Localization of phospholipase D1 to caveolin-enriched membrane via palmitoylation: Implications for epidermal growth factor signaling

Molecular Biology of the Cell

Volumn 13, Issue 11, 2002, Pages 3976-3988

  Han, Jung Min ^a   Kim, Yong ^a   Lee, Jun Sung ^a   Lee, Chang Sup ^a   Lee, Byoung Dae ^a   Ohba, Motoi ^b   Kuroki, Toshio ^b   Suh, Pann Ghill ^a   Ryu, Sung Ho ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b SHOWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE D1; THREONINE; CAV PROTEIN, RAT; CAVEOLIN; HYBRID PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE D; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C GAMMA;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL STRAIN COS7; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE TRANSFER; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; NONHUMAN; PALMITOYLATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CELL FRACTIONATION; CELL STRAIN COS1; CHEMISTRY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; RAT;

ANIMALS; CAVEOLIN 1; CAVEOLINS; CELL FRACTIONATION; CELL MEMBRANE; COS CELLS; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; PHOSPHOLIPASE D; PHOSPHORYLATION; POINT MUTATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN TRANSPORT; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE;

EID: 0036854304     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-02-0100     Document Type: Article

References (60)

1. Anderson, R.G. (1998). The caveolae membrane system. Annu. Rev. Biochem. 67, 199-225.
2. Brown, F.D., Thompson, N., Saqib, K.M., Clark, J.M., Powner, D., Thompson, N.T., Solari, R., and Wakelam, M.J. (1998). Phospholipase D1 localizes to secretory granules and lysosomes and is plasma-membrane translocated on cellular stimulation. Curr. Biol. 8, 835-838.
3. Camp, L.A., and Hofmann, S.L. (1993). Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-ras. J. Biol. Chem. 268, 22566-22574.
4. Carpenter, G., and Cohen, S. (1990). Epidermal growth factor. J. Biol. Chem. 265, 7709-7712.
5. Carrol, M.P., and May, W.S. (1994). Protein kinase C-mediated serine phosphorylation directly activates Raf-1 in murine hematopoietic cells. J. Biol. Chem. 269, 1249-1256.
6. Cockcroft, S. (1992). G-protein-regulated phospholipases C, D and A2-mediated signaling in neutrophils. Biochim. Biophys. Acta 1113, 135-160.
7. 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.
8. Cook, S.J., and Wakelam, M.J. (1992). Epidermal growth factor increases sn-1,2-diacylglycerol levels and activates phospholipase D-catalyzed phosphatidylcholine breakdown in Swiss 3T3 cells in the absence of inositol-lipid hydrolysis. Biochem. J. 285, 247-253.
9. Couet, J., Sargiacomo, M., and Lisanti, M.P. (1997). Interaction of a receptor tyrosine kinase, EGF-R, with caveolins: Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272, 30429-30438.
10. English, D., Cui, Y., and Siddiqui, R.A. (1996). Messenger functions of phosphatidic acid. Chem. Phys. Lipids 80, 117-132.
11. Exton, J.H. (1999). Regulation of phospholipase D. Biochim. Biophys. Acta 1439, 121-133.
12. Fabian, J.R., Daar, I.O., and Morrison, D.K. (1993). Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase. Mol. Cell. Biol. 13, 7170-7179.
13. Fukami, K., and Takenawa, T. (1992). Phosphatidic acid that accumulates in platelet-derived growth factor-stimulated Balb/c 3T3 cells is a potential mitogenic signal. J. Biol. Chem. 267, 10988-10993.
14. Ghosh, S., Strum, J.C., Sciorra, V.A., Daniel, L., and Bell, R.M. (1996). Raf-1 kinase possesses distinct binding domains for phosphatidylserine and phosphatidic acid: Phosphatidic acid regulates the translocation of Raf-1 in 12-O-tetradecanoyl phorbol-13-acetate-stimulated Madin-Darby canine kidney cells. J. Biol. Chem. 271, 8472-8480.
15. 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.
16. 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 ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270, 29640-29643.
17. Hammond, S.M., Jenco, J.M., Nakashima, S., Cadwallader, K., Gu, Q., Cook, S., Nozawa, Y., Prestwich, G.D., Frohman, M.A., and Morris, A.J. (1997). Characterization of two alternately spliced forms of phospholipase D1: Activation of the purified enzymes by phosphatidylinositol 4,5-bisphosphate, ADP-ribosylation factor, and Rho family monomeric GTP-binding proteins and protein kinase C-alpha. J. Biol. Chem. 272, 3860-3868.
