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Coupling between Clathrin-Coated-Pit Invagination, Cortactin Recruitment, and Membrane Scission Observed in Live Cells
Open accessAbstract
During clathrin-mediated endocytosis, membrane scission marks the isolation of a cargo-laden clathrin-coated pit (CCP) from the cell exterior. Here we used live-cell imaging of a pH-sensitive cargo to visualize the formation of clathrin-coated vesicles (CCVs) at single CCPs with a time resolution of seconds. We show that CCPs are highly dynamic and can produce multiple vesicles in succession. Using alternating evanescent field and epifluorescence illumination, we show that CCP invagination and scission are tightly coupled, with scission coinciding with maximal displacement of CCPs from the plasma membrane and with peak recruitment of cortactin-DsRed, a dynamin and F-actin binding protein. Finally, perturbing actin polymerization with latrunculin-B drastically reduces the efficiency of membrane scission and affects many aspects of CCP dynamics. We propose that CCP invagination, actin polymerization, and CCV formation are highly coordinated for efficient endocytosis.
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“Endocytosis typically requires force generation by active actin polymerization at the maturing endocytic pit52–57.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [56]
In the citing paper
“Together, these data strongly suggest that the observed heterogeneity in the dynamic behavior of CCPs (Merrifield et al., 2005; Rappoport et al., 2005; Yarar et al., 2005) could reflect differences in their content of cargo and adaptor molecules.”
From Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis (2010) · cites this paper as Merrifield et al., 2005
In the citing paper
“This idea is further supported by the observation that nonterminal events are more frequent in HeLa cells (Ehrlich et al., 2004; Merrifield et al., 2005; Loerke et al., 2009), which express relatively high levels of Dab2 and cargo (Maurer and Cooper, 2006; unpublished data).”
From Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis (2010) · cites this paper as Merrifield et al., 2005
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Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy
Aguet, F., Upadhyayula, S., Gaudin, R., Chou, Y.-Y., Cocucci, E., He, K., Chen, B., Mosaliganti, K. R., Pasham, M. R., Skillern, W., et al. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-03-0164 · Cited by 146
“…al., 2004; Boucrot and Kirchhausen, 2008; Kural et al., 2015) or TIRF microscopy to achieve high signal-to-noise ratio on the adherent surface only (Merrifield et al., 2002, 2005; Merrifield and Kaksonen, 2014; Saffarian and Kirchhausen, 2008; Saffarian et al., 2009; Aguet et al., 2013; Cocucci et…”
BackgroundFluorescence imaging of membrane dynamics.
Groves, J., Parthasarathy, R., & Forstner, M. (2008) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.10.061807.160431 · Cited by 131
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Functions of actin in endocytosis
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“It is worth noting that in the cell lines analysed to date, cortactin is only present at a subset of coated pits—in contrast to HIP1R which is present at all pits [88, 104].”
BackgroundMessa, M., Fernández-Busnadiego, R., Sun, E. W., Chen, H., Czapla, H., Wrasman, K., Wu, Y., Ko, G., Ross, T., Wendland, B., et al. (2014) · eLife · doi:10.7554/elife.03311 · Cited by 128
“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…”
BackgroundInfluentialFrancia, V., Montizaan, D., & Salvati, A. L. (2020) · Beilstein Journal of Nanotechnology · doi:10.3762/bjnano.11.25 · Cited by 142
Leonard, D. M., Hayakawa, A., Lawe, D., Lambright, D., Bellve, K., Standley, C., Lifshitz, L. M., Fogarty, K., & Corvera, S. (2008) · Journal of Cell Science · doi:10.1242/jcs.031484 · Cited by 123
“…60 seconds after addition, but in very different patterns: the Tf signal comprised both diffuse and concentrated patches distributed over the entire adherent surface, which we and others have previously shown to be regions of clathrin enrichment (Bellve et al., 2006; Merrifield et al., 2005).”
