The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
A Modular Design for the Clathrin- and Actin-Mediated Endocytosis Machinery
Open accessAbstract
Endocytosis depends on an extensive network of interacting proteins that execute a series of distinct subprocesses. Previously, we used live-cell imaging of six budding-yeast proteins to define a pathway for association of receptors, adaptors, and actin during endocytic internalization. Here, we analyzed the effects of 61 deletion mutants on the dynamics of this pathway, revealing functions for 15 proteins, and we analyzed the dynamics of 8 of these proteins. Our studies provide evidence for four protein modules that cooperate to drive coat formation, membrane invagination, actin-meshwork assembly, and vesicle scission during clathrin/actin-mediated endocytosis. We found that clathrin facilitates the initiation of endocytic-site assembly but is not needed for membrane invagination or vesicle formation. Finally, we present evidence that the actin-meshwork assembly that drives membrane invagination is nucleated proximally to the plasma membrane, opposite to the orientation observed for previously studied actin-assembly-driven motility processes.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“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 [54]
Citations
Cites
Actin Assembly and Endocytosis: From Yeast to Mammals
Engqvist-Goldstein, Å. E. Y., & Drubin, D. G. (2003) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.19.111401.093127 · Cited by 572
Self-citationMerrifield, C. J., Perrais, D., & Zenisek, D. (2005) · Cell · doi:10.1016/j.cell.2005.03.015 · Cited by 476 · cited 2×
“The Rvs proteins arrive after the actin marker Abp1p has started to accumulate but reach their peak fluorescence intensity together with Abp1p (Figures 6B and 6C), consistent with the timing of scission during mammalian endocytosis (Merrifield et al., 2005).”
Flagged first, then by citations
Research works printed but not linked: 48
- Adams, 1991, Requirement of yeast fimbrin for actin organization and morphogenesis in vivo, Nature, 354, 404, 10.1038/354404a0 · DOI
- Amatruda, 1992, Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast, J. Cell Biol., 119, 1151, 10.1083/jcb.119.5.1151 · DOI
- Ayscough, 1997, High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A, J. Cell Biol., 137, 399, 10.1083/jcb.137.2.399 · DOI
- Baggett, 2001, Clathrin function in yeast endocytosis, Traffic, 2, 297, 10.1034/j.1600-0854.2001.002005297.x · DOI
- Balguerie, 1999, Rvs167p, the budding yeast homolog of amphiphysin, colocalizes with actin patches, J. Cell Sci., 112, 2529, 10.1242/jcs.112.15.2529 · DOI
- Belmont, 1998, The yeast V159N actin mutant reveals roles for actin dynamics in vivo, J. Cell Biol., 142, 1289, 10.1083/jcb.142.5.1289 · DOI
- Campbell, 2002, A monomeric red fluorescent protein, Proc. Natl. Acad. Sci. USA, 99, 7877, 10.1073/pnas.082243699 · DOI
- Chu, 1996, The light chain subunit is required for clathrin function in Saccharomyces cerevisiae, J. Biol. Chem., 271, 33123, 10.1074/jbc.271.51.33123 · DOI
- Cope, 1999, Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast, J. Cell Biol., 144, 1203, 10.1083/jcb.144.6.1203 · DOI
- Doyle, 1996, Movement of yeast cortical actin cytoskeleton visualized in vivo, Proc. Natl. Acad. Sci. USA, 93, 3886, 10.1073/pnas.93.9.3886 · DOI
- Ehrlich, 2004, Endocytosis by random initiation and stabilization of clathrin-coated pits, Cell, 118, 591, 10.1016/j.cell.2004.08.017 · DOI · Paper page
- Evangelista, 2000, A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex, J. Cell Biol., 148, 353, 10.1083/jcb.148.2.353 · DOI
- Fazi, 2002, Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: structural and functional analysis, J. Biol. Chem., 277, 5290, 10.1074/jbc.M109848200 · DOI
- Geli, 1996, Role of type I myosins in receptor-mediated endocytosis in yeast, Science, 272, 533, 10.1126/science.272.5261.533 · DOI
- Goode, 2001, Activation of the Arp2/3 complex by the actin filament binding protein Abp1p, J. Cell Biol., 153, 627, 10.1083/jcb.153.3.627 · DOI
