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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
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“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et al., 2005; Loerke et al., 2009), which express relatively high levels of Dab2 and cargo (Maurer and Cooper, 2006; unpublished data).”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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“Once a protein coat has stably assembled on this patc”
BackgroundInvasive and adherent bacterial pathogens co-Opt host clathrin for infection.
Veiga, E., Guttman, J. A., Bonazzi, M., Boucrot, E., Toledo-Arana, A., Lin, A., Enninga, J., Pizarro-Cerdá, J., Finlay, B., Kirchhausen, T., et al. (2007) · Cell Host and Microbe · doi:10.1016/j.chom.2007.10.001 · Cited by 248
“Cell Host & and Schmid, 2003; Kirchhausen, 2000), which is required for subsequent vesicle scission (Ehrlich et al., 2004; Hinshaw, 2000; Macia et al., 2006; Merrifield et al., 2005; Orth and McNiven, 2003).”
Dawson, J. C., Legg, J. A., & Machesky, L. M. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.08.004 · Cited by 242
Structural Organization of the Actin Cytoskeleton at Sites of Clathrin-Mediated Endocytosis
Collins, A., Warrington, A., Taylor, K., & Svitkina, T. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.048 · Cited by 245
“Actin polymerization was proposed to function at multiple stages of CME, including formation, invagination, constriction, and lateral movement of clathrin-coated pits, as well as scission and departure of clathrin-coated vesicles [3, 5–7, 28–30].”
The constriction and scission machineries involved in mitochondrial fission
Kraus, F., & Ryan, M. T. (2017) · Journal of Cell Science · doi:10.1242/jcs.199562 · Cited by 244
“…0000-0002-3757-541X; M.T.R., 0000-0003-2586-8829 Jo u rn al o f Ce ll Sc ie n ce only occur if the energetic state of fission is more favourable than that of not undergoing fission (Antonny et al., 2016; Mattila et al., 2015; Merrifield et al., 2005; Sundborger et al., 2014).”
BackgroundRapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells
Doyon, J. B., Zeitler, B., Cheng, J. C., Cheng, A. T., Cherone, J. M., Santiago, Y., Lee, A. H., Vo, T. D., Doyon, Y., Miller, J. C., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2175 · Cited by 227
Under Pressure: the Differential Requirements for Actin during Yeast and Mammalian Endocytosis
Aghamohammadazadeh, S., & Ayscough, K. (2009) · Nature Cell Biology · doi:10.1038/ncb1918 · Cited by 241
Cargo Regulates Clathrin-Coated Pit Dynamics
Puthenveedu, M. A., & von Zastrow, M. (2006) · Cell · doi:10.1016/j.cell.2006.08.035 · Cited by 234
“Completion of CCP maturation occurs by recruitment of a full complement of clathrin-associated proteins including the GTPase dynamin, which is required for subsequent vesicle scission (Kaksonen et al., 2005; Merrifield et al., 2002, 2005).”
Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes
Innocenti, M., Gerboth, S., Rottner, K., Lai, F. P. L., Hertzog, M., Stradal, T. E. B., Frittoli, E., Didry, D., Polo, S., Disanza, A., et al. (2005) · Nature Cell Biology · doi:10.1038/ncb1304 · Cited by 236
“More importantly, ectopically expressed Abi1 and N-WASP extensively colocalized at the cell surface in spots whose lateral mobility — which has been shown to frequently accompany the pinching off of vesicle”
Cortactin in tumor invasiveness.
Weaver, A. M. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.02.066 · Cited by 236
pHuji, a pH-sensitive red fluorescent protein for imaging of exo- and endocytosis
Shen, Y., Rosendale, M., Campbell, R. E., & Perrais, D. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201404107 · Cited by 222
Self-citationDynamics of Arabidopsis Dynamin-Related Protein 1C and a Clathrin Light Chain at the Plasma Membrane
Konopka, C. A., Backues, S. K., & Bednarek, S. Y. (2008) · The Plant Cell · doi:10.1105/tpc.108.059428 · Cited by 223
“…proposed that there is a conformational change of the dynamin oligomer upon GTP hydrolysis (Roux et al., 2006) that along with actin polymerization (Merrifield et al., 2005) and the activity of additional membrane modifying proteins promotes the release of the clathrin-coated vesicle from the…”
BackgroundInfluentialYarar, D., Waterman-Storer, C., & Schmid, S. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.04.014 · Cited by 224
“…plays a role in membrane remodeling events such as protrusion during macropinocytosis, invagination during clathrin- and caveolin-dependent endocytosis, and vesicle fission (Kaksonen et al., 2006; Merrifield et al., 2002, 2005; Pelkmans et al., 2002; Swanson and Watts, 1995; Yarar et al., 2005).”
BackgroundActin regulation in endocytosis
Smythe, E., & Ayscough, K. R. (2006) · Journal of Cell Science · doi:10.1242/jcs.03247 · Cited by 205
“Another Arp2/3 activator, cortactin, is also recruited to coated pits, attaining maximal levels at scission (Merrifield et al., 2005).”