BackgroundThe inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics
Nakatsu, F., Perera, R. M., Lucast, L., Zoncu, R., Domin, J., Gertler, F. B., Toomre, D. K., & Camilli, P. V. D. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201005018 · Cited by 128
“Comparison of the dynamics of GFP-SHIP2 relative to cortactinDsRed, which visits late-stage CCPs together with dynamin just before fission (Merrifield et al., 2005), revealed that cortactin appeared just as SHIP2 disappeared (Fig.”
Exocytosis of post-Golgi vesicles is regulated by components of the endocytic machinery
Jaiswal, J., Rivera, V., & Simon, S. (2009) · Cell · doi:10.1016/j.cell.2009.04.064 · Cited by 120
“Third, after the detachment from the cell membrane, endocytic vesicles rapidly move out of the evanescent field (Merrifield et al., 2005).”
BackgroundEndocytic Accessory Factors and Regulation of Clathrin-Mediated EndocytosisPreprint
Merrifield, C. J., & Kaksonen, M. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016733 · Cited by 124
Self-citationTriad3A Regulates Synaptic Strength by Ubiquitination of Arc
Mabb, A. M., Je, H. S., Wall, M. J., Robinson, C. G., Larsen, R. S., Yuan, Q., Corrêa, S. A. L., & Ehlers, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.016 · Cited by 115
“We next co-expressed GFP-Triad3A with DsRed-tagged clathrin light chain (LC) in COS7 cells and examined surface colocalization using total internal reflection fluorescence microscopy (TIRFM) (Merrifield et al., 2005).”
InfluentialFlat clathrin lattices: stable features of the plasma membrane
Grove, J., Metcalf, D. J., Knight, A. E., Wavre‐Shapton, S. T., Sun, T., Protonotarios, E. D., Griffin, L. D., Lippincott‐Schwartz, J., & Marsh, M. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-06-1154 · Cited by 113
“, 2006), and data suggest that these are able to generate multiple successive cargo-laden CCVs (Merrifield et al., 2005; Taylor et al., 2011).”
BackgroundResultInfluentialLai, F. P. L., Szczodrak, M., Oelkers, J., Ladwein, M., Acconcia, F., Benesch, S., Auinger, S., Faix, J., Small, J., Polo, S., et al. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-12-1180 · Cited by 117
“Because the efficiency of actin assembly is considered crucial for clathrinmediated endocytosis (Merrifield et al., 2005; Yarar et al., 2005), these data are consistent with the lack of a phenotype when exploring the efficiency of EGF internalization (Figure 7A).”
BackgroundResultDynamin2 GTPase and Cortactin Remodel Actin Filaments*
Mooren, O. L., Kotova, T. I., Moore, A. J., & Schafer, D. A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.024398 · Cited by 116
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“This property has been used to demonstrate the inward movement of clathrin-containing structures at the plasma membrane by means of alternating TIRF and WF illumination (15,16).”
BackgroundThe role of nanobiotechnology in drug discovery.
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A Hip1R–cortactin complex negatively regulates actin assembly associated with endocytosis
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“Cortactin is localized at CCPs (Cao et al, 2003; EngqvistGoldstein et al, 2004) and, interestingly, the timing of cortactin recruitment coincides with vesicle scission (Merrifield et al, 2005).”
BackgroundResultInfluentialLessons from yeast for clathrin-mediated endocytosis
Boettner, D. R., Chi, R. J., & Lemmon, S. K. (2011) · Nature Cell Biology · doi:10.1038/ncb2403 · Cited by 112
“In mammalian cells, the Arp2/3 complex, WASp and other actin regulators (for example, WIP, syndapin and cortactin) have been visualized at the endocytic sit”
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Vesicle trafficking plays a novel role in erythroblast enucleation.
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Actin Is Crucial for All Kinetically Distinguishable Forms of Endocytosis at Synapses
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Dendritic Spines in Alzheimer’s Disease: How the Actin Cytoskeleton Contributes to Synaptic Failure
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“…intense debate, although most recent studies support such a link at least for a major subset of clathrin-dependent endocytic events (Fujimoto et al., 2000; Merrifield et al., 2002, 2005; Boucrot et al., 2006; Kaksonen et al., 2006; Tsujita et al., 2006; Ferguson et al., 2009; Boulant et al., 2011).”
