Members of the autophagy class III phosphatidylinositol 3-kinase complex I interact with GABARAP and GABARAPL1 via LIR motifs

References

• Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013 Dec;14(12):759–774. PubMed PMID: 24201109.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol. 2011;27:107–132. PubMed PMID: 21801009.
   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. PubMed PMID: 24366339; PubMed Central PMCID: PMCPMC3879710.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi C, Inoue K, et al. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell. 2008 Dec;19(12):5360–5372. PubMed PMID: 18843052; PubMed Central PMCID: PMCPMC2592660.
   PubMed Web of Science ®Google Scholar
• Kihara A, Noda T, Ishihara N, et al. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol. 2001 Feb 5;152(3):519–530. PubMed PMID: 11157979; PubMed Central PMCID: PMCPMC2196002.
   PubMed Web of Science ®Google Scholar
• Rostislavleva K, Soler N, Ohashi Y, et al. Structure and flexibility of the endosomal Vps34 complex reveals the basis of its function on membranes. Science. 2015 Oct 9;350(6257):aac7365. PubMed PMID: 26450213; PubMed Central PMCID: PMCPMC4601532.
   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. PubMed PMID: 18725538; PubMed Central PMCID: PMCPMC2518708.
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HE, et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell. 2014 Jul 17;55(2):238–252. PubMed PMID: 24954904; PubMed Central PMCID: PMCPMC4104028.
   PubMed Web of Science ®Google Scholar
• Proikas-Cezanne T, Takacs Z, Donnes P, et al. WIPI proteins: essential PtdIns3P effectors at the nascent autophagosome. J Cell Sci. 2015 Jan 15;128(2):207–217. PubMed PMID: 25568150.
   PubMed Web of Science ®Google Scholar
• Heenan EJ, Vanhooke JL, Temple BR, et al. Structure and function of Vps15 in the endosomal G protein signaling pathway. Biochemistry. 2009 Jul 14;48(27):6390–6401. PubMed PMID: 19445518; PubMed Central PMCID: PMCPMC2740480.
   PubMed Web of Science ®Google Scholar
• Panaretou C, Domin J, Cockcroft S, et al. Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex. J Biol Chem. 1997 Jan 24;272(4):2477–2485. PubMed PMID: 8999962.
   PubMed Web of Science ®Google Scholar
• Backer JM. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J. 2008 Feb 15;410(1):1–17. PubMed PMID: 18215151.
   PubMed Web of Science ®Google Scholar
• Huang W, Choi W, Hu W, et al. Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein. Cell Res. 2012 Mar;22(3):473–489. PubMed PMID: 22310240; PubMed Central PMCID: PMCPMC3292424.
   PubMed Web of Science ®Google Scholar
• Diao J, Liu R, Rong Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015 Apr 23;520(7548):563–566. PubMed PMID: 25686604; PubMed Central PMCID: PMCPMC4442024.
   PubMed Web of Science ®Google Scholar
• Fan W, Nassiri A, Zhong Q. Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc Natl Acad Sci U S A. 2011 May 10;108(19):7769–7774. PubMed PMID: 21518905; PubMed Central PMCID: PMCPMC3093500.
   PubMed Web of Science ®Google Scholar
• Baskaran S, Carlson LA, Stjepanovic G, et al. Architecture and dynamics of the autophagic phosphatidylinositol 3-kinase complex. Elife. 2014 Dec 09;3. DOI:10.7554/eLife.05115 PubMed PMID: 25490155; PubMed Central PMCID: PMCPMC4281882.
   PubMed Web of Science ®Google Scholar
• Araki Y, Ku WC, Akioka M, et al. Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J Cell Biol. 2013 Oct 28;203(2):299–313. PubMed PMID: 24165940; PubMed Central PMCID: PMCPMC3812978.
   PubMed Web of Science ®Google Scholar
• Cao Y, Wang Y, Abi Saab WF, et al. NRBF2 regulates macroautophagy as a component of Vps34 Complex I. Biochem J. 2014 Jul 15;461(2):315–322. PubMed PMID: 24785657; PubMed Central PMCID: PMCPMC4180102.
   PubMed Web of Science ®Google Scholar
• Lu J, He L, Behrends C, et al. NRBF2 regulates autophagy and prevents liver injury by modulating Atg14L-linked phosphatidylinositol-3 kinase III activity. Nat Commun. 2014 May;22(5):3920. PubMed PMID: 24849286; PubMed Central PMCID: PMCPMC4376476.
