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DOI: 10.1055/s-0038-1657656
Endothelium-derived Nitric Oxide Decreases Polymorphonuclear Leukocyte Interaction with the Deeply Injured Arterial Wall under Intermediate and High Shear Conditions
Publication History
Received 06 1996
Accepted after resubmission 26 March 1997
Publication Date:
12 July 2018 (online)
Summary
Previous studies have shown that nitric oxide (NO) inhibits specific agonist-induced polymorphonuclear leukocyte (neutrophil) and platelet aggregation in vitro. However, the inhibitory effects of NO on neutrophil interaction with the deeply injured arterial wall under conditions of flow is unknown. Therefore, we investigated the influence of NO derived from the endothelium on neutrophil and platelet interactions with the downstream arterial media under controlled flow conditions. Porcine aortic media, simulating deep arterial wall injury, was exposed to flowing porcine non-anticoagulated arterial blood for 5 min at intermediate (1006 s1) and high (3397 s1) shear conditions, and deposition of radiolabeled neutrophils and platelets was quantified. Neutrophil deposition on the exposed arterial media was reduced, by more than 30%, by pretreatment of the endothelium with the physiological precursor of NO, L-arginine, from 84.1 ± 13.7 to 57.4 ± 7.2 X 103/cm2 (p < 0.05) at 1006 s*1, and from 99.3 ± 9.8 to 65.5 ± 8.7 X KP/cm2 (p < 0.05) at 3397 s1 of shear rate, relative to control. Pretreatment of the endothelium with the inactive stereoisomer D-arginine had no effect on neutrophil deposition. These specific inhibitory effects of L-arginine were completely abolished by the inhibitor of NO synthesis, N^-nitro- L-arginine methyl ester (l-NAME) at both shear rates. Endothelial pretreatment with D-arginine, or with L-arginine, in the absence or presence of l-NAME, did not significantly influence platelet interaction with the thrombogenic arterial media at intermediate and high shear rates. These results indicate that NO derived from the endothelium can modulate and has a greater influence on neutrophil, than on platelet, interaction with the injured arterial wall exposing the media under conditions of flow typical to moderately and severely stenosed arteries.
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References
- 1 Palmer RMJ, Ashton DS, Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 1988; 333: 664-666
- 2 Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987; 327: 524-526
- 3 Feelisch M, te PoelM, Zamora R, Deussen A, Moncada S. Understanding the controversy over the identity of EDRF. Nature 1994; 368: 62-65
- 4 Clancy RM, Leszczynska-Piziak J, Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 1992; 90: 1116-1121
- 5 McCall T, Whittle BJR, Boughton-Smith NK, Moncada S. Inhibition of FMLP-induced aggregation of rabbit neutrophils by nitric oxide. Br J Pharmacol 1988; 95: 517P
- 6 Moilanen E, Vuorinen P, Kankaanranta H, Metsa-Ketela T, Vapaatalo H. Inhibition by nitric oxide-donors of human polymorphonuclear leukocyte functions. BrJ Pharmacol 1993; 109: 852-858
- 7 Riutta A, Alanko J, Mucha I, Vapaatalo H. Effects of Trolox C and SIN-1 on arachidonic acid metabolism and on cyclic GMP formation in leukocytes. Eur J Pharmacol 1994; 262: 217-222
- 8 Schröder H, Ney P, Woditsch I, Schrör K. Cyclic GMP mediates SIN-1-induced inhibition of human polymorphonuclear leukocytes. Eur J Pharmacol 1990; 182: 211-218
- 9 Sundqvist T, Forslung T, Bengtsson T, Axelsson KL. S-nitroso-N-acetyl- penicillamine reduces leukocyte adhesion to type I collagen. Inflammation 1994; 18: 625-631
- 10 Clancy R, Leszczynska J, Amin A, Levartovsky D, Abramson SB. Nitric oxide stimulates ADP ribosylation of actin in association with the inhibition of actin polymerisation in human neutrophils. J Leukoc Biol 1995; 58: 196-202
- 11 Provost P, Lam JYT, Lacoste L, Merhi Y, Waters D. Endothelium-derived nitric oxide attenuates neutrophil adhesion to endothelium under arterial flow conditions. Arterioscler Thromb 1994; 14: 331-335
