The role of diacylglyceride generation by phospholipase D and phosphatidic acid phosphatase in the activation of 5-lipoxygenase in polymorphonuclear leukocytes

Journal of Leukocyte Biology

Volumn 83, Issue 4, 2008, Pages 1019-1027

  Albert, Dana ^a   Pergola, Carlo ^b   Koeberle, Andreas ^b   Dodt, Gabriele ^b   Steinhilber, Dieter ^a   Werz, Oliver ^b  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

1 oleoyl 2 acetyl glycerol; Arachidonic acid; Inflammation; Ionophore; Leukotriene

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; BUTANOL; CALCIMYCIN; DIACYLGLYCEROL; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE D; THAPSIGARGIN;

ARTICLE; CELL NUCLEUS MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; NEUTROPHIL; NORMAL HUMAN; PRIORITY JOURNAL; ADULT; BLOOD; DRUG ANTAGONISM; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; REFERENCE VALUE;

1-BUTANOL; ADULT; ARACHIDONATE 5-LIPOXYGENASE; CALCIMYCIN; DIGLYCERIDES; ENZYME ACTIVATION; HUMANS; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE D; REFERENCE VALUES; THAPSIGARGIN;

EID: 44449157335     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0807531     Document Type: Article

References (51)

1. Werz, O., Steinhilber, D. (2006) Therapeutic options for 5-lipoxygenase inhibitors. Pharmacol. Ther. 112, 701-718.
2. Werz, O. (2002) 5-Lipoxygenase: cellular biology and molecular pharmacology. Curr. Drug Targets Inflamm. Allergy 1, 23-44.
3. Rådmark, O., Werz, O., Steinhilber, D., Samuelsson, B. (2007) 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32, 332-341.
4. Rakonjac, M., Fischer, L., Provost, P., Werz, O., Steinhilber, D., Samuelsson, B., Rådmark, O. (2006) Coactosin-like protein supports 5-lipoxygenase enzyme activity and up-regulates leukotriene A4 production. Proc. Natl. Acad. Sci. USA 103, 13150-13155.
5. Provost, P., Doucet, J., Hammarberg, T., Gerisch, G., Samuelsson, B., Rådmark, O. (2001) 5-Lipoxygenase interacts with coactosin-like protein. J. Biol. Chem. 276, 16520-16527.
6. Rouzer, C. A., Samuelsson, B. (1986) The importance of hydroperoxide activation for the detection and assay of mammalian 5-lipoxygenase. FEBS Lett. 204, 293-296.
7. Hammarberg, T., Kuprin, S., Rådmark, O., Holmgren, A. (2001) Epr investigation of the active site of recombinant human 5-lipoxygenase: inhibition by selenide. Biochemistry 40, 6371-6378.
8. Bürkert, E., Arnold, C., Hammarberg, T., Rådmark, B., Steinhilber, D., Werz, O. (2003) The C2-like β barrel domain mediates the Ca2+-dependent resistance of 5-lipoxygenase activity against inhibition by glutathione peroxidase-1. J. Biol. Chem. 278, 42846-42853.
9. Hornig, C., Albert, D., Fischer, L., Hornig, M., Rådmark, O., Steinhilber, D., Werz, O. (2005) 1-Oleoyl-2-acetylglycerol stimulates 5-lipoxygenase activity via a putative (phospho)lipid binding site within the N-terminal C2-like domain. J. Biol. Chem. 280, 26913-26921.
10. Albert, D., Burkert, E., Steinhilber, D., Werz, O. (2003) Induction of 5-lipoxygenase activation in polymorphonuclear leukocytes by 1-oleoyl-2-acetylglycerol. Biochim. Biophys. Acta 1631, 85-93.
11. Agwu, D. E., McPhail, L. C., Chabot, M. C., Daniel, L. W., Wykle, R. L., McCall, C. E. (1989) Choline-linked phosphoglycerides. A source of phosphatidic acid and diglycerides in stimulated neutrophils. J. Biol. Chem. 264, 1405-1413.
12. Cockcroft, S. (1984) Ca2+-dependent conversion of phosphatidylinositol to phosphatidate in neutrophils stimulated with fMet-Leu-Phe or ionophore A23187. Biochim. Biophys. Acta 795, 37-46.
13. Reinhold, S. L., Prescott, S. M., Zimmerman, G. A., McIntyre, T. M. (1990) Activation of human neutrophil phospholipase D by three separable mechanisms. FASEB J. 4, 208-214.
14. Balsinde, J., Diez, E., Mollinedo, F. (1988) Phosphatidylinositol- specific phospholipase D: a pathway for generation of a second messenger. Biochem. Biophys. Res. Commun. 154, 502-508.
