Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Prot Cell    2010, Vol. 1 Issue (10) : 907-915    https://doi.org/10.1007/s13238-010-0121-z      PMID: 21204017
REVIEW
The late stage of autophagy: cellular events and molecular regulation
Jingjing Tong1,2, Xianghua Yan2, Li Yu1()
1. State Key Laboratory of Biomembrane and Membrane Biotechnology, School of Life Science, Tsinghua University, Beijing 100084, China; 2. College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan 430070, China
 Download: PDF(160 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Autophagy is an intracellular degradation system that delivers cytoplasmic contents to the lysosome for degradation. It is a “self-eating” process and plays a “house-cleaner” role in cells. The complex process consists of several sequential steps—induction, autophagosome formation, fusion of lysosome and autophagosome, degradation, efflux transportation of degradation products, and autophagic lysosome reformation. In this review, the cellular and molecular regulations of late stage of autophagy, including cellular events after fusion step, are summarized.
Keywords autophagy      autophagosome      lysosome      fusion      degradation     
Corresponding Author(s): Yu Li,Email:liyulab@mail.tsinghua.edu.cn   
Issue Date: 01 October 2010
 Cite this article:   
Li Yu,Jingjing Tong,Xianghua Yan. The late stage of autophagy: cellular events and molecular regulation[J]. Prot Cell, 2010, 1(10): 907-915.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-010-0121-z
https://academic.hep.com.cn/pac/EN/Y2010/V1/I10/907
1 Aplin, A., Jasionowski, T., Tuttle, D.L., Lenk, S.E., and Dunn, W.A. Jr. (1992). Cytoskeletal elements are required for the formation and maturation of autophagic vacuoles. J Cell Physiol 152, 458–466 .
doi: 10.1002/jcp.1041520304
2 Atlashkin, V., Kreykenbohm, V., Eskelinen, E.-L., Wenzel, D., Fayyazi, A., and Fischer von Mollard, G. (2003). Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8. Mol Cell Biol 23, 5198–5207 .
doi: 10.1128/MCB.23.15.5198-5207.2003
3 Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G., and Ktistakis, N.T. (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182, 685–701 .
doi: 10.1083/jcb.200803137
4 Bache, K.G., Raiborg, C., Mehlum, A., Madshus, I.H., and Stenmark, H. (2002). Phosphorylation of Hrs downstream of the epidermal growth factor receptor. Eur J Biochem 269, 3881–3887 .
doi: 10.1046/j.1432-1033.2002.03046.x
5 Block, M.R., Glick, B.S., Wilcox, C.A., Wieland, F.T., and Rothman, J.E. (1988). Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci U S A 85, 7852–7856 .
doi: 10.1073/pnas.85.21.7852
6 Cai, H., Reinisch, K., and Ferro-Novick, S. (2007). Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12, 671–682 .
doi: 10.1016/j.devcel.2007.04.005
7 Callebaut, I., de Gunzburg, J., Goud, B., and Mornon, J.P. (2001). RUN domains: a new family of domains involved in Ras-like GTPase signaling. Trends Biochem Sci 26, 79–83 .
doi: 10.1016/S0968-0004(00)01730-8
8 Cao, X., and Barlowe, C. (2000). Asymmetric requirements for a Rab GTPase and SNARE proteins in fusion of COPII vesicles with acceptor membranes. J Cell Biol 149, 55–66 .
doi: 10.1083/jcb.149.1.55
9 Crighton, D., Wilkinson, S., O’Prey, J., Syed, N., Smith, P., Harrison, P.R., Gasco, M., Garrone, O., Crook, T., and Ryan, K.M. (2006). DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126, 121–134 .
10 Darsow, T., Rieder, S.E., and Emr, S.D. (1997). A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J Cell Biol 138, 517–529 .
doi: 10.1083/jcb.138.3.517
11 Dulubova, I., Yamaguchi, T., Wang, Y., Südhof, T.C., and Rizo, J. (2001). Vam3p structure reveals conserved and divergent properties of syntaxins. Nat Struct Biol 8, 258–264 .
doi: 10.1038/85012
12 Egami, Y., Kiryu-Seo, S., Yoshimori, T., and Kiyama, H. (2005). Induced expressions of Rab24 GTPase and LC3 in nerve-injured motor neurons. Biochem Biophys Res Commun 337, 1206–1213 .
