Recruitment dynamics of GAK and auxilin to clathrin-coated pits during endocytosis

Journal of Cell Science

Volumn 119, Issue 17, 2006, Pages 3502-3512

  Lee, Dong Won ^a   Wu, Xufeng ^a   Eisenberg, Evan ^a   Greene, Lois E ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Auxilin; Clathrin; Dynamin; GAK; TIRF

Indexed keywords

ACTIN; AUXILIN; CLATHRIN; CYCLIN G ASSOCIATED KINASE; DYNAMIN; HEAT SHOCK COGNATE PROTEIN 70; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRUCTURE; CELL VACUOLE; COATED VESICLE; CONTROLLED STUDY; DEPOLYMERIZATION; ENDOCYTOSIS; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN TRANSPORT;

ANIMALS; AUXILINS; CATTLE; CLATHRIN; COATED PITS, CELL-MEMBRANE; DNA MUTATIONAL ANALYSIS; DYNAMINS; ENDOCYTOSIS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPIDS; MICROSCOPY, FLUORESCENCE; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS;

EID: 33749392024     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03092     Document Type: Article

References (37)

1. Bar-Zvi, D., Mosley, S. T. and Branton, D. (1988). In vivo phosphorylation of clathrin-coated vesicle proteins from rat reticulocytes. J. Biol. Chem. 263, 4408-4415.
2. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
3. Cremona, O., Di Paolo, G., Weak, M. R., Luthi, A., Kim, W. T., Takei, K., Daniell, L., Nemoto, Y., Shears, S. B., Flavell, R. A. et a]. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188.
4. Damke, H., Gossen, M., Freundlieb, S., Bujard, H. and Schmid, S. L. (1995). Tightly regulated and inducible expression of dominant interfering dynamin mutant in stably transformed HeLa cells. Meth. Enzymol. 257, 209-220.
5. 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. Cell 118, 591-605.
6. Ford, M. G., Pearse, B. M., Higgins, M. K., Vallis, Y., Owen, D. J., Gibson, A., Hopkins, C. R., Evans, P. R. and McMahon, H. T. (2001). Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055.
7. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praeficke, G. J., Evans, P. R. and McMahon, H. T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
8. 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.
9. Greene, L. E. and Eisenberg, E. (1990). Dissociation of clathrin from coated vesicles by the uncoating AT?ase. J. Biol. Chem. 265, 6682-6687.
10. Greener, T., Zhao, X., Nojima, H., Eisenberg, E. and Greene, L. E. (2000). Role of cyclin G-associated kinase in uncoating clathrin-coated vesicles from non-neuronal cells. J. Biol. Chem. 275, 1365-1370.
11. Haynie, D. T. and Ponting, C. P. (1996). The N-terminal domains of tensin and auxilin are phospbatase homologues. Protein Sci. 5, 2643-2646.
12. Hinshaw, J. E. (2000). Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483-519.
13. Jiang, R., Gao, B., Prasad, K., Greene, L. E. and Eisenberg, E. (2000). Hsc70 chaperones clathrin and primes it to interact with vesicle membranes. J. Biol. Chem. 275, 8439-8447.
14. Keyel, P. A., Watkins, S. M. and Traub, L. (2004). Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy. J. Biol. Chem. 279, 13190-13204.
15. Lee, D. W., Zhao, X., Eisenberg, E. and Greene, L. E. (2005). Depletion of GAK/Auxilin 2 inhibits receptor-mediated endocytosis and recruitment of both clathrin and clathrin adaptors. J Cell Sci. 118, 4311-4321.
16. 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.
17. 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.
18. Merrifield, C. J., Perrais, D. and Zenisek, D. (2005). Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606.
19. Moskowitz, H. S., Heuser, J., McGraw, T. E. and Ryan, T. A. (2003). Targeted chemical disruption of clathrin function in living cells. Mol. Biol. Cell 14, 4437-4447.
20. Motley, A., Bright, N. A., Seaman, M. N. and Robinson, M. S. (2003). Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162, 909-918.
21. Newmyer, S. L., Christensen, A. and Sever, S. (2003). Auxilin-dynamin interactions link the uncoating ATPase chaperone machinery with vesicle formation. Dev. Cell 4, 929-940.
22. Rappoport, J. Z. and Simon, S. M. (2003). Real-time analysis of clathrin-mediated endocytosis during cell migration. J. Cell Sci. 116, 847-855.
23. Rappoport, J. Z., Taha, B. W., Lemeer, S., Bemnerah, 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.
24. Rappoport, J. Z., Benmerah, A. and Simon, S. M. (2005). Analysis of the AP-2 adaptor complex and cargo during clathrin-mediated endocytosis. Traffic 6, 539-547.
25. Roux, A., Uyhazi, K., Frost, A. and De Camilli, P. (2006). GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441, 528-531.
26. Scheele, U., Kalthoff, C. and Ungewickell, E. (2001). Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex. J. Biol. Chem. 276, 36131-36138.
27. Schlossman, D. M., Schmid, S. L., Braell, W. A. and Rothman, J. E. (1984). An enzyme that removes clathrin coats: purification of an uncoating ATPase. J. Cell Biol. 99, 723-733.
28. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
29. Umeda, A., Meyerholz, A. and Ungewickell, E. (2000). Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation. Eur. J. Cell Biol. 79, 336-342.
30. Ungewickell, E., Ungewickell, H., Holstein, S. E., Lindner, R., Prasad, K., Barouch, W., Martin, B., Greene, L. E. and Eisenberg, E. (1995). Role of auxilin in uncoating clathrin-coated vesicles. Nature 378, 632-635.
31. Wenk, M. R. and De Camilli, P. (2004). Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sei. USA 101, 8262-8269.
32. Wu, X., Zhao, X., Baylor, L., Kaushal, S., Eisenberg, E. and Greene, L. E. (2001). Clathrin exchange during clathrin-mediated endocytosis. J. Cell Biol. 155, 291-300.
33. Wu, X., Zhao, X., Puertollano, R., Bonifacino, J. S., Eisenberg, E. and Greene, L. E. (2003). Adaptor and clathrin exchange at the plasma membrane and trans-Golgi network. Mol. Biol. Cell 14, 516-528.
34. Yarar, D., Waterman-Storer, C. M. and Schmid, S. L. (2005). A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol. Biol. Cell 16, 964-975.
35. Yim, Y. I., Scarselletta, S., Zang, F., Wu, X., Lee, D. W., Kang, Y. S., Eisenberg, E. and Greene, L. E. (2005). Exchange of clathrin, AP2 and epsin on clathrin-coated pits in permeabilized tissue culture cells. J. Cell Sci. 118, 2405-2413.
36. Zeng, X. C., Bhasin, S., Wuq X., Lee, J. G., Maffi, S., Nichols, C. J., Lee, K. J., Taylor, J. P., Greene, L. E. and Eisenberg, E. (2004). Hsp70 dynamics in vivo: effect of heat shock and protein aggregation. J. Cell Sci. 117, 4991-5000.
37. Zhao, X., Greener, T., Al-Hasani, H., Cushman, S. W., Eisenberg, E. and Greene, L. E. (2001). Expression of auxilin or AP180 inhibits endocytosis by mislocalizing clathrin: evidence for formation of nascent pits containing AP1 or AP2 but not clathrin. J. Cell Sci. 114, 353-363.