Emerging roles of ATG9/ATG9A in autophagy: implications for cell and neurobiology

References

• Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000 Dec 1;290(5497):1717–1721. doi: 10.1126/science.290.5497.1717
   PubMed Web of Science ®Google Scholar
• Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2014 Jan;24(1):24–41. doi: 10.1038/cr.2013.168
   PubMed Web of Science ®Google Scholar
• Kuma A, Mizushima N. Physiological role of autophagy as an intracellular recycling system: with an emphasis on nutrient metabolism. Semin Cell Dev Biol. 2010 Sept 01;21(7):683–690. doi: 10.1016/j.semcdb.2010.03.002
   PubMed Web of Science ®Google Scholar
• Mortimore GE, Pösö AR. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu Rev Nutr. 1987;7(1):539–564. doi: 10.1146/annurev.nu.07.070187.002543
   PubMedGoogle Scholar
• Meijer AJ, Codogno P. Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol. 2004 Dec;36(12):2445–2462. doi: 10.1016/j.biocel.2004.02.002
   PubMed Web of Science ®Google Scholar
• Burman C, Ktistakis NT. Autophagosome formation in mammalian cells. Semin Immunopathol. 2010 Dec 01;32(4):397–413. doi: 10.1007/s00281-010-0222-z
   PubMed Web of Science ®Google Scholar
• Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001 Mar;2(3):211–216. doi: 10.1038/35056522
   PubMed Web of Science ®Google Scholar
• Uchiyama Y, Shibata M, Koike M, et al. Autophagy-physiology and pathophysiology. Histochem Cell Biol. 2008 Apr;129(4):407–420. doi: 10.1007/s00418-008-0406-y
   PubMed Web of Science ®Google Scholar
• Mercer TJ, Gubas A, Tooze SA. A molecular perspective of mammalian autophagosome biogenesis. J Biol Chem. 2018 Apr 13;293(15):5386–5395. doi: 10.1074/jbc.R117.810366
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009 Jul;10(7):458–467. doi: 10.1038/nrm2708
   PubMed Web of Science ®Google Scholar
• Melia TJ, Lystad AH, Simonsen A. Autophagosome biogenesis: from membrane growth to closure. J Cell Biol. 2020 Jun 1;219(6). doi: 10.1083/jcb.202002085
   PubMed Web of Science ®Google Scholar
• Nakatogawa H. Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol. 2020 Aug 01;21(8):439–458. doi: 10.1038/s41580-020-0241-0
   PubMed Web of Science ®Google Scholar
• Matoba K, Noda NN. Structural catalog of core atg proteins opens new era of autophagy research. J Biochem. 2021 Jul 3;169(5):517–525. doi: 10.1093/jb/mvab017
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Kakuta S, Watanabe TM, et al. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol. 2012 Jul 23;198(2):219–233. doi: 10.1083/jcb.201202061
   PubMed Web of Science ®Google Scholar
• Reggiori F, Shintani T, Nair U, et al. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy. 2005 Jul;1(2):101–109. doi: 10.4161/auto.1.2.1840
   PubMed Web of Science ®Google Scholar
• Noda T, Kim J, Huang WP, et al. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the cvt and autophagy pathways. J Cell Biol. 2000 Feb 7;148(3):465–480. doi: 10.1083/jcb.148.3.465
   PubMed Web of Science ®Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797. doi: 10.1093/nar/gkh340
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018 Jun 1;35(6):1547–1549. doi: 10.1093/molbev/msy096
   PubMed Web of Science ®Google Scholar
• Bult CJ, Sternberg PW. The alliance of genome resources: transforming comparative genomics. Mamm Genome. 2023 Dec;34(4):531–544. doi: 10.1007/s00335-023-10015-2
   PubMed Web of Science ®Google Scholar
• Martin FJ, Amode MR, Aneja A, et al. Ensembl 2023. Nucleic Acids Res. 2023;51(D1):D933–D941. doi: 10.1093/nar/gkac958
   PubMed Web of Science ®Google Scholar
