WIPI1 promotes fission of endosomal transport carriers and formation of autophagosomes through distinct mechanisms

References

• Ohsumi Y. Historical landmarks of autophagy research. Cell Res. 2014;24:9–23.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi C, Inoue K, et al. Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG. Mol Biol Cell. 2008;19:5360–5372.
   PubMed Web of Science ®Google Scholar
• Vicinanza M, Korolchuk VI, Ashkenazi A, et al. PI(5)P regulates autophagosome biogenesis. Mol Cell. 2015;57:219–234.
   PubMed Web of Science ®Google Scholar
• Kihara A, Noda T, Ishihara N, et al. Two Distinct Vps34 phosphatidylinositol 3–kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol. 2001;152:519–530.
   PubMed Web of Science ®Google Scholar
• Petiot A, Ogier-Denis E, Blommaart EF, et al. Distinct classes of phosphatidylinositol 3ʹ-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem. 2000;275:992–998.
   PubMed Web of Science ®Google Scholar
• Rusten TE, Vaccari T, Lindmo K, et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol. 2007;17:1817–1825.
   PubMed Web of Science ®Google Scholar
• De Lartigue J, Polson H, Feldman M, et al. PIKfyve regulation of endosome-linked pathways. Traffic. 2009;10:883–893.
   PubMed Web of Science ®Google Scholar
• Ferguson CJ, Lenk GM, Meisler MH. Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum Mol Genet. 2009;18:4868–4878.
   PubMed Web of Science ®Google Scholar
• Sharma G, Guardia CM, Roy A, et al. A family of PIKFYVE inhibitors with therapeutic potential against autophagy-dependent cancer cells disrupt multiple events in lysosome homeostasis. Autophagy. 2019;15:1694–1718.
   PubMed Web of Science ®Google Scholar
• Dove SK, Piper RC, McEwen RK, et al. Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. Embo J. 2004;23:1922–1933.
   PubMed Web of Science ®Google Scholar
• Proikas-Cezanne T, Takacs Z, Dönnes P, et al. WIPI proteins: essential PtdIns3P effectors at the nascent autophagosome. J Cell Sci. 2015;128:207–217.
   PubMed Web of Science ®Google Scholar
• Proikas-Cezanne T, Waddell S, Gaugel A, et al. WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene. 2004;23:9314–9325.
   PubMed Web of Science ®Google Scholar
• Polson HEJ, De Lartigue J, Rigden DJ, et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy. 2010;6:506–522.
   PubMed Web of Science ®Google Scholar
• Barth H, Meiling-Wesse K, Epple UD, et al. Autophagy and the cytoplasm to vacuole targeting pathway both require Aut10p. FEBS Lett. 2001;508:23–28.
   PubMed Web of Science ®Google Scholar
• Guan J, Stromhaug PE, George MD, et al. Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol Biol Cell. 2001;12:3821–3838.
   PubMed Web of Science ®Google Scholar
• Obara K, Sekito T, Niimi K, et al. The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem. 2008;283:23972–23980.
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HEJ, et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell. 2014;55:238–252.
   PubMed Web of Science ®Google Scholar
• Bakula D, Müller AJ, Zuleger T, et al. WIPI3 and WIPI4 β-propellers are scaffolds for LKB1-AMPK-TSC signalling circuits in the control of autophagy. Nat Commun. 2017;8:15637.
   PubMed Web of Science ®Google Scholar
• Liao -C-C, Ho M-Y, Liang S-M, et al. Recombinant protein rVP1 upregulates BECN1-independent autophagy, MAPK1/3 phosphorylation and MMP9 activity via WIPI1/WIPI2 to promote macrophage migration. Autophagy. 2013;9:5–19.
   PubMed Web of Science ®Google Scholar
• Chowdhury S, Otomo C, Leitner A, et al. Insights into autophagosome biogenesis from structural and biochemical analyses of the ATG2A-WIPI4 complex. Proc Natl Acad Sci USA. 2018;58:201811874.
   Google Scholar
• Stanga D, Zhao Q, Milev MP, et al. TRAPPC11 functions in autophagy by recruiting ATG2B-WIPI4/WDR45 to preautophagosomal membranes. Traffic. 2019;20:325–345.
   PubMed Web of Science ®Google Scholar
• Otomo T, Chowdhury S, Lander GC. The rod-shaped ATG2A-WIPI4 complex tethers membranes in vitro. Contact (Thousand Oaks). 2018;1:251525641881993.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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 USA. 2012;109(30):E2042–9.
