Atg9A trafficking through the recycling endosomes is required for autophagosome formation

Journal of Cell Science

Volumn 129, Issue 20, 2016, Pages 3781-3791

  Imai, Kenta ^a   Hao, Feike ^a,b   Fujita, Naonobu ^a,c   Tsuji, Yasuhiro ^a   Oe, Yukako ^a   Araki, Yasuhiro ^a   Hamasaki, Maho ^a,b   Noda, Takeshi ^a   Yoshimori, Tamotsu ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

AP 2; Atg9; Autophagy; Golgi; Recycling endosome; Sorting motif; TRAPP

Indexed keywords

ATG9A PROTEIN; MEMBRANE PROTEIN; TRANSCRIPTION FACTOR AP 2; TRAPPC8 PROTEIN; UNCLASSIFIED DRUG; ADAPTOR PROTEIN; ATG9A PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN; TYROSINE; VESICULAR TRANSPORT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; MUTATION; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANS GOLGI NETWORK; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ENDOCYTOSIS; GENE SILENCING; HELA CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; SALMONELLA; STRUCTURE ACTIVITY RELATION;

ADAPTOR PROTEIN COMPLEX 2; AMINO ACID MOTIFS; ANIMALS; AUTOPHAGOSOMES; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; ENDOCYTOSIS; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; SALMONELLA; STRUCTURE-ACTIVITY RELATIONSHIP; TRANS-GOLGI NETWORK; TYROSINE; VESICULAR TRANSPORT PROTEINS;

EID: 84989197267     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.196196     Document Type: Article

References (35)

