PTPN9-mediated dephosphorylation of VTI1B promotes ATG16L1 precursor fusion and autophagosome formation

References

• Mizushima N. Autophagy: process and function. Genes Dev. 2007 Nov 15;21(22):2861–2873. PubMed PMID: 18006683; eng.
   PubMed Web of Science ®Google Scholar
• Grasso D, Renna FJ, Vaccaro MI. Initial steps in mammalian autophagosome biogenesis. Front Cell Dev Biol. 2018;6:146. PubMed PMID: 30406104; PubMed Central PMCID: PMC6206277.
   PubMed Web of Science ®Google Scholar
• Graef M, Friedman JR, Graham C, et al. ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell. 2013 Sep;24(18):2918–2931. PubMed PMID: 23904270; PubMed Central PMCID: PMC3771953.
   PubMed Web of Science ®Google Scholar
• Ge L, Melville D, Zhang M, et al. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife. 2013 Aug 6;2:e00947. PubMed PMID: 23930225; PubMed Central PMCID: PMC3736544.
   PubMed Web of Science ®Google Scholar
• Guo Y, Chang C, Huang R, et al. AP1 is essential for generation of autophagosomes from the trans-Golgi network. J Cell Sci. 2012 Apr 1;125(Pt 7):1706–1715. PubMed PMID: 22328508.
   PubMed Web of Science ®Google Scholar
• Hailey DW, Rambold AS, Satpute-Krishnan P, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010 May 14;141(4):656–667. PubMed PMID: 20478256; PubMed Central PMCID: PMC3059894. eng.
   PubMed Web of Science ®Google Scholar
• Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER-mitochondria contact sites. Nature. 2013 Mar 21;495(7441):389–393. PubMed PMID: 23455425.
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Moreau K, Jahreiss L, et al. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol. 2010 Aug;12(8):747–757. PubMed PMID: 20639872; PubMed Central PMCID: PMC2923063. eng.
   PubMed Web of Science ®Google Scholar
• Puri C, Vicinanza M, Rubinsztein DC. Phagophores evolve from recycling endosomes. Autophagy. 2018;14(8):1475–1477. PubMed PMID: 29940791; PubMed Central PMCID: PMCPMC6103687.
   PubMed Web of Science ®Google Scholar
• Moreau K, Ravikumar B, Renna M, et al. Autophagosome precursor maturation requires homotypic fusion. Cell. 2011 Jul 22;146(2):303–317. PubMed PMID: 21784250; PubMed Central PMCID: PMCPMC3171170.
   PubMed Web of Science ®Google Scholar
• Imai K, Hao F, Fujita N, et al. Atg9A trafficking through the recycling endosomes is required for autophagosome formation. J Cell Sci. 2016 Oct 15;129(20):3781–3791. PubMed PMID: 27587839.
   PubMed Web of Science ®Google Scholar
• Xie Y, Kang R, Sun X, et al. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy. 2015;11(1):28–45. PubMed PMID: 25484070; PubMed Central PMCID: PMCPMC4502723.
   PubMed Web of Science ®Google Scholar
• Hunter T. Tyrosine phosphorylation: thirty years and counting. Curr Opin Cell Biol. 2009;21:140–146.
   PubMed Web of Science ®Google Scholar
• Wei Y, Zou Z, Becker N, et al. EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance. Cell. 2013 Sep 12;154(6):1269–1284. PubMed PMID: 24034250; PubMed Central PMCID: PMCPMC3917713.
   PubMed Web of Science ®Google Scholar
• Martin KR, Xu Y, Looyenga BD, et al. Identification of PTPsigma as an autophagic phosphatase. J Cell Sci. 2011 Mar 1;124(Pt 5):812–819. PubMed PMID: 21303930; PubMed Central PMCID: PMCPMC3039021.
   PubMed Web of Science ®Google Scholar
• Hatzihristidis T, Desai N, Hutchins AP, et al. A Drosophila-centric view of protein tyrosine phosphatases. FEBS Lett. 2015 Apr 13;589(9):951–966. PubMed PMID: 25771859.
