Remodeling of the actin cytoskeleton is coordinately regulated by protein kinase C and the ADP-ribosylation factor nucleotide exchange factor ARNO

Molecular Biology of the Cell

Volumn 9, Issue 11, 1998, Pages 3133-3146

  Frank, Scott R ^a,b   Hatfield, Jessica C ^a   Casanova, James E ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN KINASE C;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0031739953     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.11.3133     Document Type: Article

References (71)

1. Achstetter, T., Franzusoff, A., 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. Apgar, J.R. (1995). Activation of protein kinase C in rat basophilic leukemia cells stimulates increased production of phosphatidylinositol 4-phosphate and phophatidylinositol 4,5-bisphosphate: correlation with actin polymerization. Mol. Biol. Cell 6, 97-108.
3. Auger, K.R., Serunian, L.A., Soltoff, S.P., Libby, P., and Cantley, L.C. (1989). PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 57, 167-175.
4. Boman, A.L., and Kahn, R.A. (1995). Arf proteins: the membrane traffic police? Trends Biochem. Sci. 20, 147-150.
5. Brewer, C.B. (1994). Cytomegalovirus plasmid vectors for permanent lines of polarized epithelial cells. In: Protein Expression in Animal Cells, vol. 43, ed. M.G. Roth, San Diego, CA: Academic Press, 379.
6. 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.
7. 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.
8. Cavenaugh, M.M., Whitney, J.A., Carroll, K., Zhang, C.-J., Boman, A., Rosenwald, A.G., Mellman, I., and Kahn, R.A. (1996). Intracellular distribution of ARF proteins in mammalian cells: ARF6 is uniquely localized to the plasma membrane. J. Biol. Chem. 271, 21767-21774.
9. Cerione, R.A., and Zheng, Y. (1996). The Db1 family of oncogenes. Curr. Opin. Cell Biol. 8, 216-222.
10. Chardin, P., Paris, S., Antonny, B., Robineau, S., Beraud-Dufour, S., Jackson, C., and Chabre, M. (1996). A human exchange factor for ARF contains Sec7 and pleckstrin homology domains. Nature 384, 481-484.
11. 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.
12. Colley, W.C., Sung, T.-C., Roll, R., Jenco, J., Hammond, S.M., Altshuller, Y., Bar-Sagi, D., Morris, A.J., and Frohman, M.A. (1997). Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr. Biol. 7, 191-201.
13. Conricode, K.M., Smith, J.L., Burns, D.J., and Exton, J.H. (1994). Phospholipase D activation in fibroblast membranes by the alpha and beta isoforms of protein kinase C. FEBS Lett. 342, 149-153.
14. Cross, M.J., Roberts, S., Ridley, A.J., Hodgkin, M.N., Stewart, A., Claesson-Welsh, L., and Wakelam, M.J.O. (1996). Stimulation of actin stress fibre formation mediated by activation of phospholipase D. Curr. Biol. 6, 588-597.
15. Cukierman, E., Huber, I., Rotman, M., and Cassel, D. (1995). The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science 270, 1999-2002.
16. 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.
17. 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.
18. Doms, R.W., Russ, G., and Yewdell, J.W. (1989). Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J. Cell. Biol. 109, 61-72.
19. Donaldson, J.G., Finazzi, D., and Klausner, R.D. (1992). Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360, 350-352.
20. 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.
21. Downey, G.P., Chan, C.K., Lea, P., Takai, A., and Grinstein, S. (1992). Phorbol ester-induced actin assembly in neutrophils: role of protein kinase C. J. Cell Biol. 116, 695-706.
22. Frank, S., Upender, S., Hansen, S.H., and Casanova, J.E. (1998). ARNO is a guanine nucleotide exchange factor for ADP-ribosylation 6. J. Biol. Chem. 273, 23-27.
23. 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.
24. Ha, K.S., and Exton, J.H. (1993). Activation of actin polymerization by phosphatidic acid derived from phosphatidylcholine in IIC9 fibroblasts. J. Cell. Biol. 123, 1789-1796.
25. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
26. Hartwig, J.H., Kung, S., Kovacsovics, T., Janmey, P.A., Cantley, L.C., Stossel, T.P., and Toker, A. (1996). D3 phosphoinositides and outside-in integrin signaling by glycoprotein IIb-IIIa mediate platelet actin assembly and filopodial extension induced by phorbol 12-myristate 13-acetate. J. Biol. Chem. 271, 32986-32993.
27. Helms, J.B., and Rothman, J.E. (1992). Inhibition by brefeldin A of a Golgi membrane enzyme that catalyzes exchange of guanine nucleotide bound to ARF. Nature 360, 352-354.
28. Houle, M.G., Kahn, R.A., Naccache, P.H., and Bourgoin, S. (1995). ADP-ribosylation factor translocation correlates with potentiation of GTP-γ S-stimulated phospholipase D activity in membrane fractions of HL-60 cells. J. Biol. Chem. 270, 22795-22800.
29. Inglese, J., Koch, W.J., Touhara, K., and Lefkowitz, R.J. (1995). Gβγ interactions with PH domains and Ras-MAPK signaling pathways. Trends Biochem. Sci. 20, 151-156.
30. 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 homology domains. Science 275, 1927-1930.
31. 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.
32. Kolanus, W., Nagel, W., Schiller, B., Zeitlmann, L., Godar, S., Stockinger, H., and Seed, B. (1996). αLβ2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86, 233-242.
33. Kozma, R., Ahmed, S., Best, A., and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15, 1942-1952.
