CoChat
Sign Up
Cited by 88

The DOI matches its Crossref record; 16 of the 16 references it cites were found in a registry or an index.

Lipids and membrane-associated proteins in autophagy

Li, Linsen, Tong, Mindan, Fu, Yuhui, Chen, Fang, Zhang, Shen, Chen, Hanmo, Ma, Xi, Li, Defa, Liu, Xiaoxia, Zhong, Qing·2021·Protein & Cell
DOI 10.1007/s13238-020-00793-9PMC PMC8225772
Open this paper in CoChat — free account

Abstract

Autophagy is essential for the maintenance of cellular homeostasis and its dysfunction has been linked to various diseases. Autophagy is a membrane driven process and tightly regulated by membrane-associated proteins. Here, we summarized membrane lipid composition, and membrane-associated proteins relevant to autophagy from a spatiotemporal perspective. In particular, we focused on three important membrane remodeling processes in autophagy, lipid transfer for phagophore elongation, membrane scission for phagophore closure, and autophagosome-lysosome membrane fusion. We discussed the significance of the discoveries in this field and possible avenues to follow for future studies. Finally, we summarized the membrane-associated biochemical techniques and assays used to study membrane properties, with a discussion of their applications in autophagy.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s13238-020-00793-9

Cites

16 of 16 references verified0 citation errors · 0 not checkable

Statistics

Figures

Figure 1 Overview of autophagy with membrane-associated proteins highlighted. Cells go through the following steps to complete a cycle of autophagy: 1) autophagy initiation (signals activate autophagy) and nucleation of the phagophore/isolation membrane (IM, another name of the phagophore); 2) phagophore elongation; 3) closure to form the autophagosome; 4) fusion between the autophagosome and lysosome; 5) degradation of substrates in autolysosomes. Autophagy begins when cells sense the stimulation signals. The omegasome (a PI3P-enriched subdomain of ER where DFCP1 localizes through binding to PI3P) is the platform for the nucleation of the phagophore. This step involves two important complexes, the ULK1 complex and the PI3KC3C1 complex. The ULK1 complex phosphorylates and activates the PI3KC3C1 complex. The activated PI3KC3C1 complex generates PI3P from PI. Then, PI3P recruits WIPIs, which in turn recruit more autophagy machinery proteins. ATG12~ATG5-ATG16L1 recruited by WIPI2 catalyze ATG3-mediated conjugation of ATG8 family proteins with membrane resident PE, generating products like LC3II, which is the characteristic signature of autophagic membranes and is involved in ATG9 vesicle sequestration of cargo. There are multiple membrane sources of the autophagosome, including ER, Golgi, mitochondria, endosome, ERGIC, and plasma membrane. There are few possible ways for lipid transport, including ATG9 vesicle-mediated transport, COPII vesicle-mediated transport, ATG2-mediated lipid transport, etc. The cargos are sequestered while the autophagosomal membrane expands. Then, the sealing of this membrane structure by scission proteins such as ESCRT and other regulators gives rise to a double-membrane structure called the autophagosome. After becoming fully sealed, the autophagosome will recruit tethering proteins and SNARE proteins for fusion. Once fused, the acidic hydrolases in the lysosome degrade the autophagic cargos, salvaged nutrients are released back to the cytoplasm to be used by the cells, and the cis-SNARE complex is disassembled and recycled by NSF/αSNAP complex
Figure 1 Overview of autophagy with membrane-associated proteins highlighted. Cells go through the following steps to complete a cycle of autophagy: 1) autophagy initiation (signals activate autophagy) and nucleation of the phagophore/isolation membrane (IM, another name of the phagophore); 2) phagophore elongation; 3) closure to form the autophagosome; 4) fusion between the autophagosome and lysosome; 5) degradation of substrates in autolysosomes. Autophagy begins when cells sense the stimulation signals. The omegasome (a PI3P-enriched subdomain of ER where DFCP1 localizes through binding to PI3P) is the platform for the nucleation of the phagophore. This step involves two important complexes, the ULK1 complex and the PI3KC3C1 complex. The ULK1 complex phosphorylates and activates the PI3KC3C1 complex. The activated PI3KC3C1 complex generates PI3P from PI. Then, PI3P recruits WIPIs, which in turn recruit more autophagy machinery proteins. ATG12~ATG5-ATG16L1 recruited by WIPI2 catalyze ATG3-mediated conjugation of ATG8 family proteins with membrane resident PE, generating products like LC3II, which is the characteristic signature of autophagic membranes and is involved in ATG9 vesicle sequestration of cargo. There are multiple membrane sources of the autophagosome, including ER, Golgi, mitochondria, endosome, ERGIC, and plasma membrane. There are few possible ways for lipid transport, including ATG9 vesicle-mediated transport, COPII vesicle-mediated transport, ATG2-mediated lipid transport, etc. The cargos are sequestered while the autophagosomal membrane expands. Then, the sealing of this membrane structure by scission proteins such as ESCRT and other regulators gives rise to a double-membrane structure called the autophagosome. After becoming fully sealed, the autophagosome will recruit tethering proteins and SNARE proteins for fusion. Once fused, the acidic hydrolases in the lysosome degrade the autophagic cargos, salvaged nutrients are released back to the cytoplasm to be used by the cells, and the cis-SNARE complex is disassembled and recycled by NSF/αSNAP complexCC BY · PubMed Central
