3,279
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Vacuole fragmentation depends on a novel Atg18-containing retromer-complex

, , , , , & show all
Pages 278-295 | Received 21 Jul 2021, Accepted 27 Apr 2022, Published online: 15 May 2022

References

  • Wen X, Yang Y, Klionsky DJ. Moments in autophagy and disease: past and present. Mol Aspects Med. 2021:100966.
  • Gomez-Sanchez R, Tooze SA, Reggiori F. Membrane supply and remodeling during autophagosome biogenesis. Curr Opin Cell Biol. 2021;71:112–119.
  • Hollenstein DM, Kraft C. Autophagosomes are formed at a distinct cellular structure. Curr Opin Cell Biol. 2020;65:50–57.
  • Matoba K, Noda NN. Structural catalog of core Atg proteins opens new era of autophagy research. J Biochem. 2021;169:517–525.
  • Juris L, Montino M, Rube P, et al. PI3P binding by Atg21 organises Atg8 lipidation. EMBO J. 2015;34:955–973.
  • Munzel L, Neumann P, Otto FB, et al. Atg21 organizes Atg8 lipidation at the contact of the vacuole with the phagophore. Autophagy. 2020;14:1–21.
  • Hollenstein DM, Gomez-Sanchez R, Ciftci A, et al. Vac8 spatially confines autophagosome formation at the vacuole in S. cerevisiae. J Cell Sci. 2019;132:jcs235002.
  • Gatica D, Wen X, Cheong H, et al. Vac8 determines phagophore assembly site vacuolar localization during nitrogen starvation-induced autophagy. Autophagy. 2021;17(7):1636–1648.
  • Sawa-Makarska J, Baumann V, Coudevylle N, et al. Reconstitution of autophagosome nucleation defines Atg9 vesicles as seeds for membrane formation. Science (New York, NY). 2020;369:eaaz7714–12.
  • Harada K, Kotani T, Kirisako H, et al. Two distinct mechanisms target the autophagy-related E3 complex to the pre-autophagosomal structure. eLife. 2019;8:685.
  • Meiling-Wesse K, Barth H, Voss C, et al. Atg21 is required for effective recruitment of Atg8 to the preautophagosomal structure during the Cvt pathway. J Biol Chem. 2004;279:37741–37750.
  • Stromhaug P, Reggiori F, Guan J, et al. Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell. 2004;15:3553–3566.
  • Noda NN. Atg2 and Atg9: intermembrane and interleaflet lipid transporters driving autophagy. biochimica et biophysica acta molecular and cell biology of lipids. Biochimica Et Biophysica Acta. Molecular and Cell Biology of Lipids. 2021;1866:158956.
  • Yamamoto H, Kakuta S, Watanabe TM, et al. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol. 2012;198:219–233.
  • Lei Y, Tang D, Liao G, et al. The crystal structure of Atg18 reveals a new binding site for Atg2 in Saccharomyces cerevisiae. Cell Mol Life Sci. 2020;290: 1717–13.
  • Scacioc A, Schmidt C, Hofmann T, et al. Structure based biophysical characterization of the PROPPIN Atg18 shows Atg18 oligomerization upon membrane binding. Sci Rep. 2017;7:14008.
  • Krick R, Busse RA, Scacioc A, et al. Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a β-propeller protein family. Proc Natl Acad Sci U S A. 2012;109:E2042–9.
  • Baskaran S, Ragusa MJ, Boura E, et al. Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol Cell. 2012;47:339–348.
  • Watanabe Y, Kobayashi T, Yamamoto H, et al. Structure-based analyses reveal distinct binding sites for Atg2 and phosphoinositides in Atg18. J Biol Chem. 2012;287:31681–31690.
  • Nishimura T, Tooze SA. Emerging roles of ATG proteins and membrane lipids in autophagosome formation. Cell Discov. 2020;6: 32–18.
  • Krick R, Henke S, Tolstrup J, et al. Dissecting the localization and function of Atg18, Atg21 and Ygr223c. Autophagy. 2008;4:896–910.
  • Dove S, Piper R, McEwen R, et al. Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J. 2004;23:1922–1933.
  • Reggiori F, Tucker KA, Stromhaug PE, et al. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell. 2004;6:79–90.
  • Efe JA, Botelho RJ, Emr SD. Atg18 regulates organelle morphology and Fab1 kinase activity independent of its membrane recruitment by phosphatidylinositol 3,5-bisphosphate. Mol Biol Cell. 2007;18:4232–4244. DOI:10.1091/mbc.e07-04-0301
  • Jin N, Chow CY, Liu L, et al. VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3,5)P(2) in yeast and mouse. EMBO J. 2008;27:3221–3234.
  • Zieger M, Mayer A, Gruenberg JE. Yeast vacuoles fragment in an asymmetrical two-phase process with distinct protein requirements. Mol Biol Cell. 2012;23:3438–3449.
  • Gopaldass N, Fauvet B, Lashuel H, et al. Membrane scission driven by the PROPPIN Atg18. EMBO J. 2017;36:e201796859–18.
  • De Leo MG, Berger P, Mayer A. WIPI1 promotes fission of endosomal transport carriers and formation of autophagosomes through distinct mechanisms. Autophagy. 2021;17(11):3644–3670.
  • Roux KJ, Kim DI, Burke B. BioID: a Screen for Protein-Protein Interactions. Hoboken NJ USA: John Wiley & Sons, Inc; 2001.