doi: 10.1016/j.bbrc.2005.09.171
13 Epple, U.D., Suriapranata, I., Eskelinen, E.-L., and Thumm, M. (2001). Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J Bacteriol 183, 5942–5955 .
doi: 10.1128/JB.183.20.5942-5955.2001
14 Epple, U.D., Eskelinen, E.L., and Thumm, M. (2003). Intravacuolar membrane lysis in Saccharomyces cerevisiae. Does vacuolar targeting of Cvt17/Aut5p affect its function? J Biol Chem 278, 7810–7821 .
doi: 10.1074/jbc.M209309200
15 Eskelinen, E.L. (2005). Maturation of autophagic vacuoles in mammalian cells. Autophagy 1, 1–10 .
doi: 10.4161/auto.1.1.1270
16 Eskelinen, E.L., Tanaka, Y., and Saftig, P. (2003). At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol 13, 137–145 .
doi: 10.1016/S0962-8924(03)00005-9
17 Eskelinen, E.L., Schmidt, C.K., Neu, S., Willenborg, M., Fuertes, G., Salvador, N., Tanaka, Y., Lüllmann-Rauch, R., Hartmann, D., Heeren, J., . (2004). Disturbed cholesterol traffic but normal proteolytic function in LAMP-1/LAMP-2 double-deficient fibroblasts. Mol Biol Cell 15, 3132–3145 .
doi: 10.1091/mbc.E04-02-0103
18 Fader, C.M., Sánchez, D., Furlán, M., and Colombo, M.I. (2008). Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 9, 230–250 .
doi: 10.1111/j.1600-0854.2007.00677.x
19 Fass, E., Shvets, E., Degani, I., Hirschberg, K., and Elazar, Z. (2006). Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 281, 36303–36316 .
doi: 10.1074/jbc.M607031200
20 Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D., and Brown, P.O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11, 4241–4257 .
21 Gill, S.R., Schroer, T.A., Szilak, I., Steuer, E.R., Sheetz, M.P., and Cleveland, D.W. (1991). Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J Cell Biol 115, 1639–1650 .
doi: 10.1083/jcb.115.6.1639
22 Gutierrez, M.G., Munafó, D.B., Berón, W., and Colombo, M.I. (2004). Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117, 2687–2697 .
doi: 10.1242/jcs.01114
23 Hamasaki, M., and Yoshimori, T. (2010). Where do they come from? Insight into autophagosome formation. FEBS Lett 584, 1296–1301 .
doi: 10.1016/j.febslet.2010.02.061
24 Hayakawa, A., Hayes, S.J., Lawe, D.C., Sudharshan, E., Tuft, R., Fogarty, K., Lambright, D., and Corvera, S. (2004). Structural basis for endosomal targeting by FYVE domains. J Biol Chem 279, 5958–5966 .
doi: 10.1074/jbc.M310503200
25 Huynh, K.K., Eskelinen, E.L., Scott, C.C., Malevanets, A., Saftig, P., and Grinstein, S. (2007). LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26, 313–324 .
doi: 10.1038/sj.emboj.7601511
26 Itoh, T., Fujita, N., Kanno, E., Yamamoto, A., Yoshimori, T., and Fukuda, M. (2008). Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19, 2916–2925 .
doi: 10.1091/mbc.E07-12-1231
27 J?ger, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P., and Eskelinen, E.L. (2004). Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117, 4837–4848 .
doi: 10.1242/jcs.01370
28 Jahn, R., and Scheller, R.H. (2006). SNAREs—engines for membrane fusion. Nat Rev Mol Cell Biol 7, 631–643 .
doi: 10.1038/nrm2002
29 Jahreiss, L., Menzies, F.M., and Rubinsztein, D.C. (2008). The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9, 574–587 .
doi: 10.1111/j.1600-0854.2008.00701.x
30 Kanazawa, C., Morita, E., Yamada, M., Ishii, N., Miura, S., Asao, H., Yoshimori, T., and Sugamura, K. (2003). Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochem Biophys Res Commun 309, 848–856 .
