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PMID: 8363562 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Ca2+ release from platelet intracellular stores by thapsigargin and 2,5-di-(t-butyl)-1,4-benzohydroquinone: relationship to Ca2+ pools and relevance in platelet activation.

The Biochemical journal ·Vol. 294 ( Pt 1) ·1993-08-15 ·Pages 119-26

Authi KS, Bokkala S, Patel Y, Kakkar VV, Munkonge F

Abstract

The effects of the Ca(2+)-ATPase inhibitors thapsigargin (Tg) and 2,5-di-(t-butyl)-1,4-benzohydroquinone (tBuBHQ) were examined by using Ca(2+)-regulatory systems of platelet mixed membranes, saponin-permeabilized and intact platelets. Both agents inhibit Ca(2+)-ATPase activities of platelet mixed membranes, without any effect on the basal Mg(2+)-ATPase activity. Tg is more effective (EC50 = 35 nM) than tBuBHQ (EC50 = 580 nM). The effect of the two inhibitors on 45Ca2+ release from saponin-permeabilized platelets has also been characterized. 45Ca2+ uptake into non-mitochondrial intracellular stores occurs via an ATP-dependent mechanism, and if added at equilibrium the second messenger Ins(1,4,5)P3 releases 50% of the accumulated 45Ca2+. Maximally effective concentrations of Tg (1 microM) and tBuBHQ (50 microM) release 77% and 68% of the accumulated 45Ca2+. Addition of Ins(1,4,5)P3 together with either Tg or tBuBHQ resulted in a non-additive release which was the same as with either Tg or tBuBHQ alone, indicating that the Ins(1,4,5)P3-sensitive Ca2+ pool was a subset of the pool that is sensitive to the Ca(2+)-ATPase inhibitors. Release of 45Ca2+ by either Tg or tBuBHQ was not affected by heparin, which totally blocked Ins(1,4,5)P3-induced Ca2+ release, and Tg was found not to affect [32P]Ins(1,4,5)P3 binding to its receptor on mixed membranes. Thus both Tg and tBuBHQ release Ca2+ from a pool that totally overlaps the Ins(1,4,5)P3-sensitive pool without affecting Ins(1,4,5)P3 function. In intact indomethacin-treated Fura 2-loaded platelets, Tg and tBuBHQ cause Ca2+ elevation, arising from release from intracellular stores and influx from the outside. Both Tg and tBuBHQ elevated Ca2+ to similar levels, which were less and slower than those observed with thrombin. Addition of thrombin to cells already treated with Tg or tBuBHQ produced further elevation of Ca2+, indicating agonist utilization of a Ca(2+)-ATPase inhibitor-insensitive pool. In aggregation experiments Tg and tBuBHQ showed different functional effects. In indomethacin-treated cells Tg induces slow aggregation and secretion responses, whereas tBuBHQ only induces shape change. Both agents show synergistic secretory responses with the protein kinase C activator dioctanoylglycerol (DiC8). Tg also showed greater ability than tBuBHQ to release [3H]arachidonic acid (AA) from [3H]AA-labelled platelets. Additionally, in [32P]Pi-labelled platelets both Tg and tBuBHQ induced phosphorylation of myosin light chain, a 27 kDa protein and the 45 kDa protein pleckstrin, but Tg showed a greater ability than tBuBHQ to cause phosphorylation of pleckstrin. These studies indicate that Tg and tBuBHQ are effective in releasing the Ins(1,4,5)P3-sensitive Ca2+ pool in platelets.(ABSTRACT TRUNCATED AT 400 WORDS)

