Autophagosome–lysosome fusion in neurons requires INPP5E, a protein associated with Joubert syndrome

EMBO Journal

Volumn 35, Issue 17, 2016, Pages 1853-1867

  Hasegawa, Junya ^a   Iwamoto, Ryo ^a   Otomo, Takanobu ^a   Nezu, Akiko ^a   Hamasaki, Maho ^a   Yoshimori, Tamotsu ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

autophagosomes; Joubert syndrome; lysosomes; phosphoinositides

Indexed keywords

CORTACTIN; INOSITOL POLYPHOSPHATE 5 PHOSPHATASE E; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3,5 BISPHOSPHATE; POLYPHOSPHOINOSITIDE; SMALL INTERFERING RNA; SYNAPTOJANIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOACCUMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME SUBSTRATE; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; JOUBERT SYNDROME; LYSOSOME; MEMBRANE FUSION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE;

EID: 84981723836     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201593148     Document Type: Article

References (54)

1. Backer JM (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410: 1–17
2. Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93: 1019–1137
3. Bielas SL, Silhavy JL, Brancati F, Kisseleva MV, Al-Gazali L, Sztriha L, Bayoumi RA, Zaki MS, Abdel-Aleem A, Rosti RO, Kayserili H, Swistun D, Scott LC, Bertini E, Boltshauser E, Fazzi E, Travaglini L, Field SJ, Gayral S, Jacoby M et al (2009) Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies. Nat Genet 41: 1032–1036
4. Cebollero E, van der Vaart A, Zhao M, Rieter E, Klionsky DJ, Helms JB, Reggiori F (2012) Phosphatidylinositol-3-phosphate clearance plays a key role in autophagosome completion. Curr Biol 22: 1545–1553
5. Chávez M, Ena S, Van Sande J, de Kerchove d'Exaerde A, Schurmans S, Schiffmann SN (2015) Modulation of Ciliary Phosphoinositide Content Regulates Trafficking and Sonic Hedgehog Signaling Output. Dev Cell 34: 338–350
6. Dall'Armi C, Devereaux KA, Di Paolo G (2013) The role of lipids in the control of autophagy. Curr Biol 23: R33–R45
7. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651–657
8. Dooley HC, Razi M, Polson HEJ, 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
9. Ferguson CJ, Lenk GM, Meisler MH (2009) Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum Mol Genet 18: 4868–4878
10. Fujita N, Morita E, Itoh T, Tanaka A, Nakaoka M, Osada Y, Umemoto T, Saitoh T, Nakatogawa H, Kobayashi S, Haraguchi T, Guan J-L, Iwai K, Tokunaga F, Saito K, Ishibashi K, Akira S, Fukuda M, Noda T, Yoshimori T (2013) Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol 203: 115–128
11. Garcia-Gonzalo FR, Phua SC, Roberson EC, Garcia G III, Abedin M, Schurmans S, Inoue T, Reiter JF (2015) Phosphoinositides Regulate Ciliary Protein Trafficking to Modulate Hedgehog Signaling. Dev Cell 34: 400–409
12. Hasegawa J, Tokuda E, Tenno T, Tsujita K, Sawai H, Hiroaki H, Takenawa T, Itoh T (2011) SH3YL1 regulates dorsal ruffle formation by a novel phosphoinositide-binding domain. J Cell Biol 193: 901–916
13. Hong NH, Qi A, Weaver AM (2015) PI(3,5)P2 controls endosomal branched actin dynamics by regulating cortactin-actin interactions. J Cell Biol 210: 753–769
14. 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
15. Jacoby M, Cox JJ, Gayral S, Hampshire DJ, Ayub M, Blockmans M, Pernot E, Kisseleva MV, Compère P, Schiffmann SN, Gergely F, Riley JH, Pérez-Morga D, Woods CG, Schurmans S (2009) INPP5E mutations cause primary cilium signaling defects, ciliary instability and ciliopathies in human and mouse. Nat Genet 41: 1027–1031
16. Jefferies HBJ, Cooke FT, Jat P, Boucheron C, Koizumi T, Hayakawa M, Kaizawa H, Ohishi T, Workman P, Waterfield MD, Parker PJ (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9: 164–170
17. Jia D, Gomez TS, Metlagel Z, Umetani J, Otwinowski Z, Rosen MK, Billadeau DD (2010) WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc Natl Acad Sci USA 107: 10442–10447
18. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T (2001) Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2: 330–335
19. Kimura S, Noda T, Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452–460
20. Kisseleva MV, Wilson MP, Majerus PW (2000) The isolation and characterization of a cDNA encoding phospholipid-specific inositol polyphosphate 5-phosphatase. J Biol Chem 275: 20110–20116
21. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT et al (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151–175
22. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169: 425–434
23. Kong AM, Speed CJ, O'Malley CJ, Layton MJ, Meehan T, Loveland KL, Cheema S, Ooms LM, Mitchell CA (2000) Cloning and characterization of a 72-kDa inositol-polyphosphate 5-phosphatase localized to the Golgi network. J Biol Chem 275: 24052–24064
24. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432: 1032–1036
25. Lamb CA, Yoshimori T, Tooze SA (2013) The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14: 759–774
26. de Lartigue J, Polson H, Feldman M, Shokat K, Tooze SA, Urbé S, Clague MJ (2009) PIKfyve regulation of endosome-linked pathways. Traffic 10: 883–893
27. Lee J-Y, Koga H, Kawaguchi Y, Tang W, Wong E, Gao Y-S, Pandey UB, Kaushik S, Tresse E, Lu J, Taylor JP, Cuervo AM, Yao T-P (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29: 969–980
28. Li X, Wang X, Zhang X, Zhao M, Tsang WL, Zhang Y, Yau RGW, Weisman LS, Xu H (2013) Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci USA 110: 21165–21170
29. Martin S, Harper CB, May LM, Coulson EJ, Meunier FA, Osborne SL (2013) Inhibition of PIKfyve by YM-201636 dysregulates autophagy and leads to apoptosis-independent neuronal cell death. PLoS ONE 8: e60152
30. McCartney AJ, Zhang Y, Weisman LS (2014) Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays 36: 52–64
31. Mi N, Chen Y, Wang S, Chen M, Zhao M, Yang G, Ma M, Su Q, Luo S, Shi J, Xu J, Guo Q, Gao N, Sun Y, Chen Z, Yu L (2015) CapZ regulates autophagosomal membrane shaping by promoting actin assembly inside the isolation membrane. Nat Cell Biol 17: 1112–1123
32. Mizushima N, Levine B (2010) Autophagy in mammalian development and differentiation. Nat Cell Biol 12: 823–830
33. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147: 728–741
34. Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27: 107–132
35. 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
36. Oser M, Mader CC, Gil-Henn H, Magalhaes M, Bravo-Cordero JJ, Koleske AJ, Condeelis J (2010) Specific tyrosine phosphorylation sites on cortactin regulate Nck1-dependent actin polymerization in invadopodia. J Cell Sci 123: 3662–3673
37. Otomo T, Higaki K, Nanba E, Ozono K, Sakai N (2011) Lysosomal storage causes cellular dysfunction in mucolipidosis II skin fibroblasts. J Biol Chem 286: 35283–35290
38. Pampliega O, Orhon I, Patel B, Sridhar S, Díaz-Carretero A, Beau I, Codogno P, Satir BH, Satir P, Cuervo AM (2013) Functional interaction between autophagy and ciliogenesis. Nature 502: 194–200
39. Plotnikova OV, Seo S, Cottle DL, Conduit S, Hakim S, Dyson JM, Mitchell CA, Smyth IM (2015) INPP5E interacts with AURKA, linking phosphoinositide signaling to primary cilium stability. J Cell Sci 128: 364–372
40. Romani M, Micalizzi A, Valente EM (2013) Joubert syndrome: congenital cerebellar ataxia with the molar tooth. Lancet Neurol 12: 894–905
41. Saitoh T, Nakayama M, Nakano H, Yagita H, Yamamoto N, Yamaoka S (2003) TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. J Biol Chem 278: 36005–36012
42. Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki M, Suzuki A (2009) Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res 48: 307–343
43. Schneider JL, Cuervo AM (2014) Autophagy and human disease: emerging themes. Curr Opin Genet Dev 26C: 16–23
44. Settembre C, Fraldi A, Medina DL, Ballabio A (2013) Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 14: 283–296
45. Simonsen A, Tooze SA (2009) Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 186: 773–782
46. Singh R, Cuervo AM (2011) Autophagy in the cellular energetic balance. Cell Metab 13: 495–504
47. Taguchi-Atarashi N, Hamasaki M, Matsunaga K, Omori H, Ktistakis NT, Yoshimori T, Noda T (2010) Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic 11: 468–478
48. Takáts S, Nagy P, Varga Á, Pircs K, Kárpáti M, Varga K, Kovács AL, Hegedűs K, Juhász G (2013) Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J Cell Biol 201: 531–539
49. Tang Z, Lin MG, Stowe TR, Chen S, Zhu M, Stearns T, Franco B, Zhong Q (2013) Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 502: 254–257
50. Velikkakath AKG, Nishimura T, Oita E, Ishihara N, Mizushima N (2012) Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell 23: 896–909
51. Vergne I, Roberts E, Elmaoued RA, Tosch V, Delgado MA, Proikas-Cezanne T, Laporte J, Deretic V (2009) Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J 28: 2244–2258
52. Vicinanza M, D'Angelo G, Di Campli A, De Matteis MA (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J 27: 2457–2470
53. Ward DM, Vaughn MB, Shiflett SL, White PL, Pollock AL, Hill J, Schnegelberger R, Sundquist WI, Kaplan J (2005) The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. J Biol Chem 280: 10548–10555
54. Zhuo C, Ji Y, Chen Z, Kitazato K, Xiang Y, Zhong M, Wang Q, Pei Y, Ju H, Wang Y (2013) Proteomics analysis of autophagy-deficient Atg7-/- MEFs reveals a close relationship between F-actin and autophagy. Biochem Biophys Res Commun 437: 482–488