Elevated phospholipase D activity in H-Ras- but not K-Ras-transformed cells by the synergistic action of RalA and ARF6

Molecular and Cellular Biology

Volumn 23, Issue 2, 2003, Pages 645-654

  Xu, Lizhong ^a   Frankel, Paul ^a   Jackson, Desmond ^a   Rotunda, Thuy ^a   Boshans, Rita L ^b   D'Souza Schorey, Crislyn ^b   Foster, David A ^a,c  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; PHOSPHOLIPASE D; PROTEIN; PROTEIN RA1A; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; WESTERN BLOTTING;

3T3 CELLS; ADP-RIBOSYLATION FACTORS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TRANSFORMED; CELL MEMBRANE; GENES, DOMINANT; GENES, RAS; GTP PHOSPHOHYDROLASES; MICE; MODELS, BIOLOGICAL; MUTATION; PHOSPHOLIPASE D; PLASMIDS; PRECIPITIN TESTS; PROTEIN BINDING; RAL GTP-BINDING PROTEINS;

ANIMALIA;

EID: 0037222792     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.2.645-654.2003     Document Type: Article

References (81)

1. Aguirre Ghiso, J., P. Frankel, Z. Lu, H. Jiang, E. Farias, A. Olsen, L. A. Feig, E. B. de Kier Joffe, and D. A. Foster. 1999. RalA requirement for v-Src- and v-Ras-induced tumorigenicity and overproduction of urokinase-type plasminogen activator and metalloproteases. Oncogene 18:4718-4725.
2. Alam, M. S., Y. Banno, S. Nakashima, and Y. Nozawa. 1995. Defective phospholipase D activation in Ki-ras-transformed NIH3T3 cells: Evidence for downstream effector of PLC-γ1 in PDGF-mediated signal transduction. Biochem. Biophys. Res. Commun. 207:460-466.
3. Apolloni, A., I. A. Prior, M. Lindsay, R. G. Parton, and J. F. Hancock. 2000. H-Ras but not K-Ras traffics to the plasma membrane through the exocytic pathway. Mol. Cell. Biol. 20:2475-2487.
4. Bos, J. L. 1989. Ras oncogenes in human cancer: A review. Cancer Res. 49:4682-4689.
5. Boshans, R. L., S. Szanto, L. van Aelst, and C. D'Souza-Schorey. 2000. ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol. Cell. Biol. 20:3685-3694.
6. Bowman, E. P., D. J. Uhlinger, and J. D. Lambeth. 1993. Neutrophil phospholipase D is activated by a membrane-associated Rho family small molecular weight GTP-binding protein. J. Biol. Chem. 268:21509-21512.
7. Brown, H. A., S. Gutowski, C. R. Moomaw, C. Slaughter, and P. C. Sternweis. 1993. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75:1137-1144.
8. Cantor, S. B., T. Urano, and L. A. Feig. 1995. Identification and characterization of Ral-binding protein 1, a potential downstream target of Ral GTPases. Mol. Cell. Biol. 15:4578-4584.
9. Carnero, A., A. Cuadrado, L. del Peso, and J. C. Lacal. 1994. Activation of type D phospholipase by serum stimulation and ras-induced transformation in NIH3T3 cells. Oncogene 9:1387-1395.
10. Caumont, A. S., M. C. Galas, N. Vitale, D. Aunis, and M. F. Bader. 1998. Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J. Biol. Chem. 273:1373-1379.
11. Caumont, A. S., N. Vitale, M. Gensse, M. C. Galas, J. E. Casanova, and M. F. Bader. 2000. Identification of a plasma membrane-associated guanine nucleotide exchange factor for ARF6 in chromaffin cells. Possible role in the regulated exocytotic pathway. J. Biol. Chem. 275:15637-15644.
12. Chardin, P., S. Paris, B. Antonny, S. Robineau, S. Beraud-Dufour, C. L. Jackson, and M. Chabre. 1996. A human exchange factor for ARF contains Sec7- and pleckstrin-homology domains. Nature 384:481-484.
