Real-time analysis of clathrin-mediated endocytosis during cell migration

Journal of Cell Science

Volumn 116, Issue 5, 2003, Pages 847-855

  Rappoport, Joshua Z ^a   Simon, Sanford M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Cell migration; Clathrin; Dynamin; Endocytosis; Evanescent wave microscopy; Total internal reflection fluorescence microscopy (TIR FM)

Indexed keywords

BIOLOGICAL MARKER; CLATHRIN; DYNAMIN I; DYNAMIN II; GREEN FLUORESCENT PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; CELL MIGRATION; CELL STRAIN; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; CELL LINE; CELL MOVEMENT; CLATHRIN; DYNAMIN I; DYNAMIN II; ENDOCYTOSIS; IMAGE PROCESSING, COMPUTER-ASSISTED; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; RECOMBINANT FUSION PROTEINS; TIME FACTORS; TRANSFERRIN;

ANIMALIA;

EID: 0037350449     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00289     Document Type: Review

References (46)

1. Altschuler, Y., Barbas, S. M., Terlecky, L. J., Tang, K., Hardy, S., Mostov, K. E. and Schmid, S. L. (1998). Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J. Cell Biol. 143, 1871-1881.
2. Apodaca, G. (2001). Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2, 149-159.
3. Axelrod, D. (1981). Cell-substrate contacts illuminated by total internal reflection fluorescence. J. Cell Biol. 89, 141-145.
4. Bajno, L., Peng, X. R., Schreiber, A. D., Moore, H. P., Trimble, W. S. and Grinstein, S. (2000). Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation. J. Cell Biol. 149, 697-706.
5. Benmerah, A., Bayrou, M., Cerf-Bensussan, N. and Dautry-Varsat, A. (1999). Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112, 1303-1311.
6. Benmerah, A., Lamaze, C., Begue, B., Schmid, S. L., Dautry-Varsat, A. and Cerf-Bensussan, N. (1998). AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol. 140, 1055-1062.
7. Bretscher, M. S. (1996). Moving membrane up to the front of migrating cells. Cell 85, 465-467.
8. Cao, H., Garcia, F. and McNiven, M. A. (1998). Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9, 2595-2609.
9. Carter, R. E. and Sorkin, A. (1998). Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J. Biol. Chem. 273, 35000-35007.
10. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R. and Owen, D. J. (2002). Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523-535.
11. Conrad, M. E., Umbreit, J. N. and Moore, E. G. (1999). Iron absorption and transport. Am. J. Med. Sci. 318, 213-229.
12. de Curtis, I (2001). Cell migration: GAPs between membrane traffic and the cytoskeleton. EMBO Rep. 2, 277-281.
13. Doxsey, S. J., Brodsky, F. M., Blank, G. S. and Helenius, A. (1987). Inhibition of endocytosis by anti-clathrin antibodies. Cell 50, 453-463.
14. 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.
15. Fenteany, G., Janmey, P. A. and Stossel, T. P. (2000). Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10, 831-838.
16. Fialka, I., Steinlein, P., Ahorn, H., Bock, G., Burbelo, P. D., Haberfellner, M., Lottspeich, F., Paiha, K., Pasquali, C. and Huber, L. A. (1999). Identification of syntenin as a protein of the apical early endocytic compartment in Madin-Darby canine kidney cells. J. Biol. Chem. 274, 26233-26239.
17. Fuller, S. D. and Simons, K. (1986). Transferrin receptor polarity and recycling accuracy in 'tight' and 'leaky' strains of Madin-Darby canine kidney cells. J. Cell Biol. 103, 1767-1779.
18. 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.
19. Goldberg, M. B. (2001). Actin-based motility of intracellular microbial pathogens. Microbiol. Mol. Biol. Rev. 65, 595-626.
20. Hopkins, C. R., Miller, K. and Beardmore, J. M. (1985). Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J. Cell Sci. 3 (Suppl.), 173-186.
21. Jiang, W. and Hunter, T. (1998). Analysis of cell-cycle profiles in transfected cells using a membrane- targeted GFP. Biotechniques 24, 349, 350, 352, 354.
