Autophagosome maturation, endocytosis and neurodegenerative disease

Autophagy of the Nervous System: Cellular Self-Digestion in Neurons and Neurological Diseases

Volumn , Issue , 2012, Pages 37-57

  Yamamoto, Ai ^a   Simonsen, Anne ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84971291358     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9789814350457_0002     Document Type: Chapter

References (106)

1. D. De Duve, B. C. Pressman, R. Gianetto, R. Wattiaux and F. Appelmans, Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue, Biochem J 60: 604-617 (1955).
2. Z. Xie and D. J. Klionsky, Autophagosome formation: core machinery and adaptations, Nat Cell Biol 9: 1102-1109 (2007).
3. M. Kon and A. M. Cuervo, Chaperone-mediated autophagy in health and disease, FEBS Lett 584: 1399-1404 (2010).
4. N. Mizushima and B. Levine, Autophagy in mammalian development and differentiation, Nat Cell Biol 12: 823-830 (2010).
5. A. Yamamoto and A. Simonsen, The elimination of accumulated and aggregated proteins: a role for aggrephagy in neurodegeneration, Neurobiol Dis 43: 17-28 (2011).
6. R. Singh, S. Kaushik, Y. Wang, Y. Xiang, I. Novak, M. Komatsu, K. Tanaka, A. M. Cuervo and M. J. Czaja, Autophagy regulates lipid metabolism, Nature 458: 1131-1135 (2009).
7. C. Kraft, M. Peter and K. Hofmann, Selective autophagy: ubiquitin-mediated recognition and beyond, Nat Cell Biol 12: 836-841 (2010).
8. M. Tsukada and Y. Ohsumi, Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae, FEBS Lett 333: 169-174 (1993).
9. D. J. Klionsky, J. M. Cregg, W. A. Dunn, Jr., S. D. Emr, Y. Sakai, I. V. Sandoval, A. Sibirny, S. Subramani, M. Thumm, M. Veenhuis and Y. Ohsumi, A unified nomenclature for yeast autophagy-related genes, Dev Cell 5: 539-545 (2003).
10. Z. Yang and D. J. Klionsky, Eaten alive: a history of macroautophagy, Nat Cell Biol 12: 814-822 (2010).
11. C. He and D. J. Klionsky, Regulation mechanisms and signaling pathways of autophagy, Annu Rev Genet 43: 67-93 (2009).
12. A. Longatti and S. A. Tooze, Vesicular trafficking and autophagosome formation, Cell Death Differ 16: 956-965 (2009).
13. A. Simonsen and S. A. Tooze, Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes, J Cell Biol 186: 773-782 (2009).
14. P. B. Gordon and P. O. Seglen, Prelysosomal convergence of autophagic and endocytic pathways, Biochem Biophys Res Commun 151: 40-47 (1988).
15. T. E. Rusten and H. Stenmark, How do ESCRT proteins control autophagy?, J Cell Sci 122: 2179-2183 (2009).
16. S. A. Tooze and G. Schiavo, Liaisons dangereuses: autophagy, neuronal survival and neurodegeneration, Curr Opin Neurobiol 18: 504-515 (2008).
17. C. Raiborg and H. Stenmark, The ESCRT machinery in endosomal sorting of ubiq-uitylated membrane proteins, Nature 458: 445-452 (2009).
18. W. A. Dunn, Jr., Studies on the mechanisms of autophagy: maturation of the autophagic vacuole, J Cell Biol 110: 1935-1945 (1990).
19. J. Lucocq and D. Walker, Evidence for fusion between multilamellar endosomes and autophagosomes in HeLa cells, Eur J Cell Biol 72: 307-313 (1997).
20. E. L. Eskelinen, Maturation of autophagic vacuoles in mammalian cells, Autophagy 1: 1-10 (2005).
21. C. M. Fader, D. Sanchez, M. Furlan and M. I. Colombo, Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells, Traffic 9: 230-250 (2008).
