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Pharmacological Research . Vol. 26, No . 3, 1992
PLATELET-DEPENDENT MODULATION OF NEUTROPHIL FUNCTION GIANFRANCO BAZZONI, ELISABETTA DEJANA and ALDO DEL MASCHIO
Laboratory of Vascular Biology, Istituto di Ricerche Farmacologiche "Mario Negri", Via Eritrea 62, 20157 Milano, Italy Received in final form I April /992 KEY WORDS :
platelets, neutrophils, thrombosis, inflammation .
Several lines of in vitro evidence indicate that complex interactions occur between platelets and neutrophils [1] . Here we summarize the mechanisms of plateletdependent modulation of neutrophil function which may be relevant in the development of both thrombotic and inflammatory conditions . Platelet adhesion to the subendothelial matrix of a damaged vessel wall induces platelet activation and the release of substances able to cause the migration of circulating leukocytes toward the sites of injury . Platelet factor 4 (PF4 ) and platelet-derived growth factor (PDGF), two proteins released upon platelet activation, as well as arachidonic acid metabolites of the 12-lipoxygenase pathway are chemotactic for leukocytes [2-4] and may favour neutrophil accumulation in tcivo [5] . Adhesion of recruited neutrophils may be increased by platelets spread on extracellular matrix [6,7] and by platelet-derived substances, such as PDGF . serotonin and thromboxane A 2 [8-10] . Platelets may amplify neutrophil recruitment by enhancing the generation from these cells of the chemoattractant leukotriene (LT) B 4 [11] and may induce vasoconstriction by converting neutrophil-derived LTA, into the powerful aspirininsensitive vasoconstrictor LTC 4 [12] . Interestingly, high levels of LTC, and thromboxane A 2 are associated to the accumulation of both platelets and neutrophils in isolated hearts subjected to ischaemia and reperfusion [13] . Adenine nucleotides and PDGF released upon platelet activation may stimulate neutrophil degranulation, phagocytosis and respiratory burst [8,14,15] . Noteworthy, mechanisms leading to platelet adhesion to neutrophils, like those mediated by the surface molecule P-selectin (or GMP-140 [16,17]), might generate a common microenvironment, in which the transfer of mediators involved in platelet-neutrophil interactions is facilitated . Neutrophil activation may amplify the thrombotic process by releasing toxic oxygen free radicals and proteases, which are able to damage the endothelial Correspondence to : Dr Aldo Del Maschio . 1043-6618/92/070269-04/$08 .00/0
© 1992 The Italian Pharmacological Society
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integrity [18] . The consequent exposure of the thrombogenic subendothelial matrix causes further platelet adhesion and activation . Moreover, endothelial injury determined by the platelet-dependent activation of leukocytes may bring about the lack of production of the antithrombotic and vasodilatory agents prostacyclin and nitric oxide [19] . Finally, neutrophils may amplify the thrombotic process by directly causing platelet activation ; this topic is discussed in more detail in the present issue of the journal 120] . In vivo evidence for platelet-neutrophil interaction came from studies of coronary occlusion and reperfusion, showing reduced platelet accumulation in the infarcted myocardium of neutrophil-depleted animals [21] . Similarly, intradermal injection of chemotactic agents induced platelet accumulation only in neutrophilsufficient but not in neutrophil-depleted animals [22] . Moreover, platelets, besides directly acting as inflammatory cells by releasing substances endowed with phlogistic potential, may also modulate leukocyte function in several inflammatory diseases, such as asthma [23] or immune nephritis [24] . In asthma, platelet activation may be induced by a lipid mediator generated by IgE-sensitized leukocytes, namely platelet activating factor (PAF [25]) . PAF, in