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Review

Atg8 family proteins, LIR/AIM motifs and other interaction modes

Vladimir V. Rogova Institute for Pharmaceutical Chemistry, Department of Biochemistry, Chemistry and Pharmacy, Goethe University, 60438 Frankfurt, am Main, and Structural Genomics Consortium, Buchmann Institute for Molecular Life Sciences, Goethe University, 60438Frankfurt am Main, GermanyView further author information
,
Ioannis P. Nezisb School of Life Sciences, University of Warwick, CV4 7ALCoventry, UKView further author information
,
Panagiotis Tsaprasb School of Life Sciences, University of Warwick, CV4 7ALCoventry, UKView further author information
,
Hong Zhangc National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China and College of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaView further author information
,
Yasin Dagdasd Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, AustriaView further author information
,
Nobuo N. Nodae Institute for Genetic Medicine, Hokkaido University, Kita 15, Nishi 7, Kita-ku, Sapporo 060-0815, JapanView further author information
,
Hitoshi Nakatogawaf School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, JapanView further author information
,
Martina Wirthg Molecular Cell Biology of Autophagy, The Francis Crick Institute, London, UKView further author information
,
Stephane Mouilleronh Structural Biology Science Technology Platform, The Francis Crick Institute, London, UKView further author information
,
David G. McEwani Cancer Research UK Beatson Institute, Glasgow, UKView further author information
,
Christian Behrendsj Munich Cluster of Systems Neurology, Ludwig-Maximilians-Universität München, München, GermanyView further author information
,
Vojo Deretick Autophagy, Inflammation and Metabolism Center of Biochemical Research Excellence, Albuquerque, NM and Department of Molecular Genetics and Microbiology, University of New Mexico Health Sciences Center, Albuquerque, NMView further author information
,
Zvulun Elazarl Department of Biomolecular Sciences, The Weizmann Institute of Science, Rehovot, IsraelView further author information
,
Sharon A. Toozeg Molecular Cell Biology of Autophagy, The Francis Crick Institute, London, UKView further author information
,
Ivan Dikicm Institute of Biochemistry II, Medical Faculty, Goethe-University, Frankfurt am Main, and Buchmann Institute for Molecular Life Sciences, Frankfurt am Main, GermanyView further author information
,
Trond Lamarkn Autophagy Research Group, Department of Medical Biology, University of Tromsø - The Arctic University of Norway, Tromsø, NorwayView further author information
&
Terje Johansenn Autophagy Research Group, Department of Medical Biology, University of Tromsø - The Arctic University of Norway, Tromsø, NorwayCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-1451-9578View further author information
ORCID Icon show all
Article: 2188523 | Published online: 19 Mar 2023

References

  • Ohsumi Y. Historical landmarks of autophagy research. Cell research. 2014 Jan;24(1):9–47.
  • Yamamoto H, Zhang S, Mizushima N. Autophagy genes in biology and disease. Nat Rev Genet. 2023 Jan 12.
  • Maeda S, Otomo C, Otomo T. The autophagic membrane tether ATG2A transfers lipids between membranes. Elife. 2019 Jul 4;8:e45777.
  • Maeda S, Yamamoto H, Kinch LN, Garza CM, Takahashi S, Otomo C, Grishin NV, Forli S, Mizushima N, Otomo T. Structure, lipid scrambling activity and role in autophagosome formation of ATG9A. Nat Struct Mol Biol. 2020 Dec;27(12):1194–1201.
  • Matoba K, Kotani T, Tsutsumi A, Tsuji T, Mori T, Noshiro D, Sugita Y, Nomura N, Iwata S, Ohsumi Y, Fujimoto T, Nakatogawa H, Kikkawa M, Noda NN. Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nat Struct Mol Biol. 2020 Dec;27(12):1185–1193.
  • Mizushima N. The ATG conjugation systems in autophagy. Curr Opin Cell Biol. 2020 Apr;63:1–10.
  • Nakatogawa H. Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol. 2020 Aug;21(8):439–458.
  • Shpilka T, Weidberg H, Pietrokovski S, Elazar Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome biology. 2011;12(7):226.
  • Johansen T, Lamark T. Selective autophagy: ATG8 family proteins, LIR motifs and cargo receptors. Journal of molecular biology. 2020;432(1):80–103.
  • Deretic V, Lazarou M. A guide to membrane atg8ylation and autophagy with reflections on immunity. J Cell Biol. 2022 Jul 4;221(7).
  • Sakamaki JI, Ode KL, Kurikawa Y, Ueda HR, Yamamoto H, Mizushima N. Ubiquitination of phosphatidylethanolamine in organellar membranes. Mol Cell. 2022 Oct 6;82(19):3677–3692 e11.
  • Jia J, Wang F, Bhujabal Z, Peters R, Mudd M, Duque T, Allers L, Javed R, Salemi M, Behrends C, Phinney B, Johansen T, Deretic V. Stress granules and mTOR are regulated by membrane atg8ylation during lysosomal damage. J Cell Biol. 2022 Nov 7;221(11).
  • Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, Ivanov A, Capell BC, Drake AM, Shah PP, Catanzaro JM, Ricketts MD, Lamark T, Adam SA, Marmorstein R, Zong WX, Johansen T, Goldman RD, Adams PD, Berger SL. Autophagy mediates degradation of nuclear lamina. Nature. 2015 Nov 5;527(7576):105–9.
  • Huang R, Xu Y, Wan W, Shou X, Qian J, You Z, Liu B, Chang C, Zhou T, Lippincott-Schwartz J, Liu W. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell. 2015 Feb 05;57(3):456–66.
  • Jacomin AC, Petridi S, Di Monaco M, Bhujabal Z, Jain A, Mulakkal NC, Palara A, Powell EL, Chung B, Zampronio C, Jones A, Cameron A, Johansen T, Nezis IP. Regulation of Expression of Autophagy Genes by Atg8a-Interacting Partners Sequoia, YL-1, and Sir2 in Drosophila. Cell Rep. 2020 May 26;31(8):107695.
  • Xu C, Wang L, Fozouni P, Evjen G, Chandra V, Jiang J, Lu C, Nicastri M, Bretz C, Winkler JD, Amaravadi R, Garcia BA, Adams PD, Ott M, Tong W, Johansen T, Dou Z, Berger SL. SIRT1 is downregulated by autophagy in senescence and ageing. Nat Cell Biol. 2020 Oct;22(10):1170–1179.
  • Legesse-Miller A, Sagiv Y, Porat A, Elazar Z. Isolation and characterization of a novel low molecular weight protein involved in intra-Golgi traffic. J Biol Chem. 1998 Jan 30;273(5):3105–9.
  • Muller JM, Shorter J, Newman R, Deinhardt K, Sagiv Y, Elazar Z, Warren G, Shima DT. Sequential SNARE disassembly and GATE-16-GOS-28 complex assembly mediated by distinct NSF activities drives Golgi membrane fusion. J Cell Biol. 2002 Jun 24;157(7):1161–73.