- Holtzman, 1993, Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae, J. Cell Biol., 122, 635, 10.1083/jcb.122.3.635 · DOI
- Howard, 2002, Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis, J. Cell Biol., 157, 315, 10.1083/jcb.200110027 · DOI
- Huckaba, 2004, Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae, J. Cell Biol., 167, 519, 10.1083/jcb.200404173 · DOI
- Jonsdottir, 2004, Dynamics of yeast Myosin I: evidence for a possible role in scission of endocytic vesicles, Curr. Biol., 14, 1604, 10.1016/j.cub.2004.08.055 · DOI
- Kaksonen, 2003, A pathway for association of receptors, adaptors, and actin during endocytic internalization, Cell, 115, 475, 10.1016/S0092-8674(03)00883-3 · DOI · Paper page
- Kim, 2004, Capping protein binding to actin in yeast: biochemical mechanism and physiological relevance, J. Cell Biol., 164, 567, 10.1083/jcb.200308061 · DOI
- Lechler, 2000, Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization, J. Cell Biol., 148, 363, 10.1083/jcb.148.2.363 · DOI
- Martin, 2005, Effects of Arp2 and Arp3 nucleotide-binding pocket mutations on Arp2/3 complex function, J. Cell Biol., 168, 315, 10.1083/jcb.200408177 · DOI
- McCann, 1997, The I/LWEQ module: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals, Proc. Natl. Acad. Sci. USA, 94, 5679, 10.1073/pnas.94.11.5679 · DOI
- Merrifield, 2002, Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits, Nat. Cell Biol., 4, 691, 10.1038/ncb837 · DOI · Paper page
- Merrifield, 2004, Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts, Eur. J. Cell Biol., 83, 13, 10.1078/0171-9335-00356 · DOI
- Mochida, 2002, The novel adaptor protein, Mti1p, and Vrp1p, a homolog of Wiskott-Aldrich syndrome protein-interacting protein (WIP), may antagonistically regulate type I myosins in Saccharomyces cerevisiae, Genetics, 160, 923, 10.1093/genetics/160.3.923 · DOI
- Naqvi, 1998, The WASp homologue Las17p functions with the WIP homologue End5p/verprolin and is essential for endocytosis in yeast, Curr. Biol., 8, 959, 10.1016/S0960-9822(98)70396-3 · DOI
- Newpher, 2005, In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast, Dev. Cell, 9, 87, 10.1016/j.devcel.2005.04.014 · DOI
- Pantaloni, 2001, Mechanism of actin-based motility, Science, 292, 1502, 10.1126/science.1059975 · DOI
- Payne, 1988, Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain-deficient yeast, J. Cell Biol., 106, 1453, 10.1083/jcb.106.5.1453 · DOI
- Peter, 2004, BAR domains as sensors of membrane curvature: the amphiphysin BAR structure, Science, 303, 495, 10.1126/science.1092586 · DOI · Paper page
- Rodal, 2003, Negative regulation of yeast WASp by two SH3 domain-containing proteins, Curr. Biol., 13, 1000, 10.1016/S0960-9822(03)00383-X · DOI
- Rodal, 2005, Actin and septin ultrastructures at the budding yeast cell cortex, Mol. Biol. Cell, 16, 372, 10.1091/mbc.e04-08-0734 · DOI
- Sekiya-Kawasaki, 2003, Dynamic phosphoregulation of the cortical actin cytoskeleton and endocytic machinery revealed by real-time chemical genetic analysis, J. Cell Biol., 162, 765, 10.1083/jcb.200305077 · DOI
- Sivadon, 1995, Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin, Mol. Gen. Genet., 246, 485, 10.1007/BF00290452 · DOI
- Smith, 2001, The life cycle of actin patches in mating yeast, J. Cell Sci., 114, 1505, 10.1242/jcs.114.8.1505 · DOI
- Stefan, 2005, The phosphoinositide phosphatase Sjl2 is recruited to cortical actin patches in the control of vesicle formation and fission during endocytosis, Mol. Cell. Biol., 25, 2910, 10.1128/MCB.25.8.2910-2923.2005 · DOI
- Takei, 1999, Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis, Nat. Cell Biol., 1, 33, 10.1038/9004 · DOI
- Tang, 1997, EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae, Mol. Cell. Biol., 17, 4294, 10.1128/MCB.17.8.4294 · DOI
- Tang, 2000, Pan1p, End3p, and S1a1p, three yeast proteins required for normal cortical actin cytoskeleton organization, associate with each other and play essential roles in cell wall morphogenesis, Mol. Cell. Biol., 20, 12, 10.1128/MCB.20.1.12-25.2000 · DOI