• Chiduza GN, Garza-Garcia A, Almacellas E, et al. ATG9B is a tissue-specific homotrimeric lipid scramblase that can compensate for ATG9A. Autophagy. 2023 Nov;20(3):1–20. doi: 10.1080/15548627.2023.2275905
   PubMed Web of Science ®Google Scholar
• Robb GB, Carson AR, Tai SC, et al. Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J Biol Chem. 2004 Sep 3;279(36):37982–37996. doi: 10.1074/jbc.M400271200
   PubMed Web of Science ®Google Scholar
• Wang N, Tan HY, Li S, et al. Atg9b deficiency suppresses autophagy and potentiates endoplasmic reticulum stress-associated hepatocyte apoptosis in Hepatocarcinogenesis. Theranostics. 2017;7(8):2325–2338. doi: 10.7150/thno.18225
   PubMed Web of Science ®Google Scholar
• Tamura H, Shibata M, Koike M, et al. Atg9A protein, an autophagy-related membrane protein, is localized in the neurons of mouse brains. J Histochem Cytochem. 2010 May;58(5):443–453. doi: 10.1369/jhc.2010.955690
   PubMed Web of Science ®Google Scholar
• Yamada T, Carson AR, Caniggia I, et al. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem. 2005 May 6;280(18):18283–18290. doi: 10.1074/jbc.M413957200
   PubMed Web of Science ®Google Scholar
• Mailler E, Guardia CM, Bai X, et al. The autophagy protein ATG9A enables lipid mobilization from lipid droplets. Nat Commun. 2021 Nov 19;12(1):6750. doi: 10.1038/s41467-021-26999-x
   PubMed Web of Science ®Google Scholar
• Zhang X, Li C, Wang D, et al. Aberrant methylation of ATG2B, ATG4D, ATG9A and ATG9B CpG island promoter is associated with decreased mRNA expression in sporadic breast carcinoma. Gene. 2016 Sep 30;590(2):285–292. doi: 10.1016/j.gene.2016.05.036
   PubMed Web of Science ®Google Scholar
• Young AR, Chan EY, Hu XW, et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci. 2006 Sep 15;119(Pt 18):3888–3900. doi: 10.1242/jcs.03172
   PubMed Web of Science ®Google Scholar
• Saitoh T, Fujita N, Hayashi T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A. [2009 Dec 8];106(49):20842–20846. doi: 10.1073/pnas.0911267106
   PubMed Web of Science ®Google Scholar
• Kojima T, Yamada T, Akaishi R, et al. Role of the Atg9a gene in intrauterine growth and survival of fetal mice. Reprod Biol. 2015 Sep;15(3):131–138. doi: 10.1016/j.repbio.2015.05.001
   PubMed Web of Science ®Google Scholar
• Mattera R, Park SY, De Pace R, et al. AP-4 mediates export of ATG9A from the trans-Golgi network to promote autophagosome formation. Proc Natl Acad Sci U S A. [2017 Dec 12];114(50):E10697–E10706. doi: 10.1073/pnas.1717327114
   PubMed Web of Science ®Google Scholar
• Kishi-Itakura C, Koyama-Honda I, Itakura E, et al. Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J Cell Sci. [2014 Sep 15];127(Pt 18):4089–4102. doi: 10.1242/jcs.164293
   PubMed Web of Science ®Google Scholar
• Guardia CM, Tan XF, Lian T, et al. Structure of human ATG9A, the only transmembrane protein of the core autophagy machinery. Cell Rep. 2020 Jun 30;31(13):107837. doi: 10.1016/j.celrep.2020.107837
   PubMed Web of Science ®Google Scholar
• Runwal G, Stamatakou E, Siddiqi FH, et al. LC3-positive structures are prominent in autophagy-deficient cells. Sci Rep. 2019 July 12;9(1):10147. doi: 10.1038/s41598-019-46657-z
   PubMed Web of Science ®Google Scholar
• Olivas TJ, Wu Y, Yu S, et al. ATG9 vesicles comprise the seed membrane of mammalian autophagosomes. J Cell Biol. 2023 Jul 3;222(7). doi: 10.1083/jcb.202208088
   PubMed Web of Science ®Google Scholar
• Yamaguchi J, Suzuki C, Nanao T, et al. Atg9a deficiency causes axon-specific lesions including neuronal circuit dysgenesis. Autophagy. 2018;14(5):764–777. doi: 10.1080/15548627.2017.1314897