1. Barlowe, C. (2003). Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13, 295-300.
2. Behrends, C., Sowa, M. E., Gygi, S. P. and Harper, J. W. (2010). Network organization of the human autophagy system. Nature 466, 68-76.
3. Birmingham, C. L., Smith, A. C., Bakowski, M. A., Yoshimori, T. and Brumell, J. H. (2006). Autophagy controls salmonella infection in response to damage to the salmonella-containing vacuole. J. Biol. Chem. 281, 11374-11383.
4. Bonifacino, J. S. and Traub, L. M. (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447.
5. Carlos Martín Zoppino, F., Damián Militello, R., Slavin, I., álvarez, C. and Colombo, M. I. (2010). Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 11, 1246-1261.
6. Fujita, N., Morita, E., Itoh, T., Tanaka, A., Nakaoka, M., Osada, Y., Umemoto, T., Saitoh, T., Nakatogawa, H., Kobayashi, S. et al. (2013). Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 203, 115-128.
7. Guo, Y., Chang, C., Huang, R., Liu, B., Bao, L. and Liu, W. (2012). AP1 is essential for generation of autophagosomes from the trans-Golgi network. J. Cell Sci. 125, 1706-1715.
8. 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.
9. 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.
10. Kageyama, S., Omori, H., Saitoh, T., Sone, T., Guan, J.-L., Akira, S., Imamoto, F., Noda, T. and Yoshimori, T. (2011). The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol. Biol. Cell 22, 2290-2300.
11. Kampmann, M., Bassik, M. C. andWeissman, J. S. (2013). Integrated platform for genome-wide screening and construction of high-density genetic interaction maps in mammalian cells. Proc. Natl. Acad. Sci. USA 110, E2317-E2326.
12. Kawabata, T. and Yoshimori, T. (2016). Beyond starvation: an update on the autophagic machinery and its functions. J. Mol. Cell. Cardiol. 95, 2-10.
13. Knævelsrud, H., Søreng, K., Raiborg, C., Håberg, K., Rasmuson, F., Brech, A., Liestøl, K., Rusten, T. E., Stenmark, H., Neufeld, T. P. et al. (2013). Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J. Cell Biol. 202, 331-349.
14. Köchl, R., Hu, X. W., Chan, E. Y. W. and Tooze, S. A. (2006). Microtubules Facilitate Autophagosome Formation and Fusion of Autophagosomes with Endosomes. Traffic 7, 129-145.
15. Lamb, C. A., Nühlen, S., Judith, D., Frith, D., Snijders, A. P., Behrends, C. and Tooze, S. A. (2015). TBC1D14 regulates autophagy via the TRAPP complex and ATG9 traffic. EMBO J. 35, 281-301.
16. Longatti, A., Lamb, C. A., Razi, M., Yoshimura, S.-I., Barr, F. A. and Tooze, S. A. (2012). TBC1D14 regulates autophagosome formation via Rab11-and ULK1-positive recycling endosomes. J. Cell Biol. 197, 659-675.
17. Lynch-Day, M. A., Bhandari, D., Menon, S., Huang, J., Cai, H., Bartholomew, C. R., Brumell, J. H., Ferro-Novick, S. and Klionsky, D. J. (2010). Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc. Natl. Acad. Sci. USA 107, 7811-7816.
18. Morita, S., Kojima, T. and Kitamura, T. (2000). Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7, 1063-1066.
19. 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.
20. Nishimura, N. and Balch, W. E. (1997). A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277, 556-558.
21. Noda, T., Kim, J., Huang, W.-P., Baba, M., Tokunaga, C., Ohsumi, Y. and Klionsky, D. J. (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.
22. Orsi, A., Razi, M., Dooley, H. C., Robinson, D., Weston, A. E., Collinson, L. M. and Tooze, S. A. (2012). Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23, 1860-1873.
23. Popovic, D. and Dikic, I. (2014). TBC1D5 and the AP2 complex regulate ATG9 trafficking and initiation of autophagy. EMBO Rep. 15, 392-401.
24. Puri, C., Renna, M., Bento, C. F., Moreau, K. and Rubinsztein, D. C. (2013). Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154, 1285-1299.
25. Rohn, W. M., Rouille, Y., Waguri, S. and Hoflack, B. (2000). Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J. Cell Sci. 113, 2093-2101.
26. Ropolo, A., Grasso, D., Pardo, R., Sacchetti, M. L., Archange, C., Re, A. L., Seux, M., Nowak, J., Gonzalez, C. D., Iovanna, J. L. et al. (2007). The pancreatitis-induced vacuole membrane protein 1 triggers autophagy in mammalian cells. J. Biol. Chem. 282, 37124-37133.
27. Saitoh, T., Nakayama, M., Nakano, H., Yagita, H., Yamamoto, N. and Yamaoka, S. (2003). TWEAK induces NF-B2 p100 processing and long lasting NF-kB activation. J. Biol. Chem. 278, 36005-36012.
28. Saitoh, T., Fujita, N., Hayashi, T., Takahara, K., Satoh, T., Lee, H., Matsunaga, K., Kageyama, S., Omori, H., Noda, T. et al. (2009). Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. USA 106, 20842-20846.
29. Shibutani, S. T. and Yoshimori, T. (2014). A current perspective of autophagosome biogenesis. Cell Res. 24, 58-68.
30. Shirahama-Noda, K., Kira, S., Yoshimori, T. and Noda, T. (2013). TRAPPIII is responsible for vesicular transport from early endosomes to Golgi, facilitating Atg9 cycling in autophagy. J. Cell Sci. 126, 4963-4973.
31. Takahashi, Y., Meyerkord, C. L., Hori, T., Runkle, K., Fox, T. E., Kester, M., Loughran, T. P. and Wang, H.-G. (2011). Bif-1 regulates Atg9 trafficking by mediating the fission of Golgi membranes during autophagy. Autophagy 7, 61-73.
32. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2005). Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91.
33. Webber, J. L. and Tooze, S. A. (2010). Coordinated regulation of autophagy by p38a MAPK through mAtg9 and p38IP. EMBO J. 29, 27-40.
34. Young, A. R. J., Chan, E. Y. W., Hu, X. W., Kochl, R., Crawshaw, S. G., High, S., Hailey, D. W., Lippincott-Schwartz, J. and Tooze, S. A. (2006). Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119, 3888-3900.
35. Zavodszky, E., Seaman, M. N. J., Moreau, K., Jimenez-Sanchez, M., Breusegem, S. Y., Harbour, M. E. and Rubinsztein, D. C. (2014). Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy. Nat. Commun. 5, 3828.