TBC1D14 regulates autophagy via the TRAPP complex and ATG9 traffic

EMBO Journal

Volumn 35, Issue 3, 2016, Pages 281-301

  Lamb, Christopher A ^a   Nühlen, Stefanie ^b   Judith, Delphine ^a   Frith, David ^a   Snijders, Ambrosius P ^a   Behrends, Christian ^b   Tooze, Sharon A ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

Author keywords

Autophagy; Membrane Trafficking; Rab proteins; TRAPP

Indexed keywords

ATG9 PROTEIN; MEMBRANE PROTEIN; RAB PROTEIN; RAB1 PROTEIN; REGULATOR PROTEIN; TBC1D14 PROTEIN; TRAFFICKING PROTEIN PARTICLE III; UNCLASSIFIED DRUG; ATG9A PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN BINDING; TBC1D14 PROTEIN, HUMAN; TRANSPORT PROTEIN PARTICLE, TRAPP; TRAPPC8 PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; ENDOSOME; GENE OVEREXPRESSION; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; BIOLOGICAL MODEL; CELL LINE; CYTOPLASM VESICLE; HUMAN; METABOLISM; PROTEIN ANALYSIS;

AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; CELL LINE; CYTOPLASMIC VESICLES; GTPASE-ACTIVATING PROTEINS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RAB1 GTP-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84957440559     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592695     Document Type: Article

References (79)

1. Alvarez C, Garcia-Mata R, Brandon E, Sztul E, (2003) COPI recruitment is modulated by a Rab1b-dependent mechanism. Mol Biol Cell 14: 2116-2127
2. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT, (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701
3. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S, (2010) TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev Mol Cell Biol 11: 759-763
4. Bassik MC, Kampmann M, Lebbink RJ, Wang S, Hein MY, Poser I, Weibezahn J, Horlbeck MA, Chen S, Mann M, Hyman AA, Leproust EM, McManus MT, Weissman JS, (2013) A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 152: 909-922
5. Behrends C, Sowa ME, Gygi SP, Harper JW, (2010) Network organization of the human autophagy system. Nature 466: 68-76
6. Biazik J, Yla-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL, (2015) Ultrastructural relationship of the phagophore with surrounding organelles. Autophagy 11: 439-451
7. Birgisdottir ÅB, Lamark T, Johansen T, (2013) The LIR motif-crucial for selective autophagy. J Cell Sci 126: 3237-3247
8. Chan EY, Kir S, Tooze SA, (2007) siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 282: 25464-25474
9. Chan EY, Longatti A, McKnight NC, Tooze SA, (2009) Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domain using an Atg13-independent mechanism. Mol Cell Biol 29: 157-171
10. Ching YH, Munroe RJ, Moran JL, Barker AK, Mauceli E, Fennell T, Dipalma F, Lindblad-Toh K, Abcunas LM, Gilmour JF, Harris TP, Kloet SL, Luo Y, McElwee JL, Mu W, Park HK, Rogal DL, Schimenti KJ, Shen L, Shindo M, et al, (2010) High resolution mapping and positional cloning of ENU-induced mutations in the Rw region of mouse chromosome 5. BMC Genet 11: 106
11. Chung J, Kuo CJ, Crabtree GR, Blenis J, (1992) Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell 69: 1227-1236
12. Diao A, Rahman D, Pappin DJ, Lucocq J, Lowe M, (2003) The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J Cell Biol 160: 201-212
13. Dooley HC, Razi M, Polson HE, Girardin SE, Wilson MI, Tooze SA, (2014) WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 55: 238-252
14. Frasa MA, Koessmeier KT, Ahmadian MR, Braga VM, (2012) Illuminating the functional and structural repertoire of human TBC/RABGAPs. Nat Rev Mol Cell Biol 13: 67-73
15. Ge L, Melville D, Zhang M, Schekman R, (2013) The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2: e00947
16. Gordon DE, Bond LM, Sahlender DA, Peden AA, (2010) A targeted siRNA screen to identify SNAREs required for constitutive secretion in mammalian cells. Traffic 11: 1191-1204
17. Graef M, Friedman JR, Graham C, Babu M, Nunnari J, (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24: 2918-2931
18. Haas AK, Yoshimura S, Stephens DJ, Preisinger C, Fuchs E, Barr FA, (2007) Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J Cell Sci 120: 2997-3010
19. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, Amano A, Yoshimori T, (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495: 389-393
20. Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, Mizushima N, (2008) FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181: 497-510
21. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A, (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 11: 1433-1437
22. Hosokawa N, Sasaki T, Iemura S, Natsume T, Hara T, Mizushima N, (2009) Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5: 973-979
23. Huang J, Birmingham CL, Shahnazari S, Shiu J, Zheng YT, Smith AC, Campellone KG, Heo WD, Gruenheid S, Meyer T, Welch MD, Ktistakis NT, Kim PK, Klionsky DJ, Brumell JH, (2011) Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7: 17-26
24. Ishii Y, Nakahara T, Kataoka M, Kusumoto-Matsuo R, Mori S, Takeuchi T, Kukimoto I, (2013) Identification of TRAPPC8 as a host factor required for human papillomavirus cell entry. PLoS One 8: e80297
25. Itakura E, Kishi-Itakura C, Mizushima N, (2012) The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151: 1256-1269
26. Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M, (2008) Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19: 2916-2925
27. Itoh T, Kanno E, Uemura T, Waguri S, Fukuda M, (2011) OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation. J Cell Biol 192: 839-853
28. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T, (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728
29. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T, (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117: 2805-2812
30. Kakuta S, Yamamoto H, Negishi L, Kondo-Kakuta C, Hayashi N, Ohsumi Y, (2012) Atg9 vesicles recruit vesicle-tethering proteins Trs85 and Ypt1 to the autophagosome formation site. J Biol Chem 287: 44261-44269
31. Karanasios E, Stapleton E, Manifava M, Kaizuka T, Mizushima N, Walker SA, Ktistakis NT, (2013) Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci 126: 5224-5238
32. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, et al, (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445-544
33. Knaevelsrud H, Soreng K, Raiborg C, Haberg K, Rasmuson F, Brech A, Liestol K, Rusten TE, Stenmark H, Neufeld TP, Carlsson SR, Simonsen A, (2013) Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J Cell Biol 202: 331-349
34. Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N, (2013) Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 9: 1491-1499
35. Lamb CA, Dooley HC, Tooze SA, (2013a) Endocytosis and autophagy: shared machinery for degradation. BioEssays 35: 34-45
36. Lamb CA, Yoshimori T, Tooze SA, (2013b) The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14: 759-774
37. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, Jung JU, (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10: 776-787
38. Lipatova Z, Belogortseva N, Zhang XQ, Kim J, Taussig D, Segev N, (2012) Regulation of selective autophagy onset by a Ypt/Rab GTPase module. Proc Natl Acad Sci USA 109: 6981-6986
39. Liu Q, Chang JW, Wang J, Kang SA, Thoreen CC, Markhard A, Hur W, Zhang J, Sim T, Sabatini DM, Gray NS, (2010) Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J Med Chem 53: 7146-7155
40. Longatti A, Lamb CA, Razi M, Yoshimura S-I, Barr FA, Tooze SA, (2012) TBC1D14 regulates autophagosome formation via Rab11 and recycling endosomes. J Cell Biol 197: 659-675
41. Lynch-Day MA, Bhandari D, Menon S, Huang J, Cai H, Bartholomew CR, Brumell JH, Ferro-Novick S, Klionsky DJ, (2010) Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc Natl Acad Sci USA 107: 7811-7816
42. Mardones GA, Snyder CM, Howell KE, (2006) Cis-Golgi matrix proteins move directly to endoplasmic reticulum exit sites by association with tubules. Mol Biol Cell 17: 525-538