13. Chavrier, P., and B. Goud. 1999. The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11:466-475.
14. Choy, E., V. K. Chiu, J. Silletti, M. Feokitistov, T. Morimoto, D. Michaelson, I. E. Ivanov, and M. R. Philips. 1999. Endomembrane trafficking of Ras: The CAAX motif targets proteins to the ER and Golgi. Cell 98:69-80.
15. Cockcroft, S., G. M. Thomas, A. Fensome, B. Geny, E. Cunningham, I. 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.
16. Colley, W. C., T. C. Sung, R. Roll, J. Jenco, S. M. Hammond, Y. Altshuller, D. Bar-Sagi, A. J. Morris, and M. A. Frohman. 1997. Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr. Biol. 7:191-201.
17. 182-101. J. Biol. Chem. 274:2717-2724.
18. D'Souza-Schorey, C., G. Li, M. I. Colombo, and P. D. Stahl. 1995. A regulatory role for ARF6 in receptor-mediated endocytosis. Science 267:1175-1178.
19. D'Souza-Schorey, C., E. van Donselaar, V. W. Hsu, C. Yang, P. D. Stahl, and P. J. Peters. 1998. ARF6 targets recycling vesicles to the plasma membrane: Insights from an ultrastructural investigation. J. Cell Biol. 140:603-616.
20. Exton, J. H. 2000. Phospholipase D. Ann. N. Y. Acad. Sci. 905:61-68.
21. Fensome, A., E. Cunningham, S. Prosser, S. K. Tan, P. Swigart, G. Thomas, J. Hsuan, and S. Cockcroft. 1996. ARF and PITP restore GTPγS-stimulated protein secretion from cytosol-depleted HL60 cells by promoting PIP2 synthesis. Curr. Biol. 6:730-738.
22. 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.
23. Frankel, P. A., M. Ramos, J. Flom, S. Bychenok, E. Kerkhoff, U. R. Rapp, L. A. Feig, and D. A. Foster. 1999. Ral and Rho dependent activation of phospholipase D in v-Raf transformed cells. Biochem. Biophys. Res. Commun. 255:502-507.
24. Furuchi, T., and R. G. Anderson. 1998. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J. Biol. Chem. 273:21099-21104.
25. Guillemain, I., and J. H. Exton. 1997. Effects of brefeldin A on phosphatidylcholine phospholipase D and inositolphospholipid metabolism in HL-60 cells. Eur. J. Biochem. 249:812-819.
26. Hamad, N. M., J. H. Elconin, A. E. Karnoub, W. Bai, J. N. Rich, R. T. Abraham, C. J. Der, and C. M. Counter. 2002. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev. 16:2045-2057.
27. Hammond, S. M., Y. M. Altshuller, T. C. Sung, S. A. Rudge, K. Ross, J. Engebrecht, A. J. Morris, and M. A. Frohman. 1995. Human ARF-activated phosphatidylcholine-specific phospholipase D defines a new highly conserved gene family. J. Biol. Chem. 270:29640-29643.
28. Hammond, S. M., J. M. Jenco, S. Nakashima, K. Cadwallader, Q. Gu, S. Cook, Y. Nozawa, G. D. Prestwich, M. A. Frohman, and A. J. Morris. 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 α. J. Biol. Chem. 272:3860-3868.
29. Honda, A., M. Nogami, T. Yokozeki, M. Yamazaki, H. Nakamura, H. Watanabe, K. Kawamoto, K. Nakayama, A. J. Morris, M. A. Frohman, and Y. Kanaho. 1999. Phosphatidylinositol 4-phosphate 5-kinase α is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521-532.
30. Hornia, A., Z. Lu, T. Sukezane, M. Zhong, T. Joseph, P. Frankel, and D. A. Foster. 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.
31. Hueber, A. O., and G. I. Evan. 1998. Traps to catch unwary oncogenes. Trends Genet. 14:364-367.
32. Humeau, Y., N. Vitale, S. Chasserot-Golaz, J. L. Dupont, G. Du, M. A. Frohman, M. F. Bader, and B. Poulain. 2001. A role for phospholipase D1 in neurotransmitter release. Proc. Natl. Acad. Sci. USA 98:15300-15305.
