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A Dynamic Actin Cytoskeleton Functions at Multiple Stages of Clathrin-mediated Endocytosis
Abstract
Clathrin-mediated endocytosis in mammalian cells is critical for a variety of cellular processes including nutrient uptake and cell surface receptor down-regulation. Despite the findings that numerous endocytic accessory proteins directly or indirectly regulate actin dynamics and that actin assembly is spatially and temporally coordinated with endocytosis, direct functional evidence for a role of actin during clathrin-coated vesicle formation is lacking. Here, we take parallel biochemical and microscopic approaches to address the contribution of actin polymerization/depolymerization dynamics to clathrin-mediated endocytosis. When measured using live-cell fluorescence microscopy, disruption of the F-actin assembly and disassembly cycle with latrunculin A or jasplakinolide results in near complete cessation of all aspects of clathrin-coated structure (CCS) dynamics. Stage-specific biochemical assays and quantitative fluorescence and electron microscopic analyses establish that F-actin dynamics are required for multiple distinct stages of clathrin-coated vesicle formation, including coated pit formation, constriction, and internalization. In addition, F-actin dynamics are required for observed diverse CCS behaviors, including splitting of CCSs from larger CCSs, merging of CCSs, and lateral mobility on the cell surface. Our results demonstrate a key role for actin during clathrin-mediated endocytosis in mammalian cells.
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The observed heterogeneity in the dynamic behavior of CCPs could reflect differences in their content of cargo and adaptor molecules.
“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 Yarar et al., 2005
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Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility
VALE, R., REESE, T., & SHEETZ, M. (1985) · Cell · doi:10.1016/s0092-8674(85)80099-4 · Cited by 1,993 · cited 2×
“These movements are much slower than rates reported for microtubule-based kinesin or dynein driven motility (30–60 m/min; Vale et al., 1985; Vallee et al., 1988) and are consistent with motilities mediated by actin polymerization (1.2–12 m/min; Theriot et al., 1992; Loisel et al., 1999).”
BackgroundInfluentialBubb, M. R., Senderowicz, A. M., Sausville, E. A., Duncan, K. L., & Korn, E. D. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36545-6 · Cited by 811
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
Flagged first, then by citations
Research works printed but not linked: 46
- Ayscough, K. R. (2000). Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton.Curr. Biol.10, 1587-1590. · DOI
- Axelrod, D. (2001). Total internal reflection fluorescence microscopy in cell biology.Traffic2, 764-774. · DOI
- Bennett, E. M., Chen, C. Y., Engqvist-Goldstein, A. E., Drubin, D. G., and Brodsky, F. M. (2001). Clathrin hub expression dissociates the actin-binding protein Hip1R from coated pits and disrupts their alignment with the actin cytoskeleton.Traffic2, 851-858. · DOI
- Carter, L. L., Redelmeier, T. E., Woollenweber, L. A., and Schmid, S. L. (1993). Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis.J. Cell Biol.120, 37-45. · DOI
- Conner, S. D., and Schmid, S. L. (2003). Regulated portals of entry into the cell.Nature422, 37-44. · DOI
- Coue, M., Brenner, S. L., Spector, I., and Korn, E. D. (1987). Inhibition of actin polymerization by latrunculin A.FEBS Lett.213, 316-318. · DOI
- Cramer, L. P., Briggs, L. J., and Dawe, H. R. (2002). Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells.Cell Motil. Cytoskelet.51, 27-38. · DOI
- Damke, H., Baba, T., Warnock, D. E., and Schmid, S. L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation.J. Cell Biol.127, 915-934. · DOI
- Durrbach, A., Louvard, D., and Coudrier, E. (1996). Actin filaments facilitate two steps of endocytosis.J. Cell Sci.109(Pt 2), 457-465. · DOI
- 10.1091/mbc.e03-09-0639 · DOI
- Engqvist-Goldstein, A. E., Warren, R. A., Kessels, M. M., Keen, J. H., Heuser, J., and Drubin, D. G. (2001). The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro.J. Cell Biol.154, 1209-1223. · DOI
- Ehrlich, M., Boll, W., Van Oijen, A., Hariharan, R., Chandran, K., Nibert, M. L., and Kirchhausen, T. (2004). Endocytosis by random initiation and stabilization of clathrin-coated pits.Cell118, 591-605. · DOI · Paper page
- Frischknecht, F., and Way, M. (2001). Surfing pathogens and the lessons learned for actin polymerization.Trends Cell Biol.11, 30-38. · DOI
- Fujimoto, L. M., Roth, R., Heuser, J. E., and Schmid, S. L. (2000). Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells.Traffic1, 161-171. · DOI
- Gaidarov, I., Santini, F., Warren, R. A., and Keen, J. H. (1999). Spatial control of coated-pit dynamics in living cells.Nat. Cell Biol.1, 1-7. · DOI
- Giardini, P. A., Fletcher, D. A., and Theriot, J. A. (2003). Compression forces generated by actin comet tails on lipid vesicles.Proc. Natl. Acad. Sci. USA100, 6493-6498. · DOI
- Gupton, S. L., and Waterman-Storer, C. M. (2005). Live-cell fluorescent speckle microscopy (FSM) of actin cytoskeletal dynamics and their perturbation by drug perfusion. In:Cell Biology: A Laboratory Handbook, 3rd ed., ed J. Celis and J. V. Small, New York: Elsevier (in press).
