Abstract
This chapter explains in detail the steps of autophagosome formation, focusing mainly on mammals. We will explain how the molecular machinery acts in a coordinated fashion in order to achieve the membrane rearrangements required for autophagosome formation.
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Alemu EA, Lamark T, Torgersen KM et al (2012) ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. J Biol Chem 287:39275–39290. doi:10.1074/jbc.M112.378109
Axe EL, Walker SA, Manifava M et al (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182:685–701. doi:10.1083/jcb.200803137
Backer JM (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410:1–17. doi:10.1042/BJ20071427
Biazik J, Ylä-Anttila P, Vihinen H et al (2015) Ultrastructural relationship of the phagophore with surrounding organelles. Autophagy 11:439–451. doi:10.1080/15548627.2015.1017178
Bjorkoy G (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603–614. doi:10.1083/jcb.200507002
Chakrama FZ, Seguin-Py S, Le Grand JN et al (2014) GABARAPL1 (GEC1) associates with autophagic vesicles. Autophagy 6:495–505. doi:10.4161/auto.6.4.11819
Chan EYW, Longatti A, McKnight NC, Tooze SA (2009) Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol 29:157–171. doi:10.1128/MCB.01082-08
Cheong H, Yorimitsu T, Reggiori F et al (2005) Atg17 Regulates the Magnitude of the Autophagic Response. Mol Biol Cell 16:3438–3453. doi:10.1091/mbc.E04
Chew LH, Setiaputra D, Klionsky DJ, Yip CK (2013) Structural characterization of the Saccharomyces cerevisiae autophagy regulatory complex Atg17-Atg31-Atg29. Autophagy 9:1467–1474. doi:10.4161/auto.25687
Cuervo AM (2011) Chaperone-mediated autophagy: Dice’s ‘wild’ idea about lysosomal selectivity. Nature Reviews. Mol Cell Biol, 12(8), 535–541. http://doi.org/10.1038/nrm3150
Di Bartolomeo S, Corazzari M, Nazio F et al (2010) The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 191:155–168. doi:10.1083/jcb.201002100
Dooley HC, Razi M, Polson HEJ et al (2014) WIPI2 links LC3 Conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 55:238–252. doi:10.1016/j.molcel.2014.05.021
Duke EMH, Razi M, Weston A et al (2014) Imaging endosomes and autophagosomes in whole mammalian cells using correlative cryo-fluorescence and cryo-soft X-ray microscopy (cryo-CLXM). Ultramicroscopy 143:77–87. doi:10.1016/j.ultramic.2013.10.006
Dunlop EA, Hunt DK, Acosta-Jaquez HA et al (2014) ULK1 inhibits mTORC1 signaling, promotes multisite raptor phosphorylation and hinders substrate binding. Autophagy 7:737–747. doi:10.4161/auto.7.7.15491
Fan W, Nassiri A, Zhong Q (2011) Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc Natl Acad Sci USA 108:7769–7774. doi:10.1073/pnas.1016472108
Fujita N, Itoh T, Omori H et al (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 19:2092–2100. doi:10.1091/mbc.E07-12-1257
Funderburk SF, Wang QJ, Yue Z (2010) The Beclin 1–VPS34 complex—at the crossroads of autophagy and beyond. Trends Cell Biol 20:355–362. doi:10.1016/j.tcb.2010.03.002
Gammoh N, Florey O, Overholtzer M, Jiang X (2013) Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and -independent autophagy. Nat Struct Mol Biol 20:144–149. doi:10.1038/nsmb.2475
Ganley IG, Lam DH, Wang J et al (2009) ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297–12305. doi:10.1074/jbc.M900573200
Ge L, Melville D, Zhang M, Schekman R (2013) The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2:e00947. doi:10.7554/eLife.00947
Ge L, Zhang M, Schekman R (2014) Phosphatidylinositol 3-kinase and COPII generate LC3 lipidation vesicles from the ER-Golgi intermediate compartment. eLife 3:e04135. doi:10.7554/eLife.04135
Hailey DW, Rambold AS, Satpute-Krishnan P et al (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141:656–667. doi:10.1016/j.cell.2010.04.009
Hamasaki M, Furuta N, Matsuda A et al (2013) Autophagosomes form at ER–mitochondria contact sites. Nature 495:389–393. doi:10.1038/nature11910
Hanada T, Noda NN, Satomi Y et al (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282:37298–37302. doi:10.1074/jbc.C700195200
Hara T, Takamura A, Kishi C et al (2008) FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181:497–510. doi:10.1083/jcb.200712064
Hayashi-Nishino M, Fujita N, Noda T et al (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 11:1433–1437. doi:10.1038/ncb1991