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007 08;282(33):24131–24145. doi: 10.1074/jbc.M702824200
   PubMed Web of Science ®Google Scholar
• Son JH, Shim JH, Kim K-H, et al. Neuronal autophagy and neurodegenerative diseases. Exp Mol Med. 2012 Feb 01;44(2):89–98. doi: 10.3858/emm.2012.44.2.031
   PubMed Web of Science ®Google Scholar
• Stavoe AKH, Holzbaur ELF. Autophagy in neurons. Annu Rev Cell Dev Biol. 2019 Oct 6;35(1):477–500. doi: 10.1146/annurev-cellbio-100818-125242
   PubMedGoogle Scholar
• Lai LTF, Yu C, Wong JSK, et al. Subnanometer resolution cryo-EM structure of Arabidopsis thaliana ATG9. Autophagy. 2020 Mar;16(3):575–583. doi: 10.1080/15548627.2019.1639300
   PubMed Web of Science ®Google Scholar
• Maeda S, Yamamoto H, Kinch LN, et al. Structure, lipid scrambling activity and role in autophagosome formation of ATG9A. Nat Struct Mol Biol. 2020 Dec;27(12):1194–1201. doi: 10.1038/s41594-020-00520-2
   PubMed Web of Science ®Google Scholar
• Matoba K, Kotani T, Tsutsumi A, et al. Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nat Struct Mol Biol. 2020 Dec;27(12):1185–1193. doi: 10.1038/s41594-020-00518-w
   PubMed Web of Science ®Google Scholar
• Malhotra N, Khatri S, Kumar A, et al. AI-based AlphaFold2 significantly expands the structural space of the autophagy pathway. Autophagy. 2023 Dec;19(12):3201–3220. doi: 10.1080/15548627.2023.2238578
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28(1):235–242. doi: 10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Sehnal D, Bittrich S, Deshpande M, et al. Mol* viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res. 2021;49(W1):W431–W437. doi: 10.1093/nar/gkab314
   PubMed Web of Science ®Google Scholar
• Park D, Wu Y, Wang X, et al. Synaptic vesicle proteins and ATG9A self-organize in distinct vesicle phases within synapsin condensates. Nat Commun. 2023 Jan 28;14(1):455. doi: 10.1038/s41467-023-36081-3
   PubMed Web of Science ®Google Scholar
• van Vliet AR, Chiduza GN, Maslen SL, et al. ATG9A and ATG2A form a heteromeric complex essential for autophagosome formation. Mol Cell. 2022 Nov 17;82(22):4324–4339 e8. doi: 10.1016/j.molcel.2022.10.017
   PubMed Web of Science ®Google Scholar
• Noda NN. Atg2 and Atg9: intermembrane and interleaflet lipid transporters driving autophagy. Biochim Biophys Acta Mol Cell Biol Lipids. 2021 Aug;1866(8):158956. doi: 10.1016/j.bbalip.2021.158956
   PubMed Web of Science ®Google Scholar
• Kakuta S, Yamaguchi J, Suzuki C, et al. Small GTPase Rab1B is associated with ATG9A vesicles and regulates autophagosome formation. Faseb J. 2017 Sep;31(9):3757–3773. doi: 10.1096/fj.201601052R
   PubMed Web of Science ®Google Scholar
• Orsi A, Razi M, Dooley HC, et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell. 2012 May;23(10):1860–1873. doi: 10.1091/mbc.e11-09-0746
   PubMed Web of Science ®Google Scholar
• Imai K, Hao F, Fujita N, et al. Atg9A trafficking through the recycling endosomes is required for autophagosome formation. J Cell Sci. 2016 Oct 15;129(20):3781–3791. doi: 10.1242/jcs.196196
   PubMed Web of Science ®Google Scholar
• Puri C, Renna M, Bento CF, et al. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell. 2013 Sep 12;154(6):1285–1299. doi: 10.1016/j.cell.2013.08.044
   PubMed Web of Science ®Google Scholar
• Claude-Taupin A, Jia J, Bhujabal Z, et al. ATG9A protects the plasma membrane from programmed and incidental permeabilization. Nat Cell Biol. 2021 Aug;23(8):846–858. doi: 10.1038/s41556-021-00706-w
   PubMed Web of Science ®Google Scholar
