Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Nov 22;91(24):11718–11722. doi: 10.1073/pnas.91.24.11718

Activation of rat brain phospholipase D by ADP-ribosylation factors 1,5, and 6: separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes.

D Massenburg 1, J S Han 1, M Liyanage 1, W A Patton 1, S G Rhee 1, J Moss 1, M Vaughan 1
PMCID: PMC45303  PMID: 7972129

Abstract

Two major forms of phospholipase D (PLD) activity, solubilized from rat brain membranes with Triton X-100, were separated by HPLC on a heparin-5PW column with buffer containing octyl glucoside. One form was completely dependent on sodium oleate for activity. The other, which was dramatically activated by the addition of ADP-ribosylation factor (ARF) 1 and guanine 5' [gamma-thio]triphosphate, required the presence of phosphatidylinositol 4,5-bisphosphate in the phosphatidylcholine substrate for demonstration of activity, as described by others. Oleate-dependent activity was unaffected by guanine 5' [gamma-thio]triphosphate, or phosphatidylinositol 4,5-bisphosphate. Both sodium oleate-and ARF-dependent activities catalyzed transphosphatidylation, thus identifying them as PLDs. ARF-dependent PLD was activated by recombinant ARF5 (class II) and ARF6 (class III), as well as ARF1 (class I). Myristoylated recombinant ARFs were more effective than their nonmyristoylated counterparts. ARFs were originally identified as activators of cholera toxin ADP-ribosyltransferase activity. The effects of recombinant ARF proteins from the three classes on cholera toxin activity (assayed under conditions identical to those used to assay PLD activity) did not, however, correlate with those on PLD, consistent with the notion that different aspects of ARF structure are involved in the two functions.

