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January 1994, Vol 129, No. 1 >
ARTICLE | January 1994

Exudative Neutrophils: Title and subTitle BreakModulation of Microbicidal Function in the Inflammatory Microenvironment FREE

John Yee, MD; Betty Giannias; Bomi Kapadia; Louise Chartrand, RN; Nicolas V. Christou, MD, PhD, FRCSC
Arch Surg. 1994;129(1):99-105. doi:10.1001/archsurg.1994.01420250111014
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Objective:  To determine whether the inflammatory microenvironment primes neutrophils for increased microbicidal activity.

Design:  In vitro studies of host defense were performed on surgical patients.

Setting:  A tertiary care, university hospital.

Patients:  A volunteer sample of hospitalized preoperative, noninfected surgical patients.

Intervention:  Exudative neutrophils were collected from skin-blister chambers and functionally compared with circulating neutrophils.

Methods:  Flow cytometry was used to evaluate directly neutrophil microbicidal activity (using fluoresceinated Candida albicans), formyl-methionyl-leucyl-phenylalanine (fMLP)-induced superoxide production (using 123 dihydrorhodamine), and surface expression of CDllb, CD16, and the fMLP receptor. In vitro tumor necrosis factor α was used to determine the possibility and extent of further priming in both circulating and exudative neutrophils.

Results:  Exudative polymorphonuclear neutrophils have enhanced microbicidal activity, superoxide production, and expression of CDllb, CD16, and the fMLP receptor. Exogenous tumor necrosis factor was able to prime circulating neutrophils but did not further augment superoxide production in exudative neutrophils.

Conclusion:  The microbicidal activity of neutrophils is enhanced after exudation and is associated with neutrophil priming. The inability of exogenous tumor necrosis factor to further augment superoxide production after exudation suggests that this priming has been maximized.(Arch Surg. 1994;129:99-105)