  • Opitz N, Schmitt K, Hofer-Pretz V, et al. Capturing the Asc1p/receptor for activated C kinase 1 (RACK1) microenvironment at the head region of the 40S ribosome with quantitative BioID in Yeast. Mol Cell Proteomics. 2017;16:2199–2218.
  • Ma M, Burd CG. Retrograde trafficking and plasma membrane recycling pathways of the budding yeast Saccharomyces cerevisiae. Traffic. Vol. 21. Copenhagen, Denmark 2020.45–59
  • Seaman MNJ. The retromer complex: from genesis to revelations. Trends Biochem Sci. 2021;46:608–620.
  • Bean BDM, Davey M, Conibear E. Cargo selectivity of yeast sorting nexins. Traffic. 2017;18(2):110–122.
  • Efe JA, Botelho RJ, Emr SD. The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology. Curr Opin Cell Biol. 2005;17:402–408.
  • Meiling-Wesse K, Barth H, Thumm M. Ccz1p/Aut11p/Cvt16p is essential for autophagy and the cvt pathway. FEBS Lett. 2002;526:71–76.
  • Welter E, Thumm M, Krick R. Quantification of nonselective bulk autophagy in S. cerevisiae using Pgk1-GFP. Autophagy. 2010;6:794–797.
  • Müller J, Johnsson N. Split-ubiquitin and the split-protein sensors: chessman for the endgame. ChemBioChem. 2008;9:2029–2038.
  • Purushothaman LK, Arlt H, Kuhlee A, et al. Retromer-driven membrane tubulation separates endosomal recycling from Rab7/Ypt7-dependent fusion. Mol Biol Cell. 2017;28:783–791.
  • Liu Tt L, Gomez TS, Sackey BK, et al. Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol Biol Cell. 2012;23:2505–2515.
  • Balderhaar HJK, Arlt H, Ostrowicz C, et al. The Rab GTPase Ypt7 is linked to retromer-mediated receptor recycling and fusion at the yeast late endosome. J Cell Sci. 2010;123:4085–4094.
  • Popelka H, Damasio A, Hinshaw JE, et al. Structure and function of yeast Atg20, a sorting nexin that facilitates autophagy induction. Proc Natl Acad Sci U S A. 2017;114:E10112–E21.
  • Ma M, Kumar S, Purushothaman L, et al. Lipid trafficking by yeast Snx4 family SNX-BAR proteins promotes autophagy and vacuole membrane fusion. Mol Biol Cell. 2018;29:2190–2200.
  • Suzuki SW, Emr SD. Membrane protein recycling from the vacuole/lysosome membrane. J Cell Biol. 2018;256:jcb.201709162–15.
  • Segarra VA, Boettner DR, Lemmon SK. Atg27 tyrosine sorting motif is important for its trafficking and Atg9 localization. Traffic. 2015;16:365–378.
  • Ohashi Y, Munro S, Glick BS. Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol Biol Cell. 2010;21:3998–4008.
  • Shirahama-Noda K, Kira S, Yoshimori T, et al. TRAPPIII is responsible for vesicular transport from early endosomes to Golgi, facilitating Atg9 cycling in autophagy. J Cell Sci. 2013;126:4963–4973.
  • Ravussin A, Brech A, Tooze SA, et al. The phosphatidylinositol 3-phosphate-binding protein SNX4 controls ATG9A recycling and autophagy. J Cell Sci. 2021;134(3):jcs250670.
  • Zavodszky E, Seaman MNJ, Moreau K, et al. Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat Commun. 2014;5: 3828–16.
  • Tamura N, Oku M, Ito M, et al. Atg18 phosphoregulation controls organellar dynamics by modulating its phosphoinositide-binding activity. J Cell Biol. 2013;202(4):685–698.
  • Thumm M, Egner R, Koch B, et al. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 1994;349:275–280.
  • Janke C, Magiera M, Rathfelder N, et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast (Chichester. England). 2004;21:947–962.
  • Gueldener U, Heinisch J, Koehler GJ, et al. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 2002;30:e23.
  • Güldener U, Heck S, Fielder T, et al. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 1996;24:2519–2524.
  • Longtine M, McKenzie A, Demarini D, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast (Chichester. England). 1998;14:953–961.
  • Suzuki K, Kirisako T, Kamada Y, et al. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 2001;20:5971–5981.
  • Lang T, Reiche S, Straub M, et al. Autophagy and the cvt pathway both depend on AUT9. J Bacteriol. 2000;182:2125–2133.
  • Barth H, Thumm M. A genomic screen identifies AUT8 as a novel gene essential for autophagy in the yeast Saccharomyces cerevisiae. Gene. 2001;274:151–156.
  • Schmitt K, Valerius O. yRACK1/Asc1 proxiOMICs-Towards Illuminating Ships Passing in the Night. Cells. 2019;8:1384.
  • Wang X, Li X, Li Y. A modified coomassie brilliant blue staining method at nanogram sensitivity compatible with proteomic analysis. Biotechnol Lett. 2007;29:79–90.
  • Pink M, Verma N, Rettenmeier AW, et al. CBB staining protocol with higher sensitivity and mass spectrometric compatibility. Electrophoresis. 2010;31:593–598.
  • Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007;2:1896–1906.
  • Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682.