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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et al., 2005; Loerke et al., 2009), which express relatively high levels of Dab2 and cargo (Maurer and Cooper, 2006; unpublished data).”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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Intersectin-2L Regulates Caveola Endocytosis Secondary to Cdc42-mediated Actin Polymerization*
Klein, I., Predescu, D., Sharma, T., Knezevic, I., Malik, A., & Predescu, S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.035071 · Cited by 56
Receptor-mediated Endocytosis Involves Tyrosine Phosphorylation of Cortactin*
Zhu, J.-W., Yu, D., Zeng, X.-C., Zhou, K., & Zhan, X. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701997200 · Cited by 56
Imaging and Modeling the Dynamics of Clathrin-Mediated EndocytosisPreprint
Mettlen, M., & Danuser, G. M. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a017038 · Cited by 62
“…resolution of individual molecular steps in CME falls exclusively within its application area (e.g., Rappoport and Simon 2003; Keyel et al. 2004; Merrifield et al. 2005; Loerke et al. 2009; Mattheyses et al. 2011; Carroll et al. 2012) and recent studies have shown that the limits in sensitivity…”
BackgroundInfluentialA fluorescent tagging approach in Drosophila reveals late endosomal trafficking of Notch and Sanpodo
Couturier, L., Trylinski, M., Mazouni, K., Darnet, L., & Schweisguth, F. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201407071 · Cited by 52
“For instance, the difference in pH sensitivity between GFP and Cherry was used to monitor endosome fission (Merrifield et al., 2005) and autophagy (Kimura et al., 2007).”
MethodLladó, A., Timpson, P., de Muga, S. V., Moretó, J., Pol, A., Grewal, T., Daly, R., Enrich, C., & Tebar, F. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-05-0411 · Cited by 55
“…growth factor receptor (EGFR) degradation, or endosomal positioning (McNiven et al., 2000; Cao et al., 2003, 2005; Lynch et al., 2003; Cabezas et al., 2005; Merrifield et al., 2005; Sauvonnet et al., 2005; Timpson et al., 2005; Zhu et al., 2005; Mettlen et al., 2006; Le Clainche et al., 2007).”
Syndapin – a membrane remodelling and endocytic F‐BAR protein
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Prete, F., Catucci, M., Labrada, M., Gobessi, S., Castiello, M. C., Bonomi, E., Aiuti, A., Vermi, W., Cancrini, C., Metìn, A., et al. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20120363 · Cited by 57
Minimal Mesoscale Model for Protein-Mediated Vesiculation in Clathrin-Dependent Endocytosis
Agrawal, N. J., Nukpezah, J., & Radhakrishnan, R. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000926 · Cited by 52
“Recent work [15] demonstrates that the membrane invagination only begins in the presence of a growing clathrin coat [16].”
BackgroundPoulter, N. S., Pitkeathly, W. T. E., Smith, P. J., & Rappoport, J. Z. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-2080-8_1 · Cited by 62
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
Dynamin-dependent vesicle twist at the final stage of clathrin-mediated endocytosis
Cheng, X., Chen, K., Dong, B., Yang, M., Filbrun, S. L., Myoung, Y., Huang, T.-X., Gu, Y. H., Wang, G., & Fang, N. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00713-x · Cited by 62
Kirkbride, K. C., Hong, N. H., French, C. L., Clark, E. S., Jerome, W. G., & Weaver, A. M. (2012) · Cytoskeleton · doi:10.1002/cm.21051 · Cited by 46
“…can regulate endocytic trafficking, including initial endocytosis from the plasma membrane (PM) [Cao et al., 2003; Engqvist-Goldstein et al., 2004; Merrifield et al., 2005; Sauvonnet et al., 2005; Zhu et al., 2005; Zhu et al., 2007; Cao et al., 2010; Grassart et al., 2010] and recycling…”
BackgroundThe trinity of the cortical actin in the initiation of HIV-1 infection
Spear, M., Guo, J., & Wu, Y.-T. (2012) · Retrovirology · doi:10.1186/1742-4690-9-45 · Cited by 49
“viral particles [102].”