turn, exerts its phlogistic effects mainly by a platelet-dependent mechanism, since platelets are necessary for PAF-induced bronchoconstriction to become evident [26] and antigen-dependent leukocyte infiltration into the lungs is reduced in asthmatic animals following platelet depletion [23] . Furthermore, immune complex glomerulonephritis highlights the ability of platelets to amplify neutrophil-dependent tissue damage, since selective platelet depletion exerts protective effect, as evidenced by indices of renal function and morphology [24] . Finally, platelet-derived transforming growth factor-f3 (TGF-fl) induces neutrophil recruitment to synovial tissues and contributes to synovial inflammation and hyperplasia observed in rheumatoid arthritis, gout and related osteoarthritis [27] . Besides activating neutrophils, platelets may also dampen, under certain circumstances, neutrophil responsiveness . [I] Unstimulated platelets may limit the effects of neutrophil activation by inhibiting oxygen radical production [28] and reducing their cytotoxic effects [29] . Moreover, substances released upon platelet activation, such as TGF-/3 [30], and "adherence inhibiting factors" [31] inhibit neutrophil adhesion to endothelial cells, one of the first events of inflammation . A similar inhibitory effect is exerted also by soluble P-selectin [32], although its release from activated platelets has not yet been reported . Moreover, PDGF [33] and soluble P-selectin [34] reduce the generation of superoxide anions by activated neutrophils . In summary, platelet activation in thrombotic conditions may elicit neutrophil responses which may in turn worsen the thrombotic process . A similar amplification may be exerted by platelets during neutrophil involvement in inflammatory reactions . On the other hand, platelets may limit the harmful tissuedamaging effects of excessive and misdirected neutrophil activation in both thrombotic and inflammatory diseases . The pathways of reciprocal activation and inhibition between platelets and neutrophils are extremely complex . To lessen the dangers of over interpreting the conclusions summarized here, it should be considered that they may be influenced,
Pharmacological Research, Vol. 26, No . 3, 1992
271
at least in part, by the experimental conditions used, such as cell-to-cell ratio, incubation time and stimulus specificity . Since most of the data have been obtained from in vitro systems, further investigation in vivo and possibly in humans is needed to clarify their relative biological relevance . This area of investigation underlines the need for pharmacological research directed to the development of new drugs (both antithrombotic and anti-inflammatory) able to interfere with the activation of more than one cell type .
ACKNOWLEDGEMENTS This work was supported by the PF Biotecnologie e Biostrumentazione and by the Italian National Research Council (Project CNR 89 .01277 .04) .
REFERENCES 1 . Bazzoni G, Dejana E, Del Maschio A . Platelet-neutrophil interactions . Possible relevance in the pathogenesis of thrombosis and inflammation . Haematologica 1991 ; 76 : 491-9 . 2 . Deuel TF, Senior RM, Chang D, Griffin GL, Heinrikson RL, Kaiser ET . Platelet factor 4 is chemotactic for neutrophils and monocytes . Proc Natl Acad Sci USA 1981 ; 78 : 4584-7 . 3 . Deuel TF, Senior RM, Huang JS, Griffin GL . Chemotaxis of monocytes and neutrophils to platelet-derived growth factor . J Clin Invest 1982 ; 69 : 1046-9 . 4 . Goetzl EJ, Woods JM, Gorman RR . Stimulation of human eosinophil and neutrophil polymorphonuclear leukocyte chemotaxis and random migration by 12-L-hydroxy-5, 8, 10, 14-eicosatetraenoic acid . J Clin Invest 1977 ; 59 : 179-83 . 5 . Fretland DJ, Widomski DL, Zemaitis JL, Tsai BS, Djurie SW, Penning TD, Miyashiro JM, Bauer RF . 12(R)-Hydroxyeicosatetraenoic acid is a neutrophil chemoattractant in the cavine, lapine, murine and canine dermis . Prost Leuk Ess Fatty Acids Rev 1989 ; 37 : 79-81 . 