18. Hess, J.A., Ross, A.H., Qiu, R.G., Symons, M., and Exton, J.H. (1997). Role of Rho family proteins in phospholipase D activation by growth factors. J. Biol. Chem. 272, 1615-1620.
19. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
20. Honda, A., et al. (1999). Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99, 521-532.
21. Hornia, A., Lu, Z., Sukezane, T., Zhong, M., Joseph, T., Frankel, P., and Foster, D.A. (1999). Antagonistic effects of protein kinase C α and δ on both transformation and phospholipase D activity mediated by the epidermal growth factor receptor. Mol. Cell. Biol. 19, 7672-7680.
22. Jones, D., Morgan, C., and Cockcroft, S. (1999). Phospholipase D and membrane traffic: Potential roles in regulated exocytosis, membrane delivery and vesicle budding. Biochim. Biophys. Acta 1439, 229244.
23. Kaszkin, M., Seidler, L., Kast, R., and Kinzel, V. (1992). Epidermal growth factor-induced production of phosphatidylalcohols by HeLa cells and A431 cells through activation of phospholipase D. Biochem. J. 287, 51-57.
24. Kim, J.H., Han, J.M., Lee, S.M., Kim, Y., Lee, T.G., Park, J.B., Lee, S.D., Suh, P.-G., and Ryu, S.H. (1999). Phospholipase D1 in caveolae: Regulation by protein kinase Calpha and caveolin-1. Biochemistry 38, 3763-3769.
25. Kim, J.H., Lee, S.D., Han, J.M., Lee, T.G., Kim, Y., Park, J.B., Lambeth, J.D., Suh, P.G., and Ryu, S.H. (1998). Activation of phospholipase D1 by direct interaction with ADP-ribosylation factor 1 and RalA. FEBS Lett. 430, 231-235.
26. Kim, Y., Han, J.M., Han, B.R., Lee, K.A., Kim, J.H., Lee, B.D., Jang, I.H., Suh, P.G., and Ryu, S.H. (2000). Phospholipase D1 is phosphorylated and activated by protein kinase C in caveolin-enriched microdomains within the plasma membrane. J. Biol. Chem. 275, 13621-13627.
27. Kim, Y., et al. (1999a). Phosphorylation and activation of phospholipase D1 by protein kinase C in vivo: Determination of multiple phosphorylation sites. Biochemistry 38, 10344-10351.
28. Kim, Y., Kim, J.E., Lee, S.D., Lee, T.G., Kim, J.H., Park, J.B., Han, J.M., Jang, S.K., Suh, P.G., and Ryu, S.H. (1999b). Phospholipase D1 is located and activated by protein kinase C alpha in the plasma membrane in 3Y1 fibroblast cell. Biochim. Biophys. Acta 1436, 319-330.
29. Kolch, W., Heidecker, G., Kochs, G., Hummel, R., Vahidi, H., Mischak, H., Finkenzeller, G., Marme, D., and Rapp, U.R. (1993). Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 364, 249-252.
30. Kuroki, T., Kashiwagi, M., Ishino, K., Huh, N, H., and Ohba, M. (1999). Adenovirus-mediated gene transfer to keratinocytes. J. Invest. Dermatol. Symp. Proc. 4, 153-157.
31. Lee, T.G., et al. (1997). Phorbol myristate acetate-dependent association of protein kinase C alpha with phospholipase D1 in intact cells. Biochim. Biophys. Acta 1347, 199-204.
32. Lee, Y.H., Kim, H.S., Pai, J.-K., Ryu, S.H., and Suh, P.-G. (1994). Activation of phospholipase D induced by platelet-derived growth factor is dependent upon the level of phospholipase C-gamma 1. J. Biol. Chem. 269, 26842-26847.
33. Liu, P., Ying, Y., and Anderson, R.G. (1997). Platelet-derived growth factor activates mitogen-activated protein kinase in isolated caveolae. Proc. Natl. Acad. Sci. USA 94, 13666-13670.
34. 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.
35. Marais, R., Light, Y., Paterson, H.F., and Marshall, C.J. (1995). Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J. 14, 3136-3145.
36. Mineo, C., Anderson, R.G.W., and White, M.A. (1997). Physical association with Ras enhances activation of membrane-bound Raf (RafCAAX). J. Biol. Chem. 272, 10345-10348.
37. Mineo, C., Gill, G.N., and Anderson, R.G.W. (1999). Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem. 274, 30636-30643.
38. Mineo, C., James, G.L., Smart, E.J., and Anderson, R.G.W. (1996). Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J. Biol. Chem. 271, 11930-11935.
39. Mineo, C., Ying, Y.-S., Chapline, C., Jaken, S., and Anderson, R.G.W. (1998). Targeting of protein kinase Cα to caveolae. J. Cell Biol. 141, 601-610.
