Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes

Journal of Cell Science

Volumn 119, Issue 18, 2006, Pages 3888-3900

  Young, Andrew R J ^a   Chan, Edmond Y W ^a   Hu, Xiao Wen ^a   Köchl, Robert ^a   Crawshaw, Samuel G ^b   High, Stephen ^b   Halley, Dale W ^c   Lippincott Schwartz, Jennifer ^c   Tooze, Sharon A ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Autophagy; Golgi; Intracellular transport; Rab proteins; Transmembrane protein

Indexed keywords

CELL MARKER; CELL PROTEIN; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN ATG1; PROTEIN ATG9; PROTEIN TGN46; RAB PROTEIN; RAB7 PROTEIN; RAB9 PROTEIN; RAPAMYCIN; SMALL INTERFERING RNA; SOMATOMEDIN RECEPTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOSOL; ENDOSOME; ENZYME ACTIVITY; GOLGI COMPLEX; HUMAN; HUMAN CELL; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN TRANSPORT; RAT; SEQUENCE HOMOLOGY; STARVATION; STEADY STATE; UPREGULATION; YEAST;

ANIMALS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RAB GTP-BINDING PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; TRANS-GOLGI NETWORK;

MAMMALIA;

EID: 33750366092     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03172     Document Type: Article

References (55)

