Autophagosome formation in mammalian cells

Cell Structure and Function

Volumn 27, Issue 6, 2002, Pages 421-429

  Mizushima, Noboru ^a,b   Ohsumi, Yoshinori ^a   Yoshimori, Tamotsu ^c  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Apg12; Apg5; Autophagosome; Autophagy; LC3

Indexed keywords

AUTOPHAGY; CELL FUNCTION; CELL ORGANELLE; EUKARYOTE; GENETIC CONSERVATION; HUMAN; INTRACELLULAR MEMBRANE; MAMMAL CELL; MEMBRANE FORMATION; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; REVIEW; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ANIMALS; AUTOPHAGY; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LYSOSOMES; MAMMALS; PROTEIN KINASES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSPORT VESICLES;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0037005262     PISSN: 03867196     EISSN: None     Source Type: Journal    
DOI: 10.1247/csf.27.421     Document Type: Review

References (83)

1. Anglade, P., Vyas, S., Javoy-Agid, F., Herrero, M.T., Michel, P.P., Marquez, J., Mouatt-Prigent, A., Ruberg, M., Hirsch, E.C., and Agid, Y. 1997. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol., 12: 25-31.
2. 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.
3. Berg, T.O., Fengsrud, M., Stromhaug, P.E., Berg, T., and Seglen, P.O. 1998. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J. Biol. Chem., 273: 21883-21892.
4. Bishop, N. and Woodman, P. 2000. ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell, 11: 227-239.
5. Blommaart, E.F.C., Luiken, J.J.F.P., and Meijer, A.J. 1997. Autophagic proteolysis: control and specificity. Histochem. J., 29: 365-385.
6. Bolender, R.P. and Weibel, E.R. 1973. A morphometric study of the removal of phenobarbital-induced membranes from hepatocytes after cessation of treatment. J. Cell Biol., 56: 746-761.
7. Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H., and Balch, W.E. 1995. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol., 130: 781-796.
8. Cataldo, A.M., Hamilton, D.J., Barnett, J.L., Paskevich, P.A., and Nixon, R.A. 1996. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J. Neurosci., 16: 186-199.
9. A receptor clustering and modulates the channel kinetics. Proc. Natl. Acad. Sci. USA, 97: 11557-11562.
10. Clarke, P.G. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.), 181: 195-213.
11. A receptor localization and tubulin binding. Neuron, 33: 63-74.
12. Davidson, H.W. 1995. Wortmannin causes mistargeting of procathepsin D. Evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol., 130: 797-805.
13. Davies, J. and Murphy, D. 2002. Autophagy in hypothalamic neurones of rats expressing a familial neurohypophysial diabetes insipidus transgene. J. Neuroendocrinol., 14: 629-37.
14. Dunn, W.A.J. 1994. Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol., 4: 139-143.
15. Fengsrud, M., Roos, N., Berg, T., Liou, W., Slot, J.W., and Seglen, P.O. 1995. Ultrastructural and immunocytochemical characterization of autophagic vacuoles in isolated hepatocytes: effects of vinblastine and asparagine on vacuole distributions. Exp. Cell Res., 221: 504-519.
16. Goto, Y., Komiyama, A., Tanabe, Y., Katafuchi, Y., Ohtaki, E., and Nonaka, I. 1990. Myopathy in Marinesco-Sjogren syndrome: an ultrastructural study. Acta Neuropathol., 80: 123-128.
17. Hammond, E.M., Brunet, C.L., Johnson, G.D., Parkhill, J., Milner, A.E., Brady, G., Gregory, C.D., and Grand, R.J.A. 1998. Homology between a human apoptosis specific protein and the product of APG5, a gene involved in autophagy in yeast. FEBS Lett., 425: 391-395.
18. Hershko, A. and Ciechanover, A. 1998. The ubiquitin system. Annu. Rev. Biochem., 67: 425-479.
19. Hochstrasser, M. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet., 30: 405-439.
20. 14C]lactose, to distinguish between pre-lysosomal and lysosomal steps in the autophagic pathway. Exp. Cell Res., 166: 1-14.
21. Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., Noda, T., and Ohsumi, Y. 2000. A ubiquitin-like system mediates protein lipidation. Nature, 408: 488-492.
22. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J., 19: 5720-5728.
23. Kalimo, H., Savontaus, M.L., Lang, H., Paljarvi, L., Sonninen, V., Dean, P.B., Katevuo, K., and Salminen, A. 1988. X-linked myopathy with excessive autophagy: a new hereditary muscle disease. Ann. Neurol., 23: 258-265.
24. Kamada, Y., Funakoshi, T., Shintani, T., Nagano, K., Ohsumi, M., and Ohsumi, Y. 2000. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol., 150: 1507-1513.
25. Kegel, K.B., Kim, M., Sapp, E., McIntyre, C., Castano, J.G., Aronin, N., and DiFiglia, M. 2000. Huntingtin expression stimulates endosomallysosomal activity, endosome tubulation, and autophagy. J. Neurosci., 20: 7268-7278.
26. Khalfan, W.A., and Klionsky, D.J. 2002. Molecular machinery required for autophagy and the cytoplasm to vacuole targeting (Cvt) pathway in S. cerevisiae. Curr. Opin. Cell Biol., 14: 468-475.
27. Kihara, A., Kabeya, Y., Ohsumi, Y., and Yoshimori, T. 2001a. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Report, 2: 330-335.
28. Kihara, A., Noda, T., Ishihara, N., and Ohsumi, Y. 2001b. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol., 152: 519-530.
29. Kim, J., Huang, W.-P., Stromhaug, P.E., and Klionsky, D.J. 2002. Convergence of multiple autophagy and Cvt components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem., 277: 763-773.
30. Kirisako, T., Ichimura, Y., Okada, H., Kabeya, Y., Mizushima, N., Yoshimori, T., Ohsumi, M., Takao, T., Noda, T., and Ohsumi, Y. 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: 263-275.
31. Klionsky, D.J. and Emr, S.D. 2000. Autophagy as a regulated pathway of cellular degradation. Science, 290: 1717-1721.
32. AR)-associated protein GABAPAR interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc. Natl. Acad. Sci. USA, 97: 8594-8599.
33. Kopito, R.R. 2000. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol., 10: 524-530.
34. Kovacs, A.L., Reith, A., and Seglen, P.O. 1982. Accumulation of autophagosomes after inhibition of hepatocytic protein degradation by vinblastine, leupeptin or a lysosomotropic amine. Exp. Cell Res., 137: 191-201.
35. Kuma, A., Mizushima, N., Ishihara, N., and Ohsumi, Y. 2002. Formation of the ∼350 kD Apg12-Apg5-Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J. Biol. Chem., 277: 18619-18625.
36. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature, 402: 672-676.
37. Liang, X.H., Kleeman, L., Jaing, H.H., Gordon, G., Goldman, J.E., Berry, G., Herman, B., and Levine, B. 1998. Protection against fatal Sindbis virus encephalitis by Beclin, a novel Bcl-2-interacting protein. J. Virol., 72: 8586-8596.
38. Liou, W., Geuze, H.J., Geelen, M.J., and Slot, J.W. 1997. The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J. Cell Biol., 136: 61-70.
39. Mann, S.S. and Hammarback, J.A. 1994. Molecular characterization of light chain 3. J. Biol., Chem., 269: 11492-11497.
40. Masaki, R., Yamamoto, A., and Tashiro, Y. 1987. Cytochrome P-450 and NADPH-cytochrome P-450 reductase are degraded in the autolysosomes in rat liver. J. Cell Biol., 104: 1207-1215.
41. Matsuura, A., Tsukada, M., Wada, Y., and Ohsumi, Y. 1997. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene, 192: 245-50.
42. Mizushima, N., Noda, T., and Ohsumi, Y. 1999. Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J, 18: 3888-3896.
43. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M., and Ohsumi, Y. 1998a. A protein conjugation system essential for autophagy. Nature, 395: 395-398.
44. Mizushima, N., Sugita, H., Yoshimori, T., and Ohsumi, Y. 1998b. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem., 273: 33889-33892.
45. Mizushima, N., Yamamoto, A., Hatano, M., Kobayashi, Y., Kabeya, Y., Suzuki, K., Tokuhisa, T., Ohsumi, Y., and Yoshimori, T. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol., 152: 657-667.
46. Mizushima, N., Yoshimori, T., and Ohsumi, Y. 2002. Mouse Apg10 as an Apg12 conjugating enzyme: Analysis by the conjugation-mediated yeast two-hybrid method. FEBS Lett., 532: 450-454.
47. Mizushima, N., Yoshimori, T., and Ohsumi, Y. 2003. Role of the Apg12 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol., in press.
48. Mortimore, G.E. and Poso, A.R. 1987. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu. Rev. Nutr., 7: 539-564.
49. Mukaiyama, H., Oku, M., Baba, M., Samizo, T., Hammond, A.T., Glick, B.S., Kato, N., and Sakai, Y. 2002. Paz2 and 13 other PAZ gene products regulate vacuolar engulfment of peroxisomes during micropexophagy. Genes Cell, 7: 75-90.
50. 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.
51. Nishino, I., Fu, J., Tanji, K., Yamada, T., Shimojo, S., Koori, T., Mora, M., Riggs, J.E., Oh, S.J., Koga, Y., Sue, C.M., Yamamoto, A., Murakami, N., Shanske, S., Byrne, E., Bonilla, E., Nonaka, I., DiMauro, S., and Hirano, M. 2000. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature, 406: 906-910.
52. Noda, T., Suzuki, K., and Ohsumi, Y. 2002. Yeast autophagosomes: de novo formation of a membrane structure. Trends Cell Biol., 12: 231-235.
53. Nonaka, I. 1999. Distal myopathies. Curr. Opin. Neurol., 12: 493-499.
54. A receptor-associated protein (GABARAP) mediating dimer formation. Neuropharmacology, 43: 476-481.