33. Jenkins, G. H., P. L. Fisette, and R. A. Anderson. 1994. Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J. Biol. Chem. 269:11547-11554.
34. Jiang, H., Z. Lu, J.-Q Luo, A. Wolfman, and D. A. Foster. 1995. Ras mediates the activation of phospholipase D by v-Src. J. Biol. Chem. 270:6006-6009.
35. Jiang, H., J.-Q. Luo, T. Urano, Z. Lu, D. A. Foster, and L. A. Feig. 1995. Involvement of Ral GTPase in v-Src-induced phospholipase D activation. Nature 378:409-412.
36. Jiang, Y.-W., J. Song, Q. Zang, and D. A. Foster. 1994. Phosphatidylcholine-specific phospholipase D activity is elevated in v-Fps-transformed cells. Biochem. Biophys. Res. Commun. 203:1195-1203.
37. Joneson, T., and D. Bar-Sagi. 1999. Suppression of Ras-induced apoptosis by the Rac GTPase. Mol. Cell. Biol. 19:5892-5901.
38. Joseph, T., R. Wooden, A. Bryant, M. Zhong, Z. Lu, and D. A. Foster. 2001. Transformation of cells overexpressing a tyrosine kinase by phospholipase D1 and D2. Biochem. Biophys. Res. Commun. 289:1019-1024.
39. Joseph, T., A. Bryant, R. Wooden, E. Kerkhoff, U. R. Rapp, and D. A. Foster. 2002. Phospholipase D overcomes cell cycle arrest induced by high-intensity Raf signaling. Oncogene 21:3651-3658.
40. Kim, J. H., S. D. Lee, J. M. Han, T. G. Lee, Y. Kim, J. B. Park, J. D. Lambeth, P. G. Suh, and S. H. Ryu. 1998. Activation of phospholipase D1 by direct interaction with ADP-ribosylation factor 1 and RalA. FEBS Lett. 430:231-235.
41. Kim, J. H., J. M. Han, S. Lee, Y. Kim, T. G. Lee, J. B. Park, S. D. Lee, P. G. Suh, and S. H. Ryu. 1999. Phospholipase D1 in caveolae: Regulation by protein kinase Cα and caveolin-1. Biochemistry 38:3763-3769.
42. Lisanti, M. P., Z. Tang, P. E. Scherer, E. Kubler, A. J. Koleske, and M. Sargiacomo. 1995. Caveolae, transmembrane signalling and cellular transformation. Mol. Membr. Biol. 12:121-124.
43. Liscovitch, M., M. Czarny, G. Fiucci, Y. Lavie, and X. Tang. 1999. Localization and possible functions of phospholipase D isozymes. Biochim. Biophys. Acta 1439:245-263.
44. Lu, Z., A. Hornia, T. Joseph, T. Sukezane, P. Frankel, M. Zhong, S. Bychenok, L. Xu, L. A. Feig, and D. A. Foster. 2000. Phospholipase D and RalA cooperate with the EGF receptor to transform 3Y1 rat fibroblasts. Mol. Cell. Biol. 20:462-467.
45. Lucas, L., L. del Peso, P. Rodriguez, V. Penalva, and J. C. Lacal. 2000. Ras protein is involved in the physiological regulation of phospholipase D by platelet derived growth factor. Oncogene 19:431-437.
46. Luo, J.-Q., X. Liu, S. M. Hammond, W. C. Colley, L. A. Feig, M. A. Frohman, A. J. Morris, and D. A. Foster. 1997. Ral interacts directly with the ARF-responsive PIP2-dependent phospholipase D1. Biochem. Biophys. Res. Commun. 235:854-859.
47. Luo, J.-Q., X. Liu, P. Frankel, T. Rotunda, M. Ramos, J. Flom, H. Jiang, L. A. Feig, A. J. Morris, R. A. Kahn, and D. A. Foster. 1998. Functional association between RalA and ARF in active phospholipase D complexes. Proc. Natl. Acad. Sci. USA 95:3632-3637.
48. 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 facators 1,5, and 6: Separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes. Proc. Natl. Acad. Sci. USA 91:11718-11722.