   PubMed Web of Science ®Google Scholar
• Zhong Y, Morris DH, Jin L, et al. Nrbf2 protein suppresses autophagy by modulating Atg14L protein-containing Beclin 1-Vps34 complex architecture and reducing intracellular phosphatidylinositol-3 phosphate levels. J Biol Chem. 2014 Sep 19;289(38):26021–26037. PubMed PMID: 25086043; PubMed Central PMCID: PMCPMC4176228.
   PubMed Web of Science ®Google Scholar
• Young LN, Cho K, Lawrence R, et al. Dynamics and architecture of the NRBF2-containing phosphatidylinositol 3-kinase complex I of autophagy. Proc Natl Acad Sci U S A. 2016 Jul 19;113(29):8224–8229. PubMed PMID: 27385829; PubMed Central PMCID: PMCPMC4961193.
   PubMed Web of Science ®Google Scholar
• Sun Q, Fan W, Chen K, et al. Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A. 2008 Dec 09;105(49):19211–19216. PubMed PMID: 19050071; PubMed Central PMCID: PMCPMC2592986.
   PubMed Web of Science ®Google Scholar
• Matsunaga K, Morita E, Saitoh T, et al. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol. 2010 Aug 23;190(4):511–521. PubMed PMID: 20713597; PubMed Central PMCID: PMCPMC2928018.
   PubMed Web of Science ®Google Scholar
• Tan X, Thapa N, Liao Y, et al. PtdIns(4,5)P2 signaling regulates ATG14 and autophagy. Proc Natl Acad Sci U S A. 2016 Sep 27;113(39):10896–10901. PubMed PMID: 27621469; PubMed Central PMCID: PMCPMC5047215.
   PubMed Web of Science ®Google Scholar
• Park JM, Jung CH, Seo M, et al. The ULK1 complex mediates MTORC1 signaling to the autophagy initiation machinery via binding and phosphorylating ATG14. Autophagy. 2016;12(3):547–564. PubMed PMID: 27046250; PubMed Central PMCID: PMCPMC4835982.
   PubMed Web of Science ®Google Scholar
• Park JM, Seo M, Jung CH, et al. ULK1 phosphorylates Ser30 of BECN1 in association with ATG14 to stimulate autophagy induction. Autophagy. 2018 Feb;21:1–14. PubMed PMID: 29313410.
   Google Scholar
• Wold MS, Lim J, Lachance V, et al. ULK1-mediated phosphorylation of ATG14 promotes autophagy and is impaired in Huntington’s disease models. Mol Neurodegener. 2016 Dec 9;11(1):76. PubMed PMID: 27938392; PubMed Central PMCID: PMCPMC5148922.
   PubMed Web of Science ®Google Scholar
• Shpilka T, Weidberg H, Pietrokovski S, et al. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 2011;12(7):226. PubMed PMID: 21867568; PubMed Central PMCID: PMC3218822. eng.
   PubMed Web of Science ®Google Scholar
• Weidberg H, Shvets E, Shpilka T, et al. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. Embo J. 2010 Jun 2;29(11):1792–1802. PubMed PMID: 20418806; PubMed Central PMCID: PMC2885923. eng.
   PubMed Web of Science ®Google Scholar
• Birgisdottir AB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci. 2013;126:3237–3247.
   PubMed Web of Science ®Google Scholar
• Rogov V, Dotsch V, Johansen T, et al. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014 Jan 23;53(2):167–178. PubMed PMID: 24462201.
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Kumanomidou T, Sou YS, et al. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem. 2008 Aug 15;283(33):22847–22857. PubMed PMID: 18524774; eng.
   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 Aug 17;282(33):24131–24145. PubMed PMID: 17580304; eng.
   PubMed Web of Science ®Google Scholar
• Noda NN, Kumeta H, Nakatogawa H, et al. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells. 2008 Dec;13(12):1211–1218. PubMed PMID: 19021777; eng.
   PubMed Web of Science ®Google Scholar
• Noda NN, Ohsumi Y, Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 2010 Apr 2;584(7):1379–1385. PubMed PMID: 20083108; eng.
   PubMed Web of Science ®Google Scholar
• Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014 Jan 1;127(Pt 1):3–9. PubMed PMID: 24345374.
   PubMed Web of Science ®Google Scholar
• Kraft C, Kijanska M, Kalie E, et al. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. Embo J. 2012 Aug 10;31(18):3691–3703. PubMed PMID: 22885598; PubMed Central PMCID: PMC3442273.
