ATG13: Just a companion, or an executor of the autophagic program?

Autophagy

Volumn 10, Issue 6, 2014, Pages 944-956

  Alers, Sebastian ^a   Wesselborg, Sebastian ^a   Stork, Björn ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

ATG101; ATG13; Autophagy; RB1CC1; ULK1

Indexed keywords

AUTOPHAGY PROTEIN 13; PROTEIN; UNC 51 LIKE KINASE; UNCLASSIFIED DRUG; ATG1 PROTEIN, S CEREVISIAE; ATG13 PROTEIN, DROSOPHILA; ATG13 PROTEIN, HUMAN; ATG13 PROTEIN, S CEREVISIAE; CAENORHABDITIS ELEGANS PROTEIN; DROSOPHILA PROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; ULK1 PROTEIN, HUMAN; UNC-51 PROTEIN, C ELEGANS;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; AUTOPHAGOSOME; AUTOPHAGY; BINDING AFFINITY; BINDING SITE; CYTOLYSIS; DIMERIZATION; HUMAN; MITOPHAGY; NONHUMAN; PEXOPHAGY; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; YEAST; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; GENETICS; PHOSPHORYLATION; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALTERNATIVE SPLICING; ANIMALS; AUTOPHAGY; BINDING SITES; CAENORHABDITIS ELEGANS PROTEINS; DROSOPHILA PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84903618000     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28987     Document Type: Review

References (87)

1. Klionsky DJ. Autophagy revisited: a conversation with Christian de Duve. Autophagy 2008; 4:740-3; PMID:18567941
2. Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 1993; 333:169-74; PMID:8224160; http://dx.doi.org/10.1016/0014-5793(93)80398-E (Pubitemid 23306962)
3. Klionsky DJ, Cregg JM, Dunn WA Jr., Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, 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 (Pubitemid 37243044)
4. Araki Y, Ku WC, Akioka M, May AI, Hayashi Y, Arisaka F, Ishihama Y, Ohsumi Y. Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J Cell Biol 2013; 203:299-313; PMID:24165940; http://dx.doi.org/10.1083/jcb.201304123
5. 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; 20:5971-81; PMID:11689437; http://dx.doi.org/10.1093/emboj/20.21.5971 (Pubitemid 33049272)
6. Funakoshi T, Matsuura A, Noda T, Ohsumi Y. Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae. Gene 1997; 192:207-13; PMID:9224892; http://dx.doi.org/10.1016/S0378-1119(97)00031-0 (Pubitemid 27268244)
7. Kabeya Y, Kawamata T, Suzuki K, Ohsumi Y. Cis1/Atg31 is required for autophagosome formation in Saccharomyces cerevisiae. Biochem Biophys Res Commun 2007; 356:405-10; PMID:17362880; http://dx.doi.org/10.1016/j.bbrc.2007.02.150 (Pubitemid 46452560)
8. 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; PMID:10995454; http://dx.doi.org/10.1083/jcb.150.6.1507
9. Kawamata T, Kamada Y, Suzuki K, Kuboshima N, Akimatsu H, Ota S, Ohsumi M, Ohsumi Y. Characterization of a novel autophagy-specific gene, ATG29. Biochem Biophys Res Commun 2005; 338:1884-9; PMID:16289106; http://dx.doi.org/10.1016/j. bbrc.2005.10.163 (Pubitemid 41643105)
10. Kim J, Kamada Y, Stromhaug PE, Guan J, Hefner-Gravink A, Baba M, Scott SV, Ohsumi Y, Dunn WA Jr., Klionsky DJ. 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 (Pubitemid 34280222)
11. Nice DC, Sato TK, Stromhaug PE, Emr SD, Klionsky DJ. Cooperative binding of the cytoplasm to vacuole targeting pathway proteins, Cvt13 and Cvt20, to phosphatidylinositol 3-phosphate at the pre-autophagosomal structure is required for selective autophagy. J Biol Chem 2002; 277:30198-207; PMID:12048214; http://dx.doi.org/10.1074/jbc. M204736200
12. rd, Nau JJ, Weisman LS, Kamada Y, Keizer-Gunnink I, Funakoshi T, Veenhuis M, Ohsumi Y, Klionsky DJ. 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
13. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 2010; 22:132-9; PMID:20056399; http://dx.doi.org/10.1016/j. ceb.2009.12.004
14. Reggiori F, Klionsky DJ. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 2013; 194:341-61; PMID:23733851; http://dx.doi.org/10.1534/genetics.112.149013
15. Kabeya Y, Noda NN, Fujioka Y, Suzuki K, Inagaki F, Ohsumi Y. Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvationinduced autophagy in Saccharomyces cerevisiae. Biochem Biophys Res Commun 2009; 389:612-5; PMID:19755117; http://dx.doi.org/10.1016/j. bbrc.2009.09.034
16. Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y. Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 2008; 19:2039-50; PMID:18287526; http://dx.doi.org/10.1091/mbc.E07-10-1048
17. Suzuki K, Kubota Y, Sekito T, Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 2007; 12:209-18; PMID:17295840; http://dx.doi.org/10.1111/j.1365-2443.2007.01050.x (Pubitemid 46152659)
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; PMID:15901835; http://dx.doi.org/10.1091/mbc.E04-10-0894 (Pubitemid 40962611)
19. Kabeya Y, Kamada Y, Baba M, Takikawa H, Sasaki M, Ohsumi Y. Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol Biol Cell 2005; 16:2544-53; PMID:15743910; http://dx.doi.org/10.1091/mbc.E04-08-0669 (Pubitemid 40632233)
20. 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; PMID:18077553; http://dx.doi.org/10.1091/mbc. E07-08-0826 (Pubitemid 351272154)
21. Sekito T, Kawamata T, Ichikawa R, Suzuki K, Ohsumi Y. Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells 2009; 14:525-38; PMID:19371383; http://dx.doi.org/10.1111/j.1365-2443.2009.01299.x
22. 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; 126:2534-44; PMID:23549786; http://dx.doi.org/10. 1242/jcs.122960
23. Yeh YY, Shah KH, Herman PK. An Atg13 proteinmediated self-association of the Atg1 protein kinase is important for the induction of autophagy. J Biol Chem 2011; 286:28931-9; PMID:21712380; http://dx.doi.org/10.1074/jbc.M111.250324
24. Ragusa MJ, Stanley RE, Hurley JH. Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 2012; 151:1501-12; PMID:23219485; http://dx.doi.org/10.1016/j.cell.2012.11.028
25. Jao CC, Ragusa MJ, Stanley RE, Hurley JH. What the N-terminal domain of Atg13 looks like and what it does: a HORMA fold required for PtdIns 3-kinase recruitment. Autophagy 2013; 9:1112-4; PMID:23670046; http://dx.doi.org/10.4161/ auto.24896
26. Jao CC, Ragusa MJ, Stanley RE, Hurley JH. A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proc Natl Acad Sci U S A 2013; 110:5486-91; PMID:23509291; http://dx.doi.org/10.1073/pnas.1220306110
27. Kraft C, Kijanska M, Kalie E, Siergiejuk E, Lee SS, 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; 31:3691-703; PMID:22885598; http://dx.doi.org/10.1038/emboj.2012.225
28. Kamada Y, Yoshino K, Kondo C, Kawamata T, Oshiro N, Yonezawa K, Ohsumi Y. 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
29. Stephan JS, Yeh YY, Ramachandran V, Deminoff SJ, Herman PK. 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
30. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID:19225151; http://dx.doi.org/10.1091/mbc. E08-12-1249
31. Alers S, Löffler AS, Paasch F, Dieterle AM, Keppeler H, Lauber K, Campbell DG, Fehrenbacher B, Schaller M, Wesselborg S, et al. Atg13 and FIP200 act independently of Ulk1 and Ulk2 in autophagy induction. Autophagy 2011; 7:1423-33; PMID:22024743; http://dx.doi.org/10.4161/auto.7.12.18027
32. Alemu EA, Lamark T, Torgersen KM, Birgisdottir AB, Larsen KB, Jain A, Olsvik H, Øvervatn A, Kirkin V, Johansen T. ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. J Biol Chem 2012; 287:39275-90; PMID:23043107; http://dx.doi.org/10.1074/jbc.M112.378109
