., 19, 788, 10.1038/cdd.2011.149 Maejima, 2013, Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2, Nat. Med., 19, 1478, 10.1038/nm.3322 Wei, 2015, The stress-responsive kinases MAPKAPK2/MAPKAPK3 activate starvation-induced autophagy through Beclin 1 phosphorylation, Elife, 4, e05289, 10.7554/eLife.05289 Criollo, 2011, Inhibition of autophagy by TAB2 and TAB3, EMBO J., 30, 4908, 10.1038/emboj.2011.413 Liang, 2014, Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses, Cell. Host Microbe, 15, 228, 10.1016/j.chom.2014.01.009 Konno, 2013, Cyclic dinucleotides trigger ULK1 (ATG1) phosphorylation of STING to prevent sustained innate immune signaling, Cell, 155, 688, 10.1016/j.cell.2013.09.049 Sakurai, 2012, Targeting of TAK1 in inflammatory disorders and cancer, Trends Pharmacol. Sci., 33, 522, 10.1016/j.tips.2012.06.007 Inokuchi-Shimizu, 2014, TAK1-mediated autophagy and fatty acid oxidation prevent hepatosteatosis and tumorigenesis, J. Clin. Invest., 124, 3566, 10.1172/JCI74068 Barber, 2015, STING: infection, inflammation and cancer, Nat. Rev. Immunol., 15, 760, 10.1038/nri3921 Grabbe, 2011, The spatial and temporal organization of ubiquitin networks, Nat. Rev. Mol. Cell Biol., 12, 295, 10.1038/nrm3099 Oeckinghaus, 2011, Crosstalk in NF-kappaB signaling pathways, Nat. Immunol., 12, 695, 10.1038/ni.2065 Shi, 2010, TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy, Sci. Signal., 3, ra42, 10.1126/scisignal.2000751 Xia, 2013, WASH inhibits autophagy through suppression of Beclin 1 ubiquitination, EMBO J., 32, 2685, 10.1038/emboj.2013.189 Platta, 2012, Nedd4-dependent lysine-11-linked polyubiquitination of the tumour suppressor Beclin 1, Biochem. J., 441, 399, 10.1042/BJ20111424 Xu, 2014, Regulation of autophagy by E3 ubiquitin ligase RNF216 through BECN1 ubiquitination, Autophagy, 10, 2239, 10.4161/15548627.2014.981792 Zhang, 2015, G-protein-coupled receptors regulate autophagy by ZBTB16-mediated ubiquitination and proteasomal degradation of Atg14L, Elife, 4, e06734, 10.7554/eLife.06734 Liu, 2011, Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13, Cell, 147, 223, 10.1016/j.cell.2011.08.037 Jin, 2016, USP19 modulates autophagy and antiviral immune responses by deubiquitinating Beclin-1, EMBO J., 35, 866, 10.15252/embj.201593596 Elgendy, 2014, Beclin 1 restrains tumorigenesis through Mcl-1 destabilization in an autophagy-independent reciprocal manner, Nat. Commun., 5, 5637, 10.1038/ncomms6637 Wu, 2015, The exocyst at a glance, J. Cell. Sci., 128, 2957, 10.1242/jcs.156398 Bodemann, 2011, RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly, Cell, 144, 253, 10.1016/j.cell.2010.12.018 Simicek, 2013, The deubiquitylase USP33 discriminates between RALB functions in autophagy and innate immune response, Nat. Cell Biol., 15, 1220, 10.1038/ncb2847 Joffre, 2015, The pro-apoptotic STK38 kinase is a new Beclin1 partner positively regulating autophagy, Curr. Biol., 25, 2479, 10.1016/j.cub.2015.08.031 Mandell, 2014, TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition, Dev. Cell., 30, 394, 10.1016/j.devcel.2014.06.013 Kimura, 2015, TRIM-mediated precision autophagy targets cytoplasmic regulators of innate immunity, J. Cell Biol., 210, 973, 10.1083/jcb.201503023 Liu, 2016, TRIM11 suppresses AIM2 inflammasome by degrading AIM2 via p62-dependent selective autophagy, Cell. Rep., 16, 1988, 10.1016/j.celrep.2016.07.019 Ra, 2016, TRIM31 promotes Atg5/Atg7-independent autophagy