  • Sagiv Y, Legesse-Miller A, Porat A, Elazar Z. GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. EMBO J. 2000 Apr 3;19(7):1494–504.
  • Sanwald JL, Dobner J, Simons IM, Poschmann G, Stuhler K, Uffing A, Hoffmann S, Willbold D. Lack of GABARAP-Type Proteins Is Accompanied by Altered Golgi Morphology and Surfaceome Composition. Int J Mol Sci. 2020 Dec 23;22(1).
  • Gu Y, Princely Abudu Y, Kumar S, Bissa B, Choi SW, Jia J, Lazarou M, Eskelinen EL, Johansen T, Deretic V. Mammalian Atg8 proteins regulate lysosome and autolysosome biogenesis through SNAREs. EMBO J. 2019 Nov 15;38(22):e101994.
  • Kumar S, Jain A, Farzam F, Jia J, Gu Y, Choi SW, Mudd MH, Claude-Taupin A, Wester MJ, Lidke KA, Rusten TE, Deretic V. Mechanism of Stx17 recruitment to autophagosomes via IRGM and mammalian Atg8 proteins. J Cell Biol. 2018 Mar 5;217(3):997–1013.
  • Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007 Aug 17;282(33):24131–45.
  • Noda NN, Ohsumi Y, Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 2010 Apr 2;584(7):1379–85.
  • Klionsky DJ, Cregg JM, Dunn WA, Jr., Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y. A unified nomenclature for yeast autophagy-related genes. Dev Cell. 2003 Oct;5(4):539–45.
  • Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol. 2000 Oct 16;151(2):263–76.
  • Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y. A ubiquitin-like system mediates protein lipidation. Nature. 2000 Nov 23;408(6811):488–92.
  • Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007 Dec 28;282(52):37298–302.
  • Sakoh-Nakatogawa M, Matoba K, Asai E, Kirisako H, Ishii J, Noda NN, Inagaki F, Nakatogawa H, Ohsumi Y. Atg12-Atg5 conjugate enhances E2 activity of Atg3 by rearranging its catalytic site. Nat Struct Mol Biol. 2013 Apr;20(4):433–9.
  • Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 2001 Nov 1;20(21):5971–81.
  • Hirata E, Ohya Y, Suzuki K. Atg4 plays an important role in efficient expansion of autophagic isolation membranes by cleaving lipidated Atg8 in Saccharomyces cerevisiae. PloS one. 2017;12(7):e0181047.
  • Nair U, Yen WL, Mari M, Cao Y, Xie Z, Baba M, Reggiori F, Klionsky DJ. A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy. 2012 May 1;8(5):780–93.
  • Nakatogawa H, Ishii J, Asai E, Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy. 2012 Feb 1;8(2):177–86.
  • Yu ZQ, Ni T, Hong B, Wang HY, Jiang FJ, Zou S, Chen Y, Zheng XL, Klionsky DJ, Liang Y, Xie Z. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy. 2012 Jun;8(6):883–92.
  • Kaufmann A, Beier V, Franquelim HG, Wollert T. Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell. 2014 Jan 30;156(3):469–81.
  • Knorr RL, Nakatogawa H, Ohsumi Y, Lipowsky R, Baumgart T, Dimova R. Membrane morphology is actively transformed by covalent binding of the protein Atg8 to PE-lipids. PloS one. 2014;9(12):e115357.
  • Maruyama T, Alam JM, Fukuda T, Kageyama S, Kirisako H, Ishii Y, Shimada I, Ohsumi Y, Komatsu M, Kanki T, Nakatogawa H, Noda NN. Membrane perturbation by lipidated Atg8 underlies autophagosome biogenesis. Nat Struct Mol Biol. 2021 Jul;28(7):583–593.
  • Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, Griffith J, Nag S, Wang K, Moss T, Baba M, McNew JA, Jiang X, Reggiori F, Melia TJ, Klionsky DJ. SNARE proteins are required for macroautophagy. Cell. 2011 Jul 22;146(2):290–302.
  • Nakatogawa H, Ichimura Y, Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell. 2007 Jul 13;130(1):165–78.
  • Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, Kraft C, Martens S. Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J. 2012 Nov 14;31(22):4304–17.
  • Ichimura Y, Imamura Y, Emoto K, Umeda M, Noda T, Ohsumi Y. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J Biol Chem. 2004 Sep 24;279(39):40584–92.
  • Liu XM, Yamasaki A, Du XM, Coffman VC, Ohsumi Y, Nakatogawa H, Wu JQ, Noda NN, Du LL. Lipidation-independent vacuolar functions of Atg8 rely on its noncanonical interaction with a vacuole membrane protein. Elife. 2018 Nov19;7.
  • Mikawa T, Kanoh J, Ishikawa F. Fission yeast Vps1 and Atg8 contribute to oxidative stress resistance. Genes Cells. 2010 Mar;15(3):229–42.
  • Tamura N, Oku M, Sakai Y. Atg8 regulates vacuolar membrane dynamics in a lipidation-independent manner in Pichia pastoris. J Cell Sci. 2010 Dec 1;123(Pt 23):4107–16.
  • Jipa A, Vedelek V, Merenyi Z, Urmosi A, Takats S, Kovacs AL, Horvath GV, Sinka R, Juhasz G. Analysis of Drosophila Atg8 proteins reveals multiple lipidation-independent roles. Autophagy. 2021 Sep;17(9):2565–2575.
  • Kageyama T, Suzuki K, Ohsumi Y. Lap3 is a selective target of autophagy in yeast, Saccharomyces cerevisiae. Biochem Biophys Res Commun. 2009 Jan 16;378(3):551–7.
  • Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell. 2009 Jul;17(1):98–109.
  • Lu K, Psakhye I, Jentsch S. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell. 2014 Jul 31;158(3):549–63.
  • Lynch-Day MA, Klionsky DJ. The Cvt pathway as a model for selective autophagy. FEBS Lett. 2010 Apr 2;584(7):1359–66.
  • Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H, Ohsumi Y, Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015 Jun 18;522(7556):359–62.
  • Motley AM, Nuttall JM, Hettema EH. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 2012 Jun 29;31(13):2852–68.
  • Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell. 2009 Jul;17(1):87–97.
  • Suzuki K, Kondo C, Morimoto M, Ohsumi Y. Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J Biol Chem. 2010 Sep 24;285(39):30019–25.
  • Suzuki K, Morimoto M, Kondo C, Ohsumi Y. Selective autophagy regulates insertional mutagenesis by the Ty1 retrotransposon in Saccharomyces cerevisiae. Dev Cell. 2011 Aug 16;21(2):358–65.
  • Yuga M, Gomi K, Klionsky DJ, Shintani T. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J Biol Chem. 2011 Apr 15;286(15):13704–13.