Salvarezza, S., Deborde, S., Schreiner, R., Campagne, F., Kessels, M., Qualmann, B., Cáceres, A., Kreitzer, G., & Rodriguez-Boulan, E. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-08-0891 · Cited by 107
“, 2005), and actin might be required to provide the required tension in dynamin-dependent fission (Merrifield et al., 2005; Kaksonen et al., 2005).”
BackgroundRole of turgor pressure in endocytosis in fission yeast
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“, 2002) (Merrifield et al., 2005).”
Fluorescence techniques to study lipid dynamics.Preprint
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“Membrane curvature, exocytosis, and endocytosis are some other topics in which TIRF is successfully applied (Merrifield et al. 2002, 2005; Byrne et al. 2008; Nagamatsu and Ohara-Imaizumi 2008; Joselevitch and Zenisek 2009; Ohara-Imaizume et al. 2009; Aoki et al. 2010; Gorg et al. 2010; Lam et al.…”
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“Actin may also assist in the formation and movement of endocytic vesicles [82, 83].”
BackgroundActin dynamics and endocytosis in yeast and mammals
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Actin in the endocytic pathway: From yeast to mammals
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Clathrin coated pits, plaques and adhesion
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“To circumvent this type of circular reasoning a ‘pulsed-pH’ protocol was developed to detect productive scission events (Figure 3Ai-Aiii) (Merrifield et al., 2005).”
InfluentialSelf-citationSathe, M., Muthukrishnan, G., Rae, J., Disanza, A., Thattai, M., Scita, G., Parton, R. G., & Mayor, S. (2018) · Nature Communications · doi:10.1038/s41467-018-03955-w · Cited by 107
Asymmetric clathrin-mediated endocytosis drives repulsive growth cone guidance.
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Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion
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“A portion of cortactin-RFP was also found associated with intracellular vesicular structures, which is consistent with a well-established role for cortactin in endocytosis and vesicle trafficking (Cao et al., 2003; Merrifield et al., 2005).”
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“These molecular mechanisms could be similar to those regulating endocytosis, in which the recruitment of clathrin to the plasma membrane precedes the recruitment of N-WASP, Arp2/3 and actin, and actin polymerization towards membranes provides the forces needed for endocytic vesicle formatio”
Independent Expression of Synaptic and Morphological Plasticity Associated with Long-Term Depression
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Analysis of yeast endocytic site formation and maturation through a regulatory transition point
Carroll, S. Y., Stimpson, H. E. M., Weinberg, J., Toret, C. P., Sun, Y., & Drubin, D. G. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-02-0108 · Cited by 95
“Knowledge of endocytic protein spatiotemporal dynamics has provided valuable insight into the mechanisms underlying endocytic vesicle formation in yeast and mammalian cells (Liu et al., 2009; Barker et al., 2007; Sun et al., 2006; Smaczynska-de et al., 2010; Newpher et al., 2005; Merrifield et al., 2005; Ferguson et a…”
BackgroundInfluentialMyosin 1E coordinates actin assembly and cargo trafficking during clathrin-mediated endocytosis
Cheng, J. C., Grassart, A., & Drubin, D. G. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-04-0383 · Cited by 108
“However, since both Myo1E and actin localized at the tubulated CCPs in primary fibroblast cells derived from dynamin 1 and 2–knockout mice (Ferguson et al., 2009), we propose that additional factors, perhaps other PRD-containing proteins, also contribute to Myo1E recruitment to endocytic sites.”
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“Several SH3 domain-containing proteins have been proposed to perform this function for dynamin (e.g., intersectin, amphiphysin, syndapin, and cortactin) (Shupliakov et al., 1997; Merrifield et al., 2005; Anggono et al., 2006).”
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“As the V-ATPase is also required to acidify endosomal compartments, we explored the role of TMEM199 and CCDC115 in endosomal acidification using a fluorescent pH sensitive transferrin receptor (Tfnr-phl) (Merrifield et al., 2005).”
