Early Steps in Autophagy Depend on Direct Phosphorylation of Atg9 by the Atg1 Kinase

Molecular Cell

Volumn 53, Issue 3, 2014, Pages 471-483

  Papinski, Daniel ^a   Schuschnig, Martina ^a   Reiter, Wolfgang ^a   Wilhelm, Larissa ^a   Barnes, Christopher A ^b   Maiolica, Alessio ^b   Hansmann, Isabella ^a   Pfaffenwimmer, Thaddaeus ^a   Kijanska, Monika ^b   Stoffel, Ingrid ^b   Lee, SungSik ^b   Brezovich, Andrea ^a   Lou, JaneHua ^c   Turk, Benjamin E ^c   Aebersold, Ruedi ^b   Ammerer, Gustav ^a   Peter, Matthias ^b   Kraft, Claudine ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b ETH ZURICH   (Switzerland)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATG1 KINASE; ATG9 PROTEIN; PHOSPHOTRANSFERASE; PROTEIN; UNCLASSIFIED DRUG; ATG8 KINASE; ATG9 KINASE; PROTEIN KINASE;

ARTICLE; AUTOPHAGOSOME; CELL MEMBRANE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; IN VITRO STUDY; IN VIVO STUDY; MACROAUTOPHAGY; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL CELL; AUTOPHAGY; MEMBRANE VESICLE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; AMINOPEPTIDASES; ARABIDOPSIS PROTEINS; AUTOPHAGY; BINDING SITES; CONSENSUS SEQUENCE; INTRACELLULAR MEMBRANES; MASS SPECTROMETRY; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHAGOSOMES; PHOSPHORYLATION; PROTEIN KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84893742616     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.12.011     Document Type: Article

References (41)