6. Ratliff NB, Gerrard JM, White JG . Platelet-leukocyte interactions following arterial endothelial injury . Am J Pathol 1979 ; 96 : 567-580 . 7 . Morley DJ, Feuerstein IA . Adhesion of polymorphonuclear leukocytes to protein-coated and platelet adherent surfaces . Thromb Haemost 1989 ; 62 : 1023-8 . 8 . Tzeng DY, Deuel TF, Huang JS, Senior RM, Boxer LA, Baehner RL . Platelet-derived growth factor promotes polymorphonuclear leukocyte activation . Blood 1984 ; 64 : 1123-8 . 9 . Boogaerts MA, Yamada 0, Jacob HS, Moldow CF . Enhancement of granulocyteendothelial cell adherence and granulocyte-induced cytotoxicity by platelet release products . Proc Natl Acad Sci USA 1982 ; 79 : 7019-23 . 10 . Spagnuolo PJ, Ellner JJ, Hassd A, Dunn MJ . Thromboxane A2 mediates augmented polymorphonuclear leukocyte adhesiveness . J Clin Invest 1980 ; 66 : 406-14 . 11 . Maclouf J, Fruteau de Laclos B, Borgeat P . Stimulation of leukotriene biosynthesis in human blood leukocytes by platelet-derived 12-hydroperoxy-icosatetraenoic acid . Prod Natl Acad Sci USA 1982 ; 79 : 6042-6 . 12 . Maclouf AJ, Murphy RC . Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets . J Biol Chem 1988 ; 263 : 174-81 . 13 . Mullane K . Neutrophil-platelet interactions and post-ischemic myocardial injury . It) : Schroer K, Sinzinger H, eds . Prostaglandins in clinical research : cardiovascular system . New York : Alan Liss, 1989 : 289-315 .
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14 . Sakamoto H, Yokoya Y . Purification and characterization of macromolecular phagocytosis activators released from platelets . J Leak Biol 1991 ; 50 : 356-63 . 15 . Ward PA, Cunningham TW, McCulloch KK, Phan SH, Powell J, Johnson KJ . Platelet enhancement of Oz_ responses in stimulated human neutrophils . Lab Invest 1988 ; 58 : 37-47 . 16. Hamburger SA, McEver RP . GMP-140 mediates adhesion of stimulated platelets to neutrophils . Blood 1990 ; 75 : 550-4. 17 . Picker LJ, Warnock RA, Burns AR, Doerschuk CM, Berg EL, Butcher EC . The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell 1991 ; 66 : 921-33 . 18 . Ward PA . Mechanisms of endothelial cell injury . J Lab Clin Med 1991 ; 118 : 421-6 . 19 . Vane JR, Angaard EE, Botting RM . Regulatory functions of the vascular endothelium . N Engl J Med 1990 ; 323 : 27-36 . 20. Cerletti C, Evangelista V, de Gaetano G . Polymorphonuclear leukocyte-dependent modulation of platelet function : relevance to the pathogenesis of thrombosis . Pharmacol Res 1992 ; 26 : 261-8 . 21 . Bednar M, Smith B, Pinto A, Mullane KM . Neutrophil depletion suppresses "' In-labeled platelet accumulation in infarcted myocardium . J Cardiovasc Pharmacol 1985 ; 7: 906-12 . 22 . Issekutz AC, Ripley M, Jackson JR . Role of neutrophils in the deposition of platelets during acute inflammation . Lab Invest 1983 ; 49 : 716-24 . 23 . Morley J, Sanjar S, Page CP . The platelet in asthma . Lancet 1984; ii : 1142-4 . 24. Johnson RJ, Alpers CE, Pritzl P, Schulze M, Baker P, Pruchno C, Couser WG . Platelets mediate neutrophil-dependent immunecomplex nephritis in the rat . J Clin Invest 1988 ; 82 :1225-35 . 25 . Benveniste J, Henson PM, Cochrane CG . Leukocyte-dependent histamine release from rabbit platelets . The role of IgE, basophils, and a platelet-activating factor . J Exp Med 1972 ;136 :1356-77 . 26 . Vargaftig BB, Lefort J, Chignard M, Benveniste J . Platelet-activating factor induces a platelet-dependent bronchoconstriction unrelated to the formation of prostaglandin derivatives . Eur J Pharmacol 1980 ; 65 : 185-92 . 27 . Fava RA, Olsen N, Postlethwaite AE, Broadley KN, Davidson JM, Nanney LB, Lucas C, Townes AS . Transforming growth factor p1 (TGF-(31) induced neutrophil recruitment to synovial tissues : implication for TGF-(3-driven synovial inflammation and hyperplasia . J Exp Med 1991 ; 173 : 1121-32 . 