40. Ohba, M., Ishino, K., Kashiwagi, M., Kawabe, S., Chida, K., Huh, N.H., and Kuroki, T. (1998). Induction of differentiation in normal human keratinocytes by adenovirus-mediated introduction of the eta and delta isoforms of protein kinase C. Mol. Cell. Biol. 18, 5199-5207.
41. Okamoto, T., Schlegel, A., Scherer, P.E., and Lisanti, M.P. (1998). Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 273, 5419-5422.
42. Park, S.-K., Provost, J.J., Bae, C.D., Ho, W.-T., and Exton, J.H. (1997). Cloning and characterization of phospholipase D from rat brain. J. Biol. Chem. 272, 29263-29271.
43. Park, W.Y., Park, J.S., Cho, K.A., Kim, D.I., Ko, Y.G., Seo, J.S., and Park, S.C. (2000). Up-regulation of caveolin attenuates epidermal growth factor signaling in senescent cells. J. Biol. Chem. 275, 20847-20852.
44. Pike, L.J., and Miller, J.M. (1998). Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J. Biol. Chem. 273, 22298-22304.
45. Ringerike, T., Blystad, F.D., Levy, F.O., Madshus, I.H., and Stang, E. (2002). Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae. J. Cell Sci. 115, 1331-1340.
46. Rizzo, M.A., Shome, K., Watkins, S.C., and Romeo, G. (2000). The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid, and is independent of association with Ras. J. Biol. Chem. 275, 23911-23918.
47. Roth, M.G., Bi, K., Ktistakis, N.T., and Yu, S. (1999). Phospholipase D as an effector for ADP-ribosylation factor in the regulation of vesicular traffic. Chem. Phys. Lipids 98, 141-152.
48. Roy, S., Lane, A., Yan, J., McPherson, R., and Hancock, J.F. (1997). Activity of plasma membrane-recruited Raf-1 is regulated by Ras via the Raf zinc finger. J. Biol. Chem. 272, 20139-20145.
49. Shen, Y., Xu, L., and Foster, D.A. (2001). Role for phospholipase D in receptor-mediated endocytosis. Mol. Cell. Biol. 21, 595-602.
50. Slaaby, R., Jensen, T., Hansen, H.S., Frohman, M.A., and Seedorf, K. (1998). PLD2 complexes with the EGF receptor and undergoes tyrosine phosphorylation at a single site upon agonist stimulation. J. Biol. Chem. 273, 33722-33727.
51. Smart, E.J., Graf, G.A., McNiven, M.A., Sessa, W.C., Engelman, J.A., Scherer, P.E., Okamoto, T., and Lisanti, M.P. (1999). Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19, 7289-7304.
52. Sugars, J.M., Cellek, S., Manifava, M., Coadwell, J., and Ktistakis, N.T. (1999). Fatty acylation of phospholipase D1 on cysteine residues 240 and 241 determines localization on intracellular membranes. J. Biol. Chem. 274, 30023-30027.
53. Toda, K., Nogami, M., Murakami, K., Kanaho, Y., and Nakayama, K. (1999). Colocalization of phospholipase D1 and GTP-binding-defective mutant of ADP-ribosylation factor 6 to endosomes and lysosomes. FEBS Lett. 442, 221-225.
54. Uittenbogaard, A., and Smart, E.J. (2000). Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J. Biol. Chem. 275, 25595-25599.
55. Ullrich, A., and Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212.
56. Voss, M., Weernink, P.A., Haupenthal, S., Moller, U., Cool, R.H., Bauer, B., Camonis, J.H., Jakobs, K.H., and Schmidt, M. (1999). Phospholipase D stimulation by receptor tyrosine kinases mediated by protein kinase C and a Ras/Ral signaling cascade. J. Biol. Chem. 274, 34691-34698.
57. Waugh, M.G., Lawson, D., and Hsuan, J.J. (1999). Epidermal growth factor receptor activation is localized within low-buoyant density, non-caveolar membrane domains. Biochem. J. 337, 591-597.
58. Way, G., O'Luanaigh, N., and Cockcroft, S. (2000). Activation of exocytosis by cross-linking of the IgE receptor is dependent on ADP-ribosylation factor 1-regulated phospholipase D in RBL-2H3 mast cells: Evidence that the mechanism of activation is via regulation of phosphatidylinositol 4,5-bisphosphate synthesis. Biochem. J. 346, 63-70.
59. Yeo, E.-J., and Exton, J.H. (1995). Stimulation of phospholipase D by epidermal growth factor requires protein kinase C activation in Swiss 3T3 cells. J. Biol. Chem. 270, 3980-3988.
60. Zhang, Y., Altshuller, Y.M., Hammond, S.M., Hayes, F., Morris, A.J., and Frohman, M.A. (1999). Loss of receptor regulation by a phospholipase D1 mutant unresponsive to protein kinase C. EMBO J. 18, 6339-6348.