Direct Induction of Autophagy by Atg1 Inhibits Cell Growth and Induces Apoptotic Cell Death

Current Biology

Volumn 17, Issue 1, 2007, Pages 1-11

  Scott, Ryan C ^a   Juhász, Gábor ^a   Neufeld, Thomas P ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

ATG1 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN PROTEIN, DROSOPHILA; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; AUTOPHAGY; CELL ENLARGEMENT; DROSOPHILA; FEEDBACK SYSTEM; GENE EXPRESSION; PHENOTYPE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AUTOPHAGY; CELL ENLARGEMENT; DROSOPHILA; DROSOPHILA PROTEINS; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION; PHENOTYPE; PHOSPHOTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 33845874899     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2006.10.053     Document Type: Article

References (44)

1. Levine B., and Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 (2004) 463-477
2. Tsukada M., and Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333 (1993) 169-174
3. Thumm M., Egner R., Koch B., Schlumpberger M., Straub M., Veenhuis M., and Wolf D.H. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349 (1994) 275-280
4. Klionsky D.J., Cregg J.M., Dunn Jr. W.A., Emr S.D., Sakai Y., Sandoval I.V., Sibirny A., Subramani S., Thumm M., Veenhuis M., et al. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5 (2003) 539-545
5. Scott R.C., Schuldiner O., and Neufeld T.P. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7 (2004) 167-178
6. Shintani T., and Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 306 (2004) 990-995
7. Arico S., Petiot A., Bauvy C., Dubbelhuis P.F., Meijer A.J., Codogno P., and Ogier-Denis E. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276 (2001) 35243-35246
8. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., and Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402 (1999) 672-676
9. Petiot A., Ogier-Denis E., Blommaart E.F., Meijer A.J., and Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275 (2000) 992-998
10. Noda T., and Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273 (1998) 3963-3966
11. Neufeld T.P. Role of autophagy in developmental cell growth and death: insights from Drosophila. In: Klionsky D.J. (Ed). Autophagy (2004), Landes Bioscience, Georgetown 224-232
12. Wullschleger S., Loewith R., and Hall M.N. TOR signaling in growth and metabolism. Cell 124 (2006) 471-484
13. Clarke P.G. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181 (1990) 195-213
14. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., and Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6 (2004) 1221-1228
15. Veneault-Fourrey C., Barooah M., Egan M., Wakley G., and Talbot N.J. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312 (2006) 580-583
16. Yu L., Wan F., Dutta S., Welsh S., Liu Z., Freundt E., Baehrecke E.H., and Lenardo M. Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA 103 (2006) 4952-4957
17. Lum J.J., Bauer D.E., Kong M., Harris M.H., Li C., Lindsten T., and Thompson C.B. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120 (2005) 237-248
18. Kamada Y., Funakoshi T., Shintani T., Nagano K., Ohsumi M., and Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150 (2000) 1507-1513
19. Wang Z., Wilson W.A., Fujino M.A., and Roach P.J. Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol. Cell. Biol. 21 (2001) 5742-5752
20. Budovskaya Y.V., Stephan J.S., Deminoff S.J., and Herman P.K. An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 102 (2005) 13933-13938
21. Ptacek J., Devgan G., Michaud G., Zhu H., Zhu X., Fasolo J., Guo H., Jona G., Breitkreutz A., Sopko R., et al. Global analysis of protein phosphorylation in yeast. Nature 438 (2005) 679-684
22. Reggiori F., Tucker K.A., Stromhaug P.E., and Klionsky D.J. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 6 (2004) 79-90
23. Abeliovich H., Zhang C., Dunn Jr. W.A., Shokat K.M., and Klionsky D.J. Chemical genetic analysis of Apg1 reveals a non-kinase role in the induction of autophagy. Mol. Biol. Cell 14 (2003) 477-490
24. Kabeya Y., Kamada Y., Baba M., Takikawa H., Sasaki M., and Ohsumi Y. Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol. Biol. Cell 16 (2005) 2544-2553
25. Rusten T.E., Lindmo K., Juhász G., Sass M., Seglen P.O., Brech A., and Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 7 (2004) 179-192
26. Young A.R., Chan E.Y., Hu X.W., Kochl R., Crawshaw S.G., High S., Hailey D.W., Lippincott-Schwartz J., and Tooze S.A. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119 (2006) 3888-3900
27. Kirisako T., Baba M., Ishihara N., Miyazawa K., Ohsumi M., Yoshimori T., Noda T., and Ohsumi Y. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147 (1999) 435-446
28. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., and Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19 (2000) 5720-5728
29. Zinke I., Schutz C.S., Katzenberger J.D., Bauer M., and Pankratz M.J. Nutrient control of gene expression in Drosophila: microarray analysis of starvation and sugar-dependent response. EMBO J. 21 (2002) 6162-6173
30. Juhász G., Csikós G., Sinka R., Erdélyi M., and Sass M. The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Lett. 543 (2003) 154-158
31. Hennig K.M., Colombani J., and Neufeld T.P. TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J. Cell Biol. 173 (2006) 963-974
32. Hosokawa N., Hara Y., and Mizushima N. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett. 580 (2006) 2623-2629
33. Debnath J., Mills K.R., Collins N.L., Reginato M.J., Muthuswamy S.K., and Brugge J.S. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111 (2002) 29-40
34. Martin D.N., and Baehrecke E.H. Caspases function in autophagic programmed cell death in Drosophila. Development 131 (2004) 275-284
35. Puig O., Marr M.T., Ruhf M.L., and Tjian R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17 (2003) 2006-2020
36. Kunz J., Schneider U., Howald I., Schmidt A., and Hall M.N. HEAT repeats mediate plasma membrane localization of Tor2p in yeast. J. Biol. Chem. 275 (2000) 37011-37020
37. Jin S. Autophagy, mitochondrial quality control, and oncogenesis. Autophagy 2 (2006) 80-84
38. Hara T., Nakamura K., Matsui M., Yamamoto A., Nakahara Y., Suzuki-Migishima R., Yokoyama M., Mishima K., Saito I., Okano H., et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006) 885-889
39. Komatsu M., Waguri S., Chiba T., Murata S., Iwata J., Tanida I., Ueno T., Koike M., Uchiyama Y., Kominami E., et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006) 880-884
40. Yu L., Alva A., Su H., Dutt P., Freundt E., Welsh S., Baehrecke E.H., and Lenardo M.J. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304 (2004) 1500-1502
41. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., and Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122 (2005) 927-939
42. Arbeitman M.N., Furlong E.E., Imam F., Johnson E., Null B.H., Baker B.S., Krasnow M.A., Scott M.P., Davis R.W., and White K.P. Gene expression during the life cycle of Drosophila melanogaster. Science 297 (2002) 2270-2275
43. Britton J.S., Lockwood W.K., Li L., Cohen S.M., and Edgar B.A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2 (2002) 239-249
44. Xu T., and Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117 (1993) 1223-1237