1. Baskaran S., Ragusa M.J., Boura E., Hurley J.H. Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol. Cell 2012, 47:339-348.
2. Chen G.-C., Lee J.Y., Tang H.-W., Debnath J., Thomas S.M., Settleman J. Genetic interactions between Drosophila melanogaster Atg1 and paxillin reveal a role for paxillin in autophagosome formation. Autophagy 2008, 4:37-45.
3. Crooks G.E., Hon G., Chandonia J.-M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
4. Di Bartolomeo S., Corazzari M., Nazio F., Oliverio S., Lisi G., Antonioli M., Pagliarini V., Matteoni S., Fuoco C., Giunta L., et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J.Cell Biol. 2010, 191:155-168.
5. Hara T., Takamura A., Kishi C., Iemura S.-I., Natsume T., Guan J.-L., Mizushima N. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J.Cell Biol. 2008, 181:497-510.
6. Harding T.M., Morano K.A., Scott S.V., Klionsky D.J. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J.Cell Biol. 1995, 131:591-602.
7. Hutchins M.U., Klionsky D.J. Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J.Biol. Chem. 2001, 276:20491-20498.
8. Inoue Y., Klionsky D.J. Regulation of macroautophagy in Saccharomyces cerevisiae. Semin. Cell Dev. Biol. 2010, 21:664-670.
9. Kijanska M., Dohnal I., Reiter W., Kaspar S., Stoffel I., Ammerer G., Kraft C., Peter M. Activation of Atg1 kinase in autophagy by regulated phosphorylation. Autophagy 2010, 6:1168-1178.
10. Kim J., Huang W.P., Klionsky D.J. Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J.Cell Biol. 2001, 152:51-64.
11. Klionsky D.J., Cueva R., Yaver D.S. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J.Cell Biol. 1992, 119:287-299.
12. Kraft C., Reggiori F., Peter M. Selective types of autophagy in yeast. Biochim. Biophys. Acta 2009, 1793:1404-1412.
13. Kraft C., Kijanska M., Kalie E., Siergiejuk E., Lee S.S., Semplicio G., Stoffel I., Brezovich A., Verma M., Hansmann I., et al. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J. 2012, 31:3691-3703.
14. Krick R., Busse R.A., Scacioc A., Stephan M., Janshoff A., Thumm M., Kühnel K. Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a β-propeller protein family. Proc. Natl. Acad. Sci. USA 2012, 109:E2042-E2049.
15. Lang T., Reiche S., Straub M., Bredschneider M., Thumm M. Autophagy and the cvt pathway both depend on AUT9. J.Bacteriol. 2000, 182:2125-2133.
16. Lizcano J.M., Deak M., Morrice N., Kieloch A., Hastie C.J., Dong L., Schutkowski M., Reimer U., Alessi D.R. Molecular basis for the substrate specificity of NIMA-related kinase-6 (NEK6). Evidence that NEK6 does not phosphorylate the hydrophobic motif of ribosomal S6 protein kinase and serum- and glucocorticoid-induced protein kinase invivo. J.Biol. Chem. 2002, 277:27839-27849.
17. Mari M., Griffith J., Rieter E., Krishnappa L., Klionsky D.J., Reggiori F. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J.Cell Biol. 2010, 190:1005-1022.
18. Matsuura A., Tsukada M., Wada Y., Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997, 192:245-250.
19. Meiling-Wesse K., Barth H., Thumm M. Ccz1p/Aut11p/Cvt16p is essential for autophagy and the cvt pathway. FEBS Lett. 2002, 526:71-76.
20. Meléndez A., Tallóczy Z., Seaman M., Eskelinen E.-L., Hall D.H., Levine B. Autophagy genes are essential for dauer development and life-span extension in C.elegans. Science 2003, 301:1387-1391.
21. Mok J., Kim P.M., Lam H.Y.K., Piccirillo S., Zhou X., Jeschke G.R., Sheridan D.L., Parker S.A., Desai V., Jwa M., et al. Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci. Signal. 2010, 3:ra12.
22. Motley A.M., Nuttall J.M., Hettema E.H. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 2012, 31:2852-2868.
23. Noda T., Matsuura A., Wada Y., Ohsumi Y. Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 1995, 210:126-132.
24. Noda T., Kim J., Huang W.P., Baba M., Tokunaga C., Ohsumi Y., Klionsky D.J. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J.Cell Biol. 2000, 148:465-480.
25. Obenauer J.C., Cantley L.C., Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 2003, 31:3635-3641.
26. Orsi A., Razi M., Dooley H.C., Robinson D., Weston A.E., Collinson L.M., Tooze S.A. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 2012, 23:1860-1873.
27. Pinna L.A., Ruzzene M. How do protein kinases recognize their substrates?. Biochim. Biophys. Acta 1996, 1314:191-225.
28. Reggiori F., Tucker K.A., Strømhaug P.E., Klionsky D.J. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 2004, 6:79-90.
29. Reiter W., Anrather D., Dohnal I., Pichler P., Veis J., Grøtli M., Posas F., Ammerer G. Validation of regulated protein phosphorylation events in yeast by quantitative mass spectrometry analysis of purified proteins. Proteomics 2012, 12:3030-3043.
30. Rieter E., Vinke F., Bakula D., Cebollero E., Ungermann C., Proikas-Cezanne T., Reggiori F. Atg18 function in autophagy is regulated by specific sites within its β-propeller. J.Cell Sci. 2013, 126:593-604.
31. Russell R.C., Tian Y., Yuan H., Park H.W., Chang Y.-Y., Kim J., Kim H., Neufeld T.P., Dillin A., Guan K.-L. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell Biol. 2013, 15:741-750.
32. Scott R.C., Juhász G., Neufeld T.P. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 2007, 17:1-11.
33. Suzuki K., Ohsumi Y. Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett. 2007, 581:2156-2161.
34. Suzuki K., Kirisako T., Kamada Y., Mizushima N., Noda T., Ohsumi Y. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 2001, 20:5971-5981.
35. Suzuki K., Kubota Y., Sekito T., Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 2007, 12:209-218.
36. Suzuki K., Akioka M., Kondo-Kakuta C., Yamamoto H., Ohsumi Y. Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J.Cell Sci. 2013, 126:2534-2544.
37. Tang H.-W., Wang Y.-B., Wang S.-L., Wu M.-H., Lin S.-Y., Chen G.-C. Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy. EMBO J. 2011, 30:636-651.
38. Tomoda T., Bhatt R.S., Kuroyanagi H., Shirasawa T., Hatten M.E. A mouse serine/threonine kinase homologous to C.elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 1999, 24:833-846.
39. Yamamoto H., Kakuta S., Watanabe T.M., Kitamura A., Sekito T., Kondo-Kakuta C., Ichikawa R., Kinjo M., Ohsumi Y. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J.Cell Biol. 2012, 198:219-233.
40. Yuga M., Gomi K., Klionsky D.J., Shintani T. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J.Biol. Chem. 2011, 286:13704-13713.
41. Zuzuarregui A., Kupka T., Bhatt B., Dohnal I., Mudrak I., Friedmann C., Schüchner S., Frohner I.E., Ammerer G., Ogris E. M-Track: detecting short-lived protein-protein interactions invivo. Nat. Methods 2012, 9:594-596.