Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae

Journal of Cell Science

Volumn 126, Issue 11, 2013, Pages 2534-2544

  Suzuki, Kuninori ^a   Akioka, Manami ^b   Kondo Kakuta, Chika ^b   Yamamoto, Hayashi ^b   Ohsumi, Yoshinori ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Aminopeptidase I; Ape1; Ape1 complex; ATG; Autophagosome; Autophagy; Autophagy related genes; Endoplasmic reticulum exit sites; ERES; Isolation membrane; PAS; Pre autophagosomal structure; Rapamycin; Starvation; Vacuole isolation membrane contact site; VICS; Yeast

Indexed keywords

ATG1 PROTEIN; ATG12 PROTEIN; ATG13 PROTEIN; ATG16 PROTEIN; ATG17 PROTEIN; ATG18 PROTEIN; ATG8 PROTEIN; ATG9 PROTEIN; AUTOPHAGY PROTEIN 5; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGOSOME; CELL JUNCTION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; MEMBRANE FORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; TONOPLAST;

AMINOPEPTIDASE I; APE1; APE1 COMPLEX; ATG; AUTOPHAGOSOME; AUTOPHAGY; AUTOPHAGY-RELATED GENES; ENDOPLASMIC RETICULUM EXIT SITES; ERES; ISOLATION MEMBRANE; PAS; PRE-AUTOPHAGOSOMAL STRUCTURE; RAPAMYCIN; STARVATION; VACUOLE-ISOLATION MEMBRANE CONTACT SITE; VICS; YEAST;

AUTOPHAGY; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84880019176     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122960     Document Type: Article

References (56)