Full text

PDF
11721

Images in this article

11720Image
on p.11720

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anthes J. C., Eckel S., Siegel M. I., Egan R. W., Billah M. M. Phospholipase D in homogenates from HL-60 granulocytes: implications of calcium and G protein control. Biochem Biophys Res Commun. 1989 Aug 30;163(1):657–664. doi: 10.1016/0006-291x(89)92187-6. [DOI] [PubMed] [Google Scholar]
  2. Billah M. M., Eckel S., Mullmann T. J., Egan R. W., Siegel M. I. Phosphatidylcholine hydrolysis by phospholipase D determines phosphatidate and diglyceride levels in chemotactic peptide-stimulated human neutrophils. Involvement of phosphatidate phosphohydrolase in signal transduction. J Biol Chem. 1989 Oct 15;264(29):17069–17077. [PubMed] [Google Scholar]
  3. Bobak D. A., Bliziotes M. M., Noda M., Tsai S. C., Adamik R., Moss J. Mechanism of activation of cholera toxin by ADP-ribosylation factor (ARF): both low- and high-affinity interactions of ARF with guanine nucleotides promote toxin activation. Biochemistry. 1990 Jan 30;29(4):855–861. doi: 10.1021/bi00456a600. [DOI] [PubMed] [Google Scholar]
  4. Bocckino S. B., Blackmore P. F., Wilson P. B., Exton J. H. Phosphatidate accumulation in hormone-treated hepatocytes via a phospholipase D mechanism. J Biol Chem. 1987 Nov 5;262(31):15309–15315. [PubMed] [Google Scholar]
  5. Bocckino S. B., Wilson P. B., Exton J. H. Ca2+-mobilizing hormones elicit phosphatidylethanol accumulation via phospholipase D activation. FEBS Lett. 1987 Dec 10;225(1-2):201–204. doi: 10.1016/0014-5793(87)81157-2. [DOI] [PubMed] [Google Scholar]
  6. Brown H. A., Gutowski S., Moomaw C. R., Slaughter C., Sternweis P. C. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell. 1993 Dec 17;75(6):1137–1144. doi: 10.1016/0092-8674(93)90323-i. [DOI] [PubMed] [Google Scholar]
  7. Chalifa V., Möhn H., Liscovitch M. A neutral phospholipase D activity from rat brain synaptic plasma membranes. Identification and partial characterization. J Biol Chem. 1990 Oct 15;265(29):17512–17519. [PubMed] [Google Scholar]
  8. Chalifour R. J., Kanfer J. N. Microsomal phospholipase D of rat brain and lung tissues. Biochem Biophys Res Commun. 1980 Sep 30;96(2):742–747. doi: 10.1016/0006-291x(80)91417-5. [DOI] [PubMed] [Google Scholar]
  9. Cockcroft S., Thomas G. M., Fensome A., Geny B., Cunningham E., Gout I., Hiles I., Totty N. F., Truong O., Hsuan J. J. Phospholipase D: a downstream effector of ARF in granulocytes. Science. 1994 Jan 28;263(5146):523–526. doi: 10.1126/science.8290961. [DOI] [PubMed] [Google Scholar]
  10. Domino S. E., Bocckino S. B., Garbers D. L. Activation of phospholipase D by the fucose-sulfate glycoconjugate that induces an acrosome reaction in spermatozoa. J Biol Chem. 1989 Jun 5;264(16):9412–9419. [PubMed] [Google Scholar]
  11. Exton J. H. Signaling through phosphatidylcholine breakdown. J Biol Chem. 1990 Jan 5;265(1):1–4. [PubMed] [Google Scholar]
  12. Geny B., Fensome A., Cockcroft S. Rat brain cytosol contains a factor which reconstitutes guanine-nucleotide-binding-protein-regulated phospholipase-D activation in HL60 cells previously permeabilized with streptolysin O. Eur J Biochem. 1993 Jul 15;215(2):389–396. doi: 10.1111/j.1432-1033.1993.tb18045.x. [DOI] [PubMed] [Google Scholar]
  13. Hattori H., Kanfer J. N. Synaptosomal phospholipase D potential role in providing choline for acetylcholine synthesis. J Neurochem. 1985 Nov;45(5):1578–1584. doi: 10.1111/j.1471-4159.1985.tb07229.x. [DOI] [PubMed] [Google Scholar]
  14. Haun R. S., Tsai S. C., Adamik R., Moss J., Vaughan M. Effect of myristoylation on GTP-dependent binding of ADP-ribosylation factor to Golgi. J Biol Chem. 1993 Apr 5;268(10):7064–7068. [PubMed] [Google Scholar]
  15. Heller M. Phospholipase D. Adv Lipid Res. 1978;16:267–326. doi: 10.1016/b978-0-12-024916-9.50011-1. [DOI] [PubMed] [Google Scholar]
  16. Hong J. X., Haun R. S., Tsai S. C., Moss J., Vaughan M. Effect of ADP-ribosylation factor amino-terminal deletions on its GTP-dependent stimulation of cholera toxin activity. J Biol Chem. 1994 Apr 1;269(13):9743–9745. [PubMed] [Google Scholar]
  17. Huang C., Wykle R. L., Daniel L. W., Cabot M. C. Identification of phosphatidylcholine-selective and phosphatidylinositol-selective phospholipases D in Madin-Darby canine kidney cells. J Biol Chem. 1992 Aug 25;267(24):16859–16865. [PubMed] [Google Scholar]