34. Ktistakis, N., Brown, H.A., Waters, M.G., Sternweiss, P.C., and Roth, M.G. (1996). Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles. J. Cell. Biol. 108, 2169-2181.
35. 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.
36. Lippincott-Schwartz, J., Yuan, L.C., Bonifacino, J.S., and Klausner, R.D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
37. Lopez, I., Arnold, R.S., and Lambeth, J.D. (1998). Cloning and initial characterization of a human phospholipase D2 (hPLD2). ADP-ribosylation factor regulates hPLD2. J. Biol. Chem. 273, 12846-12852.
38. Mahadevan, D., et al. (1995). Structural studies on the PH domains of Db1, Sos1, IRS-1, and βARK1 and their differential binding to G βγ subunits. Biochemistry 34, 9111-9117.
39. 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.
40. 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.
41. Michiels, F., Habets, G.G.M., Stam, J.C., van der Kammen, R.A., and Collard, J.G. (1995). A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature 375, 338-340.
42. Mitchell, R., McCulloch, D., Lutz, E., Johnson, M., MacKenzie, C., Fennell, M., Fink, G., Zhou, W., and Sealfon, S.C. (1998). Rhodopsin-family receptors associate with small G proteins to activate phospholipase D. Nature 392, 411-414.
43. 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.
44. 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.
45. Myat, M.M., Anderson, S., Allen, L.A., and Aderem, A. (1997). MARCKS regulates membrane ruffling and cell spreading. Curr. Biol. 7, 611-614.
46. Nagel, W., Zeitlmann, L., Schilcher, P., Geiger, C., Kolanus, J., and Kolanus, W. (1998). Phosphoinositide 3-OH kinase activates the β2 integrin adhesion pathway and induces membrane recruitment of cytohesin-1. J. Biol. Chem. 273, 14853-14861.
47. Nobes, C.D., and Hall, A. (1995a). Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
48. Nobes, C.D., and Hall, A. (1995b). Rho, Rac, and Cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23, 456-459.
49. Paris, S., Beraud-Dufour, S., Robineau, S., Bigay, J., Antonny, B., Chabre, M., and Chardin, P. (1997). Role of protein-phospholipid interactions in the activation of ARF1 by the guanine nucleotide exchange factor ARNO. J. Biol. Chem. 272, 22221-22226.
50. Pearson, R.B., and Kemp, B.E. (1991). Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200, 62-81.
51. 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 wildtype and mutant ARF1 and ARF6: distinct pertubations of nonoverlapping membrane compartments. J. Cell Biol. 128, 1003-1017.
52. Peyroche, A., Paris, S., and Jackson, C.L. (1996). Nucleotide exchange on ARF mediated by yeast Gea1 protein. Nature 384, 479-481.
53. Radhakrishna, H., and Donaldson, J.G. (1997). ARF6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
54. 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.
55. Rameh, L.E., et al. (1997). A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272, 22059-22066.
56. Randazzo, P.A., Yang, Y.C., Rulka, C., and Kahn, R.A. (1993). Activation of ADP-ribosylation factor by Golgi membranes: evidence for a brefeldin A and protease sensitive activating factor on Golgi membranes. J. Biol. Chem. 268, 9555-9563.
57. Ridley, A.J., and Hall, A. (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.
58. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D., and Hall, A. (1992). The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
59. Rumenapp, U., Geiszt, M., Wahn, F., Schmidt, M., and Jakobs, K.H. (1995). Evidence for ADP-ribosylation-factor-mediated activation of phospholipase D by m3 muscarinic acetylcholine receptor. Eur. J. Biochem. 234, 240-244.
60. Sata, M., Donaldson, J.G., Moss, J., and Vaughan, M. (1998). Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors. Proc. Natl. Acad. Sci. USA 95, 4204-4208.
61. Schimmoller, F., Itin, C., and Pfeffer, S. (1997). Vesicle traffic: get your coat! Curr. Biol. 7, 235-237.
62. Seelig, H.P., Schranz, P., Schroter, H., Wiemann, C., Griffiths, G., and Renz, M. (1994). Molecular genetic analyses of a 376-kilodalton Golgi complex membrane protein (giantin) [retracted in Mol Cell Biol 1995 Jan;15(1):591]. Mol. Cell. Biol, 14, 2564-2576.
63. 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.
64. Shome, K., Vasudevan, C., and Romero, G. (1997). ARF proteins mediate insulin-dependent activation of phospholipase D. Curr. Biol. 7, 387-396.
65. Singer, W.D., Brown, H.A., Jiang, X., and Sternweis, P.C. (1996). Regulation of phospholipase D by protein kinase C is synergistic with ADP-ribosylation factor and independent of protein kinase activity. J. Biol. Chem. 271, 4504-4510.
66. 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.
67. Venkateswarlu, K., Oatey, P.B., Tavare, J.M., and Cullen, P.J. (1998). Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8, 463-466.
68. Welsh, C.F., Moss, J., and Vaughan, M. (1994). ADP-ribosylation factors: a family of approximately 20-kDa guanine nucleotide-binding proteins that activate cholera toxin. Mol. Cell. Biochem. 138, 157-166.
69. 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.
70. Zheng, Y., Zangrilli, D., Cerione, R.A., and Eva, A. (1996). The pleckstrin homology domain mediates transformation by oncogenic dbl through specific intracellular targeting. J. Biol. Chem. 271, 19017-19020.
71. Zigmond, S.H. (1996). Signal transduction and actin filament organization. Curr. Opin. Cell Biol. 8, 66-73.