Autophagosome Maturation and Fusion

Journal of Molecular Biology

Volumn 429, Issue 4, 2017, Pages 486-496

  Reggiori, Fulvio ^a   Ungermann, Christian ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

ATG protein; autophagosome; lysosome; membrane fusion; SNARE

Indexed keywords

ANIMAL; AUTOPHAGOSOME; CELL FUSION; CELL MATURATION; CELL VACUOLE; ENDOSOME; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST; AUTOPHAGY; CYTOSOL; HUMAN; MAMMAL; METABOLISM; PHYSIOLOGY;

SNARE PROTEIN;

ANIMALS; AUTOPHAGOSOMES; AUTOPHAGY; CYTOSOL; ENDOSOMES; HUMANS; LYSOSOMES; MAMMALS; SNARE PROTEINS; YEASTS;

EID: 85009485546     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2017.01.002     Document Type: Review

References (126)

1. [1] Arasaki, K., Shimizu, H., Mogari, H., Nishida, N., Hirota, N., Furuno, A., Kudo, Y., Baba, M., Baba, N., Cheng, J., et al. A role for the ancient SNARE syntaxin 17 in regulating mitochondrial division. Dev. Cell 32 (2015), 304–317.
2. [2] Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G., Ktistakis, N.T., Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182 (2008), 685–701.
3. [3] Balderhaar, H.J., Ungermann, C., CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J. Cell Sci. 126 (2013), 1307–1316.
4. [4] Betin, V.M., Singleton, B.K., Parsons, S.F., Anstee, D.J., Lane, J.D., Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy 9 (2013), 881–893.
5. [5] Bockler, S., Westermann, B., Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev. Cell 28 (2014), 450–458.
6. [6] Bröcker, C., Kuhlee, A., Gatsogiannis, C., Balderhaar, H.J., Hönscher, C., Engelbrecht-Vandré, S., Ungermann, C., Raunser, S., Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 1991–1996.
7. [7] Cadwell, K., Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat. Rev. Immunol. 16 (2016), 661–675.
8. [8] Cadwell, K., Liu, J.Y., Brown, S.L., Miyoshi, H., Loh, J., Lennerz, J.K., Kishi, C., Kc, W., Carrero, J.A., Hunt, S., et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456 (2008), 259–263.
9. [9] Carroll, B., Mohd-Naim, N., Maximiano, F., Frasa, M.A., McCormack, J., Finelli, M., Thoresen, S.B., Perdios, L., Daigaku, R., Francis, R.E., et al. The TBC/RabGAP Armus coordinates Rac1 and Rab7 functions during autophagy. Dev. Cell 25 (2013), 15–28.
10. [10] Cebollero, E., van der Vaart, A., Zhao, M., Rieter, E., Klionsky, D.J., Helms, J.B., Reggiori, F., Phosphatidylinositol-3-phosphate clearance plays a key role in autophagosome completion. Curr. Biol. 22 (2012), 1545–1553.
11. [11] Chavrier, P., Parton, R.G., Hauri, H.P., Simons, K., Zerial, M., Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62 (1990), 317–329.
12. [12] Cheever, M.L., Sato, T.K., de Beer, T., Kutateladze, T.G., Emr, S.D., Overduin, M., Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3 (2001), 613–618.
13. [13] Chen, D., Fan, W., Lu, Y., Ding, X., Chen, S., Zhong, Q., A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol. Cell 45 (2012), 629–641.
14. [14] Cheng, J., Fujita, A., Yamamoto, H., Tatematsu, T., Kakuta, S., Obara, K., Ohsumi, Y., Fujimoto, T., Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries. Nat. Commun., 5, 2014, 3207.
15. [15] Cui, Y., Zhao, Q., Gao, C., Ding, Y., Zeng, Y., Ueda, T., Nakano, A., Jiang, L., Activation of the Rab7 GTPase by the MON1–CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis. Plant Cell 26 (2014), 2080–2097.