Probing bioinspired transport of nanoparticles into polymersomes.
Jaskiewicz, K., Larsen, A., Lieberwirth, I., Koynov, K., Meier, W., Fytas, G., Kroeger, A., & Landfester, K. (2012) · Angewandte Chemie · doi:10.1002/anie.201108421 · Cited by 49
Dab2 regulates clathrin assembly and cell spreading
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A Discrete Presynaptic Vesicle Cycle for Neuromodulator Receptors
Jullié, D., Stoeber, M., Sibarita, J., Zieger, H. L., Bartol, T. M., Arttamangkul, S., B, T. J. S. A., Hosy, E., & von Zastrow, M. (2019) · Neuron · doi:10.1016/j.neuron.2019.11.016 · Cited by 49
“To directly visualize sites of MOR endocytosis, we used the pulsed pH (ppH) protocol to resolve individual MOR-containing endocytic events in living neurons based on the endocytic scission event rendering SEP-labeled receptors resistant to extracellular application of a membrane-impermeant acidic buffer (pH 5.5 MES) (…”
BackgroundInfluentialTctex‐1 controls ciliary resorption by regulating branched actin polymerization and endocytosis
Saito, M., Otsu, W., Hsu, K., Chuang, J.-Z., Yanagisawa, T., Shieh, V., Kaitsuka, T., Wei, F., Tomizawa, K., & Sung, C.-H. (2017) · EMBO Reports · doi:10.15252/embr.201744204 · Cited by 55
“concentrated in the CME sites; perturbing Arp2/3 activity compromises endocytosis [9,38].”
Recycling Endosomes Undergo Rapid Closure of a Fusion Pore on Exocytosis in Neuronal Dendrites
Jullié, D., Choquet, D., & Perrais, D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0799-14.2014 · Cited by 53
“This tagged protein is robustly recruited to sites of CME in non-neuronal (Taylor et al., 2011) and neuronal (our unpublished observations) cells.”
BackgroundMethodInfluentialSelf-citationRab8a regulates the exocyst-mediated kiss-and-run discharge of the Dictyostelium contractile vacuole
Essid, M., Gopaldass, N., Yoshida, K., Merrifield, C. J., & Soldati, T. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-06-0576 · Cited by 47
“Details of a similar TIRFM setup have been published (Merrifield et al., 2005).”
MethodSelf-citationBrady, R. J., Damer, C. K., Heuser, J. E., & O’Halloran, T. J. (2010) · Journal of Cell Science · doi:10.1242/jcs.066852 · Cited by 39
“…clathrin puncta were associated with actin puncta, suggesting that actin polymerization plays a role in the late stages of clathrin-mediated endocytosis in Dictyostelium, similar to endocytosis in both yeast and vertebrates (Merrifield et al., 2002; Kaksonen et al., 2003; Merrifield et al., 2005).”
BackgroundInfluentialMolecular structures of coat and coat-associated proteins: function follows form
Brett, T. J., & Traub, L. M. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.06.014 · Cited by 47
Survey of Red Fluorescence Proteins as Markers for Secretory Granule Exocytosis
Gandasi, N. R., Vestö, K., Helou, M., Yin, P., Saras, J., & Barg, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127801 · Cited by 48
“6) detect the luminal pH change during exocytosis and are therefore powerful tools to study membrane fusion and fission [9,10,24,30,34,66].”
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Barker, S. L., Lee, L., Pierce, B. D., Maldonado‐Báez, L., Drubin, D. G., & Wendland, B. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-05-0436 · Cited by 40
“The later events in internalization, possibly including vesicle scission, involve actin polymerization (Yarar et al., 2005) and Arp2/3 complex recruitment (Merrifield et al., 2005).”