1. Barbero, P., Bittova, L. and Pfeffer, S. R. (2002). Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell Biol. 156, 511-518.
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. Blommaart, E. F., Krause, U., Schellens, J. P., Vreeling-Sindelarova, H. and Meijer, A. J. (1997). The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243, 240-246.
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. Chang, T., Schroder, L. A., Thomson, J. M., Klocman, A. S., Tomasini A. J., Stromhaug, P. E. and Dunn, W. A., Jr (2005). PpATG9 encodes a novel membrane protein that traffics to vacuolar membranes, which sequester peroxisomes during pexophagy in pichia pastoris. Mol. Biol. Cell 16, 4941-4953.
6. Crawshaw, S. G., Martoglio, B., Meacock, S. L. and High, S. (2004). A misassembled transmembrane domain of a polytopic protein associates with signal peptide peptidase. Biochem. J. 384, 9-17.
7. Dittié, A. S., Klumperman, J. and Tooze, S. A. (1999). Differential distribution of mannose-6-phosphate receptors and furin in immature secretory granules. J. Cell Sci. 112 3955-3966.
8. Dunn, W. A., Jr (1990). Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110, 1923-1933.
9. Ellis, J., Jackman, M., Perez, J., Mullock, B. and Luzio, J. (1992). Membrane traffic pathways in polarised epithelial cells. In Protein Targeting: A Practical Approach (ed. A. I. Magee and T. Wileman), pp. 25-57. Washington: IRL Press.
10. Ericsson, J. L. E. (1969). Studies on induced cellular autophagy II. Characterization of the membranes bordering autophagosomes in parenchymal liver cells. Exp. Cell Res. 56, 393-405.
11. Gaffet, P., Jones, A. T. and Clague, M. J. (1997). Inhibition of calcium-independent mannose 6-phosphate receptor incorporation into trans-golgi network-derived clathrin-coated vesicles by wortmannin. J. Biol. Chem. 272, 24170-24175.
12. Goud, B., Zahraoui, A., Tavitian, A. and Saraste, J. (1990). Small GTP-binding protein associated with Golgi cisternae. Nature 345, 553-556.
13. Gronostajski, R. M. and Pardee, A. B. (1984). Protein degradation in 3T3 cells and tumorigenic transformed 3T3 cells. J. Cell Physiol. 119, 127-132.
14. Guan, J., Stromhaug, P. E., George, M. D., Habibzadegah-Tari, P., Bevan, A., Dunn, W. A., Jr 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.
15. Gutierrez, M. G,, Munafo, D. B., Beron, W. and Colombo, M. I. (2004). Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117, 2687-2697.
16. Hosokawa, N., Hara, Y. and Mizushima, N. (2006). Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett. 580, 2623-2629.
17. Jager, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P. and Eskelinen, E.-L. (2004). Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117, 4837-4848.
18. 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.
19. Kihara, A., Kabeya, Y., Ohsumi, Y. and Yoshimori, T. (2001a). Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2, 330-335.
20. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001b). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in saccharomyces cerevisiae. J. Cell Biol. 152, 519-530.
21. 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.
22. Klionsky, D. J. (2005). Autophagy. Curr. Biol. 15, R282-R283.
23. Klionsky, D. J, Cregg, J. M., Dunn, W. A., Emr, S. D., Sakai, Y., Sandoval, I. V., Sibirny, A., Subramani, S., Thumm, M., Veenhuis, M. et a]. (2003). A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545.
24. Köchl, R., Hu, X., Chan, E. and Tooze, S. A. (2006). Microtubules facilitate autophagosomal formation and fusion of autophagosomes with endosomes. Traffic 7, 129-145.
25. Lang, T., Reiche, S., Straub, M., Bredschneider, M. and Thumm, M. (2000). Autophagy and the cvt pathway both depend on AUT9. J. Bacteriol. 182, 2125-2133.
26. Locke, M. and Sykes, A. K. (1975). The role of the Golgi complex in the isolation and digestion of organelles. Tissue Cell 7, 143-158.
27. Lorenz, H., Hailey, D. W. and Lippincott-Schwartz, J. (2006). Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210.
28. Mizushima, N. (2004). Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 36, 2491-2502.
29. 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.
30. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T. and Warren, G. (1995). Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131, 1715-1726.
31. Noda T. and Ohsumi, Y. (1998). Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963-3966.
32. 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.
33. Novikoff, A. B. and Shin, W. Y. (1979). Endoplasmic reticulum and autophagy in rat hepatocyte. Proc. Natl. Acad. Sci. USA 75, 5039-5042.
34. Petiot, A., Ogier-Denis, E., Blommaart, E. F., Meijer, A. J. and Codogno, P. (2000). Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275, 992-998.
35. 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.
36. Reggiori, F., Shintani, T., Nair, U. and Klionsky, D. J. (2005). Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeast. Autophagy 1, 101-109.
37. Robb, G. B., Carson, A. R., Tai, S. C., Fish, J. E., Singh, S., Yamada, T., Scherer, S. W., Nakabayashi, K. and Marsden, P. A. (2004). Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J. Biol. Chem, 279, 37982-37996.
38. Robinson, M. S. and Bonifacino, J. S. (2001). Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444-453.
39. 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.
40. Row, P., Reaves, B., Domin, J., Luzio, J. and Davidson, H. W. (2001). Overexpression of a rat kinase-deficient phosphoinositide 3-kinase, Vps34p, inhibits cathepsin D maturation. Biochem. J. 353, 655-661.
41. Seaman, M. N. (2005). Recycle your receptors with retromer. Trends Cell Biol. 15, 68-75.
42. Seglen, P. O. (1976). Preparation of isolated rat liver cells. Methods Cell Biol. 13, 29-83.
43. Seglen, P. O., Gordon, P. B. and Holen, I. (1990). Non-selective autophagy. Semin. Cell Biol. 1, 441-448.
44. 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.
45. Slusarewicz, P., Hui, N. and Warren, G. (1994). Purification of rat liver Golgi stacks. In Cell Biology: A laboratory Handbook (ed. J. E. Celis), pp. 509-517. Orlando, FL: Academic Press.
46. Sonnichsen, B., De Renzis, S., Nielsen, E., Rietdorf J. and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
47. 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
48. Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. and Wolf, D. H. (1994). Isolation of autophagocytosis mutants of Saccharomyces ccrevisiae. FEBS Lett. 349, 275-280.
49. Tsukada, M. and Ohsumi, Y. (1993). Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174.
50. Turner, R. and Tartakoff, A. (1989). The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization. J. Cell Biol. 109, 2081-2088.
51. Ueda, T., Takeyama, Y., Ohmori, T., Ohyanagi, H., Saitoh, Y. and Takai, Y. (1991). Purification and characterization from rat liver cytosol of a GDP dissociation inhibitor (GDI) for liver 24K G, a ras p21-like GTP-binding protein, with properties similar to those of smg p25A GDI. Biochemistry 30, 909-917.
52. Yamada, T., Carson, A. R., Caniggia, I, Umebayashi, K., Yoshimori, T., Nakabayashi, K. and Scherer, S. W. (2005). Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J. Biol. Chem. 280, 18283-18290.
53. Yamamoto, A., Masaki, R. and Tashiro, Y. (1990). Characterization of the isolation membranes and the limiting membranes of autophagosomes in rat hepatocytes by lectin cytochemistry. J. Histochem. Cytochem. 38, 573-580.
54. Yan, J., Kuroyanagi, H., Kuroiwa, A., Matsuda, Y.-I., Tokumitsu, H., Tomoda, T., Shirasawa, T. and Muramatsu, M.-A. (1998). Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem. Biophys. Res. Commun. 246, 222-227.
55. Zeng, X., Overmeyer, J. H. and Maltese, W. A. (2006). Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J. Cell Sci. 119, 259-270.