16. [16] Cullup, T., Kho, A.L., Dionisi-Vici, C., Brandmeier, B., Smith, F., Urry, Z., Simpson, M.A., Yau, S., Bertini, E., McClelland, V., et al. Recessive mutations in EPG5 cause Vici syndrome, a multisystem disorder with defective autophagy. Nat. Genet. 45 (2013), 83–87.
17. [17] Darsow, T., Rieder, S.E., Emr, S.D., A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138 (1997), 517–529.
18. [18] de Lartigue, J., Polson, H., Feldman, M., Shokat, K., Tooze, S.A., Urbe, S., Clague, M.J., PIKfyve regulation of endosome-linked pathways. Traffic 10 (2009), 883–893.
19. [19] Diao, J., Liu, R., Rong, Y., Zhao, M., Zhang, J., Lai, Y., Zhou, Q., Wilz, L.M., Li, J., Vivona, S., et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature 520 (2015), 563–566.
20. [20] Dilcher, M., Kohler, B., von Mollard, G.F., Genetic interactions with the yeast Q-SNARE VTI1 reveal novel functions for the R-SNARE YKT6. J. Biol. Chem. 276 (2001), 34,537–34,544.
21. [21] Dowling, J.J., Low, S.E., Busta, A.S., Feldman, E.L., Zebrafish MTMR14 is required for excitation-contraction coupling, developmental motor function and the regulation of autophagy. Hum. Mol. Genet. 19 (2010), 2668–2681.
22. [22] Du, W., Su, Q.P., Chen, Y., Zhu, Y., Jiang, D., Rong, Y., Zhang, S., Zhang, Y., Ren, H., Zhang, C., et al. Kinesin 1 drives autolysosome tubulation. Dev. Cell 37 (2016), 326–336.
23. [23] Fader, C.M., Sanchez, D.G., Mestre, M.B., Colombo, M.I., TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta 1793 (2009), 1901–1916.
24. [24] Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerod, L., Fisher, E.M., Isaacs, A., Brech, A., Stenmark, H., Simonsen, A., Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179 (2007), 485–500.
25. [25] Fischer von Mollard, G., Stevens, T.H., The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Mol. Biol. Cell 10 (1999), 1719–1732.
26. [26] Fullgrabe, J., Ghislat, G., Cho, D.H., Rubinsztein, D.C., Transcriptional regulation of mammalian autophagy at a glance. J. Cell Sci. 129 (2016), 3059–3066.
27. [27] Ge, L., Melville, D., Zhang, M., Schekman, R., The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife, 2, 2013, e00947, 10.7554/eLife.00947.
28. [28] Gillingham, A.K., Sinka, R., Torres, I.L., Lilley, K.S., Munro, S., Toward a comprehensive map of the effectors of Rab GTPases. Dev. Cell 31 (2014), 358–373.
29. [29] Graef, M., Friedman, J.R., Graham, C., Babu, M., Nunnari, J., ER exit sites are physical and functional core autophagosome biogenesis components. Mol. Biol. Cell 24 (2013), 2918–2931.
30. [30] Guo, P., Hu, T., Zhang, J., Jiang, S., Wang, X., Sequential action of Caenorhabditis elegans Rab GTPases regulates phagolysosome formation during apoptotic cell degradation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 18,016–18,021.
31. [31] Gutierrez, M.G., Munafo, D.B., Beron, W., Colombo, M.I., Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117 (2004), 2687–2697.
32. [32] Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., et al. Autophagosomes form at ER-mitochondria contact sites. Nature 495 (2013), 389–393.
33. [33] Harding, T.M., Morano, K.A., Scott, S.V., Klionsky, D.J., Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131 (1995), 591–602.