doi: 10.1016/j.bbrc.2003.08.078
31 Kimura, S., Noda, T., and Yoshimori, T. (2008). Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 33, 109–122 .
doi: 10.1247/csf.08005
32 Klionsky, D.J. (2005). The molecular machinery of autophagy: unanswered questions. J Cell Sci 118, 7–18 .
doi: 10.1242/jcs.01620
33 Klionsky, D.J. (2007). Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8, 931–937 .
doi: 10.1038/nrm2245
34 Kouno, T., Mizuguchi, M., Tanida, I., Ueno, T., Kanematsu, T., Mori, Y., Shinoda, H., Hirata, M., Kominami, E., and Kawano, K. (2005). Solution structure of microtubule-associated protein light chain 3 and identification of its functional subdomains. J Biol Chem 280, 24610–24617 .
doi: 10.1074/jbc.M413565200
35 Kucharczyk, R., Dupre, S., Avaro, S., Haguenauer-Tsapis, R., S?onimski, P.P., and Rytka, J. (2000). The novel protein Ccz1p required for vacuolar assembly in Saccharomyces cerevisiae functions in the same transport pathway as Ypt7p. J Cell Sci 113, 4301–4311 .
36 Kucharczyk, R., Kierzek, A.M., Slonimski, P.P., and Rytka, J. (2001). The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J Cell Sci 114, 3137–3145 .
37 Kutateladze, T.G. (2006). Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim Biophys Acta 1761, 868–877 .
38 Lakadamyali, M., Rust, M.J., Babcock, H.P., and Zhuang, X. (2003). Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100, 9280–9285 .
doi: 10.1073/pnas.0832269100
39 Langosch, D., Hofmann, M., and Ungermann, C. (2007). The role of transmembrane domains in membrane fusion. Cell Mol Life Sci 64, 850–864 .
doi: 10.1007/s00018-007-6439-x
40 Lee, J.A., Beigneux, A., Ahmad, S.T., Young, S.G., and Gao, F.B. (2007). ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr Biol 17, 1561–1567 .
doi: 10.1016/j.cub.2007.07.029
41 Liang, C., Feng, P., Ku, B., Dotan, I., Canaani, D., Oh, B.H., and Jung, J.U. (2006). Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 8, 688–699 .
doi: 10.1038/ncb1426
42 Liang, C., Feng, P., Ku, B., Oh, B.H., Jung, J.U., Oh, B., and Jung, J. (2007). UVRAG: a new player in autophagy and tumor cell growth. Autophagy 3, 69–71 .
43 Liang, C., Lee, J.S., Inn, K.S., Gack, M.U., Li, Q., Roberts, E.A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., . (2008a). Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10, 776–787 .
doi: 10.1038/ncb1740
44 Liang, C., Sir, D., Lee, S., Ou, J.H., and Jung, J.U. (2008b). Beyond autophagy: the role of UVRAG in membrane trafficking. Autophagy 4, 817–820 .
45 Lindmo, K., Simonsen, A., Brech, A., Finley, K., Rusten, T.E., and Stenmark, H. (2006). A dual function for Deep orange in programmed autophagy in the Drosophila melanogaster fat body. Exp Cell Res 312, 2018–2027 .
doi: 10.1016/j.yexcr.2006.03.002
46 Lloyd, J.B. (1996). Metabolite efflux and influx across the lysosome membrane. Subcell Biochem 27, 361–386 .
47 Lloyd, T.E., Atkinson, R., Wu, M.N., Zhou, Y., Pennetta, G., and Bellen, H.J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261–269 .
48 Longatti, A., and Tooze, S.A. (2009). Vesicular trafficking and autophagosome formation. Cell Death Differ 16, 956–965 .
doi: 10.1038/cdd.2009.39
49 Lupas, A., Van Dyke, M., and Stock, J. (1991). Predicting coiled coils from protein sequences. Science 252, 1162–1164 .
doi: 10.1126/science.252.5009.1162
50 Mann, S.S., and Hammarback, J.A. (1994). Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B. J Biol Chem 269, 11492–11497 .
51 Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., . (2009). CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37, D205–D210 .
doi: 10.1093/nar/gkn845
52 Marino, Z., and Heidi, M. (2001). Rab proteins as membrane prganizers. Natl Rev 2, 107–118 .
doi: 10.1038/35052055
53 Mechler, B., and Wolf, D.H. (1981). Analysis of proteinase A function in yeast. Eur J Biochem 121, 47–52 .
doi: 10.1111/j.1432-1033.1981.tb06427.x
54 Mehrpour, M., Esclatine, A., Beau, I., and Codogno, P. (2010). Overview of macroautophagy regulation in mammalian cells. Cell Res 20, 748–762 .
doi: 10.1038/cr.2010.82
55 Mesa, R., Salomón, C., Roggero, M., Stahl, P.D., and Mayorga, L.S. (2001). Rab22a affects the morphology and function of the endocytic pathway. J Cell Sci 114, 4041–4049 .
