Epsin deficiency impairs endocytosis by stalling the actin-dependent invagination of endocytic clathrin-coated pits
Open accessAbstract
Epsin is an evolutionarily conserved endocytic clathrin adaptor whose most critical function(s) in clathrin coat dynamics remain(s) elusive. To elucidate such function(s), we generated embryonic fibroblasts from conditional epsin triple KO mice. Triple KO cells displayed a dramatic cell division defect. Additionally, a robust impairment in clathrin-mediated endocytosis was observed, with an accumulation of early and U-shaped pits. This defect correlated with a perturbation of the coupling between the clathrin coat and the actin cytoskeleton, which we confirmed in a cell-free assay of endocytosis. Our results indicate that a key evolutionary conserved function of epsin, in addition to other roles that include, as we show here, a low affinity interaction with SNAREs, is to help generate the force that leads to invagination and then fission of clathrin-coated pits.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Epsin1 has been implicated in endocytosis at synapses and can interact with both the plasma membrane and F-actin through its N-terminal ENTH domain and C-terminal tail, respectively.
“Epsin1 has been implicated in endocytosis at synapses71 and can interact with both the plasma membrane and F-actin through its N-terminal ENTH domain and C-terminal tail, respectively (Supplementary Fig. 7a)72.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [72]
Epsin1 interacts with other endocytic proteins such as Eps15 and Hip1R, both of which interact either directly or indirectly with membranes and actin.
“However, it is not clear whether Epsin1 is the sole organizer of F-actin at synapses, since it interacts with other endocytic proteins such as Eps15 and Hip1R72,88, both of which interact either directly or indirectly with membranes and actin.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [72]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Merrifield, C. J., Perrais, D., & Zenisek, D. (2005) · Cell · doi:10.1016/j.cell.2005.03.015 · Cited by 476 · cited 1× · see citing works
“DOI: 10.7554/eLife.03311 2 of 25 Research article As epsin binds ubiquitin and genetically interacts with enzymes of ubiquitin metabolism (Cadavid et al., 2000; Chen et al., 2002; Polo et al., 2002; Shih et al., 2002; Chen et al., 2003; Sigismund et al., 2005), it was proposed to function as a…”
BackgroundInfluentialChen, H., Slepnev, V. I., Di Fiore, P. P., & De Camilli, P. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.6.3257 · Cited by 138 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 72
- Aguilar RC Longhi SA Shaw JD Yeh LY Kim S Schon A Freire E Hsu A McCormick WK Watson HA Wendland B 2006 Epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins. Proceedings of the National Academy of Sciences of USA 103: 4116– 4121. doi: 10.1073/pnas.0510513103 PMC1449656 16537494 · DOI
- Aguilar RC Watson HA Wendland B 2003 The yeast Epsin Ent1 is recruited to membranes through multiple independent interactions. The Journal of Biological Chemistry 278: 10737– 10743. doi: 10.1074/jbc.M211622200 12529323 · DOI
- Badea TC Wang Y Nathans J 2003 A noninvasive genetic/pharmacologic strategy for visualizing cell morphology and clonal relationships in the mouse. The Journal of Neuroscience 23: 2314– 2322 12657690 PMC6742025
- Baggett JJ D'Aquino KE Wendland B 2003 The Sla2p talin domain plays a role in endocytosis in Saccharomyces cerevisiae. Genetics 165: 1661– 1674 14704157 PMC1462899