Figure 2 Hypothetic model for ATG2-mediated lipid transfer during autophagy. ATG2, ATG9-vesicles, and COPII-vesicles help to provide membrane sources for phagophore membrane elongation. ATG2 contains a CAD tip that binds to the PI3P interacting protein WIPI4 and an N-terminal hydrophobic cavity that binds to lipids. Inside the protein, there is an extended cavity or a series of cavities along the length of it. Two models are presented for the mechanism of lipid transfer for ATG2, the bridge-tunnel model (left), and the ferry model (middle). In the bridge model, ATG2 stably tethers the phagophore and ER, where its CAD tip interacts with WIPI4, a PI3P effector on the phagophore and its N tip hydrophobic cavity binds to the ER. The lipids could transfer in the tunnel inside ATG2 from the ER to the phagophore. In the ferry model, the CAD tip anchors on the phagophore membrane through WIPI4, while the N tip hydrophobic cavity takes lipids from ER, and swings like a ferry boat between the ER and the phagophore to transfer lipids. Simultaneously, ATG9-vesicles and COPII-vesicles can act in a vesicle-mediated membrane fusion to deliver lipids from many cellular organelles to the phagophore for its elongation
Figure 2 Hypothetic model for ATG2-mediated lipid transfer during autophagy. ATG2, ATG9-vesicles, and COPII-vesicles help to provide membrane sources for phagophore membrane elongation. ATG2 contains a CAD tip that binds to the PI3P interacting protein WIPI4 and an N-terminal hydrophobic cavity that binds to lipids. Inside the protein, there is an extended cavity or a series of cavities along the length of it. Two models are presented for the mechanism of lipid transfer for ATG2, the bridge-tunnel model (left), and the ferry model (middle). In the bridge model, ATG2 stably tethers the phagophore and ER, where its CAD tip interacts with WIPI4, a PI3P effector on the phagophore and its N tip hydrophobic cavity binds to the ER. The lipids could transfer in the tunnel inside ATG2 from the ER to the phagophore. In the ferry model, the CAD tip anchors on the phagophore membrane through WIPI4, while the N tip hydrophobic cavity takes lipids from ER, and swings like a ferry boat between the ER and the phagophore to transfer lipids. Simultaneously, ATG9-vesicles and COPII-vesicles can act in a vesicle-mediated membrane fusion to deliver lipids from many cellular organelles to the phagophore for its elongationCC BY · PubMed Central
Figure 3 Hypothetic model for ESCRT-mediated autophagosome pore closure. Phagophore pore closure model was plotted according to the ESCRT-mediated membrane scission, as the pore closure might share the same regulators and mechanism with the classic ESCRT model. The first step of phagophore closure is the recruitment of the ESCRT-I complex and other related machinery to the phagophore pore. ESCRT-I recruits the ESCRT-II and ESCRT-III complex. ESCRT-III will form oligomeric filaments, flat spirals, tubes, and conical funnels to remodel the membrane shape on the neck, and finally, scissor the membrane to form a closed double-membrane autophagosome. After scission, the AAA+ ATPase VPS4 is recruited and forms a hexamer to disassemble and recycle the ESCRT-III complex
Figure 3 Hypothetic model for ESCRT-mediated autophagosome pore closure. Phagophore pore closure model was plotted according to the ESCRT-mediated membrane scission, as the pore closure might share the same regulators and mechanism with the classic ESCRT model. The first step of phagophore closure is the recruitment of the ESCRT-I complex and other related machinery to the phagophore pore. ESCRT-I recruits the ESCRT-II and ESCRT-III complex. ESCRT-III will form oligomeric filaments, flat spirals, tubes, and conical funnels to remodel the membrane shape on the neck, and finally, scissor the membrane to form a closed double-membrane autophagosome. After scission, the AAA+ ATPase VPS4 is recruited and forms a hexamer to disassemble and recycle the ESCRT-III complexCC BY · PubMed Central
Figure 4 Model for SNARE-mediated autophagosome-lysosome fusion. Autophagosome-lysosome fusion is the key step of autophagy and is highly regulated by SNARE proteins, tethering factors, Rab GTPase, SM proteins, and other proteins. The fusion SNAREs identified so far for autophagy include STX17-SNAP29-VAMP8 and YKT6/SNAP29/STX7. Sealed autophagosome recruits the SNARE binary complex together with lysosomal SNARE protein to form a four-helix bundle to mediate autophagosome-lysosome fusion. Besides, tethering between autophagosomes and lysosomes can promote this fusion. Proteins involved in tethering include ATG14, Rab GTPase, HOPS, PLEKHM1, UVRAG, EPG5, BRUCE, TECPR1, GRASP55, etc
Figure 4 Model for SNARE-mediated autophagosome-lysosome fusion. Autophagosome-lysosome fusion is the key step of autophagy and is highly regulated by SNARE proteins, tethering factors, Rab GTPase, SM proteins, and other proteins. The fusion SNAREs identified so far for autophagy include STX17-SNAP29-VAMP8 and YKT6/SNAP29/STX7. Sealed autophagosome recruits the SNARE binary complex together with lysosomal SNARE protein to form a four-helix bundle to mediate autophagosome-lysosome fusion. Besides, tethering between autophagosomes and lysosomes can promote this fusion. Proteins involved in tethering include ATG14, Rab GTPase, HOPS, PLEKHM1, UVRAG, EPG5, BRUCE, TECPR1, GRASP55, etcCC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 16 references

