Hyperforin induces Ca2+-independent arachidonic acid release in human platelets by facilitating cytosolic phospholipase A2 activation through select phospholipid interactions

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1801, Issue 4, 2010, Pages 462-472

  Hoffmann, Marika ^a   Lopez, Jakob J ^a   Pergola, Carlo ^b   Feisst, Christian ^a   Pawelczik, Sven ^c   Jakobsson, Per Johan ^c   Sorg, Bernd L ^a   Glaubitz, Clemens ^a   Steinhilber, Dieter ^a   Werz, Oliver ^b  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Arachidonic acid; Calcium; Hyperforin; Phospholipases A2; Phosphorylation; Platelets

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ARACHIDONIC ACID; CALCIUM; EDETIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; HYPERFORIN; LIPID; LIPOSOME; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; PHOSPHOLIPID;

ARTICLE; CALCIUM CELL LEVEL; CELL FREE SYSTEM; DRUG MECHANISM; HUMAN; HUMAN EXPERIMENT; HYDROLYSIS; LIPID MEMBRANE; MOLECULAR INTERACTION; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTON NUCLEAR MAGNETIC RESONANCE; THROMBOCYTE;

ARACHIDONIC ACID; BICYCLO COMPOUNDS; BLOOD PLATELETS; CALCIUM; CYTOSOL; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; IMIDAZOLES; MAGNETIC RESONANCE SPECTROSCOPY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHLOROGLUCINOL; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASES A2; PHOSPHORYLATION; PYRIDINES; TERPENES;

EID: 76649142718     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.12.007     Document Type: Article

References (56)