BackgroundSplice isoform estrogen receptors as integral transmembrane proteins
Kim, K. H., Toomre, D., & Bender, J. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-05-0416 · Cited by 43
“Recombinant pHluorin alone, which has been used to monitor intracellular vesicle exocytosis and recycling, and transferrin receptor (TfR)-pHluorin, which has been used to delineate membrane scission events in clathrin-mediated endocytosis (Merrifield et al., 2005), were used as controls.”
MethodEndocytic pathways: combined scanning ion conductance and surface confocal microscopy study
Shevchuk, A., Hobson, P., Lab, M., Klenerman, D., Krauzewicz, N., & Korchev, Y. (2008) · Pflügers Archiv: European Journal of Physiology · doi:10.1007/s00424-007-0410-4 · Cited by 43
“mobile and move away from the surface inside the cell as soon as they bud off the cell membrane [ 16 ].”
BackgroundSH3P7/mAbp1 deficiency leads to tissue and behavioral abnormalities and impaired vesicle transport
Connert, S., Wienand, S., Thiel, C., Krikunova, M., Glyvuk, N., Tsytsyura, Y., Hilfiker-Kleiner, D., Bartsch, J.-W., Klingauf, J., & Wienands, J. (2006) · EMBO Journal · doi:10.1038/sj.emboj.7601053 · Cited by 43
“In support of this and as shown more recently, association of mAbp1 with actin comet tails occurs subsequently to dynamin function and clathrin release (Merrifield et al, 2005; Newpher et al, 2005; Yarar et al, 2005).”
Dynamin: expanding its scope to the cytoskeleton.
Menon, M., & Schafer, D. A. (2013) · International Review of Cell and Molecular Biology · doi:10.1016/b978-0-12-407699-0.00003-0 · Cited by 43
Dynamic instability of clathrin assembly provides proofreading control for endocytosis
Chen, Y., Yong, J., Martínez-Sánchez, A., Yang, Y., Wu, Y., Camilli, P. V. D., Fernández‐Busnadiego, R., & Wu, M. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201804136 · Cited by 39
“Indeed, the majority of FRAP studies show only partial recovery (Moskowitz et al., 2003; Hinrichsen et al., 2006; Loerke et al., 2009; Mettlen et al., 2010; Taylor et al., 2012; Kozik et al., 2013; Avinoam et al., 2015), which provides evidence for the addition of clathrin to an existing structure,…”
Interplay between N-WASP and CK2 optimizes clathrin-mediated endocytosis of EGFR
Galovic, M., Xu, D., Areces, L., van der Kammen, R. A., & Innocenti, M. (2011) · Journal of Cell Science · doi:10.1242/jcs.081182 · Cited by 42
“The robust association between F-actin and CCPs is surprising given that actin recruitment is often only transient (Benesch et al., 2005; Ferguson et al., 2009; Innocenti et al., 2005; Lamaze et al., 1997; Merrifield et al., 2005; Merrifield et al., 2004; Yarar et al., 2005).”
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Membrane transformations of fusion and budding
Wu, L., & Chan, C. Y. (2024) · Nature Communications · doi:10.1038/s41467-023-44539-7 · Cited by 55
Regulating dynamin dynamics during endocytosis
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A novel role for survivin in erythroblast enucleation
Keerthivasan, G., Liu, H., Gump, J. M., Dowdy, S. F., Wickrema, A., & Crispino, J. D. (2012) · Haematologica · doi:10.3324/haematol.2011.061093 · Cited by 45
Clathrin Couture: Fashioning Distinctive Membrane Coats at the Cell Surface
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“This idea is in accord with observed fluctuations in TIR-FM fluorescence intensity within the persistent lattice population [20], which are compatible with loss of (peripheral) subregions of an extended patch, leaving portions remaining at the plasma membrane [15].”