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“trafficking, data from other laboratories implicate cortactin in endocytosis and trafficking of model proteins from the Golgi apparatus (Cao et al., 2003, 2005; Merrifield et al., 2005; Zhu et al., 2005).”
Synergistic BAR–NPF interactions in actin-driven membrane remodeling
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Rabenosyn-5 defines the fate of the transferrin receptor following clathrin-mediated endocytosis
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“In all carefully studied systems actin assembly during endocytosis depends on Arp2/3 complex and its nucleation promoting factors [5, 13, 17-20].”
Greene, W., & Gao, S. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000512 · Cited by 93
“More recent studies using total internal reflection fluorescence microscopy (TIR-FM) technology to observe individual endocytic events recorded a burst of actin polymerization with concomitant internalization of clathrin-coated pits and movement of clathrincoated vesicles into the cell interior, but did not determine…”
Src Triggers Circular Ruffling and Macropinocytosis at the Apical Surface of Polarized MDCK Cells
Mettlen, M., Platek, A., van der Smissen, P., Carpentier, S., Amyere, M., Lanzetti, L., de Diesbach, P., Tyteca, D., & Courtoy, P. (2006) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2006.00412.x · Cited by 92
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“Then, we determined the exact timing of recruitment of Rab35 and OCRL with respect to CCV scission from the plasma membrane, using a state-of-the-art ‘‘pulsed pH’’ (ppH) assay established previously [39, 40].”
Self-citationCortactin Controls Cell Motility and Lamellipodial Dynamics by Regulating ECM Secretion
Sung, B., Zhu, X.-D., Kaverina, I., & Weaver, A. M. (2011) · Current Biology · doi:10.1016/j.cub.2011.06.065 · Cited by 91
“A number of studies have examined the role of cortactin in endocytosis, and most have found that KD or inhibition of cortactin reduces endocytic rates [29–36].”
Yu, C., Rafiq, N. M., Cao, F., Zhou, Y., Krishnasamy, A., Biswas, K. H., Ravasio, A., Chen, Z., Wang, Y., Kawauchi, K., et al. (2015) · Nature Communications · doi:10.1038/ncomms9672 · Cited by 93
Stenkula, K. G., Lizunov, V., Cushman, S. W., & Zimmerberg, J. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.08.005 · Cited by 90
“, 2006) and can be attributed to formation of single endocytic vesicles when correlated with the uptake of a particular cargo (Merrifield et al., 2005).”
The role of Alzheimer's disease risk genes in endolysosomal pathways
Szabo, M. P., Mishra, S., Knupp, A., & Young, J. E. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105576 · Cited by 87
“Clathrin forms a complex lattice like structure around vesicles formed by membrane invaginations(Marsh and McMahon, 1999; Merrifield et al., 2005; Pearse, 1976; Ungewickell and Hinrichsen, 2007).”
Yu, D., Wang, W., Yoder, A. C., Spear, M., & Wu, Y.-T. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000633 · Cited by 85
“The involvement of the cortical actin in early endocytosis is largely limited to membrane scission of clathrin-coated pits [57].”
BackgroundA motif in the clathrin heavy chain required for the Hsc70/auxilin uncoating reaction.
Rapoport, I., Boll, W., Yu, A.-A., Böcking, T., & Kirchhausen, T. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-09-0870 · Cited by 85
“Removal of the coat (uncoating), essential for subsequent vesicle fusion and cargo delivery, is the last step in the clathrin cycle (Ehrlich et al., 2004; Merrifield et al., 2005; Lee et al., 2006; Massol et al., 2006).”
Nanoparticle entry into cells; the cell biology weak link
Griffiths, G. W., Grüenberg, J., Marsh, M., Wohlmann, J., Jones, A. T., & Parton, R. G. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114403 · Cited by 101
Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants
Narasimhan, M., Johnson, A., Prizak, R., Kaufmann, W. A., Tan, S., Casillas‐Pérez, B., & Friml, J. (2020) · eLife · doi:10.7554/elife.52067 · Cited by 111
“…interference with actin results in a total arrest of CME in yeast (Kaksonen et al., 2005) whereas in mammalian cells, there is only an overall reduction of endocytosis but still ongoing productive CME events (Fujimoto et al., 2000; Merrifield et al., 2005; Taylor et al., 2012; Yarar et al., 2005).”
