Lipids and membrane-associated proteins in autophagy
Linsen Li, Mindan Tong, Yuhui Fu, Fang Chen, Shen Zhang, Hanmo Chen, Xi Ma, Defa Li, Xiaoxia Liu, Qing Zhong
Lipids and membrane-associated proteins in autophagy
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.
autophagy / membrane-associated proteins / membrane-associated biochemistry assays / ATG2 / ESCRT / lipid transfer / elongation / scission / fusion
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Google scholar
|
[10] |
Behrends C, Sowa ME, Gygi SP, Harper JW (2010) Network organization of the human autophagy system. Nature 466:68–76
CrossRef
Google scholar
|
[11] |
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
CrossRef
Google scholar
|
[12] |
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
CrossRef
Google scholar
|
[13] |
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
CrossRef
Google scholar
|
[14] |
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
CrossRef
Google scholar
|
[15] |
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
CrossRef
Google scholar
|
[16] |
Carlsson SR, Simonsen A (2015) Membrane dynamics in autophagosome biogenesis. J Cell Sci 128:193–205
CrossRef
Google scholar
|
[17] |
Carroll B, Mohd-Naim N, Maximiano F, Frasa MA, McCormack J, Finelli M, Thoresen SB, Perdios L, Daigaku R, Francis RE
CrossRef
Google scholar
|
[18] |
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
CrossRef
Google scholar
|
[19] |
Chan EY, Longatti A, McKnight NC, Tooze SA (2009) Kinaseinactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol 29:157–171
CrossRef
Google scholar
|
[20] |
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
CrossRef
Google scholar
|
[21] |
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
CrossRef
Google scholar
|
[22] |
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
CrossRef
Google scholar
|
[23] |
Chung T (2019) How phosphoinositides shape autophagy in plant cells. Plant Sci 281:146–158
CrossRef
Google scholar
|
[24] |
Cudjoe EK Jr, Saleh T, Hawkridge AM, Gewirtz DA (2017) Proteomics insights into autophagy. Proteomics 17:1700022
CrossRef
Google scholar
|
[25] |
Daum G, Vance JE (1997) Import of lipids into mitochondria. Prog Lipid Res 36:103–130
CrossRef
Google scholar
|
[26] |
de la Ballina LR, Munson MJ, Simonsen A (2020) Lipids and lipidbinding proteins in selective autophagy. J Mol Biol 432:135–159
CrossRef
Google scholar
|
[27] |
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
CrossRef
Google scholar
|
[28] |
Delorme-Axford E, Klionsky DJ (2018) Transcriptional and posttranscriptional regulation of autophagy in the yeast Saccharomyces cerevisiae. J Biol Chem 293:5396–5403
CrossRef
Google scholar
|
[29] |
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
CrossRef
Google scholar
|
[30] |
Diao J, Liu R, Rong Y, Zhao M, Zhang J, Lai Y, Zhou Q, Wilz LM, Li J, Vivona S
CrossRef
Google scholar
|
[31] |
Dikic I, Elazar Z (2018) Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol 19:349–364
CrossRef
Google scholar
|
[32] |
Ding X, Jiang X, Tian R, Zhao P, Li L, Wang X, Chen S, Zhu Y, Mei M, Bao S
CrossRef
Google scholar
|
[33] |
Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657
CrossRef
Google scholar
|
[34] |
Dove SK, Dong K, Kobayashi T, Williams FK, Michell RH (2009) Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve under-PPIn endo-lysosome function. Biochem J 419:1–13
CrossRef
Google scholar
|
[35] |
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
CrossRef
Google scholar
|
[36] |
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
CrossRef
Google scholar
|
[37] |
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
CrossRef
Google scholar
|
[38] |
Feng Q, Luo Y, Zhang XN, Yang XF, Hong XY, Sun DS, Li XC, Hu Y, Li XG, Zhang JF
CrossRef
Google scholar
|
[39] |
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
CrossRef
Google scholar
|
[40] |
Fujioka Y, Alam JM, Noshiro D, Mouri K, Ando T, Okada Y, May AI, Knorr RL, Suzuki K, Ohsumi Y
CrossRef
Google scholar
|
[41] |
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
CrossRef
Google scholar
|
[42] |
Gatica D, Lahiri V, Klionsky DJ (2018) Cargo recognition and degradation by selective autophagy. Nat Cell Biol 20:233–242
CrossRef
Google scholar
|
[43] |
Gatta AT, Carlton JG (2019) The ESCRT-machinery: closing holes and expanding roles. Curr Opin Cell Biol 59:121–132
CrossRef
Google scholar
|
[44] |
Ge L, Schekman R (2014) The ER-Golgi intermediate compartment feeds the phagophore membrane. Autophagy 10:170–172
CrossRef
Google scholar
|
[45] |
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
CrossRef
Google scholar
|
[46] |
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
CrossRef
Google scholar
|
[47] |
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
CrossRef
Google scholar
|
[48] |
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
CrossRef
Google scholar
|
[49] |
Graef M (2020) Recent advances in the understanding of autophagosome biogenesis. F1000Res 9.