- Taunton, 2000, Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP, J. Cell Biol., 148, 519, 10.1083/jcb.148.3.519 · DOI
- Theriot, 1992, The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization, Nature, 357, 257, 10.1038/357257a0 · DOI
- Toshima, 2005, Phosphoregulation of Arp2/3-dependent actin assembly during receptor-mediated endocytosis, Nat. Cell Biol., 7, 246, 10.1038/ncb1229 · DOI
- Wach, 1997, Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae, Yeast, 13, 1065, 10.1002/(SICI)1097-0061(19970915)13:11<1065::AID-YEA159>3.0.CO;2-K · DOI
- Warren, 2002, Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics, J. Cell Sci., 115, 1703, 10.1242/jcs.115.8.1703 · DOI
- Yarar, 2005, A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis, Mol. Biol. Cell, 16, 964, 10.1091/mbc.e04-09-0774 · DOI · Paper page
- Young, 2004, Yeast actin patches are networks of branched actin filaments, J. Cell Biol., 166, 629, 10.1083/jcb.200404159 · DOI
Cited by
Sorted by citations
Cell mechanics and the cytoskeleton
Fletcher, D. A., & Mullins, R. D. (2010) · Nature · doi:10.1038/nature08908 · Cited by 3,195
Molecular mechanism and physiological functions of clathrin-mediated endocytosis
McMahon, H. T., & Boucrot, E. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3151 · Cited by 2,223
“Pathway modularity At the heart of clathrin-coated vesicle formation is a flexible network of interactions, which can be thought of as being made up of different module”
BackgroundMechanisms of clathrin-mediated endocytosis
Kaksonen, M., & Roux, A. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.132 · Cited by 1,698
Self-citationHenne, W. M., Buchkovich, N. J., & Emr, S. D. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.05.015 · Cited by 1,586
“…of the heterodimeric Bin/Amphiphysin/Rvs (BAR) domain-containing complex Rvs161/Rvs167 promotes scission by generating Developmental Cell 21, July 19, 2011 ª2011 Elsevier Inc. 83 a highly curved vesicle neck that is stressed by the pulling forces of actin polymerization (Kaksonen et al., 2005).”
BackgroundThe ARP2/3 complex: an actin nucleator comes of age
Goley, E. D., & Welch, M. D. (2006) · Nature reviews. Molecular cell biology · doi:10.1038/nrm2026 · Cited by 1,106
“cerevisiae , the ARP2/3 complex and NPFs including Pan1, myosin-5, Las17 (the WASP homologue) and Abp1 are recruited to endocytic sites prior to, or concomitant with, actin polymerizatio”
Background
Metadata
- Authors
- Kaksonen, M., Toret, C. P., & Drubin, D. G.
- Affiliations
- University of California, Berkeley (US)
- Corresponding author
- Drubin, David G.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2005-10
- Volume
- 123
- Issue
- 2
- Pages
- 305-320
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2106252068
- Cited by
- 726
- References
- 0
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 15 · 2023: 22 · 2022: 35 · 2021: 23 · 2020: 27 · 2019: 24 · 2018: 37 · 2017: 26 · 2016: 31 · 2015: 34 · 2014: 40 · 2013: 50 · 2012: 45
- FWCI
- 17.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2882 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Sigrid Juséliuksen Säätiö
- National Institutes of Health (1s10rr019290-01)
- National Institute of General Medical Sciences (R01GM042759, R01GM050399)
- National Center for Research Resources (S10-RR019290)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- clathrin-mediated endocytosis, Saccharomyces cerevisiae, deletion mutants, protein modules, membrane invagination, vesicle scission, protein dynamics
- MeSH terms
- Red Fluorescent Protein, Actins, Carrier Proteins, Cell Membrane, Clathrin, Cytoskeletal Proteins, Endocytosis, Fungal Proteins, Kinetics, Luminescent Proteins, Membrane Glycoproteins, Microfilament Proteins, Models, Biological, Saccharomyces cerevisiae, Biomarkers, Gene Deletion, Clathrin-Coated Vesicles, Saccharomyces cerevisiae Proteins, Green Fluorescent Proteins, Actin Capping Proteins
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