  18. Kahn R. A., Gilman A. G. Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. J Biol Chem. 1984 May 25;259(10):6228–6234. [PubMed] [Google Scholar]
  19. Kahn R. A., Yucel J. K., Malhotra V. ARF signaling: a potential role for phospholipase D in membrane traffic. Cell. 1993 Dec 17;75(6):1045–1048. doi: 10.1016/0092-8674(93)90314-g. [DOI] [PubMed] [Google Scholar]
  20. Lee K. Y., Ryu S. H., Suh P. G., Choi W. C., Rhee S. G. Phospholipase C associated with particulate fractions of bovine brain. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5540–5544. doi: 10.1073/pnas.84.16.5540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martin T. W. Formation of diacylglycerol by a phospholipase D-phosphatidate phosphatase pathway specific for phosphatidylcholine in endothelial cells. Biochim Biophys Acta. 1988 Oct 14;962(3):282–296. doi: 10.1016/0005-2760(88)90258-5. [DOI] [PubMed] [Google Scholar]
  22. Moss J., Vaughan M. ADP-ribosylation factors, 20,000 M(r) guanine nucleotide-binding protein activators of cholera toxin and components of intracellular vesicular transport systems. Cell Signal. 1993 Jul;5(4):367–379. doi: 10.1016/0898-6568(93)90076-x. [DOI] [PubMed] [Google Scholar]
  23. Möhn H., Chalifa V., Liscovitch M. Substrate specificity of neutral phospholipase D from rat brain studied by selective labeling of endogenous synaptic membrane phospholipids in vitro. J Biol Chem. 1992 Jun 5;267(16):11131–11136. [PubMed] [Google Scholar]
  24. Natarajan V., Taher M. M., Roehm B., Parinandi N. L., Schmid H. H., Kiss Z., Garcia J. G. Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. J Biol Chem. 1993 Jan 15;268(2):930–937. [PubMed] [Google Scholar]
  25. Pai J. K., Siegel M. I., Egan R. W., Billah M. M. Phospholipase D catalyzes phospholipid metabolism in chemotactic peptide-stimulated HL-60 granulocytes. J Biol Chem. 1988 Sep 5;263(25):12472–12477. [PubMed] [Google Scholar]
  26. Panagia V., Ou C., Taira Y., Dai J., Dhalla N. S. Phospholipase D activity in subcellular membranes of rat ventricular myocardium. Biochim Biophys Acta. 1991 May 7;1064(2):242–250. doi: 10.1016/0005-2736(91)90308-u. [DOI] [PubMed] [Google Scholar]
  27. Price S. R., Welsh C. F., Haun R. S., Stanley S. J., Moss J., Vaughan M. Effects of phospholipid and GTP on recombinant ADP-ribosylation factors (ARFs). Molecular basis for differences in requirements for activity of mammalian ARFs. J Biol Chem. 1992 Sep 5;267(25):17766–17772. [PubMed] [Google Scholar]
  28. Rothman J. E., Orci L. Molecular dissection of the secretory pathway. Nature. 1992 Jan 30;355(6359):409–415. doi: 10.1038/355409a0. [DOI] [PubMed] [Google Scholar]
  29. Saito M., Bourque E., Kanfer J. Phosphatidohydrolase and base-exchange activity of commercial phospholipase D. Arch Biochem Biophys. 1974 Oct;164(2):420–428. doi: 10.1016/0003-9861(74)90051-4. [DOI] [PubMed] [Google Scholar]
  30. Saito M., Kanfer J. Solubilization and properties of a membrane-bound enzyme from rat brain catalyzing a base-exchange reaction. Biochem Biophys Res Commun. 1973 Jul 17;53(2):391–398. doi: 10.1016/0006-291x(73)90674-8. [DOI] [PubMed] [Google Scholar]
  31. Stutchfield J., Cockcroft S. Correlation between secretion and phospholipase D activation in differentiated HL60 cells. Biochem J. 1993 Aug 1;293(Pt 3):649–655. doi: 10.1042/bj2930649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tettenborn C. S., Mueller G. C. 12-O-tetradecanoylphorbol-13-acetate activates phosphatidylethanol and phosphatidylglycerol synthesis by phospholipase D in cell lysates. Biochem Biophys Res Commun. 1988 Aug 30;155(1):249–255. doi: 10.1016/s0006-291x(88)81076-3. [DOI] [PubMed] [Google Scholar]
  33. Tsai S. C., Adamik R., Haun R. S., Moss J., Vaughan M. Effects of brefeldin A and accessory proteins on association of ADP-ribosylation factors 1, 3, and 5 with Golgi. J Biol Chem. 1993 May 25;268(15):10820–10825. [PubMed] [Google Scholar]
  34. Wang P., Anthes J. C., Siegel M. I., Egan R. W., Billah M. M. Existence of cytosolic phospholipase D. Identification and comparison with membrane-bound enzyme. J Biol Chem. 1991 Aug 15;266(23):14877–14880. [PubMed] [Google Scholar]
  35. Welsh C. F., Moss J., Vaughan M. Isolation of recombinant ADP-ribosylation factor 6, an approximately 20-kDa guanine nucleotide-binding protein, in an activated GTP-bound state. J Biol Chem. 1994 Jun 3;269(22):15583–15587. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES