Visualization of Atg3 during autophagosome formation in Saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8146-8153

  Ngu, Meipin ^a   Hirata, Eri ^a   Suzuki, Kuninori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

AUTOPHAGOSOME; AUTOPHAGY; CONJUGATION SYSTEM; INTERMEDIATE STRUCTURES; UBIQUITIN-LIKE;

YEAST;

ATG3 PROTEIN; AUTOPHAGY RELATED PROTEIN 8; CELL PROTEIN; UNCLASSIFIED DRUG; ATG3 PROTEIN, S CEREVISIAE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOSPHATIDYLETHANOLAMINE; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN CONJUGATING ENZYME;

ARTICLE; AUTOPHAGOSOME; CELLULAR DISTRIBUTION; CONTROLLED STUDY; MACROAUTOPHAGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; TONOPLAST; AUTOPHAGY; CELL VACUOLE; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; INTRACELLULAR MEMBRANE; METABOLISM; PHAGOSOME; PROTEIN TRANSPORT;

SACCHAROMYCES CEREVISIAE;

AUTOPHAGY; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; MICROSCOPY, FLUORESCENCE; PHAGOSOMES; PHOSPHATIDYLETHANOLAMINES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-CONJUGATING ENZYMES; VACUOLES;

EID: 84925706070     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.626952     Document Type: Article

References (34)

1. Kamada, Y., Sekito, T., and Ohsumi, Y. (2004) Autophagy in yeast: a TORmediated response to nutrient starvation. Curr. Top. Microbiol. Immunol. 279, 73-84
2. 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
3. Kim, J., Huang, W. P., Stromhaug, P. E., and Klionsky, D. J. (2002) 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, 763-773
4. Suzuki, K., and Ohsumi, Y. (2007) Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett. 581, 2156-2161
5. Suzuki, K., Kubota, Y., Sekito, T., and Ohsumi, Y. (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12, 209-218
6. Suzuki, K., and Ohsumi, Y. (2010) Current knowledge of the pre-autophagosomal structure (PAS). FEBS Lett. 584, 1280-1286
7. Baba, M., Takeshige, K., Baba, N., and Ohsumi, Y. (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J. Cell Biol. 124, 903-913
8. 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
9. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., and Ohsumi, Y. (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446
10. Suzuki, K., Akioka, M., Kondo-Kakuta, C., Yamamoto, H., and Ohsumi, Y. (2013) Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J. Cell Sci. 126, 2534-2544
11. 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
12. Geng, J., and Klionsky, D. J. (2008) The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy: protein modifications: beyond the usual suspects' review series. EMBO Rep. 9, 859-864
13. 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, 263-276
14. Tanida, I., Mizushima, N., Kiyooka, M., Ohsumi, M., Ueno, T., Ohsumi, Y., and Kominami, E. (1999) Apg7p/Cvt2p: a novel protein-activating enzyme essential for autophagy. Mol. Biol. Cell 10, 1367-1379
15. Yamaguchi, M., Noda, N. N., Nakatogawa, H., Kumeta, H., Ohsumi, Y., and Inagaki, F. (2010) Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway. J. Biol. Chem. 285, 29599-29607
16. Kuma, A., Mizushima, N., Ishihara, N., and Ohsumi, Y. (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
17. Hanada, T., Noda, N. N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F., and Ohsumi, Y. (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282, 37298-37302
18. Nakatogawa, H., Ichimura, Y., and Ohsumi, Y. (2007) Atg8, a ubiquitinlike protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130, 165-178
19. Ichimura, Y., Imamura, Y., Emoto, K., Umeda, M., Noda, T., and Ohsumi, Y. (2004) In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J. Biol. Chem. 279, 40584-40592
20. Yamada, Y., Suzuki, N. N., Hanada, T., Ichimura, Y., Kumeta, H., Fujioka, Y., Ohsumi, Y., and Inagaki, F. (2007) The crystal structure of Atg3, an autophagy-related ubiquitin carrier protein (E2) enzyme that mediates Atg8 lipidation. J. Biol. Chem. 282, 8036-8043
21. Robinson, J. S., Klionsky, D. J., Banta, L. M., and Emr, S. D. (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 8, 4936-4948
22. Suzuki, K., Morimoto, M., Kondo, C., and Ohsumi, Y. (2011) Selective autophagy regulates insertional mutagenesis by the Ty1 retrotransposon in Saccharomyces cerevisiae. Dev. Cell 21, 358-365
23. Jones, G. M., Stalker, J., Humphray, S., West, A., Cox, T., Rogers, J., Dunham, I., and Prelich, G. (2008) A systematic library for comprehensive overexpression screens in Saccharomyces cerevisiae. Nat. Methods 5, 239-241
24. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
25. Suzuki, K., Nakamura, S., Morimoto, M., Fujii, K., Noda, N. N., Inagaki, F., and Ohsumi, Y. (2014) Proteomic profiling of autophagosome cargo in Saccharomyces cerevisiae. PLoS One 9, e91651
26. Horvath, A., and Riezman, H. (1994) Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10, 1305-1310
27. Suzuki, K., Kamada, Y., and Ohsumi, Y. (2002) Studies of cargo delivery to the vacuole mediated by autophagosomes in Saccharomyces cerevisiae. Dev. Cell 3, 815-824
28. Kamada, Y., Yoshino, K., Kondo, C., Kawamata, T., Oshiro, N., Yonezawa, K., and Ohsumi, Y. (2010) Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol. Cell. Biol. 30, 1049-1058
29. Baba, M., Osumi, M., Scott, S. V., Klionsky, D. J., and Ohsumi, Y. (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol. 139, 1687-1695
30. Klionsky, D. J., Cueva, R., and Yaver, D. S. (1992) Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell Biol. 119, 287-299
31. Shintani, T., and Klionsky, D. J. (2004) Cargo proteins facilitate the forma- tion of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 279, 29889-29894
32. Hanada, T., Satomi, Y., Takao, T., and Ohsumi, Y. (2009) The aminoterminal region of Atg3 is essential for association with phosphatidylethanolamine in Atg8 lipidation. FEBS Lett. 583, 1078-1083
33. Kaiser, S. E., Mao, K., Taherbhoy, A. M., Yu, S., Olszewski, J. L., Duda, D. M., Kurinov, I., Deng, A., Fenn, T. D., Klionsky, D. J., and Schulman, B. A. (2012) Noncanonical E2 recruitment by the autophagy E1 revealed by Atg7-Atg3 and Atg7-Atg10 structures. Nat. Struct. Mol. Biol. 19, 1242-1249
34. 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, 657-668