BackgroundDeterminants of endocytic membrane geometry, stability, and scission
Kishimoto, T., Sun, Y., Buser, C., Liu, J., Michelot, A., & Drubin, D. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113413108 · Cited by 79
Dynamics of clathrin and adaptor proteins during endocytosis
Rappoport, J. Z., Kemal, S., Benmerah, A., & Simon, S. M. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00160.2006 · Cited by 72
Fluorescence Applications in Molecular Neurobiology
Taraska, J. W., & Zagotta, W. N. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.002 · Cited by 93
Dyachok, J., Shao, M., Vaughn, K. C., Bowling, A. J., Facette, M. R., Djakovic, S. N., Clark, L. G., & Smith, L. G. (2008) · Molecular Plant · doi:10.1093/mp/ssn059 · Cited by 79
“Regulation of membrane dynamics seems to be the most obvious possibility given the well established role played by the Arp2/3 complex in endocytosis in yeast and mammalian cells (Kaksonen et al., 2006; Sun et al., 2006; Merrifield et al., 2004, 2005).”
BackgroundInteraction between Epsin/Yap180 Adaptors and the Scaffolds Ede1/Pan1 Is Required for Endocytosis
Maldonado‐Báez, L., Dores, M. R., Perkins, E. M., Drivas, T. G., Hicke, L., & Wendland, B. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-10-1019 · Cited by 67
“…trigger the transition from early (cargo-gathering) to late (vesicle scission) events in endocytic internalization, although the mechanism is unknown (Ehrlich et al., 2004; Kaksonen et al., 2005; Merrifield et al., 2005; Naslavsky and Caplan, 2005; Newpher et al., 2005; Newpher and Lemmon, 2006).”
BackgroundTakano, K., Toyooka, K., & Suetsugu, S. (2008) · EMBO Journal · doi:10.1038/emboj.2008.216 · Cited by 75
Jia, D., Gomez, T. S., Billadeau, D. D., & Rosen, M. K. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-12-1059 · Cited by 200
“There, N-WASP controls actin dynamics, which is important for both membrane invagination and vesicle scission (Merrifield et al., 2005; Yarar et al., 2005).”
An alternative mechanism of clathrin-coated pit closure revealed by ion conductance microscopy
Shevchuk, A., Novák, P., Taylor, M. J., Diakonov, I. A., Ziyadeh-Isleem, A., Bitoun, M., Guicheney, P., Lab, M. J., Gorelik, J., Merrifield, C. J., et al. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201109130 · Cited by 86
“By labeling different molecules and following how their fluorescence changes, it has been possible to build up a picture of the time course of the major events taking place during CME (Merrifield et al., 2002, 2005; Rappoport, 2008).”
InfluentialSelf-citationMeasuring the Hierarchy of Molecular Events During Clathrin‐Mediated Endocytosis
Loerke, D., Mettlen, M., Schmid, S. L., & Danuser, G. M. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01197.x · Cited by 76
Differential Requirements for Clathrin-dependent Endocytosis at Sites of Cell–Substrate Adhesion
Batchelder, E., & Yarar, D. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-12-1044 · Cited by 74
“Distinct requirements for actin assembly during clathrin-coated vesicle formation have been reported in different cell types (Schafer et al., 1998; Fujimoto et al., 2000; Blanpied et al., 2002; Moskowitz et al., 2003; Merrifield et al., 2005; Yarar et al., 2005; Boucrot et al., 2006; Lee et al., 2006), and have also b…”
BackgroundMethodInfluentialPlasma Membrane Domains Specialized for Clathrin-mediated Endocytosis in Primary Cells*
Bellve, K., Leonard, D. M., Standley, C., Lifshitz, L. M., Tuft, R., Hayakawa, A., Corvera, S., & Fogarty, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m511370200 · Cited by 74
Molecularly Distinct Clathrin-Coated Pits Differentially Impact EGFR Fate and Signaling
Pascolutti, R., Algisi, V., Conte, A., Raimondi, A., Pasham, M. R., Upadhyayula, S., Gaudin, R., Maritzen, T., Barbieri, E., Caldieri, G., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.017 · Cited by 80
“This could be due to incomplete ablation of eps15/eps15L1/epsin1 or to participation of other endocytic proteins in CCP formation, as also supported by extant literature (Kaksonen and Roux, 2018; Mettlen et al., 2009; Merrifield et al., 2005).”