He H, Dang Y, Dai F et al (2003) Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 278:29278–29287. doi:10.1074/jbc.M303800200
Hosokawa N, Hara T, Kaizuka T et al (2009a) Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20:1981–1991. doi:10.1091/mbc.E08-12-1248
Hosokawa N, Sasaki T, Iemura S-I et al (2009b) Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5:973–979
Huang J, Birmingham CL, Shahnazari S, Shiu J, Zheng YT, Smith AC, Campellone KG, Do Heo W, Gruenheid S, Meyer T, Welch MD, Ktistakis NT, Kim PK, Klionsky DJ, Brumell JH (2011) Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7:17–26
Hurley JH, Schulman BA (2014) Atomistic autophagy: the structures of cellular self-digestion. Cell 157:300–311. doi:10.1016/j.cell.2014.01.070
Ichimura Y, Kirisako T, Takao T et al (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488–492. doi:10.1038/35044114
Ichimura Y, Kumanomidou T, Sou Y-S et al (2008) Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 283:22847–22857. doi:10.1074/jbc.M802182200
Itakura E, Mizushima N (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6:764–776
Itakura E, Kishi C, Inoue K, Mizushima N (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19:5360–5372. doi:10.1091/mbc.E08-01-0080
Itakura E, Kishi-Itakura C, Kishi-Itakura C et al (2012) Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci 125:1488–1499. doi:10.1242/jcs.094110
Jao CC, Ragusa MJ, Stanley RE, Hurley JH (2013) A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proc Natl Acad Sci USA 110:5486–5491. doi:10.1073/pnas.1220306110
Jeffries TR, Dove SK, Michell RH, Parker PJ (2004) PtdIns-specific MPR pathway association of a novel WD40 repeat protein, WIPI49. Mol Biol Cell 15:2652–2663. doi:10.1091/mbc.E03-10-0732
Johansen T, Lamark T (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7:279–296. doi:10.4161/auto.7.3.14487
Johansen T, Lamark T (2014) Selective autophagy goes exclusive. Nat Cell Biol 16:395–397
Jung CH, Jun CB, Ro S-H et al (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992–2003. doi:10.1091/mbc.E08-12-1249
Jung CH, Seo M, Otto NM (2011) ULK1 inhibits the kinase activity of mTORC1 and cell proliferation. Autophagy 1212–1221
Kabeya Y (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728. doi:10.1093/emboj/19.21.5720
Kabeya Y, Mizushima N, Yamamoto A et al (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117:2805–2812. doi:10.1242/jcs.01131
Kakuta S, Yamamoto H, Negishi L, Kondo-Kakuta C, Hayashi N, Ohsumi Y (2012) Atg9 vesicles recruit vesicle-tethering proteins Trs85 and Ypt1 to the autophagosome formation site. J Biol Chem 287:44261–44269. doi:10.1074/jbc.M112.411454
Karanasios E, Stapleton E, Manifava M et al (2013) Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci 126:5224–5238. doi:10.1242/jcs.132415
Kirisako T, Ichimura Y, Okada H et al (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151:263–276. doi:10.1083/jcb.151.2.263
Knævelsrud H, Søreng K, Raiborg C et al (2013) Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J Cell Biol 202:331–349. doi:10.1083/jcb.201205129
Komatsu M, Waguri S, Koike M et al (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131:1149–1163. doi:10.1016/j.cell.2007.10.035
Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N (2013) Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 9:1491–1499. doi:10.4161/auto.25529
Kraft C, Kijanska M, Kalie E et al (2012) Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J 31:3691–3703. doi:10.1038/emboj.2012.225
Ktistakis NT, Karanasios E, Manifava M (2014) Dynamics of autophagosome formation: a pulse and a sequence of waves. Biochem Soc Trans 42:1389–1395. doi:10.1042/BST20140183
Lamb CA, Dooley HC, Tooze SA (2013a) Endocytosis and autophagy: Shared machinery for degradation. BioEssays: news rev mol cell dev biol 35:34–45. doi:10.1002/bies.201200130
Lamb CA, Yoshimori T, Tooze SA. (2013b) The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14(12):759–774 (2013 Dec, Epub 2013 Nov 8)
Li X, He L, Che KH et al (2012) Imperfect interface of Beclin1 coiled-coil domain regulates homodimer and heterodimer formation with Atg14L and UVRAG. Nat commun 3:662. doi:10.1038/ncomms1648
Lipatova Z, Belogortseva N, Zhang XQ, Kim J, Taussig D, Segev N (2012) Regulation of selective autophagy onset by a Ypt/Rab GTPase module. Proc Natl Acad Sci USA 2012:6981–6986. doi:10.1073/pnas.1121299109