Research works printed but not linked: 176

  1. Abada A, Levin-Zaidman S, Porat Z, Dadosh T, Elazar Z (2017) SNARE priming is essential for maturation of autophagosomes but not for their formation. Proc Natl Acad Sci USA 114:12749–12754 · DOI
  2. Asao H, Sasaki Y, Arita T, Tanaka N, Endo K, Kasai H, Takeshita T, Endo Y, Fujita T, Sugamura K (1997) Hrs is associated with STAM, a signal-transducing adaptor molecule. Its suppressive effect on cytokine-induced cell growth. J Biol Chem 272:32785–32791 · DOI
  3. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT (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 · Paper page
  4. Baba T, Toth DJ, Sengupta N, Kim YJ, Balla T (2019) Phosphatidylinositol 4,5-bisphosphate controls Rab7 and PLEKHM1 membrane cycling during autophagosome-lysosome fusion. EMBO J 38:e100312 · DOI
  5. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002a) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3:271–282 · DOI
  6. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD (2002b) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3:283–289 · DOI
  7. Baskaran S, Ragusa MJ, Boura E, Hurley JH (2012) Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol Cell 47:339–348 · DOI
  8. Bas L, Papinski D, Licheva M, Torggler R, Rohringer S, Schuschnig M, Kraft C (2018) Reconstitution reveals Ykt6 as the autophagosomal SNARE in autophagosome–vacuole fusion. J Cell Biol 217:3656–3669 · DOI · Paper page
  9. Bean BD, Dziurdzik SK, Kolehmainen KL, Fowler CM, Kwong WK, Grad LI, Davey M, Schluter C, Conibear E (2018) Competitive organelle-specific adaptors recruit Vps13 to membrane contact sites. J Cell Biol 217:3593–3607 · DOI
  10. Besprozvannaya M, Dickson E, Li H, Ginburg KS, Bers DM, Auwerx J, Nunnari J (2018) GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells. Elife 7:e31019 · DOI · Paper page
  11. Bian X, Zhang Z, Xiong Q, De Camilli P, Lin C (2019) A programmable DNA-origami platform for studying lipid transfer between bilayers. Nat Chem Biol 15:830–837 · DOI
  12. Bielli A, Haney CJ, Gabreski G, Watkins SC, Bannykh SI, Aridor M (2005) Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. The Journal of cell biology 171:919–924 · DOI
  13. Buchkovich NJ, Henne WM, Tang S, Emr SD (2013) Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Dev Cell 27:201–214 · DOI
  14. Caillat C, Macheboeuf P, Wu Y, McCarthy AA, Boeri-Erba E, Effantin G, Gottlinger HG, Weissenhorn W, Renesto P (2015) Asymmetric ring structure of Vps4 required for ESCRT-III disassembly. Nat Commun 6:8781 · DOI
  15. Carlsson SR, Simonsen A (2015) Membrane dynamics in autophagosome biogenesis. J Cell Sci 128:193–205
  16. Carroll B, Mohd-Naim N, Maximiano F, Frasa MA, McCormack J, Finelli M, Thoresen SB, Perdios L, Daigaku R, Francis RE et al (2013) The TBC/RabGAP Armus coordinates Rac1 and Rab7 functions during autophagy. Dev Cell 25:15–28 · DOI
  17. Chang C, Young LN, Morris KL, von Bülow S, Schöneberg J, Yamamoto-Imoto H, Oe Y, Yamamoto K, Nakamura S, Stjepanovic G (2019) Bidirectional control of autophagy by BECN1 BARA domain dynamics. Mol Cell 73(339–353):e336
  18. Chan EY, 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 · Paper page
  19. Chen D, Fan W, Lu Y, Ding X, Chen S, Zhong Q (2012) A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol Cell 45:629–641 · DOI
  20. Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S, Roux A (2015) Relaxation of loaded ESCRT-III spiral springs drives membrane deformation. Cell 163:866–879 · DOI
  21. Chowdhury S, Otomo C, Leitner A, Ohashi K, Aebersold R, Lander GC, Otomo T (2018) Insights into autophagosome biogenesis from structural and biochemical analyses of the ATG2A-WIPI4 complex. Proc Natl Acad Sci 115:E9792–E9801 · DOI
  22. Chung T (2019) How phosphoinositides shape autophagy in plant cells. Plant Sci 281:146–158 · DOI
  23. Cudjoe EK Jr, Saleh T, Hawkridge AM, Gewirtz DA (2017) Proteomics insights into autophagy. Proteomics 17:1700022 · DOI
  24. Daum G, Vance JE (1997) Import of lipids into mitochondria. Prog Lipid Res 36:103–130 · DOI
  25. de la Ballina LR, Munson MJ, Simonsen A (2020) Lipids and lipid-binding proteins in selective autophagy. J Mol Biol 432:135–159 · DOI
  26. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B (1997) Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta (BBA) 1325:108–116 · DOI
  27. Delorme-Axford E, Klionsky DJ (2018) Transcriptional and post-transcriptional regulation of autophagy in the yeast Saccharomyces cerevisiae. J Biol Chem 293:5396–5403 · DOI
  28. Diao J, Ishitsuka Y, Lee H, Joo C, Su Z, Syed S, Shin YK, Yoon TY, Ha T (2012) A single vesicle-vesicle fusion assay for in vitro studies of SNAREs and accessory proteins. Nat Protoc 7:921–934 · DOI