  • Farre JC, Manjithaya R, Mathewson RD, Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell. 2008 Mar;14(3):365–76.
  • Kawaguchi K, Yurimoto H, Oku M, Sakai Y. Yeast methylotrophy and autophagy in a methanol-oscillating environment on growing Arabidopsis thaliana leaves. PloS one. 2011;6(9):e25257.
  • Fukuda T, Ebi Y, Saigusa T, Furukawa K, Yamashita SI, Inoue K, Kobayashi D, Yoshida Y, Kanki T. Atg43 tethers isolation membranes to mitochondria to promote starvation-induced mitophagy in fission yeast. Elife. 2020 Nov 3;9.
  • Zhao D, Zou CX, Liu XM, Jiang ZD, Yu ZQ, Suo F, Du TY, Dong MQ, He W, Du LL. A UPR-Induced Soluble ER-Phagy Receptor Acts with VAPs to Confer ER Stress Resistance. Mol Cell. 2020 Sep 17;79(6):963–977 e3.
  • Lee CW, Wilfling F, Ronchi P, Allegretti M, Mosalaganti S, Jentsch S, Beck M, Pfander B. Selective autophagy degrades nuclear pore complexes. Nat Cell Biol. 2020 Feb;22(2):159–166.
  • Shpilka T, Welter E, Borovsky N, Amar N, Shimron F, Peleg Y, Elazar Z. Fatty acid synthase is preferentially degraded by autophagy upon nitrogen starvation in yeast. Proc Natl Acad Sci U S A. 2015 Feb 3;112(5):1434–9.
  • Tomioka Y, Kotani T, Kirisako H, Oikawa Y, Kimura Y, Hirano H, Ohsumi Y, Nakatogawa H. TORC1 inactivation stimulates autophagy of nucleoporin and nuclear pore complexes. J Cell Biol. 2020 Jul 6;219(7).
  • Wilfling F, Lee CW, Erdmann PS, Zheng Y, Sherpa D, Jentsch S, Pfander B, Schulman BA, Baumeister W. A Selective Autophagy Pathway for Phase-Separated Endocytic Protein Deposits. Mol Cell. 2020 Dec 3;80(5):764–778 e7.
  • Bartholomew CR, Suzuki T, Du Z, Backues SK, Jin M, Lynch-Day MA, Umekawa M, Kamath A, Zhao M, Xie Z, Inoki K, Klionsky DJ. Ume6 transcription factor is part of a signaling cascade that regulates autophagy. Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11206–10.
  • Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol. 1999 Oct 18;147(2):435–46.
  • Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008 Aug;19(8):3290–8.
  • Maqbool A, Hughes RK, Dagdas YF, Tregidgo N, Zess E, Belhaj K, Round A, Bozkurt TO, Kamoun S, Banfield MJ. Structural Basis of Host Autophagy-related Protein 8 (ATG8) Binding by the Irish Potato Famine Pathogen Effector Protein PexRD54. J Biol Chem. 2016 Sep 16;291(38):20270–20282.
  • Kellner R, De la Concepcion JC, Maqbool A, Kamoun S, Dagdas YF. ATG8 expansion: a driver of selective autophagy diversification? Trends in plant science. 2017;22(3):204–214.
  • Norizuki T, Kanazawa T, Minamino N, Tsukaya H, Ueda T. Marchantia polymorpha, a New Model Plant for Autophagy Studies. Front Plant Sci. 2019;10:935.
  • Nguyen TN, Padman BS, Zellner S, Khuu G, Uoselis L, Lam WK, Skulsuppaisarn M, Lindblom RSJ, Watts EM, Behrends C, Lazarou M. ATG4 family proteins drive phagophore growth independently of the LC3/GABARAP lipidation system. Mol Cell. 2021 May 6;81(9):2013–2030 e9.
  • Seo E, Woo J, Park E, Bertolani SJ, Siegel JB, Choi D, Dinesh-Kumar SP. Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy genes in the plant lineage and cross-kingdom processing of ATG8 by ATG4. Autophagy. 2016 Nov;12(11):2054–2068.
  • Zess EK, Jensen C, Cruz-Mireles N, De la Concepcion JC, Sklenar J, Stephani M, Imre R, Roitinger E, Hughes R, Belhaj K. N-terminal β-strand underpins biochemical specialization of an ATG8 isoform. PLoS biology. 2019;17(7):e3000373.
  • Teper-Bamnolker P, Danieli R, Peled-Zehavi H, Belausov E, Abu-Abied M, Avin-Wittenberg T, Sadot E, Eshel D. Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death. Autophagy. 2021 Oct;17(10):3109–3123.
  • Wu F, Watanabe Y, Guo XY, Qi X, Wang P, Zhao HY, Wang Z, Fujioka Y, Zhang H, Ren JQ, Fang TC, Shen YX, Feng W, Hu JJ, Noda NN, Zhang H. Structural Basis of the Differential Function of the Two C. elegans Atg8 Homologs, LGG-1 and LGG-2, in Autophagy. Mol Cell. 2015 Dec 17;60(6):914–29.
  • Wu F, Li Y, Wang F, Noda NN, Zhang H. Differential function of the two Atg4 homologues in the aggrephagy pathway in Caenorhabditis elegans. J Biol Chem. 2012 Aug 24;287(35):29457–67.
  • Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, Lu Q, Huang X, Yang P, Li X, Wang X, Kovacs AL, Yu L, Zhang H. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell. 2010 Jun 11;141(6):1042–55.
  • Zhang H, Wu F, Wang X, Du H, Wang X, Zhang H. The two C. elegans ATG-16 homologs have partially redundant functions in the basal autophagy pathway. Autophagy. 2013 Dec;9(12):1965–74.
  • Liang Q, Yang P, Tian E, Han J, Zhang H. The C. elegans ATG101 homolog EPG-9 directly interacts with EPG-1/Atg13 and is essential for autophagy. Autophagy. 2012 Oct;8(10):1426–33.
  • Yang P, Zhang H. The coiled-coil domain protein EPG-8 plays an essential role in the autophagy pathway in C. elegans. Autophagy. 2011 Feb;7(2):159–65.
  • Lin L, Yang P, Huang X, Zhang H, Lu Q, Zhang H. The scaffold protein EPG-7 links cargo-receptor complexes with the autophagic assembly machinery. J Cell Biol. 2013 Apr 1;201(1):113–29.
  • Lu Q, Yang P, Huang X, Hu W, Guo B, Wu F, Lin L, Kovacs AL, Yu L, Zhang H. The WD40 repeat PtdIns(3) P-bindingprotein EPG-6 regulates progression of omegasomes to autophagosomes. Dev Cell. 2011 Aug 16;21(2):343–57.
