Download PDF
Thromb Haemost 1993; 70(05): 826-833
DOI: 10.1055/s-0038-1649678
Platelets
Schattauer GmbH Stuttgart

Different Roles of Prostaglandins in Thromboembolic Processes in Arterioles and Venules In Vivo

Mirjam G A oude Egbrink
The Departments of Physiology and Biophysics, Cardiovascular Research Institute Maastricht, University of Limburg, Maastricht, The Netherlands
,
Geert-Jan Tangelder
The Departments of Physiology and Biophysics, Cardiovascular Research Institute Maastricht, University of Limburg, Maastricht, The Netherlands
,
Dick W Slaaf
The Departments of Physiology and Biophysics, Cardiovascular Research Institute Maastricht, University of Limburg, Maastricht, The Netherlands
,
Robert S Reneman
The Departments of Physiology and Biophysics, Cardiovascular Research Institute Maastricht, University of Limburg, Maastricht, The Netherlands
› Author Affiliations
Further Information

Publication History

Received 08 January 1993

Accepted after revision 21 June 1993

Publication Date:
05 July 2018 (online)

  PDF Download  Permissions and Reprints

Summary

The involvement of prostaglandins in thromboembolic processes, as induced by wall puncture, was studied in rabbit mesenteric arterioles and venules using intravital videomicroscopy. Inhibition of prostaglandin formation with aspirin (100 mg/kg, i. v.) significantly increased in arterioles duration of embolization (from 91 to 200 s) and number of emboli produced (from 4 to 8.5 per vessel), while rate of embolus production was not influenced. In venules, aspirin only influenced embolization rate (a significant decrease from one embolus/14 s to one/23 s). Specific blockade of TXA2-receptors by sulotroban (30 mg/kg, i. v) only influenced the arteriolar reaction: it significantly decreased embolization duration (from 560 to 218 s) and number of emboli produced (from 23 to 10 emboli per vessel), without affecting embolization rate. These findings indicate that both platelet activating and inhibiting prostaglandins play a more important role in thromboembolism in arterioles than in venules; this suggests a difference in prostaglandin synthetic capacity between arteriolar and venular endothelium.

 