   PubMed Web of Science ®Google Scholar
• Huynh H, Wang X, Li W, et al. Homotypic secretory vesicle fusion induced by the protein tyrosine phosphatase MEG2 depends on polyphosphoinositides in T cells. J Immunol. 2003 Dec 15;171(12):6661–6671. PubMed PMID: 14662869.
   PubMed Web of Science ®Google Scholar
• Huynh H, Bottini N, Williams S, et al. Control of vesicle fusion by a tyrosine phosphatase. Nat Cell Biol. 2004 Sep;6(9):831–839. PubMed PMID: 15322554. DOI:https://doi.org/10.1038/ncb1164
   Google Scholar
• Wang X, Huynh H, Gjorloff-Wingren A, et al. Enlargement of secretory vesicles by protein tyrosine phosphatase PTP-MEG2 in rat basophilic leukemia mast cells and Jurkat T cells. J Immunol. 2002 May 1;168(9):4612–4619. PubMed PMID: 11971009.
   PubMed Web of Science ®Google Scholar
• Wang Y, Vachon E, Zhang J, et al. Tyrosine phosphatase MEG2 modulates murine development and platelet and lymphocyte activation through secretory vesicle function. J Exp Med. 2005 Dec 5;202(11):1587–1597. PubMed PMID: 16330817; PubMed Central PMCID: PMCPMC2213338.
   PubMed Web of Science ®Google Scholar
• Yuan T, Wang Y, Zhao ZJ, et al. Protein-tyrosine phosphatase PTPN9 negatively regulates ErbB2 and epidermal growth factor receptor signaling in breast cancer cells. J Biol Chem. 2010 May 14;285(20):14861–14870. PubMed PMID: 20335174; PubMed Central PMCID: PMCPMC2865303.
   PubMed Web of Science ®Google Scholar
• Cho CY, Koo SH, Wang Y, et al. Identification of the tyrosine phosphatase PTP-MEG2 as an antagonist of hepatic insulin signaling. Cell Metab. 2006 May;3(5):367–378. PubMed PMID: 16679294. DOI:https://doi.org/10.1016/j.cmet.2006.03.006
   Google Scholar
• Wang Y, Li L, Hou C, et al. SNARE-mediated membrane fusion in autophagy. Semin Cell Dev Biol. 2016 Dec;60:97–104. PubMed PMID: 27422330; PubMed Central PMCID: PMCPMC5161566.
   PubMed Web of Science ®Google Scholar
• Rusten TE, Lindmo K, Juhasz G, et al. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell. 2004 Aug;7(2):179–192. PubMed PMID: 15296715. DOI:https://doi.org/10.1016/j.devcel.2004.07.005
   Google Scholar
• Vietri M, Radulovic M, Stenmark H. The many functions of ESCRTs. Nat Rev Mol Cell Biol. 2019 Nov 8. PubMed PMID: 31705132. DOI:https://doi.org/10.1038/s41580-019-0177-4
   Google Scholar
• Nezis IP, Shravage BV, Sagona AP, et al. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J Cell Biol. 2010 Aug 23;190(4):523–531. PubMed PMID: 20713604; PubMed Central PMCID: PMCPMC2928014.
   PubMed Web of Science ®Google Scholar
• Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013 Dec;14(12):759–774. PubMed PMID: 24201109.
   PubMed Web of Science ®Google Scholar
• Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008 Aug 25;182(4):685–701. PubMed PMID: 18725538.
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HE, et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell. 2014 Jul 17;55(2):238–252. PubMed PMID: 24954904; PubMed Central PMCID: PMCPMC4104028.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012 Dec 7;151(6):1256–1269. PubMed PMID: 23217709.
