Post-golgi sec proteins are required for autophagy in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 21, Issue 13, 2010, Pages 2257-2269

  Geng, Jiefei ^a   Nair, Usha ^a   Yasumura Yorimitsu, Kyoko ^a   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; GUANOSINE TRIPHOSPHATASE; MUTANT PROTEIN; PROTEIN SEC2; PROTEIN SEC4; RAB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ENVIRONMENTAL CHANGE; GOLGI COMPLEX; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE;

AUTOPHAGY; GOLGI APPARATUS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PHAGOSOMES; PHENOTYPE; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 77954184503     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E09-11-0969     Document Type: Article

References (72)

1. Abeliovich, H., Zhang, C., Dunn, W. A., Jr., Shokat, K. M., and Klionsky, D. J. (2003). Chemical genetic analysis of Apg1 reveals a non-kinase role in the induction of autophagy. Mol. Biol. Cell 14, 477-490.
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. Babst, M., Wendland, B., Estepa, E. J., and Emr, S. D. (1998). The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993.
4. Babu, P., Bryan, J. D., Panek, H. R., Jordan, S. L., Forbrich, B. M., Kelley, S. C., Colvin, R. T., and Robinson, L. C. (2002). Plasma membrane localization of the Yck2p yeast casein kinase 1 isoform requires the C-terminal extension and secretory pathway function. J. Cell Sci. 115, 4957-4968.
5. Benli, M., Doring, F., Robinson, D. G., Yang, X., and Gallwitz, D. (1996). Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J. 15, 6460-6475. (Pubitemid 26413779)
6. Cheong, H., Nair, U., Geng, J., and Klionsky, D. J. (2007). The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 668-681.
7. Cheong, H., Yorimitsu, T., Reggiori, F., Legakis, J. E., Wang, C.-W., and Klionsky, D. J. (2005). Atg17 regulates the magnitude of the autophagic response. Mol. Biol. Cell 16, 3438-3453.
8. Christianson, T. W., Sikorski, R. S., Dante, M., Shero, J. H., and Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
9. Darsow, T., Rieder, S. E., and Emr, S. D. (1997). A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138, 517-529.
10. Dunn, W. A., Jr., Cregg, J. M., Kiel, J.A.K.W., van der Klei, I. J., Oku, M., Sakai, Y., Sibirny, A. A., Stasyk, O. V., and Veenhuis, M. (2005). Pexophagy: the selective autophagy of peroxisomes. Autophagy 1, 75-83.
11. Elkind, N. B., Walch-Solimena, C., and Novick, P. J. (2000). The role of the COOH terminus of Sec2p in the transport of post-Golgi vesicles. J. Cell Biol. 149, 95-110.
12. Fengsrud, M., Erichsen, E. S., Berg, T. O., Raiborg, C., and Seglen, P. O. (2000). Ultrastructural characterization of the delimiting membranes of isolated autophagosomes and amphisomes by freeze-fracture electron microscopy. Eur. J. Cell Biol. 79, 871-882.
13. 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.
14. Geng, J., and Klionsky, D. J. (2008a). Quantitative regulation of vesicle formation in yeast non-specific autophagy. Autophagy 4, 955-957.
15. Geng, J., and Klionsky, D. J. (2008b). The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. EMBO Rep. 9, 859-864.
16. Grosshans, B. L., Andreeva, A., Gangar, A., Niessen, S., Yates, J. R., Brennwald, P., and Novick, P. J. (2006). The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J. Cell Biol. 172, 55-66.
17. Gueldener, U., Heinisch, J., Koehler, G. J., Voss, D., and Hegemann, J. H. (2002). A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30, e23
18. Guo, W., Roth, D., Walch-Solimena, C., and Novick, P. J. (1999). The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18, 1071-1080.
19. Harding, T. M., Morano, K. A., Scott, S. V., and Klionsky, D. J. (1995). Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131, 591-602.
20. He, C., Baba, M., Cao, Y., and Klionsky, D. J. (2008). Self-interaction is critical for Atg9 transport and function at the phagophore assembly site during autophagy. Mol. Biol. Cell 19, 5506-5516.
21. He, C., Song, H., Yorimitsu, T., Monastyrska, I., Yen, W.-L., Legakis, J. E., and Klionsky, D. J. (2006). Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J. Cell Biol. 175, 925-935.
22. Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J., and Riezman, H. (1997). Transport through the yeast endocytic pathway occurs through morphologically distinct compartments and requires an active secretory pathway and Sec18p/N-ethylmaleimide-sensitive fusion protein. Mol. Biol. Cell 8, 13-31.
23. Hirsimaki, Y., Hirsimaki, P., and Lounatmaa, K. (1982). Vinblastine-induced autophagic vacuoles in mouse liver and Ehrlich ascites tumor cells as assessed by freeze-fracture electron microscopy. Eur J. Cell Biol. 27, 298-301.
24. Huang, J., and Klionsky, D. J. (2007). Autophagy and human disease. Cell Cycle 6, 1837-1849.
25. Hutchins, M. U., and Klionsky, D. J. (2001). Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 276, 20491-20498.
26. 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.
27. 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.
28. Itzen, A., Rak, A., and Goody, R. S. (2007). Sec2 is a highly efficient exchange factor for the Rab protein Sec4. J. Mol. Biol. 365, 1359-1367.
29. Iwata, J., Ezaki, J., Komatsu, M., Yokota, S., Ueno, T., Tanida, I., Chiba, T., Tanaka, K., and Kominami, E. (2006). Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 281, 4035-4041.
30. Jedd, G., Mulholland, J., and Segev, N. (1997). Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 137, 563-580.