56 Mima, J., Hickey, C.M., Xu, H., Jun, Y., and Wickner, W. (2008). Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. EMBO J 27, 2031–2042 .
doi: 10.1038/emboj.2008.139
57 Mizushima, N. (2007). Autophagy: process and function. Genes Dev 21, 2861–2873 .
doi: 10.1101/gad.1599207
58 Munafó, D.B., and Colombo, M.I. (2002). Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24. Traffic 3 , 472–482 .
doi: 10.1034/j.1600-0854.2002.30704.x
59 Nakamura, N., Matsuura, A., Wada, Y., and Ohsumi, Y. (1997). Acidification of vacuoles is required for autophagic degradation in the yeast, Saccharomyces cerevisiae. J Biochem 121, 338–344 .
60 Nakatogawa, H., Suzuki, K., Kamada, Y., and Ohsumi, Y. (2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10, 458–467 .
doi: 10.1038/nrm2708
61 Nara, A., Mizushima, N., Yamamoto, A., Kabeya, Y., Ohsumi, Y., and Yoshimori, T. (2002). SKD1 AAA ATPase-dependent endosomal transport is involved in autolysosome formation. Cell Struct Funct 27, 29–37 .
doi: 10.1247/csf.27.29
62 Nichols, B.J., Ungermann, C., Pelham, H.R.B., Wickner, W.T., and Haas, A. (1997). Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature 387, 199–202 .
doi: 10.1038/387199a0
63 Novick, P., and Zerial, M. (1997). The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 9, 496–504 .
doi: 10.1016/S0955-0674(97)80025-7
64 Odorizzi, G., Babst, M., and Emr, S.D. (1998). Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847–858 .
65 Odorizzi, G., Babst, M., and Emr, S.D. (2000). Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci 25, 229–235 .
doi: 10.1016/S0968-0004(00)01543-7
66 Olkkonen, V.M., Dupree, P., Killisch, I., Lütcke, A., Zerial, M., and Simons, K. (1993). Molecular cloning and subcellular localization of three GTP-binding proteins of the rab subfamily. J Cell Sci 106, 1249–1261 .
67 Pankiv, S., Alemu, E.A., Brech, A., Bruun, J.A., Lamark, T., Overvatn, A., Bj?rk?y, G., and Johansen, T. (2010). FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol 188, 253–269 .
doi: 10.1083/jcb.200907015
68 Parlati, F., McNew, J.A., Fukuda, R., Miller, R., S?llner, T.H., and Rothman, J.E. (2000). Topological restriction of SNARE-dependent membrane fusion. Nature 407, 194–198 .
doi: 10.1038/35025076
69 Parr, C.L., Keates, R.A., Bryksa, B.C., Ogawa, M., and Yada, R.Y. (2007). The structure and function of Saccharomyces cerevisiae proteinase A. Yeast 24, 467–480 .
doi: 10.1002/yea.1485
70 Peplowska, K., Cabrera, M., and Ungermann, C. (2008). UVRAG reveals its second nature. Nat Cell Biol 10, 759–761 .
doi: 10.1038/ncb0708-759
71 Price, A., Seals, D., Wickner, W., and Ungermann, C. (2000a). The docking stage of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J Cell Biol 148, 1231–1238 .
doi: 10.1083/jcb.148.6.1231
72 Price, A., Wickner, W., and Ungermann, C. (2000b). Proteins needed for vesicle budding from the Golgi complex are also required for the docking step of homotypic vacuole fusion. J Cell Biol 148, 1223–1229 .
doi: 10.1083/jcb.148.6.1223
73 Pulipparacharuvil, S., Akbar, M.A., Ray, S., Sevrioukov, E.A., Haberman, A.S., Rohrer, J., and Kr?mer, H. (2005). Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J Cell Sci 118, 3663–3673 .
doi: 10.1242/jcs.02502
74 Raiborg, C., and Stenmark, H. (2009). The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452 .
doi: 10.1038/nature07961
75 Ravikumar, B., Acevedo-Arozena, A., Imarisio, S., Berger, Z., Vacher, C., O’Kane, C.J., Brown, S.D., and Rubinsztein, D.C. (2005). Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37, 771–776 .
doi: 10.1038/ng1591
76 Ravikumar, B., Futter, M., Jahreiss, L., Korolchuk, V.I., Lichtenberg , M., Luo, S., Massey, D.C., Menzies, F.M., Narayanan, U., Renna, M., . (2009). Mammalian macroautophagy at a glance. J Cell Biol 122, 1707–1711 .
