Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy

Molecular Biology of the Cell

Volumn 15, Issue 8, 2004, Pages 3553-3566

  Strømhaug, Per E ^a,b   Reggiori, Fulvio ^a   Guan, Ju ^a   Wang, Chao Wen ^a   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE I; BINDING PROTEIN; NITROGEN; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHOINOSITIDE BINDING PROTEIN; PROTEIN ATG12; PROTEIN ATG18; PROTEIN ATG21; PROTEIN ATG5; PROTEIN YGR223C; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL ORGANELLE; CELL VACUOLE; CONJUGATE; CONJUGATION; CYTOPLASM; LIPID TRANSPORT; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

AMINOPEPTIDASES; AUTOPHAGY; CELL MEMBRANE; ENDOPEPTIDASES; GENE DELETION; LIPID METABOLISM; MICROTUBULE-ASSOCIATED PROTEINS; PHAGOSOMES; PHOSPHATIDYLINOSITOLS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES;

EID: 3342951135     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-02-0147     Document Type: Article

References (36)

1. Abeliovich, H., Dunn, W.A., Jr., Kim, J., and Klionsky, D.J. (2000). Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol. 151, 1025-1034.
2. Barth, H., Meiling-Wesse, K., Epple, U.D., and Thumm, M. (2001). Autophagy and the cytoplasm to vacuole targeting pathway both require Aut10p. FEBS Lett. 508, 23-28.
3. Barth, H., Meiling-Wesse, K., Epple, U.D., and Thumm, M. (2002). Mai1p is essential for maturation of proaminopeptidase 1 but not for autophagy. FEBS Lett. 512, 173-179.
4. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
5. Dove, S.K., et al. (2004). Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. (2004). EMBO J. 23, 1922-1933.
6. Gary, J.D., Wurmser, A.E., Bonangelino, C.J., Weisman, L.S., and Emr, S.D. (1998). Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J. Cell Biol. 143, 65-79.
7. Guan, J., Stromhaug, P.E., George, M.D., Habibzadegah-Tari, P., Bevan, A., Dunn, Jr., W.A., and Klionsky, D.J. (2001). Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol. Biol. Cell 12, 3821-3838.
8. Herman, P.K., and Emr, S.D. (1990). Characterization of Vps34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 6742-6754.
9. Hutchins, M.U., Veenhuis, M., and Klionsky, D.J. (1999). Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J. Cell Sci. 112, 4079-4087.
10. James, P., Halladay, J., and Craig, E.A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
11. Jeffries, T.R., Dove, S.K., Michell, R.H., and Parker, P.J. (2004). PtdIns-specific MPR pathway association of a novel WD40 repeat protein, WIPI49. Mol. Biol. Cell 15, 2652-2663.
12. 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.
13. Kim, J., Huang, W.-P., and Klionsky, D.J. (2001a). Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut7p, Aut1p, and the autophagy conjugation complex. J. Cell Biol. 252, 51-64.
14. 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.
15. Kim, J., Kamada, Y., Stromhaug, P.E., Guan, J., Hefner-Gravink, A., Baba, M., Scott, S.V., Ohsumi, Y., Dunn, Jr., W.A., and Klionsky, D.J. (2001b). Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J. Cell Biol. 253, 381-396.
16. 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.
17. Klionsky, D.J., et al. (2003). A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545.
18. 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.
19. Longtine, M.S., McKenzie, A., III, 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.
20. 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. 252, 657-668.
21. Nice, D.C., Sato, T.K., Strømhaug, P.E., Emr, S.D., and Klionsky, D.J. (2002). Cooperative binding of the cytoplasm to vacuole targeting pathway proteins, Cvt13 and Cvt20, to phosphatidylinositol 3-phosphate at the pre-autophagosomal structure is required for selective autophagy. J. Biol. Chem. 277, 30198-30207.
22. Noda, T., Kim, I., 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. 248, 465-480.
23. Noda, T., Matsuura, A., Wada, Y., and Ohsumi, Y. (1995). Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 220, 126-132.
24. Noda, T., and Ohsumi, Y. (2004). Macroautophagy in yeast. In: Autophagy, ed. D.J. Klionsky, Georgetown, TX: Landes Bioscience, 70-83.
25. Ohsumi, Y. (2001). Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell. Biol. 2, 211-216.
26. Paz, Y., Elazar, Z., and Pass, D. (1999). Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J. Biol. Chem. 275, 25445-25450.
27. Reggiori, F., Tucker, K.A., Stromhaug, P.E., and Klionsky, D.J. (2004). The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 6, 79-90.
28. Reggiori, P., Wang, C.-W., Stromhaug, P.E., Shintani, T., and Klionsky, D.J. (2003). Vps51 is part of the yeast Vps fifty-three tethering complex essential for retrograde traffic from the early endosome and Cvt vesicle completion. J. Biol. Chem. 278, 5009-5020.
29. 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.
30. 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.
31. Shintani, T., Suzuki, K., Kamada, Y., Noda, T., and Ohsumi, Y. (2001). Apg2p functions in autophagosome formation on the perivacuolar structure. J. Biol. Chem. 276, 30452-30460.
32. Stack, J.H., DeWald, D.B., Takegawa, K., and Emr, S.D. (1995). Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 229, 321-334.
33. Stromhaug, P.E. and Klionsky, D.J. (2004). Cytoplasm to vacuole targeting. In: Autophagy, ed. D.J. Klionsky, Georgetown, TX: Landes Bioscience, 84-106.
34. 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.
35. Yamamoto, A., DeWald, D.B., Boronenkov, I.V., Anderson, R.A., Emr, S.D., and Koshland, D. (1995). Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast. Mol. Biol. Cell 6, 525-539.
36. Yu, J.W., and Lemmon, M.A. (2001). All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate. J. Biol. Chem. 276, 44179-44184.