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Ohbayashi S, Sakoh-Nakatogawa M, et al. The autophagy-related protein kinase Atg1 interacts with the ubiquitin-like protein Atg8 via the Atg8 family interacting motif to facilitate autophagosome formation. J Biol Chem. 2012 Aug 17;287(34):28503–28507. PubMed PMID: 22778255; PubMed Central PMCID: PMC3436563.
   PubMed Web of Science ®Google Scholar
• Alemu EA, Lamark T, Torgersen KM, et al. 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):39275–39290. PubMed PMID: 23043107; PubMed Central PMCID: PMC3501051.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Noda NN, Nakatogawa H, et al. Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway. J Biol Chem. 2010 Sep 17;285(38):29599–29607. PubMed PMID: 20615880; eng.
   PubMed Web of Science ®Google Scholar
• Abreu S, Kriegenburg F, Gomez-Sanchez R, et al. Conserved Atg8 recognition sites mediate Atg4 association with autophagosomal membranes and Atg8 deconjugation. EMBO Rep. 2017 May;18(5):765–780. PubMed PMID: 28330855; PubMed Central PMCID: PMCPMC5412903.
   PubMed Web of Science ®Google Scholar
• Satoo K, Noda NN, Kumeta H, et al. The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. Embo J. 2009 May 6;28(9):1341–1350. PubMed PMID: 19322194; PubMed Central PMCID: PMC2683054. eng.
   PubMed Web of Science ®Google Scholar
• Skytte Rasmussen M, Mouilleron S, Kumar Shrestha B, et al. 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. PubMed PMID: 28287329; PubMed Central PMCID: PMCPMC5446077.
   PubMed Web of Science ®Google Scholar
• Fogel AI, Dlouhy BJ, Wang C, et al. Role of membrane association and Atg14-dependent phosphorylation in beclin-1-mediated autophagy. Mol Cell Biol. 2013 Sep;33(18):3675–3688. PubMed PMID: 23878393; PubMed Central PMCID: PMCPMC3753860.
   PubMed Web of Science ®Google Scholar
• Kim J, Kim YC, Fang C, et al. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell. 2013 Jan 17;152(1–2):290–303. PubMed PMID: 23332761; PubMed Central PMCID: PMCPMC3587159.
   PubMed Web of Science ®Google Scholar
• Rozenknop A, Rogov VV, Rogova NY, et al. Characterization of the interaction of GABARAPL-1 with the LIR motif of NBR1. J Mol Biol. 2011 Jul 15;410(3):477–487. PubMed PMID: 21620860; eng.
   PubMed Web of Science ®Google Scholar
• Egan DF, Chun MG, Vamos M, et al. Small molecule inhibition of the autophagy kinase ULK1 and identification of ULK1 substrates. Mol Cell. 2015 Jul 16;59(2):285–297. PubMed PMID: 26118643; PubMed Central PMCID: PMCPMC4530630.
   PubMed Web of Science ®Google Scholar
• Lystad AH, Ichimura Y, Takagi K, et al. Structural determinants in GABARAP required for the selective binding and recruitment of ALFY to LC3B-positive structures. EMBO Rep. 2014 May;15(5):557–565. PubMed PMID: 24668264; PubMed Central PMCID: PMC4210083.
   PubMed Web of Science ®Google Scholar
• Olsvik HL, Lamark T, Takagi K, et al. 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 Oct 14. DOI:10.1074/jbc.M115.686915. PubMed PMID: 26468287.
   PubMed Web of Science ®Google Scholar
• Bhujabal Z, Birgisdottir AB, Sjottem E, et al. FKBP8 recruits LC3A to mediate Parkin-independent mitophagy. EMBO Rep. 2017 Jun;18(6):947–961. PubMed PMID: 28381481; PubMed Central PMCID: PMCPMC5452039.
   PubMed Web of Science ®Google Scholar
• Wei Y, An Z, Zou Z, et al. The stress-responsive kinases MAPKAPK2/MAPKAPK3 activate starvation-induced autophagy through Beclin 1 phosphorylation. Elife. 2015 Feb 18;4. DOI:10.7554/eLife.05289 PubMed PMID: 25693418; PubMed Central PMCID: PMCPMC4337728.
   Web of Science ®Google Scholar
• Fujiwara N, Usui T, Ohama T, et al. 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):10858–10866. PubMed PMID: 26994142; PubMed Central PMCID: PMCPMC4865930.