77 Recacha, R., Boulet, A., Jollivet, F., Monier, S., Houdusse, A., Goud, B., and Khan, A.R. (2009). Structural basis for recruitment of Rab6-interacting protein 1 to Golgi via a RUN domain. Structure 17, 21–30 .
doi: 10.1016/j.str.2008.10.014
78 Rieder, S.E., and Emr, S.D. (1997). A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol Biol Cell 8, 2307–2327 .
79 Rothman, J.E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55–63 .
doi: 10.1038/372055a0
80 Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272, 227–234 .
doi: 10.1126/science.272.5259.227
81 Rusten, T.E., and Stenmark, H. (2009). How do ESCRT proteins control autophagy? J Cell Sci 122, 2179–2183 .
doi: 10.1242/jcs.050021
82 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., . (2007). ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17, 1817–1825 .
doi: 10.1016/j.cub.2007.09.032
83 Saftig, P., Beertsen, W., and Eskelinen, E.L. (2008). LAMP-2: a control step for phagosome and autophagosome maturation. Autophagy 4, 510–512 .
84 Sato, T.K., Darsow, T., and Emr, S.D. (1998). Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking. Mol Cell Biol 18, 5308–5319 .
85 Sato, T.K., Rehling, P., Peterson, M.R., and Emr, S.D. (2000). Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol Cell 6, 661–671 .
doi: 10.1016/S1097-2765(00)00064-2
86 Satoh, A.K., O’Tousa, J.E., Ozaki, K., and Ready, D.F. (2005). Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132, 1487–1497 .
doi: 10.1242/dev.01704
87 Schroer, T.A., and Sheetz, M.P. (1991). Two activators of microtubule-based vesicle transport. J Cell Biol 115, 1309–1318 .
doi: 10.1083/jcb.115.5.1309
88 Seals, D.F., Eitzen, G., Margolis, N., Wickner, W.T., and Price, A. (2000). A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci U S A 97, 9402–9407 .
doi: 10.1073/pnas.97.17.9402
89 Seglen, P.O., Berg, T.O., Blankson, H., Fengsrud, M., Holen, I., and Str?mhaug, P.E. (1996). Structural aspects of autophagy. Adv Exp Med Biol 389, 103–111 .
90 Shirahama, K., Noda, T., and Ohsumi, Y. (1997). Mutational analysis of Csc1/Vps4p: involvement of endosome in regulation of autophagy in yeast. Cell Struct Funct 22, 501–509 .
doi: 10.1247/csf.22.501
91 S?llner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H., and Rothman, J.E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418 .
92 Somsel Rodman, J., and Wandinger-Ness, A. (2000). Rab GTPases coordinate endocytosis. J Cell Sci 113, 183–192 .
93 Stroupe, C., Collins, K.M., Fratti, R.A., and Wickner, W. (2006). Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 25, 1579–1589 .
doi: 10.1038/sj.emboj.7601051
94 Sugawara, K., Suzuki, N.N., Fujioka, Y., Mizushima, N., Ohsumi, Y., and Inagaki, F. (2004). The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8. Genes Cells 9, 611–618 .
doi: 10.1111/j.1356-9597.2004.00750.x
95 Suriapranata, I., Epple, U.D., Bernreuther, D., Bredschneider, M., Sovarasteanu, K., and Thumm, M. (2000). The breakdown of autophagic vesicles inside the vacuole depends on Aut4p. J Cell Sci 113, 4025–4033 .
96 Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H.D., Sun, M., Sato, Y., Liang, C., Jung, J.U., Cheng, J.Q., Mulé, J.J., . (2007). Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9, 1142–1151 .
doi: 10.1038/ncb1634
97 Takahashi, Y., Meyerkord, C.L., and Wang, H.G. (2008). BARgaining membranes for autophagosome formation: Regulation of autophagy and tumorigenesis by Bif-1/Endophilin B1. Autophagy 4, 121–124 .