BackgroundMethodInfluentialMoesin Regulates the Trafficking of Nascent Clathrin-coated Vesicles
González, J. B., Machado, J. D., García-Expósito, L., & Valenzuela-Fernández, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805311200 · Cited by 43
Membrane re-modelling by BAR domain superfamily proteins via molecular and non-molecular factors
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Self-citationVisualization of retrovirus uptake and delivery into acidic endosomes
Miyauchi, K., Marin, M., & Melikyan, G. (2011) · Biochemical Journal · doi:10.1042/bj20101588 · Cited by 39
“Similar to the strategy used to detect the formation of endocytic vesicles [13], virus internalization was monitored by assessing the changes in mean fluorescence of multiple viral particles in buffers of varied acidity.”
InfluentialMultiple Roles of Actin in Exo- and Endocytosis
Wu, L., & Chan, C. Y. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.841704 · Cited by 76
“…not generalize to non-secretory vesicle endocytosis in mammalian cells, where F-actin is thought to be needed to overcome membrane tension only when plasma membrane tension is high (Merrifield et al., 2005; Yarar et al., 2005; Ferguson et al., 2009; Saffarian et al., 2009; Boulant et al., 2011).”
BackgroundYuan, Q., Yang, F., Xiao, Y., Tan, S., Husain, N., Ren, M., Hu, Z., Martinowich, K., Ng, J. S., Kim, P. J., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.019 · Cited by 37
Intracellular transport based on actin polymerization
Khaitlina, S. (2014) · Biochemistry (Moscow) · doi:10.1134/s0006297914090089 · Cited by 37
PICK1 is implicated in organelle motility in an Arp2/3 complex–independent manner
Madasu, Y., Yang, C., Boczkowska, M., Bethoney, K. A., Zwolak, A., Rębowski, G., Svitkina, T., & Domínguez, R. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-10-1448 · Cited by 36
“The recruitment of actin assembly factors such as the Arp2/3 complex regulator cortactin to sites of endocytosis follows a similar time course as invagination (Merrifield et al., 2005), and actin network assembly coincides precisely with the onset of invagination (Kukulski et al.”
BackgroundEHD2 mediates trafficking from the plasma membrane by modulating Rac1 activity.
Benjamin, S., Weidberg, H., Rapaport, D., Pekar, O., Nudelman, M., Segal, D., Hirschberg, K., Katzav, S., Ehrlich, M., & Horowitz, M. (2011) · Biochemical Journal · doi:10.1042/bj20111010 · Cited by 36
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“New actin polymerization at the site of clathrin-coated pit formation may stretch the nascent pit, pushing it away from the membrane (Kaksonen et al., 2005; Merrifield et al., 2005).”
BackgroundHeuser, J. (2006) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2006.05.011 · Cited by 34
An Engineered Minimal WASP-Myosin Fusion Protein Reveals Essential Functions for Endocytosis
Lewellyn, E. B., Pedersen, R. T. A., Hong, J. M., Lu, R., Morrison, H. M., & Drubin, D. G. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.10.007 · Cited by 35
“Like the WASP/Myosin complex in yeast, mammalian proteins including N-WASP, cortactin, and the class I myosin Myosin 1E are recruited to endocytic sites and orchestrate actin polymerization (Merrifield et al., 2005)(Cheng et al.”
BackgroundConibear, E., & Tam, Y. Y. C. (2009) · Springer eBooks · doi:10.1007/978-0-387-93877-6_4 · Cited by 12
Functional recruitment of dynamin requires multimeric interactions for efficient endocytosis
Rosendale, M., Van, T. N. N., Grillo‐Bosch, D., Sposini, S., Claverie, L., Gauthereau, I., Claverol, S., Choquet, D., Sainlos, M., & Perrais, D. (2019) · Nature Communications · doi:10.1038/s41467-019-12434-9 · Cited by 37
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“In fibroblast cells, vesicle scission is observed at the time when the actin polymerization burst reaches its peak level [61].”