1. Ghosh M., Tucker D.E., Burchett S.A., and Leslie C.C. Properties of the group IV phospholipase A2 family. Prog. Lipid Res. 45 (2006) 487-510
2. Hirabayashi T., Murayama T., and Shimizu T. Regulatory mechanism and physiological role of cytosolic phospholipase A2. Biol. Pharm. Bull. 27 (2004) 1168-1173
3. Dogne J.M., Hanson J., and Pratico D. Thromboxane, prostacyclin and isoprostanes: therapeutic targets in atherogenesis. Trends Pharmacol. Sci. 26 (2005) 639-644
4. Yoshimoto T., and Takahashi Y. Arachidonate 12-lipoxygenases. Prostaglandins Other Lipid Mediat. 68-69 (2002) 245-262
5. Nalefski E.A., Sultzman L.A., Martin D.M., Kriz R.W., Towler P.S., Knopf J.L., and Clark J.D. Delineation of two functionally distinct domains of cytosolic phospholipase A2, a regulatory Ca(2+)-dependent lipid-binding domain and a Ca(2+)-independent catalytic domain. J. Biol. Chem. 269 (1994) 18239-18249
6. Perisic O., Fong S., Lynch D.E., Bycroft M., and Williams R.L. Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J. Biol. Chem. 273 (1998) 1596-1604
7. Kramer R.M., Roberts E.F., Um S.L., Borsch-Haubold A.G., Watson S.P., Fisher M.J., and Jakubowski J.A. p38 mitogen-activated protein kinase phosphorylates cytosolic phospholipase A2 (cPLA2) in thrombin-stimulated platelets. Evidence that proline-directed phosphorylation is not required for mobilization of arachidonic acid by cPLA2. J. Biol. Chem. 271 (1996) 27723-27729
8. Borsch-Haubold A.G., Kramer R.M., and Watson S.P. Inhibition of mitogen-activated protein kinase kinase does not impair primary activation of human platelets. Biochem. J. 318 Pt 1 (1996) 207-212
9. Hefner Y., Borsch-Haubold A.G., Murakami M., Wilde J.I., Pasquet S., Schieltz D., Ghomashchi F., Yates III J.R., Armstrong C.G., Paterson A., Cohen P., Fukunaga R., Hunter T., Kudo I., Watson S.P., and Gelb M.H. Serine 727 phosphorylation and activation of cytosolic phospholipase A2 by MNK1-related protein kinases. J. Biol. Chem. 275 (2000) 37542-37551
10. Muthalif M.M., Benter I.F., Uddin M.R., and Malik K.U. Calcium/calmodulin-dependent protein kinase IIalpha mediates activation of mitogen-activated protein kinase and cytosolic phospholipase A2 in norepinephrine-induced arachidonic acid release in rabbit aortic smooth muscle cells. J. Biol. Chem. 271 (1996) 30149-30157
11. Muthalif M.M., Hefner Y., Canaan S., Harper J., Zhou H., Parmentier J.H., Aebersold R., Gelb M.H., and Malik K.U. Functional interaction of calcium-/calmodulin-dependent protein kinase II and cytosolic phospholipase A(2). J. Biol. Chem. 276 (2001) 39653-39660
12. Shimizu M., Nakamura H., Hirabayashi T., Suganami A., Tamura Y., and Murayama T. Ser515 phosphorylation-independent regulation of cytosolic phospholipase A(2)alpha (cPLA(2)alpha) by calmodulin-dependent protein kinase: possible interaction with catalytic domain A of cPLA(2)alpha. Cell Signal. 20 (2008) 815-824
13. Qiu Z.H., Gijon M.A., de Carvalho M.S., Spencer D.M., and Leslie C.C. The role of calcium and phosphorylation of cytosolic phospholipase A2 in regulating arachidonic acid release in macrophages. J. Biol. Chem. 273 (1998) 8203-8211
14. Mosior M., Six D.A., and Dennis E.A. Group IV cytosolic phospholipase A2 binds with high affinity and specificity to phosphatidylinositol 4, 5-bisphosphate resulting in dramatic increases in activity. J. Biol. Chem. 273 (1998) 2184-2191
15. Huwiler A., Johansen B., Skarstad A., and Pfeilschifter J. Ceramide binds to the CaLB domain of cytosolic phospholipase A2 and facilitates its membrane docking and arachidonic acid release. FASEB J. 15 (2001) 7-9
16. Pettus B.J., Bielawska A., Subramanian P., Wijesinghe D.S., Maceyka M., Leslie C.C., Evans J.H., Freiberg J., Roddy P., Hannun Y.A., and Chalfant C.E. Ceramide 1-phosphate is a direct activator of cytosolic phospholipase A2. J. Biol. Chem. 279 (2004) 11320-11326
17. Nakamura H., Hirabayashi T., Someya A., Shimizu M., and Murayama T. Inhibition of arachidonic acid release and cytosolic phospholipase A2 alpha activity by D-erythro-sphingosine. Eur. J. Pharmacol. 484 (2004) 9-17
18. Klapisz E., Masliah J., Bereziat G., Wolf C., and Koumanov K.S. Sphingolipids and cholesterol modulate membrane susceptibility to cytosolic phospholipase A(2). J. Lipid Res. 41 (2000) 1680-1688
19. Medina M.A., Martinez-Poveda B., Amores-Sanchez M.I., and Quesada A.R. Hyperforin: more than an antidepressant bioactive compound?. Life Sci. 79 (2006) 105-111
20. Beerhues L. Hyperforin. Phytochemistry 67 (2006) 2201-2207
21. Albert D., Zundorf I., Dingermann T., Muller W.E., Steinhilber D., and Werz O. Hyperforin is a dual inhibitor of cyclooxygenase-1 and 5-lipoxygenase. Biochem. Pharmacol. 64 (2002) 1767-1775
22. Feisst C., Pergola C., Rakonjac M., Rossi A., Koeberle A., Dodt G., Hoffmann M., Hoernig C., Fischer L., Steinhilber D., Franke L., Schneider G., Radmark O., Sautebin L., and Werz O. Hyperforin is a novel type of 5-lipoxygenase inhibitor with high efficacy in vivo. Cell. Mol. Life Sci. 66 (2009) 2759-2771
23. Radmark O., Werz O., Steinhilber D., and Samuelsson B. 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32 (2007) 332-341
24. Kulkarni S., Das S., Funk C.D., Murray D., and Cho W. Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J. Biol. Chem. 277 (2002) 13167-13174
25. Grynkiewicz G., Poenie M., and Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 (1985) 3440-3450
26. Huster D., Arnold K., and G.K. Investigation of lipid organization in biological membranes by two-dimensional nuclear overhauser enhancement spectroscopy. J Phys Chem B 103 (1999) 243-251