22. J. Morvan, R. Kochl, R. Watson, L. M. Collinson, H. B. Jefferies and S. A. Tooze, In vitro reconstitution of fusion between immature autophagosomes and endosomes, Autophagy 5: 676-689 (2009).
23. A. Nara, N. Mizushima, A. Yamamoto, Y. Kabeya, Y. Ohsumi and T. Yoshimori, SKD1 AAA ATPase-dependent endosomal transport is involved in autolysosome formation, Cell Struct Funct 27: 29-37 (2002).
24. M. Filimonenko, S. Stuffers, C. Raiborg, A. Yamamoto, L. Malerod, E. M. Fisher, A. Isaacs, A. Brech, H. Stenmark and A. Simonsen, Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease, J Cell Biol 179: 485-500 (2007).
25. J. A. Lee, A. Beigneux, S. T. Ahmad, S. G. Young and F. B. Gao, ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration, Curr Biol 17: 1561-1567 (2007).
26. T. E. Rusten, M. Filimonenko, L. M. Rodahl, H. Stenmark and A. Simonsen, ESCRTing autophagic clearance of aggregating proteins, Autophagy 4: 233-236 (2007).
27. M. Razi, E. Y. Chan and S. A. Tooze, Early endosomes and endosomal coatomer are required for autophagy, J Cell Biol 185: 305-321 (2009).
28. B. Ravikumar, S. Imarisio, S. Sarkar, C. J. O’Kane and D. C. Rubinsztein, Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease, J Cell Sci 121: 1649-1660 (2008).
29. T. Itoh, N. Fujita, E. Kanno, A. Yamamoto, T. Yoshimori and M. Fukuda, Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation, Mol Biol Cell 19: 2916-2925 (2008).
30. B. Ravikumar, K. Moreau, L. Jahreiss, C. Puri and D. C. Rubinsztein, Plasma membrane contributes to the formation of pre-autophagosomal structures, Nat Cell Biol 12: 747-757 (2010).
31. Y. Hirota and Y. Tanaka, A small GTPase, human Rab32, is required for the formation of autophagic vacuoles under basal conditions, Cell Mol Life Sci 66: 2913-2932 (2009).
32. M. G. Gutierrez, D. B. Munafo, W. Beron and M. I. Colombo, Rab7 is required for the normal progression of the autophagic pathway in mammalian cells, J Cell Sci 117: 2687-2697 (2004).
33. S. Jager, C. Bucci, I. Tanida, T. Ueno, E. Kominami, P. Saftig and E. L. Eskelinen, Role for Rab7 in maturation of late autophagic vacuoles, J Cell Sci 117: 4837-4848 (2004).
34. D. B. Munafo and M. I. Colombo, Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24, Traffic 3: 472-482 (2002).
35. C. M. Fader and M. I. Colombo, Autophagy and multivesicular bodies: two closely related partners, Cell Death Differ 16: 70-78 (2009).
36. N. Furuta, N. Fujita, T. Noda, T. Yoshimori and A. Amano, Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lyso-somes, Mol Biol Cell 21: 1001-1010 (2010).
37. T. Darsow, S. E. Rieder and S. D. Emr, A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole, J Cell Biol 138: 517-529 (1997).
38. N. Ishihara, M. Hamasaki, S. Yokota, K. Suzuki, Y. Kamada, A. Kihara, T. Yoshimori, T. Noda and Y. Ohsumi, Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion, Mol Biol Cell 12: 3690-3702 (2001).
39. D. F. Seals, G. Eitzen, N. Margolis, W. T. Wickner and A. Price, A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion, Proc Natl Acad Sci USA 97: 9402-9407 (2000).
40. D. P. Nickerson, C. L. Brett and A. J. Merz, Vps-C complexes: gatekeepers of endolysosomal traffic, Curr Opin Cell Biol 21: 543-551 (2009).
41. K. Lindmo, A. Simonsen, A. Brech, K. Finley, T. E. Rusten and H. Stenmark, A dual function for Deep orange in programmed autophagy in the Drosophila melanogaster fat body, Exp Cell Res 312: 2018-2027 (2006).