BackgroundPhysical and functional connection between auxilin and dynamin during endocytosis
Sever, S., Skoch, J., Newmyer, S., Ramachandran, R., Ko, D., Mckee, M., Bouley, R., Ausiello, D., Hyman, B., & Bacskai, B. (2006) · EMBO Journal · doi:10.1038/sj.emboj.7601298 · Cited by 34
“Live-cell imaging of clathrin (Merrifield et al, 2005) and downregulation of clathrin in cells (Iversen et al, 2003) together suggested that clathrin assembly may play a role in Received: 9 February 2006; accepted: 1 August 2006; published online: 31 August 2006 *Corresponding author.”
BackgroundTuba, A GEF for CDC42, Links Dynamin to Actin Regulatory Proteins
Cestra, G., Kwiatkowski, A. V., Salazar, M. A. G., Gertler, F. B., & Camilli, P. V. D. (2005) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)04047-4 · Cited by 34
He, Z., Fan, J., Kang, L., Lu, J., Xue, Y., Xu, P., Xu, T., & Chen, L. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00730.x · Cited by 37
Imaging single endocytic events reveals diversity in clathrin, dynamin, and vesicle dynamics
Mattheyses, A., Atkinson, C., & Simon, S. M. (2011) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2011.01235.x · Cited by 32
“The relationship between the fluorescent protein signals and the biophysical events which are common to all endocytosed vesicles including membrane deformation, neck constriction, vesicle scission and vesicle internalization are currently unclear (14).”
BackgroundMethodAsymmetry as the key to clathrin cage assembly.
den Otter, W. D., Renes, M., & Briels, W. J. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.06.011 · Cited by 32
Domain-Driven Morphogenesis of Cellular Membranes
Shnyrova, A. V., Frolov, V. A., & Zimmerberg, J. J. (2009) · Current Biology · doi:10.1016/j.cub.2009.07.063 · Cited by 35
Phosphoinositide 3-Kinase C2α Links Clathrin to Microtubule-dependent Movement
Zhao, Y., Gaidarov, I., & Keen, J. H. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606998200 · Cited by 33
Zong, W.-J., Huang, X., Zhang, C., Yuan, T., Zhu, L.-L., Fan, M., & Chen, L.-Y. (2014) · Biomedical Optics Express · doi:10.1364/boe.5.001530 · Cited by 31
Kelley, L. C., & Weed, S. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044363 · Cited by 35
“cytoplasmic membrane surfaces during internalization [28,34,62].”
BackgroundCortactin depletion results in short tubulobulbar complexes and spermiation failure in rat testes
Young, J. S., de Asis, M. A., Guttman, J. A., & Vogl, A. W. (2012) · Biology Open · doi:10.1242/bio.20122519 · Cited by 29
“Cortactin is known to coordinate membrane dynamics and cytoskeletal remodeling in other systems (Schafer, 2002) – two features that also make it a key player during the process of clathrin-mediated endocytosis (Merrifield et al., 2005).”
BackgroundListeria monocytogenes Exploits Host Caveolin for Cell-to-Cell Spreading
Dhanda, A. S., Yu, C., Lulic, K. T., Vogl, A. W., Rausch, V., Yang, D., Nichols, B. J., Kim, S. H., Polo, S., Hansen, C. G., et al. (2020) · mBio · doi:10.1128/mbio.02857-19 · Cited by 32
“While some of these accessory proteins (dynamin-2 [19, 20] and actin [21, 22]) are shared by both endocytic mechanisms, most remain segregated to their respective internalization pathways.”
BackgroundYuan, T., Liu, L., Zhang, Y., Wei, L., Zhao, S., Zheng, X., Huang, X., Boulanger, J., Gueudry, C., Lu, J., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.09.004 · Cited by 33
“…disappearance of pre-existing LCa puncta from the fusion sites occurred with a mean latency of 13.1 ± 1.6 s (n = 80) after exocytosis and accelerated coupled CME 5- to 7-fold over classical CME (60–100 s in non-excitable cells) (Ehrlich et al., 2004; Loerke et al., 2009; Merrifield et al., 2005).”