  29. Diao J, Liu R, Rong Y, Zhao M, Zhang J, Lai Y, Zhou Q, Wilz LM, Li J, Vivona S et al (2015) ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature 520:563–566 · DOI
  30. Dikic I, Elazar Z (2018) Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol 19:349–364 · DOI · Paper page
  31. Ding X, Jiang X, Tian R, Zhao P, Li L, Wang X, Chen S, Zhu Y, Mei M, Bao S et al (2019) RAB2 regulates the formation of autophagosome and autolysosome in mammalian cells. Autophagy 15:1774–1786 · DOI
  32. Dove SK, Dong K, Kobayashi T, Williams FK, Michell RH (2009) Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. Biochem J 419:1–13 · DOI
  33. Dudley LJ, Cabodevilla AG, Makar AN, Sztacho M, Michelberger T, Marsh JA, Houston DR, Martens S, Jiang X, Gammoh N (2019) Intrinsic lipid binding activity of ATG16L1 supports efficient membrane anchoring and autophagy. EMBO J 38:e100554 · DOI
  34. Ebner P, Poetsch I, Deszcz L, Hoffmann T, Zuber J, Ikeda F (2018) The IAP family member BRUCE regulates autophagosome–lysosome fusion. Nat Commun 9:1–15 · DOI
  35. Feng Q, Luo Y, Zhang XN, Yang XF, Hong XY, Sun DS, Li XC, Hu Y, Li XG, Zhang JF et al (2020) MAPT/Tau accumulation represses autophagy flux by disrupting IST1-regulated ESCRT-III complex formation: a vicious cycle in Alzheimer neurodegeneration. Autophagy 16:641–658 · DOI
  36. Fujioka Y, Noda NN, Nakatogawa H, Ohsumi Y, Inagaki F (2010) Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J Biol Chem 285:1508–1515 · DOI
  37. Fujioka Y, Alam JM, Noshiro D, Mouri K, Ando T, Okada Y, May AI, Knorr RL, Suzuki K, Ohsumi Y et al (2020) Phase separation organizes the site of autophagosome formation. Nature 578:301–305 · DOI
  38. Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 19:2092–2100 · DOI
  39. Gatica D, Lahiri V, Klionsky DJ (2018) Cargo recognition and degradation by selective autophagy. Nat Cell Biol 20:233–242 · DOI · Paper page
  40. Gatta AT, Carlton JG (2019) The ESCRT-machinery: closing holes and expanding roles. Curr Opin Cell Biol 59:121–132 · DOI
  41. Ge L, Schekman R (2014) The ER-Golgi intermediate compartment feeds the phagophore membrane. Autophagy 10:170–172 · DOI
  42. 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
  43. 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
  44. Ge L, Zhang M, Kenny SJ, Liu D, Maeda M, Saito K, Mathur A, Xu K, Schekman R (2017) Remodeling of ER-exit sites initiates a membrane supply pathway for autophagosome biogenesis. EMBO Rep 18:1586–1603 · DOI
  45. Gómez-Sánchez R, Rose J, Guimarães R, Mari M, Papinski D, Rieter E, Geerts WJ, Hardenberg R, Kraft C, Ungermann C (2018) Atg9 establishes Atg2-dependent contact sites between the endoplasmic reticulum and phagophores. J Cell Biol 217:2743–2763 · DOI
  46. Graef M (2020) Recent advances in the understanding of autophagosome biogenesis. F1000Res 9. · DOI
  47. Graef M, Friedman JR, Graham C, Babu M, Nunnari J (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24:2918–2931 · DOI
  48. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141:656–667 · DOI
  49. Hasegawa J, Iwamoto R, Otomo T, Nezu A, Hamasaki M, Yoshimori T (2016) Autophagosome-lysosome fusion in neurons requires INPP5E, a protein associated with Joubert syndrome. EMBO J 35:1853–1867 · DOI
  50. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 11:1433–1437 · DOI
  51. He S, Ni D, Ma B, Lee J-H, Zhang T, Ghozalli I, Pirooz SD, Zhao Z, Bharatham N, Li B (2013) PtdIns (3) P-bound UVRAG coordinates Golgi–ER retrograde and Atg9 transport by differential interactions with the ER tether and the beclin 1 complex. Nat Cell Biol 15:1206–1219 · DOI
  52. Hollenstein DM, Kraft C (2020) Autophagosomes are formed at a distinct cellular structure. Curr Opin Cell Biol 65:50–57 · DOI
  53. Ho CY, Alghamdi TA, Botelho RJ (2012) Phosphatidylinositol-3,5-bisphosphate: no longer the poor PIP2. Traffic 13:1–8 · DOI
  54. Huang X, Sun S, Wang X, Fan F, Zhou Q, Lu S, Cao Y, Wang QW, Dong MQ, Yao J et al (2019) Mechanistic insights into the SNARE complex disassembly. Sci Adv 5:eaau8164 · DOI
  55. Hurley JH, Young LN (2017) Mechanisms of autophagy initiation. Annu Rev Biochem 86:225–244 · DOI
  56. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M et al (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488–492 · DOI
  57. Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, Yoshimori T, Noda T, Ohsumi Y (2001) Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12:3690–3702 · DOI
  58. Itakura E, Kishi-Itakura C, Mizushima N (2012) The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151:1256–1269 · DOI
  59. Jang DJ, Lee JA (2016) The roles of phosphoinositides in mammalian autophagy. Arch Pharm Res 39:1129–1136 · DOI
  60. Jeynov B, Lay D, Schmidt F, Tahirovic S, Just WW (2006) Phosphoinositide synthesis and degradation in isolated rat liver peroxisomes. FEBS Lett 580:5917–5924 · DOI