- Banerjee B Kestner CA Stukenberg PT 2014 EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B. The Journal of Cell Biology 204: 947– 963. doi: 10.1083/jcb.201307119 24616220 PMC3998792 · DOI
- Banfalvi G 2011 Overview of cell synchronization. In: Cell Cycle Synchronization Methods in Molecular Biology. Totowa, NJ: Humana Press Vol 761 p. 1– 23. doi: 10.1007/978-1-61779-182-6_1 21755438 · DOI
- Boucrot E Pick A Çamdere G Liska N Evergren E McMahon HT Kozlov MM 2012 Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149: 124– 136. doi: 10.1016/j.cell.2012.01.047 22464325 PMC3465558 · DOI
- Boulant S Kural C Zeeh JC Ubelmann F Kirchhausen T 2011 Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nature Cell Biology 13: 1124– 1131. doi: 10.1038/ncb2307 PMC3167020 21841790 · DOI
- Bradley SV Hyun TS Oravecz-Wilson KI Li L Waldorff EI Ermilov AN Goldstein SA Zhang CX Drubin DG Varela K Parlow A Dlugosz AA Ross TS 2007 Degenerative phenotypes caused by the combined deficiency of murine HIP1 and HIP1r are rescued by human HIP1. Human Molecular Genetics 16: 1279– 1292. doi: 10.1093/hmg/ddm076 17452370 · DOI
- Brady RJ Wen Y O’Halloran TJ 2008 The ENTH and C-terminal domains of Dictyostelium epsin cooperate to regulate the dynamic interaction with clathrin-coated pits. Journal of Cell Science 121: 3433– 3444. doi: 10.1242/jcs.032573 18827012 · DOI
- Brady RJ Damer CK Heuser JE O'Halloran TJ 2010 Regulation of Hip1r by epsin controls the temporal and spatial coupling of actin filaments to clathrin-coated pits. Journal of Cell Science 123: 3652– 3661. doi: 10.1242/jcs.066852 20923836 PMC2964106 · DOI
- Brett TJ Legendre-Guillemin V McPherson PS Fremont DH 2006 Structural definition of the F-actin-binding THATCH domain from HIP1R. Nature Structural & Molecular Biology 13: 121– 130. doi: 10.1038/nsmb1043 16415883 · DOI
- Cadavid AL Ginzel A Fischer JA 2000 The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127: 1727– 1736 10725248
- Chen H De Camilli P 2005 The association of epsin with ubiquitinated cargo along the endocytic pathway is negatively regulated by its interaction with clathrin. Proceedings of the National Academy of Sciences of USA 102: 2766– 2771. doi: 10.1073/pnas.0409719102 PMC549477 15701696 · DOI
- Chen H Fre S Slepnev VI Capua MR Takei K Butler MH Di Fiore PP De Camilli P 1998 Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394: 793– 797. doi: 10.1038/29555 9723620 · DOI
- Chen H Ko G Zatti A Di Giacomo G Liu L Raiteri E Perucco E Collesi C Min W Zeiss C De Camilli P Cremona O 2009 Embryonic arrest at midgestation and disruption of notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proceedings of the National Academy of Sciences of USA 106: 13838– 13843. doi: 10.1073/pnas.0907008106 PMC2728981 19666558 · DOI
- Chen H Polo S Di Fiore PP De Camilli P 2003 Rapid Ca2+-dependent decrease of protein ubiquitination at synapses. Proceedings of the National Academy of Sciences of USA 100: 14908– 14913. doi: 10.1073/pnas.2136625100 PMC299851 14657369 · DOI
- Chen X Zhang B Fischer JA 2002 A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of fat facets. Genes & Development 16: 289– 294. doi: 10.1101/gad.961502 11825870 PMC155328 · DOI
- Cheng J Grassart A Drubin DG 2012 Myosin 1E coordinates actin assembly and cargo trafficking during clathrin-mediated endocytosis. Molecular Biology of the Cell 23: 2891– 2904. doi: 10.1091/mbc.E11-04-0383 22675027 PMC3408416 · DOI
- Drake MT 2000 Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. Journal of Biological Chemistry 275: 6479– 6489. doi: 10.1074/jbc.275.9.6479 10692452 · DOI
- Engqvist-Goldstein AE Kessels MM Chopra VS Hayden MR Drubin DG 1999 An actin-binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles. The Journal of Cell Biology 147: 1503– 1518. doi: 10.1083/jcb.147.7.1503 10613908 PMC2174256 · DOI
