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Thromb Haemost 1990; 63(01): 091-096
DOI: 10.1055/s-0038-1645693
Original Article
Schattauer GmbH Stuttgart

Platelet Modulation of Neutrophil Superoxide Anion Production

Dudley G Moon
The Department of Physiology and cell Biology, Albany Medical College, Albany, New York, USA
,
Hoyte van Der Zee
*   The Department of Anesthesiology, Albany Medical College, Albany, New York, USA
,
Lisa K Weston
The Department of Physiology and cell Biology, Albany Medical College, Albany, New York, USA
,
Paul W Gudewicz
The Department of Physiology and cell Biology, Albany Medical College, Albany, New York, USA
,
John W Fenton II
**   Wadsworth Center for Laboratories and Resarch, New York State Department of Health, Albany, New York, USA
,
John E Kaplan
The Department of Physiology and cell Biology, Albany Medical College, Albany, New York, USA
› Author Affiliations
Further Information

Publication History

Received 21 April 1988

Accepted after revision12 October 1989

Publication Date:
02 July 2018 (online)

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Summary

The effect of platelets on polymorphonuclear leukocytes (PMN) O− 2 production was examined using autologous sheep and human cell systems. Coincubation of sheep platelets with sheep PMNs in the absence of thrombin resulted in a significant inhibition in basal PMN O− 2 production. The platelet-derived inhibitory activity was released into the medium and could be destroyed by adenosine deaminase suggesting that the inhibitor was adenosine. Addition of alpha-thrombin or platelet activating factor (PAF) enhanced PMN O− 2 production but only when platelets were present. The enhancement of O− 2 production in response to thrombin was dependent upon the thrombin concentration and the platelet-PMN ratio. With a platelet:PMN ratio of 30:1, addition of 10 nM thrombin to sheep cells resulted in a 5-fold increase in O− 2 production, whereas addition of 10 nM PAF caused a 2-fold increase in O− 2. Addition of thrombin or PAF to either PMNs or platelets by themselves did not initiate an increase in O− 2 generation. The response of human cells was similar except that both thrombin and PAF triggered a 2-fold increase in PMN O− 2 production in the presence of platelets. The platelet-derived enhancement activity was not released into the medium and was not blocked by WEB 2086, NDGA, ETYA, aspirin or adenosine deaminase. The enhancement effect appeared to be localized to the platelet membrane and we believe requires platelet-PMN contact.

Keywords

Platelet - neutrophil interactions - Oxygen radicals
 

  • References

  • 1 Jungi TW, Spycher MO, Nydegger VE, Barandon S. Platelet-leukocyte interaction, selective binding of thrombin-stimulated platelets to human monocytes, polymorphonuclear leukocytes and related cell lines. Blood 1986; 67: 629-636
    PubMedGoogle Scholar
  • 2 Kjeldsberg CR, Swanson J. Platelet satdlitism. Blood 1974; 13: 831-836
    PubMedGoogle Scholar
  • 3 Yoo D, Weems H, Lessin LS. Platelet-to-leukocyte adherence phenomena. Platelet satellitism and phagocytosis by neutrophiE associated with in vitro platelet dysfunction. Acta Haematol 1982 68. 142-148
    PubMedGoogle Scholar
  • 4 Redl H, Hammerschmidt DE, Schlag G. Augmentation by platelets of granulocyte aggregation in response to chemotaxins. Blood 1983; 61: 125-131
    PubMedGoogle Scholar
  • 5 Rhee B-G, Hall ER, McIntire LV. Platelet modulation of polymorphonuclear leukocyte shear induced aggregation. Blood 1986; 67: 240-246
    PubMedGoogle Scholar
  • 6 Rasp FL, Clawson CC, Repine JE. Plaleleis increase neutrophil adherence in vitro to nylon fiber. J Lab Clin Med 1981; 97: 812-819
    PubMedGoogle Scholar
  • 7 Clawson CC. Modification of neutrophil function by platelets. In: Platelets: Production, Function, Transfusion and Storage Baldini M, Ebbe S. eds Grune & Stratton; New York: 1974: 287-297
  • 8 Tahamont MV, Malik AB. Granulocytes mediate the increase in pulmonary vascular permeability after thrombin embolism. J Appl Physiol 1983; 54: 1489-1495
    CrossrefPubMedGoogle Scholar
  • 9 Till GO, Johnson KJ, Kunkel R, Ward PA. Intravascular activation of complement and acute lung injury: Dependency on neutrophils and toxic oxygen metabolites. J Clin Invest 1982; 69: 1126-1135
    CrossrefPubMedGoogle Scholar
  • 10 Zimmerman GA, McIntyre TM, Prescott SM. Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Invest 1985; 76: 2235-2246
    CrossrefPubMedGoogle Scholar
  • 11 Malik AB, Lo SK, Bizios R. Thrombin-induced alterations in endothelial permeability. New York Acad Sci 1986; 485: 293-309
    CrossrefPubMedGoogle Scholar
  • 12 Minnear FL, Martin D, Hill L, Taylor AE, Malik AB. Pulmonary morphologic and vascular permeability changes induced by intravascular coagulation in the dog. Am J Physiol 1987; 253: H634-H644
    PubMedGoogle Scholar
  • 13 Burhop KE, Garcia JG N, Selig WM, Lo SK, van der ZeeH, Kaplan JE, Malik AB. Platelet-activating factor increases lung vascular permeability to protein. J Appl Physiol 1986; 61: 2210-2217
    CrossrefPubMedGoogle Scholar
  • 14 Corash L, Tan H, Gralnick HR. Heterogeneity of human whole blood platelet population. I. Relationship between bouyant density, cell volume and ultrastructure. Blood 1977 49. 71-87
    PubMedGoogle Scholar
  • 15 Fenton II JW, Fasco MJ, Strackrow AB. Human thrombins Production, evaluation and properties of alpha-thrombin. J Biol Chem 1977; 252: 3587-3598
    PubMedGoogle Scholar
  • 16 Moon DG, Kaplan JE, Mazurkiewicz JE. The inhibitory effect of plasma fibronectin on collagen-induced platelet aggregation. Blood 1986; 67: 450-457
    PubMedGoogle Scholar
  • 17 Bjorkman SE. A new method for enumeration of platelets. Acta Haematol 1959; 22: 377-379
    CrossrefPubMedGoogle Scholar
  • 18 Boyum A. Separation of leukocytes from blood and bone marrow. Scand J Clin Lab Invest 1968; (Suppl. 97) 21: 77-89
    CrossrefPubMedGoogle Scholar
  • 19 Roth JA, Keiberle ML. Isolation of neutrophils and eosinophils from the peripheral blood of cattle. J Immunol Methods 1981; 45: 153-164
    CrossrefPubMedGoogle Scholar
  • 20 Babior BM, Kipnes RS, Curnette JT. Biological defense mechanisms: The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 1973; 52: 741-744
    CrossrefPubMedGoogle Scholar
  • 21 Sokal RR, Rohlf FJ. Biometry. 2nd ed WH Freeman; San Francisco: 1981
    Google Scholar
  • 22 McGarrity ST, Stephenson AH, Hyers TM, Webster RO. Inhibition of neutrophil superoxide anion generation by platelet products: Role nf adenine nucleotides. J Leukocyte Biol 1988; 44: 411-421
    CrossrefPubMedGoogle Scholar
  • 23 Cronstein BN, Rosenstein ED, Kramer SB, Weissman G, Himchhorn R. Adenosine: a pliysiolugical modulator ol superoxide anion generation by human neutrophils. Adenosine acts via an A2 receptor on human neutrophils. I Immunol 1985 135. 1366-1371
    PubMedGoogle Scholar
  • 24 Wilson E, Easter SM, Gooding IR, Lambeth JD. Platelet-derived growth factor stimulates phagocytosis and blocks agonist-induced activation of the neutiophil oxidative burst: A possible cellular mechanism to protect against oxygen radical damage. Proc Natl Acad Sci 1987; 84: 2213-2217
    CrossrefPubMedGoogle Scholar
  • 25 Ward PA, Cunningham TW, McCulloch KK, Phan SH, Powell J, Johnson KJ. Platelet enhancement of O2 responses in stimulated human neutrophils: Identification of platelet factor as adenine nucleotide. Lab Invest 1988; 58: 37-47
    PubMedGoogle Scholar
  • 26 Del Masehio A, Cnrvazier E, Maillet b, Kazatchkine MD, Macloud J. Platelet-dependent induction and amplification of polymorphonuclear leucocyte lysosomal enzyme release. Dr J Haematol 1989; 72: 329-335
    PubMedGoogle Scholar
  • 27 Goldstein TM, Roos D, Kaplan II B, Weissman G. Complement and immunoglobulins stimulate superoxide production by human leukocytes independently of phagocytosis. J Clin Invest 1975; 56: 1155-1163
    CrossrefPubMedGoogle Scholar
  • 28 Lo SK, Perlman MB, Niehaus G, Malik AB. Thrombin-induced alterations in lung fluid balance in awake sheep. J Appl Physiol 1985; 58: 1421-1427
    CrossrefPubMedGoogle Scholar
  • 29 Johnson A, Perlman MB, Blumenstock FA, Malik AB. Superoxide dismutase prevents the thrombin-induced increase in lung vascular permeability: Role of superoxide in mediating the alterations in lung fluid balance. Circ Res 1986; 59: 405-415
    CrossrefPubMedGoogle Scholar
  • 30 Tvedten HW, Till GO, Ward PA. Mediators of lung injury in mice following systemic activation of complement. Am J Pathol 1985; 119: 92-100
    PubMedGoogle Scholar