  61. Jiang P, Nishimura T, Sakamaki Y, Itakura E, Hatta T, Natsume T, Mizushima N (2014) The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell 25:1327–1337 · DOI · Paper page
  62. Johansen T, Lamark T (2020) Selective autophagy: ATG8 family proteins, LIR motifs and cargo receptors. J Mol Biol 432:80–103 · DOI
  63. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992–2003 · DOI · Paper page
  64. Jun Y, Wickner W (2007) Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc Natl Acad Sci 104:13010–13015 · DOI
  65. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728 · DOI · Paper page
  66. Karanasios E, Stapleton E, Manifava M, Kaizuka T, Mizushima N, Walker SA, Ktistakis NT (2013) Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci 126:5224–5238
  67. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155 · DOI
  68. Knaevelsrud H, Soreng K, Raiborg C, Haberg K, Rasmuson F, Brech A, Liestol K, Rusten TE, Stenmark H, Neufeld TP et al (2013) Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J Cell Biol 202:331–349 · DOI
  69. Komada M, Kitamura N (1995) Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol Cell Biol 15:6213–6221 · DOI · Paper page
  70. Kostelansky MS, Schluter C, Tam YY, Lee S, Ghirlando R, Beach B, Conibear E, Hurley JH (2007) Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129:485–498 · DOI · Paper page
  71. Kriegenburg F, Ungermann C, Reggiori F (2018) Coordination of autophagosome–lysosome fusion by ATG8 family members. Curr Biol 28:R512–R518 · DOI
  72. Kriegenburg F, Bas L, Gao J, Ungermann C, Kraft C (2019) The multi-functional SNARE protein Ykt6 in autophagosomal fusion processes. Cell Cycle 18:639–651 · DOI
  73. Ktistakis NT (2019) Who plays the ferryman: ATG2 channels lipids into the forming autophagosome. J Cell Biol 218:1767 · DOI
  74. Kumar N, Leonzino M, Hancock-Cerutti W, Horenkamp FA, Li P, Lees JA, Wheeler H, Reinisch KM, De Camilli P (2018) VPS13A and VPS13C are lipid transport proteins differentially localized at ER contact sites. J Cell Biol 217:3625–3639 · DOI
  75. Kyoung M, Srivastava A, Zhang Y, Diao J, Vrljic M, Grob P, Nogales E, Chu S, Brunger AT (2011) In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc Natl Acad Sci 108:E304–E313 · DOI · Paper page
  76. Kyoung M, Zhang Y, Diao J, Chu S, Brunger AT (2013) Studying calcium-triggered vesicle fusion in a single vesicle-vesicle content and lipid-mixing system. Nat Protoc 8:1–16 · DOI
  77. Lai LTF, Ye H, Zhang W, Jiang L, Lau WCY (2019) Structural biology and electron microscopy of the autophagy molecular machinery. Cells 8:1627 · DOI
  78. Laraia L, Friese A, Corkery DP, Konstantinidis G, Erwin N, Hofer W, Karatas H, Klewer L, Brockmeyer A, Metz M (2019) The cholesterol transfer protein GRAMD1A regulates autophagosome biogenesis. Nat Chem Biol 15:710–720 · DOI
  79. Lemus L, Ribas JL, Sikorska N, Goder V (2016) An ER-localized SNARE protein is exported in specific COPII vesicles for autophagosome biogenesis. Cell Rep 14:1710–1722 · DOI
  80. Liu X, Seven AB, Camacho M, Esser V, Xu J, Trimbuch T, Quade B, Su L, Ma C, Rosenmund C et al (2016) Functional synergy between the Munc13 C-terminal C1 and C2 domains. Elife 5:e13696 · DOI
  81. Liu X, Seven AB, Xu J, Esser V, Su L, Ma C, Rizo J (2017) Simultaneous lipid and content mixing assays for in vitro reconstitution studies of synaptic vesicle fusion. Nat Protoc 12:2014–2028 · DOI
  82. Li L, Zhong Q (2016) Autophagosome-lysosome fusion: PIs to the rescue. EMBO J 35:1845–1847 · DOI
  83. Lystad AH, Simonsen A (2016) Phosphoinositide-binding proteins in autophagy. FEBS Lett 590:2454–2468 · DOI
  84. Lystad AH, Carlsson SR, Laura R, Kauffman KJ, Nag S, Yoshimori T, Melia TJ, Simonsen A (2019) Distinct functions of ATG16L1 isoforms in membrane binding and LC3B lipidation in autophagy-related processes. Nat Cell Biol 21:372–383 · DOI
  85. Maeda S, Otomo C, Otomo T (2019) The autophagic membrane tether ATG2A transfers lipids between membranes. Elife 8:e45777 · DOI
  86. Matsui T, Jiang P, Nakano S, Sakamaki Y, Yamamoto H, Mizushima N (2018) Autophagosomal YKT6 is required for fusion with lysosomes independently of syntaxin 17. J Cell Biol 217:2633–2645 · DOI · Paper page
  87. Matsushita M, Suzuki NN, Obara K, Fujioka Y, Ohsumi Y, Inagaki F (2007) Structure of Atg5.Atg16, a complex essential for autophagy. J Biol Chem 282:6763–6772 · DOI
  88. Ma C, Su L, Seven AB, Xu Y, Rizo J (2013) Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science 339:421–425 · DOI
  89. Ma M, Liu J-J, Li Y, Huang Y, Ta N, Chen Y, Fu H, Ye M-D, Ding Y, Huang W (2017) Cryo-EM structure and biochemical analysis reveal the basis of the functional difference between human PI3KC3-C1 and-C2. Cell Res 27:989–1001 · DOI