42. E. A. Sevrioukov, J. P. He, N. Moghrabi, A. Sunio and H. Kramer, A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila, Mol Cell 4: 479-486 (1999).
43. S. Pulipparacharuvil, M. A. Akbar, S. Ray, E. A. Sevrioukov, A. S. Haberman, J. Rohrer and H. Kramer, Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules, J Cell Sci 118: 3663-3673 (2005).
44. A. E. Wurmser, T. K. Sato and S. D. Emr, 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: 551-562 (2000).
45. J. Rink, E. Ghigo, Y. Kalaidzidis and M. Zerial, Rab conversion as a mechanism of progression from early to late endosomes, Cell 122: 735-749 (2005).
46. K. Peplowska, D. F. Markgraf, C. W. Ostrowicz, G. Bange and C. Ungermann, The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis, Dev Cell 12: 739-750 (2007).
47. K. B. Hendil, A. M. Lauridsen and P. O. Seglen, Both endocytic and endogenous protein degradation in fibroblasts is stimulated by serum/amino acid deprivation and inhibited by 3-methyladenine, Biochem J 272: 577-581 (1990).
48. E. F. Blommaart, U. Krause, J. P. Schellens, H. Vreeling-Sindelarova and A. J. Meijer, The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes, Eur J Biochem 243: 240-246 (1997).
49. S. S. Skanland, S. Walchli, A. Utskarpen, A. Wandinger-Ness and K. Sandvig, Phosphoinositide-regulated retrograde transport of ricin: crosstalk between hVps34 and sorting nexins, Traffic 8: 297-309 (2007).
50. E. Itakura, C. Kishi, K. Inoue and N. Mizushima, Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG, Mol Biol Cell 19: 5360-5372 (2008).
51. Q. Sun, W. Fan, K. Chen, X. Ding, S. Chen and Q. Zhong, 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 (2008).
52. M. N. Seaman, E. G. Marcusson, J. L. Cereghino and S. D. Emr, Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products, J Cell Biol 137: 79-92 (1997).
53. P. Burda, S. M. Padilla, S. Sarkar and S. D. Emr, Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3-kinase, J Cell Sci 115: 3889-3900 (2002).
54. K. Matsunaga, T. Saitoh, K. Tabata, H. Omori, T. Satoh, N. Kurotori, I. Maejima, K. Shirahama-Noda, T. Ichimura, T. Isobe, S. Akira, T. Noda and T. Yoshimori, Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages, Nat Cell Biol 11: 385-396 (2009).
55. Y. Zhong, Q. J. Wang, X. Li, Y. Yan, J. M. Backer, B. T. Chait, N. Heintz and Z. Yue, Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex, Nat Cell Biol 11: 468-476 (2009).
56. C. Liang, J. S. Lee, K. S. Inn, M. U. Gack, Q. Li, E. A. Roberts, I. Vergne, V. Deretic, P. Feng, C. Akazawa and J. U. Jung, Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking, Nat Cell Biol 10: 776-787 (2008).
57. M. Koike, H. Nakanishi, P. Saftig, J. Ezaki, K. Isahara, Y. Ohsawa, W. Schulz-Schaeffer, T. Watanabe, S. Waguri, S. Kametaka, M. Shibata, K. Yamamoto, E. Kominami, C. Peters, K. von Figura and Y. Uchiyama, Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons, J Neurosci 20: 6898-6906 (2000).
58. Y. Tanaka, G. Guhde, A. Suter, E. L. Eskelinen, D. Hartmann, R. Lullmann-Rauch, P. M. Janssen, J. Blanz, K. von Figura and P. Saftig, Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice, Nature 406: 902-906 (2000).