31. Kaneko, Y., Hayashi, N., Toh-e, A., Banno, I., and Oshima, Y. (1987). Structural characteristics of the PHO8 gene encoding repressible alkaline phosphatase in Saccharomyces cerevisiae. Gene 58, 137-148.
32. Kanki, T., Wang, K., Cao, Y., Baba, M., and Klionsky, D. J. (2009). Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98-109.
33. 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.
34. 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.
35. 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.
36. Klionsky, D. J., and Emr, S. D. (1989). Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J. 8, 2241-2250.
37. Labbé, S., and Thiele, D. J. (1999). Copper ion inducible and repressible promoter systems in yeast. Methods Enzymol. 306, 145-153.
38. Legakis, J. E., Yen, W.-L., and Klionsky, D. J. (2007). A cycling protein complex required for selective autophagy. Autophagy 3, 422-432.
39. Liang, Y., Morozova, N., Tokarev, A. A., Mulholland, J. W., and Segev, N. (2007). The role of Trs65 in the Ypt/Rab guanine nucleotide exchange factor function of the TRAPP II complex. Mol. Biol. Cell 18, 2533-2541.
40. 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.
41. 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, TRAPP III, to the phagophore to promote autophagy. Proc. Natl. Acad. Sci. USA 107, 7811-7816.
42. Medkova, M., France, Y. E., Coleman, J., and Novick, P. (2006). The rab exchange factor Sec2p reversibly associates with the exocyst. Mol. Biol. Cell 17, 2757-2769.
43. Mizuta, K., and Warner, J. R. (1994). Continued functioning of the secretory pathway is essential for ribosome synthesis. Mol. Cell. Biol. 14, 2493-2502.
44. Monastyrska, I., He, C., Geng, J., Hoppe, A. D., Li, Z., and Klionsky, D. J. (2008). Arp2 links autophagic machinery with the actin cytoskeleton. Mol. Biol. Cell 19, 1962-1975.
45. Nair, J., Müller, H., Peterson, M., and Novick, P. J. (1990). Sec2 protein contains a coiled-coil domain essential for vesicular transport and a dispensable carboxy terminal domain. J. Cell Biol. 110, 1897-1909. (Pubitemid 120026956)
46. Nakagawa, I., et al. (2004). Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040.
47. Nanduri, J., Mitra, S., Andrei, C., Liu, Y., Yu, Y., Hitomi, M., and Tartakoff, A. M. (1999). An unexpected link between the secretory path and the organization of the nucleus. J. Biol. Chem. 274, 33785-33789.
48. 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.
49. 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.
50. Ortiz, D., Medkova, M., Walch-Solimena, C., and Novick, P. J. (2002). Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 157, 1005-1015.
51. 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.
52. Reggiori, F., Tucker, K. A., Stromhaug, P. E., and Klionsky, D. J. (2004a). The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 6, 79-90.
53. Reggiori, F., Wang, C.-W., Nair, U., Shintani, T., Abeliovich, H., and Klionsky, D. J. (2004b). Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 2189-2204.
54. 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.
55. Scott, S. V., Hefner-Gravink, A., Morano, K. A., Noda, T., Ohsumi, Y., and Klionsky, D. J. (1996). Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl. Acad. Sci. USA 93, 12304-12308.
56. 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.
57. Shorer, H., Amar, N., Meerson, A., and Elazar, Z. (2005). Modulation of N-ethylmaleimide-sensitive factor activity upon amino acid deprivation. J. Biol. Chem. 280, 16219-16226.
58. Stevens, T., Esmon, B., and Schekman, R. (1982). Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell 30, 439-448.
59. Stromhaug, P. E., Berg, T. O., Fengsrud, M., and Seglen, P. O. (1998). Purification and characterization of autophagosomes from rat hepatocytes. Biochem. J. 335(Pt 2), 217-224. (Pubitemid 28491054)
60. Stromhaug, 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.
61. 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.
62. Suzuki, K., Kubota, Y., Sekito, T., and Ohsumi, Y. (2007). Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12, 209-218.
63. 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.
64. van der Vaart, A., Griffith, J., and Reggiori, F. (2010). Exit from the Golgi is required for the expansion of the autophagosomal phagophore in yeast Saccharomyces cerevisiae. Mol. Biol. Cell 21, 2270-2284.
65. Walch-Solimena, C., Collins, R. N., and Novick, P. J. (1997). Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 137, 1495-1509. (Pubitemid 27282232)
66. Walworth, N. C., Brennwald, P., Kabcenell, A. K., Garrett, M., and Novick, P. J. (1992). Hydrolysis of GTP by Sec4 protein plays an important role in vesicular transport and is stimulated by a GTPase-activating protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 2017-2028.
67. Wu, J.-Q., and Pollard, T. D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
68. Xie, Z., and Klionsky, D. J. (2007). Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109.
69. Xie, Z., Nair, U., Geng, J., Szefler, M. B., Rothman, E. D., and Klionsky, D. J. (2009). Indirect estimation of the area density of Atg8 on the phagophore. Autophagy 5, 217-220.
70. Xie, Z., Nair, U., and Klionsky, D. J. (2008). Atg8 controls phagophore expansion during autophagosome formation. Mol. Biol. Cell 19, 3290-3298.
71. Yen, W.-L., Legakis, J. E., Nair, U., and Klionsky, D. J. (2007). Atg27 is required for autophagy-dependent cycling of Atg9. Mol. Biol. Cell 18, 581-593.
72. Yen, W.-L., Shintani, T., Nair, U., Cao, Y., Richardson, B. C., Li, Z., Hughson, F. M., Baba, M., and Klionsky, D. J. (2009). The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J. Cell Biol. 188, 101-114.