BackgroundInfluentialThe Mechanochemistry of Endocytosis
Liu, J., Sun, Y., Drubin, D. G., & Oster, G. F. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000204 · Cited by 222
“Multicolor real-time fluorescence microscopy studies in mammalian cells and yeast established that proteins are sequentially recruited to the endocytic site to drive membrane invagination and vesicle scission [3,4,5,6,7,8,9,10,11,12].”
BackgroundActin and dynamin2 dynamics and interplay during clathrin-mediated endocytosis
Grassart, A., Cheng, A. T., Hong, S. H., Zhang, F., Zenzer, N., Feng, Y., Briner, D. M., Davis, G. D., Malkov, D., & Drubin, D. G. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201403041 · Cited by 196
“…organization By studying the dynamics of clathrin at the plasma membrane, several groups have observed high heterogeneity in clathrin lifetime (Ehrlich et al., 2004; Merrifield et al., 2005; Yarar et al., 2005; Loerke et al., 2009; Boulant et al., 2011; Banerjee et al., 2012; Taylor et al., 2012).”
Chadda, R., Howes, M. T., Plowman, S. J., Hancock, J. F., Parton, R. G., & Mayor, S. (2007) · Traffic : the International Journal of Intracellular Transport · doi:10.1111/j.1600-0854.2007.00565.x · Cited by 218
Imaging endocytic clathrin structures in living cells
Kirchhausen, T. L. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.09.002 · Cited by 199
“To obtain temporal information regarding the time of membrane scission from the donor plasma membrane of the budding clathrin-coated membrane, a visual method was used to detect the exposure or protection from the incubation medium of the ectodomain of the transferrin (Tf) receptor [ 26 ].”
InfluentialWASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond.
Rottner, K., Hänisch, J., & Campellone, K. G. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.08.014 · Cited by 204
Kiss‐and‐run and full‐collapse fusion as modes of exo‐endocytosis in neurosecretion
Harata, N. C., Aravanis, A. M., & Tsien, R. W. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03987.x · Cited by 190
Cdc42 and Vesicle Trafficking in Polarized Cells
Harris, K. P., & Tepaß, U. (2010) · Traffic · doi:10.1111/j.1600-0854.2010.01102.x · Cited by 187
“Also, actin dynamics are involved in several aspects of vesicle formation (34), and WASp and Arp2/3 have been implicated indirectly in the process of scission (63,64).”
BackgroundA new role for cortactin in invadopodia: regulation of protease secretion.
Clark, E. S., & Weaver, A. M. (2008) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2008.01.008 · Cited by 193
“Indeed, in endocytosis, cortactin and dynamin are both important and may function together in vesicle fission and/or movement away from the membrane (Cao et al., 2003; Lanzetti, 2007; Merrifield et al., 2005; Weed and Parsons, 2001; Zhu et al., 2005).”
BackgroundActin in membrane trafficking.
Lanzetti, L. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.04.017 · Cited by 193
Cortactin: The Gray Eminence of the Cytoskeleton
Cosen-Binker, L. I., & Kapùs, A. (2006) · Physiology · doi:10.1152/physiol.00012.2006 · Cited by 192
“(69) studied the dynamics of individual CCPs using evanescent field microscopy and a witty technique, the pH-sensitive labeling of transferrin receptors, with which the closure and scission of CCPs can be resolved in real time.”
BackgroundCureton, D., Massol, R. H., Whelan, S. P. J., & Kirchhausen, T. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001127 · Cited by 184
Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains.
Co, C., Wong, D. T., Gierke, S., Chang, V., & Taunton, J. (2007) · Cell · doi:10.1016/j.cell.2006.12.049 · Cited by 182
Jain, K. (2008) · Humana Press · doi:10.1007/978-1-61779-983-9 · Cited by 179
Soykan, T., Kaempf, N., Sakaba, T., Vollweiter, D., Goerdeler, F., Puchkov, D., Kononenko, N. L., & Haucke, V. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.011 · Cited by 178
Dynamics of Endocytic Vesicle Creation
Perrais, D., & Merrifield, C. J. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.10.002 · Cited by 162
Self-citationCargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis
Mettlen, M., Loerke, D., Yarar, D., Danuser, G., & Schmid, S. L. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200908078 · Cited by 177
“…as sites at which multiple rounds of CCV formation were observed to occur from an apparently single CCP. Nonterminal events are frequently observed in HeLa cells (Merrifield et al., 2005; Loerke et al., 2009), but rarely detected in control BSC1 cells (Ehrlich et al., 2004; Loerke et al., 2009).”
BackgroundInfluentialTwo synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages
Perera, R. M., Zoncu, R., Lucast, L., Camilli, P. V. D., & Toomre, D. K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609795104 · Cited by 187
Focusing on clathrin-mediated endocytosis.
Rappoport, J. Z. (2008) · Biochemical Journal · doi:10.1042/bj20080474 · Cited by 172
A Feedback Loop between Dynamin and Actin Recruitment during Clathrin-Mediated Endocytosis
Taylor, M. J., Lampe, M., & Merrifield, C. J. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001302 · Cited by 142
“This finding is consistent with previous studies that have observed latrunculinresistant clathrin endocytic events [7,33,47,48].”