49. Melendez, A. J., M. M. Harnett, and J. M. Allen. 2001. Crosstalk between ARF6 and protein kinase Cα in FcγRI-mediated activation of phospholipase D1. Curt. Biol. 11:869-874.
50. Moss, J., and M. Vaughan. 1998. Molecules in the ARF orbit. J. Biol. Chem. 273:21431-21434.
51. Mwanjewe, J., M. Spitaler, M. Ebner, M. Windegger, M. Geiger, S. Kampfer, J. Hofmann, F. Uberall, and H. H. Grunicke. 2001. Regulation of phospholipase D isoenzymes by transforming Ras and atypical protein kinase C-iota. Biochem. J. 359:211-217.
52. Noh, D. Y., S. J. Ahn, R. A. Lee, I. A. Park, J. H. Kim, P. G. Suh, S. H. Ryu, K. H. Lee, and J. S. Han. 2000. Overexpression of phospholipase D1 in human breast cancer tissues. Cancer Lett. 161:207-214.
53. Peyroche, A., B. Antonny, S. Robineau, J. Acker, J. Cherfils, and C. L. Jackson. 1999. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: Involvement of specific residues of the Sec7 domain. Mol. Cell 3:275-285.
54. Powner, D. J., M. N. Hodgkin, and M. J. Wakelam. 2002. Antigen-stimulated activation of phospholipase D1b by Rac1, ARF6, and PKCα in RBL-2H3 cells. Mol. Biol. Cell 13:1252-1262.
55. Prior, I. A., A. Harding, J. Yan, J. Sluimer, R. G. Parton, and J. F. Hancock. 2001. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:368-375.
56. Rizzo, M. A., K. Shome, C. Vasudevan, D. B. Stolz, T. C. Sung, M. A. Frohman, S. C. Watkins, and G. Romero. 1999. Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent raf-1 translocation to the plasma membrane and the activation of the mitogen-activated protein kinase pathway. J. Biol. Chem. 274:1131-1139.
57. Robineau, S., M. Chabre, and B. Antonny. 2000. Binding site of brefeldin A at the interface between the small G protein ADP-ribosylation factor 1 (ARF1) and the nucleotide-exchange factor Sec7 domain. Proc Natl. Acad. Sci. USA 97:9913-9918.
58. Roy, S., R. Luetterforst, A. Harding, A. Apolloni, M. Etheridge, E. Stang, B. Rolls, J. F. Hancock, and R. G. Parton. 1999. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1:98-105.
59. Santy, L. C., and J. E. Casanova. 2001. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154:599-610.
60. Schmidt, M., M. Vo, M. Thiel, B. Bauer, A. Granna, E. Tapp, R. H. Cool, J. deGunzburg, C. von Eichel-Streiber, and K. H. Jakobs. 1998. Specific inhibition of phorbol ester-stimulated phospholipase D by Clostridium sordellii lethal toxin and Clostridium difficile toxin B-1470 in HEK-293 cells. Restoration by Ral GTPases. J. Biol. Chem. 273:7413-7422.
61. Shen, Y., L. Xu, and D. A. Foster. 2001. A role for phospholipase D in receptor-mediated endocytosis. Mol. Cell. Biol. 21:595-602.
62. Shome, K., Y. Nie, and G. Romero. 1998. ADP-ribosylation factor proteins mediate agonist-induced activation of phospholipase D. J. Biol. Chem. 273:30836-30841.
63. Shome, K., M. A. Rizzo, C. Vasudevan, B. Andresen, and G. Romero. 2000. The activation of phospholipase D by endothelin-1, angiotensin II, and platelet-derived growth factor in vascular smooth muscle A10 cells is mediated by small G proteins of the ADP-ribosylation factor family. Endocrinology 141:2200-2208.
64. Shome, K., C. Vasudevon, and G. Romero. 1997. ARF proteins mediate insulin-dependent activation of phospholipase D. Curr. Biol. 7:387-396.