  • Wang Z, Miao G, Xue X, Guo X, Yuan C, Wang Z, Zhang G, Chen Y, Feng D, Hu J, Zhang H. The Vici Syndrome Protein EPG5 Is a Rab7 Effector that Determines the Fusion Specificity of Autophagosomes with Late Endosomes/Lysosomes. Mol Cell. 2016 Sep 1;63(5):781–95.
  • Berry DL, Baehrecke EH. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell. 2007 Dec 14;131(6):1137–48.
  • Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A, Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell. 2004 Aug;7(2):179–92.
  • Scott RC, Juhasz G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol. 2007 Jan 9;17(1):1–11.
  • Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell. 2004 Aug;7(2):167–78.
  • Jacomin AC, Nezis IP. Using Fluorescent Reporters to Monitor Autophagy in the Female Germline Cells in Drosophila melanogaster. Methods Mol Biol. 2016;1457:69–78.
  • Nezis IP, Lamark T, Velentzas AD, Rusten TE, Bjorkoy G, Johansen T, Papassideri IS, Stravopodis DJ, Margaritis LH, Stenmark H, Brech A. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy. 2009 Apr;5(3):298–302.
  • Nezis IP, Shravage BV, Sagona AP, Lamark T, Bjorkoy G, Johansen T, Rusten TE, Brech A, Baehrecke EH, Stenmark H. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J Cell Biol. 2010 Aug 23;190(4):523–31.
  • Betran E, Thornton K, Long M. Retroposed new genes out of the X in Drosophila. Genome Res. 2002 Dec;12(12):1854–9.
  • Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 2010 Jun 2;29(11):1792–802.
  • Jatana N, Ascher DB, Pires DEV, Gokhale RS, Thukral L. Human LC3 and GABARAP subfamily members achieve functional specificity via specific structural modulations. Autophagy. 2019 Apr 14:1–17.
  • Satoo K, Noda NN, Kumeta H, Fujioka Y, Mizushima N, Ohsumi Y, Inagaki F. The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J. 2009 May 6;28(9):1341–50.
  • Skytte Rasmussen M, Mouilleron S, Kumar Shrestha B, Wirth M, Lee R, Bowitz Larsen K, Abudu Princely Y, O’Reilly N, Sjottem E, Tooze SA, Lamark T, Johansen T. ATG4B contains a C-terminal LIR motif important for binding and efficient cleavage of mammalian orthologs of yeast Atg8. Autophagy. 2017 May 04;13(5):834–853.
  • Alemu EA, Lamark T, Torgersen KM, Birgisdottir AB, Larsen KB, Jain A, Olsvik H, Overvatn A, Kirkin V, Johansen T. ATG8 Family Proteins Act as Scaffolds for Assembly of the ULK Complex: SEQUENCE REQUIREMENTS FOR LC3-INTERACTING REGION (LIR) MOTIFS. J Biol Chem. 2012 Nov 16;287(47):39275–90.
  • Birgisdottir AB, Mouilleron S, Bhujabal Z, Wirth M, Sjottem E, Evjen G, Zhang W, Lee R, O’Reilly N, Tooze SA, Lamark T, Johansen T. Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs. Autophagy. 2019 Aug;15(8):1333–1355.
  • Bozic M, van den Bekerom L, Milne BA, Goodman N, Roberston L, Prescott AR, Macartney TJ, Dawe N, McEwan DG. A conserved ATG2-GABARAP family interaction is critical for phagophore formation. EMBO Rep. 2020 Mar 4;21(3):e48412.
  • Kraft C, Kijanska M, Kalie E, Siergiejuk E, Lee SS, Semplicio G, Stoffel I, Brezovich A, Verma M, Hansmann I, Ammerer G, Hofmann K, Tooze S, Peter M. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J. 2012 Aug 10;31(18):3691–703.
  • Rogov VV, Stolz A, Ravichandran AC, Rios‐Szwed DO, Suzuki H, Kniss A, Löhr F, Wakatsuki S, Dötsch V, Dikic I, Dobson RCJ, McEwan DG. Structural and functional analysis of the GABARAP interaction motif (GIM). EMBO reports. 2017;18(8):1382–1396.
  • Wirth M, Zhang W, Razi M, Nyoni L, Joshi D, O’Reilly N, Johansen T, Tooze SA, Mouilleron S. Molecular determinants regulating selective binding of autophagy adapters and receptors to ATG8 proteins. Nat Commun. 2019 May 3;10(1):2055.
  • Nguyen TN, Padman BS, Usher J, Oorschot V, Ramm G, Lazarou M. Atg8 family LC3/GABARAP proteins are crucial for autophagosome-lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation. J Cell Biol. 2016 Dec 19;215(6):857–874.
  • Vaites LP, Paulo JA, Huttlin EL, Harper JW. Systematic Analysis of Human Cells Lacking ATG8 Proteins Uncovers Roles for GABARAPs and the CCZ1/MON1 Regulator C18orf8/RMC1 in Macroautophagic and Selective Autophagic Flux. Mol Cell Biol. 2018 Jan 1;38(1):e00392–17.
  • Szalai P, Hagen LK, Saetre F, Luhr M, Sponheim M, Overbye A, Mills IG, Seglen PO, Engedal N. Autophagic bulk sequestration of cytosolic cargo is independent of LC3, but requires GABARAPs. Exp Cell Res. 2015 Apr 10;333(1):21–38.
  • Tomczyk S, Suknovic N, Schenkelaars Q, Wenger Y, Ekundayo K, Buzgariu W, Bauer C, Fischer K, Austad S, Galliot B. Deficient autophagy in epithelial stem cells drives aging in the freshwater cnidarian Hydra. Development. 2020 Jan 23;147(2).
  • Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, Kominami E, Yamane T, Tanaka K, Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem. 2008 Aug 15;283(33):22847–57.
  • Noda NN, Kumeta H, Nakatogawa H, Satoo K, Adachi W, Ishii J, Fujioka Y, Ohsumi Y, Inagaki F. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells. 2008 Dec;13(12):1211–8.
  • Johansen T, Birgisdottir AB, Huber J, Kniss A, Dotsch V, Kirkin V, Rogov VV. Methods for Studying Interactions Between Atg8/LC3/GABARAP and LIR-Containing Proteins. Methods Enzymol. 2017;587:143–169.
  • Rozenknop A, Rogov VV, Rogova NY, Löhr F, Güntert P, Dikic I, Dötsch V. Characterization of the interaction of GABARAPL-1 with the LIR motif of NBR1. Journal of molecular biology. 2011;410(3):477–487.
  • Rogov VV, Suzuki H, Fiskin E, Wild P, Kniss A, Rozenknop A, Kato R, Kawasaki M, McEwan DG, Löhr F. Structural basis for phosphorylation-triggered autophagic clearance of Salmonella. Biochemical Journal. 2013;454(3):459–466.