  • References

  • 1 Mustard JF, Packham MA. Factors influencing platelet function: adhesion, release, and aggregation. Pharmacol Rev 1970; 22: 97-187
    PubMedGoogle Scholar
  • 2 Moncada S, Gryglewski R, Bunting S, Vane JR. An enzyme isolated from arteries transforms prostaglandin endoperoxides to an unstable substance that inhibits platelet aggregation. Nature 1976; 263: 663-665
    CrossrefPubMedGoogle Scholar
  • 3 Gryglewski RJ, Bunting S, Moncada S, Flower RJ, Vane JR. Arterial walls are protected against deposition of platelet thrombi by a substance (prostaglandin X) which they make from prostaglandin endoperoxides. Prostaglandins 1976; 12: 685-713
    CrossrefPubMedGoogle Scholar
  • 4 Hamberg M, Svensson J, Samuelsson B. Thromboxanes: a new group of biologically active compounds derived from prostaglandin endoperoxides. Proc Nat Acad Sci USA 1975; 72: 2994-2998
    CrossrefPubMedGoogle Scholar
  • 5 Mehta J, Roberts A. Human vascular tissues produce thromboxane as well as prostacyclin. Am J Physiol 1983; 244: R839-R844
    PubMedGoogle Scholar
  • 6 Yang Z, von SegesserL, Bauer E, Stulz P, Turina M, Lüscher TF. Different activation of the endothelial L-arginine and cyclooxygenase pathway in the human internal mammary artery and saphenous vein. Circ Res 1991; 68: 52-60
    CrossrefPubMedGoogle Scholar
  • 7 Moncada S, Vane JR. Arachidonic acid metabolites and the interactions between platelets and blood-vessel walls. N Engl J Med 1979; 300: 1142-1147
    CrossrefPubMedGoogle Scholar
  • 8 Haslam RJ, McClenaghan MD. Measurement of circulating prostacyclin. Nature 1981; 292: 364-366
    CrossrefPubMedGoogle Scholar
  • 9 Blair IA, Barrow SE, Waddell KA, Lewis PJ, Dollery CT. Prostacyclin is not a circulating hormone in man. Prostaglandins 1982; 23: 579-589
    CrossrefPubMedGoogle Scholar
  • 10 Fitzgerald GA, Catella F, Oates JA. Eicosanoid biosynthesis in human cardiovascular disease. Human Pathol 1987; 18: 248-252
    CrossrefPubMedGoogle Scholar
  • 11 Gerritsen ME. Functional heterogeneity of vascular endothelial cells. Biochem Pharmacol 1987; 36: 2701-2711
    CrossrefPubMedGoogle Scholar
  • 12 Revtyak GE, Johnson AR, Campbell WB. Prostaglandin synthesis in bovine coronary endothelial cells: comparison with other commonly studied endothelial cells. Thromb Res 1987; 48: 671-683
    CrossrefPubMedGoogle Scholar
  • 13 Gerritsen ME, Cheli CD. Arachidonic acid and prostaglandin endoperoxide metabolism in isolated rabbit and coronary microvessels and isolated and cultivated coronary micro vessel endothelial cells. J Clin Invest 1983; 72: 1658-1671
    CrossrefPubMedGoogle Scholar
  • 14 oude EgbrinkMGA, Tangelder GJ, Slaaf DW, Reneman RS. Thromboembolic reaction following wall puncture in arterioles and venules of the rabbit mesentery. Thromb Haemostas 1988; 59: 23-28
    PubMedGoogle Scholar
  • 15 Roth GJ, Stanford N, Majerus PW. Acetylation of prostaglandin synthase by aspirin. Proc Nat Acad Sci USA 1975; 72: 3073-3076
    CrossrefPubMedGoogle Scholar
  • 16 Ellis EF, Wright KF, Jones PS, Richardson DW, Ellis CK. Effect of oral aspirin dose on platelet aggregation and vascular prostacyclin (PGI2) synthesis in humans and rabbits. J Cardiovasc Pharmacol 1980; 2: 387-397
    CrossrefPubMedGoogle Scholar
  • 17 Buchanan MR, Dejana E, Gent M. Enhanced platelet accumulation onto injured carotis arteries in rabbits after aspirin treatment. J Clin Invest 1981; 67: 503-508
    CrossrefPubMedGoogle Scholar
  • 18 Stegmeier K, Pill J, Müller-Beckmann B, Schmidt FH, Witte E-C, Wolff H-P, Patscheke H. The pharmacological profile of the thromboxane A2 antagonist BM 13.177: A new anti-platelet and antithrombotic drug. Thromb Res 1984; 35: 379-395
    CrossrefPubMedGoogle Scholar
  • 19 oude EgbrinkMGA, Tangelder GJ, Slaaf DW, Reneman RS. Effect of blood gases and pH on thromboembolic reactions in rabbit mesenteric microvessels. Eur J Physiol (Pflüigers Arch) 1989; 414: 324-330
    CrossrefPubMedGoogle Scholar
  • 20 Slaaf DW, Alewijnse R, Wayland H. Use of telescopic imaging in intravital microscopy: a simple solution for conventional microscopes. Int J Microcirc Clin Exp 1982; 1: 121-134
    PubMedGoogle Scholar
  • 21 Intaglietta M, Tompkins WR. Microvascular measurements by video image shearing and splitting. Microvasc Res 1973; 5: 309-312
    CrossrefPubMedGoogle Scholar
  • 22 Slaaf DW, Rood JPSM, Tangelder GJ, Jeurens TJM, Alewijnse R, Reneman RS, Arts T. A bidirectional optical (BDO) three-stage prism grating system for on-line measurement of red blood cell velocity in microvessels. Microvasc Res 1981; 22: 110-122
    CrossrefPubMedGoogle Scholar
  • 23 Slaaf DW, Tangelder GJ, Reneman RS, Arts T. Dual sensor model calculations applied to blood cell velocity profiles obtained by direct observation in vivo. Int J Microcirc Clin Exp 1986; 5: 242 (abstr)
    PubMedGoogle Scholar
  • 24 Tangelder GJ, Slaaf DW, Muijtjens AMM, Arts T, oude EgbrinkMGA, Reneman RS. Velocity profiles of blood platelets and red blood cells flowing in arterioles of the rabbit mesentery. Circ Res 1986; 59: 505-514
    CrossrefPubMedGoogle Scholar
  • 25 oude EgbrinkMGA, Tangelder GJ, Slaaf DW, Reneman RS. Influence of platelet-vessel wall interactions on leukocyte rolling in vivo. Circ Res 1992; 70: 355-363
    CrossrefPubMedGoogle Scholar
  • 26 Arfors K-E, Bergqvist D, Bygdeman S, McKenzie FN, Svensjö E. The effect of inhibition of the platelet release reaction on platelet behaviour in vitro and in vivo. Scand J Haematol 1972; 9: 322-332
    PubMedGoogle Scholar
  • 27 Bergqvist D. Haemostatic plug formation in the rabbit mesentery. A methodological study. Upsala J Med Sci 1974; 79: 28-38
    CrossrefPubMedGoogle Scholar
  • 28 Arfors K-E, Arturson G, Bergqvist D, Svensjö E. The effect of inhibition of prostaglandin synthesis on microvascular haemostasis and macromolecular leakage. Thromb Res 1976; 8: 393-402
    PubMedGoogle Scholar
  • 29 Rosenblum WI, El-Sabban F, Ellis EF. Aspirin and indomethacin enhance platelet aggregation in mouse mesenteric arterioles. Am J Physiol 1980; 239: H220-H226
    PubMedGoogle Scholar
  • 30 Gu J-M, Acland RD, Anderson GL, Wyllie F, Barker JH. Poor surgical technique produces more emboli after arterial anastomosis of an island flap. Br J Plast Surg 1991; 44: 126-129
    CrossrefPubMedGoogle Scholar
  • 31 Stockmans F, Deckmyn H, Gruwez J, Vermylen J, Acland R. Continuous quantitative monitoring of mural, platelet-dependent, thrombus kinetics in the crushed rat femoral vein. Thromb Haemostas 1991; 65: 425-431
    PubMedGoogle Scholar
  • 32 Barker JH, Acland RD, Anderson GL, Patel J. Microcirculatory disturbances following the passage of emboli in an experimental free-flap model. Plast Reconstr Surg 1992; 90: 95-102
    CrossrefPubMedGoogle Scholar
  • 33 Kelton JG, Hirsh J, Carter CJ, Buchanan MR. Thrombogenic effect of high-dose aspirin in rabbits. Relationship to inhibition of vessel wall synthesis of prostaglandin I2-like activity. J Clin Invest 1978; 62: 892-895
    CrossrefPubMedGoogle Scholar
  • 34 Kinlough-Rathborne RL, Packham MA, Mustard JF. Synergism between platelet aggregating agents: the role of the arachidonate pathway. Thromb Res 1977; 11: 567-580
    CrossrefPubMedGoogle Scholar
  • 35 oude EgbrinkMGA, Tangelder GJ, Slaaf DW, Weijmer-van VelzenS, Reneman RS. Influence of hypercapnia and hypoxia on rabbit platelet aggregation. Thromb Res 1990; 57: 863-875
    CrossrefPubMedGoogle Scholar
  • 36 Diczfalusy U, Falardeau P, Hammarström S. Conversion of prostaglandin endoperoxides to C17-hydroxy acids catalyzed by human platelet thromboxane synthase. FEBS lett 1977; 84: 271-274
    CrossrefPubMedGoogle Scholar
  • 37 Engels W, Endert J, Kamps M, van derVusse G, van BilsenM, Reneman RS. Extraction and determination of eicosanoids in biological samples by reverse-phase high-performance liquid chromatography. Prog appl Microcirc 1987; 12: 316-321
    PubMedGoogle Scholar
  • 38 Claeys M, Kivits GAA, Christ-Hazelhof E, Nugteren DH. Metabolic profile of linoleic acid in porcine leukocytes through the lipoxygenase pathway. Biochim Biophys Acta 1985; 837: 35-51
    CrossrefPubMedGoogle Scholar
  • 39 Tukey JW. Exploratory Data Analysis. Reading, MA, Addison-Wesley Publishing Company; 1977
    Google Scholar
  • 40 Buchanan MR, Hirsh J. Effect of aspirin and salicylate on platelet-vessel wall interactions in rabbits. Arteriosclerosis 1984; 4: 403-406
    CrossrefPubMedGoogle Scholar
  • 41 Frazer CE, Ritter JM. Recovery of prostacyclin synthesis by rabbit aortic endothelium and other tissues after inhibition by aspirin. Br J Pharmacol 1987; 91: 251-256
    CrossrefPubMedGoogle Scholar
  • 42 Charo IF, Shak S, Karasek MA, Davison PM, Goldstein IM. Prostaglandin I2 is not a major metabolite of arachidonic acid in cultured endothelial cells from human foreskin microvessels. J Clin Invest 1984; 74: 914-919
    CrossrefPubMedGoogle Scholar
  • 43 Ubatuba FB, Moncada S, Vane JR. The effect of prostacyclin (PGI2) on platelet behaviour. Thrombus formation in vivo and bleeding time. Thromb Haemostas 1979; 41: 425-435
    PubMedGoogle Scholar
  • 44 Kinlough-Rathbone RL, Packham MA, Reimers H-J, Cazenave J-P, Mustard JF. Mechanisms of platelet shape change, aggregation, and release induced by collagen, thrombin, or A23. J Lab Clin Med 1977; 90: 707-719
    PubMedGoogle Scholar
  • 45 Kinlough-Rathbone RL, Cazenave J-P, Packham MA, Mustard JF. Effect of inhibitors of the arachidonate pathway on the release of granule contents from rabbit platelets adherent to collagen. Lab Invest 1980; 42: 28-34
    PubMedGoogle Scholar
  • 46 oude EgbrinkMG A, Tangelder GJ, Slaaf DW, Reneman RS. Fluid dynamics and the thromboembolic reaction in mesenteric arterioles and venules. Am J Physiol 1991; 260: H1826-H1833
    PubMedGoogle Scholar
  • 47 Faint RW, Mackie IJ, Machin SJ. Platelet aggregation is inhibited by a nitric oxide-like factor released from human neutrophils in vitro. Br J Haematol 1991; 77: 539-545
    PubMedGoogle Scholar
  • 48 Moncada S, Higgs EA, Vane JR. Human arterial and venous tissues generate prostacyclin (prostaglandin X), a potent inhibitor of platelet aggregation. Lancet 1977; i: 18-20
    PubMedGoogle Scholar
  • 49 Villa S, de GaetanoG. Prostacyclin-like activity in rat vascular tissues. Fast, long-lasting inhibition by treatment with lysine acetylsalicylate. Prostaglandins 1977; 14: 1117-1124
    CrossrefPubMedGoogle Scholar
  • 50 Johnson AR. Human pulmonary endothelial cells in culture. Activities of cells from arteries and cells from veins. J Clin Invest 1980; 65: 841-850
    CrossrefPubMedGoogle Scholar
  • 51 Brash AR. A review of possible roles of the platelet 12-lipoxygenase. Circulation 1985; 72: 702-707
    CrossrefPubMedGoogle Scholar
  • 52 Fonlupt P, Croset M, Lagarde M. 12-HETE inhibits the binding of PGH2/TXA2 receptor ligands in human platelets. Thromb Res 1991; 63: 239-248
    CrossrefPubMedGoogle Scholar
  • 53 Hadjiagapiou C, Spector AA. 12-Hydroxyeicosatetraenoic acid reduces prostacyclin production by endothelial cells. Prostaglandins 1986; 31: 1135-1144
    CrossrefPubMedGoogle Scholar
  • 54 Mehta P, Mehta J, Lawson D, Krop I, Letts LG. Leukotrienes potentiate the effects of epinephrine and thrombin on human platelet aggregation. Thromb Res 1986; 41: 731-738
    CrossrefPubMedGoogle Scholar