CrossRef
Google scholar
|
[50] |
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
CrossRef
Google scholar
|
[51] |
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
CrossRef
Google scholar
|
[52] |
Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282:37298–37302
CrossRef
Google scholar
|
[53] |
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
CrossRef
Google scholar
|
[54] |
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
CrossRef
Google scholar
|
[55] |
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
CrossRef
Google scholar
|
[56] |
Hollenstein DM, Kraft C (2020) Autophagosomes are formed at a distinct cellular structure. Curr Opin Cell Biol 65:50–57
CrossRef
Google scholar
|
[57] |
Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N
CrossRef
Google scholar
|
[58] |
Ho CY, Alghamdi TA, Botelho RJ (2012) Phosphatidylinositol-3,5-bisphosphate: no longer the poor PIP2. Traffic 13:1–8
CrossRef
Google scholar
|
[59] |
Huang X, Sun S, Wang X, Fan F, Zhou Q, Lu S, Cao Y, Wang QW, Dong MQ, Yao J
CrossRef
Google scholar
|
[60] |
Hurley JH, Young LN (2017) Mechanisms of autophagy initiation. Annu Rev Biochem 86:225–244
CrossRef
Google scholar
|
[61] |
Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M
CrossRef
Google scholar
|
[62] |
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
CrossRef
Google scholar
|
[63] |
Itakura E, Kishi-Itakura C, Mizushima N (2012) The hairpin-type tailanchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151:1256–1269
CrossRef
Google scholar
|
[64] |
Jang DJ, Lee JA (2016) The roles of phosphoinositides in mammalian autophagy. Arch Pharm Res 39:1129–1136
CrossRef
Google scholar
|
[65] |
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
CrossRef
Google scholar
|
[66] |
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
CrossRef
Google scholar
|
[67] |
Johansen T, Lamark T (2020) Selective autophagy: ATG8 family proteins, LIR motifs and cargo receptors. J Mol Biol 432:80–103
CrossRef
Google scholar
|
[68] |
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
CrossRef
Google scholar
|
[69] |
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
CrossRef
Google scholar
|
[70] |
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
CrossRef
Google scholar
|
[71] |
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
CrossRef
Google scholar
|
[72] |
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
CrossRef
Google scholar
|
[73] |
Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 147:435–446
CrossRef
Google scholar
|
[74] |
Knaevelsrud H, Soreng K, Raiborg C, Haberg K, Rasmuson F, Brech A, Liestol K, Rusten TE, Stenmark H, Neufeld TP
CrossRef
Google scholar
|
[75] |
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
CrossRef
Google scholar
|
[76] |
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
CrossRef
Google scholar
|
[77] |
Kriegenburg F, Ungermann C, Reggiori F (2018) Coordination of autophagosome–lysosome fusion by ATG8 family members. Curr Biol 28:R512–R518
CrossRef
Google scholar
|
[78] |
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
CrossRef
Google scholar
|
[79] |
Ktistakis NT (2019) Who plays the ferryman: ATG2 channels lipids into the forming autophagosome. J Cell Biol 218:1767
CrossRef
Google scholar
|
[80] |
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
CrossRef
Google scholar
|
[81] |
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
CrossRef
Google scholar
|
[82] |
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
CrossRef
Google scholar
|
[83] |
Lai LTF, Ye H, Zhang W, Jiang L, Lau WCY (2019) Structural biology and electron microscopy of the autophagy molecular machinery. Cells 8:1627
CrossRef
Google scholar
|
[84] |
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
CrossRef
Google scholar
|
[85] |
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
CrossRef
Google scholar
|
[86] |
Levine B, Kroemer G (2019) Biological functions of autophagy genes: a disease perspective. Cell 176:11–42
CrossRef
Google scholar
|
[87] |
Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C
CrossRef
Google scholar
|
[88] |
Liu X, Seven AB, Camacho M, Esser V, Xu J, Trimbuch T, Quade B, Su L, Ma C, Rosenmund C
CrossRef
Google scholar
|
[89] |
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
CrossRef
Google scholar
|
[90] |
Li L, Zhong Q (2016) Autophagosome-lysosome fusion: PIs to the rescue. EMBO J 35:1845–1847
CrossRef
Google scholar
|
[91] |
Lystad AH, Simonsen A (2016) Phosphoinositide-binding proteins in autophagy. FEBS Lett 590:2454–2468
CrossRef
Google scholar
|
[92] |
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 autophagyrelated processes. Nat Cell Biol 21:372–383
CrossRef
Google scholar
|
[93] |
Maeda S, Otomo C, Otomo T(2019) The autophagic membrane tether ATG2A transfers lipids between membranes. Elife 8: e45777
CrossRef
Google scholar
|
[94] |
Maruyama T, Noda NN (2018) Autophagy-regulating protease Atg4: structure, function, regulation and inhibition. J Antibiot 71:72–78
CrossRef
Google scholar
|
[95] |
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
CrossRef
Google scholar
|
[96] |
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
CrossRef
Google scholar
|
[97] |
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
CrossRef
Google scholar
|
[98] |
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
CrossRef
Google scholar
|
[99] |
McEwan DG, Popovic D, Gubas A, Terawaki S, Suzuki H, Stadel D, Coxon FP, Miranda de Stegmann D, Bhogaraju S, Maddi K
CrossRef
Google scholar
|
[100] |
Melia TJ, Lystad AH, Simonsen A (2020) Autophagosome biogenesis: from membrane growth to closure. J Cell Biol 219: e202002085
CrossRef
Google scholar
|
[101] |
Mercer TJ, Gubas A, Tooze SA (2018) A molecular perspective of mammalian autophagosome biogenesis. J Biol Chem 293:5386–5395
CrossRef
Google scholar
|
[102] |
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
CrossRef
Google scholar
|
[103] |
Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873
CrossRef
Google scholar
|
[104] |
Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132
CrossRef
Google scholar
|
[105] |
Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC (2011) Autophagosome precursor maturation requires homotypic fusion. Cell 146:303–317
CrossRef
Google scholar
|
[106] |
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
CrossRef
Google scholar
|
[107] |
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
CrossRef
Google scholar
|
[108] |
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
CrossRef
Google scholar
|
[109] |
Nakamura S, Yoshimori T (2017) New insights into autophagosome–lysosome fusion. J Cell Sci 130:1209–1216
CrossRef
Google scholar
|
[110] |
Nakatogawa H (2020) Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol
CrossRef
Google scholar
|
[111] |
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
CrossRef
Google scholar
|
[112] |
Nascimbeni AC, Codogno P, Morel E (2017) Phosphatidylinositol-3-phosphate in the regulation of autophagy membrane dynamics. FEBS J 284:1267–1278
CrossRef
Google scholar
|
[113] |
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
CrossRef
Google scholar
|
[114] |
Nishimura T, Tooze SA (2020) Emerging roles of ATG proteins and membrane lipids in autophagosome formation. Cell Discov 6:32
CrossRef
Google scholar
|
[115] |
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
CrossRef
Google scholar
|
[116] |
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
CrossRef
Google scholar
|
[117] |
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
CrossRef
Google scholar
|
[118] |
Osawa T, Noda NN (2019) Atg2: A novel phospholipid transfer protein that mediates de novo autophagosome biogenesis. Protein Sci 28:1005–1012
CrossRef
Google scholar
|
[119] |
Osawa T, Alam JM, Noda NN (2019a) Membrane-binding domains in autophagy. Chem Phys Lipids 218:1–9
CrossRef
Google scholar
|
[120] |
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
CrossRef
Google scholar
|
[121] |
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
CrossRef
Google scholar
|
[122] |
Otomo T, Maeda S (2019) ATG2A transfers lipids between membranes in vitro. Autophagy 15:2031–2032
CrossRef
Google scholar
|
[123] |
Otomo T, Chowdhury S, Lander GC (2018) The rod-shaped ATG2AWIPI4 complex tethers membranes in vitro. Contact1:2515256418819936
CrossRef
Google scholar
|
[124] |
Palamiuc L, Ravi A, Emerling BM (2020) Phosphoinositides in autophagy: current roles and future insights. FEBS J 287:222–238
CrossRef
Google scholar
|
[125] |
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
CrossRef
Google scholar
|
[126] |
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
CrossRef
Google scholar
|
[127] |
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
CrossRef
Google scholar
|
[128] |
Preiss R (2017) Autophagy gene overexpression in Saccharomyces cerevisiae for accelerated sparkling wine production
|
[129] |
Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154:1285–1299
CrossRef
Google scholar
|
[130] |
Ragusa MJ, Stanley RE, Hurley JH (2012) Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151:1501–1512
CrossRef
Google scholar
|
[131] |
Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC (2010) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12:747–757
CrossRef
Google scholar
|
[132] |
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
CrossRef
Google scholar
|
[133] |
Reggiori F, Ungermann C (2017) Autophagosome maturation and fusion. J Mol Biol 429:486–496
CrossRef
Google scholar
|
[134] |
Reggiori F, Shintani T, Chong H, Nair U, Klionsky DJ (2005) Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1:101–109
CrossRef
Google scholar
|
[135] |
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
CrossRef
Google scholar
|
[136] |
Rong Y, Liu M, Ma L, Du W, Zhang H, Tian Y, Cao Z, Li Y, Ren H, Zhang C
CrossRef
Google scholar
|
[137] |
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
CrossRef
Google scholar
|
[138] |
Rusten TE, Stenmark H (2009) How do ESCRT proteins control autophagy? J Cell Sci 122:2179–2183
CrossRef
Google scholar
|
[139] |
Schoneberg J, Lee IH, Iwasa JH, Hurley JH (2017) Reversetopology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18:5–17
CrossRef
Google scholar
|
[140] |
Schoneberg J, Pavlin MR, Yan S, Righini M, Lee IH, Carlson LA, Bahrami AH, Goldman DH, Ren X, Hummer G
CrossRef
Google scholar
|
[141] |
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
CrossRef
Google scholar
|
[142] |
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
CrossRef
Google scholar
|
[143] |
Shatz O, Holland P, Elazar Z, Simonsen A (2016) Complex relations between phospholipids, autophagy, and neutral lipids. Trends Biochem Sci 41:907–923
CrossRef
Google scholar
|
[144] |
Shibutani ST, Yoshimori T (2014) A current perspective of autophagosome biogenesis. Cell Res 24:58–68
CrossRef
Google scholar
|
[145] |
Shima T, Kirisako H, Nakatogawa H (2019) COPII vesicles contribute to autophagosomal membranes. J Cell Biol 218:1503–1510
CrossRef
Google scholar
|
[146] |
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
CrossRef
Google scholar
|
[147] |
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
CrossRef
Google scholar
|
[148] |
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
CrossRef
Google scholar
|
[149] |
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
CrossRef
Google scholar
|
[150] |
Stadel D, Millarte V, Tillmann KD, Huber J, Tamin-Yecheskel BC, Akutsu M, Demishtein A, Ben-Zeev B, Anikster Y, Perez F
CrossRef
Google scholar
|
[151] |
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
CrossRef
Google scholar
|
[152] |
Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q (2008) Identification of Barkor as a mammalian autophagy-specificfactor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci 105:19211–19216
CrossRef
Google scholar
|
[153] |
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
CrossRef
Google scholar
|
[154] |
Suzuki H, Osawa T, Fujioka Y, Noda NN (2017) Structural biology of the core autophagy machinery. Curr Opin Struct Biol 43:10–17
CrossRef
Google scholar
|
[155] |
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
CrossRef
Google scholar
|
[156] |
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
CrossRef
Google scholar
|
[157] |
Takahashi Y, He H, Tang Z, Hattori T, Liu Y, Young MM, Serfass JM, Chen L, Gebru M, Chen C
CrossRef
Google scholar
|
[158] |
Takahashi Y, Liang X, Hattori T, Tang Z, He H, Chen H, Liu X, Abraham T, Imamura-Kawasawa Y, Buchkovich NJ
CrossRef
Google scholar
|
[159] |
Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P
CrossRef
Google scholar
|
[160] |
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
CrossRef
Google scholar
|
[161] |
Thorburn A (2018) Autophagy and disease. J Biol Chem 293:5425–5430
CrossRef
Google scholar
|
[162] |
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
CrossRef
Google scholar
|
[163] |
Tsuboyama K, Koyama-Honda I, Sakamaki Y, Koike M, Morishita H, Mizushima N (2016) The ATG conjugation systems are important for degradation of the inner autophagosomal membrane. Science 354:1036–1041
CrossRef
Google scholar
|
[164] |
Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–174
CrossRef
Google scholar
|
[165] |
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
CrossRef
Google scholar
|
[166] |
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
CrossRef
Google scholar
|
[167] |
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
CrossRef
Google scholar
|
[168] |
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
CrossRef
Google scholar
|
[169] |
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
CrossRef
Google scholar
|
[170] |
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
CrossRef
Google scholar
|
[171] |
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
CrossRef
Google scholar
|
[172] |
Wherrett JR, Huterer S (1972) Enrichment of bis-(monoacylglyceryl) phosphate in lysosomes from rat liver. J Biol Chem 247:4114–4120
|
[173] |
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
CrossRef
Google scholar
|
[174] |
Wickner W, Rizo J (2017) A cascade of multiple proteins and lipids catalyzes membrane fusion. Mol Biol Cell 28:707–711
CrossRef
Google scholar
|
[175] |
Wollert T, Hurley JH (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464:864–869
CrossRef
Google scholar
|
[176] |
Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290–3298
CrossRef
Google scholar
|
[177] |
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
CrossRef
Google scholar
|
[178] |
Xu J, Camacho M, Xu Y, Esser V, Liu X, Trimbuch T, Pan YZ, Ma C, Tomchick DR, Rosenmund C
CrossRef
Google scholar
|
[179] |
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
CrossRef
Google scholar
|
[180] |
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
CrossRef
Google scholar
|
[181] |
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
CrossRef
Google scholar
|
[182] |
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
CrossRef
Google scholar
|
[183] |
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
CrossRef
Google scholar
|
[184] |
Yu L, Chen Y, Tooze SA (2018) Autophagy pathway: cellular and molecular mechanisms. Autophagy 14:207–215
CrossRef
Google scholar
|
[185] |
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
CrossRef
Google scholar
|
[186] |
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
CrossRef
Google scholar
|
[187] |
Zhang A, Meng Y, Li Q, Liang Y (2020) The ESCRT complex negatively regulates Erg6 degradation under specific glucose restriction conditions. Traffic
CrossRef
Google scholar
|
[188] |
Zhao YG, Zhang H (2019) Autophagosome maturation: an epic journey from the ER to lysosomes. J Cell Biol 218:757–770
CrossRef
Google scholar
|
[189] |
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
CrossRef
Google scholar
|
[190] |
Zhen Y, Spangenberg H, Munson MJ, Brech A, Schink KO, Tan KW, Sorensen V, Wenzel EM, Radulovic M, Engedal N
CrossRef
Google scholar
|
[191] |
Zhou F, Wu Z, Zhao M, Murtazina R, Cai J, Zhang A, Li R, Sun D, Li W, Zhao L
CrossRef
Google scholar
|
[192] |
Zinser E, Daum G (1995) Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast 11:493–536
CrossRef
Google scholar
|
[193] |
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
CrossRef
Google scholar
|
/
〈 | 〉 |