   PubMed Web of Science ®Google Scholar
• Li J, Chen Z, Stang MT, et al. Transiently expressed ATG16L1 inhibits autophagosome biogenesis and aberrantly targets RAB11-positive recycling endosomes. Autophagy. 2017 Feb;13(2):345–358. PubMed PMID: 27875067; PubMed Central PMCID: PMCPMC5724932.
   PubMed Web of Science ®Google Scholar
• Puri C, Renna M, Bento CF, et al. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell. 2013 Sep 12;154(6):1285–1299. PubMed PMID: 24034251; PubMed Central PMCID: PMCPMC3791395.
   PubMed Web of Science ®Google Scholar
• Flint AJ, Tiganis T, Barford D, et al. Development of “substrate-trapping” mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1680–1685. PubMed PMID: 9050838; PubMed Central PMCID: PMCPMC19976.
   PubMed Web of Science ®Google Scholar
• Hao Q, Samten B, Ji HL, et al. Tyrosine phosphatase PTP-MEG2 negatively regulates vascular endothelial growth factor receptor signaling and function in endothelial cells. Am J Physiol Cell Physiol. 2012 Sep 1;303(5):C548–53. PubMed PMID: 22763125; PubMed Central PMCID: PMCPMC3468344.
   PubMed Web of Science ®Google Scholar
• Burgo A, Casano AM, Kuster A, et al. Increased activity of the vesicular soluble N-ethylmaleimide-sensitive factor attachment protein receptor TI-VAMP/VAMP7 by tyrosine phosphorylation in the Longin domain. J Biol Chem. 2013 Apr 26;288(17):11960–11972. PubMed PMID: 23471971; PubMed Central PMCID: PMCPMC3636883.
   PubMed Web of Science ®Google Scholar
• Emperador-Melero J, Toonen RF, Verhage M. Vti proteins: beyond endolysosomal trafficking. Neuroscience. 2019 Nov 10;420:32–40. PubMed PMID: 30471354.
   PubMed Web of Science ®Google Scholar
• Furuta N, Fujita N, Noda T, et al. Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Mol Biol Cell. 2010 Mar 15;21(6):1001–1010. PubMed PMID: 20089838; PubMed Central PMCID: PMCPMC2836953.
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007 Sep-Oct;3(5):452–460. PubMed PMID: 17534139.
   PubMed Web of Science ®Google Scholar
• Abada A, Levin-Zaidman S, Porat Z, et al. SNARE priming is essential for maturation of autophagosomes but not for their formation. Proc Natl Acad Sci U S A. 2017 Nov 28;114(48):12749–12754. PubMed PMID: 29138318; PubMed Central PMCID: PMCPMC5715740.
   PubMed Web of Science ®Google Scholar
• Menzies FM, Fleming A, Caricasole A, et al. Autophagy and neurodegeneration: pathogenic Mechanisms and therapeutic opportunities. Neuron. 2017 Mar 8;93(5):1015–1034. PubMed PMID: 28279350.
   PubMed Web of Science ®Google Scholar
• Fujikake N, Shin M, Shimizu S. Association between autophagy and neurodegenerative diseases. Front Neurosci. 2018;12:255. PubMed PMID: 29872373; PubMed Central PMCID: PMCPMC5972210.
   PubMed Web of Science ®Google Scholar
• Sang TK, Li C, Liu W, et al. Inactivation of Drosophila Apaf-1 related killer suppresses formation of polyglutamine aggregates and blocks polyglutamine pathogenesis. Hum Mol Genet. 2005 Feb 1;14(3):357–372. PubMed PMID: 15590702.
   PubMed Web of Science ®Google Scholar
• Charlton-Perkins M, Cook TA. Building a fly eye: terminal differentiation events of the retina, corneal lens, and pigmented epithelia. Curr Top Dev Biol. 2010;93:129–173. PubMed PMID: 20959165; PubMed Central PMCID: PMCPMC5534335.
   PubMed Web of Science ®Google Scholar
• Zhao YG, Zhang H. Autophagosome maturation: an epic journey from the ER to lysosomes. J Cell Biol. 2019 Mar 4;218(3):757–770. PubMed PMID: 30578282; PubMed Central PMCID: PMCPMC6400552.