• Majumder P, Edmison D, Rodger C, et al. AP-4 regulates neuronal lysosome composition, function, and transport via regulating export of critical lysosome receptor proteins at the trans-Golgi network. Mol Biol Cell. 2022 Oct 1;33(12):ar102. doi: 10.1091/mbc.E21-09-0473
   PubMed Web of Science ®Google Scholar
• Davies AK, Itzhak DN, Edgar JR, et al. AP-4 vesicles contribute to spatial control of autophagy via RUSC-dependent peripheral delivery of ATG9A. Nat Commun. 2018 Sep 27;9(1):3958. doi: 10.1038/s41467-018-06172-7
   PubMedGoogle Scholar
• De Pace R, Skirzewski M, Damme M, et al. Altered distribution of ATG9A and accumulation of axonal aggregates in neurons from a mouse model of AP-4 deficiency syndrome. PLOS Genet. 2018 Apr;14(4):e1007363. doi: 10.1371/journal.pgen.1007363
   PubMed Web of Science ®Google Scholar
• Ivankovic D, Drew J, Lesept F, et al. Axonal autophagosome maturation defect through failure of ATG9A sorting underpins pathology in AP-4 deficiency syndrome. Autophagy. 2020 Mar;16(3):391–407. doi: 10.1080/15548627.2019.1615302
   PubMed Web of Science ®Google Scholar
• Kannangara AR, Poole DM, McEwan CM, et al. BioID reveals an ATG9A interaction with ATG13-ATG101 in the degradation of p62/SQSTM1-ubiquitin clusters. EMBO Rep. 2021 Oct 5;22(10):e51136. doi: 10.15252/embr.202051136
   PubMed Web of Science ®Google Scholar
• Binotti B, Ninov M, Cepeda AP, et al. ATG9 resides on a unique population of small vesicles in presynaptic nerve terminals. Autophagy. 2023 Oct;20(4):1–19. doi: 10.1080/15548627.2023.2274204
   PubMed Web of Science ®Google Scholar
• Zhou C, Ma K, Gao R, et al. Regulation of mATG9 trafficking by src- and ULK1-mediated phosphorylation in basal and starvation-induced autophagy. Cell Res. 2017 Feb;27(2):184–201. doi: 10.1038/cr.2016.146
   PubMed Web of Science ®Google Scholar
• Popovic D, Dikic I. TBC1D5 and the AP2 complex regulate ATG9 trafficking and initiation of autophagy. EMBO Rep. 2014 Apr;15(4):392–401. doi: 10.1002/embr.201337995
   PubMed Web of Science ®Google Scholar
• Guo Y, Chang C, Huang R, et al. AP1 is essential for generation of autophagosomes from the trans-Golgi network. J Cell Sci. [2012 Apr 1];125(Pt 7):1706–1715. doi: 10.1242/jcs.093203
   PubMed Web of Science ®Google Scholar
• Yang S, Park D, Manning L, et al. Presynaptic autophagy is coupled to the synaptic vesicle cycle via ATG-9. Neuron. 2022 Mar 2;110(5):824–840 e10. doi: 10.1016/j.neuron.2021.12.031
   PubMed Web of Science ®Google Scholar
• Stavoe AK, Hill SE, Hall DH, et al. KIF1A/UNC-104 transports ATG-9 to regulate neurodevelopment and autophagy at synapses. Dev Cell. 2016 Jul 25;38(2):171–185. doi: 10.1016/j.devcel.2016.06.012
   PubMed Web of Science ®Google Scholar
• Xuan Z, Yang S, Clark B, et al. The active zone protein clarinet regulates synaptic sorting of ATG-9 and presynaptic autophagy. PLOS Biol. 2023 Apr;21(4):e3002030. doi: 10.1371/journal.pbio.3002030
   PubMed Web of Science ®Google Scholar
• Xuan Z, Colón-Ramos DA. The active zone protein CLA-1 (clarinet) bridges two subsynaptic domains to regulate presynaptic sorting of ATG-9. Autophagy. 2023 Oct;19(10):2807–2808. doi: 10.1080/15548627.2023.2229227
   PubMed Web of Science ®Google Scholar
• Okerlund ND, Schneider K, Leal-Ortiz S, et al. Bassoon controls presynaptic autophagy through Atg5. Neuron. 2017 Feb 22;93(4):897–913.e7. doi: 10.1016/j.neuron.2017.01.026
   PubMed Web of Science ®Google Scholar
• Ke X, Bittencourt C, Van Tendeloo G. Possibilities and limitations of advanced transmission electron microscopy for carbon-based nanomaterials. Beilstein J Nanotechnol. 2015;6:1541–1557. doi: 10.3762/bjnano.6.158