  90. McEwan DG, Popovic D, Gubas A, Terawaki S, Suzuki H, Stadel D, Coxon FP, Miranda de Stegmann D, Bhogaraju S, Maddi K et al (2015) PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Mol Cell 57:39–54 · DOI · Paper page
  91. Melia TJ, Lystad AH, Simonsen A (2020) Autophagosome biogenesis: from membrane growth to closure. J Cell Biol 219:e202002085 · DOI
  92. Mercer TJ, Gubas A, Tooze SA (2018) A molecular perspective of mammalian autophagosome biogenesis. J Biol Chem 293:5386–5395 · DOI
  93. Miao G, Zhang Y, Chen D, Zhang H (2020) The ER-localized transmembrane protein TMEM39A/SUSR2 regulates autophagy by controlling the trafficking of the PtdIns(4)P phosphatase SAC1. Mol Cell 77(618–632):e615
  94. Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873 · DOI
  95. Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC (2011) Autophagosome precursor maturation requires homotypic fusion. Cell 146:303–317 · DOI
  96. Muñoz-Braceras S, Calvo R, Escalante R (2015) TipC and the chorea-acanthocytosis protein VPS13A regulate autophagy in Dictyostelium and human HeLa cells. Autophagy 11:918–927 · DOI
  97. Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen W-L, Griffith J, Nag S, Wang K, Moss T (2011) SNARE proteins are required for macroautophagy. Cell 146:290–302 · DOI
  98. Naito T, Ercan B, Krshnan L, Triebl A, Koh DHZ, Wei F-Y, Tomizawa K, Torta FT, Wenk MR, Saheki Y (2019) Movement of accessible plasma membrane cholesterol by the GRAMD1 lipid transfer protein complex. eLife 8:e51401 · DOI · Paper page
  99. Nakamura S, Yoshimori T (2017) New insights into autophagosome–lysosome fusion. J Cell Sci 130:1209–1216 · DOI
  100. Nakatogawa H (2020) Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol · DOI
  101. 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
  102. Nascimbeni AC, Codogno P, Morel E (2017) Phosphatidylinositol-3-phosphate in the regulation of autophagy membrane dynamics. FEBS J 284:1267–1278 · DOI
  103. Nath S, Dancourt J, Shteyn V, Puente G, Fong WM, Nag S, Bewersdorf J, Yamamoto A, Antonny B, Melia TJ (2014) Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nat Cell Biol 16:415–424 · DOI
  104. Nishimura T, Tooze SA (2020) Emerging roles of ATG proteins and membrane lipids in autophagosome formation. Cell Discov 6:32 · DOI
  105. Odorizzi G, Babst M, Emr SD (1998) Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95:847–858 · DOI · Paper page
  106. Ogawa M, Yoshikawa Y, Kobayashi T, Mimuro H, Fukumatsu M, Kiga K, Piao Z, Ashida H, Yoshida M, Kakuta S (2011) A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 9:376–389 · DOI
  107. Omari S, Makareeva E, Roberts-Pilgrim A, Mirigian L, Jarnik M, Ott C, Lippincott-Schwartz J, Leikin S (2018) Noncanonical autophagy at ER exit sites regulates procollagen turnover. Proc Natl Acad Sci 115:E10099–E10108 · DOI
  108. Osawa T, Noda NN (2019) Atg2: A novel phospholipid transfer protein that mediates de novo autophagosome biogenesis. Protein Sci 28:1005–1012 · DOI
  109. Osawa T, Alam JM, Noda NN (2019a) Membrane-binding domains in autophagy. Chem Phys Lipids 218:1–9 · DOI
  110. Osawa T, Ishii Y, Noda NN (2019b) Human ATG2B possesses a lipid transfer activity which is accelerated by negatively charged lipids and WIPI4. Genes Cells 25:65 · DOI
  111. Osawa T, Kotani T, Kawaoka T, Hirata E, Suzuki K, Nakatogawa H, Ohsumi Y, Noda NN (2019c) Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat Struct Mol Biol 26:281–288 · DOI
  112. Otomo T, Maeda S (2019) ATG2A transfers lipids between membranes in vitro. Autophagy 15:2031–2032 · DOI
  113. Otomo T, Chowdhury S, Lander GC (2018) The rod-shaped ATG2A-WIPI4 complex tethers membranes in vitro. Contact 1:2515256418819936 · DOI
  114. Palamiuc L, Ravi A, Emerling BM (2020) Phosphoinositides in autophagy: current roles and future insights. FEBS J 287:222–238 · DOI
  115. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131–24145 · DOI · Paper page
  116. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P (2000) Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275:992–998 · DOI
  117. Polson HE, de Lartigue J, Rigden DJ, Reedijk M, Urbé S, Clague MJ, Tooze SA (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6:506–522 · DOI · Paper page
  118. Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154:1285–1299 · DOI
  119. Ragusa MJ, Stanley RE, Hurley JH (2012) Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151:1501–1512 · DOI · Paper page
  120. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3:1389–1402 · DOI
  121. Reggiori F, Ungermann C (2017) Autophagosome maturation and fusion. J Mol Biol 429:486–496 · DOI
  122. Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, Kraft C, Martens S (2012) Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J 31:4304–4317 · DOI
  123. Rong Y, Liu M, Ma L, Du W, Zhang H, Tian Y, Cao Z, Li Y, Ren H, Zhang C et al (2012) Clathrin and phosphatidylinositol-4,5-bisphosphate regulate autophagic lysosome reformation. Nat Cell Biol 14:924–934 · DOI · Paper page