   PubMed Web of Science ®Google Scholar
• Guo B, Liang Q, Li L, et al. O-GlcNAc-modification of SNAP-29 regulates autophagosome maturation. Nat Cell Biol. 2014 Dec;16(12):1215–1226. PubMed PMID: 25419848.
   PubMed Web of Science ®Google Scholar
• Malmersjo S, Di Palma S, Diao J, et al. Phosphorylation of residues inside the SNARE complex suppresses secretory vesicle fusion. Embo J. 2016 Aug 15;35(16):1810–1821. PubMed PMID: 27402227; PubMed Central PMCID: PMCPMC5010044.
   PubMed Web of Science ®Google Scholar
• Laidlaw KME, Livingstone R, Al-Tobi M, et al. SNARE phosphorylation: a control mechanism for insulin-stimulated glucose transport and other regulated exocytic events. Biochem Soc Trans. 2017 Dec 15;45(6):1271–1277. PubMed PMID: 29101310.
   PubMed Web of Science ®Google Scholar
• Kumar S, Gu Y, Abudu YP, et al. Phosphorylation of syntaxin 17 by TBK1 controls autophagy initiation. Dev Cell. 2019 Apr 8;49(1):130–144e6. PubMed PMID: 30827897.
   PubMed Web of Science ®Google Scholar
• Nozawa T, Minowa-Nozawa A, Aikawa C, et al. The STX6-VTI1B-VAMP3 complex facilitates xenophagy by regulating the fusion between recycling endosomes and autophagosomes. Autophagy. 2017 Jan 2;13(1):57–69. PubMed PMID: 27791468; PubMed Central PMCID: PMCPMC5240839.
   PubMed Web of Science ®Google Scholar
• Pohl C, Dikic I. Cellular quality control by the ubiquitin-proteasome system and autophagy. Science. 2019 Nov 15;366(6467):818–822. PubMed PMID: 31727826.
   PubMed Web of Science ®Google Scholar
• Krench M, Littleton JT. Neurotoxicity pathways in Drosophila models of the polyglutamine disorders. Curr Top Dev Biol. 2017;121:201–223. PubMed PMID: 28057300.
   PubMed Web of Science ®Google Scholar
• Chen DY, Li MY, Wu SY, et al. The Bro1-domain-containing protein Myopic/HDPTP coordinates with Rab4 to regulate cell adhesion and migration. J Cell Sci. 2012 Oct 15;125(Pt 20):4841–4852. PubMed PMID: 22825871.
   PubMed Web of Science ®Google Scholar
• Chen SF, Kang ML, Chen YC, et al. Autophagy-related gene 7 is downstream of heat shock protein 27 in the regulation of eye morphology, polyglutamine toxicity, and lifespan in Drosophila. J Biomed Sci. 2012 May 23;19:52. PubMed PMID: 22621211; PubMed Central PMCID: PMCPMC3483682.
   PubMed Web of Science ®Google Scholar
• Tang HW, Liao HM, Peng WH, et al. Atg9 interacts with dTRAF2/TRAF6 to regulate oxidative stress-induced JNK activation and autophagy induction. Dev Cell. 2013 Dec 9;27(5):489–503. PubMed PMID: 24268699.
   PubMed Web of Science ®Google Scholar
• Barysch SV, Jahn R, Rizzoli SO. A fluorescence-based in vitro assay for investigating early endosome dynamics. Nat Protoc. 2010 Jun;5(6):1127–1137. PubMed PMID: 20539288.
   PubMed Web of Science ®Google Scholar
• Moreau K, Puri C, Rubinsztein DC. Methods to analyze SNARE-dependent vesicular fusion events that regulate autophagosome biogenesis. Methods. 2015 Mar;75:19–24. PubMed PMID: 25461811; PubMed Central PMCID: PMC4358838.
   PubMed Web of Science ®Google Scholar