  • Abert C, Kontaxis G, Martens S. Accessory Interaction Motifs in the Atg19 Cargo Receptor Enable Strong Binding to the Clustered Ubiquitin-related Atg8 Protein. J Biol Chem. 2016 Sep 2;291(36):18799–808.
  • Farre JC, Burkenroad A, Burnett SF, Subramani S. Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep. 2013 May;14(5):441–9.
  • Li J, Zhu R, Chen K, Zheng H, Zhao H, Yuan C, Zhang H, Wang C, Zhang M. Potent and specific Atg8-targeting autophagy inhibitory peptides from giant ankyrins. Nature chemical biology. 2018 Aug;14(8):778–787.
  • Mochida K, Yamasaki A, Matoba K, Kirisako H, Noda NN, Nakatogawa H. Super-assembly of ER-phagy receptor Atg40 induces local ER remodeling at contacts with forming autophagosomal membranes. Nat Commun. 2020 Jul 3;11(1):3306.
  • Paz Y, Elazar Z, Fass D. Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J Biol Chem. 2000 Aug 18;275(33):25445–50.
  • Coyle JE, Qamar S, Rajashankar KR, Nikolov DB. Structure of GABARAP in two conformations: implications for GABAA receptor localization and tubulin binding. Neuron. 2002;33(1):63–74.
  • Krichel C, Möckel C, Schillinger O, Huesgen PF, Sticht H, Strodel B, Weiergräber OH, Willbold D, Neudecker P. Solution structure of the autophagy-related protein LC3C reveals a polyproline II motif on a mobile tether with phosphorylation site. Scientific reports. 2019;9(1):1–15.
  • Stangler T, Mayr LM, Willbold D. Solution Structure of Human GABAA Receptor-associated Protein GABARAP IMPLICATIONS FOR BIOLOGICAL FUNCTION AND ITS REGULATION. Journal of Biological Chemistry. 2002;277(16):13363–13366.
  • Weidberg H, Shpilka T, Shvets E, Abada A, Shimron F, Elazar Z. LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Developmental cell. 2011;20(4):444–454.
  • Chu CT, Ji J, Dagda RK, Jiang JF, Tyurina YY, Kapralov AA, Tyurin VA, Yanamala N, Shrivastava IH, Mohammadyani D. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nature cell biology. 2013;15(10):1197–1205.
  • Thielmann Y, Mohrlüder J, Koenig BW, Stangler T, Hartmann R, Becker K, Höltje HD, Willbold D. An indole‐binding site is a major determinant of the ligand specificity of the GABA type A receptor‐associated protein GABARAP. Chembiochem. 2008;9(11):1767–1775.
  • Cook WJ, Jeffrey LC, Kasperek E, Pickart CM. Structure of tetraubiquitin shows how multiubiquitin chains can be formed. Journal of molecular biology. 1994;236(2):601–609.
  • Marshall RS, Hua Z, Mali S, McLoughlin F, Vierstra RD. ATG8-Binding UIM Proteins Define a New Class of Autophagy Adaptors and Receptors. Cell. 2019 Apr 18;177(3):766–781 e24.
  • Kuznetsov SA, Gelfand VI. 18 kDa microtubule‐associated protein: identification as a new light chain (LC‐3) of microtubule‐associated protein 1 (MAP‐1). FEBS letters. 1987;212(1):145–148.
  • Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW. GABA A-receptor-associated protein links GABA A receptors and the cytoskeleton. Nature. 1999;397(6714):69–72.
  • Grunwald DS, Otto NM, Park J-M, Song D, Kim D-H. GABARAPs and LC3s have opposite roles in regulating ULK1 for autophagy induction. Autophagy. 2020;16(4):600–614.
  • Joachim J, Jefferies HB, Razi M, Frith D, Snijders AP, Chakravarty P, Judith D, Tooze SA. Activation of ULK kinase and autophagy by GABARAP trafficking from the centrosome is regulated by WAC and GM130. Mol Cell. 2015;60(6):899–913.
  • Holdgaard SG, Cianfanelli V, Pupo E, Lambrughi M, Lubas M, Nielsen JC, Eibes S, Maiani E, Harder LM, Wesch N, Foged MM, Maeda K, Nazio F, de la Ballina LR, Dotsch V, Brech A, Frankel LB, Jaattela M, Locatelli F, Barisic M, Andersen JS, Bekker-Jensen S, Lund AH, Rogov VV, Papaleo E, Lanzetti L, De Zio D, Cecconi F. Selective autophagy maintains centrosome integrity and accurate mitosis by turnover of centriolar satellites. Nat Commun. 2019 Sep 13;10(1):4176.
  • Joachim J, Razi M, Judith D, Wirth M, Calamita E, Encheva V, Dynlacht BD, Snijders AP, O’Reilly N, Jefferies HB. Centriolar satellites control GABARAP ubiquitination and GABARAP-mediated autophagy. Current Biology. 2017;27(14):2123–2136. e7.
  • von Muhlinen N, Akutsu M, Ravenhill BJ, Foeglein A, Bloor S, Rutherford TJ, Freund SM, Komander D, Randow F. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol Cell. 2012 Nov 9;48(3):329–42.
  • Bu F, Yang M, Guo X, Huang W, Chen L. Multiple functions of ATG8 family proteins in plant autophagy. Frontiers in Cell and Developmental Biology. 2020;8:466.
  • Suzuki H, Tabata K, Morita E, Kawasaki M, Kato R, Dobson RC, Yoshimori T, Wakatsuki S. Structural basis of the autophagy-related LC3/Atg13 LIR complex: recognition and interaction mechanism. Structure. 2014;22(1):47–58.
  • Rogov VV, Suzuki H, Marinković M, Lang V, Kato R, Kawasaki M, Buljubašić M, Šprung M, Rogova N, Wakatsuki S. Phosphorylation of the mitochondrial autophagy receptor Nix enhances its interaction with LC3 proteins. Scientific reports. 2017;7(1):1–12.
  • Rahman A, Lorincz P, Gohel R, Nagy A, Csordas G, Zhang Y, Juhasz G, Nezis IP. GMAP is an Atg8a-interacting protein that regulates Golgi turnover in Drosophila. Cell Rep. 2022 May 31;39(9):110903.
  • Tusco R, Jacomin AC, Jain A, Penman BS, Larsen KB, Johansen T, Nezis IP. Kenny mediates selective autophagic degradation of the IKK complex to control innate immune responses. Nat Commun. 2017 Nov 2;8(1):1264.
  • Wesch N, Kirkin V, Rogov VV. Atg8-Family Proteins-Structural Features and Molecular Interactions in Autophagy and Beyond. Cells. 2020 Sep 1;9(9).
  • Shrestha BK, Rasmussen MS, Abudu YP, Bruun J-A, Larsen KB, Alemu EA, Sjøttem E, Lamark T, Johansen T. NIMA-related kinase 9–mediated phosphorylation of the microtubule-associated LC3B protein at Thr-50 suppresses selective autophagy of p62/sequestosome 1. Journal of Biological Chemistry. 2020;295(5):1240–1260.