28 . Moon DG, van Der Zee H, Weston LK, Gudewicz PW, Fenton II JW, Kaplan JE . Platelet modulation of neutrophil superoxide anion production . Thromb Haemost 1990 ; 63 : 91-6 . 29 . Dallegri F, Ballestrero A, Ottonello L, Patrone F . Platelets as inhibitory cells in neutrophil-mediated cytolysis . J Lab Clin Med 1989 ; 114 : 502-9 . 30 . Gamble JR, Vadas MA . Endothelial adhesiveness for blood neutrophils is inhibited by transforming growth factor-(3 . Science 1988 ; 242 : 97-9 . 31 . Iwabuchi K, Yamashita T . Platelet-derived adherence-inhibiting factor in humans . Blood 1990 ;76 :2368-73 . 32 . Gamble JR, Skinner MP, Berndt MC, Vadas MA . Prevention of activated neutrophil adhesion to endothelium by soluble adhesion protein GMP 140 . Science 1990 ; 249 : 414-7 . 33 . Wilson E, Laster SM, Gooding LR, Lambeth JD . Platelet-derived growth factor stimulates phagocytosis and blocks agonist-induced activation of the neutrophil respiratory burst : a possible cellular mechanism to protect against oxigen radical damage . Proc Nat Acad Sci USA 1987 ; 84 : 2213-7 . 34 . Wong CS, Gamble JR, Skinner MP, Lucas CM, Berndt MC, Vadas MA . Adhesion protein GMP140 inhibits superoxide anion release by human neutrophils . Proc Natl Acad Sci USA 1991 ; 88 : 2397-401 .
Pharmacological Research . Vol. 26, No . 3, 1992
PLATELET-DEPENDENT MODULATION OF NEUTROPHIL FUNCTION GIANFRANCO BAZZONI, ELISABETTA DEJANA and ALDO DEL MASCHIO
Laboratory of Vascular Biology, Istituto di Ricerche Farmacologiche "Mario Negri", Via Eritrea 62, 20157 Milano, Italy Received in final form I April /992 KEY WORDS :
platelets, neutrophils, thrombosis, inflammation .
Several lines of in vitro evidence indicate that complex interactions occur between platelets and neutrophils [1] . Here we summarize the mechanisms of plateletdependent modulation of neutrophil function which may be relevant in the development of both thrombotic and inflammatory conditions . Platelet adhesion to the subendothelial matrix of a damaged vessel wall induces platelet activation and the release of substances able to cause the migration of circulating leukocytes toward the sites of injury . Platelet factor 4 (PF4 ) and platelet-derived growth factor (PDGF), two proteins released upon platelet activation, as well as arachidonic acid metabolites of the 12-lipoxygenase pathway are chemotactic for leukocytes [2-4] and may favour neutrophil accumulation in tcivo [5] . Adhesion of recruited neutrophils may be increased by platelets spread on extracellular matrix [6,7] and by platelet-derived substances, such as PDGF . serotonin and thromboxane A 2 [8-10] . Platelets may amplify neutrophil recruitment by enhancing the generation from these cells of the chemoattractant leukotriene (LT) B 4 [11] and may induce vasoconstriction by converting neutrophil-derived LTA, into the powerful aspirininsensitive vasoconstrictor LTC 4 [12] . Interestingly, high levels of LTC, and thromboxane A 2 are associated to the accumulation of both platelets and neutrophils in isolated hearts subjected to ischaemia and reperfusion [13] . Adenine nucleotides and PDGF released upon platelet activation may stimulate neutrophil degranulation, phagocytosis and respiratory burst [8,14,15] . Noteworthy, mechanisms leading to platelet adhesion to neutrophils, like those mediated by the surface molecule P-selectin (or GMP-140 [16,17]), might generate a common microenvironment, in which the transfer of mediators involved in platelet-neutrophil interactions is facilitated . Neutrophil activation may amplify the thrombotic process by releasing toxic oxygen free radicals and proteases, which are able to damage the endothelial Correspondence to : Dr Aldo Del Maschio . 1043-6618/92/070269-04/$08 .00/0
© 1992 The Italian Pharmacological Society
270
Pharmacological Research, Vol . 26, No . 3, /992