   PubMed Web of Science ®Google Scholar
• Coumans F, Brisson A, Buzás E, et al. Methodological guidelines to study extracellular vesicles. Circ Res. 2017 May 12;120:1632–1648. doi: 10.1161/CIRCRESAHA.117.309417
   PubMed Web of Science ®Google Scholar
• Noda T. Autophagy in the context of the cellular membrane-trafficking system: the enigma of Atg9 vesicles. Biochem Soc Trans. 2017 Dec 15;45(6):1323–1331. doi: 10.1042/BST20170128
   PubMedGoogle Scholar
• Taoufiq Z, Ninov M, Villar-Briones A, et al. Hidden proteome of synaptic vesicles in the mammalian brain. Proc Natl Acad Sci USA. 2020 Dec 29;117(52):33586–33596. doi: 10.1073/pnas.2011870117
   PubMed Web of Science ®Google Scholar
• Ren X, Nguyen TN, Lam WK, et al. Structural basis for ATG9A recruitment to the ULK1 complex in mitophagy initiation. Sci Adv. [2023 Feb 15];9(7):eadg2997. doi: 10.1126/sciadv.adg2997
   PubMed Web of Science ®Google Scholar
• Nguyen A, Lugarini F, David C, et al. Metamorphic proteins at the basis of human autophagy initiation and lipid transfer. Mol Cell. 2023 Jun 15;83(12):2077–2090 e12. doi: 10.1016/j.molcel.2023.04.026
   PubMed Web of Science ®Google Scholar
• Merrill NM, Schipper JL, Karnes JB, et al. PI3K-C2α knockdown decreases autophagy and maturation of endocytic vesicles. PLOS ONE. 2017;12(9):e0184909. doi: 10.1371/journal.pone.0184909
   PubMed Web of Science ®Google Scholar
• Ghanbarpour A, Valverde DP, Melia TJ, et al. A model for a partnership of lipid transfer proteins and scramblases in membrane expansion and organelle biogenesis. Proc Natl Acad Sci USA. 2021 Apr 20;118(16). doi: 10.1073/pnas.2101562118
   PubMed Web of Science ®Google Scholar
• Suzuki K, Ohsumi Y. Current knowledge of the pre-autophagosomal structure (PAS). FEBS Lett. 2010 Apr 02;584(7):1280–1286. doi: 10.1016/j.febslet.2010.02.001
   PubMed Web of Science ®Google Scholar
• Ktistakis NT, Tooze SA. Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 2016 Aug 01;26(8):624–635. doi: 10.1016/j.tcb.2016.03.006
   PubMed Web of Science ®Google Scholar
• Goldsmith J, Ordureau A, Harper JW, et al. Brain-derived autophagosome profiling reveals the engulfment of nucleoid-enriched mitochondrial fragments by basal autophagy in neurons. Neuron. [2022 Mar 16];110(6):967–976 e8. doi: 10.1016/j.neuron.2021.12.029
   PubMed Web of Science ®Google Scholar
• Karanasios E, Walker SA, Okkenhaug H, et al. Autophagy initiation by ULK complex assembly on ER tubulovesicular regions marked by ATG9 vesicles. Nat Commun. 2016 Aug 11;7(1):12420. doi: 10.1038/ncomms12420
   PubMed Web of Science ®Google Scholar
• Kageyama S, Omori H, Saitoh T, et al. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell. 2011 Jul 1;22(13):2290–2300. doi: 10.1091/mbc.e10-11-0893
   PubMed Web of Science ®Google Scholar
• Holzer E, Martens S, Tulli S. The role of ATG9 vesicles in autophagosome biogenesis. J Mol Biol. 2024 Feb 10;436(15):168489. doi: 10.1016/j.jmb.2024.168489
   PubMed Web of Science ®Google Scholar
• Valverde DP, Yu S, Boggavarapu V, et al. ATG2 transports lipids to promote autophagosome biogenesis. J Cell Biol. [2019 Jun 3];218(6):1787–1798. doi: 10.1083/jcb.201811139
   PubMed Web of Science ®Google Scholar
• Gomez-Sanchez R, Rose J, Guimaraes R, et al. Atg9 establishes Atg2-dependent contact sites between the endoplasmic reticulum and phagophores. J Cell Biol. 2018 Aug 6;217(8):2743–2763. doi: 10.1083/jcb.201710116
   PubMed Web of Science ®Google Scholar
