EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization

EMBO Journal

Volumn 18, Issue 6, 1999, Pages 1480-1491

  Franco, Michel ^d   Peters, Peter J ^b   Boretto, Joëlle ^a   Van Donselaar, Elly ^b   Neri, Antonino ^c   D'Souza Schorey, Crislyn ^e   Chavrier, Philippe ^a  

^a INSERM   (France)

^b UTRECHT UNIVERSITY   (Netherlands)

^c FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^d INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e NONE

Author keywords

Actin; ARF6; Endocytosis; Guanine nucleotide exchange factor; Rac1

Indexed keywords

ACTIN; CELL MEMBRANE PROTEIN; CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PLECKSTRIN; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY;

ANIMALIA;

EID: 0033560032     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.6.1480     Document Type: Article

References (61)

1. Achstetter, T., Franzusoff, A., Field, C. and Schekman, R. (1988) SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus. J. Biol. Chem., 263, 11711-11717.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
3. Bednarek, S.Y., Orci, L. and Schekman, R. (1996) Traffic COPs and the formation of vesicle coats. Trends Cell Biol., 6, 468-473.
4. 2+ and the β-phosphate to destabilize GDP on ARF1. EMBO J., 17, 3651-3659.
5. Bretscher, M.S. and Aguado-Velasco, C. (1998a) Membrane traffic during cell locomotion. Curr. Opin. Cell Biol., 10, 537-541.
6. Bretscher, M.S. and Aguado-Velasco, C. (1998b) EGF induces recycling membrane to form ruffles. Curr. Biol., 8, 721-724.
7. Brown, H.A., Gutowski, S., Moomaw, C.R., Slaughter, C. and Sternweis, P.C. (1993) ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell, 75, 1137-1144.
8. Caumont, A.S., Galas, M.C., Vitale, N., Aunis, D. and Bader, M.F. (1998) Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J. Biol. Chem., 273, 1373-1379.
9. Chardin, P., Paris, S., Antonny, B., Robineau, S., Béraud-Dufour, S., Jackson, C.L. and Chabre, M. (1996) A human exchange factor for ARF contains Sec7-and pleckstrin-homology domains. Nature, 384, 481-484.
10. Cherfils, J., Menetrey, J., Mathieu, M., Le Bras, G., Robineau, S., Beraud-Dufour. S., Antonny, B. and Chardin, P. (1998) Structure of the Sec7 domain of the Arf exchange factor ARNO. Nature, 392, 101-105.
11. Cockcroft, S. et al. (1994) Phospholipase D: a downstream effector of ARF in granulocytes. Science, 263, 523-526.
12. Daro, E., Van der Sluijs, P., Galli, J. and Mellman, I. (1996) Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc. Natl Acad. Sci. USA, 93, 9559-9564.
13. Donaldson, J.G. and Klausner, R.D. (1994) ARF: a key regulatory switch in membrane traffic and organelle structure. Curr. Opin. Cell Biol., 6, 527-532.
14. D'Souza-Schorey, C., Li, G., Colombo, M.I. and Stahl, P.D. (1995) A regulatory role for ARF6 in receptor-mediated endocytosis. Science. 267, 1175-1178.
15. D'Souza-Schorey, C., Boshans, R.L., McDonough, M., Stahl, P.D. and Van Aelst, L. (1997) A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. EMBO J., 16, 5445-5454.
16. D'Souza-Schorey, C., van Donselaar, E., Hsu, V.W., Yang, C., Stahl, P.D. and Peters. P.J. (1998) ARF6 targets recycling vesicles to the plasma membrane: insights from an ultrastructural investigation. J. Cell Biol., 140, 603-616.
17. Dutartre, H., Davoust, J., Gorvel, J.P. and Chavrier, P. (1996) Cytokinesis arrest and redistribution of actin-cytoskeleton regulatory components in cells expressing the rho GTPase CDC42Hs. J. Cell Sci., 109, 367-377.
18. Evan, G.I., Lewis, G.K., Ramsay, G. and Bishop, J.M. (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell Biol., 5, 3610-3616.
19. 2+ levels. J. Biol. Chem., 270, 1337-1341.
20. Franco, M., Boretto, J., Robineau, S., Monier, S., Goud, B., Chardin, P. and Chavrier.P. (1998) ARNO3, a Sec7-domain guanine nucleolide exchange factor for ADP ribosylation factor 1, is involved in the control of golgi structure and function. Proc. Natl Acad. Sci. USA, 95, 9926-9931.