integrity [18] . The consequent exposure of the thrombogenic subendothelial matrix causes further platelet adhesion and activation . Moreover, endothelial injury determined by the platelet-dependent activation of leukocytes may bring about the lack of production of the antithrombotic and vasodilatory agents prostacyclin and nitric oxide [19] . Finally, neutrophils may amplify the thrombotic process by directly causing platelet activation ; this topic is discussed in more detail in the present issue of the journal 120] . In vivo evidence for platelet-neutrophil interaction came from studies of coronary occlusion and reperfusion, showing reduced platelet accumulation in the infarcted myocardium of neutrophil-depleted animals [21] . Similarly, intradermal injection of chemotactic agents induced platelet accumulation only in neutrophilsufficient but not in neutrophil-depleted animals [22] . Moreover, platelets, besides directly acting as inflammatory cells by releasing substances endowed with phlogistic potential, may also modulate leukocyte function in several inflammatory diseases, such as asthma [23] or immune nephritis [24] . In asthma, platelet activation may be induced by a lipid mediator generated by IgE-sensitized leukocytes, namely platelet activating factor (PAF [25]) . PAF, in turn, exerts its phlogistic effects mainly by a platelet-dependent mechanism, since platelets are necessary for PAF-induced bronchoconstriction to become evident [26] and antigen-dependent leukocyte infiltration into the lungs is reduced in asthmatic animals following platelet depletion [23] . Furthermore, immune complex glomerulonephritis highlights the ability of platelets to amplify neutrophil-dependent tissue damage, since selective platelet depletion exerts protective effect, as evidenced by indices of renal function and morphology [24] . Finally, platelet-derived transforming growth factor-f3 (TGF-fl) induces neutrophil recruitment to synovial tissues and contributes to synovial inflammation and hyperplasia observed in rheumatoid arthritis, gout and related osteoarthritis [27] . Besides activating neutrophils, platelets may also dampen, under certain circumstances, neutrophil responsiveness . [I] Unstimulated platelets may limit the effects of neutrophil activation by inhibiting oxygen radical production [28] and reducing their cytotoxic effects [29] . Moreover, substances released upon platelet activation, such as TGF-/3 [30], and "adherence inhibiting factors" [31] inhibit neutrophil adhesion to endothelial cells, one of the first events of inflammation . A similar inhibitory effect is exerted also by soluble P-selectin [32], although its release from activated platelets has not yet been reported . Moreover, PDGF [33] and soluble P-selectin [34] reduce the generation of superoxide anions by activated neutrophils . In summary, platelet activation in thrombotic conditions may elicit neutrophil responses which may in turn worsen the thrombotic process . A similar amplification may be exerted by platelets during neutrophil involvement in inflammatory reactions . On the other hand, platelets may limit the harmful tissuedamaging effects of excessive and misdirected neutrophil activation in both thrombotic and inflammatory diseases . The pathways of reciprocal activation and inhibition between platelets and neutrophils are extremely complex . To lessen the dangers of over interpreting the conclusions summarized here, it should be considered that they may be influenced,
Pharmacological Research, Vol. 26, No . 3, 1992
271
at least in part, by the experimental conditions used, such as cell-to-cell ratio, incubation time and stimulus specificity . Since most of the data have been obtained from in vitro systems, further investigation in vivo and possibly in humans is needed to clarify their relative biological relevance . This area of investigation underlines the need for pharmacological research directed to the development of new drugs (both antithrombotic and anti-inflammatory) able to interfere with the activation of more than one cell type .