1. Adams, A., Gottschling, D. E., Kaiser, C. A. and Stearns, T. (1998). Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. 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.
3. Bruns, C., McCaffery, J. M., Curwin, A. J., Duran, J. M. and Malhotra, V. (2011). Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J. Cell Biol. 195, 979-992.
4. Connerly, P. L., Esaki, M., Montegna, E. A., Strongin, D. E., Levi, S., Soderholm, J. and Glick, B. S. (2005). Sec16 is a determinant of transitional ER organization. Curr. Biol. 15, 1439-1447.
5. Dove, S. K., Piper, R. C., McEwen, R. K., Yu, J. W., King, M. C., Hughes, D. C., Thuring, J., Holmes, A. B., Cooke, F. T., Michell, R. H. et al. (2004). Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J. 23, 1922-1933.
6. Geng, J., Baba, M., Nair, U. and Klionsky, D. J. (2008). Quantitative analysis of autophagy-related protein stoichiometry by fluorescence microscopy. J. Cell Biol. 182, 129-140.
7. 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.
8. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T. and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437.
9. Horvath, A. and Riezman, H. (1994). Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10, 1305-1310.
10. Ishihara, N., Hamasaki, M., Yokota, S., Suzuki, K., Kamada, Y., Kihara, A., Yoshimori, T., Noda, T. and Ohsumi, Y. (2001). Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell 12, 3690-3702.
11. Kabeya, Y., Kamada, Y., Baba, M., Takikawa, H., Sasaki, M. and Ohsumi, Y. (2005). Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol. Biol. Cell 16, 2544-2553.
12. Kabeya, Y., Noda, N. N., Fujioka, Y., Suzuki, K., Inagaki, F. and Ohsumi, Y. (2009). Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 389, 612-615.
13. 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.
14. 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.
15. Kametaka, S., Okano, T., Ohsumi, M. and Ohsumi, Y. (1998). Apg14p and Apg6/ Vps30p form a protein complex essential for autophagy in the yeast, Saccharomyces cerevisiae. J. Biol. Chem. 273, 22284-22291.
16. Kawamata, T., Kamada, Y., Kabeya, Y., Sekito, T. and Ohsumi, Y. (2008). Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol. Biol. Cell 19, 2039-2050.
17. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152, 519-530.
18. 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.
19. 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.
20. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
21. Lynch-Day, M. A. and Klionsky, D. J. (2010). The Cvt pathway as a model for selective autophagy. FEBS Lett. 584, 1359-1366.
22. Matsushita, M., Suzuki, N. N., Obara, K., Fujioka, Y., Ohsumi, Y. and Inagaki, F. (2007). Structure of Atg5?Atg16, a complex essential for autophagy. J. Biol. Chem. 282, 6763-6772.
23. 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, 245-250.
24. 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.
25. Mizushima, N., Kuma, A., Kobayashi, Y., Yamamoto, A., Matsubae, M., Takao, T., Natsume, T., Ohsumi, Y. and Yoshimori, T. (2003). Mouse Apg16L, a novel WDrepeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J. Cell Sci. 116, 1679-1688.
26. Mizushima, N., Yoshimori, T. and Ohsumi, Y. (2011). The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132.
27. 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.
28. Nakatogawa, H., Ishii, J., Asai, E. and Ohsumi, Y. (2012a). Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 8, 177-186.
29. Nakatogawa, H., Ohbayashi, S., Sakoh-Nakatogawa, M., Kakuta, S., Suzuki, S. W., Kirisako, H., Kondo-Kakuta, C., Noda, N. N., Yamamoto, H. and Ohsumi, Y. (2012b). The autophagy-related protein kinase Atg1 interacts with the ubiquitinlike protein Atg8 via the Atg8 family interacting motif to facilitate autophagosome formation. J. Biol. Chem. 287, 28503-28507.
30. Noda, T., Matsuura, A., Wada, Y. and Ohsumi, Y. (1995). Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 210, 126-132.
31. 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.
32. Obara, K., Noda, T., Niimi, K. and Ohsumi, Y. (2008a). Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 13, 537-547.
33. Obara, K., Sekito, T., Niimi, K. and Ohsumi, Y. (2008b). The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 283, 23972-23980.
34. Okamoto, M., Yoko-o, T., Umemura, M., Nakayama, K. and Jigami, Y. (2006). Glycosylphosphatidylinositol-anchored proteins are required for the transport of detergent-resistant microdomain-associated membrane proteins Tat2p and Fur4p. J. Biol. Chem. 281, 4013-4023.
35. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and Stevens, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
36. Reggiori, F., Shintani, T., Nair, U. and Klionsky, D. J. (2005). Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1, 101-109.
37. 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.
38. Rossanese, O. W., Reinke, C. A., Bevis, B. J., Hammond, A. T., Sears, I. B., O'Connor, J. and Glick, B. S. (2001). A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 153, 47-62.
39. Sato, K., Sato, M. and Nakano, A. (2003). Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol. Biol. Cell 14, 3605-3616.
40. Shintani, T. and Klionsky, D. J. (2004). Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 279, 29889-29894.
41. Shintani, T., Huang, W. P., Stromhaug, P. E. and Klionsky, D. J. (2002). Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev. Cell 3, 825-837.
42. 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.
43. Stephan, J. S., Yeh, Y. Y., Ramachandran, V., Deminoff, S. J. and Herman, P. K. (2009). The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc. Natl. Acad. Sci. USA 106, 17049-17054.
44. Strømhaug, P. E., Reggiori, F., Guan, J., Wang, C. W. and Klionsky, D. J. (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.
45. 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.
46. 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.
47. Suzuki, K., Noda, T. and Ohsumi, Y. (2004). Interrelationships among Atg proteins during autophagy in Saccharomyces cerevisiae. Yeast 21, 1057-1065.
48. Suzuki, K., Kubota, Y., Sekito, T. and Ohsumi, Y. (2007). Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12, 209-218.
49. Suzuki, K., Kondo, C., Morimoto, M. and Ohsumi, Y. (2010). Selective transport of a-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J. Biol. Chem. 285, 30019-30025.
50. 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.
51. 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.
52. Wang, C.W., Kim, J., Huang,W. P., Abeliovich, H., Stromhaug, P. E., Dunn,W. A., Jr and Klionsky, D. J. (2001). Apg2 is a novel protein required for the cytoplasmto vacuole targeting, autophagy, and pexophagy pathways. J. Biol. Chem. 276, 30442-30451.
53. Xie, Z. and Klionsky, D. J. (2007). Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109.
54. Yamamoto, H., Kakuta, S., Watanabe, T. M., Kitamura, A., Sekito, T., Kondo-Kakuta, C., Ichikawa, R., Kinjo, M. and Ohsumi, Y. (2012). Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J. Cell Biol. 198, 219-233.
55. Ylä-Anttila, P., Vihinen, H., Jokitalo, E. and Eskelinen, E. L. (2009). 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180-1185.
56. Yorimitsu, T. and Sato, K. (2012). Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol. Biol. Cell 23, 2930-2942.