Retrograde Transport: Two (or More) Roads Diverged in an Endosomal Tree?
Johannes, L., & Wunder, C. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01200.x · Cited by 79
Grassart, A., Meas‐Yedid, V., Dufour, A., Olivo‐Marín, J., Dautry‐Varsat, A., & Sauvonnet, N. (2010) · Traffic · doi:10.1111/j.1600-0854.2010.01075.x · Cited by 82
Regarding the Amazing Choreography of Clathrin Coats
Traub, L. M. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001037 · Cited by 73
“Furthermore, time-resolved imaging reveals that the small clathrin buds (seen as #200-nm diameter diffraction-limited spots) and large clathrin patches can have different lifetimes [19,23,24].”
Dynamin-2 Function and Dysfunction Along the Secretory Pathway
González-Jamett, A. M., Momboisse, F., Haro-Acuña, V., Bevilacqua, J., Caviedes, P., & Cárdenas, A. M. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00126 · Cited by 71
“The recruitment of dynamin at endocytosis sites (39) also depends on its interaction with SH3-domain-containing proteins and phosphoinositides present at the plasma membrane via its PRD (40) and PH domain, respectively (41).”
BackgroundThe Generation of Curved Clathrin Coats from Flat Plaques
den Otter, W. K., & Briels, W. J. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01241.x · Cited by 64
An unmet actin requirement explains the mitotic inhibition of clathrin-mediated endocytosis
Kaur, S., Fielding, A. B., Gassner, G., Carter, N. J., & Royle, S. J. (2014) · bioRxiv · doi:10.1101/001701 · Cited by 68
“…microscopy studies clearly show that it is recruited to a subset of CME events in human cells (Collins et al., 2011; Merrifield et al., 2002; Merrifield et al., 2005; Taylor et al., 2012; Taylor et al., 2011) and that it is important for internalisation of pathogens such as Listeria…”
BackgroundDynamic Interaction of Amphiphysin with N-WASP Regulates Actin Assembly*
Yamada, H., Padilla-Parra, S., Park, S.-J., Itoh, T., Chaineau, M., Monaldi, I., Cremona, O., Benfenati, F., Camilli, P. D., Coppey-Moisan, M., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.064204 · Cited by 68
Hartig, S. M., Ishikura, S., Hicklen, R. S., Feng, Y., Blanchard, E. G., Voelker, K., Pichot, C., Grange, R., Raphael, R., Klip, A., et al. (2009) · Journal of Cell Science · doi:10.1242/jcs.041343 · Cited by 68
“In support of our observations, recent evidence has also shown periodic activity of N-WASp and Dynamin during clathrin-mediated endocytosis (Merrifield et al., 2002; Merrifield et al., 2005).”
BackgroundPodocyte endocytosis in the regulation of the glomerular filtration barrier
Inoue, K., & Ishibe, S. (2015) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00136.2015 · Cited by 65
“For example, dynamin, a GTPase that mediates the fission reaction during clathrin-mediated endocytosis, has been shown to interact with actin-nucleating protein Arp2/3 (57) and cortactin (66, 69).”
BackgroundMorphological changes of plasma membrane and protein assembly during clathrin-mediated endocytosis
Yoshida, A., Sakai, N., Uekusa, Y., Imaoka, Y., Itagaki, Y., Suzuki, Y., & Yoshimura, S. H. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2004786 · Cited by 68
The proposed functions of membrane curvatures mediated by the BAR domain superfamily proteins
Suetsugu, S. (2010) · The Journal of Biochemistry · doi:10.1093/jb/mvq049 · Cited by 59
Immunostimulation Effect of Jellyfish Collagen
Sugahara, T., Ueno, M., Goto, Y., Shiraishi, R., Doi, M., Akiyama, K., & Yamauchi, S. (2006) · Bioscience, biotechnology and biochemistry · doi:10.1271/bbb.60076 · Cited by 64
Cong, V. T., Houng, J. L., Kavallaris, M., Chen, X., Tilley, R. D., & Gooding, J. J. (2022) · Chemical Society Reviews · doi:10.1039/d1cs00707f · Cited by 129
African swine fever virus-cell interactions: From virus entry to cell survival
Alonso, C., Galindo, I., Cuesta-Geijo, M. Á., Cabezas, M., Hernáez, B., & Muñoz-Moreno, R. (2012) · Virus Research · doi:10.1016/j.virusres.2012.12.006 · Cited by 66
“These molecules take part in membrane bending and elongation, and final fission of the endocytic vesicle ( Fig. 1) (Merrifield et al., 2005; Taylor et al., 2011) .”
BackgroundUeda, Y., Neel, N., Schutyser, E., Raman, D., & Richmond, A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3579 · Cited by 63
The initiation of clathrin-mediated endocytosis is mechanistically highly flexible
Brach, T., Godlee, C., Moeller-Hansen, I., Boeke, D., & Kaksonen, M. (2014) · Current Biology · doi:10.1016/j.cub.2014.01.048 · Cited by 62
Dynamics of Intracellular Clathrin/AP1- and Clathrin/AP3-Containing Carriers
Kural, C., Tacheva-Grigorova, S. K., Boulant, S., Cocucci, E., Baust, T., Duarte, D., & Kirchhausen, T. L. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.025 · Cited by 68
“…coverslip have been studied by two-dimensional (2D) time-lapse imaging, using confocal or total internal reflection fluorescence microscopy (Cocucci et al., 2012; Ehrlich et al., 2004; Merrifield et al., 2005; Mettlen et al., 2009; Saffarian et al., 2009; Taylor et al., 2011; Yarar et al., 2005).”
MethodDual pools of actin at presynaptic terminals
Bleckert, A., Photowala, H., & Alford, S. T. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00789.2011 · Cited by 68
Local actin polymerization during endocytic carrier formation
Hinze, C., & Boucrot, E. (2018) · Biochemical Society Transactions · doi:10.1042/bst20170355 · Cited by 68
Egea, G., Serra‐Peinado, C., Salcedo-Sicilia, L., & Gutiérrez-Martínez, E. (2013) · Histochemistry and Cell Biology · doi:10.1007/s00418-013-1115-8 · Cited by 63
“2a) similarly to what happens during endocytosis (Merrifield 2004; Merrifield et al. 2005; Taylor et al. 2012), and/or for its translocation to closely arranged microtubule tracks”
BackgroundHayashi, H., Inamura, K., Aida, K., Naoi, S., Horikawa, R., Nagasaka, H., Takatani, T., Fukushima, T., Hattori, A., Yabuki, T., et al. (2012) · Hepatology · doi:10.1002/hep.25591 · Cited by 62
Quantitative analysis of endocytosis with cytoplasmic pHluorin chimeras
Prosser, D. C., Whitworth, K., & Wendland, B. (2010) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2010.01088.x · Cited by 59
Plant dynamin-related protein families DRP1 and DRP2 in plant development
Bednarek, S. Y., & Backues, S. K. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380797 · Cited by 58
Hayakawa, A., Leonard, D. M., Murphy, S. T., Hayes, S. J., Soto, M. C., Fogarty, K., Standley, C., Bellve, K., Lambright, D., Mello, C., et al. (2006) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0508832103 · Cited by 58
Rosendale, M., Jullié, D., Choquet, D., & Perrais, D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.081 · Cited by 73
“However, as opposed to what had previously been observed in other cell types (Merrifield et al., 2005), the fluorescence at pH 7.”