ACKNOWLEDGEMENTS This work was supported by the PF Biotecnologie e Biostrumentazione and by the Italian National Research Council (Project CNR 89 .01277 .04) .
REFERENCES 1 . Bazzoni G, Dejana E, Del Maschio A . Platelet-neutrophil interactions . Possible relevance in the pathogenesis of thrombosis and inflammation . Haematologica 1991 ; 76 : 491-9 . 2 . Deuel TF, Senior RM, Chang D, Griffin GL, Heinrikson RL, Kaiser ET . Platelet factor 4 is chemotactic for neutrophils and monocytes . Proc Natl Acad Sci USA 1981 ; 78 : 4584-7 . 3 . Deuel TF, Senior RM, Huang JS, Griffin GL . Chemotaxis of monocytes and neutrophils to platelet-derived growth factor . J Clin Invest 1982 ; 69 : 1046-9 . 4 . Goetzl EJ, Woods JM, Gorman RR . Stimulation of human eosinophil and neutrophil polymorphonuclear leukocyte chemotaxis and random migration by 12-L-hydroxy-5, 8, 10, 14-eicosatetraenoic acid . J Clin Invest 1977 ; 59 : 179-83 . 5 . Fretland DJ, Widomski DL, Zemaitis JL, Tsai BS, Djurie SW, Penning TD, Miyashiro JM, Bauer RF . 12(R)-Hydroxyeicosatetraenoic acid is a neutrophil chemoattractant in the cavine, lapine, murine and canine dermis . Prost Leuk Ess Fatty Acids Rev 1989 ; 37 : 79-81 . 6. Ratliff NB, Gerrard JM, White JG . Platelet-leukocyte interactions following arterial endothelial injury . Am J Pathol 1979 ; 96 : 567-580 . 7 . Morley DJ, Feuerstein IA . Adhesion of polymorphonuclear leukocytes to protein-coated and platelet adherent surfaces . Thromb Haemost 1989 ; 62 : 1023-8 . 8 . Tzeng DY, Deuel TF, Huang JS, Senior RM, Boxer LA, Baehner RL . Platelet-derived growth factor promotes polymorphonuclear leukocyte activation . Blood 1984 ; 64 : 1123-8 . 9 . Boogaerts MA, Yamada 0, Jacob HS, Moldow CF . Enhancement of granulocyteendothelial cell adherence and granulocyte-induced cytotoxicity by platelet release products . Proc Natl Acad Sci USA 1982 ; 79 : 7019-23 . 10 . Spagnuolo PJ, Ellner JJ, Hassd A, Dunn MJ . Thromboxane A2 mediates augmented polymorphonuclear leukocyte adhesiveness . J Clin Invest 1980 ; 66 : 406-14 . 11 . Maclouf J, Fruteau de Laclos B, Borgeat P . Stimulation of leukotriene biosynthesis in human blood leukocytes by platelet-derived 12-hydroperoxy-icosatetraenoic acid . Prod Natl Acad Sci USA 1982 ; 79 : 6042-6 . 12 . Maclouf AJ, Murphy RC . Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets . J Biol Chem 1988 ; 263 : 174-81 . 13 . Mullane K . Neutrophil-platelet interactions and post-ischemic myocardial injury . It) : Schroer K, Sinzinger H, eds . Prostaglandins in clinical research : cardiovascular system . New York : Alan Liss, 1989 : 289-315 .