in intestinal cells, Nat. Commun., 7, 11726, 10.1038/ncomms11726 Kim, 2012, IFN-inducible GTPases in host cell defense, Cell. Host Microbe, 12, 432, 10.1016/j.chom.2012.09.007 Chauhan, 2015, IRGM governs the core autophagy machinery to conduct antimicrobial defense, Mol. Cell, 58, 507, 10.1016/j.molcel.2015.03.020 Singh, 2010, Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria, Nat. Cell Biol., 12, 1154, 10.1038/ncb2119 Efeyan, 2013, Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival, Nature, 493, 679, 10.1038/nature11745 Yu, 2010, Termination of autophagy and reformation of lysosomes regulated by mTOR, Nature, 465, 942, 10.1038/nature09076 Xia, 2014, RNF2 is recruited by WASH to ubiquitinate AMBRA1 leading to downregulation of autophagy, Cell Res., 24, 943, 10.1038/cr.2014.85 Liu, 2016, Cul3–KLHL20 ubiquitin ligase governs the turnover of ULK1 and VPS34 complexes to control autophagy termination, Mol. Cell, 61, 84, 10.1016/j.molcel.2015.11.001 Lee, 2010, The Cullin 3 substrate adaptor KLHL20 mediates DAPK ubiquitination to control interferon responses, EMBO J., 29, 1748, 10.1038/emboj.2010.62 Xiao, 2015, FBXL20-mediated Vps34 ubiquitination as a p53 controlled checkpoint in regulating autophagy and receptor degradation, Genes Dev., 29, 184, 10.1101/gad.252528.114 Feng, 2015, How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy, Trends Cell Biol., 25, 354, 10.1016/j.tcb.2015.02.002 Hurley, 2014, Atomistic autophagy: the structures of cellular self-digestion, Cell, 157, 300, 10.1016/j.cell.2014.01.070 Kvansakul, 2013, Structural biology of the Bcl-2 family and its mimicry by viral proteins, Cell. Death Dis., 4, e909, 10.1038/cddis.2013.436 Marino, 2014, Self-consumption: the interplay of autophagy and apoptosis, Nat. Rev. Mol. Cell Biol., 15, 81, 10.1038/nrm3735 Strappazzon, 2015, AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1, Cell Death Differ., 22, 419, 10.1038/cdd.2014.139 Fimia, 2013, Ambra1 at the crossroad between autophagy and cell death, Oncogene, 32, 3311, 10.1038/onc.2012.455 Molejon, 2013, The VMP1–Beclin 1 interaction regulates autophagy induction, Sci. Rep., 3, 1055, 10.1038/srep01055 Tang, 2010, Endogenous HMGB1 regulates autophagy, J. Cell Biol., 190, 881, 10.1083/jcb.200911078 Murthy, 2014, A Crohn's disease variant in Atg16l1 enhances its degradation by caspase 3, Nature, 506, 456, 10.1038/nature13044 Strappazzon, 2016, Prosurvival AMBRA1 turns into a proapoptotic BH3-like protein during mitochondrial apoptosis, Autophagy, 12, 963, 10.1080/15548627.2016.1164359 Zhu, 2015, Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation, J. Clin. Invest., 125, 1098, 10.1172/JCI76344 Banreti, 2013, The emerging role of acetylation in the regulation of autophagy, Autophagy, 9, 819, 10.4161/auto.23908 Lin, 2012, GSK3–TIP60–ULK1 signaling pathway links growth factor deprivation to autophagy, Science, 336, 477, 10.1126/science.1217032 Sun, 2015, Acetylation of Beclin 1 inhibits autophagosome maturation and promotes tumour growth, Nat. Commun., 6, 7215, 10.1038/ncomms8215 Huang, 2015, Deacetylation of nuclear LC3 drives autophagy initiation under starvation, Mol. Cell, 57, 456, 10.1016/j.molcel.2014.12.013 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 Sebti, 2014, BAT3 modulates p300-dependent acetylation of p53 and autophagy-related protein 7 (ATG7) during autophagy, Proc. Natl. Acad. Sci. U.S.A., 111, 4115, 10.1073/pnas.1313618111