ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA

Molecular and Cellular Biology

Volumn 20, Issue 10, 2000, Pages 3685-3694

  Boshans, Rita L ^a   Szanto, Stacey ^a   Van Aelst, Linda ^b   D'Souza Schorey, Crislyn ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR;

ACTIN FILAMENT; ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; FLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ACTINS; ADP-RIBOSYLATION FACTORS; ANIMALS; BIOLOGICAL TRANSPORT; BOMBESIN; CELL MEMBRANE; CHO CELLS; CRICETINAE; CYTOSKELETON; ENDOSOMES; EPIDERMAL GROWTH FACTOR; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN;

EID: 0034095215     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.10.3685-3694.2000     Document Type: Article

References (57)

1. Aprikian, A. G., L. Tremblay, K. Han, and S. Chevalier. 1997. Bombesin stimulates the motility of human prostate-carcinoma cells through tyrosine phosphorylation of focal adhesion kinase and of integrin-associated proteins. Int. J. Cancer 72:498-504.
2. Bretscher, M. S. 1996. Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 87:601-606.
3. Bretscher, M. S., and C. Aguado-Velasco. 1998. EGF induces recycling membrane to form ruffles. Curr. Biol. 8:721-724.
4. Brown, H. A., S. Gutowski, C. R. Moomaw, C. Slaughter, and P. C. Sternweiss. 1993. ADP-ribosylation factor, a small GTP-dependent regulatory protein stimulates phospholipase D activity. Cell 75:1137-1144.
5. Charlesworth, A., and E. Rozengurt. 1997. Bombesin and neuromedin B stimulate the activation of p42(mapk) and p74(raf-1) via a protein kinase C-independent pathway in Rat-1 cells. Oncogene 14:2323-2329.
6. Cockroft, S., G. M. H. Thomas, A. Fensome, B. Geny, E. Cunningham, L. Gout, I. Hiles, N. F. Totty, O. Truong, and J. J. Hsuan. 1994. Phospholipase D: a downstream effector of ARF in granulocytes. Science 263:523-526.
7. De Vries, L., and M. Farquhar Gist. 1999. RGS proteins: more than just GAPs for heterotrimeric G proteins. Trends Cell Biol. 9:138-144.
8. D'Souza-Schorey, C., C. Li, M. I. Colombo, and P. D. Stahl. 1995. A regulatory role for ARF6 in receptor-mediated endocytosis. Science 267:1175-1178.
9. D'Souza-Schorey, C., R. L. Boshans, M. McDonough, P. D. Stahl, and L. van Aelst. 1997. A role for POR 1, a Rac 1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. EMBO J. 16:5445-5454.
10. D'Souza-Schorey, C., E. van Donselaar, V. Hsu, C. Yang, P. D. Stahl, and P. J. Peters. 1998. ARF6 targets recycling endosomal vesicles to the plasma membrane: insights from an ultrastructural investigation. J. Cell Biol. 140: 603-616.
11. D'Souza-Schorey, C., B. Boettner, and L. van Aelst. 1998. Rac regulates integrin-mediated cytoskeletal spreading and increased adhesion of T lymphocytes. Mol. Cell. Biol. 18:3936-3946.
12. Franco, M., P. J. Peters, J. Boretto, E. van Donselaar, A. Neri, C. D'Souza-Schorey, and P. Chavrier. 1999. EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. EMBO J. 18:1480-1491.
13. Galas, M.-C., J. B. Helms, N. Vitale, D. Thierese, D. Aunis, and M.-F. Bader. 1997. Regulated exocytois in Chromaffin cells. A potential role for a secretory granule associated ARF6 protein. J. Biol. Chem. 272:2788-2798.
14. Guan, K. L., and M. Han. 1999. A G-protein signaling network mediated by an RGS protein. Genes Dev. 13:1763-1767.
15. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
16. Hammond, S. M., Y. M. Altschuller, T. Sung, S. A. Rudge, K. Rose, J. Engebrecht, A. J. Morrise, and M. A. Frohman. 1995. Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270:29640-29643.
17. Hart, M. J., X. Jiang, T. Kozasa, W. Roscoe, W. D. Singer, A. G. Gilman, P. C. Sternweis, and G. Bollag. 1998. Direct stimulation of guanine nucleotide exchange activity of p115 RhoGEF by Gα13. Science 280:2112-2114.
18. Hawkins, P. T., A. Eguinoa, R.-G. Qiu, D. Stokoe, F. T. Cooke, R. Walters, S. Wennstrom, L. Claessen-Welsh, T. Evans, M. Symons, and L. Stephens. 1995. PDGF stimulates an increase in GTP-Rac via activation of phospho-inositide 3-kinase. Curr. Biol. 5:393-403.
19. Heximer, S. P., N. Watson, M. E. Linder, K. J. Blumer, and J. R. Helper. 1997. RGS2/G0S8 is a selective inhibitor of Gqalpha function Proc. Natl. Acad. Sci. USA 94:14389-14393.
20. Hopkins, C. R., A. Gibson, M. Shipman, D. K. Strickland, and I. S. Trowbridge. 1994. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125:1265-1274.
21. Kahn, R. A., and A. G. Gilman. 1986. The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP-binding protein. J. Biol. Chem. 261:7906-7911.
22. Kozasa, T., X. Jiang, M. J. Hart, P. M. Sternweis, W. D. Singer, A. G. Gilman, G. Bollag, and P. C. Sternweis. 1998. p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science 280:2109-2111.
23. Kozma, R., S. Ahmed, A. Best, and L. Lim. 1995. The Ras-related protein Cdc42 Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 Fibroblasts. Mol. Cell. Biol. 15:1942-1952.
24. Kranenburg, O., M. Poland, F. P. van Horck, D. Drechsel, A. Hall, and W. H. Moolenaar. 1999. Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 10:1851-1857.
25. Ktistakis, N., H. A. Brown, M. G. Waters, P. C. Sternweiss, and M. G. Roth. 1996. Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles. J. Cell Biol. 108:2169-2181.
