Activation of Atg1 kinase in autophagy by regulated phosphorylation

Autophagy

Volumn 6, Issue 8, 2010, Pages 1168-1178

  Kijanska, Monika ^a   Dohnal, Ilse ^b   Reiter, Wolfgang ^b   Kaspar, Susanne ^a,c   Stoffel, Ingrid ^a   Ammerer, Gustav ^b   Kraft, Claudine ^a   Peter, Matthias ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Cellular metabolism; Signal transduction

Indexed keywords

ATG1 ENZYME; ATG13 ENZYME; PROTEIN SERINE THREONINE KINASE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; MASS SPECTROMETRY; NONHUMAN; PHAGOSOME; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION;

EID: 78649299852     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.6.8.13849     Document Type: Article

References (40)

1. Harding TM, Morano KA, Scott SV, Klionsky DJ. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 1995; 131:591-602.
2. Hutchins MU, Klionsky DJ. Vacuolar localization of oligomeric alpha-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J Biol Chem 2001; 276:20491-8.
3. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-9.
4. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91.
5. Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963-6.
6. Scott SV, Nice DC, 3rd, Nau JJ, Weisman LS, Kamada Y, Keizer-Gunnink I, et al. Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J Biol Chem 2000; 275:25840-9.
7. Hosokawa N, Sasaki T, Iemura S, Natsume T, Hara T, Mizushima N. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 2009; 5:973-9.
8. Yeh YY, Wrasman K, Herman PK. Autophosphorylation Within the Atg1 Activation Loop is Required for Both Kinase Activity and the Induction of Autophagy in Saccharomyces cerevisiae. Genetics 2010.
9. Nolen B, Taylor S, Ghosh G. Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 2004; 15:661-75.
10. Goldberg J, Nairn AC, Kuriyan J. Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I. Cell 1996; 84:875-87.
11. Johnson LN, Noble ME, Owen DJ. Active and inactive protein kinases: structural basis for regulation. Cell 1996; 85:149-58.
12. Sicheri F, Moarefi I, Kuriyan J. Crystal structure of the Src family tyrosine kinase Hck. Nature 1997; 385:602-9.
13. Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell 1995; 80:187-97.
14. Ahn JY, Li X, Davis HL, Canman CE. Phosphorylation of threonine 68 promotes oligomerization and autophosphorylation of the Chk2 protein kinase via the forkhead-associated domain. J Biol Chem 2002; 277:19389-95.
15. Xu YJ, Davenport M, Kelly TJ. Two-stage mechanism for activation of the DNA replication checkpoint kinase Cds1 in fission yeast. Genes Dev 2006; 20:990-1003.
16. Tagwerker C, Flick K, Cui M, Guerrero C, Dou Y, Auer B, et al. A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivocross-linking. Mol Cell Proteomics 2006; 5:737-48.
17. Wolf-Yadlin A, Hautaniemi S, Lauffenburger DA, White FM. Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks. Proc Natl Acad Sci USA 2007; 104:5860-5.
18. Cheong H, Yorimitsu T, Reggiori F, Legakis JE, Wang CW, Klionsky DJ. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell 2005; 16:3438-53.
19. Klionsky DJ, Cueva R, Yaver DS. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 1992; 119:287-99.
20. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150:1507-13.
21. Matsuura A, Tsukada M, Wada Y, Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997; 192:245-50.
22. Cheong H, Nair U, Geng J, Klionsky DJ. 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 2008; 19:668-81.
23. Mellado M, Rodriguez-Frade JM, Manes S, Martinez AC. Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu Rev Immunol 2001; 19:397-421.
24. Weiss A, Schlessinger J. Switching signals on or off by receptor dimerization. Cell 1998; 94:277-80.
25. Rosenberg OS, Deindl S, Sung RJ, Nairn AC, Kuriyan J. Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 2005; 123:849-60.
26. Budovskaya YV, Stephan JS, Reggiori F, Klionsky DJ, Herman PK. The Ras/cAMP-dependent protein kinase signaling pathway regulates an early step of the autophagy process in Saccharomyces cerevisiae. J Biol Chem 2004; 279:20663-71.
27. Stephan JS, Yeh YY, Ramachandran V, Deminoff SJ, Herman PK. The Tor and cAMP-dependent protein kinase signaling pathways coordinately control autophagy in Saccharomyces cerevisiae. Autophagy 2010; 6.
28. Kamada Y, Yoshino K, Kondo C, Kawamata T, Oshiro N, Yonezawa K, et al. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 2009; 30:1049-58.
29. Yorimitsu T, He C, Wang K, Klionsky DJ. Tap42-associated protein phosphatase type 2A negatively regulates induction of autophagy. Autophagy 2009; 5:616-24.
30. De Wever V, Reiter W, Ballarini A, Ammerer G, Brocard C. A dual role for PP1 in shaping the Msn2-dependent transcriptional response to glucose starvation. EMBO J 2005; 24:4115-23.
31. De Virgilio C, Loewith R. Cell growth control: little eukaryotes make big contributions. Oncogene 2006; 25:6392-415.
32. Arsham AM, Neufeld TP. Thinking globally and acting locally with TOR. Curr Opin Cell Biol 2006; 18:589-97.
33. Budovskaya YV, Stephan JS, Deminoff SJ, Herman PK. An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA 2005; 102:13933-8.
34. Murakami A, Kimura K, Nakano A. The inactive form of a yeast casein kinase I suppresses the secretory defect of the sec12 mutant. Implication of negative regulation by the Hrr25 kinase in the vesicle budding from the endoplasmic reticulum. J Biol Chem 1999; 274:3804-10.
35. Watson HA, Cope MJ, Groen AC, Drubin DG, Wendland B. In vivo role for actin-regulating kinases in endocytosis and yeast epsin phosphorylation. Mol Biol Cell 2001; 12:3668-79.
36. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science 2010; 327:425-31.
37. Abeliovich H, Zhang C, Dunn WA Jr, Shokat KM, Klionsky DJ. Chemical genetic analysis of Apg1 reveals a non-kinase role in the induction of autophagy. Mol Biol Cell 2003; 14:477-90.
38. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 2002; 418:387-91.
39. Tagwerker C, Zhang H, Wang X, Larsen LS, Lathrop RH, Hatfield GW, et al. HB tag modules for PCR-based gene tagging and tandem affinity purification in Saccharomyces cerevisiae. Yeast 2006; 23:623-32.
40. Mazanek M, Roitinger E, Hudecz O, Hutchins JR, Hegemann B, Mitulovic G, et al. A new acid mix enhances phosphopeptide enrichment on titanium- and zirconium dioxide for mapping of phosphorylation sites on protein complexes. J Chromatogr B Analyt Technol Biomed Life Sci 2010; 878:515-24.