Role of Hydrogen Peroxide in the Neutrophil-mediated Release of Prostacyclin from Cultured Endothelial Cells

Overview

Journal J Clin Invest

Specialty General Medicine

Date 1984 Aug 1

PMID 6378974

Citations 25

Authors

J M Harlan

K S Callahan

Affiliations

Soon will be listed here.

Abstract

We have examined the effect of activated neutrophils on the release of prostacyclin (PGI2) from cultured endothelial cells by radioimmunoassay and thin layer chromatography of its stable metabolite, 6-keto-prostaglandin F1 alpha (6-keto-PGF1 alpha). Phorbol myristate acetate-activated neutrophils induced a time- and dose-dependent release of 6-keto-PGF1 alpha from human and bovine endothelial cell monolayers, whereas phorbol myristate acetate alone and neutrophils alone did not. Pretreatment of the endothelial cells with aspirin prevented neutrophil-mediated 6-keto-PGF1 alpha release, indicating that it did not depend upon neutrophil-generated endoperoxides. Phorbol myristate acetate-activated neutrophils from a patient with chronic granulomatous disease failed to induce endothelial 6-keto-PGF1 alpha release. Addition of catalase but not of superoxide dismutase significantly reduced human and bovine endothelial 6-keto-PGF1 alpha release by phorbol myristate acetate-activated neutrophils. Catalase-inhibitable endothelial 6-keto-PGF1 alpha release was also observed after the addition of the hydrogen peroxide-generating system, glucose-glucose oxidase, to bovine and human endothelial cell monolayers. Bovine endothelial 6-keto-PGF1 alpha release induced by exogenously generated hydrogen peroxide was attenuated by the phospholipase inhibitor mepacrine, suggesting that hydrogen peroxide may act by triggering endothelial membrane phospholipase activation. The release of 6-keto-PGF1 alpha by enzymatically or neutrophil-generated hydrogen peroxide was not associated with endothelial cell lysis as assessed by 51Cr release. We conclude that exogenously generated hydrogen peroxide or a hydrogen peroxide-derived product mediates rapid nonlytic release of PGI2 from cultured endothelial cells.

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References

Gorman R, Bunting S, MILLER O . Modulation of human platelet adenylate cyclase by prostacyclin (PGX). Prostaglandins. 1977; 13(3):377-88. DOI: 10.1016/0090-6980(77)90018-1. View

Egan R, Paxton J, KUEHL Jr F . Mechanism for irreversible self-deactivation of prostaglandin synthetase. J Biol Chem. 1976; 251(23):7329-35. View

Wright D, Bralove D, Gallin J . The differential mobilization of human neutrophil granules. Effects of phorbol myristate acetate and ionophore A23187. Am J Pathol. 1977; 87(2):273-84. PMC: 2032029. View

Weksler B, Marcus A, Jaffe E . Synthesis of prostaglandin I2 (prostacyclin) by cultured human and bovine endothelial cells. Proc Natl Acad Sci U S A. 1977; 74(9):3922-6. PMC: 431786. DOI: 10.1073/pnas.74.9.3922. View

Williams T, Peck M . Role of prostaglandin-mediated vasodilatation in inflammation. Nature. 1977; 270(5637):530-2. DOI: 10.1038/270530a0. View

Sacks T, MOLDOW C, Craddock P, Bowers T, JACOB H . Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes. An in vitro model of immune vascular damage. J Clin Invest. 1978; 61(5):1161-7. PMC: 372636. DOI: 10.1172/JCI109031. View

Wall R, Harker L, Quadracci L, Striker G . Factors influencing endothelial cell proliferation in vitro. J Cell Physiol. 1978; 96(2):203-13. DOI: 10.1002/jcp.1040960209. View

Komoriya K, Ohmori H, Azuma A, Kurozumi S, Hashimoto Y, Nicolaou K . Prostaglandin I2 as a potentiator of acute inflammation in rats. Prostaglandins. 1978; 15(4):557-64. DOI: 10.1016/0090-6980(78)90052-7. View

Higgs E, Moncada S, Vane J . Inflammatory effects of prostacyclin (PGI2) and 6-oxo-PGF1alpha in the rat paw. Prostaglandins. 1978; 16(2):153-62. DOI: 10.1016/0090-6980(78)90018-7. View

10.

Ford-Hutchinson A, Walker J, Davidson E, Smith M . PGI2: a potential mediator of inflammation. Prostaglandins. 1978; 16(2):253-8. DOI: 10.1016/0090-6980(78)90027-8. View

11.

Weksler B, Ley C, Jaffe E . Stimulation of endothelial cell prostacyclin production by thrombin, trypsin, and the ionophore A 23187. J Clin Invest. 1978; 62(5):923-30. PMC: 371849. DOI: 10.1172/JCI109220. View

12.

Schwartz S . Selection and characterization of bovine aortic endothelial cells. In Vitro. 1978; 14(12):966-80. DOI: 10.1007/BF02616210. View

13.

Weiss S, Turk J, NEEDLEMAN P . A mechanism for the hydroperoxide-mediated inactivation of prostacyclin synthetase. Blood. 1979; 53(6):1191-6. View

14.

Hirata F, CORCORAN B, Venkatasubramanian K, Schiffmann E, Axelrod J . Chemoattractants stimulate degradation of methylated phospholipids and release of arachidonic acid in rabbit leukocytes. Proc Natl Acad Sci U S A. 1979; 76(6):2640-3. PMC: 383663. DOI: 10.1073/pnas.76.6.2640. View

15.

Hemler M, Cook H, Lands W . Prostaglandin biosynthesis can be triggered by lipid peroxides. Arch Biochem Biophys. 1979; 193(2):340-5. DOI: 10.1016/0003-9861(79)90038-9. View

16.

Boxer L, Allen J, Schmidt M, Yoder M, Baehner R . Inhibition of polymorphonuclear leukocyte adherence by prostacyclin. J Lab Clin Med. 1980; 95(5):672-8. View

17.

Hemler M, Lands W . Evidence for a peroxide-initiated free radical mechanism of prostaglandin biosynthesis. J Biol Chem. 1980; 255(13):6253-61. View

18.

Mullane K, Moncada S . Prostacyclin release and the modulation of some vasoactive hormones. Prostaglandins. 1980; 20(1):25-49. DOI: 10.1016/0090-6980(80)90004-0. View

19.

Polgar P, Taylor L . Stimulation of prostaglandin synthesis by ascorbic acid via hydrogen peroxide formation. Prostaglandins. 1980; 19(5):693-700. DOI: 10.1016/0090-6980(80)90168-9. View

20.

Marcus A, Weksler B, Jaffe E, Broekman M . Synthesis of prostacyclin from platelet-derived endoperoxides by cultured human endothelial cells. J Clin Invest. 1980; 66(5):979-86. PMC: 371534. DOI: 10.1172/JCI109967. View