BackgroundMethodInfluentialStockler, S., Corvera, S., Lambright, D., Fogarty, K., Nosova, E., Leonard, D. M., Steinfeld, R., Ackerley, C., Shyr, C., Au, N., et al. (2014) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-014-0141-5 · Cited by 30
Loebrich, S. (2014) · Communicative & Integrative Biology · doi:10.4161/cib.28740 · Cited by 30
Stochastic model of clathrin-coated pit assembly.
Banerjee, A., Berezhkovskii, A., & Nossal, R. (2012) · Biophysical Journal · doi:10.1016/j.bpj.2012.05.010 · Cited by 30
Big gulps: specialized membrane domains for rapid receptor-mediated endocytosis
McNiven, M. A. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.08.007 · Cited by 29
Bidirectional transport between the trans-Golgi network and the endosomal system
Anitei, M., Wassmer, T., Stange, C., & Hoflack, B. (2010) · Molecular Membrane Biology · doi:10.3109/09687688.2010.522601 · Cited by 32
“2009) that are under a tension likely provided by actin polymerization (Merrifield et al. 2005).”
BackgroundDynamics of Membrane Clathrin‐Coated Structures During Cytokinesis
Warner, A. K., Keen, J. H., & Wang, Y.-L. (2006) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2005.00377.x · Cited by 29
Dynamin- and Rab5-dependent endocytosis is required to preventDrosophilaphotoreceptor degeneration
Pinal, N., & Pichaud, F. (2011) · Journal of Cell Science · doi:10.1242/jcs.082115 · Cited by 27
“Interestingly, both ARF6 and RhoA co-immunoprecipitate with rhodopsin-family receptors in N1321N1 cells, an association that depends upon the conserved NPxxY motif located immediately distal to the seventh transmembrane helix (Mitchell et al., 1998).”
BackgroundMendoza, K. C., McLane, V. D., Kim, S., & Griffin, J. D. (2010) · Brain Research · doi:10.1016/j.brainres.2010.02.041 · Cited by 28
“Recent developments in the field of bionanotechnology have yielded new approaches to supplement molecular studies at the subcellular level (Bergen et al., 2008; Grimm et al., 2004; Kukowska-Latallo et al., 2005; Merrifield et al., 2005).”
A Functional GFP Fusion for Imaging Clathrin‐Mediated Endocytosis
Rappoport, J., & Simon, S. (2008) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2008.00770.x · Cited by 28
Weinberg, Z. Y., Zajac, A. S., Phan, T., Shiwarski, D. J., & Puthenveedu, M. A. (2017) · Molecular Pharmacology · doi:10.1124/mol.116.106633 · Cited by 29
Synaptic vesicles are “primed” for fast clathrin-mediated endocytosis at the ribbon synapse
Pelassa, I., Zhao, C., Pasche, M., Odermatt, B., & Lagnado, L. (2014) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2014.00091 · Cited by 23
“A direct method for investigating the molecular dynamics of endocytosis in living cells is total internal reflection fluorescence microscopy (TIRFM), which allows the movement of fluorophores within ∼50 nm of the surface membrane to be imaged in real-time (Merrifield et al., 2002, 2005).”
MethodStudying Individual Events in Biology
Wennmalm, S., & Simon, S. M. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.062305.094225 · Cited by 26
Xu, C., Fu, X., Zhu, S., & Liu, J.-J. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-05-0326 · Cited by 27
“…and kept increasing during the time monitored (Figure 5B), in agreement with the dynamics of both clathrin-dependent and -independent endocytosis (Merrifield et al., 2005; Mettlen et al., 2009; Basquin et al., 2015), colocalization between WAVE1 and ligand-activated TrkB (pTrk) in hippocampal…”
BackgroundEvolutionary Changes on the Way to Clathrin-Mediated Endocytosis in Animals
Dergai, M., Iershov, A., Novokhatska, O., Pankivskyi, S., & Rynditch, A. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw028 · Cited by 26
“Polymerization of actin was shown to precede vesicle fission in animal cells (Merrifield et al. 2005).”