   PubMed Web of Science ®Google Scholar
• Liang R, Ren J, Zhang Y, et al. Structural conservation of the two phosphoinositide-binding sites in WIPI proteins. J Mol Biol. 2019;431:1494–1505.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jeffries TR, Dove SK, Michell RH, et al. PtdIns-specific MPR pathway association of a novel WD40 repeat protein, WIPI49. Mol Biol Cell. 2004;15:2652–2663.
   PubMed Web of Science ®Google Scholar
• Orsi A, Razi M, Dooley HC, et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell. 2012;23:1860–1873.
   PubMed Web of Science ®Google Scholar
• Puri C, Vicinanza M, Ashkenazi A, et al. The RAB11A-positive compartment is a primary platform for autophagosome assembly mediated by WIPI2 recognition of PI3P-RAB11A. Dev Cell. 2018;45:114–118.
   PubMed Web of Science ®Google Scholar
• Fraser J, Simpson J, Fontana R, et al. Targeting of early endosomes by autophagy facilitates EGFR recycling and signalling. EMBO Rep. 2019;20:e47734.
   PubMed Web of Science ®Google Scholar
• Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol. 1996;12:575–625.
   PubMed Web of Science ®Google Scholar
• Anderson RG, Brown MS, Beisiegel U, et al. Surface distribution and recycling of the low density lipoprotein receptor as visualized with antireceptor antibodies. J Cell Biol. 1982;93:523–531.
   PubMed Web of Science ®Google Scholar
• Dautry-Varsat A, Ciechanover A, Lodish HF. pH and the recycling of transferrin during receptor-mediated endocytosis. PNAS. 1983;80:2258–2262.
   PubMed Web of Science ®Google Scholar
• Hopkins CR. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell. 1983;35:321–330.
   PubMed Web of Science ®Google Scholar
• Umeda A, Fujita H, Kuronita T, et al. Distribution and trafficking of MPR300 is normal in cells with cholesterol accumulated in late endocytic compartments: evidence for early endosome-to-TGN trafficking of MPR300. J Lipid Res. 2003;44:1821–1832.
   PubMed Web of Science ®Google Scholar
• Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell. 2001;106:145–155.
   PubMed Web of Science ®Google Scholar
• Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol. 2004;5:121–132.
   PubMed Web of Science ®Google Scholar
• Luzio JP, Hackmann Y, Dieckmann NMG, et al. The biogenesis of lysosomes and lysosome-related organelles. Cold Spring Harb Perspect Biol. 2014;6: a016840–0.
   PubMed Web of Science ®Google Scholar
• Cullen PJ, Steinberg F. To degrade or not to degrade: mechanisms and significance of endocytic recycling. Nat Rev Mol Cell Biol. 2018;19:679–696.
   PubMed Web of Science ®Google Scholar
• Ma M, Burd CG. Retrograde trafficking and plasma membrane recycling pathways of the budding yeast Saccharomyces cerevisiae. Traffic. 2019;21:45–59:tra.12693.
   PubMed Web of Science ®Google Scholar
• Seaman MNJ. Back from the brink: retrieval of membrane proteins from terminal compartments: unexpected pathways for membrane protein retrieval from vacuoles and endolysosomes. BioEssays. 2019;41:e1800146.
   PubMed Web of Science ®Google Scholar
• Chen K-E, Healy MD, Collins BM. Towards a molecular understanding of endosomal trafficking by Retromer and Retriever. Traffic. 2019;20:tra.12649.
   Web of Science ®Google Scholar
• Derivery E, Sousa C, Gautier JJ, et al. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell. 2009;17:712–723.
   PubMed Web of Science ®Google Scholar
• Gomez TS, Billadeau DD. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell. 2009;17:699–711.
   PubMed Web of Science ®Google Scholar
• Phillips-Krawczak CA, Singla A, Starokadomskyy P, et al. COMMD1 is linked to the WASH complex and regulates endosomal trafficking of the copper transporter ATP7A. Mol Biol Cell. 2015;26:91–103.
   PubMed Web of Science ®Google Scholar
• Rojas R, Kametaka S, Haft CR, et al. Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol. 2007;27:1112–1124.
   PubMed Web of Science ®Google Scholar
• Temkin P, Lauffer B, Jäger S, et al. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol. 2011;13:715–721.