- 12 Merhi Y, Lam JYT, Lacoste L-L, Latour JG, Guidoin R, Waters D. Effects of thrombocytopenia and shear rate on neutrophil and platelet deposition on endothelial and medial arterial surfaces. Arterioscler Thromb 1993; 13: 951-957
- 13 Merhi Y, Guidoin R, Provost P, Leung T-K, Lam JYT. Increase of neutrophil adhesion and vasoconstriction with platelet deposition after deep arterial injury by angioplasty. Am Heart J 1995; 129: 445-451
- 14 Radomski MW, Palmer RMJ, Moncada S. Comparative pharmacology of endothelium-derived relaxing factor, nitric oxide and prostacyclin in platelets. BrJ Pharmacol 1987; 92: 181-187
- 15 Radomski MW, Palmer RMJ, Moncada S. The anti-aggregating properties of vascular endothelium: interactions between prostacyclin and nitric oxide. Br J Pharmacol 1987; 92: 639-646
- 16 Furlong B, Henderson AH, Lewis MJ, Smith JA. Endothelium-derived relaxing factor inhibits in vitro platelet aggregation. Br J Pharmacol 1987; 90: 687-692
- 17 Turitto VT, Baumgartner HR. Platelet interaction with subendothelium in a perfusion system: physical role of red blood cells. Microvasc Res 1975; 09: 335-344
- 18 Valles J, Santos MT, Aznar J, Marcus AJ, Martinez-Sales V, Portoles M, Broekman MJ, Safier LB. Erythrocytes metabolically enhance collagen- induced platelet responsiveness via increased thromboxane production, adenosine diphosphate release, and recruitment. Blood 1991; 78: 154-162
- 19 Bazzoni G, Dejana E, Del MaschioA. Platelet-neutrophil interactions. Possible relevance in the pathogenesis of thrombosis and inflammation. Haematologica 1991; 76: 491-499
- 20 Badimon L, Badimon J-J, Galvez A, Chesebro JH, Fuster V. Influence of arterial damage and wall shear rate on platelet deposition. Ex vivo study in a swine model. Arteriosclerosis 1986; 06: 312-320
- 21 Turitto VT, Baumgartner HR. Platelet-surface Interactions. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Salzman EW. eds. J. B. Lippincott Company; Philadelphia, PA: 1982. pp 364-379
- 22 Rees DD, Palmer RMJ, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 1990; 101: 746-752
- 23 Provost P, Merhi Y. BW755C, a dual lipoxygenase/cyclooxygenase inhibitor, reduces mural platelet and neutrophil deposition and vasoconstriction after angioplasty injury in pigs. J Pharmacol Exp Ther 1996; 77: 217-221
- 24 Merhi Y, Provost P, Guidoin R, Latour J-G. Importance of platelets in neutrophil adhesion and vasoconstriction following arterial injury by angioplasty in pigs. Arterioscler Thromb Vase Biol. 1997 (in press)
- 25 Goldsmith HL, Turitto VT. Rheological aspects of thrombosis and hemostasis: basic principles and applications. Thromb Haemost 1986; 55: 415-435
- 26 Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 1991; 88: 4651-4655
- 27 de GraafJC, Banga JD, Moncada S, Palmer RMJ, de GrootPG, Sixma JJ. Nitric oxide functions as an inhibitor of platelet adhesion under flow conditions. Circulation 1992; 85: 2284-2290
- 28 Hecker M, Mitchell JA, Harris HJ, Katsura M, Thiemermann C, Vane JR. Endothelial cells metabolize NG-monomethyl-L-arginine to L-citrulline and subsequently to L-arginine. Biochem Biophys Res Comm 1990; 167: 1037-1043
- 29 Steele PM, Chesebro JH, Stanson AW, Holmes Jr DR, Dewanjee MK, Badimon L, Fuster V. Balloon angioplasty: natural history of the pathophysiological response to injury in a pig model. Circ Res 1985; 57: 105-112
- 30 De ServiS, Mazzone A, Ricevuti G, Fioravanti A, Bramucci E, Angoli L, Stefano G, Specchia G. Granulocyte activation after coronary angioplasty in humans. Circulation 1990; 82: 140-146
- 31 Lundgren-Akerlund E, Olofsson AM, Berger E, Arfors KE. CDllb/CD18- dependent polymorphonuclear leukocyte interaction with matrix proteins in adhesion and migration. Scand J Immunol 1993; 37: 569-574
- 32 Garnotel R, Monboisse JC, Randoux A, Haye B, Borel JP. The binding of type I collagen to lymphocyte function-associated antigen (LFA) 1 integrin triggers the respiratory burst of human polymorphonuclear neutrophils. Role of calcium signaling and tyrosine phosphorylation of LFA-1. J Biol Chem 1995; 270: 27495-27503