BackgroundCytoskeleton and Golgi-apparatus interactions: a two-way road of function and structure
Egea, G., Serra‐Peinado, C., Gavilán, M. P., & Rios, R. M. (2015) · Cell Health and Cytoskeleton · doi:10.2147/chc.s57108 · Cited by 36
Recent insights into the building and cycling of synaptic vesicles.
Shupliakov, O., & Brodin, L. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.02.035 · Cited by 26
Cantallops, I., & Cline, H. T. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20529 · Cited by 25
“pHluorin-tagged transferin receptors have been used to visualize mobility of proteins through dynamic endocytotic compartments in nonneuronal cells (Merrifield et al., 2005) and neurons (Park et al.”
BackgroundKochubey, O., Majumdar, A., & Klingauf, J. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00492.x · Cited by 22
Immature olfactory sensory neurons provide complementary input in the healthy olfactory system
Gregory, J. D., Herzog, R. S., Curtis, K. A., Marar, M. I., & Cheetham, C. E. (2025) · bioRxiv · doi:10.1007/978-4-431-55166-9 · Cited by 25
Clathrin Assembly Defines the Onset and Geometry of Cortical Patterning
Yang, Y., Xiong, D., Pipathsouk, A., Weiner, O. D., & Wu, M. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.10.028 · Cited by 21
“Successful endocytic events from these clathrin plagues have been inferred based on the recruitment of late stage markers, such as actin and Dynamin (Merrifield et al., 2005).”
BackgroundRab11 Regulates the Mast Cell Exocytic Response
Wilson, J. D., Shelby, S., Holowka, D., & Baird, B. (2016) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/tra.12418 · Cited by 25
Macro, L., Jaiswal, J., & Simon, S. (2012) · Journal of Cell Science · doi:10.1242/jcs.108837 · Cited by 25
“Thus, a robust measure for CME requires demonstration of cargo internalization together with the disappearance of clathrin from the cell membrane, as seen in mammalian systems (Ehrlich et al., 2004; Merrifield et al., 2005; Rappoport et al., 2005; Mattheyses et al., 2011).”
Backgroundvan Rossum, A. V., Gibcus, J., van der Wal, J. E., & Schuuring, E. (2005) · Breast Cancer Research · doi:10.1186/bcr1316 · Cited by 25
Brain Endothelial Cells Utilize Glycolysis for the Maintenance of the Transcellular Permeability
Kim, E. S., Kim, K., Lee, C.-H., Jeon, M.-T., Lee, S. B., Lee, J. H., & Kim, D.-G. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02778-7 · Cited by 24
“6A), a molecule that is a marker involved in Clath-coated pit formation utilized for the entry of molecules [43, 44].”
BackgroundRegulation of EGF-stimulated activation of the PI-3K/AKT pathway by exocyst-mediated exocytosis
An, S. J., Anneken, A., Xi, Z., Choi, C.-S., Schlessinger, J., & Toomre, D. (2022) · bioRxiv · doi:10.1073/pnas.2208947119 · Cited by 24
“…with exocytosis, we performed two-color imaging experiments with the pH-sensitive exocytosis reporter transferrin receptor-pHluorin (TfRc-pH; Merrifield et al, 2005), which emits in the green channel (∼509 nm), and the PI(3,4,5)P3 biosensor with its GFP replaced by TagRFP-T, a fluorescent…”
MethodAn active tethering mechanism controls the fate of vesicles
An, S. J., Rivera-Molina, F., Anneken, A., Xi, Z., McNellis, B., Polejaev, V. I., & Toomre, D. (2021) · Nature Communications · doi:10.1038/s41467-021-25465-y · Cited by 24
Hartwig, C. L., Monis, W. J., Chen, X., Dickman, D. K., Pazour, G. J., & Faúndez, V. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22542 · Cited by 29
“Membrane invagination, scission, and release of a vesicle from its donor membrane all require Arp2/3-dependent actin polymerization (Carreno et al., 2004; Kaksonen et al., 2005, 2006; Merrifield et al., 2005; Yarar et al., 2005; Collins et al., 2011; Picco et al., 2015).”
