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Thromb Haemost 1989; 62(04): 1121-1125
DOI: 10.1055/s-0038-1647130
Original Article
Miscellaneous
Schattauer GmbH Stuttgart

Purified Human Plasma Kallikrein Does Not Stimulate but Primes Neutrophils for Superoxide Production

Werner Zimmerli
1   The Department of Research, University Hospital Basel, Switzerland
,
Isabelle Huber
2   The Central Hematology Laboratory, Inselspital, University of Bern, Switzerland
,
Bonno N Bouma
3   The Department of Hematology, University Hospital Utrecht, The Netherlands
,
Bernhard Lämmle
2   The Central Hematology Laboratory, Inselspital, University of Bern, Switzerland
› Author Affiliations
Further Information

Publication History

Received 03 May 1989

Accepted after revision 18 August 1989

Publication Date:
24 July 2018 (online)

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Summary

In patients with septicemia and septic shock the contact phase of blood coagulation is activated. It has been suggested that polymorphonuclear leukocytes (PMN) are directly activated by purified plasma kallikrein. This has been recently questioned because granulocytic elastase release induced by recalcification of normal and prekallikrein-deficient plasma was similar. We studied the interaction of different preparations of purified human plasma kallikrein with PMN. Cytosolic calcium shifts were measured with the quin2 method, PMN aggregation was assayed in an aggregometer, and superoxide production was quantitated as superoxide dismutase inhibitable cytochrome c reduction in a continuous assay. No increase of cytosolic free calcium was found during at least 5 min after adding 10 μg/ml plasma kallikrein to PMN. Similarly, highly purified plasma kallikrein from two different sources did not induce PMN aggregation at all, nor did it stimulate superoxide production. However, sequential exposure of PMN to plasma kallikrein and formylpeptide increased the superoxide production compared to stimulation with formylpeptide alone. This phenomenon which is called priming was observed at plasma kallikrein concentrations ≥7 μg/ml. The active site of the molecule was required for the priming, because plasma prekallikrein, active site-inactivated plasma kallikrein, and soybean trypsin inhibitor treated kallikrein did not prime PMN. This indicates that the contact activation system may play a role in host defence against bacterial infection.

Keywords

Neutrophils - Kallikrein - Priming
 

  • References

  • 1 Mason JW, Kleeberg U, Dolan P, Colman RW. Plasma kallikrein and Hageman factor in gram-negative bacteremia. Ann Intern Med 1970; 73: 545-551
    CrossrefPubMedGoogle Scholar
  • 2 Colman RW, Wong PY. Participation of Hageman factor dependent pathways in human disease states. Thromb Haemostas 1977; 38: 751-775
    PubMedGoogle Scholar
  • 3 Ratnoff OD, Saito H. Surface-mediated reactions. Curr Top Hematol 1979; 02: 001-057
    PubMedGoogle Scholar
  • 4 Kalter ES, Timmermans A, Bouma BN. The kinin generating system during sepsis and bacterial shock. Agents Actions 1982; 09 Suppl 638-644
    PubMedGoogle Scholar
  • 5 Lämmie B, Tran TH, Ritz R, Duckert F. Plasma prekallikrein, factor XII, antithrombin III, C1-inhibitor and α2-macroglobulin in critically ill patients with suspected disseminated intravascular coagulation (DIC). Am J Clin Pathol 1984; 82: 396-404
    CrossrefPubMedGoogle Scholar
  • 6 Aasen AO, Smith-Erichsen N, Amundsen E. Plasma kallikrein-kinin system in septicemia. Arch Surg 1983; 118: 343-346
    CrossrefPubMedGoogle Scholar
  • 7 Saito H, Goldsmith G, Waldmann R. Fitzgerald factor (high molecular weight kininogen) clotting activity in human plasma in health and disease and in various animal plasmas. Blood 1976; 48: 941-947
    PubMedGoogle Scholar
  • 8 Hirsch EF, Nakajima T, Oshima G, Erdös EG, Herman CM. Kinin system responses in sepsis after trauma in man. J Surg Res 1974; 17: 147-153
    CrossrefPubMedGoogle Scholar
  • 9 Colman RW, Edelman R, Scott CF, Gilman RH. Plasma kallikrein activation and inhibition during typhoid fever. J Clin Invest 1978; 61: 287-296
    CrossrefPubMedGoogle Scholar
  • 10 Zimmerli W, Reber A-M. Mechanisms of neutrophil (PMN) priming by endotoxin-activated-serum. 5th International Symposium of Infections in the immunocompromised host, Noordwijkerhout (NL) 05.06.1988 (Abstr)
    PubMedGoogle Scholar
  • 11 Guthrie LA, McPhail LC, Henson PM, Johnston RB. Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. J Exp Med 1984; 160: 1656-1671
    CrossrefPubMedGoogle Scholar
  • 12 Larrick JW, Graham D, Toy K, Lin LS, Senyk G, Fendly BM. Recombinant tumor necrosis factor causes activation of human granulocytes. Blood 1987; 69: 640-644
    PubMedGoogle Scholar
  • 13 Bender JG, McPhail LC, Van Epps DE. Exposure of human neutrophils to chemotactic factors potentiates activation of the respiratory burst enzyme. J Immunol 1983; 130: 2316-2323
    PubMedGoogle Scholar
  • 14 Gustafson EJ, Colman RW. Interaction of polymorphonuclear cells with contact activation factors. Sem Thromb Hemostas 1987; 13: 095-105
    Article in Thieme ConnectPubMedGoogle Scholar
  • 15 Schapira M, Despland E, Scott CF, Boxer LA, Colman RW. Purified human plasma kallikrein aggregates human blood neutrophils. J Clin Invest 1982; 69: 1199-1202
    CrossrefPubMedGoogle Scholar
  • 16 Wachtfogel YT, Kucich U, James HL, Scott CF, Schapira M, Zimmerman M, Cohen AB, Colman RW. Human plasma kallikrein releases neutrophil elastase during blood coagulation. J Clin Invest 1983; 72: 1672-1677
    CrossrefPubMedGoogle Scholar
  • 17 Wachtfogel YT, Pixley RA, Kucich U, Abrams W, Weinbaum G, Schapira M, Colman RW. Purified plasma factor XIIa aggregates human neutrophils and causes degranulation. Blood 1986; 67: 1731-1737
    PubMedGoogle Scholar
  • 18 Plow EF, Plescia J. Neutrophil secretion during blood coagulation: Evidence for a prekallikrein independent pathway. Thromb Haemostas 1988; 59: 360-363
    PubMedGoogle Scholar
  • 19 Metcalf JA, Gallin JI, Nauseef WM, Root RK. Laboratory Manual of Neutrophil Function. 1. Raven Press; New York: 1986: 191 pp
    Google Scholar
  • 20 Hugli TE, Gerard C, Kawahara M, Scheetz II ME, Barton R, Briggs S, Koppel G, Russel S. Isolation of three separate anaphylatoxins from complement-activated human serum. Mol Cell Biochem 1981; 41: 59-66
    PubMedGoogle Scholar
  • 21 Griffin JH, Cochrane CG. Human factor XII (Hageman factor). Methods Enzymol 1976; 45: 056-065
    PubMedGoogle Scholar
  • 22 Kerbiriou DM, Griffin JH. Human high molecular weight kininogen. Studies of structure-function relationships and of proteolysis of the molecule occurring during contact activation of plasma J Biol Chem 1979; 254: 12020-12027
    PubMedGoogle Scholar
  • 23 Van der Graaf F, Tuns G, Bouma BN, Griffin JH. Isolation and functional properties of the heavy and light chains of human plasma kallikrein. J Biol Chem 1982; 257: 14300-14305
    PubMedGoogle Scholar
  • 24 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193: 265-275
    PubMedGoogle Scholar
  • 25 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685
    CrossrefPubMedGoogle Scholar
  • 26 Burger G, Schleuning WD, Schapira M. Human plasma prekallikrein. Immunoaffinity purification and activation to α- and β-kallikrein J Biol Chem 1986; 261: 324-327
    PubMedGoogle Scholar
  • 27 Zimmerli W, Seligmann B, Gallin JI. Exudation primes human and guinea pig neutrophils for subsequent responsiveness to the chemotactic peptide N-formyl-thionyl-leucyl-phenylalanine and increases complement component C3bi receptor expression. J Clin Invest 1986; 33: 925-933
    PubMedGoogle Scholar
  • 28 Lew PD, Wollheim CB, Waldvogel FA, Pozzan T. Modulation of cytosolic-free calcium transients by changes in intracellular calciumbuffering capacity: Correlation with exocytosis and O2 −production in human neutrophils. J Cell Biol 1984; 99: 1212-1220
    CrossrefPubMedGoogle Scholar
  • 29 Zimmerli W, Lew PD, Waldvogel FA. Pathogenesis of foreign body infection. Evidence for a local granulocyte defect J Clin Invest 1984; 73: 1191-1200
    CrossrefPubMedGoogle Scholar
  • 30 Dinarello CA, Mier JW. Lymphokines. N Engl J Med 1987; 317: 940-945
    CrossrefPubMedGoogle Scholar
  • 31 Michie HR, Manogue KR, Spriggs DR, Revhaug A, O’Dwyer S, Dinarello CA, Cerami A, Wolff SM, Wilmore DW. Detection of circulating tumor necrosis factor after endotoxin administration. N Engl J Med 1988; 318: 1481-1486
    CrossrefPubMedGoogle Scholar
  • 32 Figari IS, Mori NA, Palladino MA. Regulation of neutrophil migration and superoxide production by recombinant tumor necrosis factors -α and -β: Comparison to recombinant interferon- and interleukin-1α. Blood 1987; 70: 979-984
    PubMedGoogle Scholar
  • 33 Fleischmann J, Golde DW, Weisbart RH, Gasson JC. Granulocytemacrophage colony-stimulating factor enhances phagocytosis of bacteria by human neutrophils. Blood 1986; 68: 708-711
    PubMedGoogle Scholar
  • 34 Roberts RL, Gallin JI. Rapid method for isolation of normal human peripheral blood eosinophils on discontinuous Percoll gradients and comparison with neutrophils. Blood 1985; 65: 433-440
    PubMedGoogle Scholar