- 33 Bohnsack JF, Zhou X-N. Divalent cation substitution reveals CD 18- and very late antigen-dependent pathways that mediate human neutrophil adherence to fibronectin. J Immunol 1992; 149: 1340-1347
- 34 Bohnsack JF. CD ll/CD 18-independent neutrophil adherence to laminin is mediated by the integrin VLA-6. Blood 1992; 79: 1545-1552
- 35 Nathan C, Srimal S, Farber C, Sanchez E, Kabbash L, Asch A, Gailit J, Wright SD. Cytokine-induced respiratory burst of human neutrophils: dependence on extracellular matrix protein and CD ll/CD 18 integrins. J Cell Biol 1989; 109: 1341-1349
- 36 Merhi Y, Lacoste LL, Lam JYT. Neutrophil implications in platelet deposition and vasoconstriction after deep arterial injury by angioplasty in pigs. Circulation 1994; 90: 997-1002
- 37 Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu Y-M, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-851
- 38 Yeo EL, Sheppard J-AI, Feuerstein IA. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiological shear conditions (an injury vessel wall model). Blood 1994; 83: 2498-2507
- 39 Diacovo TG, Roth SJ, Buccola JM, Bainton DF, Springer TA. Neutrophil rolling, arrest, and transmigration accross activated, surface-adherent platelets via sequential action of P-selectin and the β2-integrin CD 1 lb/CD 18. Blood 1996; 88: 146-157
- 40 Michelson AD, Benoit SE, Furman MI, Breckwoldt WL, Rohrer MJ, Barnard MR, Loscalzo J. Effects of nitric oxide/EDRF on platelet surface glycoproteins. Am J Physiol 1996; 270: H1640-H1648
- 41 Langford EJ, Wainwright RJ, Martin JF. Platelet activation in acute myocardial infarction and unstable angina is inhibited by nitric oxide donors. Arterioscler Thromb Vase Biol 1996; 16: 51-55
- 42 Murohara T, Parkinson SJ, Waldman SA, Lefer AM. Inhibition of nitric oxide biosynthesis promotes P-selectin expression in platelets: role of protein kinase C. Arterioscler Thromb Vase Biol 1995; 15: 2068-2075
- 43 Forslund T, Sundqvist T. Nitric oxide reduces hydrogen peroxide production from human polymorphonuclear neutrophils. Eur J Clin Invest 1995; 25: 09-14
- 44 Provost P, Tremblay J, Merhi Y. The antiadhesive and antithrombotic effects of the nitric oxide donor SIN-1 are combined with a decreased vasoconstriction in a porcine model of balloon angioplasty. Arterioscler Thromb Vase Biol. 1997 (in press)
- 45 Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel DJ, Valeri CR, Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an s-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 1992; 89: 7674-7677
- 46 Myers PR, Minor Jr RL, Guerra Jr R, Bates JN, Harrison DG. Vasorelaxant properties of the endothelium-derived relaxing factor more closely resemble s-nitrosocysteine than nitric oxide. Nature 1990; 345: 161-163
- 47 Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, Michel T, Singel DJ, Loscalzo J. s-Nitrosylation of proteins with nitric oxide: Synthesis and characterization of biologically active compounds. Proc Natl Acad Sci USA 1992; 89: 444-448
- 48 Malinski T, Taha Z, Grunfeld S, Patton S, Kapturczak M, Tomboulian P. Diffusion of nitric oxide in the aorta wall monitored in situ by porphyrinic microsensors. Biochem Biophys Res Commun 1993; 193: 1076-1082
- 49 Freiman PC, Mitchell GG, Heistad DD, Armstrong ML, Harrison DG. Atherosclerosis impairs endothelium-dependent vascular relaxation to acetylcholine and thrombin in primates. Circ Res 1986; 58: 783-789
- 50 Lefer AM, Ma X-l. Decreased basal nitric oxide release in hypercholesterolemia increases neutrophil adherence to rabbit coronary artery endothelium. Arterioscler Thromb 1993; 13: 771-776
- 51 Ma X-l, Weyrich AS, Lefer DJ, Lefer AM. Diminished basal nitric oxide release after myocardial ischemia and reperfusion promotes neutrophil adherence to coronary endothelium. Circ Res 1993; 72: 403-412
- 52 Siegfried MR, Erhardt J, Rider T, Ma X-l, Lefer AM. Cardioprotection and attenuation of endothelial dysfunction by organic nitric oxide donors in myocardial ischemia-reperfusion. J Pharmacol Exp Ther 1992; 260: 668-675
