Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts

Nature Cell Biology

Volumn 9, Issue 12, 2007, Pages 1381-1391

  Balasubramanian, Nagaraj ^a   Scott, David W ^a   Castle, J David ^a   Casanova, James E ^a   Schwartz, Martin Alexander ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHOLERA TOXIN B SUBUNIT; F ACTIN; FIBRONECTIN; GANGLIOSIDE MANNOSIDE 1; MANNOSIDE; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ANCHORAGE; CELL MEMBRANE; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; FIBROBLAST; LIPID RAFT; MEMBRANE BINDING; MICROTUBULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACTINS; ADP-RIBOSYLATION FACTORS; ANIMALS; CELL ADHESION; CELL SHAPE; CELLS, CULTURED; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EXOCYTOSIS; FIBROBLASTS; FIBRONECTINS; GOLGI APPARATUS; MEMBRANE MICRODOMAINS; MICE; MICROTUBULES; RAC1 GTP-BINDING PROTEIN;

EID: 36749073357     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1657     Document Type: Article

References (49)

1. del Pozo, M.A. et al. Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839-842 (2004).
2. del Pozo, M.A. et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nature Cell Biol 7, 901-908 (2005).
3. Palazzo, A. F., Eng, C. H., Schlaepfer, D. D., Marcantonio, E. E. & Gundersen, G. G. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303, 836-839 (2004).
4. Vasanji, A., Ghosh, P. K., Graham, L. M., Eppell, S. J. & Fox, P. L. Polarization of plasma membrane microviscosity during endothelial cell migration. Dev. Cell 6, 29-41 (2004).
5. 2-rich raft assemblies. Biochem. Soc. Symp. 72, 119-127 (2005).
6. Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1, 31-39 (2000).
7. Hancock, J. F. Lipid rafts: Contentious only from simplistic standpoints. Nature Rev. Mol. Cell Biol. 7, 456-462 (2006).
8. Manes, S. et al. Membrane raft microdomains mediate front-rear polarity in migrating cells. EMBO J. 18, 6211-6220 (1999).
9. Gaus, K., Le Lay, S., Balasubramanian, N. & Schwartz, M. A. Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 174, 725-734 (2006).
10. Donaldson, J. G. Multiple roles for Arf6: Sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576 (2003).
11. D'Souza-Schorey, C. & Chavrier, R ARF proteins: Roles in membrane traffic and beyond. Nature Rev. Mol. Cell Biol. 7, 347-358 (2006).
12. Sabe, H. Requirement for Arf6 in cell adhesion, migration, and cancer cell invasion. J. Biochem. (Tokyo) 134, 485-489 (2003).
13. Radhakrishna, H., Al-Awar, O., Khachikian, Z. & Donaldson, J. G. ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J. Cell Sci. 112, 855-866 (1999).
14. Cheung, H. T. & Terry, D. S. Effects of nocodazole, a new synthetic microtubule inhibitor, on movement and spreading of mouse peritoneal macrophages. Cell Biol. Int Rep. 4, 1125-1129 (1980).
15. Gundersen, G. G. & Bulinski, J. C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl Acad. Sci. USA 85, 5946-5950 (1988).
16. Krendel, M., Zenke, F. T. & Bokoch, G. M. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nature Cell Biol. 4, 294-301 (2002).
17. Le, P. U. & Nabi, I. R. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J. Cell Sci. 116, 1059-1071 (2003).
18. Prigozhina, N. L. & Waterman-Storer, C. M. Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr. Biol. 14, 88-98 (2004).
19. Presley, J. F. et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81-85 (1997).
20. Pelkmans, L., Kartenbeck, J. & Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature Cell Biol. 3, 473-483 (2001).
21. Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GPI-anchored proteins are delivered to recycling endosomesvia a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411-423 (2002).
22. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. & Parton, R. G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924 (1996).