• Osawa T, Kotani T, Kawaoka T, et al. Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat Struct Mol Biol. 2019 Apr;26(4):281–288. doi: 10.1038/s41594-019-0203-4
   PubMed Web of Science ®Google Scholar
• Graef M. Membrane tethering by the autophagy ATG2A-WIPI4 complex. Proc Natl Acad Sci U S A. 2018 Oct 16;115(42):10540–10541. doi: 10.1073/pnas.1814759115
   PubMed Web of Science ®Google Scholar
• Zheng J-X, Li Y, Ding Y-H, et al. Architecture of the ATG2B-WDR45 complex and an aromatic Y/HF motif crucial for complex formation. Autophagy. 2017 Nov 02;13(11):1870–1883. doi: 10.1080/15548627.2017.1359381
   PubMed Web of Science ®Google Scholar
• Vargas Duarte P, Reggiori F. The organization and function of the phagophore-ER membrane contact sites. Contact (Thousand Oaks). Contact. 2023 Jan-Dec;6:25152564231183898. doi: 10.1177/25152564231183898
   Google Scholar
• Moretti F, Bergman P, Dodgson S, et al. TMEM41B is a novel regulator of autophagy and lipid mobilization. EMBO Rep. 2018 Sep 01;19(9):e45889. doi: 10.15252/embr.201845889
   PubMed Web of Science ®Google Scholar
• Morita K, Hama Y, Izume T, et al. Genome-wide CRISPR screen identifies TMEM41B as a gene required for autophagosome formation. J Cell Biol. 2018;217(11):3817–3828. doi: 10.1083/jcb.201804132
   PubMed Web of Science ®Google Scholar
• Shoemaker CJ, Huang TQ, Weir NR, et al. CRISPR screening using an expanded toolkit of autophagy reporters identifies TMEM41B as a novel autophagy factor. PLOS Biol. 2019;17(4):e2007044. doi: 10.1371/journal.pbio.2007044
   PubMed Web of Science ®Google Scholar
• Chen A, Ding WX, Ni HM. Scramblases as regulators of autophagy and lipid homeostasis: implications for NAFLD. Autophagy Rep. 2022;1(1):143–160. doi: 10.1080/27694127.2022.2055724
   PubMedGoogle Scholar
• Sawa-Makarska J, Baumann V, Coudevylle N, et al. Reconstitution of autophagosome nucleation defines Atg9 vesicles as seeds for membrane formation. Science. 2020 Sep 4;369(6508). doi: 10.1126/science.aaz7714
   PubMed Web of Science ®Google Scholar
• Broadbent DG, Barnaba C, Perez GI, et al. Quantitative analysis of autophagy reveals the role of ATG9 and ATG2 in autophagosome formation. J Cell Biol. 2023 Jul 3;222(7). doi: 10.1083/jcb.202210078
   PubMed Web of Science ®Google Scholar
• Pfisterer SG, Bakula D, Frickey T, et al. Lipid droplet and early autophagosomal membrane targeting of Atg2A and Atg14L in human tumor cells[S]. J Lipid Res. 2014 July 01;55(7):1267–1278. doi: 10.1194/jlr.M046359
   PubMed Web of Science ®Google Scholar
• Velikkakath AKG, Nishimura T, Oita E, et al. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell. 2012;23(5):896–909. doi: 10.1091/mbc.e11-09-0785
   PubMed Web of Science ®Google Scholar
• Bradberry MM, Mishra S, Zhang Z, et al. Rapid and gentle immunopurification of brain synaptic vesicles. J Neurosci. 2022 Apr 27;42(17):3512–3522. doi: 10.1523/JNEUROSCI.2521-21.2022
   PubMed Web of Science ®Google Scholar
• Chantranupong L, Saulnier JL, Wang W, et al. Rapid purification and metabolomic profiling of synaptic vesicles from mammalian brain. Elife. 2020 Oct 12;9:e59699. doi: 10.7554/eLife.59699
   PubMed Web of Science ®Google Scholar
• Hanna MG, Suen PH, Wu Y, et al. SHIP164 is a chorein motif lipid transfer protein that controls endosome–golgi membrane traffic. J Cell Biol. 2022;221(6):e202111018. doi: 10.1083/jcb.202111018
   PubMed Web of Science ®Google Scholar
• van Vliet AR, Jefferies HBJ, Faull PA, et al. Exploring the ATG9A interactome uncovers interaction with VPS13A. J Cell Sci. 2024;137(4):jcs261081. doi: 10.1242/jcs.261081
   PubMedGoogle Scholar
• Nishida Y, Nakamura M, Urata Y, et al. Novel pathogenic VPS13A gene mutations in Japanese patients with chorea-acanthocytosis. Neurol Genet. 2019 Jun;5(3):e332. doi: 10.1212/NXG.0000000000000332
   PubMed Web of Science ®Google Scholar
• García-García E, Chaparro-Cabanillas N, Coll-Manzano A, et al. Unraveling the spatiotemporal distribution of VPS13A in the mouse brain. Int J Mol Sci. 2021 Dec 1;22(23):13018. doi: 10.3390/ijms222313018
   PubMed Web of Science ®Google Scholar
• Hayashi-Nishino M, Fujita N, Noda T, et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol. 2009 Dec;11(12):1433–1437. doi: 10.1038/ncb1991
   PubMed Web of Science ®Google Scholar
• Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008 Aug 25;182(4):685–701. doi: 10.1083/jcb.200803137
   PubMed Web of Science ®Google Scholar
• Walker SA, Ktistakis NT. Autophagosome biogenesis machinery. J Mol Biol. 2020 Apr 03;432(8):2449–2461. doi: 10.1016/j.jmb.2019.10.027
   PubMed Web of Science ®Google Scholar
• Hailey DW, Rambold AS, Satpute-Krishnan P, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010 May 14;141(4):656–667. doi: 10.1016/j.cell.2010.04.009
   PubMed Web of Science ®Google Scholar
• Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER–mitochondria contact sites. Nature. 2013 Mar 01;495(7441):389–393. doi: 10.1038/nature11910
   PubMed Web of Science ®Google Scholar
• Wen JK, Wang YT, Chan CC, et al. Atg9 antagonizes TOR signaling to regulate intestinal cell growth and epithelial homeostasis in Drosophila. Elife. 2017 Nov 16;6. doi: 10.7554/eLife.29338
   Web of Science ®Google Scholar
• Hanaoka H, Noda T, Shirano Y, et al. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 2002 Jul;129(3):1181–1193. doi: 10.1104/pp.011024
   PubMed Web of Science ®Google Scholar
• Tóth ML, Sigmond T, Borsos E, et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy. 2008 Apr;4(3):330–338. doi: 10.4161/auto.5618
   PubMed Web of Science ®Google Scholar
• Hashimoto Y, Ookuma S, Nishida E. Lifespan extension by suppression of autophagy genes in caenorhabditis elegans. Genes Cells. 2009 Jun;14(6):717–726. doi: 10.1111/j.1365-2443.2009.01306.x
   PubMed Web of Science ®Google Scholar
• Hensel LL, Grbić V, Baumgarten DA, et al. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell. 1993;5(5):553–564. doi: 10.1105/tpc.5.5.553
   PubMed Web of Science ®Google Scholar
• Saitoh T, Fujita N, Jang MH, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature. 2008 Nov 13;456(7219):264–268. doi: 10.1038/nature07383
   PubMed Web of Science ®Google Scholar
• Kuma A, Komatsu M, Mizushima N. Autophagy-monitoring and autophagy-deficient mice. Autophagy. [2017 Oct 3];13(10):1619–1628. doi: 10.1080/15548627.2017.1343770
   PubMed Web of Science ®Google Scholar
• Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004 Dec 23;432(7020):1032–1036. doi: 10.1038/nature03029
   PubMed Web of Science ®Google Scholar
• Kiss V, Jipa A, Varga K, et al. Drosophila Atg9 regulates the actin cytoskeleton via interactions with profilin and ena. Cell Death Differ. 2020 May;27(5):1677–1692. doi: 10.1038/s41418-019-0452-0
   PubMed Web of Science ®Google Scholar
• Campisi D, Desrues L, Dembélé KP, et al. The core autophagy protein ATG9A controls dynamics of cell protrusions and directed migration. J Cell Biol. 2022 Mar 7;221(3). doi: 10.1083/jcb.202106014
   PubMed Web of Science ®Google Scholar
• Nishiyama J, Miura E, Mizushima N, et al. Aberrant membranes and double-membrane structures accumulate in the axons of Atg5-null purkinje cells before neuronal death. Autophagy. 2007 Nov-Dec;3(6):591–596. doi: 10.4161/auto.4964