  • Wilkinson DS, Jariwala JS, Anderson E, Mitra K, Meisenhelder J, Chang JT, Ideker T, Hunter T, Nizet V, Dillin A. Phosphorylation of LC3 by the Hippo kinases STK3/STK4 is essential for autophagy. Molecular cell. 2015;57(1):55–68.
  • Huber J, Obata M, Gruber J, Akutsu M, Löhr F, Rogova N, Güntert P, Dikic I, Kirkin V, Komatsu M. An atypical LIR motif within UBA5 (ubiquitin like modifier activating enzyme 5) interacts with GABARAP proteins and mediates membrane localization of UBA5. Autophagy. 2020;16(2):256–270.
  • Olsvik HL, Lamark T, Takagi K, Larsen KB, Evjen G, Overvatn A, Mizushima T, Johansen T. FYCO1 Contains a C-terminally Extended, LC3A/B-preferring LC3-interacting Region (LIR) Motif Required for Efficient Maturation of Autophagosomes during Basal Autophagy. J Biol Chem. 2015 Dec 04;290(49):29361–74.
  • Shvets E, Fass E, Scherz-Shouval R, Elazar Z. The N-terminus and Phe52 residue of LC3 recruit p62/SQSTM1 into autophagosomes. J Cell Sci. 2008 Aug 15;121(Pt 16):2685–95.
  • Cheng X, Wang Y, Gong Y, Li F, Guo Y, Hu S, Liu J, Pan L. Structural basis of FYCO1 and MAP1LC3A interaction reveals a novel binding mode for Atg8-family proteins. Autophagy. 2016 Aug 2;12(8):1330–9.
  • Lystad AH, Ichimura Y, Takagi K, Yang Y, Pankiv S, Kanegae Y, Kageyama S, Suzuki M, Saito I, Mizushima T, Komatsu M, Simonsen A. Structural determinants in GABARAP required for the selective binding and recruitment of ALFY to LC3B-positive structures. EMBO Rep. 2014 May;15(5):557–65.
  • Turco E, Witt M, Abert C, Bock-Bierbaum T, Su MY, Trapannone R, Sztacho M, Danieli A, Shi X, Zaffagnini G, Gamper A, Schuschnig M, Fracchiolla D, Bernklau D, Romanov J, Hartl M, Hurley JH, Daumke O, Martens S. FIP200 Claw Domain Binding to p62 Promotes Autophagosome Formation at Ubiquitin Condensates. Mol Cell. 2019 Feb 26.
  • Zhou Z, Liu J, Fu T, Wu P, Peng C, Gong X, Wang Y, Zhang M, Li Y, Wang Y, Xu X, Li M, Pan L. Phosphorylation regulates the binding of autophagy receptors to FIP200 Claw domain for selective autophagy initiation. Nat Commun. 2021 Mar 10;12(1):1570.
  • Smith MD, Harley ME, Kemp AJ, Wills J, Lee M, Arends M, von Kriegsheim A, Behrends C, Wilkinson S. CCPG1 Is a Non-canonical Autophagy Cargo Receptor Essential for ER-Phagy and Pancreatic ER Proteostasis. Dev Cell. 2018 Jan 22;44(2):217–232 e11.
  • Ravenhill BJ, Boyle KB, von Muhlinen N, Ellison CJ, Masson GR, Otten EG, Foeglein A, Williams R, Randow F. The Cargo Receptor NDP52 Initiates Selective Autophagy by Recruiting the ULK Complex to Cytosol-Invading Bacteria. Mol Cell. 2019 Feb 28.
  • Gammoh N, Florey O, Overholtzer M, Jiang X. Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and -independent autophagy. Nat Struct Mol Biol. 2013 Feb;20(2):144–9.
  • Nishimura T, Kaizuka T, Cadwell K, Sahani MH, Saitoh T, Akira S, Virgin HW, Mizushima N. FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep. 2013 Mar 1;14(3):284–91.
  • Popelka H, Klionsky DJ. The RB1CC1 Claw-binding motif: a new piece in the puzzle of autophagy regulation. Autophagy. 2022 Feb;18(2):237–239.
  • Gohel R, Kournoutis A, Petridi S, Nezis IP. Molecular mechanisms of selective autophagy in Drosophila. Int Rev Cell Mol Biol. 2020;354:63–105.
  • Tsapras P, Petridi S, Chan S, Geborys M, Jacomin AC, Sagona AP, Meier P, Nezis IP. Selective autophagy controls innate immune response through a TAK1/TAB2/SH3PX1 axis. Cell Rep. 2022 Jan 25;38(4):110286.
  • Birgisdottir AB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci. 2013;126:3237–3247.
  • Sawa-Makarska J, Abert C, Romanov J, Zens B, Ibiricu I, Martens S. Cargo binding to Atg19 unmasks further Atg8-binding sites to mediate membrane-cargo apposition during selective autophagy. Nat Cell Biol. 2014;16.
  • Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005 Nov 14;171:603–614.
  • Ciuffa R, Lamark T, Tarafder AK, Guesdon A, Rybina S, Hagen WJ, Johansen T, Sachse C. The Selective Autophagy Receptor p62 Forms a Flexible Filamentous Helical Scaffold. Cell Rep. 2015 May 5;11(5):748–58.
  • Wurzer B, Zaffagnini G, Fracchiolla D, Turco E, Abert C, Romanov J, Martens S. Oligomerization of p62 allows for selection of ubiquitinated cargo and isolation membrane during selective autophagy. Elife. 2015 Sep 28;4:e08941.
  • Keown JR, Black MM, Ferron A, Yap M, Barnett MJ, Pearce FG, Stoye JP, Goldstone DC. A helical LC3-interacting region mediates the interaction between the retroviral restriction factor Trim5alpha and mammalian autophagy-related ATG8 proteins. J Biol Chem. 2018 Nov 23;293(47):18378–18386.
  • Mandell MA, Jain A, Arko-Mensah J, Chauhan S, Kimura T, Dinkins C, Silvestri G, Munch J, Kirchhoff F, Simonsen A, Wei Y, Levine B, Johansen T, Deretic V. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev Cell. 2014 Aug 25;30(4):394–409.
  • Ma P, Schwarten M, Schneider L, Boeske A, Henke N, Lisak D, Weber S, Mohrluder J, Stoldt M, Strodel B, Methner A, Hoffmann S, Weiergraber OH, Willbold D. Interaction of Bcl-2 with the autophagy-related GABAA receptor-associated protein (GABARAP): biophysical characterization and functional implications. J Biol Chem. 2013 Dec 27;288(52):37204–15.