23. Yamashiro, D. J. & Maxfield, F. R. Acidification of endocytic compartments and the intracellular pathways of ligands and receptors. J. Cell Biochem. 26, 231-246 (1984).
24. Weigert, R., Yeung, A. C., Li, J. & Donaldson, J. G. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol. Biol. Cell 15, 3758-3770 (2004).
25. D'Souza-Schorey, C. & Chavrier, P. ARF6 targets recycling vesicles to the plasma membrane: Insights from an ultrastructural investigation. J. Cell Biol. 140, 603-616 (1998).
26. Zhang, Q., Calafat, J., Janssen, H. & Greenberg, S. ARF6 is required for growth factor- and rac-mediated membrane ruffling in macrophages at a stage distal to rac membrane targeting. Mol. Cell. Biol. 19, 8158-8168 (1999).
27. Song, J., Khachikian, Z., Radhakrishna, H. & Donaldson, J. G. Localization of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J. Cell Sci. 111, 2257-2267 (1998).
28. Price, L. S., Leng, J., Schwartz, M. A. & Bokoch, G. M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol, Cell 9, 1863-1871 (1998).
29. del Pozo, M. A., Price, L. S., Alderson, N. B., Ren, X. D. & Schwartz, M. A. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19, 2008-2014 (2000).
30. Santy, L. C. & Casanova, J. E. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610 (2001).
31. Goldfinger, L. E., Ptak, C., Jeffery, E. D., Shabanowitz, J., Hunt, D. F., Ginsberg, M. H. RLIP76 (RaIBP1) is an R-Ras effector that mediates adhesion-dependent Rac activation and cell migration. J. Cell Biol. 174, 877-888 (2006).
32. Santy, L. C. Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J. Biol. Chem. 277, 40185-40188 (2002).
33. Schmoranzer, J., Kreitzer, G. & Simon, S. M. Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J. Cell Sci. 116, 4513-4519 (2003).
34. Ren, Y., Li, R., Zheng, Y. & Busch, H. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273, 34954-34960 (1998).
35. Kawasaki, Y. et al. Asef, a link between the tumor suppressor APG and G-protein signaling. Science 289, 1194-1197 (2000).
36. Torgersen, M. L., Skretting, G., van Deurs, B. & Sandvig, K. Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114, 3737-3747 (2001).
37. Nabi, I. R. & Le, P. U. Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673-677 (2003).
38. Nichols, B. J. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nature Cell Biol. 4, 374-378 (2002).
39. 2 rafts. EMBO J. 20, 4332-4336 (2001).
40. Pletjushkina, O. J. et al. Induction of cortical oscillations in spreading cells by depolymerization of microtubules. Cell Motil. Cytoskel. 48, 235-244 (2001).
41. Rosania, G. R. & Swanson, J, A. Microtubules can modulate pseudopod activity from a distance inside macrophages. Cell Motil. Cytoskel. 34, 230-245 (1996).
42. Grande-Garcia, A. et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 177, 683-694 (2007).
43. Etienne-Manneville, S. Actin and microtubules in cell motility: Which one is in control? Traffic 5, 470-477 (2004).
44. Moissoglu, K., Slepchenko, B. M., Meller, N., Horwitz, A. F. & Schwartz, M. A. In vivo dynamics of Rac-membrane interactions. Mol. Biol. Cell 17, 2770-2779 (2006).
45. Santy, L. C., Ravichandran, K. S. & Casanova, J. E. The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation tothe downstream activation of Racl. Curr Biol. 15, 1749-1754 (2005).
46. Cotton, M. et al. Endogenous ARF6 interacts with Rac1 upon angiotensin II stimulation to regulate membrane ruffling and cell migration. Mol. Biol. Cell 18, 501-511 (2007).
47. Prag, S. et al. Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42. Mol. Biol. Cell 18, 2935-2948 (2007).
48. Ren, M. et al. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl Acad. Sci. USA 95, 6187-6192 (1998).
49. Choi, S. et al. ARF6 and EFA6A regulate the development and maintenance of dendritic spines. J. Neurosci. 26, 4811-4819 (2006).