Hrr25 phosphorylates the autophagic receptor Atg34 to promote vacuolar transport of α-mannosidase under nitrogen starvation conditions

FEBS Letters

Volumn 588, Issue 21, 2014, Pages 3862-3869

  Mochida, Keisuke ^a   Ohsumi, Yoshinori ^a   Nakatogawa, Hitoshi ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Autophagosome; Casein kinase 1; Nitrogen starvation; Selective autophagy; Vacuolar enzyme; Yeast

Indexed keywords

ADAPTOR PROTEIN; ALPHA MANNOSIDASE; AMS1 PROTEIN; ATG11 PROTEIN; ATG34 PROTEIN; CASEIN KINASE I; HRR25 PROTEIN; NITROGEN; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; ATG11 PROTEIN, S CEREVISIAE; ATG34 PROTEIN, S CEREVISIAE; CELL RECEPTOR; HRR25 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; INTRACELLULAR TRANSPORT; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; UPREGULATION; VACUOLAR TRANSPORT; CELL VACUOLE; CYTOLOGY; DEFICIENCY; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

ALPHA-MANNOSIDASE; AUTOPHAGY; CASEIN KINASE I; NITROGEN; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84908227585     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.09.032     Document Type: Article

References (35)

1. H. Nakatogawa, K. Suzuki, Y. Kamada, and Y. Ohsumi Dynamics and diversity in autophagy mechanisms: lessons from yeast Nat. Rev. Mol. Cell Biol. 10 2009 458 467
2. Z. Yang, and D.J. Klionsky Eaten alive: a history of macroautophagy Nat. Cell Biol. 12 2010 814 822
3. N. Mizushima, T. Yoshimori, and Y. Ohsumi The role of Atg proteins in autophagosome formation Annu. Rev. Cell Dev. Biol. 27 2011 107 132
4. J. Kim, S.V. Scott, M.N. Oda, and D.J. Klionsky Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway J. Cell Biol. 137 1997 609 618
5. S.V. Scott, J. Guan, M.U. Hutchins, J. Kim, and D.J. Klionsky Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway Mol. Cell 7 2001 1131 1141
6. M.U. Hutchins, and D.J. Klionsky Vacuolar localization of oligomeric alpha-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae J. Biol. Chem. 276 2001 20491 20498
7. T. Shintani, W.P. Huang, P.E. Stromhaug, and D.J. Klionsky Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway Dev. Cell 3 2002 825 837
8. M. Yuga, K. Gomi, D.J. Klionsky, and T. Shintani Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae J. Biol. Chem. 286 2011 13704 13713
9. K. Suzuki, C. Kondo, M. Morimoto, and Y. Ohsumi Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p J. Biol. Chem. 285 2010 30019 30025
10. Y. Watanabe, N.N. Noda, H. Kumeta, K. Suzuki, Y. Ohsumi, and F. Inagaki Selective transport of alpha-mannosidase by autophagic pathways: structural basis for cargo recognition by Atg19 and Atg34 J. Biol. Chem. 285 2010 30026 30033
11. C. Janke A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes Yeast 21 2004 947 962
12. H. Nakatogawa, J. Ishii, E. Asai, and Y. Ohsumi Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis Autophagy 8 2012 177 186
13. K. Nishimura, T. Fukagawa, H. Takisawa, T. Kakimoto, and M. Kanemaki An auxin-based degron system for the rapid depletion of proteins in non plant cells Nat. Methods 6 2009 917 922
14. M.K. Sung, and W.K. Huh Bimolecular fluorescence complementation analysis system for in vivo detection of protein-protein interaction in Saccharomyces cerevisiae Yeast 24 2007 767 775
15. H. Nakatogawa, and Y. Ohsumi SDS-PAGE techniques to study ubiquitin-like conjugation systems in yeast autophagy Methods Mol. Biol. 832 2012 519 529
16. T. Yoshihisa, and Y. Anraku A novel pathway of import of alpha-mannosidase, a marker enzyme of vacuolar membrane, in Saccharomyces cerevisiae J. Biol. Chem. 265 1990 22418 22425
17. Tanaka, C., et al., Hrr25 triggers selective autophagy-related pathways by phosphorylating receptor proteins. J. Cell Biol. (in press).
18. H. Nakatogawa, Y. Ichimura, and Y. Ohsumi Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion Cell 130 2007 165 178
19. A. Breitkreutz A global protein kinase and phosphatase interaction network in yeast Science 328 2012 1043 1046
20. M.F. Hoekstra, R.M. Liskay, A.C. Ou, A.J. DeMaggio, D.G. Burbee, and F. Heffron HRR25, a putative protein kinase from budding yeast: association with repair of damaged DNA Science 253 1991 1031 1034
21. A.J. DeMaggio, R.A. Lindberg, T. Hunter, and M.F. Hoekstra The budding yeast HRR25 gene product is a casein kinase I isoform Proc. Natl. Acad. Sci. U.S.A. 89 1992 7008 7012
22. M. Petronczki Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1 Cell 126 2006 1049 1064
23. T. Schafer, B. Maco, E. Petfalski, D. Tollervey, B. Bottcher, U. Aebi, and E. Hurt Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit Nature 441 2006 651 655
24. C. Lord, D. Bhandari, S. Menon, M. Ghassemian, D. Nycz, J. Hay, P. Ghosh, and S. Ferro-Novick Sequential interactions with Sec23 control the direction of vesicle traffic Nature 473 2011 181 186
25. T. Noda, and Y. Ohsumi Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast J. Biol. Chem. 273 1998 3963 3966
26. A. Murakami, K. Kimura, and A. Nakano 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. 274 1999 3804 3810
27. T. Pfaffenwimmer Hrr25 kinase promotes selective autophagy by phosphorylating the cargo receptor Atg19 EMBO Rep. 15 2014 862 870
28. H. Hirayama, J. Seino, T. Kitajima, Y. Jigami, and T. Suzuki Free oligosaccharides to monitor glycoprotein endoplasmic reticulum-associated degradation in Saccharomyces cerevisiae J. Biol. Chem. 285 2010 12390 12404
29. M. Hamasaki, T. Noda, M. Baba, and Y. Ohsumi Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast Traffic 6 2005 56 65
30. A.M. Motley, J.M. Nuttall, and E.H. Hettema Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae EMBO J. 31 2012 2852 2868
31. J.C. Farre, A. Burkenroad, S.F. Burnett, and S. Subramani Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11 EMBO Rep. 14 2013 441 449
32. T. Kanki, K. Wang, Y. Cao, M. Baba, and D.J. Klionsky Atg32 is a mitochondrial protein that confers selectivity during mitophagy Dev. Cell 17 2009 98 109
33. K. Okamoto, N. Kondo-Okamoto, and Y. Ohsumi Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy Dev. Cell 17 2009 87 97
34. T. Kanki Casein kinase 2 is essential for mitophagy EMBO Rep. 14 2013 788 794
35. T. Darsow, S.E. Rieder, and S.D. Emr A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole J. Cell Biol. 138 1997 517 529