59. E. L. Eskelinen, C. K. Schmidt, S. Neu, M. Willenborg, G. Fuertes, N. Salvador, Y. Tanaka, R. Lullmann-Rauch, D. Hartmann, J. Heeren, K. von Figura, E. Knecht and P. Saftig, Disturbed cholesterol traffic but normal proteolytic function in LAMP- 1/LAMP-2 double-deficient fibroblasts, Mol Biol Cell 15: 3132-3145 (2004).
60. S. Pankiv, T. H. Clausen, T. Lamark, A. Brech, J. A. Bruun, H. Outzen, A. Overvatn, G. Bjorkoy and T. Johansen, p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy, J Biol Chem 282: 24131-24145 (2007).
61. S. Kimura, T. Noda and T. Yoshimori, Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3, Autophagy 3: 452-460 (2007).
62. P. E. Stromhaug and P. O. Seglen, Evidence for acidity of prelysosomal autophagic/endocytic vacuoles (amphisomes), Biochem J 291(Pt 1): 115-121 (1993).
63. R. Kochl, X. W. Hu, E. Y. Chan and S. A. Tooze, Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes, Traffic 7: 129-145 (2006).
64. S. Kimura, T. Noda and T. Yoshimori, Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes, Cell Struct Funct 33: 109-122 (2008).
65. E. Fass, E. Shvets, I. Degani, K. Hirschberg and Z. Elazar, Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes, J Biol Chem 281: 36303-36316 (2006).
66. L. Jahreiss, F. M. Menzies and D. C. Rubinsztein, The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes, Traffic 9: 574-587 (2008).
67. Q. Cai, L. Lu, J. H. Tian, Y. B. Zhu, H. Qiao and Z. H. Sheng, Snapin-regulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons, Neuron 68: 73-86 (2010).
68. M. Yuzaki, Snapin snaps into the dynein complex for late endosome-lysosome trafficking and autophagy, Neuron 68: 4-6 (2010).
69. S. Pankiv, E. A. Alemu, A. Brech, J. A. Bruun, T. Lamark, A. Overvatn, G. Bjorkoy and T. Johansen, 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 (2010).
70. Z. Yue, A. Horton, M. Bravin, P. L. DeJager, F. Selimi and N. Heintz, A novel protein complex linking the delta 2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice, Neuron 35: 921-933 (2002).
71. T. Hara, K. Nakamura, M. Matsui, A. Yamamoto, Y. Nakahara, R. Suzuki-Migishima, M. Yokoyama, K. Mishima, I. Saito, H. Okano and N. Mizushima, Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice, Nature 441: 885-889 (2006).
72. M. Komatsu, S. Waguri, T. Chiba, S. Murata, J. Iwata, I. Tanida, T. Ueno, M. Koike, Y. Uchiyama, E. Kominami and K. Tanaka, Loss of autophagy in the central nervous system causes neurodegeneration in mice, Nature 441: 880-884 (2006).
73. B. Boland, A. Kumar, S. Lee, F. M. Platt, J. Wegiel, W. H. Yu and R. A. Nixon, Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer’s disease, J Neurosci 28: 6926-6937 (2008).
74. J. H. Lee, W. H. Yu, A. Kumar, S. Lee, P. S. Mohan, C. M. Peterhoff, D. M. Wolfe, M. Martinez-Vicente, A. C. Massey, G. Sovak, Y. Uchiyama, D. Westaway, A. M. Cuervo and R. A. Nixon, Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations, Cell 141: 1146-1158 (2010).
75. G. Skibinski, N. J. Parkinson, J. M. Brown, L. Chakrabarti, S. L. Lloyd, H. Hummerich, J. E. Nielsen, J. R. Hodges, M. G. Spillantini, T. Thusgaard, S. Brandner, A. Brun, M. N. Rossor, A. Gade, P. Johannsen, S. A. Sorensen, S. Gydesen, E. M. Fisher and J. Collinge, Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia, Nat Genet 37: 806-808 (2005).
76. N. Parkinson, P. G. Ince, M. O. Smith, R. Highley, G. Skibinski, P. M. Andersen, K. E. Morrison, H. S. Pall, O. Hardiman, J. Collinge, P. J. Shaw and E. M. Fisher, ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B), Neurology 67: 1074-1077 (2006).