InfluentialSelf-citationChuang, C.-K., Yang, T.-H., Chen, T.-H., Yang, C.-F., & Chen, W.-J. (2015) · Journal of General Virology · doi:10.1099/jgv.0.000015 · Cited by 57
“In turn, the receptor-mediated endocytosis of extracellular molecules requires the involvement of clathrin that is highly dynamic and can be recycled after each round of endocytosis (McMahon & Boucrot, 2011; Merrifield et al., 2005).”
BackgroundEscherichia coli Producing CNF1 Toxin Hijacks Tollip to Trigger Rac1‐Dependent Cell Invasion
Visvikis, O., Boyer, L., Torrino, S., Doye, A., Lemonnier, M., Lorès, P., Rolando, M., Flatau, G., Mettouchi, A., Bouvard, D., et al. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01174.x · Cited by 58
Clathrin‐mediated endocytosis: What works for small, also works for big
Pizarro‐Cerdá, J., Bonazzi, M., & Cossart, P. (2010) · BioEssays · doi:10.1002/bies.200900172 · Cited by 50
Mechanical requirements for membrane fission: Common facts from various examples
Lenz, M., Morlot, S., & Roux, A. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.11.012 · Cited by 57
Dynamin participates in the maintenance of anterior polarity in the C. elegans embryo
Nakayama, Y., Shivas, J. M., Poole, D. S., Squirrell, J., Kulkoski, J. M., Schleede, J. B., & Skop, A. R. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.04.009 · Cited by 57
“Given that dynamin can regulate both endocytic and actin dynamics in animal cells, and that actin regulators play a central role in endocytosis (Kaksonen et al., 2006; Merrifield, 2004; Merrifield et al., 2002, 2005; Smythe and Figure 5 .”
BackgroundSamaniego, R., Sánchez-Martı́n, L., Estecha, A., & Sánchez‐Mateos, P. (2007) · Journal of Cell Science · doi:10.1242/jcs.006296 · Cited by 50
“However, CSs also include a population of larger and more complex structures that may support multiple rounds of vesicle formation before being disassembled and correspond to platforms for cargo selection (Merrifield et al., 2005; Perrais and Merrifield, 2005).”
BackgroundEndocytosis in the axon initial segment maintains neuronal polarity
Eichel, K., Uenaka, T., Belapurkar, V., Lu, R., Cheng, S.-Q., Pak, J. S., Taylor, C. A., Südhof, T., Malenka, R., Wernig, M., et al. (2022) · Nature · doi:10.1038/s41586-022-05074-5 · Cited by 56
“The TfR-SEP plasmid was used 42 and described 60 previously.”
Self-citation
Metadata
- Authors
- Merrifield, C. J., Perrais, D., & Zenisek, D.
- Affiliations
- MRC Laboratory of Molecular Biology (GB)
- Centre National de la Recherche Scientifique (FR)
- Yale University (US)
- Corresponding author
- Merrifield, Christien J.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2005-05
- Volume
- 121
- Issue
- 4
- Pages
- 593-606
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2001532503
- Cited by
- 476
- References
- 0
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 6 · 2023: 14 · 2022: 15 · 2021: 10 · 2020: 9 · 2019: 11 · 2018: 18 · 2017: 17 · 2016: 13 · 2015: 21 · 2014: 36 · 2013: 12 · 2012: 34
- FWCI
- 16.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- clathrin-mediated endocytosis, membrane fission, clathrin-coated vesicles, cortactin, actin polymerization, latrunculin B, vesicle formation, dynamin, F-actin
- MeSH terms
- Actins, Animals, Cell Membrane, Coated Pits, Cell-Membrane, Endocytosis, Microfilament Proteins, Microscopy, Fluorescence, Polymers, Thiazoles, Microscopy, Video, Bridged Bicyclo Compounds, Heterocyclic, Clathrin-Coated Vesicles, Swiss 3T3 Cells, Cortactin, Mice, Thiazolidines
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