   PubMed Web of Science ®Google Scholar
• Rogov VV, Stolz A, Ravichandran AC, et al. Structural and functional analysis of the GABARAP interaction motif (GIM). EMBO Rep. 2017 Aug;18(8):1382–1396. PubMed PMID: 28655748; PubMed Central PMCID: PMCPMC5538626.
   PubMed Web of Science ®Google Scholar
• Wu F, Watanabe Y, Guo XY, et al. 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):914–929. PubMed PMID: 26687600.
   PubMed Web of Science ®Google Scholar
• Szalai P, Hagen LK, Saetre F, et al. Autophagic bulk sequestration of cytosolic cargo is independent of LC3, but requires GABARAPs. Exp Cell Res. 2015 Apr 10;333(1):21–38. PubMed PMID: 25684710.
   PubMed Web of Science ®Google Scholar
• Nguyen TN, Padman BS, Usher J, et al. 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. PubMed PMID: 27864321; PubMed Central PMCID: PMCPMC5166504.
   PubMed Web of Science ®Google Scholar
• McEwan DG, Popovic D, Gubas A, et al. PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Mol Cell. 2015 Jan 8;57(1):39–54. PubMed PMID: 25498145.
   PubMed Web of Science ®Google Scholar
• Joachim J, Jefferies HB, Razi M, et al. Activation of ULK kinase and autophagy by GABARAP trafficking from the centrosome is regulated by WAC and GM130. Mol Cell. 2015 Dec 17;60(6):899–913. PubMed PMID: 26687599; PubMed Central PMCID: PMCPMC4691241.
   PubMed Web of Science ®Google Scholar
• Hurley JH, Young LN. Mechanisms of autophagy initiation. Annu Rev Biochem. 2017 Mar 15. DOI:10.1146/annurev-biochem-061516-044820. PubMed PMID: 28301741.
   PubMed Web of Science ®Google Scholar
• Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER-mitochondria contact sites. Nature. 2013 Mar 21;495(7441):389–393. PubMed PMID: 23455425.
   PubMed Web of Science ®Google Scholar
• Nath S, Dancourt J, Shteyn V, et al. Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nat Cell Biol. 2014 May;16(5):415–424. PubMed PMID: 24747438; PubMed Central PMCID: PMCPMC4111135.
   PubMed Web of Science ®Google Scholar
• Pankiv S, Alemu EA, Brech A, et al. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol. 2010 Jan 25;188(2):253–269. PubMed PMID: 20100911; PubMed Central PMCID: PMC2812517. eng.
   PubMed Web of Science ®Google Scholar
• Stjepanovic G, Baskaran S, Lin MG, et al. Vps34 kinase domain dynamics regulate the autophagic PI 3-kinase complex. Mol Cell. 2017 Aug 3;67(3):528–534 e3. PubMed PMID: 28757208; PubMed Central PMCID: PMCPMC5573195.
   PubMed Web of Science ®Google Scholar
• Lamark T, Perander M, Outzen H, et al. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem. 2003 Sep 5;278(36):34568–34581. PubMed PMID: 12813044.
   PubMed Web of Science ®Google Scholar
• Johansen T, Birgisdottir AB, Huber J, et al. Methods for studying interactions between Atg8/LC3/GABARAP and LIR-containing proteins. Methods Enzymol. 2017;587:143–169. PubMed PMID: 28253953.
   PubMed Web of Science ®Google Scholar
• Winter G, Lobley CM, Prince SM. Decision making in xia2. Acta Crystallogr D Biol Crystallogr. 2013 Jul;69(Pt 7):1260–1273. PubMed PMID: 23793152; PubMed Central PMCID: PMCPMC3689529.
   PubMedGoogle Scholar
• McCoy AJ, Grosse-Kunstleve RW, Adams PD, et al. Phaser crystallographic software. J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658–674. PubMed PMID: 19461840; PubMed Central PMCID: PMCPMC2483472.
   PubMed Web of Science ®Google Scholar
• Adams PD, Afonine PV, Bunkoczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213–221. PubMed PMID: 20124702; PubMed Central PMCID: PMCPMC2815670.
   PubMed Web of Science ®Google Scholar
• Emsley P, Lohkamp B, Scott WG, et al. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486–501. PubMed PMID: 20383002; PubMed Central PMCID: PMCPMC2852313.
   PubMed Web of Science ®Google Scholar
• Vaguine AA, Richelle J, Wodak SJ. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D Biol Crystallogr. 1999 Jan;55(Pt 1):191–205. PubMed PMID: 10089410.
   PubMedGoogle Scholar