98 Takeshige, K., Baba, M., Tsuboi, S., Noda, T., and Ohsumi, Y. (1992). Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 119, 301–311 .
doi: 10.1083/jcb.119.2.301
99 Tamai, K., Tanaka, N., Nara, A., Yamamoto, A., Nakagawa, I., Yoshimori, T., Ueno, Y., Shimosegawa, T., and Sugamura, K. (2007). Role of Hrs in maturation of autophagosomes in mammalian cells. Biochem Biophys Res Commun 360, 721–727 .
doi: 10.1016/j.bbrc.2007.06.105
100 Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E.L., Hartmann, D., Lüllmann-Rauch, R., Janssen, P.M., Blanz, J., von Figura, K., and Saftig, P. (2000). Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406, 902–906 .
doi: 10.1038/35022595
101 Teter, S.A., Eggerton, K.P., Scott, S.V., Kim, J., Fischer, A.M., and Klionsky, D.J. (2001). Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J Biol Chem 276, 2083–2087 .
102 Ungermann, C., and Langosch, D. (2005). Functions of SNAREs in intracellular membrane fusion and lipid bilayer mixing. J Cell Sci 118, 3819–3828 .
doi: 10.1242/jcs.02561
103 Ungermann, C., Nichols, B.J., Pelham, H.R.B., and Wickner, W. (1998). A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion. J Cell Biol 140, 61–69 .
doi: 10.1083/jcb.140.1.61
104 Ungermann, C., von Mollard, G.F., Jensen, O.N., Margolis, N., Stevens, T.H., and Wickner, W. (1999). Three v-SNAREs and two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential for homotypic fusion. J Cell Biol 145, 1435–1442 .
doi: 10.1083/jcb.145.7.1435
105 Ungermann, C., and Wickner, W. (1998). Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complex integrity and vacuole docking and fusion. EMBO J 17, 3269–3276 .
doi: 10.1093/emboj/17.12.3269
106 Wang, C.-W., and Klionsky, D.J. (2003). The molecular mechanism of autophagy. Mol Med 9, 65–76 .
107 Wang, C.-W., Stromhaug, P.E., Kauffman, E.J., Weisman, L.S., and Klionsky, D.J. (2003). Yeast homotypic vacuole fusion requires the Ccz1-Mon1 complex during the tethering/docking stage. J Cell Biol 163, 973–985 .
doi: 10.1083/jcb.200308071
108 Wang, C.-W., Stromhaug, P.E., Shima, J., and Klionsky, D.J. (2002). The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J Biol Chem 277, 47917–47927 .
doi: 10.1074/jbc.M208191200
109 Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., S?llner, T.H., and Rothman, J.E. (1998). SNAREpins: minimal machinery for membrane fusion. Cell 92, 759–772 .
110 White, S.R., and Lauring, B. (2007). AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8, 1657–1667 .
doi: 10.1111/j.1600-0854.2007.00642.x
111 Wurmser, A.E., Sato, T.K., and Emr S.D. (2000).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, 551–62 .
doi: 10.1083/jcb.151.3.551
112 Xie, Z., and Klionsky, D.J. (2007). Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9, 1102–1109 .
doi: 10.1038/ncb1007-1102
113 Xu, H., Jun, Y., Thompson, J., Yates, J., and Wickner, W. (2010). HOPS prevents the disassembly of trans-SNARE complexes by Sec17p/Sec1p during membrane fusion. J EMBO 29, 1948–1960 .
doi: 10.1038/emboj.2010.97
114 Yang, Z., Huang, J., Geng, J., Nair, U., and Klionsky, D.J. (2006). Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol Biol Cell 17, 5094–5104 .
doi: 10.1091/mbc.E06-06-0479
115 Yorimitsu, T., and Klionsky, D.J. (2005). Autophagy: molecular machinery for self-eating. Cell Death Differ 12, 1542–1552 .
doi: 10.1038/sj.cdd.4401765
116 Yu, L., McPhee, C.K., Zheng, L., Mardones, G.A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F., . (2010). Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 17, 942–946 .
doi: 10.1038/nature09076
[1] Kun Liu, Jiani Cao, Xingxing Shi, Liang Wang, Tongbiao Zhao. Cellular metabolism and homeostasis in pluripotency regulation[J]. Protein Cell, 2020, 11(9): 630-640.