33. Mercer CA, Kaliappan A, Dennis PB. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009; 5:649-62; PMID:19287211; http://dx.doi.org/10.4161/auto.5.5.8249
34. Karanasios E, Stapleton E, Manifava M, Kaizuka T, Mizushima N, Walker SA, Ktistakis NT. Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci 2013; 126:5224-38; PMID:24013547; http://dx.doi.org/10.1242/jcs.132415
35. Joo JH, Dorsey FC, Joshi A, Hennessy-Walters KM, Rose KL, McCastlain K, Zhang J, Iyengar R, Jung CH, Suen DF, et al. Hsp90-Cdc37 chaperone complex regulates Ulk1- and Atg13-mediated mitophagy. Mol Cell 2011; 43:572-85; PMID:21855797; http://dx.doi.org/10.1016/j.molcel.2011.06.018
36. Shang L, Chen S, Du F, Li S, Zhao L, Wang X. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci U S A 2011; 108:4788-93; PMID:21383122; http://dx.doi.org/10.1073/pnas.1100844108
37. Hsu PP, Kang SA, Rameseder J, Zhang Y, Ottina KA, Lim D, Peterson TR, Choi Y, Gray NS, Yaffe MB, et al. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 2011; 332:1317-22; PMID:21659604; http://dx.doi.org/10.1126/science.1199498
38. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villén J, Haas W, Sowa ME, Gygi SP. 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
39. Schreiber TB, Mäusbacher N, Kéri G, Cox J, Daub H. An integrated phosphoproteomics work flow reveals extensive network regulation in early lysophosphatidic acid signaling. Mol Cell Proteomics 2010; 9:1047-62; PMID:20071362; http://dx.doi.org/10.1074/mcp.M900486-MCP200
40. Trinidad JC, Barkan DT, Gulledge BF, Thalhammer A, Sali A, Schoepfer R, Burlingame AL. Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol Cell Proteomics 2012; 11:215-29; PMID:22645316; http://dx.doi.org/10.1074/mcp. O112.018366
41. Villén J, Beausoleil SA, Gerber SA, Gygi SP. Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci U S A 2007; 104:1488-93; PMID:17242355; http://dx.doi.org/10.1073/pnas.0609836104 (Pubitemid 46214617)
42. Wiśniewski JR, Nagaraj N, Zougman A, Gnad F, Mann M. Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J Proteome Res 2010; 9:3280-9; PMID:20415495; http://dx.doi.org/10. 1021/pr1002214
43. Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villén J, Kubica N, Hoffman GR, Cantley LC, Gygi SP, et al. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 2011; 332:1322-6; PMID:21659605; http://dx.doi.org/10.1126/science. 1199484
44. Zanivan S, Gnad F, Wickström SA, Geiger T, Macek B, Cox J, Fässler R, Mann M. Solid tumor proteome and phosphoproteome analysis by high resolution mass spectrometry. J Proteome Res 2008; 7:5314-26; PMID:19367708; http://dx.doi.org/10.1021/pr800599n
45. Aravind L, Koonin EV. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 1998; 23:284-6; PMID:9757827; http://dx.doi.org/10.1016/S0968-0004(98)01257-2
46. Sironi L, Mapelli M, Knapp S, De Antoni A, Jeang KT, Musacchio A. Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J 2002; 21:2496-506; PMID:12006501; http://dx.doi.org/10.1093/emboj/21.10.2496 (Pubitemid 34546721)
47. Kihara A, Noda T, Ishihara N, Ohsumi Y. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 2001; 152:519-30; PMID:11157979; http://dx.doi.org/10.1083/jcb.152.3.519 (Pubitemid 34280235)
48. Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 2009; 186:773-82; PMID:19797076; http://dx.doi.org/10.1083/jcb.200907014
49. 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; PMID:19597335; http://dx.doi.org/10.4161/auto.5.7.9296
50. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182:685-701; PMID:18725538; http://dx.doi.org/10.1083/jcb.200803137
51. Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 2010; 6:764-76; PMID:20639694; http://dx.doi.org/10.4161/auto.6.6.12709
52. Miller-Fleming L, Cheong H, Antas P, Klionsky DJ. Detection of Saccharomyces cerevisiae Atg13 by western blot. Autophagy 2014; 10:514-7; PMID:24430166; http://dx.doi.org/10.4161/auto.27707
53. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JA. ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 2007; 3:106-16; PMID:17204848 (Pubitemid 46449098)
54. Ogura K, Wicky C, Magnenat L, Tobler H, Mori I, Müller F, Ohshima Y. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev 1994; 8:2389-400; PMID:7958904; http://dx.doi.org/10.1101/gad.8.20.2389 (Pubitemid 24323818)
55. Kuroyanagi H, Yan J, Seki N, Yamanouchi Y, Suzuki Y, Takano T, Muramatsu M, Shirasawa T. Human ULK1, a novel serine/threonine kinase related to UNC-51 kinase of Caenorhabditis elegans: cDNA cloning, expression, and chromosomal assignment. Genomics 1998; 51:76-85; PMID:9693035; http://dx.doi.org/10.1006/ geno.1998.5340 (Pubitemid 28373375)
56. Yan J, Kuroyanagi H, Kuroiwa A, Matsuda Y, Tokumitsu H, Tomoda T, Shirasawa T, Muramatsu M. Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem Biophys Res Commun 1998; 246:222-7; PMID:9600096; http://dx.doi.org/10.1006/bbrc.1998.8546 (Pubitemid 28413955)
57. Yan J, Kuroyanagi H, Tomemori T, Okazaki N, Asato K, Matsuda Y, Suzuki Y, Ohshima Y, Mitani S, Masuho Y, et al. Mouse ULK2, a novel member of the UNC-51-like protein kinases: unique features of functional domains. Oncogene 1999; 18:5850-9; PMID:10557072; http://dx.doi.org/10.1038/sj.onc.1202988 (Pubitemid 29520441)
58. Chan EY, Longatti A, McKnight NC, Tooze SA. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol 2009; 29:157-71; PMID:18936157; http://dx.doi.org/10.1128/MCB.01082-08
59. Hara T, Mizushima N. Role of ULK-FIP200 complex in mammalian autophagy: FIP200, a counterpart of yeast Atg17? Autophagy 2009; 5:85-7; PMID:18981720; http://dx.doi.org/10.4161/auto.5.1.7180
60. Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, Mizushima N. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 2008; 181:497-510; PMID:18443221; http://dx.doi.org/10.1083/jcb.200712064 (Pubitemid 351645039)
61. Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature 2010; 466:68-76; PMID:20562859; http://dx.doi.org/10.1038/nature09204
62. Ganley IG, Lam H, Wang J, Ding X, Chen S, Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305; PMID:19258318; http://dx.doi.org/10.1074/jbc.M900573200
63. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91; PMID:19211835; http://dx.doi.org/10.1091/mbc.E08-12-1248
64. Chang YY, Neufeld TP. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell 2009; 20:2004-14; PMID:19225150; http://dx.doi.org/10.1091/mbc. E08-12-1250
65. Tian E, Wang F, Han J, Zhang H. epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans. Autophagy 2009; 5:608-15; PMID:19377305; http://dx.doi.org/10.4161/auto.5.5.8624
66. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77:71-94; PMID:4366476
67. Lai T, Garriga G. The conserved kinase UNC-51 acts with VAB-8 and UNC-14 to regulate axon outgrowth in C. elegans. Development 2004; 131:5991-6000; PMID:15539493; http://dx.doi.org/10.1242/dev.01457 (Pubitemid 40123914)
68. Ogura K, Shirakawa M, Barnes TM, Hekimi S, Ohshima Y. The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes Dev 1997; 11:1801-11; PMID:9242488; http://dx.doi.org/10.1101/gad.11.14.1801 (Pubitemid 27315210)