   PubMed Web of Science ®Google Scholar
• Lucas M, Gershlick DC, Vidaurrazaga A, et al. Structural Mechanism for Cargo Recognition by the Retromer Complex. Cell. 2016;167:1623–1635.e14.
   PubMed Web of Science ®Google Scholar
• Hierro A, Rojas AL, Rojas R, et al. Functional architecture of the retromer cargo-recognition complex. Nature. 2007;449:1063–1067.
   PubMed Web of Science ®Google Scholar
• Kovtun O, Leneva N, Bykov YS, et al. Structure of the membrane-assembled retromer coat determined by cryo-electron tomography. Nature. 2018;561:561–564.
   PubMed Web of Science ®Google Scholar
• Bar-Ziv R, Tlusty T, Moses E, et al. Pearling in cells: a clue to understanding cell shape. PNAS. 1999;96:10140–10145.
   PubMed Web of Science ®Google Scholar
• Markin VS, Tanelian DL, Jersild RA, et al. Biomechanics of stretch-induced beading. Biophys J. 1999;76:2852–2860.
   PubMed Web of Science ®Google Scholar
• Simunovic M, Manneville J-B, Renard H-F, et al. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell. 2017;170:172–184.e11.
   PubMed Web of Science ®Google Scholar
• Antonny B, Burd C, De Camilli P, et al. Membrane fission by dynamin: what we know and what we need to know. Embo J. 2016;35:e201694613.
   Web of Science ®Google Scholar
• Gopaldass N, Fauvet B, Lashuel H, et al. Membrane scission driven by the PROPPIN Atg18. Embo J. 2017;36:3274–3291.
   PubMed Web of Science ®Google Scholar
• Zieger M, Mayer A. Yeast vacuoles fragment in an asymmetrical two-phase process with distinct protein requirements. Mol Biol Cell. 2012;23:3438–3449.
   PubMed Web of Science ®Google Scholar
• Busse RA, Scacioc A, Krick R, et al. Characterization of PROPPIN-Phosphoinositide Binding and Role of Loop 6CD in PROPPIN-Membrane Binding. Biophys J. 2015;108:2223–2234.
   PubMed Web of Science ®Google Scholar
• Tamura N, Oku M, Ito M, et al. Atg18 phosphoregulation controls organellar dynamics by modulating its phosphoinositide-binding activity. J Cell Biol. 2013;202:685–698.
   PubMed Web of Science ®Google Scholar
• Rutherford AC, Traer C, Wassmer T, et al. The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J Cell Sci. 2006;119:3944–3957.
   PubMed Web of Science ®Google Scholar
• Schink KO, Raiborg C, Stenmark H. Phosphatidylinositol 3-phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. BioEssays. 2013;35:900–912.
   PubMed Web of Science ®Google Scholar
• McCartney AJ, Zhang Y, Weisman LS. Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays. 2014;36:52–64.
   PubMed Web of Science ®Google Scholar
• Krick R, Tolstrup J, Appelles A, et al. The relevance of the phosphatidylinositolphosphat-binding motif FRRGT of Atg18 and Atg21 for the Cvt pathway and autophagy. FEBS Lett. 2006;580:4632–4638.
   PubMed Web of Science ®Google Scholar
• Gaugel A, Bakula D, Hoffmann A, et al. Defining regulatory and phosphoinositide-binding sites in the human WIPI-1 β-propeller responsible for autophagosomal membrane localization downstream of mTORC1 inhibition. J Mol Signal. 2012;7:16.
   PubMedGoogle Scholar
• Hasegawa J, Strunk BS, Weisman LS. PI5P and PI(3,5)P2: minor, but Essential Phosphoinositides. Cell Struct Funct. 2017;42:49–60.
   PubMed Web of Science ®Google Scholar
• Proikas-Cezanne T, Ruckerbauer S, Stierhof Y-D, et al. Human WIPI-1 puncta-formation: a novel assay to assess mammalian autophagy. FEBS Lett. 2007;581:3396–3404.
   PubMed Web of Science ®Google Scholar
• Hopkins CR, Trowbridge IS. Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J Cell Biol. 1983;97:508–521.
   PubMed Web of Science ®Google Scholar
• Beguinot L, Lyall RM, Willingham MC, et al. Down-regulation of the epidermal growth factor receptor in KB cells is due to receptor internalization and subsequent degradation in lysosomes. PNAS. 1984;81:2384–2388.