77. J. A. Lee and F. B. Gao, ESCRT, autophagy, and frontotemporal dementia, BMB Rep 41: 827-832 (2008).
78. I. R. Mackenzie, M. Neumann, E. H. Bigio, N. J. Cairns, I. Alafuzoff, J. Kril, G. G. Kovacs, B. Ghetti, G. Halliday, I. E. Holm, P. G. Ince, W. Kamphorst, T. Revesz, A. J. Rozemuller, S. Kumar-Singh, H. Akiyama, A. Baborie, S. Spina, D. W. Dickson, J. Q. Trojanowski and D. M. Mann, Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update, Acta Neuropathol 119: 1-4 (2010).
79. L. E. Cox, L. Ferraiuolo, E. F. Goodall, P. R. Heath, A. Higginbottom, H. Mortiboys, H. C. Hollinger, J. A. Hartley, A. Brockington, C. E. Burness, K. E. Morrison, S. B. Wharton, A. J. Grierson, P. G. Ince, J. Kirby and P. J. Shaw, Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS), PloS One 5: e9872 (2010).
80. H. Urwin, A. Authier, J. E. Nielsen, D. Metcalf, C. Powell, K. Froud, D. S. Malcolm, I. Holm, P. Johannsen, J. Brown, E. M. Fisher, J. van der Zee, M. Bruyland, C. Van Broeckhoven, J. Collinge, S. Brandner, C. Futter and A. M. Isaacs, Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations, Hum Mol Genet 19: 2228-2238 (2010).
81. A. Belly, G. Bodon, B. Blot, A. Bouron, R. Sadoul and Y. Goldberg, CHMP2B mutants linked to frontotemporal dementia impair maturation of dendritic spines, J Cell Sci 123: 2943-2954 (2010).
82. A. J. Shirk, S. K. Anderson, S. H. Hashemi, P. F. Chance and C. L. Bennett, SIMPLE interacts with NEDD4 and TSG101: evidence for a role in lysosomal sorting and implications for Charcot-Marie-Tooth disease, J Neurosci Res 82: 43-50 (2005).
83. B. Y. Kim, J. A. Olzmann, G. S. Barsh, L. S. Chin and L. Li, Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking, Mol Biol Cell 18: 1129-1142 (2007).
84. T. E. Rusten, T. Vaccari, K. Lindmo, L. M. Rodahl, I. P. Nezis, C. Sem-Jacobsen, F. Wendler, J. P. Vincent, A. Brech, D. Bilder and H. Stenmark, ESCRTs and Fab1 regulate distinct steps of autophagy, Curr Biol 17: 1817-1825 (2007).
85. N. T. Sweeney, J. E. Brenman, Y. N. Jan and F. B. Gao, The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila, Curr Biol 16: 1006-1011 (2006).
86. I. E. Holm, E. Englund, I. R. Mackenzie, P. Johannsen and A. M. Isaacs, A reassessment of the neuropathology of frontotemporal dementia linked to chromosome 3, J Neuropathol Exp Neurol 66: 884-891 (2007).
87. A. Simonsen, H. C. Birkeland, D. J. Gillooly, N. Mizushima, A. Kuma, T. Yoshimori, T. Slagsvold, A. Brech and H. Stenmark, Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes, J Cell Sci 117: 4239-4251 (2004).
88. M. Filimonenko, P. Isakson, K. D. Finley, M. Anderson, H. Jeong, T. J. Melia, B. J. Bartlett, K. M. Myers, H. C. Birkeland, T. Lamark, D. Krainc, A. Brech, H. Stenmark, A. Simonsen and A. Yamamoto, The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy, Mol Cell 38: 265-279 (2010).
89. P. Szyniarowski, E. Corcelle-Termeau, T. Farkas, M. Hoyer-Hansen, J. Nylandsted, T. Kallunki and M. Jaattela, A comprehensive siRNA screen for kinases that suppress macroautophagy in optimal growth conditions, Autophagy 7: 892-903 (2011).