69. rd, Josowitz R, Krasieva TB, Lamorte VJ, Suzuki E, Gindhart JG, Furukubo-Tokunaga K, Tomoda T. UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly. Genes Dev 2008; 22:3292-307; PMID:19056884; http://dx.doi.org/10.1101/gad.1734608
70. Lee EJ, Tournier C. The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy. Autophagy 2011; 7:689-95; PMID:21460635; http://dx.doi.org/10.4161/auto.7.7.15450
71. Tomoda T, Bhatt RS, Kuroyanagi H, Shirasawa T, Hatten ME. A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 1999; 24:833-46; PMID:10624947; http://dx.doi.org/10.1016/S0896-6273(00)81031-4 (Pubitemid 30017663)
72. Zhou X, Babu JR, da Silva S, Shu Q, Graef IA, Oliver T, Tomoda T, Tani T, Wooten MW, Wang F. Unc- 51-like kinase 1/2-mediated endocytic processes regulate filopodia extension and branching of sensory axons. Proc Natl Acad Sci U S A 2007; 104:5842-7; PMID:17389358; http://dx.doi.org/10.1073/pnas.0701402104 (Pubitemid 47175621)
73. Rajesh S, Bago R, Odintsova E, Muratov G, Baldwin G, Sridhar P, Rajesh S, Overduin M, Berditchevski F. Binding to syntenin-1 protein defines a new mode of ubiquitin-based interactions regulated by phosphorylation. J Biol Chem 2011; 286:39606-14; PMID:21949238; http://dx.doi.org/10.1074/jbc. M111.262402
74. Tomoda T, Kim JH, Zhan C, Hatten ME. Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev 2004; 18:541-58; PMID:15014045; http://dx.doi.org/10.1101/gad.1151204 (Pubitemid 38372811)
75. Wong PM, Puente C, Ganley IG, Jiang X. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 2013; 9:124-37; PMID:23295650; http://dx.doi.org/10.4161/auto.23323
76. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149:274-93; PMID:22500797; http://dx.doi.org/10.1016/j. cell.2012.03.017
77. McEwan DG, Dikic I. Not all autophagy membranes are created equal. Cell 2010; 141:564-6; PMID:20478247; http://dx.doi.org/10.1016/j. cell.2010.04.030
78. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 2009; 11:1433-7; PMID:19898463; http://dx.doi.org/10. 1038/ncb1991
79. Matsunaga K, Morita E, Saitoh T, Akira S, Ktistakis NT, Izumi T, Noda T, Yoshimori T. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol 2010; 190:511-21; PMID:20713597; http://dx.doi.org/10.1083/jcb.200911141
80. Ylä-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009; 5:1180-5; PMID:19855179; http://dx.doi.org/10.4161/auto.5.8.10274
81. Suzuki H, Tabata K, Morita E, Kawasaki M, Kato R, Dobson RC, Yoshimori T, Wakatsuki S. Structural basis of the autophagy-related LC3/Atg13 LIR complex: recognition and interaction mechanism. Structure 2014; 22:47-58; PMID:24290141; http://dx.doi.org/10.1016/j.str.2013.09.023
82. Takaesu G, Kobayashi T, Yoshimura A. TGFβ- activated kinase 1 (TAK1)-binding proteins (TAB)2 and 3 negatively regulate autophagy. J Biochem 2012; 151:157-66; PMID:21976705; http://dx.doi.org/10.1093/jb/mvr123
83. 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; 191:155-68; PMID:20921139; http://dx.doi.org/10.1083/jcb.201002100
84. Russell RC, Tian Y, Yuan H, Park HW, Chang YY, Kim J, Kim H, Neufeld TP, Dillin A, Guan KL. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 2013; 15:741-50; PMID:23685627; http://dx.doi.org/10.1038/ncb2757
85. Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29:1792-802; PMID:20418806; http://dx.doi.org/10.1038/emboj.2010.74
86. Okazaki N, Yan J, Yuasa S, Ueno T, Kominami E, Masuho Y, Koga H, Muramatsu M. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res 2000; 85:1-12; PMID:11146101; http://dx.doi.org/10.1016/S0169-328X(00)00218-7 (Pubitemid 32056233)
87. Suttangkakul A, Li F, Chung T, Vierstra RD. The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 2011; 23:3761-79; PMID:21984698; http://dx.doi.org/10. 1105/tpc.111.090993