  124. Russell RC, Tian Y, Yuan H, Park HW, Chang YY, Kim J, Kim H, Neufeld TP, Dillin A, Guan KL (2013) ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 15:741–750 · DOI · Paper page
  125. Rusten TE, Stenmark H (2009) How do ESCRT proteins control autophagy? J Cell Sci 122:2179–2183 · DOI
  126. Schoneberg J, Lee IH, Iwasa JH, Hurley JH (2017) Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18:5–17 · DOI
  127. Schoneberg J, Pavlin MR, Yan S, Righini M, Lee IH, Carlson LA, Bahrami AH, Goldman DH, Ren X, Hummer G et al (2018) ATP-dependent force generation and membrane scission by ESCRT-III and Vps4. Science 362:1423–1428 · DOI
  128. Schütter M, Giavalisco P, Brodesser S, Graef M (2020) Local fatty acid channeling into phospholipid synthesis drives phagophore expansion during autophagy. Cell 180(135–149):e114
  129. Schu PV, Takegawa K, Fry MJ, Stack JH, Waterfield MD, Emr SD (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260:88–91 · DOI · Paper page
  130. Shatz O, Holland P, Elazar Z, Simonsen A (2016) Complex relations between phospholipids, autophagy, and neutral lipids. Trends Biochem Sci 41:907–923 · DOI
  131. Shibutani ST, Yoshimori T (2014) A current perspective of autophagosome biogenesis. Cell Res 24:58–68 · DOI
  132. Shima T, Kirisako H, Nakatogawa H (2019) COPII vesicles contribute to autophagosomal membranes. J Cell Biol 218:1503–1510 · DOI
  133. Shintani T, Suzuki K, Kamada Y, Noda T, Ohsumi Y (2001) Apg2p functions in autophagosome formation on the perivacuolar structure. J Biol Chem 276:30452–30460 · DOI
  134. Sitarska E, Xu J, Park S, Liu X, Quade B, Stepien K, Sugita K, Brautigam CA, Sugita S, Rizo J (2017) Autoinhibition of Munc18-1 modulates synaptobrevin binding and helps to enable Munc13-dependent regulation of membrane fusion. Elife 6:e24278 · DOI
  135. Slessareva JE, Routt SM, Temple B, Bankaitis VA, Dohlman HG (2006) Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein α subunit at the endosome. Cell 126:191–203 · DOI
  136. Soreng K, Munson MJ, Lamb CA, Bjorndal GT, Pankiv S, Carlsson SR, Tooze SA, Simonsen A (2018) SNX18 regulates ATG9A trafficking from recycling endosomes by recruiting Dynamin-2. EMBO Rep 19:e44837 · DOI
  137. Stadel D, Millarte V, Tillmann KD, Huber J, Tamin-Yecheskel BC, Akutsu M, Demishtein A, Ben-Zeev B, Anikster Y, Perez F et al (2015) TECPR2 cooperates with LC3C to regulate COPII-dependent ER export. Mol cell 60:89–104 · DOI · Paper page
  138. Stroupe C, Collins KM, Fratti RA, Wickner W (2006) Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 25:1579–1589 · DOI
  139. Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q (2008) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci 105:19211–19216 · DOI · Paper page
  140. Sun Q, Zhang J, Fan W, Wong KN, Ding X, Chen S, Zhong Q (2011) The RUN domain of rubicon is important for hVps34 binding, lipid kinase inhibition, and autophagy suppression. J Biol Chem 286:185–191 · DOI · Paper page
  141. Suzuki H, Osawa T, Fujioka Y, Noda NN (2017) Structural biology of the core autophagy machinery. Curr Opin Struct Biol 43:10–17 · DOI
  142. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mul JJ (2007) Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9:1142–1151 · DOI
  143. Takahashi Y, Meyerkord CL, Hori T, Runkle K, Fox TE, Kester M, Loughran TP, Wang HG (2011) Bif-1 regulates Atg9 trafficking by mediating the fission of Golgi membranes during autophagy. Autophagy 7:61–73 · DOI
  144. Takahashi Y, He H, Tang Z, Hattori T, Liu Y, Young MM, Serfass JM, Chen L, Gebru M, Chen C et al (2018) An autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure. Nat Commun 9:2855 · DOI · Paper page
  145. Takahashi Y, Liang X, Hattori T, Tang Z, He H, Chen H, Liu X, Abraham T, Imamura-Kawasawa Y, Buchkovich NJ et al (2019) VPS37A directs ESCRT recruitment for phagophore closure. J Cell Biol 218:3336–3354 · DOI
  146. Tang Z, Takahashi Y, He H, Hattori T, Chen C, Liang X, Chen H, Young MM, Wang HG (2019) TOM40 targets Atg2 to mitochondria-associated ER membranes for phagophore expansion. Cell Rep 28(1744–1757):e1745
  147. Thorburn A (2018) Autophagy and disease. J Biol Chem 293:5425–5430 · DOI
  148. Tong J, Manik MK, Im YJ (2018) Structural basis of sterol recognition and nonvesicular transport by lipid transfer proteins anchored at membrane contact sites. Proc Natl Acad Sci 115:E856–E865 · DOI
  149. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–174 · DOI
  150. Valverde DP, Yu S, Boggavarapu V, Kumar N, Lees JA, Walz T, Reinisch KM, Melia TJ (2019) ATG2 transports lipids to promote autophagosome biogenesis. J Cell Biol 218:1787–1798 · DOI
  151. Velikkakath AK, Nishimura T, Oita E, Ishihara N, Mizushima N (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