55. Ohsumi, Y. 2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol., 2: 211-216.
56. Okamoto, K., Hirai, S., Iizuka, T., Yanagisawa, T., and Watanabe, M. 1991. Reexamination of granulovacuolar degeneration. Acta. Neuropathol. (Berl), 82: 340-345.
57. Okazaki, N., Yan, J., Yuasa, S., Ueno, T., Kominami, E., Masuho, Y., Koga, H., and Muramatsu, M. 2000. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res. Mol. Brain Res., 85: 1-12.
58. Petersen, A., Larsen, K.E., Behr, G.G., Romero, N., Przedborski, S., Brundin, P., and Sulzer, D. 2001. Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration. Hum. Mol. Genet., 10: 1243-1254.
59. Petiot, A., Ogier-Denis, E., Blommaart, E.F., Meijer, A.J., and Codogno, P. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem., 275: 992-998.
60. Ravikumar, B., Duden, R., and Rubinsztein, D.C. 2002. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet., 11: 1107-1117.
61. Reggiori, F. and Klionsky, D.J. 2002. Autophagy in the eukaryotic cell. Eukaryotic Cell, 1: 11-21.
62. Sagiv, Y., Legesse-Miller, A., Porat, A., and Elazar, Z. 2000. GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. EMBO J., 19: 1494-1504.
63. Sakai, Y., Koller, A., Rangell, L.K., Keller, G.A., and Subramani, S. 1998. Peroxisome degradation by microautophagy in Pichia pastoris: Identification of specific steps and morphological intermediates. J. Cell Biol., 141: 625-636.
64. Schweichel, J.U. and Merker, H.J. 1973. The morphology of various types of cell death in prenatal tissues. Teratology, 7: 253-266.
65. Seglen, P.O. and Bohley, P. 1992. Autophagy and other vacuolar protein degradation mechanisms. Experientia, 48: 158-172.
66. Seglen, P.O. and Gordon, P.B. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA, 79: 1889-1892.
67. A receptor-associated protein GABARAP: implications for biolgoical function and its regulation. J. Biol. Chem., 277: 13363-13366.
68. Stromhaug, P.E., Bevan, A., and Dunn, W.A., Jr. 2001. GSA11 encodes a unique 208-kDa protein required for pexophagy and autophagy in Pichia pastoris. J. Biol. Chem., 276: 42422-42435.
69. Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T., and Ohsumi, Y. 2001. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J, 20: 5971-5981.
70. 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.
71. Tanida, I., Tanida-Miyake, E., Komatsu, M., Ueno, T., and Kominami, E. 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.
72. Tanida, I., Tanida-Miyake, E., Ueno, T., and Kominami, E. 2001. The human homolog of Saccharomyces cerevisiae Apg7p is a protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J. Biol. Chem., 276: 1701-1706.
73. 1-antitrypsin deficient liver: consultative activation of autophagy. Am. J. Physiol. Gastrointest. Liver Physiol., 283: G1156-G1165.
74. Teckman, J.H. and Perlmutter, D.H. 2000. Retention of mutant α1-antitrypsin Z in endoplasmic reticulum is associated with an autophagic response. Am. J. Physiol. Gastrointest. Liver Physiol., 279: G961-G974.
75. Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenbuis, M., and Wolf, D.H. 1994. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett., 349: 275-280.
76. Tooze, J., Hollinshead, M., Ludwig, T., Howell, K., Hoflack, B., and Kern, H. 1990. In exocrine pancreas, the basolateral endocytic pathway converges with the autophagic pathway immediately after the early endosome. J. Cell Biol., 111: 329-345.
77. Tsukada, M. and Ohsumi, Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett., 333: 169-174.
78. A receptors and the cytoskeleton. Nature, 397: 69-72.
79. Yamamoto, A., Masaki, R., and Tashiro, Y. 1990. Characterization of the isolation membranes and the limiting membranes of autophagosomes in rat hepatocytes by lectin cytochemistry. J. Histochem. Cytochem., 38: 573-580.
80. Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R., and Tashiro, Y. 1998. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct., 23: 33-42.
81. Yan, J., Kuroyanagi, H., Kuroiwa, A., Matsuda, Y., Tokumitsu, H., Tomoda, T., Shirasawa, T., and Muramatsu, M. 1998. Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem. Biophys. Res. Commun., 246: 222-227.
82. Yoshimori, T., Yamagata, F., Yamamoto, A., Mizushima, N., Kabeya, Y., Nara, A., Miwako, I., Ohashi, M., Ohsumi, M., and Ohsumi, Y. 2000. The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Mol. Biol. Cell, 11: 747-763.
83. Yung, H.W., Xue, L., and Tolkovsky, A.M. 2002. Apoptosis-specific protein (ASP 45 kDa) is distinct from human Apg5, the homologue of the yeast autophagy gene apg5. FEBS Lett., 531: 168-172.