MeSH Terms
Binding Sites Blood Platelets/drug effects,metabolism Calcium/metabolism Calcium-Transporting ATPases/antagonists & inhibitors,metabolism Cells, Cultured Humans Hydroquinones/pharmacology In Vitro Techniques Inositol 1,4,5-Trisphosphate/metabolism Platelet Activation Saponins Terpenes/pharmacology Thapsigargin
Chemicals
Hydroquinones Saponins Terpenes 2,5-di-tert-butylhydroquinone Thapsigargin Inositol 1,4,5-Trisphosphate Calcium-Transporting ATPases Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Authi K S
Platelet Section, Thrombosis Research Institute, Chelsea, London, U.K.
Bokkala S
Patel Y
Kakkar V V
Munkonge F
References (48)
48 references, click to expand
  1. Interaction of membrane systems in blood platelets.
    Am J Pathol. 1972 Feb;66(2):295-312 PMID: 5009975
  2. Drug action of thapsigargin on the Ca2+ pump protein of sarcoplasmic reticulum.
    J Biol Chem. 1991 Dec 5;266(34):22912-8 PMID: 1835973
  3. A conformational mechanism for formation of a dead-end complex by the sarcoplasmic reticulum ATPase with thapsigargin.
    J Biol Chem. 1992 Jan 15;267(2):1286-92 PMID: 1530936
  4. Localisation of the [32P]IP3 binding site on human platelet intracellular membranes isolated by high-voltage free-flow electrophoresis.
    FEBS Lett. 1992 Feb 24;298(2-3):173-6 PMID: 1544439
  5. Localization of cyclo-oxygenase and thromboxane synthetase in human platelet intracellular membranes.
    Biochem J. 1982 Jun 15;204(3):847-51 PMID: 6812567
  6. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate.
    Nature. 1983 Nov 3-9;306(5938):67-9 PMID: 6605482
  7. Inhibition of calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles.
    J Biol Chem. 1984 Jun 25;259(12):7547-53 PMID: 6736019
  8. Characterization of the calcium-sequestering process associated with human platelet intracellular membranes isolated by free-flow electrophoresis.
    Biochem J. 1984 Sep 1;222(2):413-7 PMID: 6433901
  9. Diacylglycerol lipase activity in human platelet intracellular and surface membranes. Some kinetic properties and fatty acid specificity.
    FEBS Lett. 1985 Jan 21;180(1):95-101 PMID: 3917938
  10. Inositol 1,4,5-trisphosphate releases Ca2+ from a Ca2+-transporting membrane vesicle fraction derived from human platelets.
    J Biol Chem. 1985 Jan 25;260(2):956-62 PMID: 2981853
  11. Exogenous sn-1,2-diacylglycerols containing saturated fatty acids function as bioregulators of protein kinase C in human platelets.
    J Biol Chem. 1985 Feb 10;260(3):1358-61 PMID: 3155733
  12. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  13. Inositol triphosphate-induced Ca2+ release from human platelet membranes.
    Biochem Biophys Res Commun. 1985 May 16;128(3):1274-80 PMID: 3159385
  14. Inositol 1,4,5-trisphosphate-induced release of sequestered Ca2+ from highly purified human platelet intracellular membranes.
    Biochem J. 1985 Aug 15;230(1):247-53 PMID: 3931630
  15. Studies on the bivalent-cation-activated ATPase activities of highly purified human platelet surface and intracellular membranes.
    Biochem J. 1986 Feb 1;233(3):661-8 PMID: 2939826
  16. Metabolic and functional consequences of introducing inositol 1,4,5-trisphosphate into saponin-permeabilized human platelets.
    Biochem J. 1986 Feb 1;233(3):707-18 PMID: 2939827
  17. The inflammatory and tumor-promoting sesquiterpene lactone, thapsigargin, activates platelets by selective mobilization of calcium as shown by protein phosphorylations.
    Biochim Biophys Acta. 1987 Jan 19;927(1):65-73 PMID: 3098302
  18. The calcium mobilizing tumor promoting agent, thapsigargin elevates the platelet cytoplasmic free calcium concentration to a higher steady state level. A possible mechanism of action for the tumor promotion.
    Biochem Biophys Res Commun. 1987 Feb 13;142(3):654-60 PMID: 2950855
  19. Inositol 1,4,5-trisphosphate and 5'-GTP induce calcium release from different intracellular pools.
    FEBS Lett. 1987 Jun 22;218(1):153-8 PMID: 3496244
  20. Solubilization, purification, and characterization of an inositol trisphosphate receptor.
    J Biol Chem. 1988 Jan 25;263(3):1530-4 PMID: 2826483
  21. "Calciosome," a cytoplasmic organelle: the inositol 1,4,5-trisphosphate-sensitive Ca2+ store of nonmuscle cells?
    Proc Natl Acad Sci U S A. 1988 Feb;85(4):1091-5 PMID: 3257572
  22. Calcium entry into the inositol 1,4,5-trisphosphate-releasable calcium pool is mediated by a GTP-regulatory mechanism.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2499-503 PMID: 3357878
  23. A novel tumour promoter, thapsigargin, transiently increases cytoplasmic free Ca2+ without generation of inositol phosphates in NG115-401L neuronal cells.
    Biochem J. 1988 Jul 1;253(1):81-6 PMID: 3138987
  24. Inositol 1,3,4,5-tetrakisphosphate induces Ca2+ sequestration in rat liver cells.