21. Frank, S., Upender, S., Hansen, S.H. and Casanova, J.E. (1998) ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6. J. Biol. Chem., 273, 23-27.
22. Franzusoff, A. and Schekman, R. (1989) Functional compartments of the yeast Golgi apparatus are defined by the sec7 mutation. EMBO J., 8, 2695-2702.
23. Fuerst, T.R., Niles, E.G., Studier, E.G. and Moss, B. (1986) Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophages T7 RNA polymerase. Proc. Natl Acad. Sci. USA, 83, 8122-8126.
24. Galas, M.C., Helms, J.B., Vitale, N., Thierse, D., Aunis, D. and Bader, M.F. (1997) Regulated exocytosis in chromaffin cells. A potential role for a secretory granule-associated ARF6 protein. J. Biol. Chem., 272, 2788-2793.
25. Ghosh, R., Gelman, D. and Maxfield, F. (1994) Quantitication of low density lipoprotein and transferrin endocytic sorting in HEp2 cells using confocal microscopy. J. Cell Sci., 107, 2177-2189.
26. Gruenberg, J. and Maxfield, F.R. (1995) Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol., 7, 552-563.
27. Guillemot, J.C., Montcourrier, P., Vivier, E., Davoust, J. and Chavrier, P. (1997) Selective control of membrane ruffling and actin plaque assembly by the Rho GTPases Rac1 and CDC42 in Fc εRI-activated rat basophilic leukemia (RBL-2H3) cells. J. Cell Sci., 110, 2215-2225.
28. Hopkins, C.R., Gibson, A., Shipman, M., Strickland, D.K. and Trowbridge, I.S. (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.
29. Klarlund, J.K., Guilherme, A., Holik, J.J., Virbasius, J.V., Chawla, A. and Czech, M.P. (1997) Signaling by phosphoinositide-3,4,5-trisphosphate through proteins containing pleckstrin and Sec7 humology domains. Science, 275, 1927-1930.
30. Klarlund, J.K., Rameh, L.E., Cantley, L.C., Buxton, J.M., Holik, J.J., Sakelis, C., Patki, V., Corvera, S. and Czech, M.P. (1998) Regulation of GRP1-catalyzed ADP ribosylation factor guanine nucleotide exchange by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem., 273, 1859-1862.
31. Kozma, R., Sarner, S., Ahmed, S. and Lim, L. (1997) Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1 and acetylcholine and collapse induced hy RhoA and lysophosphatidic acid. Mol. Cell. Biol., 17, 1201-1211.
32. Lamaze, C., Chuang, T.H., Terlecky, L.J., Bokoch, G.M. and Schmid, S.L. (1996) Regulation of receptor-mediated endocytosis by Rho and Rac. Nature, 382, 177-179.
33. Leeuwen, F.N., Kain, H.E., Kammen, R.A., Michiels, F., Kranenburg, O.W. and Collard, J.G. (1997) The guanine nucleotide exchange factor Tiaml affects neuronal morphology: opposing roles for the small GTPases Rac and Rho. J. Cell Biol., 139, 797-807.
34. Lemmon, M.A., Falasca, M., Ferguson, K.M. and Schlessinger, J. (1997) Regulatory recruitment of signalling molecules to the cell membrane by pleckstrin-homology domains. Trends Cell Biol., 7, 237-242.
35. Liu, L. and Pohajdak, B. (1992) Cloning and sequencing of a human cDNA from cytolytic NK/T cells with homology to yeast SEC7. Biochim. Bioplns. Acta, 1132, 75-78.
36. Luo, L., Hensch, T.K., Ackerman, L., Barbel, S., Jan, L.Y. and Jan, Y.N. (1996) Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature, 379, 837-840.
37. Massenburg, D., Han, J.S., Liyanage, M., Patton, W.A., Rhee, S.G., Moss, J. and Vaughan, M. (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.
38. McGraw, T.E., Greenfield, L. and Maxfield, F.R. (1987) Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J. Cell Biol., 105, 207-214.
39. Meacci, E., Tsai, S.C., Adamik, R., Moss, J. and Vaughan, M. (1997) Cytohesin-1, a cytosolic guanine nucleotide-exchange protein for ADP-ribosylation factor. Proc. Natl Acad. Sci. USA, 94, 1745-1748.