  152. Wang K, Yang Z, Liu X, Mao K, Nair U, Klionsky DJ (2012) Phosphatidylinositol 4-kinases are required for autophagic membrane trafficking. J Biol Chem 287:37964–37972 · DOI
  153. Wang Z, Miao G, Xue X, Guo X, Yuan C, Wang Z, Zhang G, Chen Y, Feng D, Hu J (2016) The Vici syndrome protein EPG5 is a Rab7 effector that determines the fusion specificity of autophagosomes with late endosomes/lysosomes. Mol Cell 63:781–795 · DOI · Paper page
  154. Watanabe Y, Kobayashi T, Yamamoto H, Hoshida H, Akada R, Inagaki F, Ohsumi Y, Noda NN (2012) Structure-based analyses reveal distinct binding sites for Atg2 and phosphoinositides in Atg18. J Biol Chem 287:31681–31690 · DOI
  155. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Söllner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772 · DOI
  156. Wetzel L, Blanchard S, Rama S, Beier V, Kaufmann A, Wollert T (2020) TECPR1 promotes aggrephagy by direct recruitment of LC3C autophagosomes to lysosomes. Nat Commun 11:1–16 · DOI
  157. Wherrett JR, Huterer S (1972) Enrichment of bis-(monoacylglyceryl) phosphate in lysosomes from rat liver. J Biol Chem 247:4114–4120 · DOI
  158. White KI, Zhao M, Choi UB, Pfuetzner RA, Brunger AT (2018) Structural principles of SNARE complex recognition by the AAA+ protein NSF. Elife 7:e38888 · DOI
  159. Wickner W, Rizo J (2017) A cascade of multiple proteins and lipids catalyzes membrane fusion. Mol Biol Cell 28:707–711 · DOI
  160. Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290–3298 · DOI · Paper page
  161. Xu Z, Yang L, Xu S, Zhang Z, Cao Y (2015) The receptor proteins: pivotal roles in selective autophagy. Acta Biochim Biophys Sin 47:571–580 · DOI
  162. Xu J, Camacho M, Xu Y, Esser V, Liu X, Trimbuch T, Pan YZ, Ma C, Tomchick DR, Rosenmund C et al (2017) Mechanistic insights into neurotransmitter release and presynaptic plasticity from the crystal structure of Munc13-1 C1C2BMUN. Elife 6:e22567 · DOI · Paper page
  163. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, Kondo-Kakuta C, Ichikawa R, Kinjo M, Ohsumi Y (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 198:219–233 · DOI · Paper page
  164. 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 · DOI
  165. Yorikawa C, Shibata H, Waguri S, Hatta K, Horii M, Katoh K, Kobayashi T, Uchiyama Y, Maki M (2005) Human CHMP6, a myristoylated ESCRT-III protein, interacts directly with an ESCRT-II component EAP20 and regulates endosomal cargo sorting. Biochem J 387:17–26 · DOI
  166. Yu Z-Q, Ni T, Hong B, Wang H-Y, Jiang F-J, Zou S, Chen Y, Zheng X-L, Klionsky DJ, Liang Y (2012) Dual roles of Atg8− PE deconjugation by Atg4 in autophagy. Autophagy 8:883–892 · DOI
  167. Yu H, Rathore SS, Lopez JA, Davis EM, James DE, Martin JL, Shen J (2013) Comparative studies of Munc18c and Munc18-1 reveal conserved and divergent mechanisms of Sec1/Munc18 proteins. Proc Natl Acad Sci USA 110:E3271–3280 · DOI
  168. Yu L, Chen Y, Tooze SA (2018) Autophagy pathway: cellular and molecular mechanisms. Autophagy 14:207–215 · DOI
  169. Zambrano F, Fleischer S, Fleischer B (1975) Lipid composition of the Golgi apparatus of rat kidney and liver in comparison with other subcellular organelles. Biochim Biophys Acta (BBA) 380:357–369 · DOI
  170. Zhang X, Wang L, Ireland SC, Ahat E, Li J, Bekier ME, Zhang Z, Wang Y (2019) GORASP2/GRASP55 collaborates with the PtdIns3K UVRAG complex to facilitate autophagosome-lysosome fusion. Autophagy 15:1787–1800 · DOI
  171. Zhang A, Meng Y, Li Q, Liang Y (2020) The ESCRT complex negatively regulates Erg6 degradation under specific glucose restriction conditions. Traffic · DOI
  172. Zhao YG, Zhang H (2019) Autophagosome maturation: an epic journey from the ER to lysosomes. J Cell Biol 218:757–770 · DOI
  173. Zhao M, Wu S, Zhou Q, Vivona S, Cipriano DJ, Cheng Y, Brunger AT (2015) Mechanistic insights into the recycling machine of the SNARE complex. Nature 518:61–67 · DOI
  174. Zhou F, Wu Z, Zhao M, Murtazina R, Cai J, Zhang A, Li R, Sun D, Li W, Zhao L et al (2019) Rab5-dependent autophagosome closure by ESCRT. J Cell Biol 218:1908–1927 · DOI
  175. Zinser E, Daum G (1995) Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast 11:493–536 · DOI
  176. Zucchi PC, Zick M (2011) Membrane fusion catalyzed by a Rab, SNAREs, and SNARE chaperones is accompanied by enhanced permeability to small molecules and by lysis. Mol Biol Cell 22:4635–4646 · DOI

Cited by

Sorted by citations

Metadata

Authors
Li, L., Tong, M., Fu, Y., Chen, F., Zhang, S., Chen, H., Ma, X., Li, D., Liu, X., & Zhong, Q.
Venue
Protein & Cell
Publisher
Oxford University Press (OUP)
Published
2020-11-05
Volume
12
Issue
7
Pages
520-544
ISSN
  • 1674-800X
  • 1674-8018
DOI
10.1007/s13238-020-00793-9
PMC
PMC8225772
Cited by
88
References
16
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review