The core molecular machinery of autophagosome formation

Autophagy and Cancer

Volumn , Issue , 2013, Pages 25-45

  Jin, Meiyan ^a   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Autophagy; Lysosome; Phagophore; Protein degradation; Protein trafficking; Stress; Vacuole

Indexed keywords

EID: 84983227373     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-6561-4_2     Document Type: Chapter

References (108)

1. Abeliovich H et al (2003) Chemical genetic analysis of Apg1 reveals a non-kinase role in the induction of autophagy. Mol Biol Cell 14:477-490.
2. Axe EL et al (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182:685-701.
3. Baskaran S et al (2012) Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol Cell 47:339-348.
4. Chan EY (2009) mTORC1 phosphorylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci Signal 2:pe51.
5. Chan EYW, Kir S, Tooze SA (2007) siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 282:25464-25474.
6. Chang CY, Huang W-P (2007) Atg19 mediates a dual interaction cargo sorting mechanism in selective autophagy. Mol Biol Cell 18:919-929.
7. Cheong H et al (2005) Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell 16:3438-3453.
8. Cheong H et al (2008) The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol Biol Cell 19:668-681.
9. Fimia GM et al (2007) Ambra1 regulates autophagy and development of the nervous system. Nature 447:1121-1125.
10. Fujita N et al (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 19:2092-2100.
11. Fujioka Y et al (2010) Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J Biol Chem 285:1508-1515.
12. Furuya N et al (2005) The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 1:46-52.
13. Furuya T et al (2010) Negative regulation of Vps34 by Cdk mediated phosphorylation. Mol Cell 38:500-511.
14. Ganley IG et al (2009) ULK1 ATG13 FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297-12305.
15. Guan J et al (2001) Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol Biol Cell 12:3821-3838.
16. Hanada T et al (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282:37298-37302.
17. Hara T et al (2008) FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181:497-510.
18. Harding TM et al (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131:591-602.
19. He C et al (2006) Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J Cell Biol 175:925-935.
20. Hochstrasser M (2009) Origin and function of ubiquitin-like proteins. Nature 458:422-429.
21. Hosokawa N et al (2009a) Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20:1981-1991.
22. Hosokawa N et al (2009b) Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5:973-979.
23. Huang W-P et al (2000) The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem 275:5845-5851.
24. Huang W et al (2012) Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein. Cell Res 22:473-489.
25. Ichimura Y et al (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488-492.
26. Itakura E, Mizushima N (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6:764-776.
27. Itakura E et al (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19:5360-5372.
28. Juhasz G et al (2008) The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181:655-666.
29. Jung CH et al (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992-2003.
30. Kabeya Y et al (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117:2805-2812.
31. Kabeya Y et al (2005) Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol Biol Cell 16:2544-2553.
32. Kabeya Y et al (2007) Cis1/Atg31 is required for autophagosome formation in Saccharomyces cerevisiae. Biochem Biophys Res Commun 356:405-410.
33. Kamada Y et al (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150:1507-1513.
34. Kametaka S et al (1998) Apg14p and Apg6/Vps30p form a protein complex essential for autophagy in the yeast Saccharomyces cerevisiae. J Biol Chem 273:22284-22291.
35. Kawamata T et al (2005) Characterization of a novel autophagy-specific gene, ATG29. Biochem Biophys Res Commun 338:1884-1889.
36. Kawamata T et al (2008) Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19:2039-2050.
37. Kihara A et al (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152:519-530.
38. Kirisako T et al (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151:263-276.
39. Klionsky DJ et al (2003) A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539-545.
40. Kobayashi T, Suzuki K, Ohsumi Y (2012) Autophagosome formation can be achieved in the absence of Atg18 by expressing engineered PAS-targeted Atg2. FEBS Lett 586:2473-2478.
41. Krick R et al (2012) Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a beta-propeller protein family. Proc Natl Acad Sci USA 109:E2042-E2049.
42. Kuma A et al (2002) Formation of the approximately 350-kDa Apg12-Apg5-Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem 277:18619-18625.
43. Kundu M et al (2008) Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112:1493-1502.
44. Legakis JE, Yen W-L, Klionsky DJ (2007) A cycling protein complex required for selective autophagy. Autophagy 3:422-432.
45. Li M et al (2011) Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem 286:7327-7338.
46. Liang XH et al (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676.
47. Liang C et al (2006) Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 8:688-699.
48. Lin SY et al (2012) GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science 336:477-481.
49. Matsunaga K et al (2009) Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 11:385-396.
50. Matsuura A et al (1997) Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192:245-250.
51. Mercer CA, Kaliappan A, Dennis PB (2009) A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5:649-662.
52. Mizushima N (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22:132-139.
53. Mizushima N et al (1998) A protein conjugation system essential for autophagy. Nature 395:395-398.
54. Mizushima N, Noda T, Ohsumi Y (1999) Apg16p is required for the function of the Apg12p- Apg5p conjugate in the yeast autophagy pathway. EMBO J 18:3888-3896.
55. Mizushima N et al (2001) Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152:657-668.