  • Habisov S, Huber J, Ichimura Y, Akutsu M, Rogova N, Loehr F, McEwan DG, Johansen T, Dikic I, Doetsch V, Komatsu M, Rogov VV, Kirkin V. Structural and Functional Analysis of a Novel Interaction Motif within UFM1-activating Enzyme 5 (UBA5) Required for Binding to Ubiquitin-like Proteins and Ufmylation. J Biol Chem. 2016 Apr 22;291(17):9025–41.
  • Kwon DH, Kim L, Kim BW, Kim JH, Roh KH, Choi EJ, Song HK. A novel conformation of the LC3-interacting region motif revealed by the structure of a complex between LC3B and RavZ. Biochem Biophys Res Commun. 2017 Aug 26;490(3):1093–1099.
  • Goodwin JM, Walkup WGt, Hooper K, Li T, Kishi-Itakura C, Ng A, Lehmberg T, Jha A, Kommineni S, Fletcher K, Garcia-Fortanet J, Fan Y, Tang Q, Wei M, Agrawal A, Budhe SR, Rouduri SR, Baird D, Saunders J, Kiselar J, Chance MR, Ballabio A, Appleton BA, Brumell JH, Florey O, Murphy LO. GABARAP sequesters the FLCN-FNIP tumor suppressor complex to couple autophagy with lysosomal biogenesis. Sci Adv. 2021 Oct;7(40):eabj2485.
  • Farnung J, Muhar M, Liang JR, Tolmachova KA, Benoit RM, Corn JE, Bode JW. Human ATG3 contains a non-canonical LIR motif crucial for its enzymatic activity in autophagy. bioRxiv. 2022:2022.08.02.502437.
  • Chino H, Yamasaki A, Ode KL, Ueda HR, Noda NN, Mizushima N. Phosphorylation by casein kinase 2 enhances the interaction between ER-phagy receptor TEX264 and ATG8 proteins. EMBO Rep. 2022 Jun 7;23(6):e54801.
  • Di Rita A, Peschiaroli A, Pasquale D, Strobbe D, Hu Z, Gruber J, Nygaard M, Lambrughi M, Melino G, Papaleo E. HUWE1 E3 ligase promotes PINK1/PARKIN-independent mitophagy by regulating AMBRA1 activation via IKKα. Nature communications. 2018;9(1):1–18.
  • Kuang Y, Ma K, Zhou C, Ding P, Zhu Y, Chen Q, Xia B. Structural basis for the phosphorylation of FUNDC1 LIR as a molecular switch of mitophagy. Autophagy. 2016;12(12):2363–2373.
  • Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, Dotsch V, Bumann D, Dikic I. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth [Research Support, Non-U.S. Gov’t]. Science. 2011 Jul 8;333(6039):228–33.
  • Wirth M, Mouilleron S, Zhang W, Sjottem E, Princely Abudu Y, Jain A, Lauritz Olsvik H, Bruun JA, Razi M, Jefferies HBJ, Lee R, Joshi D, O’Reilly N, Johansen T, Tooze SA. Phosphorylation of the LIR Domain of SCOC Modulates ATG8 Binding Affinity and Specificity. J Mol Biol. 2021 Jun 25;433(13):166987.
  • Zhou J, Rasmussen NL, Olsvik HL, Akimov V, Hu Z, Evjen G, Kaeser-Pebernard S, Sankar DS, Roubaty C, Verlhac P, van de Beck N, Reggiori F, Abudu YP, Blagoev B, Lamark T, Johansen T, Dengjel J. TBK1 phosphorylation activates LIR-dependent degradation of the inflammation repressor TNIP1. J Cell Biol. 2023 Feb 6;222(2).
  • Zhu Y, Massen S, Terenzio M, Lang V, Chen-Lindner S, Eils R, Novak I, Dikic I, Hamacher-Brady A, Brady NR. Modulation of Serines 17 and 24 in the LC3-interacting Region of Bnip3 Determines Pro-survival Mitophagy versus Apoptosis. J Biol Chem. 2013 Jan 11;288(2):1099–113.
  • Sakurai S, Tomita T, Shimizu T, Ohto U. The crystal structure of mouse LC3B in complex with the FYCO1 LIR reveals the importance of the flanking region of the LIR motif. Acta Crystallogr F Struct Biol Commun. 2017 Mar 1;73(Pt 3):130–137.
  • Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, Bilusic I, Theurillat JP, Overvatn A, Ishii T, Elazar Z, Komatsu M, Dikic I, Johansen T. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell. 2009 Feb 27;33(4):505–16.
  • Mao J, Xia Q, Liu C, Ying Z, Wang H, Wang G. A critical role of Hrd1 in the regulation of optineurin degradation and aggresome formation. Hum Mol Genet. 2017 May 15;26(10):1877–1889.
  • Hamacher-Brady A, Brady NR. Mitophagy programs: mechanisms and physiological implications of mitochondrial targeting by autophagy. Cell Mol Life Sci. 2016 Feb;73(4):775–95.
  • Chen G, Han Z, Feng D, Chen Y, Chen L, Wu H, Huang L, Zhou C, Cai X, Fu C, Duan L, Wang X, Liu L, Liu X, Shen Y, Zhu Y, Chen Q. A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol Cell. 2014 May 8;54(3):362–77.
  • Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P, Ma Q, Zhu C, Wang R, Qi W, Huang L, Xue P, Li B, Wang X, Jin H, Wang J, Yang F, Liu P, Zhu Y, Sui S, Chen Q. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells [Research Support, Non-U.S. Gov’t]. Nat Cell Biol. 2012 Feb;14(2):177–85.
  • Wu W, Tian W, Hu Z, Chen G, Huang L, Li W, Zhang X, Xue P, Zhou C, Liu L, Zhu Y, Zhang X, Li L, Zhang L, Sui S, Zhao B, Feng D. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep. 2014 May;15(5):566–75.
  • Di Lorenzo G, Iavarone F, Maddaluno M, Plata-Gomez AB, Aureli S, Quezada Meza CP, Cinque L, Palma A, Reggio A, Cirillo C, Sacco F, Stolz A, Napolitano G, Marin O, Pinna LA, Ruzzene M, Limongelli V, Efeyan A, Grumati P, Settembre C. Phosphorylation of FAM134C by CK2 controls starvation-induced ER-phagy. Sci Adv. 2022 Sep 2;8(35):eabo1215.
  • Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature. 2010;466(7302):68–76.
  • Amar N, Lustig G, Ichimura Y, Ohsumi Y, Elazar Z. Two newly identified sites in the ubiquitin-like protein Atg8 are essential for autophagy. EMBO Rep. 2006 Jun;7(6):635–42.
  • Nthiga TM, Kumar Shrestha B, Sjottem E, Bruun JA, Bowitz Larsen K, Bhujabal Z, Lamark T, Johansen T. CALCOCO1 acts with VAMP-associated proteins to mediate ER-phagy. EMBO J. 2020 Aug 3;39(15):e103649.