65. Someya, A., M. Sata, K. Takeda, G. Pacheco-Rodriguez, V. J. Ferrans, J. Moss, and M. Vaughan. 2001. ARF-GEP(100), a guanine nucleotide-exchange protein for ADP-ribosylation factor 6. Proc. Natl. Acad. Sci. USA 98:2413-2418.
66. Song, J., L. M. Pfeffer, and D. A. Foster. 1991. v-Src increases diacylglycerol levels via a type D phospholipase-mediated hydrolysis of phosphatidylcholine. Mol. Cell. Biol. 11:4903-4908.
67. Song, J., and D. A. Foster. 1993. v-Src activates a phospholipase D activity that is distinguishable from phospholipase D activity activated by protein kinase C. Biochem. J. 294:711-717.
68. Song, S. K., S. Li, T. Okamoto, L. A. Quilliam, M. Sargiacomo, and M. P. Lisanti. 1996. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271:9690-9697.
69. Toda, K., M. Nogami, K. Murakami, Y. Kanaho, and K. Nakayama. 1999. Colocalization of phospholipase D1 and GTP-binding-defective mutant of ADP-ribosylation factor 6 to endosomes and lysosomes. FEBS Lett. 442: 221-225.
70. Urano, T., R. Emkey, and L. A. Feig. 1996. Ral GTPases mediate a distinct downstream signaling pathway from Ras that facilitates cellular transformation. EMBO J. 16:810-816.
71. Vitale, N., A. S. Caumont, S. Chasserot-Golaz, G. Du, S. Wu, V. A. Sciorra, A. J. Morris, M. A. Frohman, and M. F. Bader. 2001. Phospholipase D1: A key factor for the exocytotic machinery in neuroendocrine cells. EMBO J. 20:2424-2434.
72. Voice, J. K., R. L. Klemke, A. Le, and J. H. Jackson. 1999. Four human ras homologs differ in their abilities to activate Raf-1, induce transformation, and stimulate cell motility. J. Biol. Chem. 274:17164-17170.
73. Voss, M., P. A. Weernink, S. Haupenthal, U. Moller, R. H. Cool, B. Bauer, J. H. Camonis, K. H. Jakobs, and M. Schmidt. 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.
74. Walsh, A. B., and D. Bar-Sagi. 2001. Differential activation of the Rac pathway by Ha-Ras and K-Ras. J. Biol. Chem. 276:15609-15615.
75. White, M. A., and R. G. W. Anderson. 2001. Which Ras rides the raft? Nat. Cell Biol. 3:E172.
76. Wolthuis, R. M. F., B. Franke, M. van Triest, B. Bauer, R. H. Cool, J. H. Camonis, J.-W. Akkerman, and J. L. Bos. 1998. Activation of the small GTPase Ral in platelets. Mol. Cell. Biol. 18:2486-2491.
77. Wolthuis, R. M. F., F. Zwartkruis, T. C. Moen, and J. L. Bos. 1998. Ras-dependent activation of the small GTPase Ral. Curr. Biol. 8:471-474.
78. Xu, L., Y. Shen, T. Joseph, A. Bryant, J. Q. Luo, P. Frankel, T. Rotunda, and D. A. Foster. 2000. Mitogenic phospholipase D activity is restricted to caveolin-enriched membrane microdomains. Biochem. Biophys. Res. Commun. 273:77-83.
79. Yan, J., S. Roy, A. Apolloni, A. Lane, and J. F. Hancock. 1998. Ras isoforms vary in their ability to activate Raf-1 and phosphoinositide 3-kinase. J. Biol. Chem. 273:24052-24056.
80. Zhao, Y., H. Ehara, Y. Akao, M. Shamoto, Y. Nakagawa, Y. Banno, T. Deguchi, N. Ohishi, K. Yagi, and Y. Nozawa. 2000. Increased activity and intranuclear expression of phospholipase D2 in human renal cancer. Biochem. Biophys. Res. Commun. 278:140-143.
81. Zhong, M., T. Joseph, D. Jackson, S. Beychenok, and D. A. Foster. 2002. Elevated phospholipase D induces apoptosis in normal rat fibroblasts. Biochem. Biophys. Res. Commun. 298:474-477.