    Science. 1988 Nov 25;242(4882):1176-8 PMID: 2847317
  25. Introduction of antibody (PL/IM 430) to a 100 kDa protein into permeabilised platelets inhibits intracellular sequestration of Ca2+.
    Biosci Rep. 1988 Aug;8(4):379-88 PMID: 2847821
  26. Action of guanosine 5'-[beta-thio]diphosphate on thrombin-induced activation and Ca2+ mobilization in saponin-permeabilized and intact human platelets.
    Biochem J. 1988 Nov 1;255(3):885-93 PMID: 3063257
  27. Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane.
    J Biol Chem. 1989 Jul 25;264(21):12266-71 PMID: 2663854
  28. GTP-activated communication between distinct inositol 1,4,5-trisphosphate-sensitive and -insensitive calcium pools.
    Nature. 1989 Jul 20;340(6230):236-9 PMID: 2787892
  29. The inositol 1,4,5-trisphosphate-binding site in adrenal cortical cells is distinct from the endoplasmic reticulum.
    J Biol Chem. 1989 Aug 25;264(24):14078-84 PMID: 2547781
  30. 2,5-Di-(tert-butyl)-1,4-benzohydroquinone rapidly elevates cytosolic Ca2+ concentration by mobilizing the inositol 1,4,5-trisphosphate-sensitive Ca2+ pool.
    J Biol Chem. 1989 Sep 15;264(26):15192-8 PMID: 2788653
  31. Inositol phosphates and cell signalling.
    Nature. 1989 Sep 21;341(6239):197-205 PMID: 2550825
  32. Distribution of two distinct Ca2+-ATPase-like proteins and their relationships to the agonist-sensitive calcium store in adrenal chromaffin cells.
    Nature. 1989 Nov 2;342(6245):72-4 PMID: 2530452
  33. Role of Ca2(+)-ATPases in regulation of cellular Ca2+ signalling, as studied with the selective microsomal Ca2(+)-ATPase inhibitor, thapsigargin.
    Agents Actions. 1990 Jan;29(1-2):8-15 PMID: 2139301
  34. Inositol 1,3,4,5-tetrakisphosphate stimulates calcium release from bovine adrenal microsomes by a mechanism independent of the inositol 1,4,5-trisphosphate receptor.
    Biochem J. 1990 Jun 1;268(2):333-8 PMID: 2163607
  35. Subcellular distribution of the calcium-storing inositol 1,4,5-trisphosphate-sensitive organelle in rat liver. Possible linkage to the plasma membrane through the actin microfilaments.
    Biochem J. 1991 Mar 15;274 ( Pt 3):643-50 PMID: 1849402
  36. Bovine adrenal chromaffin cells contain an inositol 1,4,5-trisphosphate-insensitive but caffeine-sensitive Ca2+ store that can be regulated by intraluminal free Ca2+.
    Biochem J. 1991 May 1;275 ( Pt 3):697-701 PMID: 1645520
  37. Cytoplasmic calcium oscillations: a two pool model.
    Cell Calcium. 1991 Feb-Mar;12(2-3):63-72 PMID: 2059999
  38. Calcium mobilization in human platelets by receptor agonists and calcium-ATPase inhibitors.
    FEBS Lett. 1991 Jun 17;284(1):1-4 PMID: 1647969
  39. Comparison between the effects of the microsomal Ca(2+)-translocase inhibitors thapsigargin and 2,5-di-(t-butyl)-1,4-benzohydroquinone on cellular calcium fluxes.
    Biochem J. 1991 Jul 15;277 ( Pt 2):553-6 PMID: 1830474
  40. Demonstration of two forms of calcium pumps by thapsigargin inhibition and radioimmunoblotting in platelet membrane vesicles.
    J Biol Chem. 1991 Aug 5;266(22):14593-6 PMID: 1830588
  41. Cytosolic and stored calcium antagonistically control tyrosine phosphorylation of specific platelet proteins.
    J Biol Chem. 1991 Sep 5;266(25):16911-6 PMID: 1832159
  42. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps.
    J Biol Chem. 1991 Sep 15;266(26):17067-71 PMID: 1832668
  43. The role of caffeine-sensitive Ca2+ stores in agonist- and inositol 1,4,5-trisphosphate-induced Ca2+ release from bovine adrenal chromaffin cells.
    Biochem J. 1991 Sep 15;278 ( Pt 3):643-50 PMID: 1898353
  44. Different calcium pools in human platelets and their role in thromboxane A2 formation.
    J Biol Chem. 1991 Oct 15;266(29):19232-7 PMID: 1833401
  45. Agonist-sensitive and -insensitive intracellular Ca2+ pools. Separate Ca(2+)-releasing mechanisms revealed by manoalide and benzohydroquinone.
    Biochem J. 1991 Oct 15;279 ( Pt 2):367-75 PMID: 1659378
  46. H+ uptake increases GTP-induced connection of inositol 1,4,5-trisphosphate- and caffeine-sensitive calcium pools in pancreatic microsomal vesicles.
    Biochem Biophys Res Commun. 1991 Oct 31;180(2):755-64 PMID: 1835385
  47. Activation of human platelets by exposure to a monoclonal antibody, PM6/248, to glycoprotein IIb-IIIa.
    Br J Haematol. 1991 Oct;79(2):277-85 PMID: 1958486
  48. Cytochemical localization of adenylate cyclase and of calcium ion, magnesium ion-activated ATPases in the dense tubular system of human blood platelets.
    Biochim Biophys Acta. 1978 Sep 6;542(3):357-71 PMID: 150866
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1993-08-15
Pages
119-26
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1134574
Subset
IM
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