   PubMed Web of Science ®Google Scholar
• Mallard F, Antony C, Tenza D, et al. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J Cell Biol. 1998;143:973–990.
   PubMed Web of Science ®Google Scholar
• Kupcho K, Somberg R, Bulleit B, et al. A homogeneous, nonradioactive high-throughput fluorogenic protein kinase assay. Anal Biochem. 2003;317:210–217.
   PubMed Web of Science ®Google Scholar
• Chi RJ, Harrison MS, Burd CG. Biogenesis of endosome-derived transport carriers. Cell Mol Life Sci. 2015;72:3441–3455.
   PubMed Web of Science ®Google Scholar
• Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6: a022616–6.
   PubMed Web of Science ®Google Scholar
• Pfeffer SR. Rab GTPase regulation of membrane identity. Curr Opin Cell Biol. 2013;25:414–419.
   PubMed Web of Science ®Google Scholar
• Gillooly DJ, Morrow IC, Lindsay M, et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. Embo J. 2000;19:4577–4588.
   PubMed Web of Science ®Google Scholar
• Li X, Wang X, Zhang X, et al. Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:21165–21170.
   PubMed Web of Science ®Google Scholar
• Wallroth A, Haucke V. Phosphoinositide conversion in endocytosis and the endolysosomal system. J Biol Chem. 2018;293:1526–1535.
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19:5720–5728.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. 3rd Ed. Autophagy. 2016; Vol. 12, p. 1–222
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Boucrot E, Pick A, Camdere G, et al. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent bar domains. Cell. 2012;149:124–136.
   PubMed Web of Science ®Google Scholar
• Velikkakath AKG, Nishimura T, Oita E, et al. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell. 2012;23:896–909.
   PubMed Web of Science ®Google Scholar
• Maeda S, Otomo C, Otomo T. The autophagic membrane tether ATG2A transfers lipids between membranes. elife. 2019;8:E3179.
   Web of Science ®Google Scholar
• Osawa T, Kotani T, Kawaoka T, et al. Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat Struct Mol Biol. 2019;26:281–288.
   PubMed Web of Science ®Google Scholar
• Wang Y, Pennock S, Chen X, et al. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol Cell Biol. 2002;22:7279–7290.
   PubMed Web of Science ®Google Scholar
• Schartl M, Wilde B, Laisney JAGC, et al. A mutated EGFR is sufficient to induce malignant melanoma with genetic background-dependent histopathologies. J Invest Dermatol. 2010;130:249–258.
   PubMed Web of Science ®Google Scholar
• Girotti MR, Pedersen M, Sanchez-Laorden B, et al. Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov. 2013;3:158–167.
   PubMed Web of Science ®Google Scholar
• Bardeesy N, Kim M, Xu J, et al. Role of epidermal growth factor receptor signaling in RAS-driven melanoma. Mol Cell Biol. 2005;25:4176–4188.
   PubMed Web of Science ®Google Scholar
• Cendrowski J, Mamińska A, Miaczynska M. Endocytic regulation of cytokine receptor signaling. Cytokine Growth Factor Rev. 2016;32:63–73.
   PubMed Web of Science ®Google Scholar
• Simunovic M, Voth GA, Callan-Jones A, et al. When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol. 2015;25:780–792.
   PubMed Web of Science ®Google Scholar
• Daumke O, Roux A, Haucke V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell. 2014;156:882–892.
   PubMed Web of Science ®Google Scholar
• Chi RJ, Liu J, West M, et al. Fission of SNX-BAR-coated endosomal retrograde transport carriers is promoted by the dynamin-related protein Vps1. J Cell Biol. 2014;204:793–806.
   PubMed Web of Science ®Google Scholar
• Arlt H, Reggiori F, Ungermann C. Retromer and the dynamin Vps1 cooperate in the retrieval of transmembrane proteins from vacuoles. J Cell Sci. 2015;128:645–655.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Peters C, Baars TL, Buhler S, et al. Mutual control of membrane fission and fusion proteins. Cell. 2004;119:667–678.
   PubMed Web of Science ®Google Scholar
• Alpadi K, Kulkarni A, Namjoshi S, et al. Dynamin-SNARE interactions control trans-SNARE formation in intracellular membrane fusion. Nat Commun. 2013;4:1704.