27. Seno K., Okuno T., Nishi K., Murakami Y., Watanabe F., Matsuura T., Wada M., Fujii Y., Yamada M., Ogawa T., Okada T., Hashizume H., Kii M., Hara S., Hagishita S., Nakamoto S., Yamada K., Chikazawa Y., Ueno M., Teshirogi I., Ono T., and Ohtani M. Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J Med Chem 43 (2000) 1041-1044
28. Purdon A.D., and Smith J.B. Turnover of arachidonic acid in the major diacyl and ether phospholipids of human platelets. J. Biol. Chem. 260 (1985) 12700-12704
29. Purdon A.D., Patelunas D., and Smith J.B. Evidence for the release of arachidonic acid through the selective action of phospholipase A2 in thrombin-stimulated human platelets. Biochim. Biophys. Acta 920 (1987) 205-214
30. Kramer R.M., Jakubowski J.A., Vaillancourt R., and Deykin D. Effect of membrane cholesterol on phospholipid metabolism in thrombin-stimulated platelets. Enhanced activation of platelet phospholipase(s) for liberation of arachidonic acid. J. Biol. Chem. 257 (1982) 6844-6849
31. Adam P., Arigoni D., Bacher A., and Eisenreich W. Biosynthesis of hyperforin in Hypericum perforatum. J. Med. Chem. 45 (2002) 4786-4793
32. Yau W.-M., and Gawrisch K. Lateral lipid diffusion dominates NOESY cross-relaxation in membranes. J Am Chem Soc 122 (2000) 3971-3972
33. Channon J.Y., and Leslie C.C. A calcium-dependent mechanism for associating a soluble arachidonoyl-hydrolyzing phospholipase A2 with membrane in the macrophage cell line RAW 264.7. J. Biol. Chem. 265 (1990) 5409-5413
34. Evans J.H., Spencer D.M., Zweifach A., and Leslie C.C. Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276 (2001) 30150-30160
35. Shinohara H., Balboa M.A., Johnson C.A., Balsinde J., and Dennis E.A. Regulation of delayed prostaglandin production in activated P388D1 macrophages by group IV cytosolic and group V secretory phospholipase A2s. J. Biol. Chem. 274 (1999) 12263-12268
36. Gijon M.A., Spencer D.M., Siddiqi A.R., Bonventre J.V., and Leslie C.C. Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that Do and Do not mobilize calcium. Novel role of mitogen-activated protein kinase pathways in cytosolic phospholipase A2 regulation. J. Biol. Chem. 275 (2000) 20146-20156
37. Evans J.H., and Leslie C.C. The cytosolic phospholipase A2 catalytic domain modulates association and residence time at Golgi membranes. J. Biol. Chem. 279 (2004) 6005-6016
38. Lehr M., and Griessbach K. Involvement of different protein kinases and phospholipases A2 in phorbol ester (TPA)-induced arachidonic acid liberation in bovine platelets. Mediators Inflamm. 9 (2000) 31-34
39. Beckett C.S., Kell P.J., Creer M.H., and McHowat J. Phospholipase A2-catalyzed hydrolysis of plasmalogen phospholipids in thrombin-stimulated human platelets. Thromb. Res. 120 (2007) 259-268
40. Six D.A., and Dennis E.A. Essential Ca(2+)-independent role of the group IVA cytosolic phospholipase A(2) C2 domain for interfacial activity. J. Biol. Chem. 278 (2003) 23842-23850
41. Casas J., Gijon M.A., Vigo A.G., Crespo M.S., Balsinde J., and Balboa M.A. Phosphatidylinositol 4, 5-bisphosphate anchors cytosolic group IVA phospholipase A2 to perinuclear membranes and decreases its calcium requirement for translocation in live cells. Mol. Biol. Cell 17 (2006) 155-162
42. Leslie C.C., and Channon J.Y. Anionic phospholipids stimulate an arachidonoyl-hydrolyzing phospholipase A2 from macrophages and reduce the calcium requirement for activity. Biochim. Biophys. Acta 1045 (1990) 261-270
43. Hixon M.S., Ball A., and Gelb M.H. Calcium-dependent and -independent interfacial binding and catalysis of cytosolic group IV phospholipase A2. Biochemistry 37 (1998) 8516-8526
44. Shattil S.J., Anaya-Galindo R., Bennett J., Colman R.W., and Cooper R.A. Platelet hypersensitivity induced by cholesterol incorporation. J. Clin. Invest. 55 (1975) 636-643
45. Brown R.E. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 111 Pt 1 (1998) 1-9
46. Mishra S., and Joshi P.G. Lipid raft heterogeneity: an enigma. J Neurochem 103 Suppl 1 (2007) 135-142
47. Bate C., Tayebi M., and Williams A. Sequestration of free cholesterol in cell membranes by prions correlates with cytoplasmic phospholipase A2 activation. BMC Biol. 6 (2008) 8
48. Graziani A., Bricko V., Carmignani M., Graier W.F., and Groschner K. Cholesterol- and caveolin-rich membrane domains are essential for phospholipase A2-dependent EDHF formation. Cardiovasc. Res. 64 (2004) 234-242
49. Grimmer S., Ying M., Walchli S., van Deurs B., and Sandvig K. Golgi vesiculation induced by cholesterol occurs by a dynamin- and cPLA2-dependent mechanism. Traffic 6 (2005) 144-156
50. Chap H., Perret B., Mauco G., Simon M.F., and Douste-Blazy L. Organization and role of platelet membrane phospholipids as studied with purified phospholipases. Agents Actions 9 (1979) 400-406
51. Verkleij A.J., and Post J.A. Membrane phospholipid asymmetry and signal transduction. J. Membr. Biol. 178 (2000) 1-10
52. Oruch R., Pryme I.F., and Holmsen H. Effects of psychotropic drugs on the thrombin-induced liberation of arachidonate in human platelets. Saudi Med. J. 29 (2008) 1397-1407
53. Roz N., and Rehavi M. Hyperforin inhibits vesicular uptake of monoamines by dissipating pH gradient across synaptic vesicle membrane. Life Sci. 73 (2003) 461-470
54. Schempp C.M., Kirkin V., Simon-Haarhaus B., Kersten A., Kiss J., Termeer C.C., Gilb B., Kaufmann T., Borner C., Sleeman J.P., and Simon J.C. Inhibition of tumour cell growth by hyperforin, a novel anticancer drug from St. John's wort that acts by induction of apoptosis. Oncogene 21 (2002) 1242-1250
55. Eckert G.P., and Muller W.E. Effects of hyperforin on the fluidity of brain membranes. Pharmacopsychiatry 34 Suppl 1 (2001) S22-25
56. Eckert G.P., Keller J.H., Jourdan C., Karas M., Volmer D.A., Schubert-Zsilavecz M., and Muller W.E. Hyperforin modifies neuronal membrane properties in vivo. Neurosci Lett 367 (2004) 139-143