- Engqvist-Goldstein AE Warren RA Kessels MM Keen JH Heuser J Drubin DG 2001 The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. The Journal of Cell Biology 154: 1209– 1223. doi: 10.1083/jcb.200106089 11564758 PMC2150824 · DOI
- Engqvist-Goldstein AE Zhang CX Carreno S Barroso C Heuser JE Drubin DG 2004 RNAi-mediated Hip1R silencing results in stable association between the endocytic machinery and the actin assembly machinery. Molecular Biology of the Cell 15: 1666– 1679. doi: 10.1091/mbc.E03-09-0639 14742709 PMC379265 · DOI
- Ferguson SM Brasnjo G Hayashi M Wölfel M Collesi C Giovedi S Raimondi A Gong L-W Ariel P Paradise S O'toole E Flavell R Cremona O Miesenböck G Ryan TA De Camilli P 2007 A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316: 570– 574. doi: 10.1126/science.1140621 17463283 · DOI
- Ferguson SM De Camilli P 2012 Dynamin, a membrane-remodelling GTPase. Nature Reviews Molecular Cell Biology 13: 75– 88. doi: 10.1038/nrm3266 PMC3519936 22233676 · DOI
- Ferguson SM Raimondi A Paradise S Shen H Mesaki K Ferguson A Destaing O Ko G Takasaki J Cremona O O Toole E De Camilli P 2009 Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Developmental Cell 17: 811– 822. doi: 10.1016/j.devcel.2009.11.005 20059951 PMC2861561 · DOI
- Ford MG Mills IG Peter BJ Vallis Y Praefcke GJ Evans PR McMahon HT 2002 Curvature of clathrin-coated pits driven by epsin. Nature 419: 361– 366. doi: 10.1038/nature01020 12353027 · DOI · Paper page
- Gottfried I Ehrlich M Ashery U 2010 The Sla2p/HIP1/HIP1R family: similar structure, similar function in endocytosis? Biochemical Society Transactions 38: 187– 191. doi: 10.1042/BST0380187 20074057 · DOI
- Hawryluk MJ Keyel PA Mishra SK Watkins SC Heuser JE Traub LM 2006 Epsin 1 is a Polyubiquitin‐Selective Clathrin‐Associated Sorting Protein. Traffic 7: 262– 281. doi: 10.1111/j.1600-0854.2006.00383.x 16497222 · DOI
- Hirst J Miller SE Taylor MJ Mollard von GF Robinson MS 2004 EpsinR is an adaptor for the SNARE protein Vti1b. Molecular Biology of the Cell 15: 5593– 5602. doi: 10.1091/mbc.E04-06-0468 15371541 PMC532037 · DOI
- Itoh T Erdmann KS Roux A Habermann B Werner H De Camilli P 2005 Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Developmental Cell 9: 791– 804. doi: 10.1016/j.devcel.2005.11.005 16326391 · DOI
- Itoh T Koshiba S Kigawa T Kikuchi A Yokoyama S Takenawa T 2001 Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291: 1047– 1051. doi: 10.1126/science.291.5506.1047 11161217 · DOI · Paper page
- Kaksonen M Sun Y Drubin DG 2003 A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115: 475– 487. doi: 10.1016/S0092-8674(03)00883-3 14622601 · DOI · Paper page
- Kaksonen M Toret CP Drubin DG 2006 Harnessing actin dynamics for clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biology 7: 404– 414. doi: 10.1038/nrm1940 16723976 · DOI · Paper page
- Kaur S Fielding AB Gassner G Carter NJ Royle SJ 2014 An unmet actin requirement explains the mitotic inhibition of clathrin-mediated endocytosis. eLife 3: e00829. doi: 10.7554/eLife.00829 24550251 PMC3924242 · DOI
- Ko G Paradise S Chen H Graham M Vecchi M Bianchi F Cremona O Di Fiore PP De Camilli P 2010 Selective high-level expression of epsin 3 in gastric parietal cells, where it is localized at endocytic sites of apical canaliculi. Proceedings of the National Academy of Sciences of USA 107: 21511– 21516. doi: 10.1073/pnas.1016390107 PMC3003030 21115825 · DOI
- Koo SJ Markovic S Puchkov D Mahrenholz CC Beceren-Braun F Maritzen T Dernedde J Volkmer R Oschkinat H Haucke V 2011 SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proceedings of the National Academy of Sciences of USA 108: 13540– 13545. doi: 10.1073/pnas.1107067108 PMC3158172 21808019 · DOI
- Le Clainche C Pauly BS Zhang CX Engqvist-Goldstein AEY Cunningham K Drubin DG 2007 A Hip1R–cortactin complex negatively regulates actin assembly associated with endocytosis. The EMBO Journal 26: 1199– 1210. doi: 10.1038/sj.emboj.7601576 17318189 PMC1817625 · DOI
- Legendre-Guillemin V Metzler M Charbonneau M Gan L Chopra V Philie J Hayden MR McPherson PS 2002 HIP1 and HIP12 display differential binding to F-actin, AP2, and clathrin. Identification of a novel interaction with clathrin light chain. The Journal of Biological Chemistry 277: 19897– 19904. doi: 10.1074/jbc.M112310200 11889126 · DOI
- Liu Z Zheng Y 2009 A requirement for epsin in mitotic membrane and spindle organization. The Journal of Cell Biology 186: 473– 480. doi: 10.1083/jcb.200902071 19704019 PMC2733747 · DOI
- Meloty-Kapella L Shergill B Kuon J Botvinick E Weinmaster G 2012 Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Developmental Cell 22: 1299– 1312. doi: 10.1016/j.devcel.2012.04.005 22658936 PMC3400432 · DOI
- Metzler M Legendre-Guillemin V Gan L Chopra V Kwok A McPherson PS Hayden MR 2001 HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. The Journal of Biological Chemistry 276: 39271– 39276. doi: 10.1074/jbc.C100401200 11517213 · DOI
- Miller SE Collins BM McCoy AJ Robinson MS Owen DJ 2007 A SNARE-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles. Nature 450: 570– 574. doi: 10.1038/nature06353 18033301 · DOI
- Miller SE Sahlender DA Graham SC Höning S Robinson MS Peden AA Owen DJ 2011 The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147: 1118– 1131. doi: 10.1016/j.cell.2011.10.038 22118466 PMC3267021 · DOI · Paper page
- Musse AA Meloty-Kapella L Weinmaster G 2012 Notch ligand endocytosis: mechanistic basis of signaling activity. Seminars in Cell & Developmental Biology 23: 429– 436. doi: 10.1016/j.semcdb.2012.01.011 22306180 PMC3507467 · DOI
- Overstreet E Chen X Wendland B Fischer JA 2003 Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Current Biology 13: 854– 860. doi: 10.1016/S0960-9822(03)00326-9 12747835 · DOI
- Pasula S Cai X Dong Y Messa M McManus J Chang B Liu X Zhu H Mansat RS Yoon S-J Hahn S Keeling J Saunders D Ko G Knight J Newton G Luscinskas F Sun X Towner R Lupu F Xia L Cremona O De Camilli P Min W Chen H 2012 Endothelial epsin deficiency decreases tumor growth by enhancing VEGF signaling. The Journal of Clinical Investigation 122: 4424– 4438. doi: 10.1172/JCI64537 23187125 PMC3533553 · DOI
- Polo S Sigismund S Faretta M Guidi M Capua MR Bossi G Chen H De Camilli P Di Fiore PP 2002 A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416: 451– 455. doi: 10.1038/416451a 11919637 · DOI
- Rosenthal JA Chen H Slepnev VI Pellegrini L Salcini AE Di Fiore PP De Camilli P 1999 The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. The Journal of Biological Chemistry 274: 33959– 33965. doi: 10.1074/jbc.274.48.33959 10567358 · DOI
- Rossé C L'Hoste S Offner N Picard A Camonis J 2003 RLIP, an effector of the Ral GTPases, is a platform for Cdk1 to phosphorylate epsin during the switch off of endocytosis in mitosis. The Journal of Biological Chemistry 278: 30597– 30604. doi: 10.1074/jbc.M302191200 12775724 · DOI
- Roux A Uyhazi K Frost A De Camilli P 2006 GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441: 528– 531. doi: 10.1038/nature04718 16648839 · DOI
- Royle SJ 2013 Protein adaptation: mitotic functions for membrane trafficking proteins. Nature Reviews Molecular Cell Biology 14: 592– 599. doi: 10.1038/nrm3641 23942451 · DOI