REFERENCES

1 +
Sha'afi R,  Molski TFP Activation of the neutrophil . Prog Allergy . 1988;;42:1-64.
2 +
Zimmerli W, Seligman B, Gallin JI.  Exudation primes human and guinea pig neutrophils for subsequent responsiveness to the chemotactic peptide N-formylmethionylleucylphenylalanine and increases complement component C3bi receptor expression . J Clin Invest . 1986;;77:925-933.
3 +
Zimmerli W, Lew PD, Cohen HJ, Waldvogel FA.  Comparative superoxide generating system of granulocytes from blood and peritoneal exudates . Infect Immun . 1984;;46:625-630.
4 +
Van Epps DE, Garcia ML.  Enhancement of neutrophil function as a result of prior exposure to chemotactic factor . J Clin Invest . 1980;;66:167-175.
5 +
Wright DG, Gallin Jl.  Secretory responses of human neutrophils . J Immunol . 1979;;123:235-294.
6 +
Paty PB, Graeff RW, Mathes SJ, Hunt TK.  Superoxide production by wound neutrophils . Arch Surg . 1990;;125:65-69.
7 +
Paty PB, Graeff RW, Waldman FM, Hunt TK, Mathes SJ.  Biologic priming of neutrophils in subcutaneous wounds . Arch Surg . 1988;;123:1509-1513.
8 +
Nurcombe HL, Bucknall RC, Edwards SW.  Neutrophils isolated from the synovial fluid of patients with rheumatoid arthritis . Ann Rheum Dis . 1991;;50:147-153.
9 +
Holman RG, Maier RV.  Superoxide production by neutrophils in a model of adult respiratory distress syndrome . Arch Surg . 1988;;123:1491-1495.
10 +
Biasi D, Bambara LM, Carletto A, et al.  Factor-specific changes in oxidative burst response of human neutrophils in skin-window exudates . Inflammation . 1993;;17:13-23.
11 +
Rokke O, Revhaug A, Giercksky K-E.  Polymorphonuclear leukocyte activation after trauma . Acta Chir Scand . 1989;;155:233-239.
12 +
Deitch EA, Lu Q, Xu DZ, Specian RD.  Effect of local and systemic burn microenvironment on neutrophil activation as assessed by complement receptor expression and morphology . J Trauma . 1990;;30:259-268.
13 +
Forehand JR, Pabst MJ, Phillips WA, Johnston RB Jr.  Lipopolysaccharide priming of human neutrophils for an enhanced respiratory burst . J Clin Invest . 1989;;83:74-83.
14 +
Guthrie LA, McPhail LC, Henson PM, Johnston RB Jr.  Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide . J Exp Med . 1984;;160:1654-1671.
15 +
Aida Y, Pabst MJ.  Priming of neutrophils by lipopolysaccharide or enhanced release of superoxide . J Immunol . 1990;;145:3017-3025.
16 +
Vosbeck K, Tobias P, Mueller H, et al.  Priming of polymorphonuclear granulocytes by lipopolysaccharides and its complexes with lipopolysaccharide binding protein and high density lipoprotein . J Leukoc Biol . 1990;;47:97-104.
17 +
Berkow RL, Wang D, Larrick JW, Dodson RW, Howard TH.  Enhancement of neutrophil superoxide production by pre-incubation with recombinant human tumor necrosis factor . J Immunol . 1987;;139:3783-3791.
18 +
Tennenberg SD, Solomkin JS.  Activation of neutrophils by cachectin/tumor necrosis factor . J Leukoc Biol . 1990;;47:217-223.
19 +
Kharazmi A, Nielsen H, Rechnitzer C, Bendtzen K.  Interleukin 6 primes human neutrophil and monocyte oxidative burst response . Immunol Lett . 1989;;21:177-184.
20 +
Daniels RH, Finnen MJ, Hill ME, Lackie JM.  Recombinant human monocyte IL-8 primes NADPH-oxidase and phospholipase A2 activation in human neutrophils . Immunology . 1991;;75:157-163.
21 +
Gay JC, Beckman JK, Brash AR, Oates JA, Lukens JN.  Enhancement of neutrophil oxidative metabolism by leukotriene B4 . Blood . 1984;;64:780-785.
22 +
Gay JC.  Priming of neutrophil oxidative responses by platelet-activating factor . J Lipid Mediat . 1990;;2( (suppl) ):S161-S175.
23 +
Fu K, Arkins S, Fuh G, et al.  Growth hormone augments superoxide anoin secretion of human neutrophils by binding to the prolactin receptor . J Clin Invest . 1992;; 89:451-457.
24 +
Khwaja A, Carver JE, Linch DC.  Interactions of granulocyte-macrophage colony-stimulating factor (CSF), granulocyte CSF, and tumor necrosis factor alpha in the priming of the neutrophil respiratory burst . Blood . 1992;;79:745-753.
25 +
Ginis I, Tauber Al.  Activation mechanisms of adherent human neutrophils . Blood . 1990;;76:1233-1239.
26 +
Zimmerli W, Reber A-M, Dahinden CA.  The role of formylpeptide receptors, C5a receptors, and cytosolic-free calcium in neutrophil priming . J Infect Dis . 1990;;161:242-249.
27 +
Axtell RA, Sandborg RR, Smolen JE, Ward PA, Boxer LA.  Exposure of human neutrophils to exogenous nucleotides causes elevation in intracellular calcium, transmembrane calcium fluxes, and an alteration of a cytosolic factor resulting in enhanced superoxide production in response to fMLP and arachidonic acid . Blood . 1990;;75:1324-1332.
28 +
Yee J, Christou NV.  Neutrophil priming by lipopolysaccharide involves heterogeneity in calcium-mediated signal transduction . J Immunol . 1993;;150:1988-1997.
29 +
Haslett C, Guthrie LA, Kopianiak MM, Johnston RB Jr.  Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide . Am J Pathol . 1985;;119:101-110.
30 +
Bjerknes R.  Flow cytometric assay for combined measurement of phagocytosis and intracellular killing of Candida albicans . J Immunol Methods . 1984;;72:229-241.
31 +
Rothe G, Oser A, Valet G.  Dihydrorhodamine 123 . Naturwissenschaften . 1988;;75:354-355.
32 +
Emmendorffer A, Hecht M, Lohmann-Matthes M-L, Roessler J.  A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123 . J Immunol Methods . 1990;;131:269-275.
33 +
Zimmerman GA, Prescott SM, McIntyre TM.  Endothelial cell interactions with granulocytes: tethering and signaling molecules . Immunol Today . 1992;;13:93-100.
34 +
Norgauer J, Eberle M, Fay SP, Lemke HD, Sklar LA.  Kinetics of N-formyl peptide receptor up-regulation during stimulation in human neutrophils . J Immunol . 1991;; 146:975-980.
35 +
Wright SD, Ramos RA, Hermanowski-Vosatka A, Rockwell P, Detmers PA.  Activation of the adhesive capacity of CR3 on neutrophils by endotoxin . J Exp Med . 1991;;173:1281-1286.
36 +
Macey MG, Jiang XP, Veys P, McCarthy D, Newland AC.  Expression of functional antigens on neutrophils . J Immunol Methods . 1992;;149:37-42.
37 +
Porteu F, Nathan C.  Shedding of tumor necrosis factor receptors by activated human neutrophils . J Exp Med . 1990;;172:599-607.