- 53 Lefer AM, Siegfried MR, Ma X-l. Protection of ischemia-reperfusion injury by sydnonimine NO donors via inhibition of neutrophil-endothelium interaction. J Cardiovasc Pharmacol 1993; 22 (Suppl. 07) S27-S33
- 54 Hansen PR. Role of neutrophils in myocardial ischemia and reperfusion. Circulation 1995; 91: 1872-1885
- 55 Tsao PS, Ma X-l, Lefer AM. Activated neutrophils aggravate endothelial dysfunction after reperfusion of the ischemic feline myocardium. Am Heart J 1992; 123: 1464-1471
- 56 Nishida M, Kuzuya T, Hoshida S, Kim Y, Kitabatake A, Kamada T, Tada M. Polymorphonuclear leukocytes induced vasoconstriction in isolated canine coronary arteries. Circ Res 1990; 66: 253-258
- 57 Weiss SJ. Tissue destruction by neutrophils. N Eng J Med 1989; 320: 365-376
- 58 Groves PH, Penny WJ, Cheadle HA, Lewis MJ. Exogenous nitric oxide inhibits in vivo platelet adhesion following balloon angioplasty. Cardiovasc Res 1992; 26: 615-619
- 59 Groves PH, Lewis MJ, Cheadle HA, Penny WJ. SIN-1 reduces platelet adhesion and platelet thrombus formation in a porcine model of balloon angioplasty. Circulation 1993; 87: 590-597
- 60 Ovize M, de LorgerilM, Cathignol D, Delaye J, Renaud S. Inhibition of coronary artery thrombosis by SIN-1, a donor of nitric oxide. J Cardiovasc Pharmacol 1990; 16: 641-645
- 61 Darius H, Ahland B, Rucker W, Klaus W, Peskar BA, Schror K. The effects of molsidomine and its metabolite SIN-1 on coronary vessel tone, platelet aggregation, and eicosanoid formation in vitro-inhibition of 12-HPETE biosynthesis. J Cardiovasc Pharmacol 1984; 06: 115-121
- 62 Bult H, Fret HRL, Herman AG. Interaction between SIN-1 and prostacyclin in inhibiting platelet aggregation. J Cardiovasc Pharmacol 1989; 14 (Suppl. 11) S120-S123
- 63 Selak MA, Chignard M, Smith JB. Cathepsin G is a strong platelet agonist released by neutrophils. Biochem J 1988; 251: 293-299
- 64 Kornecki E, Ehrlich YH, De MarsDD, Lenox RH. Exposure of fibrinogen receptors in human platelets by surface proteolysis with elastase. J Clin Invest 1986; 77: 750-756
- 65 Handin RI, Karabin R, Boxer GJ. Enhancement of platelet function by superoxide anion. J Clin Invest 1977; 59: 959-965
- 66 Snyder F. Platelet-activating factor and related acetylated lipids as potent biologically active cellular mediators. Am J Physiol 1990; 259: C697-C708
- 67 Wainwright CL, Martorana PA. Pirsidomine, a novel nitric oxide donor, suppresses ischemic arrythmias in anesthetized pigs. J Cardiovasc Pharmacol 1993; 22 (Suppl. 07) S44-S50
- 68 Karlberg K-E, Chen J, Egberg N, Sylven C. SIN-1 partially and RGDS totally counteracts platelet aggregation as assessed in vitro by two independent whole blood methods. Thromb Res 1993; 72: 531-540
- 69 Groves PH, Banning AP, Penny WJ, Newby AC, Cheadle HA, Lewis MJ. The effects of exogenous nitric oxide on smooth muscle cell proliferation following porcine carotid angioplasty. Cardiovasc Res 1995; 30: 87-96
- 70 Jen CJ, Mclntire LV. Characteristics of shear-induced aggregation in whole blood. J Lab Clin Med 1984; 103: 115-124
- 71 Mruk JS, Chesebro JH, Webster MWI. Platelet aggregation and interaction with the coagulation system: implications for antithrombotic therapy in arterial thrombosis. Coron Artery Dis 1990; 01: 149-158
- 72 Radomski MW, Palmer RMJ, Moncada S. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc Natl Acad Sci USA 1990; 87: 5193-5197
- 73 Lam JYT, Chesebro JH, Steele PM, Dewanjee MK, Badimon L, Fuster V. Deep arterial injury during experimental angioplasty: relation to a positive indium-111-labeled scintigram, quantitative platelet deposition and mural thrombosis. J Am Coll Cardiol 1986; 08: 1380-1386
- 74 Ruggeri ZM. Mechanisms of shear-induced platelet adhesion and aggregation. Thromb Haemost 1993; 70: 119-123
- 75 Maalej N, Folts JD. Increased shear stress overcomes the antithrombotic platelet inhibitory effect of aspirin in stenosed dog coronary arteries. Circulation 1996; 93: 1201-1205
- 76 Nishikawa M, Kanamori M, Hidaka H. Inhibition of platelet aggregation and stimulation of guanylate cyclase by an antianginal agent molsidomine and its metabolites. J Pharmacol Exp Ther 1982; 220: 183-190