22. Kamiguchi, H. and Lemmon, V. (2000). Recycling of the cell adhesion molecule L1 in axonal growth cones. J. Neurosci. 20, 3676-3686.
23. Kamiguchi, H., Long, K. E., Pendergast, M., Schaefer, A. W., Rapoport, I., Kirchhausen, T. and Lemmon, V. (1998). The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J. Neurosci. 18, 5311-5321.
24. Kirchhausen, T. (2002). Clathrin adaptors really adapt. Cell 109, 413-416.
25. Lamaze, C. and Schmid, S. L. (1995). Recruitment of epidermal growth factor receptors into coated pits requires their activated tyrosine kinase. J. Cell Biol. 129, 47-54.
26. Lampson, M. A., Schmoranzer, J., Zeigerer, A., Simon, S. M. and McGraw, T. E. (2001). Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles. Mol. Biol. Cell 12, 3489-3501.
27. McNiven, M. A., Kim, L., Krueger, E. W., Orth, J. D., Cao, H. and Wong, T. W. (2000). Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187-198.
28. 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.
29. Ochoa, G. C., Slepnev, V. I., Neff, L., Ringstad, N., Takei, K., Daniell, L., Kim, W., Cao, H., McNiven, M., Baron, R. et al. (2000). A functional link between dynamin and the actin cytoskeleton at podosomes. J. Cell Biol. 150, 377-389.
30. Palecek, S. P., Schmidt, C. E., Lauffenburger, D. A. and Horwitz, A. F. (1996). Integrin dynamics on the tail region of migrating fibroblasts. J. Cell Sci. 109, 941-952.
31. Pollard, T. D., Blanchoin, L. and Mullins, R. D. (2000). Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545-576.
32. Raub, T. J. and Kuentzel, S. L. (1989). Kinetic and morphological evidence for endocytosis of mammalian cell integrin receptors by using an anti-fibronectin receptor beta subunit monoclonal antibody. Exp. Cell Res. 184, 407-426.
33. Sabo, S. L., Ikin, A. F., Buxbaum, J. D. and Greengard, P. (2001). The Alzheimer amyloid precursor protein (APP) and FE65, an APP-binding protein, regulate cell movement. J. Cell Biol. 153, 1403-1414.
34. 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.
35. Schmid, S. L. (1997). Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548.
36. Schmid, S. L. and Sorkin, A. D. (2002). Days and knights discussing membrane dynamics in endocytosis: meeting report from the Euresco/EMBL Membrane Dynamics in Endocytosis, 6-11 October in Tomar, Portugal. Traffic 3, 77-85.
37. Schmoranzer, J., Goulian, M., Axelrod, D. and Simon, S. M. (2000). Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J. Cell Biol. 149, 23-32.
38. Sheetz, M. P., Felsenfeld, D., Galbraith, C. G. and Choquet, D. (1999). Cell migration as a five-step cycle. Biochem. Soc. Symp. 65, 233-243,
39. Sieczkarski, S. B. and Whittaker, G. R. (2002). Dissecting virus entry via endocytosis. J. Gen. Virol. 83, 1535-1545.
40. Sun, T. X., van Hoek, A., Huang, Y., Bouley, R., McLaughlin, M. and Brown, D. (2002). Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin. Am. J. Physiol. Renal Physiol. 282, F998-F1011.
41. Tabb, J. S., Molyneaux, B. J., Cohen, D. L., Kuznetsov, S. A. and Langford, G. M. (1998). Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234.
42. Takei, K. and Haucke, V. (2001). Clathrin-mediated endocytosis: membrane factors pull the trigger. Trends Cell Biol. 11, 385-391.
43. Takei, K., McPherson, P. S., Schmid, S. L. and de Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
44. ter Haar, E., Musacchio, A., Harrison, S. C. and Kirchhausen, T. (1998). Atomic structure of clathrin: a beta propeller terminal domain joins an alpha zigzag linker. Cell 95, 563-573.
45. Tsuboi, T., Terakawa, S., Scalettar, B. A., Fantus, C., Roder, J. and Jeromin, A. (2002). Sweeping model of dynamin activity. Visualization of coupling between exocytosis and endocytosis under an evanescent wave microscope with green fluorescent proteins. J. Biol. Chem. 277, 15957-15961.
46. Watanabe, N. and Mitchison, T. J. (2002). Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295, 1083-1086.