- Schmid SL 1997 Clathrin-coated vesicle formation and protein sorting:an integrated process. Annual Review of Biochemistry 66: 511– 548. doi: 10.1146/annurev.biochem.66.1.511 9242916 · DOI
- Shergill B Meloty-Kapella L Musse AA Weinmaster G Botvinick E 2012 Optical tweezers studies on notch: single-molecule interaction strength is independent of ligand endocytosis. Developmental Cell 22: 1313– 1320. doi: 10.1016/j.devcel.2012.04.007 22658935 PMC3376165 · DOI
- Shih SC Katzmann DJ Schnell JD Sutanto M Emr SD Hicke L 2002 Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nature Cell Biology 4: 389– 393. doi: 10.1038/ncb790 11988742 · DOI
- Shupliakov O Bloom O Gustafsson JS Kjaerulff O Low P Tomilin N Pieribone VA Greengard P Brodin L 2002 Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proceedings of the National Academy of Sciences of USA 99: 14476– 14481. doi: 10.1073/pnas.212381799 PMC137908 12381791 · DOI · Paper page
- Sigismund S Woelk T Puri C Maspero E Tacchetti C Transidico P Di Fiore PP Polo S 2005 Clathrin-independent endocytosis of ubiquitinated cargos. Proceedings of the National Academy of Sciences of USA 102: 2760– 2765. doi: 10.1073/pnas.0409817102 PMC549482 15701692 · DOI
- Skruzny M Brach T Ciuffa R Rybina S Wachsmuth M Kaksonen M 2012 Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proceedings of the National Academy of Sciences of USA 109: E2533– E2542. doi: 10.1073/pnas.1207011109 PMC3458359 22927393 · DOI
- Slepnev VI De Camilli P 2000 Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Reviews Neuroscience 1: 161– 172. doi: 10.1038/35044540 11257904 · DOI
- Sochacki KA Shtengel G van Engelenburg SB Hess HF Taraska JW 2014 Correlative super-resolution fluorescence and metal-replica transmission electron microscopy. Nature Methods 11: 305– 308. doi: 10.1038/nmeth.2816 24464288 PMC3943662 · DOI
- Stukenberg PT Lustig KD McGarry TJ King RW Kuang J Kirschner MW 1997 Systematic identification of mitotic phosphoproteins. Current Biology 7: 338– 348. doi: 10.1016/S0960-9822(06)00157-6 9115395 · DOI
- Taylor MJ Lampe M Merrifield CJ 2012 A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLOS Biology 10: e1001302. doi: 10.1371/journal.pbio.1001302 22505844 PMC3323523 · DOI
- Taylor MJ Perrais D Merrifield CJ 2011 A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLOS Biology 9: e1000604. doi: 10.1371/journal.pbio.1000604 21445324 PMC3062526 · DOI · Paper page
- Tronche F Kellendonk C Kretz O Gass P Anlag K Orban PC Bock R Klein R Schütz G 1999 Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nature Genetics 23: 99– 103. doi: 10.1038/12703 10471508 · DOI
- Wendland B 1999 Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. The EMBO Journal 18: 4383– 4393. doi: 10.1093/emboj/18.16.4383 10449404 PMC1171513 · DOI
- Wendland B 2002 Opinion: epsins: adaptors in endocytosis? Nature Reviews Molecular Cell Biology 3: 971– 977. doi: 10.1038/nrm970 12461563 · DOI
- Wilbur JD Chen C-Y Manalo V Hwang PK Fletterick RJ Brodsky FM 2008 Actin binding by Hip1 (huntingtin-interacting protein 1) and Hip1R (Hip1-related protein) is regulated by clathrin light chain. The Journal of Biological Chemistry 283: 32870– 32879. doi: 10.1074/jbc.M802863200 18790740 PMC2583295 · DOI
- Wu M De Camilli P 2012 Supported native plasma membranes as platforms for the reconstitution and visualization of endocytic membrane budding. Methods in Cell Biology 108: 1– 18. doi: 10.1016/B978-0-12-386487-1.00001-8 PMC12020404 22325595 · DOI
- Wu M Huang B Graham M Raimondi A Heuser JE Zhuang X De Camilli P 2010 Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system. Nature Cell Biology 12: 902– 908. doi: 10.1038/ncb2094 PMC3338250 20729836 · DOI