  • Abreu S, Kriegenburg F, Gomez-Sanchez R, Mari M, Sanchez-Wandelmer J, Skytte Rasmussen M, Soares Guimaraes R, Zens B, Schuschnig M, Hardenberg R, Peter M, Johansen T, Kraft C, Martens S, Reggiori F. Conserved Atg8 recognition sites mediate Atg4 association with autophagosomal membranes and Atg8 deconjugation. EMBO Rep. 2017 May;18(5):765–780.
  • Jain A, Rusten TE, Katheder N, Elvenes J, Bruun JA, Sjottem E, Lamark T, Johansen T. p62/sequestosome-1, autophagy-related gene 8 and autophagy in Drosophila are regulated by Nuclear factor erythroid 2-related factor 2 (NRF2), independent of transcription factor TFEB. J Biol Chem. 2015 Apr 30.
  • Kalvari I, Tsompanis S, Mulakkal NC, Osgood R, Johansen T, Nezis IP, Promponas VJ. iLIR: A web resource for prediction of Atg8-family interacting proteins. Autophagy. 2014 May;10(5):913–25.
  • Jacomin AC, Samavedam S, Charles H, Nezis IP. iLIR@viral: A web resource for LIR motif-containing proteins in viruses. Autophagy. 2017 Oct 3;13(10):1782–1789.
  • Jacomin AC, Samavedam S, Promponas V, Nezis IP. iLIR database: A web resource for LIR motif-containing proteins in eukaryotes. Autophagy. 2016 Oct 2;12(10):1945–1953.
  • Chatzichristofi A, Sagris V, Pallaris A, Eftychiou M, Kalvari I, Price N, Theodosiou T, Iliopoulos I, Nezis IP, Promponas VJ. LIRcentral: a manually curated online database of experimentally validated functional LIR-motifs. bioRxiv. 2022:2022.06.21.496832.
  • Ibrahim T, Khandare V, Mirkin FG, Tumtas Y, Bubeck D, Bozkurt TO. AF2-multimer guided high accuracy prediction of typical and atypical ATG8 binding motifs. bioRxiv. 2022:2022.09.25.509395.
  • Weiergräber OH, Stangler T, Thielmann Y, Mohrlüder J, Wiesehan K, Willbold D. Ligand binding mode of GABAA receptor-associated protein. Journal of molecular biology. 2008;381(5):1320–1331.
  • Stolz A, Putyrski M, Kutle I, Huber J, Wang C, Major V, Sidhu SS, Youle RJ, Rogov VV, Dötsch V. Fluorescence‐based ATG 8 sensors monitor localization and function of LC 3/GABARAP proteins. The EMBO journal. 2017;36(4):549–564.
  • Picchianti L, de Medina Hernández VS, Zhan N, Irwin NAT, Stephani M, Hornegger H, Beveridge R, Sawa-Makarska J, Lendl T, Grujic N, Martens S, Richards TA, Clausen T, Ramundo S, Karagöz GE, Dagdas Y. Shuffled ATG8 interacting motifs form an ancestral bridge between UFMylation and C53-mediated autophagy. bioRxiv. 2022:2022.04.26.489478.
  • Stephani M, Picchianti L, Gajic A, Beveridge R, Skarwan E, Sanchez de Medina Hernandez V, Mohseni A, Clavel M, Zeng Y, Naumann C, Matuszkiewicz M, Turco E, Loefke C, Li B, Durnberger G, Schutzbier M, Chen HT, Abdrakhmanov A, Savova A, Chia KS, Djamei A, Schaffner I, Abel S, Jiang L, Mechtler K, Ikeda F, Martens S, Clausen T, Dagdas Y. A cross-kingdom conserved ER-phagy receptor maintains endoplasmic reticulum homeostasis during stress. Elife. 2020 Aug 27;9.
  • Ma P, Schillinger O, Schwarten M, Lecher J, Hartmann R, Stoldt M, Mohrlüder J, Olubiyi O, Strodel B, Willbold D. Conformational polymorphism in autophagy-related protein GATE-16. Biochemistry. 2015;54(35):5469–5479.
  • Shvets E, Abada A, Weidberg H, Elazar Z. Dissecting the involvement of LC3B and GATE-16 in p62 recruitment into autophagosomes. Autophagy. 2011;7(7):683–688.
  • Chen C, Li J-G, Chen Y, Huang P, Wang Y, Liu-Chen L-Y. GEC1 interacts with the κ opioid receptor and enhances expression of the receptor. Journal of Biological Chemistry. 2006;281(12):7983–7993.
  • Kneussel M, Haverkamp S, Fuhrmann JC, Wang H, Wässle H, Olsen RW, Betz H. The γ-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proceedings of the National Academy of Sciences. 2000;97(15):8594–8599.
  • Yang Z, Wilkie-Grantham RP, Yanagi T, Shu CW, Matsuzawa S, Reed JC. ATG4B (Autophagin-1) phosphorylation modulates autophagy. J Biol Chem. 2015 Oct 30;290(44):26549–61.
  • Fujiwara N, Usui T, Ohama T, Sato K. Regulation of Beclin 1 Protein Phosphorylation and Autophagy by Protein Phosphatase 2A (PP2A) and Death-associated Protein Kinase 3 (DAPK3). J Biol Chem. 2016 May 13;291(20):10858–66.
  • Kim J, Kim YC, Fang C, Russell RC, Kim JH, Fan W, Liu R, Zhong Q, Guan KL. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell. 2013 Jan 17; 152 (1–2): 290–303.
  • Wei Y, An Z, Zou Z, Sumpter R, Su M, Zang X, Sinha S, Gaestel M, Levine B. The stress-responsive kinases MAPKAPK2/MAPKAPK3 activate starvation-induced autophagy through Beclin 1 phosphorylation. Elife. 2015 Feb 18;4.
  • Poole LP, Bock-Hughes A, Berardi DE, Macleod KF. ULK1 promotes mitophagy via phosphorylation and stabilization of BNIP3. Sci Rep. 2021 Oct 15;11(1):20526.
  • Wu H, Xue D, Chen G, Han Z, Huang L, Zhu C, Wang X, Jin H, Wang J, Zhu Y, Liu L, Chen Q. The BCL2L1 and PGAM5 axis defines hypoxia-induced receptor-mediated mitophagy. Autophagy. 2014 Oct 1;10(10):1712–25.
  • Egan DF, Chun MG, Vamos M, Zou H, Rong J, Miller CJ, Lou HJ, Raveendra-Panickar D, Yang CC, Sheffler DJ, Teriete P, Asara JM, Turk BE, Cosford ND, Shaw RJ. Small Molecule Inhibition of the Autophagy Kinase ULK1 and Identification of ULK1 Substrates. Mol Cell. 2015 Jul 16;59(2):285–97.

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