26. Lamaze, C., T. H. Chuang, L. J. Trelecky, G. M. Bockoch, and S. L. Schmid. 1996. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 382:177-179.
27. Langille, S. E., V. Patki, J. K. Klarlund, J. M. Buxton, J. J. Holik, A. Chawla, S. Corvera, and M. P. Czech. 1999. ADP-ribosylation factor 6 as a target of guanine nucleotide exchange factor GRP1. J. Biol. Chem. 274:27099-27104.
28. 2+- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377: 75-79.
29. Lenhard, J. M., M. I. Colombo, and P. D. Stahl. 1994. Heterotrimeric GTP-binding proteins and ADP-ribosylation factor regulate priming of endosomal membranes for fusion. Arch. Biochem. Biophys. 312:474-479.
30. Liang, J. O., and S. Kornfeld. 1997. Comparative activity of ADP-ribosylation factor family members in the early steps of coated vesicle formation on rat liver Golgi membranes. J. Biol. Chem. 272:414-418.
31. Massenburg, D., J.-S. Han, M. Liyanage, W. A. Patton, S. G. Rhee, J. Moss, and M. Vaughan. 1994. Activation of rat brain phospholipase D by ADP-ribosylation factors 1, 5, and 6: separation of ADP ribosylation factor dependent and oleate dependent enzymes. Proc. Natl. Acad. Sci. USA 91: 11718-11722.
32. McGraw, T. E., L. Greenefield, and F. R. Maxfield. 1987. Functional expression of human transferrin receptor cDNA in chinese hamster ovary cells deficient in endogenous transferrin receptor. J. Cell Biol. 105:207-214.
33. Milusheva, E. A., N. I. Kortezova, Z. N. Mizhorkova, M. Papasova, D. H. Coy, A. Balint, E. S. Vizi, and G. Varga. 1998. Role of different bombesin receptor subtypes mediating contractile activity in cat upper gastrointestinal tract. Peptides 19:549-556.
34. Minden, A., A. Lin, F. X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
35. Moolenaar, W. H., O. Kranenburg, F. F. Postma, and C. C. M. Zondag. 1997. Lysophosphatidic acid: G-protein signalling and cellular responses. Curr. Opin. Cell Biol. 9:168-173.
36. Moss, J., and M. Vaughan. 1995. Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J. Biol. Chem. 246:2606-2614.
37. Moss, J., and M. Vaughan. 1998. Molecules in the ARF orbit. J. Biol. Chem. 273:21431-21434.
38. Nobes, C. D., and A. Hall. 1995. Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamelipodia, and filopodia. Cell 81:53-62.
39. Nobes, C. D., P. Hawkins, L. Stephens, and A. Hall. 1995. Activation of GTP-binding proteins Rho and Rac by growth factor receptors. J. Cell Sci. 108:226-233.
40. Nobes, C. D., and A. Hall. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1235-1244.
41. Norman, J. C., L. S. Price, A. J. Ridley, and A. Koffer. 1996. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell 7:1426-1442.
42. Peters, P. J., V. W. Hsu, C. E. Ooi, D. Finazzi, S. B. Teal, V. Oorschot, J. G. Donaldson, and R. D. Klausner. 1995. Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol. 128:1003-1017.
43. Pigeon, C., M. Le Romancer, C. Linard, M. J. Lewin, and F. Reyl-Desmars. 1996. Bombesin activation of phospholipase C beta 1 in rat acinar pancreatic cells involves the pertussis toxin-sensitive G alpha 13 protein. Regul. Pept. 62:153-159.
44. Radhakrishna, H., R. D. Klausner, and J. G. Donaldson. 1996. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol. 134:935-946.
45. Radhakrishna, H., and J. G. Donaldson. 1997. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139:49-61.
46. Radhakrishna, H., O. Al-awar, Z. Khachikian, and J. G. Donaldson. 1999. ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J. Cell Sci. 112:855-866.
47. Ren, X. D., W. B. Kiosses, and M. A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578-585.
48. Ridley, A. J., and A. Hall. 1992. The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389-399.
49. Ridley, A. J., H. F. Paterson, C. L. Johnston, D. Diekman, and A. Hall. 1992. The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
50. Sanders, L. C., F. Matsumara, G. M. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21 activated kinase. Science 283:2083-2085.
51. 2+ but not by protein kinase C, and is enhanced by disruption of rho/ cytoskeletal pathways. J. Clin. Investig. 100:1037-1046.
52. Uehata, M., T. Ishizaki, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1997. Calcium sensitization of smooth muscle mediated by a Rho associated protein kinase in hypertension. Nature 389:990-994.
53. van Aelst, L., T. Joneson, and D. Bar-Sagi. 1996. Identification of a novel Rac1 interacting protein involved in membrane ruffling. EMBO J. 15:3778-3786.
54. van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
55. van Leeuwen, F., H. E. Kain, R. A. Kammen, F. Michiels, O. W. Kranenburg, and J. G. Collard. 1997. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J. Cell Biol. 139:797-807.
56. van Leeuwen, F., S. van Delft, H. E. Kain, R. A. van der Kammen, and J. G. Collard. 1999. Rac regulates the phosphorylation of myosin II heavy chain, actinomyosin disassembly and cell spreading. Nat. Cell Biol. 1:242-248.
57. Wang, J. L., S. Kalyanaraman, M. D. Vivo, and N. Gautam. 1996. Bombesin and thrombin affect discrete pools of intracellular calcium through different G-proteins. Biochem. J. 320:87-91.