43. Marie M, Dale HA, Sannerud R, Saraste J, (2009) The function of the intermediate compartment in pre-Golgi trafficking involves its stable connection with the centrosome. Mol Biol Cell 20: 4458-4470
44. Mercer CA, Kaliappan A, Dennis PB, (2009) A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5: 649-662
45. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, Natsume T, Ohsumi Y, Yoshimori T, (2003) Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 116: 1679-1688
46. Mizushima N, Levine B, Cuervo AM, Klionsky DJ, (2008) Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075
47. Mizushima N, Sugita H, Yoshimori T, Ohsumi Y, (1998) A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 273: 33889-33892
48. Mochizuki Y, Ohashi R, Kawamura T, Iwanari H, Kodama T, Naito M, Hamakubo T, (2013) Phosphatidylinositol 3-phosphatase myotubularin-related protein 6 (MTMR6) is regulated by small GTPase Rab1B in the early secretory and autophagic pathways. J Biol Chem 288: 1009-1021
49. Moreau K, Fleming A, Imarisio S, Lopez Ramirez A, Mercer JL, Jimenez-Sanchez M, Bento CF, Puri C, Zavodszky E, Siddiqi F, Lavau CP, Betton M, O'Kane CJ, Wechsler DS, Rubinsztein DC, (2014) PICALM modulates autophagy activity and tau accumulation. Nat Commun 5: 4998
50. Moreau K, Ravikumar B, Puri C, Rubinsztein DC, (2012) Arf6 promotes autophagosome formation via effects on phosphatidylinositol 4,5-bisphosphate and phospholipase D. J Cell Biol 196: 483-496
51. Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein David C, (2011) Autophagosome precursor maturation requires homotypic fusion. Cell 146: 303-317
52. Nazarko TY, Huang J, Nicaud JM, Klionsky DJ, Sibirny AA, (2005) Trs85 is required for macroautophagy, pexophagy and cytoplasm to vacuole targeting in Yarrowia lipolytica and Saccharomyces cerevisiae. Autophagy 1: 37-45
53. Orsi A, Razi M, Dooley H, Robinson D, Weston A, Collinson L, Tooze S, (2012) Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, is required for autophagy. Mol Biol Cell 23: 1860-1873
54. Papinski D, Schuschnig M, Reiter W, Wilhelm L, Barnes CA, Maiolica A, Hansmann I, Pfaffenwimmer T, Kijanska M, Stoffel I, Lee SS, Brezovich A, Lou JH, Turk BE, Aebersold R, Ammerer G, Peter M, Kraft C, (2014) Early steps in autophagy depend on direct phosphorylation of Atg9 by the Atg1 kinase. Mol Cell 53: 471-483
55. Perez-Victoria FJ, Schindler C, Magadan JG, Mardones GA, Delevoye C, Romao M, Raposo G, Bonifacino JS, (2010) Ang2/fat-free is a conserved subunit of the Golgi-associated retrograde protein complex. Mol Biol Cell 21: 3386-3395
56. Polson HEJ, de Lartigue J, Rigden DJ, Reedijk M, Urbe S, Clague MJ, Tooze SA, (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6: 506-522
57. Popovic D, Akutsu M, Novak I, Harper JW, Behrends C, Dikic I, (2012) Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol Cell Biol 32: 1733-1744
58. Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC, (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154: 1285-1299
59. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC, (2010) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12: 747-757
60. Rink J, Ghigo E, Kalaidzidis Y, Zerial M, (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749
61. Rosa P, Barr FA, Stinchcombe JC, Binacchi C, Huttner WB, (1992) Brefeldin A inhibits the formation of constitutive secretory vesicles and immature secretory granules from the trans-Golgi network. Eur J Cell Biol 59: 265-274
62. Roux KJ, Kim DI, Raida M, Burke B, (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol 196: 801-810
63. Sabatini DM, Erdjument-Bromage H, Lui M, Tempst P, Snyder SH, (1994) RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78: 35-43
64. Sacher M, Jiang Y, Barrowman J, Scarpa A, Burston J, Zhang L, Schieltz D, Yates JR 3rd, Abeliovich H, Ferro-Novick S, (1998) TRAPP, a highly conserved novel complex on the cis-Golgi that mediates vesicle docking and fusion. EMBO J 17: 2494-2503
65. Satoh A, Wang Y, Malsam J, Beard MB, Warren G, (2003) Golgin-84 is a rab1 binding partner involved in Golgi structure. Traffic 4: 153-161
66. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M, (2011) Global quantification of mammalian gene expression control. Nature 473: 337-342
67. Scrivens PJ, Noueihed B, Shahrzad N, Hul S, Brunet S, Sacher M, (2011) C4orf41 and TTC-15 are mammalian TRAPP components with a role at an early stage in ER-to-Golgi trafficking. Mol Biol Cell 22: 2083-2093
68. Shirahama-Noda K, Kira S, Yoshimori T, Noda T, (2013) TRAPPIII is responsible for vesicular transport from early endosomes to Golgi, facilitating Atg9 cycling in autophagy. J Cell Sci 126: 4963-4973
69. Tan D, Cai Y, Wang J, Zhang J, Menon S, Chou HT, Ferro-Novick S, Reinisch KM, Walz T, (2013) The EM structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway. Proc Natl Acad Sci USA 110: 19432-19437
70. Tempel W, Tong Y, Dimov S, Bochkarev A, Park H, (2008) First crystallographic models of human TBC domains in the context of a family-wide structural analysis. Proteins 71: 497-502
71. Wang J, Menon S, Yamasaki A, Chou HT, Walz T, Jiang Y, Ferro-Novick S, (2013) Ypt1 recruits the Atg1 kinase to the preautophagosomal structure. Proc Natl Acad Sci USA 110: 9800-9805
72. Webber JL, Tooze SA, (2010) New insights into the function of Atg9. FEBS Lett 584: 1319-1326
73. Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA, Lichtenberg M, Menzies FM, Ravikumar B, Imarisio S, Brown S, O'Kane CJ, Rubinsztein DC, (2010) alpha-Synuclein impairs macroautophagy: implications for Parkinson's disease. J Cell Biol 190: 1023-1037
74. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, Kondo-Kakuta C, Ichikawa R, Kinjo M, Ohsumi Y, (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 198: 219-233
75. Yamasaki A, Menon S, Yu S, Barrowman J, Meerloo T, Oorschot V, Klumperman J, Satoh A, Ferro-Novick S, (2009) mTrs130 is a component of a mammalian TRAPPII complex, a Rab1 GEF that binds to COPI-coated vesicles. Mol Biol Cell 20: 4205-4215
76. Yla-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL, (2009) 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5: 1180-1185
77. Young ARJ, Chan EYW, Hu XW, Köchl R, Crawshaw SG, High S, Hailey DW, Lippincott-Schwartz J, Tooze SA, (2006) Starvation and ULK1-dependent cycling of Mammalian Atg9 between the TGN and endosomes. J Cell Sci 119: 3888-3900
78. Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI, (2010) Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 11: 1246-1261
79. Zou S, Chen Y, Liu Y, Segev N, Yu S, Liu Y, Min G, Ye M, Zeng Y, Zhu X, Hong B, Bjorn LO, Liang Y, Li S, Xie Z, (2013) Trs130 participates in autophagy through GTPases Ypt31/32 in Saccharomyces cerevisiae. Traffic 14: 233-246