40. Monier, S., Chardin, P., Robineau, S. and Goud, B. (1998) Overexpression of the ARF1 exchange factor ARNO inhibits the early secretory pathway and causes the disassembly of the Golgi complex. J. Cell Sci., 111, 3427-3436.
41. Morinaga, N., Moss, J. and Vaughan, M. (1997) Cloning and expression of a cDNA encoding a bovine brain brefeldin A-sensitive guanine nucleotide-exchange protein for ADP-ribosylation factor. Proc. Natl Acad. Sci. USA, 94, 12926-12931.
42. Mossessova, E., Gulbis, J.M. and Goldberg, J. (1998) Structure of the guanine nucleotide exchange factor Sec7 domain of human arno and analysis of the interaction with ARF GTPase. Cell. 92, 415-423.
43. Murphy, C. et al. (1996) Endosome dynamics regulated by a Rho protein. Nature, 384, 427-432.
44. Norman, J.C., Price, L.S., Ridley, A.J. and Koffer, A. (1996) The small GTP-binding proteins. Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell, 7, 1429-1442.
45. Novick, P. and Zerial, M. (1997) The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol., 9, 496-504.
46. Ooi, C.E., Dell'Angelica, E.C. and Bonifacino, J.S. (1998) ADP-Ribosylation factor 1 (ARFI) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol., 142, 391-402.
47. Orci, L., Palmer, D.J., Amherdt, M. and Rothman, J.E. (1993) Coated vesicle assembly in the Golgi requires only coatomer and ARF proteins from the cytosol. Nature, 364, 732-734.
48. Perletti, L., Talarico, D., Trecca, D., Ronchetti, D., Fracchiolla, N.S., Maiolo, A.T. and Neri, A. (1997) Identification of a novel gene, PSD, adjacent to NFKB2/lyt-10, which contains Sec7 and pleckstrin-homology domains. Genomics, 46, 251-259.
49. Peters, P.J., Hsu, V.W., Ooi, C.E., Finazzi, D., Teal, S.B., Oorschot, V., Donaldson, J.G. and Klausner, R.D. (1995) Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol., 128, 1003-1017.
50. Peyroche, A., Paris, S. and Jackson, C.L. (1996) Nucleotide exchange on ARF mediated by yeast Geal protein. Nature, 384, 479-481.
51. Radhakrishna, H. and Donaldson, J.G. (1997) ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol., 139, 49-61.
52. Radhakrishna, H., Klausner, R.D. and Donaldson, J.G. (1996) Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol., 134, 935-947.
53. Rojo, M., Pepperkok, R., Emery, G., Kellner, R., Stang, E., Parton, R.G. and Gruenberg, J. (1997) Involvement of the transmembrane protein p23 in biosynthetic transport. J. Cell Biol., 139, 1119-1135.
54. Serafini, T., Orci, L., Amherdt, M., Brunner, M., Kahn, R.A. and Rothman, J.E. (1991) ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell, 67, 239-253.
55. Shevell, D.E., Leu, W.M., Gillmor, C.S., Xia, G., Feldmann, K.A. and Chua, N.H. (1994) EMB30 is essential for normal cell division, cell expansion and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell. 77, 1051-1062.
56. Stamnes, M.A. and Rothman, J.E. (1993) The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-Ribosylation Factor, a small GTP-binding protein. Cell, 73, 999-1005.
57. Tanigawa, G., Orci, L., Amherdt, M., Ravazzola, M., Helms, J.B. and Rothman, J.E. (1993) Hydrolysis of bound GTP by ARF protein triggers uncoating of Golgi-derived COP-coated vesicles. J. Cell Biol., 123, 1365-1371.
58. Traub, L.M., Ostrom, J.A. and Kornfeld, S. (1993) Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol. 123, 561-573.
59. Tsuchiya, M., Price, S.R., Tsai, S.C. Moss, J. and Vaughan, M. (1991) Molecular identification of ADP-ribosylation factor mRNAs and their expression in mammalian cells. J. Biol. Chem., 266, 2772-2777.
60. Van Aelst, L., Joneson, T. and Bar-Sagi, D. (1996) Identification of a novel Rac1-interacting protein involved in membrane ruffling. EMBO J., 15, 3778-3786.
61. Yang, C.Z., Heimberg, H., D'Souza-Schorey, C., Mueckler, M.M. and Stahl, P.D. (1998) Subcellular distribution and differential expression of endogenous ADP-ribosylation factor 6 in mammalian cells. J. Biol. Chem., 273, 4006-4011.