- Xie X Cho B Fischer JA 2012 Drosophila Epsin's role in Notch ligand cells requires three Epsin protein functions: the lipid binding function of the ENTH domain, a single Ubiquitin interaction motif, and a subset of the C-terminal protein binding modules. Developmental Biology 363: 399– 412. doi: 10.1016/j.ydbio.2012.01.004 22265678 PMC3288543 · DOI
- Yang S Cope MJ Drubin DG 1999 Sla2p is associated with the yeast cortical actin cytoskeleton via redundant localization signals. Molecular Biology of the Cell 10: 2265– 2283. doi: 10.1091/mbc.10.7.2265 10397764 PMC25442 · DOI
- Zoncu R Perera RM Sebastian R Nakatsu F Chen H Balla T Ayala G Toomre D De Camilli PV 2007 Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proceedings of the National Academy of Sciences of USA 104: 3793– 3798. doi: 10.1073/pnas.0611733104 PMC1805489 17360432 · DOI
Cited by
Sorted by citations
Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis
Ogunmowo, T. H., Jing, H., Raychaudhuri, S., Kusick, G. F., Imoto, Y., Li, S., Itoh, K., Ma, Y., Jafri, H., Dalva, M. B., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38595-2 · Cited by 51 · see citing works
“However, it is not clear whether Epsin1 is the sole organizer of F-actin at synapses, since it interacts with other endocytic proteins such as Eps15 and Hip1R 72,88 , both of which interact either directly or indirectly with membranes and actin.”
CCDC32 stabilizes clathrin-coated pits and drives their invagination
Yang, Z., Yang, C., Huang, Z., Xu, P., Li, Y., Han, L., Peng, L., Wei, X., Pak, J. E., Svitkina, T., et al. (2026) · eLife · doi:10.7554/elife.107039.3 · Cited by 3 · see citing works
- Authors
- Messa, M., Fernández-Busnadiego, R., Sun, E. W., Chen, H., Czapla, H., Wrasman, K., Wu, Y., Ko, G., Ross, T., Wendland, B., & De Camilli, P.
- Affiliations
- Howard Hughes Medical Institute (US)
- Program in Cellular Neuroscience, Neurodegeneration and Repair, Department of Cell Biology, Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, United States
- Johns Hopkins University (US)
- The University of Texas Southwestern Medical Center (US)
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2014-08-13
- Volume
- 3
- Pages
- e03311-e03311
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC4161027
- OpenAlex
- W2070297191
- Cited by
- 128
- References
- 2
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 2 · 2023: 3 · 2022: 14 · 2021: 19 · 2020: 21 · 2019: 10 · 2018: 15 · 2017: 8 · 2016: 14 · 2015: 8 · 2014: 1
- FWCI
- 5.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- Howard Hughes Medical Institute
- National Institute of Neurological Disorders and Stroke (R37NS036251)
- National Institute on Drug Abuse (DA018343)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK082700, DK45735)
- National Institute of General Medical Sciences (R01GM60979, NIGMST32007231)
- National Cancer Institute (R01CA098730)
- American Heart Association (0835544N)
- Alexander von Humboldt-Stiftung
- National Institutes of Health (5T32GM007223-38/39)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- epsin, clathrin-mediated endocytosis, actin cytoskeleton, clathrin adaptor proteins, cell division defects, embryonic fibroblasts
- MeSH terms
- Actins, Animals, Clathrin, Coated Pits, Cell-Membrane, Embryo, Mammalian, Endocytosis, Fibroblasts, Actin Cytoskeleton, Protein Binding, Signal Transduction, Gene Expression, Mice, Knockout, Adaptor Proteins, Vesicular Transport, SNARE Proteins, Mice, Primary Cell Culture
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review