BackgroundThe actin regulatory protein HS1 is required for antigen uptake and presentation by dendritic cells
Huang, Y.-P., Biswas, C., Dehring, D. A. K., Sriram, U., Williamson, E., Li, S., Clarke, F., Gallucci, S., Argon, Y., & Burkhardt, J. (2011) · Journal of Immunology · doi:10.4049/jimmunol.1100870 · Cited by 24
Myosin light chain kinase and Src control membrane dynamics in volume recovery from cell swelling
Barfod, E. T., Moore, A. L., de Graaf, B. G. V., & Lidofsky, S. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-06-0514 · Cited by 24
Clathrin: the molecular shape shifter
Wood, K. M., & Smith, C. J. (2021) · Biochemical Journal · doi:10.1042/bcj20200740 · Cited by 36
Annexin A2 is SUMOylated on its N‐terminal domain: Regulation by insulin
Caron, D., Boutchueng-Djidjou, M., Tanguay, R. M., & Faure, R. L. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.03.007 · Cited by 22
Guttman, J. A., Lin, A., Veiga, E., Cossart, P., & Finlay, B. (2010) · Infection and Immunity · doi:10.1128/iai.00161-10 · Cited by 22
Zhang, J., Dong, B., & Siminovitch, K. A. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00846.x · Cited by 19
“These include cortactin, which binds to coated pits, primarily at the time of scission, and activates Arp2 ⁄3 directly and also indirectly, by enhancing WASp-mediated Arp2 ⁄3 activation (172).”
BackgroundSakaushi, S., Inoue, K., Zushi, H., Senda-Murata, K., Fukada, T., Oka, S., & Sugimoto, K. (2007) · Bioscience, biotechnology and biochemistry · doi:10.1271/bbb.60720 · Cited by 22
Galli, V., Sebastián, R., Moutel, S., Ecard, J., Perez, F., & Roux, A. (2017) · eLife · doi:10.7554/elife.25197 · Cited by 20
“The dynamics of the fission reaction has been studied extensively in cells; it requires 5–10 s and is highly stochastic (Merrifield et al., 2005), consistent with in vitro fission rates in optimal conditions (Morlot et al., 2012).”
BackgroundInfluentialMembrane indentation triggers clathrin lattice reorganization and fluidization
Cordella, N., Lampo, T. J., Melosh, N. A., & Spakowitz, A. J. (2014) · Soft Matter · doi:10.1039/c4sm01650e · Cited by 21
Myosin Light Chain Kinase Accelerates Vesicle Endocytosis at the Calyx of Held Synapse
Yue, H.-Y., & Xu, J.-H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3744-13.2014 · Cited by 21
“Although a role of actin in endocytosis is not yet established at mammalian central synapses (Sankaranarayanan et al., 2003), it has been demonstrated in other synapses and nonneuronal cells (Brodin et al., 2000; Merrifield et al., 2005; Girao et al., 2008; Mooren et al., 2012).”
BackgroundYao, L.-H., Rao, Y., Chi, B., Kurilova, S., Varga, K. T., Wang, C.-Y., Weller, B. D., Cho, W., Cheng, J., & Gong, L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2171-13.2013 · Cited by 21
“Additionally, our results demonstrate that actin polymerization disruption causes an increase in the fission-pore duration, reiterating the critical role of actin polymerization in vesicle fission during CME (Merrifield et al., 2005; Yarar et al., 2005).”
Background
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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