Longatti A, Lamb CA, Razi M et al (2012) TBC1D14 regulates autophagosome formation via Rab11—and ULK1-positive recycling endosomes. J Cell Biol 197:659–675. doi:10.1083/jcb.201111079
Lu Q, Hu W, Kovács AL et al (2011) The WD40 repeat PtdIns(3)P-Binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Dev Cell 21:343–357. doi:10.1016/j.devcel.2011.06.024
Lynch-Day MA, Bhandari D, Menon S, Huang J, Cai H, Bartholomew CR, Brumell JH, Ferro-Novick S, Klionsky DJ (2010) Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc Natl Acad Sci USA 107:7811–7816. doi:10.1073/pnas.1000063107
Mao K, Chew LH, Inoue-Aono Y et al (2013) Atg29 phosphorylation regulates coordination of the Atg17-Atg31-Atg29 complex with the Atg11 scaffold during autophagy initiation—PubMed—NCBI. Proc Natl Acad Sci USA 110:E2875–E2884. doi:10.1073/pnas.1300064110
Mapelli M, Musacchio A (2007) MAD contortions: conformational dimerization boosts spindle checkpoint signaling. Curr Opin Struct Biol 17:716–725. doi:10.1016/j.sbi.2007.08.011
Mari M, Griffith J, Rieter E et al (2010) An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J Cell Biol 190:1005–1022
Masaki R (1987) Cytochrome P-450 and NADPH-cytochrome P-450 reductase are degraded in the autolysosomes in rat liver [published erratum appears in J Cell Biol 1987 Jul; 105(1):609]. J Cell Biol 104:1207–1215. doi:10.1083/jcb.104.5.1207
Matsumoto G, Wada K, Okuno M et al (2011) Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell 44:279–289. doi:10.1016/j.molcel.2011.07.039
Matsunaga K, Saitoh T, Tabata K et al (2009) Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 11:385–396. doi:10.1038/ncb1846
Matsunaga K, Morita E, Saitoh T et al (2010) Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol 190:511–521. doi:10.1083/jcb.200911141
Mauthe M, Jacob A, Freiberger S et al (2011) Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy 7:1448–1461. doi:10.4161/auto.7.12.17802
Mercer CA, Kaliappan A, Dennis PB (2009) A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5:649–662
Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741. doi:10.1016/j.cell.2011.10.026
Mizushima N, Yamamoto A, Hatano M et al (2001) Dissection of autophagosome formation using Apg5-Deficient mouse embryonic stem cells. J Cell Biol 152:657–668. doi:10.1083/jcb.152.4.657
Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132. doi:10.1146/annurev-cellbio-092910-154005
Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a Ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130:165–178. doi:10.1016/j.cell.2007.05.021
Nishimura T, Kaizuka T, Cadwell K et al (2013) FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep 14:284–291. doi:10.1038/embor.2013.6
Ohsumi Y, Mizushima N, Noda T et al (1998) A protein conjugation system essential for autophagy. Nature 395:395–398. doi:10.1038/26506
Okazaki N, Yan J, Yuasa S et al (2000) Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Mol Brain Res 85:1–12. doi:10.1016/S0169-328X(00)00218-7
Orenstein SJ, Cuervo AM (2010) Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin Cell Dev Biol 21:719–726. doi:10.1016/j.semcdb.2010.02.005
Orsi A, Razi M, Dooley HC et al (2012) Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, is required for autophagy. Mol Biol Cell 23:1860–1873. doi:10.1091/mbc.E11-09-0746
Pankiv S, Clausen TH, Lamark T et al (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131–24145. doi:10.1074/jbc.m702824200
Pilli M, Arko-Mensah J, Ponpuak M et al (2012) TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity 37:223–234. doi:10.1016/j.immuni.2012.04.015
Polson HEJJ, De Lartigue J, Rigden DJ et al (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6:506–522. doi:10.4161/auto.6.4.11863
Proikas-Cezanne T, Waddell S, Gaugel A et al (2004) WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23:9314–9325. doi:10.1038/sj.onc.1208331
Puri C, Renna M, Bento CF et al (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154:1285–1299. doi:10.1016/j.cell.2013.08.044
Ragusa MJ, Stanley RE, Hurley JH (2012) Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151:1501–1512. doi:10.1016/j.cell.2012.11.028
Ravikumar B, Moreau K, Jahreiss L et al (2010) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12:747–757. doi:10.1038/ncb2078
Razi M, Chan EYW, Tooze SA (2009) Early endosomes and endosomal coatomer are required for autophagy. J Cell Biol 185:305–321. doi:10.1083/jcb.200810098
Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ (2004) The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 6:79–90. doi:10.1016/S1534-5807(03)00402-7
Rogov V, Dötsch V, Johansen T, Kirkin V (2014) Interactions between autophagy receptors and Ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell 53:167–178. doi:10.1016/j.molcel.2013.12.014
Rostislavleva K, Soler N, Ohashi Y, et al (2015) Structure and flexibility of the endosomal Vps34 complex reveals the basis of its function on membranes. Science 350:aac7365–aac7365. doi: 10.1126/science.aac7365
Russell RC, Tian Y, Yuan H et al (2013) ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 15:741–750. doi:10.1038/ncb2757
Saitoh T, Fujita N, Hayashi T et al (2009) Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci USA 106:20842–20846. doi:10.1073/pnas.0911267106
Sekito T, Kawamata T, Ichikawa R, Suzuki K, Ohsumi Y (2009) Atg17 recruits Atg9 to organize the preautophagosomal structure. Genes Cells 14:525–38. doi:10.1111/j.1365-2443.2009.01299.x
Simonsen A, Tooze SA (2009) Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 186:773–782. doi:10.1083/jcb.200907014
Sun Q, Fan W, Chen K et al (2008a) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 105:19211–19216. doi:10.1073/pnas.0810452105
Sun Q, Fan W, Chen K et al (2008b) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III. Autophagy 105:19211–19216
Suzuki K, Kubota Y, Sekito T, Ohsumi Y (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12:209–218. doi:10.1111/j.1365-2443.2007.01050.x
Suzuki H, Kaizuka T, Mizushima N, Noda NN (2015) Structure of the Atg101-Atg13 complex reveals essential roles of Atg101 in autophagy initiation—PubMed—NCBI. Nat Struct Mol Biol 22:572–580. doi:10.1038/nsmb.3036
Tanida I, Ueno T, Kominami E (2004) Human light chain 3/MAP1LC3B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 279:47704–47710. doi:10.1074/jbc.M407016200
Uemura T, Yamamoto M, Kametaka A et al (2014) A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol Cell Biol 34:1695–1706. doi:10.1128/MCB.01327-13
van der Klei IJ, Harder W, Veenhuis M (1991) Biosynthesis and assembly of alcohol oxidase, a peroxisomal matrix protein in methylotrophic yeasts: A review. Yeast (Chichester, England) 7:195–209. doi:10.1002/yea.320070302
Velikkakath AKG, Nishimura T, Oita E et al (2012) Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell 23:896–909. doi:10.1091/mbc.E11-09-0785
Wang J, Menon S, Yamasaki A, Chou H-T, Walz T, Jiang Y, Ferro-Novick S (2013) Ypt1 recruits the Atg1 kinase to the preautophagosomal structure. Proc Natl Acad Sci USA 110:9800–9805. doi:10.1073/pnas.1302337110
Webber JL, Tooze SA (2009) Coordinated regulation of autophagy by p38α MAPK through mAtg9 and p38IP. EMBO J 29:27–40. doi:10.1038/emboj.2009.321
Weidberg H, Shvets E, Shpilka T et al (2010) LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 29:1792–1802. doi:10.1038/emboj.2010.74
Weidberg H, Shpilka T, Shvets E et al (2011) LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Dev Cell 20:444–454. doi:10.1016/j.devcel.2011.02.006
Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290–3298. doi:10.1091/mbc.E07-12-1292
Xin Y, Yu L, Chen Z et al (2001) Cloning, expression patterns, and chromosome localization of three human and two mouse homologues of GABAA receptor-associated protein. Genomics 74:408–413. doi:10.1006/geno.2001.6555
Yamamoto H, Kakuta S, Watanabe TM et al (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 198:219–233. doi:10.1083/jcb.201202061
Ylä-Anttila P, Vihinen H, Jokitalo E, Eskelinen E-L (2009) 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5:1180–1185
Young ARJ, Chan EYW, Hu XW et al (2006) Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 119:3888–3900. doi:10.1242/jcs.03172
Zhong Y, Wang QJ, Li X et al (2009) Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1–phosphatidylinositol-3-kinase complex. Nat Cell Biol 11:468–476. doi:10.1038/ncb1854
Zoppino FCM, Militello RD, Slavin I, Alvarez C, Colombo MI (2010) Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 11:1246–1261. doi:10.1111/j.1600-0854.2010.01086.x
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Karanasios, E., Ktistakis, N.T. (2016). Autophagosome Formation. In: Autophagy at the Cell, Tissue and Organismal Level. SpringerBriefs in Cell Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-33145-4_4
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