90. G. D. Watts, J. Wymer, M. J. Kovach, S. G. Mehta, S. Mumm, D. Darvish, A. Pestronk, M. P. Whyte and V. E. Kimonis, Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein, Nat Genet 36: 377-381 (2004).
91. J. S. Ju, R. A. Fuentealba, S. E. Miller, E. Jackson, D. Piwnica-Worms, R. H. Baloh and C. C. Weihl, Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease, J Cell Biol 187: 875-888 (2009).
92. E. Tresse, F. A. Salomons, J. Vesa, L. C. Bott, V. Kimonis, T. P. Yao, N. P. Dantuma and J. P. Taylor, VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD, Autophagy 6: 217-227 (2010).
93. J. Y. Lee, H. Koga, Y. Kawaguchi, W. Tang, E. Wong, Y. S. Gao, U. B. Pandey, S. Kaushik, E. Tresse, J. Lu, J. P. Taylor, A. M. Cuervo and T. P. Yao, HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy, EMBO J 29: 969-980 (2010).
94. D. W. Hailey, A. S. Rambold, P. Satpute-Krishnan, K. Mitra, R. Sougrat, P. K. Kim and J. Lippincott-Schwartz, Mitochondria supply membranes for autophagosome biogenesis during starvation, Cell 141: 656-667 (2010).
95. E. L. Axe, S. A. Walker, M. Manifava, P. Chandra, H. L. Roderick, A. Habermann, G. Griffiths and N. T. Ktistakis, Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum, J Cell Biol 182: 685-701 (2008).
96. M. Hayashi-Nishino, N. Fujita, T. Noda, A. Yamaguchi, T. Yoshimori and A. Yamamoto, A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation, Nat Cell Biol 11: 1433-1437 (2009).
97. P. Yla-Anttila, H. Vihinen, E. Jokitalo and E. L. Eskelinen, 3D tomography reveals connections between the phagophore and endoplasmic reticulum, Autophagy 5: 1180-1185 (2009).
98. K. Matsunaga, E. Morita, T. Saitoh, S. Akira, N. T. Ktistakis, T. Izumi, T. Noda and T. Yoshimori, Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L, J Cell Biol 190: 511-521 (2010).
99. H. E. Polson, J. de Lartigue, D. J. Rigden, M. Reedijk, S. Urbe, M. J. Clague and S. A. Tooze, Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagoph-ores and positively regulates LC3 lipidation, Autophagy 6: 506-522 (2010).
100. J. L. Webber and S. A. Tooze, New insights into the function of Atg9, FEBS Lett 584: 1319-1326 (2010).
101. M. Mari, J. Griffith, E. Rieter, L. Krishnappa, D. J. Klionsky and F. Reggiori, An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis, J Cell Biol 190: 1005-1022 (2010).
102. N. Roudier, C. Lefebvre and R. Legouis, CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans, Traffic 6: 695-705 (2005).
103. K. Tamai, M. Toyoshima, N. Tanaka, N. Yamamoto, Y. Owada, H. Kiyonari, K. Murata, Y. Ueno, M. Ono, T. Shimosegawa, N. Yaegashi, M. Watanabe and K. Sugamura, Loss of hrs in the central nervous system causes accumulation of ubiquitinated proteins and neurodegeneration, Am J Pathol 173: 1806-1817 (2008).
104. K. Shirahama, T. Noda and Y. Ohsumi, Mutational analysis of Csc1/Vps4p: involvement of endosome in regulation of autophagy in yeast, Cell Struct Funct 22: 501-509 (1997).
105. Y. Zhong, Q. J. Wang, X. Li, Y. Yan, J. M. Backer, B. T. Chait, N. Heintz and Z. Yue, Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex, Nat Cell Biol 11: 468-476 (2009).
106. S. E. Rieder and S. D. Emr, A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole, Mol Biol Cell 8: 2307-2327 (1997).