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1 +
Sha'afi R,  Molski TFP Activation of the neutrophil . Prog Allergy . 1988;;42:1-64.
2 +
Zimmerli W, Seligman B, Gallin JI.  Exudation primes human and guinea pig neutrophils for subsequent responsiveness to the chemotactic peptide N-formylmethionylleucylphenylalanine and increases complement component C3bi receptor expression . J Clin Invest . 1986;;77:925-933.
3 +
Zimmerli W, Lew PD, Cohen HJ, Waldvogel FA.  Comparative superoxide generating system of granulocytes from blood and peritoneal exudates . Infect Immun . 1984;;46:625-630.
4 +
Van Epps DE, Garcia ML.  Enhancement of neutrophil function as a result of prior exposure to chemotactic factor . J Clin Invest . 1980;;66:167-175.
5 +
Wright DG, Gallin Jl.  Secretory responses of human neutrophils . J Immunol . 1979;;123:235-294.
6 +
Paty PB, Graeff RW, Mathes SJ, Hunt TK.  Superoxide production by wound neutrophils . Arch Surg . 1990;;125:65-69.
7 +
Paty PB, Graeff RW, Waldman FM, Hunt TK, Mathes SJ.  Biologic priming of neutrophils in subcutaneous wounds . Arch Surg . 1988;;123:1509-1513.
8 +
Nurcombe HL, Bucknall RC, Edwards SW.  Neutrophils isolated from the synovial fluid of patients with rheumatoid arthritis . Ann Rheum Dis . 1991;;50:147-153.
9 +
Holman RG, Maier RV.  Superoxide production by neutrophils in a model of adult respiratory distress syndrome . Arch Surg . 1988;;123:1491-1495.
10 +
Biasi D, Bambara LM, Carletto A, et al.  Factor-specific changes in oxidative burst response of human neutrophils in skin-window exudates . Inflammation . 1993;;17:13-23.
11 +
Rokke O, Revhaug A, Giercksky K-E.  Polymorphonuclear leukocyte activation after trauma . Acta Chir Scand . 1989;;155:233-239.
12 +
Deitch EA, Lu Q, Xu DZ, Specian RD.  Effect of local and systemic burn microenvironment on neutrophil activation as assessed by complement receptor expression and morphology . J Trauma . 1990;;30:259-268.
13 +
Forehand JR, Pabst MJ, Phillips WA, Johnston RB Jr.  Lipopolysaccharide priming of human neutrophils for an enhanced respiratory burst . J Clin Invest . 1989;;83:74-83.
14 +
Guthrie LA, McPhail LC, Henson PM, Johnston RB Jr.  Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide . J Exp Med . 1984;;160:1654-1671.
15 +
Aida Y, Pabst MJ.  Priming of neutrophils by lipopolysaccharide or enhanced release of superoxide . J Immunol . 1990;;145:3017-3025.
16 +
Vosbeck K, Tobias P, Mueller H, et al.  Priming of polymorphonuclear granulocytes by lipopolysaccharides and its complexes with lipopolysaccharide binding protein and high density lipoprotein . J Leukoc Biol . 1990;;47:97-104.
17 +
Berkow RL, Wang D, Larrick JW, Dodson RW, Howard TH.  Enhancement of neutrophil superoxide production by pre-incubation with recombinant human tumor necrosis factor . J Immunol . 1987;;139:3783-3791.
18 +
Tennenberg SD, Solomkin JS.  Activation of neutrophils by cachectin/tumor necrosis factor . J Leukoc Biol . 1990;;47:217-223.
19 +
Kharazmi A, Nielsen H, Rechnitzer C, Bendtzen K.  Interleukin 6 primes human neutrophil and monocyte oxidative burst response . Immunol Lett . 1989;;21:177-184.
20 +
Daniels RH, Finnen MJ, Hill ME, Lackie JM.  Recombinant human monocyte IL-8 primes NADPH-oxidase and phospholipase A2 activation in human neutrophils . Immunology . 1991;;75:157-163.
21 +
Gay JC, Beckman JK, Brash AR, Oates JA, Lukens JN.  Enhancement of neutrophil oxidative metabolism by leukotriene B4 . Blood . 1984;;64:780-785.
22 +
Gay JC.  Priming of neutrophil oxidative responses by platelet-activating factor . J Lipid Mediat . 1990;;2( (suppl) ):S161-S175.
23 +
Fu K, Arkins S, Fuh G, et al.  Growth hormone augments superoxide anoin secretion of human neutrophils by binding to the prolactin receptor . J Clin Invest . 1992;; 89:451-457.
24 +
Khwaja A, Carver JE, Linch DC.  Interactions of granulocyte-macrophage colony-stimulating factor (CSF), granulocyte CSF, and tumor necrosis factor alpha in the priming of the neutrophil respiratory burst . Blood . 1992;;79:745-753.
25 +
Ginis I, Tauber Al.  Activation mechanisms of adherent human neutrophils . Blood . 1990;;76:1233-1239.
26 +
Zimmerli W, Reber A-M, Dahinden CA.  The role of formylpeptide receptors, C5a receptors, and cytosolic-free calcium in neutrophil priming . J Infect Dis . 1990;;161:242-249.
27 +
Axtell RA, Sandborg RR, Smolen JE, Ward PA, Boxer LA.  Exposure of human neutrophils to exogenous nucleotides causes elevation in intracellular calcium, transmembrane calcium fluxes, and an alteration of a cytosolic factor resulting in enhanced superoxide production in response to fMLP and arachidonic acid . Blood . 1990;;75:1324-1332.
28 +
Yee J, Christou NV.  Neutrophil priming by lipopolysaccharide involves heterogeneity in calcium-mediated signal transduction . J Immunol . 1993;;150:1988-1997.
29 +
Haslett C, Guthrie LA, Kopianiak MM, Johnston RB Jr.  Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide . Am J Pathol . 1985;;119:101-110.
30 +
Bjerknes R.  Flow cytometric assay for combined measurement of phagocytosis and intracellular killing of Candida albicans . J Immunol Methods . 1984;;72:229-241.
31 +
Rothe G, Oser A, Valet G.  Dihydrorhodamine 123 . Naturwissenschaften . 1988;;75:354-355.
32 +
Emmendorffer A, Hecht M, Lohmann-Matthes M-L, Roessler J.  A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123 . J Immunol Methods . 1990;;131:269-275.
33 +
Zimmerman GA, Prescott SM, McIntyre TM.  Endothelial cell interactions with granulocytes: tethering and signaling molecules . Immunol Today . 1992;;13:93-100.
34 +
Norgauer J, Eberle M, Fay SP, Lemke HD, Sklar LA.  Kinetics of N-formyl peptide receptor up-regulation during stimulation in human neutrophils . J Immunol . 1991;; 146:975-980.
35 +
Wright SD, Ramos RA, Hermanowski-Vosatka A, Rockwell P, Detmers PA.  Activation of the adhesive capacity of CR3 on neutrophils by endotoxin . J Exp Med . 1991;;173:1281-1286.
36 +
Macey MG, Jiang XP, Veys P, McCarthy D, Newland AC.  Expression of functional antigens on neutrophils . J Immunol Methods . 1992;;149:37-42.
37 +
Porteu F, Nathan C.  Shedding of tumor necrosis factor receptors by activated human neutrophils . J Exp Med . 1990;;172:599-607.

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