MethodInfluentialSelf-citationSirotkin, V., Berro, J., Macmillan, K., Zhao, L., & Pollard, T. D. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-02-0157 · Cited by 166
Subcellular membrane curvature mediated by the BAR domain superfamily proteins
Suetsugu, S., Toyooka, K., & Senju, Y. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.12.002 · Cited by 155
Kirkbride, K. C., Sung, B., Sinha, S., & Weaver, A. M. (2011) · Cell Adhesion & Migration · doi:10.4161/cam.5.2.14773 · Cited by 164
Membrane deformation by protein coats.
Antonny, B. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.06.003 · Cited by 163
Antonescu, C. N., Aguet, F., Danuser, G. M., & Schmid, S. L. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-04-0362 · Cited by 180
“…we and others have begun to establish a temporal hierarchy of functional requirements of EAPs in CCP initiation, stabilization, and maturation (Merrifield et al., 2005; Rappoport et al., 2006; Saffarian and Kirchhausen, 2008; Mettlen et al., 2009; Loerke et al., 2011; Taylor et al., 2011).”
BackgroundDynamin recruitment and membrane scission at the neck of a clathrin-coated pit
Cocucci, E., Gaudin, R., & Kirchhausen, T. L. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-07-1240 · Cited by 142
“…neck of a coated pit and release of a coated vesicle from the plasma membrane coincide with a peak in dynamin recruitment (Ehrlich et al., 2004; Merrifield et al., 2005; Taylor et al., 2011, 2012; Aguet et al., 2013), but direct information concerning the number of dynamin molecules that…”
BackgroundRole of lipids and actin in the formation of clathrin-coated pits
Boucrot, E., Saffarian, S., Massol, R., Kirchhausen, T. L., & Ehrlich, M. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.09.025 · Cited by 145
Molecular basis for SH3 domain regulation of F-BAR–mediated membrane deformation
Rao, Y., Ma, Q., Vahedi-Faridi, A., Sundborger, A., Pechstein, A., Puchkov, D., Luo, L., Shupliakov, O., Saenger, W., & Haucke, V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003478107 · Cited by 149
Wu, M., Huang, B., Graham, M. M., Raimondi, A., Heuser, J. E., Zhuang, X., & Camilli, P. V. D. (2010) · Nature Cell Biology · doi:10.1038/ncb2094 · Cited by 141
The cellular functions of clathrin
Royle, S. J. (2006) · Cellular and Molecular Life Sciences (CMLS) · doi:10.1007/s00018-005-5587-0 · Cited by 148
Cortactin has an essential and specific role in osteoclast actin assembly.
Tehrani, S., Faccio, R., Chandrasekar, I., Ross, F., & Cooper, J. A. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-03-0187 · Cited by 146
“This viral titer had no cytotoxic effects on target cells.”
BackgroundEndocytic adaptors: recruiters, coordinators and regulators
Maldonado‐Báez, L., & Wendland, B. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.08.001 · Cited by 123
Clathrin‐Coated Pits: Vive La Différence?
Benmerah, A., & Lamaze, C. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00585.x · Cited by 142
Imaging single events at the cell membrane.
Jaiswal, J., & Simon, S. (2007) · Nature Chemical Biology · doi:10.1038/nchembio855 · Cited by 135
Keyel, P. A., Mishra, S. K., Roth, R., Heuser, J. E., Watkins, S. C., & Traub, L. M. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-05-0421 · Cited by 134
“Protein levels were standardized using a Coomassie blue–based filter paper binding assay (Minamide and Bamburg, 1990); 25 g was loaded per lane.”
MethodAlto, N. M., Weflen, A. W., Rardin, M. J., Yarar, D., Lazar, C., Tonikian, R., Koller, A., Taylor, S. S., Boone, C., Sidhu, S., et al. (2007) · Journal of Cell Biology · doi:10.1083/jcb.200705021 · Cited by 134
Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism
Moreno-Ruiz, E., Galán-Díez, M., Zhu, W., Fernández-Ruiz, E., d'Enfert, C., Filler, S. G., Cossart, P., & Veiga, E. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01319.x · Cited by 133
“…C. albicans internalization The GTPase dynamin is required for clathrin-coated pits to pinch off the plasma membrane and form endocytic vesicles (Hinshaw, 2000; Kirchhausen, 2000; Conner and Schmid, 2003; Orth and McNiven, 2003; Ehrlich et al., 2004; Merrifield et al., 2005; Macia et al., 2006).”
BackgroundRecruitment dynamics of GAK and auxilin to clathrin-coated pits during endocytosis
Lee, D., Wu, X., Eisenberg, E., & Greene, L. E. (2006) · Journal of Cell Science · doi:10.1242/jcs.03092 · Cited by 129
“…field about 30 seconds after it disappeared from the evanescent field (Merrifield et al., 2002); also during the period of decreasing dynamin and clathrin intensity, actin, Arp2/3 and cortactin were recruited to the CCPs (Merrifield et al., 2002; Merrifield et al., 2004; Merrifield et al., 2005).”
BackgroundResultInfluential
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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