[2] Xin Zhou, Yu He, Xiaofang Huang, Yuting Guo, Dong Li, Junjie Hu. Reciprocal regulation between lunapark and atlastin facilitates ER three-way junction formation[J]. Protein Cell, 2019, 10(7): 510-525.
[3] Ying Lv, Sheng Zhou, Shengyan Gao, Hongyu Deng. Remodeling of host membranes during herpesvirus assembly and egress[J]. Protein Cell, 2019, 10(5): 315-326.
[4] Junsheng Yang, Zhuangzhuang Zhao, Mingxue Gu, Xinghua Feng, Haoxing Xu. Release and uptake mechanisms of vesicular Ca2+ stores[J]. Protein Cell, 2019, 10(1): 8-19.
[5] Crystal A. Lee, Lih-Shen Chin, Lian Li. Hypertonia-linked protein Trak1 functions with mitofusins to promote mitochondrial tethering and fusion[J]. Protein Cell, 2018, 9(8): 693-716.
[6] Na Qu, Zhao Ma, Mengrao Zhang, Muaz N. Rushdi, Christopher J. Krueger, Antony K. Chen. Inhibition of retroviral Gag assembly by non-silencing miRNAs promotes autophagic viral degradation[J]. Protein Cell, 2018, 9(7): 640-651.
[7] Yang Li, Yu Zhang, Qiwen Gan, Meng Xu, Xiao Ding, Guihua Tang, Jingjing Liang, Kai Liu, Xuezhao Liu, Xin Wang, Lingli Guo, Zhiyang Gao, Xiaojiang Hao, Chonglin Yang. C. elegans-based screen identifies lysosome-damaging alkaloids that induce STAT3-dependent lysosomal cell death[J]. Protein Cell, 2018, 9(12): 1013-1026.
[8] Liming Liu. Pharmacokinetics of monoclonal antibodies and Fc-fusion proteins[J]. Protein Cell, 2018, 9(1): 15-32.
[9] Xing Guo, Xiuliang Huang, Mark J. Chen. Reversible phosphorylation of the 26S proteasome[J]. Protein Cell, 2017, 8(4): 255-272.
[10] Peipei Liu, Jinliang Huang, Qian Zheng, Leiming Xie, Xinping Lu, Jie Jin, Geng Wang. Mammalian mitochondrial RNAs are degraded in the mitochondrial intermembrane space by RNASET2[J]. Protein Cell, 2017, 8(10): 735-749.
[11] Zhi-Dong Liu,Su Zhang,Jian-Jin Hao,Tao-Rong Xie,Jian-Sheng Kang. Cellular model of neuronal atrophy induced by DYNC1I1 deficiency reveals protective roles of RAS-RAF-MEK signaling[J]. Protein Cell, 2016, 7(9): 638-650.
[12] Jintao Bao,Liangjun Zheng,Qi Zhang,Xinya Li,Xuefei Zhang,Zeyang Li,Xue Bai,Zhong Zhang,Wei Huo,Xuyang Zhao,Shujiang Shang,Qingsong Wang,Chen Zhang,Jianguo Ji. Deacetylation of TFEB promotes fibrillar Aβ degradation by upregulating lysosomal biogenesis in microglia[J]. Protein Cell, 2016, 7(6): 417-433.
[13] Xuechen Lv,Junlin Liu,Qiaoyun Shi,Qiwen Tan,Dong Wu,John J. Skinner,Angela L. Walker,Lixia Zhao,Xiangxiang Gu,Na Chen,Lu Xue,Pei Si,Lu Zhang,Zeshi Wang,Vsevolod Katritch,Zhi-jie Liu,Raymond C. Stevens. In vitro expression and analysis of the 826 human G protein-coupled receptors[J]. Protein Cell, 2016, 7(5): 325-337.
[14] Jiaxiang Shao,Xiao Yang,Tengyuan Liu,Tingting Zhang,Qian Reuben Xie,Weiliang Xia. Autophagy induction by SIRT6 is involved in oxidative stress-induced neuronal damage[J]. Protein Cell, 2016, 7(4): 281-290.
[15] Yan-Cheng Tang,Hong-Xia Tian,Tao Yi,Hu-Biao Chen. The critical roles of mitophagy in cerebral ischemia[J]. Protein Cell, 2016, 7(10): 699-713.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed