Phosphorylation of Atg9 regulates movement to the phagophore assembly site and the rate of autophagosome formation

Autophagy

Volumn 12, Issue 4, 2016, Pages 648-658

  Feng, Yuchen ^a   Backues, Steven K ^a,d   Baba, Misuzu ^b   Heo, Jin Mi ^c   Harper, J Wade ^c   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b KOGAKUIN UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

^d EASTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

autophagy; lysosome; stress; vacuole; yeast

Indexed keywords

AUTOPHAGY PROTEIN 1 KINASE; AUTOPHAGY PROTEIN 23; AUTOPHAGY PROTEIN 27; AUTOPHAGY PROTEIN 9; MEMBRANE PROTEIN; MUTANT PROTEIN; PHOSPHOPROTEIN; PROTEIN KINASE; SERINE; UNCLASSIFIED DRUG; ATG9 PROTEIN, S CEREVISIAE; AUTOPHAGY RELATED PROTEIN; PHOSPHOSERINE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTRON MICROSCOPY; MACROAUTOPHAGY; MOLECULAR DYNAMICS; NONHUMAN; PHAGOPHORE; PROCEDURES; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; STABLE ISOTOPE BY AMINO ACID IN CELL CULTURE; YEAST; AMINO ACID SEQUENCE; CHEMISTRY; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; AUTOPHAGOSOMES; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; MEMBRANE PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84964470500     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1157237     Document Type: Article

References (60)

1. D.J.Klionsky, E.H.Baehrecke, J.H.Brumell, C.T.Chu, P.Codogno, A.M.Cuervo, J.Debnath, V.Deretic, Z.Elazar, E.-L.Eskelinen, et al. A comprehensive glossary of autophagy-related molecules and processes (2nd edition). Autophagy 2011; 7:1273-94; PMID:21997368; http://dx.doi.org/10.4161/auto.7.11.17661
2. Y.Feng, D.He, Z.Yao, D.J.Klionsky. The machinery of macroautophagy. Cell Res 2014; 24:24-41; PMID:24366339; http://dx.doi.org/10.1038/cr.2013.168
3. M.Deffieu, I.Bhatia-Kissova, B.Salin, A.Galinier, S.Manon, N.Camougrand. Glutathione participates in the regulation of mitophagy in yeast. J Biol Chem 2009; 284:14828-37; PMID:19366696; http://dx.doi.org/10.1074/jbc.M109.005181
4. W.A.Dunn, Jr., J.M.Cregg, J.A.K.W.Kiel, I.J.van der Klei, M.Oku, Y.Sakai, A.A.Sibirny, O.V.Stasyk, M.Veenhuis. Pexophagy: the selective autophagy of peroxisomes. Autophagy 2005; 1:75-83; PMID:16874024; http://dx.doi.org/10.4161/auto.1.2.1737
5. D.J.Klionsky, J.M.Cregg, W.A.Dunn, Jr., S.D.Emr, Y.Sakai, I.V.Sandoval, A.Sibirny, S.Subramani, M.Thumm, M.Veenhuis, et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003; 5:539-45; PMID:14536056; http://dx.doi.org/10.1016/S1534-5807(03)00296-X
6. F.Reggiori, D.J.Klionsky. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 2013; 194:341-61; PMID:23733851; http://dx.doi.org/10.1534/genetics.112.149013
7. P.Boya, F.Reggiori, P.Codogno. Emerging regulation and functions of autophagy. Nat Cell Biol 2013; 15:713-20; PMID:23817233; http://dx.doi.org/10.1038/ncb2788
8. Y.Feng, Z.Yao, D.J.Klionsky. How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy. Trends Cell Biol 2015; 25:354-63; PMID:25759175; http://dx.doi.org/10.1016/j.tcb.2015.02.002
9. Y.Xie, R.Kang, X.Sun, M.Zhong, J.Huang, D.J.Klionsky, D.Tang. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 2015; 11:28-45; PMID:25484070; http://dx.doi.org/10.4161/15548627.2014.984267
10. K.Mao, L.H.Chew, Y.Inoue-Aono, H.Cheong, U.Nair, H.Popelka, C.K.Yip, D.J.Klionsky. Atg29 phosphorylation regulates coordination of the Atg17-Atg31-Atg29 complex with the Atg11 scaffold during autophagy initiation. Proc Natl Acad Sci U S A 2013; 110:E2875-84; PMID:23858448; http://dx.doi.org/10.1073/pnas.1300064110
11. Y.Kamada, K.Yoshino, C.Kondo, T.Kawamata, N.Oshiro, K.Yonezawa, Y.Ohsumi. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol Cell Biol 2010; 30:1049-58; PMID:19995911; http://dx.doi.org/10.1128/MCB.01344-09
12. J.S.Stephan, Y.Y.Yeh, V.Ramachandran, S.J.Deminoff, P.K.Herman. The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci U S A 2009; 106:17049-54; PMID:19805182; http://dx.doi.org/10.1073/pnas.0903316106
13. D.S.Wilkinson, J.S.Jariwala, E.Anderson, K.Mitra, J.Meisenhelder, J.T.Chang, T.Ideker, T.Hunter, V.Nizet, A.Dillin, et al. Phosphorylation of LC3 by the Hippo kinases STK3/STK4 is essential for autophagy. Mol Cell 2015; 57:55-68; PMID:25544559; http://dx.doi.org/10.1016/j.molcel.2014.11.019
14. D.Papinski, M.Schuschnig, W.Reiter, L.Wilhelm, C.A.Barnes, A.Maiolica, I.Hansmann, T.Pfaffenwimmer, M.Kijanska, I.Stoffel, et al. Early steps in autophagy depend on direct phosphorylation of Atg9 by the Atg1 kinase. Mol Cell 2014; 53:471-83; PMID:24440502; http://dx.doi.org/10.1016/j.molcel.2013.12.011
15. T.Noda, J.Kim, W.-P.Huang, M.Baba, C.Tokunaga, Y.Ohsumi, D.J.Klionsky. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148:465-80; PMID:10662773; http://dx.doi.org/10.1083/jcb.148.3.465
16. F.Reggiori, K.A.Tucker, P.E.Stromhaug, D.J.Klionsky. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 2004; 6:79-90; PMID:14723849; http://dx.doi.org/10.1016/S1534-5807(03)00402-7
17. M.Mari, J.Griffith, E.Rieter, L.Krishnappa, D.J.Klionsky, F.Reggiori. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J Cell Biol 2010; 190:1005-22; PMID:20855505; http://dx.doi.org/10.1083/jcb.200912089
18. H.Yamamoto, S.Kakuta, T.M.Watanabe, A.Kitamura, T.Sekito, C.Kondo-Kakuta, R.Ichikawa, M.Kinjo, Y.Ohsumi. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012; 198:219-33; PMID:22826123; http://dx.doi.org/10.1083/jcb.201202061
19. F.Reggiori, T.Shintani, U.Nair, D.J.Klionsky. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 2005; 1:101-9; PMID:16874040; http://dx.doi.org/10.4161/auto.1.2.1840
20. W.-L.Yen, J.E.Legakis, U.Nair, D.J.Klionsky. Atg27 is required for autophagy-dependent cycling of Atg9. Mol Biol Cell 2007; 18:581-93; PMID:17135291; http://dx.doi.org/10.1091/mbc.E06-07-0612
21. S.K.Backues, D.Chen, J.Ruan, Z.Xie, D.J.Klionsky. Estimating the size and number of autophagic bodies by electron microscopy. Autophagy 2014; 10:155-64; PMID:24270884; http://dx.doi.org/10.4161/auto.26856
22. A.R.J.Young, E.Y.W.Chan, X.W.Hu, R.Köchl, S.G.Crawshaw, S.High, D.W.Hailey, J.Lippincott-Schwartz, S.A.Tooze. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888-900; PMID:16940348; http://dx.doi.org/10.1242/jcs.03172
23. C.He, M.Baba, Y.Cao, D.J.Klionsky. Self-interaction is critical for Atg9 transport and function at the phagophore assembly site during autophagy. Mol Biol Cell 2008; 19:5506-16; PMID:18829864; http://dx.doi.org/10.1091/mbc.E08-05-0544
24. Y.Kamada, T.Funakoshi, T.Shintani, K.Nagano, M.Ohsumi, Y.Ohsumi. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150:1507-13; PMID:10995454; http://dx.doi.org/10.1083/jcb.150.6.1507
25. T.Noda, Y.Ohsumi. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963-6; PMID:9461583; http://dx.doi.org/10.1074/jbc.273.7.3963
26. T.Pfaffenwimmer, W.Reiter, T.Brach, V.Nogellova, D.Papinski, M.Schuschnig, C.Abert, G.Ammerer, S.Martens, C.Kraft. Hrr25 kinase promotes selective autophagy by phosphorylating the cargo receptor Atg19. EMBO Rep 2014; 15:862-70; PMID:24968893; http://dx.doi.org/10.15252/embr.201438932
27. C.Tanaka, L.J.Tan, K.Mochida, H.Kirisako, M.Koizumi, E.Asai, M.Sakoh-Nakatogawa, Y.Ohsumi, H.Nakatogawa. Hrr25 triggers selective autophagy-related pathways by phosphorylating receptor proteins. J Cell Biol 2014; 207:91-105; PMID:25287303; http://dx.doi.org/10.1083/jcb.201402128
28. Z.Yang, J.Geng, W.L.Yen, K.Wang, D.J.Klionsky. Positive or negative roles of different cyclin-dependent kinase Pho85-cyclin complexes orchestrate induction of autophagy in Saccharomyces cerevisiae. Mol Cell 2010; 38:250-64; PMID:20417603; http://dx.doi.org/10.1016/j.molcel.2010.02.033
29. M.Jin, D.He, S.K.Backues, M.A.Freeberg, X.Liu, J.K.Kim, D.J.Klionsky. Transcriptional regulation by Pho23 modulates the frequency of autophagosome formation. Curr Biol 2014; 24:1314-22; PMID:24881874; http://dx.doi.org/10.1016/j.cub.2014.04.048
30. H.Liu, J.H.Naismith. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol 2008; 8:91; PMID:19055817; http://dx.doi.org/10.1186/1472-6750-8-91
31. D.J.Klionsky. Monitoring autophagy in yeast: the Pho8Δ60 assay. Methods Mol Biol 2007; 390:363-71; PMID:17951700; http://dx.doi.org/10.1007/978-1-59745-466-7_24
32. H.Hanaoka, T.Noda, Y.Shirano, T.Kato, H.Hayashi, D.Shibata, S.Tabata, Y.Ohsumi. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 2002; 129:1181-93; PMID:12114572; http://dx.doi.org/10.1104/pp.011024
33. T.Yamada, A.R.Carson, I.Caniggia, K.Umebayashi, T.Yoshimori, K.Nakabayashi, S.W.Scherer. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem 2005; 280:18283-90; PMID:15755735; http://dx.doi.org/10.1074/jbc.M413957200
34. S.V.Scott, A.Hefner-Gravink, K.A.Morano, T.Noda, Y.Ohsumi, D.J.Klionsky. Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc Natl Acad Sci U S A 1996; 93:12304-8; PMID:8901576; http://dx.doi.org/10.1073/pnas.93.22.12304
35. D.J.Klionsky, R.Cueva, D.S.Yaver. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 1992; 119:287-99; PMID:1400574; http://dx.doi.org/10.1083/jcb.119.2.287
36. T.Yorimitsu, D.J.Klionsky. Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol Biol Cell 2005; 16:1593-605; PMID:15659643; http://dx.doi.org/10.1091/mbc.E04-11-1035
37. F.Reggiori, C.-W.Wang, U.Nair, T.Shintani, H.Abeliovich, D.J.Klionsky. Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol Biol Cell 2004; 15:2189-204; PMID:15004240; http://dx.doi.org/10.1091/mbc.E03-07-0479
38. K.Suzuki, Y.Kamada, Y.Ohsumi. Studies of cargo delivery to the vacuole mediated by autophagosomes in Saccharomyces cerevisiae. Dev Cell 2002; 3:815-24; PMID:12479807; http://dx.doi.org/10.1016/S1534-5807(02)00359-3
39. S.V.Scott, J.Guan, M.U.Hutchins, J.Kim, D.J.Klionsky. Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway. Mol Cell 2001; 7:1131-41; PMID:11430817; http://dx.doi.org/10.1016/S1097-2765(01)00263-5
40. R.Leber, E.Silles, I.V.Sandoval, M.J.Mazon. Yol082p, a novel CVT protein involved in the selective targeting of aminopeptidase I to the yeast vacuole. J Biol Chem 2001; 276:29210-7; PMID:11382752; http://dx.doi.org/10.1074/jbc.M101438200
41. S.V.Scott, D.C.Nice, III, J.J.Nau, L.S.Weisman, Y.Kamada, I.Keizer-Gunnink, T.Funakoshi, M.Veenhuis, Y.Ohsumi, D.J.Klionsky. 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; PMID:10837477; http://dx.doi.org/10.1074/jbc.M002813200
42. J.E.Legakis, W.L.Yen, D.J.Klionsky. A cycling protein complex required for selective autophagy. Autophagy 2007; 3:422-32; PMID:17426440; http://dx.doi.org/10.4161/auto.4129
43. Y.Cao, U.Nair, K.Yasumura-Yorimitsu, D.J.Klionsky. A multiple ATG gene knockout strain for yeast two-hybrid analysis. Autophagy 2009; 5:699-705; PMID:19337029; http://dx.doi.org/10.4161/auto.5.5.8382
44. Y.Cao, H.Cheong, H.Song, D.J.Klionsky. In vivo reconstitution of autophagy in Saccharomyces cerevisiae. J Cell Biol 2008; 182:703-13; PMID:18725539; http://dx.doi.org/10.1083/jcb.200801035
45. S.K.Backues, D.P.Orban, A.Bernard, K.Singh, Y.Cao, D.J.Klionsky. Atg23 and Atg27 act at the early stages of Atg9 trafficking in S. cerevisiae. Traffic 2015; 16:172-90; PMID:25385507; http://dx.doi.org/10.1111/tra.12240
46. K.A.Tucker, F.Reggiori, W.A.Dunn, Jr., D.J.Klionsky. Atg23 is essential for the cytoplasm to vacuole targeting pathway and efficient autophagy but not pexophagy. J Biol Chem 2003; 278:48445-52; PMID:14504273; http://dx.doi.org/10.1074/jbc.M309238200
47. J.Kim, Y.Kamada, P.E.Stromhaug, J.Guan, A.Hefner-Gravink, M.Baba, S.V.Scott, Y.Ohsumi, W.A.Dunn, Jr., D.J.Klionsky. Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J Cell Biol 2001; 153:381-96; PMID:11309418; http://dx.doi.org/10.1083/jcb.153.2.381
48. M.K.Sung, W.K.Huh. Bimolecular fluorescence complementation analysis system for in vivo detection of protein-protein interaction in Saccharomyces cerevisiae. Yeast 2007; 24:767-75; PMID:17534848; http://dx.doi.org/10.1002/yea.1504
49. K.Mao, X.Liu, Y.Feng, D.J.Klionsky. The progression of peroxisomal degradation through autophagy requires peroxisomal division. Autophagy 2014; 10:652-61; PMID:24451165; http://dx.doi.org/10.4161/auto.27852
50. K.Wang, Z.Yang, X.Liu, K.Mao, U.Nair, D.J.Klionsky. Phosphatidylinositol 4-kinases are required for autophagic membrane trafficking. J Biol Chem 2012; 287:37964-72; PMID:22977244; http://dx.doi.org/10.1074/jbc.M112.371591
51. L.Zheng, U.Baumann, J.L.Reymond. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res 2004; 32:e115; PMID:15304544; http://dx.doi.org/10.1093/nar/gnh110
52. N.Dephoure, S.P.Gygi. A solid phase extraction-based platform for rapid phosphoproteomic analysis. Methods 2011; 54:379-86; PMID:21440633; http://dx.doi.org/10.1016/j.ymeth.2011.03.008
53. E.L.Huttlin, M.P.Jedrychowski, J.E.Elias, T.Goswami, R.Rad, S.A.Beausoleil, J.Villen, W.Haas, M.E.Sowa, S.P.Gygi. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010; 143:1174-89; PMID:21183079; http://dx.doi.org/10.1016/j.cell.2010.12.001
54. J.E.Elias, S.P.Gygi. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 2007; 4:207-14; PMID:17327847; http://dx.doi.org/10.1038/nmeth1019
55. S.A.Beausoleil, J.Villen, S.A.Gerber, J.Rush, S.P.Gygi. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 2006; 24:1285-92; PMID:16964243; http://dx.doi.org/10.1038/nbt1240
56. R.Wright. Transmission electron microscopy of yeast. Microsc Res Tech 2000; 51:496-510; PMID:11169854; http://dx.doi.org/10.1002/1097-0029(20001215)51:6%3c496::AID-JEMT2%3e3.0.CO;2-9
57. T.Noda, D.J.Klionsky. The quantitative Pho8Δ60 assay of nonspecific autophagy. Methods Enzymol 2008; 451:33-42; PMID:19185711; http://dx.doi.org/10.1016/S0076-6879(08)03203-5
58. T.Noda, A.Matsuura, Y.Wada, Y.Ohsumi. Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 1995; 210:126-32; PMID:7741731; http://dx.doi.org/10.1006/bbrc.1995.1636
59. J.S.Robinson, D.J.Klionsky, L.M.Banta, S.D.Emr. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 1988; 8:4936-48; PMID:3062374; http://dx.doi.org/10.1128/MCB.8.11.4936
60. T.Kanki, K.Wang, M.Baba, C.R.Bartholomew, M.A.Lynch-Day, Z.Du, J.Geng, K.Mao, Z.Yang, W.-L.Yen, et al. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol Biol Cell 2009; 20:4730-8; PMID:19793921; http://dx.doi.org/10.1091/mbc.E09-03-0225