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Pharmacological Research, Vol . 26, No . 3, 1992
14 . Sakamoto H, Yokoya Y . Purification and characterization of macromolecular phagocytosis activators released from platelets . J Leak Biol 1991 ; 50 : 356-63 . 15 . Ward PA, Cunningham TW, McCulloch KK, Phan SH, Powell J, Johnson KJ . Platelet enhancement of Oz_ responses in stimulated human neutrophils . Lab Invest 1988 ; 58 : 37-47 . 16. Hamburger SA, McEver RP . GMP-140 mediates adhesion of stimulated platelets to neutrophils . Blood 1990 ; 75 : 550-4. 17 . Picker LJ, Warnock RA, Burns AR, Doerschuk CM, Berg EL, Butcher EC . The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell 1991 ; 66 : 921-33 . 18 . Ward PA . Mechanisms of endothelial cell injury . J Lab Clin Med 1991 ; 118 : 421-6 . 19 . Vane JR, Angaard EE, Botting RM . Regulatory functions of the vascular endothelium . N Engl J Med 1990 ; 323 : 27-36 . 20. Cerletti C, Evangelista V, de Gaetano G . Polymorphonuclear leukocyte-dependent modulation of platelet function : relevance to the pathogenesis of thrombosis . Pharmacol Res 1992 ; 26 : 261-8 . 21 . Bednar M, Smith B, Pinto A, Mullane KM . Neutrophil depletion suppresses "' In-labeled platelet accumulation in infarcted myocardium . J Cardiovasc Pharmacol 1985 ; 7: 906-12 . 22 . Issekutz AC, Ripley M, Jackson JR . Role of neutrophils in the deposition of platelets during acute inflammation . Lab Invest 1983 ; 49 : 716-24 . 23 . Morley J, Sanjar S, Page CP . The platelet in asthma . Lancet 1984; ii : 1142-4 . 24. Johnson RJ, Alpers CE, Pritzl P, Schulze M, Baker P, Pruchno C, Couser WG . Platelets mediate neutrophil-dependent immunecomplex nephritis in the rat . J Clin Invest 1988 ; 82 :1225-35 . 25 . Benveniste J, Henson PM, Cochrane CG . Leukocyte-dependent histamine release from rabbit platelets . The role of IgE, basophils, and a platelet-activating factor . J Exp Med 1972 ;136 :1356-77 . 26 . Vargaftig BB, Lefort J, Chignard M, Benveniste J . Platelet-activating factor induces a platelet-dependent bronchoconstriction unrelated to the formation of prostaglandin derivatives . Eur J Pharmacol 1980 ; 65 : 185-92 . 27 . Fava RA, Olsen N, Postlethwaite AE, Broadley KN, Davidson JM, Nanney LB, Lucas C, Townes AS . Transforming growth factor p1 (TGF-(31) induced neutrophil recruitment to synovial tissues : implication for TGF-(3-driven synovial inflammation and hyperplasia . J Exp Med 1991 ; 173 : 1121-32 . 28 . Moon DG, van Der Zee H, Weston LK, Gudewicz PW, Fenton II JW, Kaplan JE . Platelet modulation of neutrophil superoxide anion production . Thromb Haemost 1990 ; 63 : 91-6 . 29 . Dallegri F, Ballestrero A, Ottonello L, Patrone F . Platelets as inhibitory cells in neutrophil-mediated cytolysis . J Lab Clin Med 1989 ; 114 : 502-9 . 30 . Gamble JR, Vadas MA . Endothelial adhesiveness for blood neutrophils is inhibited by transforming growth factor-(3 . Science 1988 ; 242 : 97-9 . 31 . Iwabuchi K, Yamashita T . Platelet-derived adherence-inhibiting factor in humans . Blood 1990 ;76 :2368-73 . 32 . Gamble JR, Skinner MP, Berndt MC, Vadas MA . Prevention of activated neutrophil adhesion to endothelium by soluble adhesion protein GMP 140 . Science 1990 ; 249 : 414-7 . 33 . Wilson E, Laster SM, Gooding LR, Lambeth JD . Platelet-derived growth factor stimulates phagocytosis and blocks agonist-induced activation of the neutrophil respiratory burst : a possible cellular mechanism to protect against oxigen radical damage . Proc Nat Acad Sci USA 1987 ; 84 : 2213-7 . 34 . Wong CS, Gamble JR, Skinner MP, Lucas CM, Berndt MC, Vadas MA . Adhesion protein GMP140 inhibits superoxide anion release by human neutrophils . Proc Natl Acad Sci USA 1991 ; 88 : 2397-401 .