56. Mizushima N, Yoshimori T, Ohsumi Y (2002) Mouse Apg10 as an Apg12-conjugating enzyme: analysis by the conjugation-mediated yeast two-hybrid method. FEBS Lett 532:450-454.
57. Mizushima N et al (2003) Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 116:1679-1688.
58. Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107-132.
59. Monastyrska I et al (2008) Arp2 links autophagic machinery with the actin cytoskeleton. Mol Biol Cell 19:1962-1975.
60. Nair U et al (2012) A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy 8(5):780-793.
61. Nakatogawa H et al (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10:458-467.
62. Nice DC et al (2002) Cooperative binding of the cytoplasm to vacuole targeting pathway proteins, Cvt13 and Cvt20, to phosphatidylinositol 3-phosphate at the pre-autophagosomal structure is required for selective autophagy. J Biol Chem 277:30198-30207.
63. Noda T et al (2000) Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 148:465-480.
64. Obara K, Sekito T, Ohsumi Y (2006) Assortment of phosphatidylinositol 3-kinase complexes- Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell 17:1527-1539.
65. Obara K et al (2008) Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 13:537-547.
66. Orsi A et al (2012) Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell 23:1860-1873.
67. Petiot A et al (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.
68. Polson HE et al (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6:506-522.
69. Reggiori F et al (2004) The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 6:79-90.
70. Reggiori F et al (2005) Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1:101-109.
71. Sekito T et al (2009) Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells 14:525-538.
72. Shintani T et al (1999) Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast. EMBO J 18:5234-5241.
73. Shintani T et al (2001) Apg2p functions in autophagosome formation on the perivacuolar structure. J Biol Chem 276:30452-30460.
74. Skwarek LC, Boulianne GL (2009) Great expectations for PIP: phosphoinositides as regulators of signaling during development and disease. Dev Cell 16:12-20.
75. Stack JH, Emr SD (1994) Vps34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities. J Biol Chem 269:31552-31562.
76. Stack JH et al (1993) A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J 12:2195-2204.
77. Stack JH et al (1995) Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J Cell Biol 129:321-334.
78. Straub M, Bredschneider M, Thumm M (1997) AUT3, a serine/threonine kinase gene, is essential for autophagocytosis in Saccharomyces cerevisiae. J Bacteriol 179:3875-3883.
79. Stromhaug PE, Klionsky DJ (2001) Approaching the molecular mechanism of autophagy. Traffic 2:524-531.
80. Stromhaug PE et al (2004) Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell 15:3553-3566.
81. Sugawara K et al (2004) The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8. Genes Cells 9:611-618.
82. Sun Q et al (2008) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 105:19211-19216.
83. Suzuki NN et al (2005) The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy 1:119-126.
84. Suzuki K et al (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12:209-218.
85. Takahashi Y et al (2007) Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9:1142-1151.
86. Tanida I et al (1999) Apg7p/Cvt2p: a novel protein-activating enzyme essential for autophagy. Mol Biol Cell 10:1367-1379.
87. Tanida I et al (2001) The human homolog of Saccharomyces cerevisiae Apg7p is a proteinactivating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem 276:1701-1706.
88. Tanida I et al (2002) Human Apg3p/Aut1p homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP-LC3, and facilitates the conjugation of hApg12p to hApg5p. J Biol Chem 277:13739-13744.
89. Tanida I et al (2003) GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3. Biochem Biophys Res Commun 300:637-644.
90. Tanida I et al (2006) Atg8L/Apg8L is the fourth mammalian modifier of mammalian Atg8 conjugation mediated by human Atg4B, Atg7 and Atg3. FEBS J 273:2553-2562.
91. Thumm M et al (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349:275-280.
92. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169-174.
93. Tucker KA et al (2003) Atg23 is essential for the cytoplasm to vacuole targeting pathway and efficient autophagy but not pexophagy. J Biol Chem 278:48445-48452.
94. Wang C-W et al (2001) Apg2 is a novel protein required for the cytoplasm to vacuole targeting, autophagy, and pexophagy pathways. J Biol Chem 276:30442-30451.
95. Weidberg H et al (2010) LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 29:1792-1802.
96. Weidberg H, Shvets E, Elazar Z (2011) Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 80:125-156.
97. Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9:1102-1109.
98. Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290-3298.
99. Yamada T et al (2005) Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem 280:18283-18290.
100. Yan Y et al (2009) hVps15, but not Ca 2+ /CaM, is required for the activity and regulation of hVps34 in mammalian cells. Biochem J 417:747-755.
101. Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1-32.
102. Yeh YY, Wrasman K, Herman PK (2010) Autophosphorylation within the Atg1 activation loop is required for both kinase activity and the induction of autophagy in Saccharomyces cerevisiae. Genetics 185:871-882.
103. Yen W-L et al (2007) Atg27 is required for autophagy-dependent cycling of Atg9. Mol Biol Cell 18:581-593.
104. Yorimitsu T et al (2007) Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18:4180-4189.
105. Young ARJ et al (2006) Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 119:3888-3900.
106. Yu ZQ et al (2012) Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy 8:883-892.
107. Zeng X, Overmeyer JH, Maltese WA (2006) Functional specificity of the mammalian Beclin- Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 119:259-270.
108. Zhong Y et al (2009) Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 11:468-476.