34. [34] Hegedűs, K., Takats, S., Boda, A., Jipa, A., Nagy, P., Varga, K., Kovacs, A.L., Juhasz, G., The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy. Mol. Biol. Cell 27 (2016), 3132–3142.
35. [35] Heuser, J., Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 108 (1989), 855–864.
36. [36] Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., et al. A ubiquitin-like system mediates protein lipidation. Nature 408 (2000), 488–492.
37. [37] Ishihara, N., Hamasaki, M., Yokota, S., Suzuki, K., Kamada, Y., Kihara, A., Yoshimori, T., Noda, T., Ohsumi, Y., Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell 12 (2001), 3690–3702.
38. [38] Itakura, E., Kishi-Itakura, C., Mizushima, N., The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151 (2012), 1256–1269.
39. [39] Jahreiss, L., Menzies, F.M., Rubinsztein, D.C., The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9 (2008), 574–587.
40. [40] Jefferies, H.B., Cooke, F.T., Jat, P., Boucheron, C., Koizumi, T., Hayakawa, M., Kaizawa, H., Ohishi, T., Workman, P., Waterfield, M.D., et al. A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep. 9 (2008), 164–170.
41. [41] Jewell, J.L., Russell, R.C., Guan, K.L., Amino acid signalling upstream of mTOR. Nat. Rev. Mol. Cell Biol. 14 (2013), 133–139.
42. [42] Jiang, P., Nishimura, T., Sakamaki, Y., Itakura, E., Hatta, T., Natsume, T., Mizushima, N., The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol. Biol. Cell 25 (2014), 1327–1337.
43. [43] Khatter, D., Raina, V.B., Dwivedi, D., Sindhwani, A., Bahl, S., Sharma, M., The small GTPase Arl8b regulates assembly of the mammalian HOPS complex on lysosomes. J. Cell Sci. 128 (2015), 1746–1761.
44. [44] Kim, J., Huang, W.-P., Stromhaug, P.E., Klionsky, D.J., Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277 (2002), 763–773.
45. [45] Kinchen, J.M., Ravichandran, K.S., Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464 (2010), 778–782.
46. [46] Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., Ohsumi, Y., Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147 (1999), 435–446.
47. [47] Knaevelsrud, H., Soreng, K., Raiborg, C., Haberg, K., Rasmuson, F., Brech, A., Liestol, K., Rusten, T.E., Stenmark, H., Neufeld, T.P., et al. Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J. Cell Biol. 202 (2013), 331–349.
48. [48] Korolchuk, V.I., Saiki, S., Lichtenberg, M., Siddiqi, F.H., Roberts, E.A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F.M., et al. Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 13 (2011), 453–460.
49. [49] Kraft, C., Martens, S., Mechanisms and regulation of autophagosome formation. Curr. Opin. Cell Biol. 24 (2012), 496–501.
50. [50] Kraft, C., Peter, M., Hofmann, K., Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12 (2010), 836–841.
51. [51] Krämer, L., Ungermann, C., HOPS drives vacuole fusion by binding the vacuolar SNARE complex and the Vam7 PX domain via two distinct sites. Mol. Biol. Cell 22 (2011), 2601–2611.
52. [52] Kucharczyk, R., Kierzek, A.M., Slonimski, P.P., Rytka, J., The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J. Cell Sci. 114 (2001), 3137–3145.
53. [53] Kümmel, D., Ungermann, C., Principles of membrane tethering and fusion in endosome and lysosome biogenesis. Curr. Opin. Cell Biol. 29 (2014), 61–66.
54. [54] Lamb, C.A., Yoshimori, T., Tooze, S.A., The autophagosome: origins unknown, biogenesis complex. Nat. Rev. Mol. Cell Biol. 14 (2013), 759–774.
55. [55] Lang, T., Reiche, S., Straub, M., Bredschneider, M., Thumm, M., Autophagy and the Cvt pathway both depend on AUT9. J. Bacteriol. 182 (2000), 2125–2133.
56. [56] Lin, X., Yang, T., Wang, S., Wang, Z., Yun, Y., Sun, L., Zhou, Y., Xu, X., Akazawa, C., Hong, W., et al. RILP interacts with HOPS complex via VPS41 subunit to regulate endocytic trafficking. Sci. Rep., 4, 2014, 7282.
57. [57] Liu, X., Mao, K., Yu, A.Y., Omairi-Nasser, A., Austin, J. II, Glick, B.S., Yip, C.K., Klionsky, D.J., The Atg17–Atg31–Atg29 complex coordinates with Atg11 to recruit the Vam7 SNARE and mediate autophagosome-vacuole fusion. Curr. Biol. 26 (2016), 150–160.
58. [58] Lobingier, B.T., Merz, A.J., Sec1/Munc18 protein Vps33 binds to SNARE domains and the quaternary SNARE complex. Mol. Biol. Cell 23 (2012), 4611–4622.
59. [59] Longatti, A., Lamb, C.A., Razi, M., Yoshimura, S., Barr, F.A., Tooze, S.A., TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes. J. Cell Biol. 197 (2012), 659–675.
60. [60] Lürick, A., Kuhlee, A., Brocker, C., Kümmel, D., Raunser, S., Ungermann, C., The Habc domain of the SNARE Vam3 interacts with the HOPS tethering complex to facilitate vacuole fusion. J. Biol. Chem. 290 (2015), 5405–5413.
61. [61] Mari, M., Griffith, J., Rieter, E., Krishnappa, L., Klionsky, D.J., Reggiori, F., An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J. Cell Biol. 190 (2010), 1005–1022.
62. [62] Martin, S., Harper, C.B., May, L.M., Coulson, E.J., Meunier, F.A., Osborne, S.L., Inhibition of PIKfyve by YM-201636 dysregulates autophagy and leads to apoptosis-independent neuronal cell death. PLoS One, 8, 2013, e60152, 10.1371/journal.pone.0060152.
63. [63] Martinez, J., Cunha, L.D., Park, S., Yang, M., Lu, Q., Orchard, R., Li, Q.Z., Yan, M., Janke, L., Guy, C., et al. Noncanonical autophagy inhibits the autoinflammatory, lupus-like response to dying cells. Nature 533 (2016), 115–119.
64. [64] Matsunaga, K., Saitoh, T., Tabata, K., Omori, H., Satoh, T., Kurotori, N., Maejima, I., Shirahama-Noda, K., Ichimura, T., Isobe, T., et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 11 (2009), 385–396.
65. [65] McCartney, A.J., Zhang, Y., Weisman, L.S., Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays 36 (2014), 52–64.
66. [66] McEwan, D.G., Popovic, D., Gubas, A., Terawaki, S., Suzuki, H., Stadel, D., Coxon, F.P., Miranda de Stegmann, D., Bhogaraju, S., Maddi, K., et al. PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Mol. Cell 57 (2015), 39–54.
67. [67] McEwan, D.G., Richter, B., Claudi, B., Wigge, C., Wild, P., Farhan, H., McGourty, K., Coxon, F.P., Franz-Wachtel, M., Perdu, B., et al. PLEKHM1 regulates Salmonella-containing vacuole biogenesis and infection. Cell Host Microbe 17 (2015), 58–71.
68. [68] McLelland, G.L., Lee, S.A., McBride, H.M., Fon, E.A., Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system. J. Cell Biol. 214 (2016), 275–291.
69. [69] Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M., Ohsumi, Y., A protein conjugation system essential for autophagy. Nature 395 (1998), 395–398.
70. [70] Mizushima, N., Yoshimori, T., Ohsumi, Y., The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27 (2011), 107–132.
71. [71] Mochizuki, Y., Ohashi, R., Kawamura, T., Iwanari, H., Kodama, T., Naito, M., Hamakubo, T., Phosphatidylinositol 3-phosphatase myotubularin-related protein 6 (MTMR6) is regulated by small GTPase Rab1B in the early secretory and autophagic pathways. J. Biol. Chem. 288 (2013), 1009–1021.
72. [72] Monastyrska, I., Rieter, E., Klionsky, D.J., Reggiori, F., Multiple roles of the cytoskeleton in autophagy. Biol. Rev. Camb. Philos. Soc. 84 (2009), 431–448.
73. [73] Nair, U., Yen, W.L., Mari, M., Cao, Y., Xie, Z., Baba, M., Reggiori, F., Klionsky, D.J., A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy 8 (2012), 780–793.
74. [74] Nakatogawa, H., Ichimura, Y., Ohsumi, Y., Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130 (2007), 165–178.
75. [75] Nakatogawa, H., Ishii, J., Asai, E., Ohsumi, Y., Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 8 (2012), 177–186.
76. [76] Nakatogawa, H., Suzuki, K., Kamada, Y., Ohsumi, Y., Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10 (2009), 458–467.
77. [77] Nguyen, T.N., Padman, B.S., Usher, J., Oorschot, V., Ramm, G., Lazarou, M., Atg8 family LC3/GABARAP proteins are crucial for autophagosome-lysosome fusion but not autophagosome formation during PINK1/parkin mitophagy and starvation. J. Cell Biol. 215 (2016), 857–874.
78. [78] Nicot, A.S., Fares, H., Payrastre, B., Chisholm, A.D., Labouesse, M., Laporte, J., The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. Mol. Biol. Cell 17 (2006), 3062–3074.
79. [79] Noda, T., Kim, J., Huang, W.-P., Baba, M., Tokunaga, C., Ohsumi, Y., Klionsky, D.J., Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J. Cell Biol. 148 (2000), 465–480.
80. [80] Noda, T., Ohsumi, Y., Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273 (1998), 3963–3966.
81. [81] Nordmann, M., Cabrera, M., Perz, A., Brocker, C., Ostrowicz, C., Engelbrecht-Vandre, S., Ungermann, C., The Mon1–Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr. Biol. 20 (2010), 1654–1659.
82. [82] Odorizzi, G., Babst, M., Emr, S.D., Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95 (1998), 847–858.
83. [83] Ohashi, Y., Munro, S., Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol. Biol. Cell 21 (2010), 3998–4008.
84. [84] Orsi, A., Razi, M., Dooley, H.C., Robinson, D., Weston, A.E., Collinson, L.M., Tooze, S.A., Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23 (2012), 1860–1873.
85. [85] Parrish, W.R., Stefan, C.J., Emr, S.D., Essential role for the myotubularin-related phosphatase Ymr1p and the synaptojanin-like phosphatases Sjl2p and Sjl3p in regulation of phosphatidylinositol 3-phosphate in yeast. Mol. Biol. Cell 15 (2004), 3567–3579.
86. [86] Patel, K.K., Miyoshi, H., Beatty, W.L., Head, R.D., Malvin, N.P., Cadwell, K., Guan, J.L., Saitoh, T., Akira, S., Seglen, P.O., et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J. 32 (2013), 3130–3144.
87. [87] Pous, C., Codogno, P., Lysosome positioning coordinates mTORC1 activity and autophagy. Nat. Cell Biol. 13 (2011), 342–344.
88. [88] Proikas-Cezanne, T., Robenek, H., Freeze-fracture replica immunolabelling reveals human WIPI-1 and WIPI-2 as membrane proteins of autophagosomes. J. Cell. Mol. Med. 15 (2011), 2007–2010.
89. [89] Puri, C., Renna, M., Bento, C.F., Moreau, K., Rubinsztein, D.C., Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154 (2013), 1285–1299.
90. [90] Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C., Rubinsztein, D.C., Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12 (2010), 747–757.
91. [91] Razi, M., Chan, E.Y., Tooze, S.A., Early endosomes and endosomal coatomer are required for autophagy. J. Cell Biol. 185 (2009), 305–321.
92. [92] Reggiori, F., Tucker, K.A., Stromhaug, P.E., Klionsky, D.J., The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 6 (2004), 79–90.
93. [93] Rong, Y., Liu, M., Ma, L., Du, W., Zhang, H., Tian, Y., Cao, Z., Li, Y., Ren, H., Zhang, C., et al. Clathrin and phosphatidylinositol-4,5-bisphosphate regulate autophagic lysosome reformation. Nat. Cell Biol. 14 (2012), 924–934.
94. [94] Rong, Y., McPhee, C.K., Deng, S., Huang, L., Chen, L., Liu, M., Tracy, K., Baehrecke, E.H., Yu, L., Lenardo, M.J., Spinster is required for autophagic lysosome reformation and mTOR reactivation following starvation. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 7826–7831.
95. [95] Rusten, T.E., Vaccari, T., Lindmo, K., Rodahl, L.M., Nezis, I.P., Sem-Jacobsen, C., Wendler, F., Vincent, J.P., Brech, A., Bilder, D., et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 17 (2007), 1817–1825.
96. [96] Sanchez-Wandelmer, J., Ktistakis, N.T., Reggiori, F., ERES: sites for autophagosome biogenesis and maturation?. J. Cell Sci. 128 (2015), 185–192.
97. [97] Sanjuan, M.A., Dillon, C.P., Tait, S.W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J.L., Withoff, S., et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450 (2007), 1253–1257.
98. [98] Seals, D.F., Eitzen, G., Margolis, N., Wickner, W.T., Price, A., A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 9402–9407.
99. [99] Stolz, A., Ernst, A., Dikic, I., Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 16 (2014), 495–501.
100. [100] Stroupe, C., Collins, K.M., Fratti, R.A., Wickner, W., Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J. 25 (2006), 1579–1589.
101. [101] Suzuki, K., Akioka, M., Kondo-Kakuta, C., Yamamoto, H., Ohsumi, Y., Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J. Cell Sci. 126 (2013), 2534–2544.
102. [102] Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T., Ohsumi, Y., The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20 (2001), 5971–5981.
103. [103] Suzuki, K., Kubota, Y., Sekito, T., Ohsumi, Y., Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12 (2007), 209–218.
104. [104] Tabata, K., Matsunaga, K., Sakane, A., Sasaki, T., Noda, T., Yoshimori, T., Rubicon and PLEKHM1 negatively regulate the endocytic/autophagic pathway via a novel Rab7-binding domain. Mol. Biol. Cell 21 (2010), 4162–4172.
105. [105] Taguchi-Atarashi, N., Hamasaki, M., Matsunaga, K., Omori, H., Ktistakis, N.T., Yoshimori, T., Noda, T., Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic 11 (2010), 468–478.
106. [106] Takats, S., Pircs, K., Nagy, P., Varga, A., Karpati, M., Hegedus, K., Kramer, H., Kovacs, A.L., Sass, M., Juhasz, G., Interaction of the HOPS complex with syntaxin 17 mediates autophagosome clearance in Drosophila. Mol. Biol. Cell 25 (2014), 1338–1354.
107. [107] Terawaki, S., Camosseto, V., Prete, F., Wenger, T., Papadopoulos, A., Rondeau, C., Combes, A., Rodriguez Rodrigues, C., Vu Manh, T.P., Fallet, M., et al. RUN and FYVE domain-containing protein 4 enhances autophagy and lysosome tethering in response to interleukin-4. J. Cell Biol. 210 (2015), 1133–1152.
108. [108] Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M., Wolf, D.H., Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349 (1994), 275–280.
109. [109] Torggler, R., Papinski, D., Brach, T., Bas, L., Schuschnig, M., Pfaffenwimmer, T., Rohringer, S., Matzhold, T., Schweida, D., Brezovich, A., et al. Two independent pathways within selective autophagy converge to activate Atg1 kinase at the vacuole. Mol. Cell 64 (2016), 221–235.
110. [110] Tsuboyama, K., Koyama-Honda, I., Sakamaki, Y., Koike, M., Morishita, H., Mizushima, N., The ATG conjugation systems are important for degradation of the inner autophagosomal membrane. Science 354 (2016), 1036–1041.
111. [111] Tsukada, M., Ohsumi, Y., Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333 (1993), 169–174.
112. [112] van der Kant, R., Fish, A., Janssen, L., Janssen, H., Krom, S., Ho, N., Brummelkamp, T., Carette, J., Rocha, N., Neefjes, J., Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J. Cell Sci. 126 (2013), 3462–3474.
113. [113] van der Vaart, A., Griffith, J., Reggiori, F., Exit from the Golgi is required for the expansion of the autophagosomal phagophore in yeast Saccharomyces cerevisiae. Mol. Biol. Cell 21 (2010), 2270–2284.
114. [114] Vergne, I., Roberts, E., Elmaoued, R.A., Tosch, V., Delgado, M.A., Proikas-Cezanne, T., Laporte, J., Deretic, V., Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J. 28 (2009), 2244–2258.
115. [115] Wang, C.-W., Stromhaug, P.E., Shima, J., Klionsky, D.J., The Ccz1–Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J. Biol. Chem. 277 (2002), 47,917–47,927.
116. [116] Wang, C.W., Stromhaug, P.E., Kauffman, E.J., Weisman, L.S., Klionsky, D.J., Yeast homotypic vacuole fusion requires the Ccz1–Mon1 complex during the tethering/docking stage. J. Cell Biol. 163 (2003), 973–985.
117. [117] Wang, Z., Miao, G., Xue, X., Guo, X., Yuan, C., Wang, Z., Zhang, G., Chen, Y., Feng, D., Hu, J., et al. The vici syndrome protein EPG5 is a Rab7 effector that determines the fusion specificity of autophagosomes with late endosomes/lysosomes. Mol. Cell 63 (2016), 781–795.
118. [118] Weidberg, H., Shpilka, T., Shvets, E., Abada, A., Shimron, F., Elazar, Z., LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Dev. Cell 20 (2011), 444–454.
119. [119] Weidberg, H., Shvets, E., Shpilka, T., Shimron, F., Shinder, V., Elazar, Z., LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29 (2010), 1792–1802.
120. [120] Wu, Y., Cheng, S., Zhao, H., Zou, W., Yoshina, S., Mitani, S., Zhang, H., Wang, X., PI3P phosphatase activity is required for autophagosome maturation and autolysosome formation. EMBO Rep. 15 (2014), 973–981.
121. [121] Wurmser, A.E., Sato, T.K., Emr, S.D., New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151 (2000), 551–562.
122. [122] Yamamoto, H., Kakuta, S., Watanabe, T.M., Kitamura, A., Sekito, T., Kondo-Kakuta, C., Ichikawa, R., Kinjo, M., Ohsumi, Y., Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J. Cell Biol. 198 (2012), 219–233.
123. [123] Yang, Z., Klionsky, D.J., Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22 (2010), 124–131.
124. [124] Young, A.R.J., Chan, E.Y.W., Hu, X.W., Köchl, R., Crawshaw, S.G., High, S., Hailey, D.W., Lippincott-Schwartz, J., Tooze, S.A., Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119 (2006), 3888–3900.
125. [125] Yu, L., McPhee, C.K., Zheng, L., Mardones, G.A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F., et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465 (2010), 942–946.
126. [126] Yu, Z.Q., Ni, T., Hong, B., Wang, H.Y., Jiang, F.J., Zou, S., Chen, Y., Zheng, X.L., Klionsky, D.J., Liang, Y., et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy 8 (2012), 883–892.