   PubMed Web of Science ®Google Scholar
• Hara T, Nakamura K, Matsui M, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006 Jun 15;441(7095):885–889. doi: 10.1038/nature04724
   PubMed Web of Science ®Google Scholar
• Trentesaux C, Fraudeau M, Pitasi CL, et al. Essential role for autophagy protein ATG7 in the maintenance of intestinal stem cell integrity. Proc Natl Acad Sci USA. 2020 May 19;117(20):11136–11146. doi: 10.1073/pnas.1917174117
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Chiba T, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006 Jun 15;441(7095):880–884. doi: 10.1038/nature04723
   PubMed Web of Science ®Google Scholar
• Moreno-De-Luca A, Helmers SL, Mao H, et al. Adaptor protein complex-4 (AP-4) deficiency causes a novel autosomal recessive cerebral palsy syndrome with microcephaly and intellectual disability. J Med Genet. 2011 Feb;48(2):141–144. doi: 10.1136/jmg.2010.082263
   PubMed Web of Science ®Google Scholar
• Aggarwal A, Reichert H, VijayRaghavan K. A locomotor assay reveals deficits in heterozygous Parkinson’s disease model and proprioceptive mutants in adult Drosophila. Proc Natl Acad Sci USA. 2019 Dec 3;116(49):24830–24839. doi: 10.1073/pnas.1807456116
   PubMed Web of Science ®Google Scholar
• Cao M, Wu Y, Ashrafi G, et al. Parkinson sac domain mutation in synaptojanin 1 impairs clathrin uncoating at synapses and triggers dystrophic changes in dopaminergic axons. Neuron. 2017 Feb 22;93(4):882–896 e5. doi: 10.1016/j.neuron.2017.01.019
   PubMed Web of Science ®Google Scholar
• Winslow AR, Chen CW, Corrochano S, et al. α-Synuclein impairs macroautophagy: implications for Parkinson’s disease. J Cell Biol. 2010 Sep 20;190(6):1023–1037. doi: 10.1083/jcb.201003122
   PubMed Web of Science ®Google Scholar
• Yi S, Wang L, Ho MS, et al. The autophagy protein Atg9 functions in glia and contributes to parkinsonian symptoms in a drosophila model of Parkinson’s disease. Neural Regen Res. 2024 May;19(5):1150–1155. doi: 10.4103/1673-5374.382259
   PubMed Web of Science ®Google Scholar
• Bhukel A, Beuschel CB, Maglione M, et al. Autophagy within the mushroom body protects from synapse aging in a non-cell autonomous manner. Nat Commun. 2019 Mar 21;10(1):1318. doi: 10.1038/s41467-019-09262-2
   PubMedGoogle Scholar
• Kakanj P, Bhide S, Moussian B, et al. Autophagy-mediated plasma membrane removal promotes the formation of epithelial syncytia. Embo J. 2022 Jun 14;41(12):e109992. doi: 10.15252/embj.2021109992
   PubMed Web of Science ®Google Scholar
• Vale-Costa S, Etibor TA, Brás D, et al. ATG9A regulates the dissociation of recycling endosomes from microtubules to form liquid influenza a virus inclusions. PLOS Biol. 2023;21(11):e3002290. doi: 10.1371/journal.pbio.3002290
   PubMed Web of Science ®Google Scholar
• Papin L, Lehmann M, Lagisquet J, et al. The autophagy nucleation factor ATG9 forms nanoclusters with the HIV-1 receptor DC-SIGN and regulates early antiviral autophagy in human dendritic cells. Int J Mol Sci. 2023 May 19;24(10):9008. doi: 10.3390/ijms24109008
   PubMed Web of Science ®Google Scholar
• Mailler E, Waheed AA, Park SY, et al. The autophagy protein ATG9A promotes HIV-1 infectivity. Retrovirology. 2019 Jul 3;16(1):18. doi: 10.1186/s12977-019-0480-3
   PubMedGoogle Scholar
• Tang HW, Liao HM, Peng WH, et al. Atg9 interacts with dTRAF2/TRAF6 to regulate oxidative stress-induced JNK activation and autophagy induction. Dev Cell. 2013 Dec 9;27(5):489–503. doi: 10.1016/j.devcel.2013.10.017
   PubMed Web of Science ®Google Scholar