15. Billah, M. M., Eckel, S., Mullmann, T. J., Egan, R. W., Siegel, M. I. (1989) 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. 264, 17069-17077.
16. Lin, P., Gilfillan, A. M. (1992) The role of calcium and protein kinase C in the IgE-dependent activation of phosphatidylcholine-specific phospholipase D in a rat mast (RBL 2H3) cell line. Eur. J. Biochem. 207, 163-168.
17. Werz, O., Burkert, E., Samuelsson, B., Rådmark, O., Steinhilber, D. (2002) Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes. Blood 99, 1044-1052.
18. Werz, O., Steinhilber, D. (1996) Selenium-dependent peroxidases suppress 5-lipoxygenase activity in B-lymphocytes and immature myeloid cells - the presence of peroxidase-insensitive 5-lipoxygenase activity in differentiated myeloid cells. Eur. J. Biochem. 242, 90-97.
19. Werz, O., Klemm, J., Samuelsson, B., Rådmark, O. (2001) Phorbol ester up-regulates capacities for nuclear translocation and phosphorylation of 5-lipoxygenase in Mono Mac 6 cells and human polymorphonuclear leukocytes. Blood 97, 2487-2495.
20. McDermott, M., Wakelam, M. J., Morris, A. J. (2004) Phospholipase D. Biochem. Cell Biol. 82, 225-253.
21. Morris, A. J., Frohman, M. A., Engebrecht, J. (1997) Measurement of phospholipase D activity. Anal. Biochem. 252, 1-9.
22. Borgeat, P., Samuelsson, B. (1979) Arachidonic acid metabolism in polymorphonuclear leukocytes: effects of ionophore A23187. Proc. Natl. Acad. Sci. USA 76, 2148-2152.
23. Wong, A., Cook, M. N., Foley, J. J., Sarau, H. M., Marshall, P., Hwang, S. M. (1991) Influx of extracellular calcium is required for the membrane translocation of 5-lipoxygenase and leukotriene synthesis. Biochemistry 30, 9346-9354.
24. Pappu, A. S., Hauser, G. (1983) Propranolol-induced inhibition of rat brain cytoplasmic phosphatidate phosphohydrolase. Neurochem. Res. 8, 1565-1575.
25. Balsinde, J., Dennis, E. A. (1996) Bromoenol lactone inhibits magnesium-dependent phosphatidate phosphohydrolase and blocks triacylglycerol biosynthesis in mouse P388D1 macrophages. J. Biol. Chem. 271, 31937-31941.
26. Luo, M., Jones, S. M., Peters-Golden, M., Brock, T. G. (2003) Nuclear localization of 5-lipoxygenase as a determinant of leukotriene B4 synthetic capacity. Proc. Natl. Acad. Sci. USA 100, 12165-12170.
27. Bleasdale, J. E., Thakur, N. R., Gremban, R. S., Bundy, G. L., Fitzpatrick, F. A., Smith, R. J., Bunting, S. (1990) Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255, 756-768.
28. Feisst, C., Albert, D., Steinhilber, D., Werz, O. (2005) The aminosteroid phospholipase C antagonist U-73122 (1-[6-[[17-β-3-methoxyestra-1,3,5(10)- trien-17-yl]amino]hexyl]-1H-pyrro le-2,5-dione) potently inhibits human 5-lipoxygenase in vivo and in vitro. Mol. Pharmacol. 67, 1751-1757.
29. Muller-Decker, K. (1989) Interruption of TPA-induced signals by an antiviral and antitumoral xanthate compound: inhibition of a phospholipase C-type reaction. Biochem. Biophys. Res. Commun. 162, 198-205.
30. Schutze, S., Potthoff, K., Machleidt, T., Berkovic, D., Wiegmann, K., Kronke, M. (1992) TNF activates NF-κ B by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell 71, 765-776.
31. Rider, L. G., Niedel, J. E. (1987) Diacylglycerol accumulation and superoxide anion production in stimulated human neutrophils. J. Biol. Chem. 262, 5603-5608.
32. Fensome, A., Whatmore, J., Morgan, C., Jones, D., Cockcroft, S. (1998) ADP-ribosylation factor and Rho proteins mediate fMLP-dependent activation of phospholipase D in human neutrophils. J. Biol. Chem. 273, 13157-13164.
33. Mullmann, T. J., Siegel, M. I., Egan, R. W., Billah, M. M. (1990) Complement C5a activation of phospholipase D in human neutrophils. A major route to the production of phosphatidates and diglycerides. J. Immunol. 144, 1901-1908.
34. Kanaho, Y., Kanoh, H., Saitoh, K., Nozawa, Y. (1991) Phospholipase D activation by platelet-activating factor, leukotriene B4, and formyl-methionyl-leucyl-phenylalanine in rabbit neutrophils. Phospholipase D activation is involved in enzyme release. J. Immunol. 146, 3536-3541.
35. Denys, A., Aires, V., Hichami, A., Khan, N. A. (2004) Thapsigargin-stimulated MAP kinase phosphorylation via CRAC channels and PLD activation: inhibitory action of docosahexaenoic acid. FEBS Lett. 564, 177-182.
36. Gelas, P., Ribbes, G., Record, M., Terce, F., Chap, H. (1989) Differential activation by fMet-Leu-Phe and phorbol ester of a plasma membrane phosphatidylcholine-specific phospholipase D in human neutrophil. FEBS Lett. 251, 213-218.
37. Park, M. A., Lee, M. J., Lee, S. H., Jung, D. K., Kwak, J. Y. (2002) Anti-apoptotic role of phospholipase D in spontaneous and delayed apoptosis of human neutrophils. FEBS Lett. 519, 45-49.
38. Randall, R. W., Bonser, R. W., Thompson, N. T., Garland, L. G. (1990) A novel and sensitive assay for phospholipase D in intact cells. FEBS Lett. 264, 87-90.
39. Bechoua, S., Daniel, L. W. (2001) Phospholipase D is required in the signaling pathway leading to p38 MAPK activation in neutrophil-like HL-60 cells, stimulated by N-formyl-methionyl-leucyl-phenylalanine. J. Biol. Chem. 276, 31752-31759.
40. Lin, P. Y., Wiggan, G. A., Gilfillan, A. M. (1991) Activation of phospholipase D in a rat mast (RBL 2H3) cell line. A possible unifying mechanism for IgE-dependent degranulation and arachidonic acid metabolite release. J. Immunol. 146, 1609-1616.
41. Lin, P. Y., Wiggan, G. A., Welton, A. F., Gilfillan, A. M. (1991) Differential effects of propranolol on the IgE-dependent, or calcium ionophore-stimulated, phosphoinositide hydrolysis and calcium mobilization in a mast (RBL 2H3) cell line. Biochem. Pharmacol. 41, 1941-1948.
42. Hazen, S. L., Zupan, L. A., Weiss, R. H., Getman, D. P., Gross, R. W. (1991) Suicide inhibition of canine myocardial cytosolic calcium-independent phospholipase A2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2. J. Biol. Chem. 266, 7227-7232.
43. Ackermann, E. J., Conde-Frieboes, K., Dennis, E. A. (1995) Inhibition of macrophage Ca(2+)-independent phospholipase A2 by bromoenol lactone and trifluoromethyl ketones. J. Biol. Chem. 270, 445-450.
44. Brock, T. G. (2005) Regulating leukotriene synthesis: the role of nuclear 5-lipoxygenase. J. Cell. Biochem. 96, 1203-1211.
45. Rådmark, O., Samuelsson, B. (2005) Regulation of 5-lipoxygenase enzyme activity. Biochem. Biophys. Res. Commun. 338, 102-110.
46. Kulkarni, S., Das, S., Funk, C. D., Murray, D., Cho, W. (2002) Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J. Biol. Chem. 277, 13167-13174.
47. Pande, A. H., Moe, D., Nemec, K. N., Qin, S., Tan, S., Tatulian, S. A. (2004) Modulation of human 5-lipoxygenase activity by membrane lipids. Biochemistry 43, 14653-14666.
48. Pande, A. H., Qin, S., Tatulian, S. A. (2005) Membrane fluidity is a key modulator of membrane binding, insertion, and activity of 5-lipoxygenase. Biophys. J. 88, 4084-4094.
49. Jose Lopez-Andreo, M., Gomez-Fernandez, J. C., Corbalan-Garcia, S. (2003) The simultaneous production of phosphatidic acid and diacylglycerol is essential for the translocation of protein kinase Cε to the plasma membrane in RBL-2H3 cells. Mol. Biol. Cell 14, 4885-4895.
50. Medkova, M., Cho, W. (1999) Interplay of C1 and C2 domains of protein kinase C-α in its membrane binding and activation. J. Biol. Chem. 274, 19852-19861.
51. Werz, O., Burkert, E., Fischer, L., Szellas, D., Dishart, D., Samuelsson, B., Rådmark, O., Steinhilber, D. (2002) Extracellular signal-regulated kinases phosphorylate 5-lipoxygenase and stimulate 5-lipoxygenase product formation in leukocytes. FASEB J. 16, 1441-1443.