EGF- and NGF-stimulated translocation of cytohesin-1 to the plasma membrane of PC12 cells requires PI 3-kinase activation and a functional cytohesin-1 PH domain

Journal of Cell Science

Volumn 112, Issue 12, 1999, Pages 1957-1965

  Venkateswarlu, Kanamarlapudi ^a   Gunn Moore, Frank ^a   Tavaré, Jeremy M ^a   Cullen, Peter J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

ARF; Cytohesin 1; Neurite outgrowth; PC12 cell; PI 3 kinase

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHIMERIC PROTEIN; CYTOHESIN 1; EPIDERMAL GROWTH FACTOR; GLYCEROL; GLYCEROL DERIVATIVE; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; INOSITOL 1,3,4,5 TETRAKISPHOSPHATE; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PLECKSTRIN; TRIPHOSPHOINOSITIDE; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CELL STRAIN; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME ACTIVATION; LASER MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; RAT; STRUCTURE ACTIVITY RELATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BIOLOGICAL TRANSPORT; CELL ADHESION MOLECULES; CELL MEMBRANE; EPIDERMAL GROWTH FACTOR; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INDICATORS AND REAGENTS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; NERVE GROWTH FACTORS; PC12 CELLS; PHOSPHORUS RADIOISOTOPES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS;

ANIMALIA; EUKARYOTA;

EID: 0032805160     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R. J., Reese, C. B. and Cohen, P. (1997). Characterisation of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7, 261-269.
2. Alessi, D. R., and Cohen, P. (1998). Mechanism of activation and function of protein kinase B. Curr. Biol. 8, 55-62.
3. Anderson, K. E., Coadwell, J., Stephens, L. R. and Hawkins, P. T. (1998). Translocation of PDK-1 to the plasma membrane is important in allowing PDK-1 to activate protein kinase B. Curr. Biol. 8, 684-691.
4. 2+ and the β-phosphate to destabilise GDP on ARF1. EMBO J. 17, 3651-3659.
5. Betz, S. F., Schnuchel, A., Wang, H., Olejniczak, E. T., Meadows, R. P., Lipsky, B. P., Harris, E. A. S., Stauntin, D. E. and Fesik, S. W. (1998). Solution structure of the cytohesin-1 (B2-1). Sec7 domain and its interaction with the GTPase ARF1. Proc. Natl. Acad. Sci. USA 95, 7909-7914.
6. Brown, F. D., Thompson, N., Saqib, K. M., Clark, J. M., Powner, D., Thompson, N. T., Solari, R. and Wakelam, M. J. O. (1998). Phospholipase D1 localises to secretory granules and lysosomes and is plasma-membrane translocated on cellular stimulation. Curr. Biol. 8, 835-838.
7. Carter, A. N. and Downes, C. P. (1992). PI 3-kinase is activated by NGF and EGF in PC12 cells. J. Biol. Chem. 267, 14563-14567.
8. Cavenagh, M. M., Whitney, J. A., Carroll, K., Zhang, C-J., Boman, A. L., Rosenwald, A. G., Mellman, I. And Kahn, R. A. (1996). Intracellular distribution of ARF proteins in mammalian cells. ARF6 is uniquely localised to the plasma membrane. J. Biol. Chem. 271, 21767-21774.
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-homology and PH domains. Nature 384, 481-484.
10. Cherfils, J., Menetrey, J., Mathieu, M., Le Bras, G., Robineau, S., Béraud-Dufour, S., Antonny, B. and Chardin, P. (1998). Structure of the Sec7 domain of the ARF exchange factor ARNO. Nature 392, 101-105.
11. Clapham, D. E. (1995). Calcium Signalling. Cell 80, 259-268.
12. Cockcroft, S., Thomas, G. M. H., Fensome, A., Geny, B., Cunningham, E., Gout, I., Hiles, I., Totty, N. F., Truong, O. and Hsuan, J. J. (1994). Phospholipase D - a downstream effector of ARF in granuloyctes. Science 263, 523-526.
13. 4 are located predominantly in the plasma membrane of human platelets. Biochem. J. 298, 739-742.
14. 4 receptor. Biochem. J. 305, 139-143.
15. 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.
16. Divecha, N. and Irvine, R. F. (1995). Phospholipid signalling. Cell 80, 269-278.
17. 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.
18. Fantl, W. J., Escobedo, J. A., Martin, G. A., Turck, C. W., del Rosario, M., McCormack, F. and Williams, L. T. (1992). Distinct phosphotyrosines on a growth-factor receptor bind to specific molecules that mediate different signalling pathways. Cell 69, 413-423.
19. Frank, S., Upender, S., Hansen, S. H. and Casanova, J. E. (1998). ARNO is a guanine nucleotide exchange factor for ARF6. J. Biol. Chem. 273, 23-27.
20. Hammond, S. M., Altshuller, Y. M., Sung, T. C., Rudge, S. A., Rose, K., Engebrecht, J., Morris, A. J. and Frohman, M. A. (1995). Human ARF-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270, 29640-29643.
21. 3-binding protein from rat brain. J. Biol. Chem. 271, 18859-18868.
22. Hawkins, P. T., Welch, H., McGregor, A., Eguinoa, A., Gobert, S., Krugmann, S., Anderson, K., Stokoe, D. and Stephens, L. R. (1997). Signalling via PI 3-kinase. Biochem. Soc. Trans. 25, 1147-1151.
23. Hyvonen, M. and Saraste, M. (1997). Structure of the PH domain and Btk motif from Bruton's tyrosine kinase: Molecular explanations for X-linked agammaglobulinaemia. EMBO J. 16, 3396-3404.
24. Jackson, T. R., Blader, I. J., Hammonds-Odie, L. P., Burga, C. R., Cooke, F., Hawkins, P. T., Wolf, A. G., Heldman, K. A. and Theibert, A. B. (1996). Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a PI 3-kinase. J. Cell Sci. 109, 289-300.
25. 3 without subsequent activation. Biochem. J. 315, 709-713.
26. Joly, M., Kazlauskas, A. and Corvera, S. (1995). PI 3-kinase activity is required at a postendocytic step in PDGF receptor trafficking. J. Biol. Chem. 270, 13225-13230.
27. Katayama, K., Kodaki, T., Nagamachi, Y. and Yamashita, S. (1998). Cloning, differential regulation and tissue distribution of alternatively spliced isoforms of ARF-dependent phospholipase D from rat liver. Biochem. J. 329, 647-652.
28. Kavran, J. M., Klein, D. E., Lee, A., Falasca, M., Isakoff, S. J., Skolnik, E. Y. and Lemmon, M. A. (1998). Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508.
29. Kimura, K. D., Hattori, S., Kabuyama, Y., Shizawa, Y., Takayanagi, J., Nakamura, S., Toki, S., Matsuda, Y., Onodera, K. and Fukui, Y. (1994). Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of PI 3-kinase. J. Biol. Chem. 269, 18961-18967.
30. Kita, Y, Kimura, K. D., Kobayashi, M., Ihara, S., Kaibuchi, K., Kuroda, S., Ui, M., Iba, H., Konishi, H., Kikkawa, U., Nagata, S. and Fukui, Y. (1998). Microinjection of activated PI 3-kinase induces process outgrowth in rat PC12 cells through the Rac-JNK signal transduction pathway. J. Cell Sci. 111, 907-915.
31. 3 through proteins containing pleckstrin and Sec7 homology domains. Science 275, 1927-1930.
32. 3. J. Biol. Chem. 273, 1859-1862.
33. Kobayashi, M., Nagata, S., Kita, Y., Nakatsu, N., Ihara, S., Kaibuchi, K., Kuroda, S., Ui, M., Iba, H., Konish, H., Kikkawa, U., Saitoh, I. and Fukui, Y. (1997). Expression of a constitutively active PI 3-kinase induces process formation in rat PC12 cells. J. Biol. Chem. 272, 16089-16092.
34. 2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86, 233-242.
35. Lemmon, M. A., Fergusson, K. M. and Schlessinger, J. (1996). PH domains: Diverse sequences with a common fold recruit signalling molecules to the cell surface. Cell 85, 621-624.
36. Liu, L. and Pohajdak, B. (1992). Cloning and sequencing of a human cDNA from cytolytic NK/T cells with homology to yeast SEC7. Biochim. Biophys. Acta 1132, 75-78.
37. IP4BP PH domain directing plasma membrane targeting. Curr. Biol. 7, 1007-1010.
38. Meacci, E., Tsai, S.-C., Adamik, R., Moss, J. and Vaughan, M. (1997). Cytohesin-1, a cytosolic guanine nucleotide-exchange protein for ARF. Proc. Natl. Acad. Sci. USA 94, 1745-1748.
39. Meers, P., Mealy, T. and Tauber, A. I. (1993). Annexin-1 interactions with human neutrophil specific granules - fusogenicity and coaggregation with plasma membrane vesicles. Biochim. Biophys. Acta 1147, 177-184.
40. Mellor, H. and Parker, P. J. (1998). The extended protein kinase C superfamily. Biochem. J. 332, 281-292.
41. Morgan, C. P., Sengelov, H., Whatmore, J., Borregaard, N. and Cockcroft, S. (1997). ARF-regulated phospholipase D activity localises to secretory vesicles and mobilises to the plasma membrane following N-methionyl-formyl-leucyl-phenylalanine stimulation of human neutrophils. Biochem. J. 325, 581-585.
42. Moss, J. and Vaughan, M. (1995). Structure and function of ARF proteins -activators of cholera-toxin and critical components of intracellular vesicular transport processes. J. Biol. Chem. 270, 12327-12330.
43. Nagel, W., Zeitlmann, L., Schilcher, P., Geiger, C., Kolanus, J. and Kolanus, W. (1998). PI 3-kinase activates the β2 integrin adhesion pathway and induces membrane recruitment of cytohesin-1. J. Biol. Chem. 278, 14853-14861.
44. Oatey, P. B., Weering, D., Dobson, S., Gould, G. and Tavaré, J. M. (1997). GLUT4 vesicle dynamics in living 3T3 L1 adipocytes visualised with GFP. Biochem. J. 327, 637-642.
45. Okada, T., Kawano, Y., Sakakibara, T., Hazeki, O. and Ui, M. (1994). Essential role of PI 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes: studies with a selective inhibitor wortmannin. J. Biol. Chem. 269, 3568-3573.
46. Paris, S., Béraud-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 nucleotides exchange factor ARNO. J. Biol. Chem. 272, 22221-22226.
47. 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.
48. Peyroche, A., Paris, S. and Jackson, C. L. (1996). Nucleotide exchange on ARF mediated by yeast Gea1 protein. Nature 384, 479-481.
49. Radhakrishna, H. and Donaldson, J. G. (1997). ARF6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
50. Raffioni, S. and Bradshaw, R. A. (1992). Activation of PI 3-kinase by EGF, bFGF and NGF in PC12 pheochromocytoma cells. Proc. Natl. Acad. Sci. USA 89, 9121-9125.
51. Salim, K., Bottomley, M. J., Querfurth, E., Zvelebil, M., Gout, I., Scaife, R., Margolis, R. L., Gigg, R., Edvard-Smith, C. I., Driscoll, P. C., Waterfield, M. D. and Panayotou, G. (1996). Distinct specificity in the recognition of phosphoinositides by the PH domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15, 6241-6250.
52. Schiavo, G., Gu, Q.-M., Prestwich, G. D., Sollner, T. H. and Rothman, J. E. (1996). Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. USA 93, 13327-13332.
53. Song, J., Khachikian, Z., Radhakrishna, H. and Donaldson, J. G. (1998). Localisation of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J. Cell Sci. 111, 2257-2267.
54. Spiegel, S., Foster, D. and Kolesnick, R. (1996). Signal transduction through lipid second messengers. Curr. Opin. Cell Biol. 8, 159-167.
55. 3: a new intracellular signalling system? Biochim. Biophys. Acta 1179, 27-75.
56. 3-dependent activation of protein kinase B. Science 279, 710-714.
57. Thomas, A. P., Bird, G. St. J., Hajnoczky, G., Robb-Gaspers, L. D. and Putney, J. W. Jr. (1996). Spatial and temporal aspects of cellular calcium signalling. FASEB J. 10, 1505-1517.
58. Toker, A. and Cantley, L. C. (1997). Signalling through the lipid products of PI 3-kinase. Nature 387, 673-767.
59. Vanhaesebroek, B., Leevers, S. J., Panayotou, G. and Waterfield, M. D. (1997). PI 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci. 22, 267-272.
60. Vasudevan, C., Han, W., Tan, Y., Nie, Y., Li, D., Shome, K., Watkins, S. C., Levitan, E. S. and Romero, G. (1998). The distribution and translocation of the G protein ARF1 in live cells is determined by its GTPase activity. J. Cell Sci. 111, 1277-1285.
61. Venkateswarlu, K., Oatey, P. B., Tavaré, J. M. and Cullen, P. J. (1998). Insulin-dependent translocation of ARNO to the plasma membrane of 3T3 L1 adipocytes requires PI 3-kinase. Curr. Biol. 8, 463-466.
62. Wennström, S., Hawkins, P. T., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T. R., Claesson-Welsh, L. and Stephens, L. R. (1994). Activation of PI 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
63. Wymann, M. and Acaro, A. (1994). PDGF-induced PI 3-kinase activation mediates actin rearrangements in fibroblasts. Biochem. J. 298, 517-520.
64. 6 in mammalian cells. J. Biol. Chem. 273, 4006-4011.