- Heuser, J. E., and Anderson, R. G. (1989). Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation.J. Cell Biol.108, 389-400. · DOI
- Kaksonen, M., Sun, Y., Drubin, D. G. (2003). A pathway for association of receptors, adaptors, and actin during endocytic internalization.Cell115,475-487. · DOI · Paper page
- Keyel, P. A., Watkins, S. C., and Traub, L. M. (2004). Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy.J. Biol. Chem.279, 13190-13204. · DOI
- Lamaze, C., Fujimoto, L. M., Yin, H. L., and Schmid, S. L. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells.J. Biol. Chem.272, 20332-20335. · DOI
- Loisel, T. P., Boujemaa, R., Pantaloni, D., and Carlier, M. F. (1999). Reconstitution of actin-based motility ofListeriaandShigellausing pure proteins.Nature401, 613-616. · DOI
- Ma, L., Cantley, L. C., Janmey, P. A., and Kirschner, M. W. (1998). Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly inXenopusegg extracts.J. Cell Biol.140, 1125-1136. · DOI
- Maples, C. J., Ruiz, W. G., and Apodaca, G. (1997). Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darby canine kidney cells.J. Biol. Chem.272, 6741-6751. · DOI
- Merrifield, C. J. (2004). Seeing is believing: imaging actin dynamics at single sites of endocytosis.Trends Cell Biol.14, 352-358. · DOI
- Merrifield, C. J., Feldman, M. E., Wan, L., and Almers, W. (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits.Nat. Cell Biol.4, 691-698. · DOI · Paper page
- Merrifield, C. J., Moss, S. E., Ballestrem, C., Imhof, B. A., Giese, G., Wunderlich, I., and Almers, W. (1999). Endocytic vesicles move at the tips of actin tails in cultured mast cells.Nat. Cell Biol.1, 72-74. · DOI
- Merrifield, C. J., Qualmann, B., Kessels, M. M., and Almers, W. (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, 13-18. · DOI
- 10.1091/mbc.e03-04-0230 · DOI
- Pantaloni, D., Le Clainche, C., and Carlier, M. F. (2001). Mechanism of actin-based motility.Science292, 1502-1506. · DOI
- Qualmann, B., and Kessels, M. M. (2002). Endocytosis and the cytoskeleton.Int. Rev. Cytol.220, 93-144. · DOI
- Qualmann, B., Kessels, M. M., and Kelly, R. B. (2000). Molecular links between endocytosis and the actin cytoskeleton.J. Cell Biol.150, F111-F116. · DOI
- Rappoport, J., Simon, S., and Benmerah, A. (2004). Understanding living clathrin-coated pits.Traffic5, 327-337. · DOI
- Rappoport, J. Z., and Simon, S. M. (2003). Real-time analysis of clathrin-mediated endocytosis during cell migration.J. Cell Sci.116, 847-855. · DOI
- Rappoport, J. Z., Taha, B. W., Lemeer, S., Benmerah, A., and Simon, S. M. (2003). The AP-2 complex is excluded from the dynamic population of plasma membrane-associated clathrin.J. Biol. Chem.278, 47357-47360. · DOI
- Rozelle, A. L., Machesky, L. M., Yamamoto, M., Driessens, M. H., Insall, R. H., Roth, M. G., Luby-Phelps, K., Marriott, G., Hall, A., and Yin, H. L. (2000). Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3.Curr. Biol.10, 311-320. · DOI
- Santini, F., Gaidarov, I., and Keen, J. H. (2002). G protein-coupled receptor/arrestin3 modulation of the endocytic machinery.J. Cell Biol.156, 665-676. · DOI · Paper page
- Schmid, S. L., and Carter, L. (1990). ATP is required for receptor-mediated endocytosis in intact cells.J. Cell Biol.111, 2307-2318. · DOI
- Sever, S., Damke, H., and Schmid, S. L. (2000). Dynamin:GTP control the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis.J. Cell Biol.150, 1137-1147. · DOI
- Slepnev, V. I., and De Camilli, P. (2000). Accessory factors in clathrin-dependent synaptic vesicle endocytosis.Nat. Rev. Neurosci.1, 161-172. · DOI
- Smythe, E., Carter, L. L., and Schmid, S. L. (1992). Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors.J. Cell Biol.119, 1163-1171. · DOI
- Steyer, J. A., and Almers, W. (2001). A real-time view of life within 100 nm of the plasma membrane.Nat. Rev. Mol. Cell. Biol.2, 268-275. · DOI
- Taunton, J., Rowning, B. A., Coughlin, M. L., Wu, M., Moon, R. T., Mitchison, T. J., and Larabell, C. A. (2000). Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP.J. Cell Biol.148, 519-530. · DOI
- Theriot, J. A., Mitchison, T. J., Tilney, L. G., and Portnoy, D. A. (1992). The rate of actin-based motility of intracellularListeria monocytogenesequals the rate of actin polymerization.Nature357, 257-260. · DOI
- Vallee, R. B., Wall, J. S., Paschal, B. M., and Shpetner, H. S. (1988). Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein.Nature332, 561-563. · DOI
- Waterman-Storer, C. M. (2002). Fluorescent speckle microscopy (FSM) of microtubules and actin in living cells. In:Current Protocols in Cell Biology, ed. J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, New York: John Wiley, Unit 4.10.
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“Typically, endocytosis that requires active actin polymerization is blocked by both treatments 58 – 60 .”
Metadata
- Authors
- Yarar, D., Waterman-Storer, C. M., & Schmid, S. L.
- Affiliations
- Department of Cell Biology, The Scripps Research Institute, La Jolla, CA 92037
- Venue
- Molecular Biology of the Cell
- Published
- 2005-02
- Volume
- 16
- Issue
- 2
- Pages
- 964-975
- ISSN
- 1059-1524
- 1939-4586
- Cited by
- 408
- References
- 3
- Language
- en
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