   PubMed Web of Science ®Google Scholar
• Michaillat L, Mayer A. Identification of genes affecting vacuole membrane fragmentation in Saccharomyces cerevisiae. PLoS ONE. 2013;8:e54160.
   PubMed Web of Science ®Google Scholar
• Michaillat L, Baars TL, Mayer A. Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol Biol Cell. 2012;23:881–895.
   PubMed Web of Science ®Google Scholar
• Daumke O, Lundmark R, Vallis Y, et al. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature. 2007;449:923–927.
   PubMed Web of Science ®Google Scholar
• Cai B, Xie S, Caplan S, et al. GRAF1 forms a complex with MICAL-L1 and EHD1 to cooperate in tubular recycling endosome vesiculation. Front Cell Dev Biol. 2014;2:22.
   PubMed Web of Science ®Google Scholar
• Deo R, Kushwah MS, Kamerkar SC, et al. ATP-dependent membrane remodeling links EHD1 functions to endocytic recycling. Nat Commun. 2018;9:5187.
   PubMed Web of Science ®Google Scholar
• Cai B, Caplan S, Naslavsky N. cPLA2α and EHD1 interact and regulate the vesiculation of cholesterol-rich, GPI-anchored, protein-containing endosomes. Mol Biol Cell. 2012;23:1874–1888.
   PubMed Web of Science ®Google Scholar
• Zhang J, Reiling C, Reinecke JB, et al. Rabankyrin-5 interacts with EHD1 and Vps26 to regulate endocytic trafficking and retromer function. Traffic. 2012;13:745–757.
   PubMed Web of Science ®Google Scholar
• McKenzie JE, Raisley B, Zhou X, et al. Retromer guides STxB and CD8-M6PR from early to recycling endosomes, EHD1 guides STxB from recycling endosome to Golgi. Traffic. 2012;13:1140–1159.
   PubMed Web of Science ®Google Scholar
• Boucrot E, Ferreira APA, Almeida-Souza L, et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 2015;517:460–465.
   PubMed Web of Science ®Google Scholar
• Renard H-F, Simunovic M, Lemière J, et al. Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature. 2015;517:493–496.
   PubMed Web of Science ®Google Scholar
• Riezman H, Munn A, Geli MI, et al. Actin-, myosin- and ubiquitin-dependent endocytosis. Experientia. 1996;52:1033–1041.
   PubMedGoogle Scholar
• Römer W, Pontani -L-L, Sorre B, et al. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell. 2010;140:540–553.
   PubMed Web of Science ®Google Scholar
• Simonetti B, Cullen PJ. Actin-dependent endosomal receptor recycling. Curr Opin Cell Biol. 2019;56:22–33.
   PubMed Web of Science ®Google Scholar
• Suzuki SW, Emr SD. Membrane protein recycling from the vacuole/lysosome membrane. J Cell Biol. 2018;217(5):1623–1632. jcb.201709162.
   Web of Science ®Google Scholar
• Stromhaug PE, 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.
   PubMed Web of Science ®Google Scholar
• Colquhoun D. Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br J Pharmacol. 1998;125:924–947.
   PubMed Web of Science ®Google Scholar
• Shalem O, Sanjana NE, Hartenian E, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 2014;343(6166):84–87. .
   PubMed Web of Science ®Google Scholar
• Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11:783–784.
   PubMed Web of Science ®Google Scholar
• Bagnis C, Bailly P, Chapel-Fernandes S. Using an EGFPmeter to evaluate the lentiviral vector production: tricks and traps. Methods Mol Biol. 2009;515:151–163.
   PubMedGoogle Scholar
• Vicinanza M, Di Campli A, Polishchuk E, et al. OCRL controls trafficking through early endosomes via PtdIns4,5P2-dependent regulation of endosomal actin. Embo J. 2011;30(24):4970–4985.
   PubMed Web of Science ®Google Scholar
• Manders EMM, Verbeek FJ, Aten JA. Measurement of co-localization of objects in dual-colour confocal images. J Microsc. 2011;169:375–382.
   Google Scholar
• Canny J. A computational approach to edge detection. IEEE Trans Pattern Anal Mach Intell. 1986;8:679–698.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–675.
   PubMed Web of Science ®Google Scholar
• Gautier R, Douguet D, Antonny B, et al. HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics. 2008;24:2101–2102.
   PubMed Web of Science ®Google Scholar