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Two patterns of early neutrophil accumulation in acute inflammatory lesions

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Abstract

A model of acute inflammation in the skin of sheep was developed using111In]oxine-labeled neutrophils to quantify the accumulation of neutrophils in inflammatory lesions. Peak accumulation occurred during the first hour in lesions induced by zymosan-activated sheep plasma (ZAP, 100%) and during the second hour in lesions induced by endotoxin (10−11 moles) and casein (2 x 10−8 moles). The accumulation of neutrophils after the final stimulus diminished when lesions were restimulated every 2 h on two or more occasions. Thus desensitization of inflammatory lesions previously observed in rabbit skin is not restricted to that species. The early accumulation of neutrophils in primary and restimulated lesions was measured in lesions from 10 min to 2 h old. In primary lesions, ZAP induced significant neutrophil accumulation by 10 min, whereas 30 to 45 min elapsed before significant neutrophil accumulation occurred in lesions induced with endotoxin and casein. The initial responses in restimulated lesions were not diminished, but there was a failure of neutrophil accumulation to continue for as long as occurred in primary lesions. This finding indicates that regulation of the neutrophil influx into dermal inflammatory lesions may occur at a point after occupancy of the putative tissue receptors in the pathway which leads to accumulation of neutrophils at the injection site. The results indicate that there are at least two patterns of neutrophil accumulation in primary inflammatory lesions. The delayed pattern of neutrophil accumulation induced by casein and endotoxin resembles the enhanced binding of neutrophils to stimulated endothelial cultures in vitro, whereas the basis for the immediate response induced by ZAP remains conjectural. It is proposed that the primary action of chemotactic agents may be to provoke changes in the adhesive properties of endothelium and resident connective tissue cells thus permitting the migration of neutrophils into inflammatory lesions.

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References

  1. Colditz, I. G., andH. Z. Movat. 1984. Kinetics of neutrophil accumulation in acute inflammatory lesions induced by chemotaxins and chemotaxinigens.J. Immunol. 133:2168–2172.

    Google Scholar 

  2. Colditz, I. G., andM. I. Cybulsky. 1987. Some characteristics of inflammation induced by muramyl dipeptide, endotoxin and concanavalin A.Inflammation 11:1–11.

    Google Scholar 

  3. Cybulsky, M. I., I. G. Colditz, andH. Z. Movat. 1986. The role of interleukin-1 in neutrophil leukocyte emigration induced by endotoxin.Am. J. Pathol. 124:367–372.

    Google Scholar 

  4. Issekutz, A. C., andH. Z. Movat, 1980. The in vivo quantitation and kinetics of rabbit neutrophil leukocyte accumulation in the skin in response to chemotactic agents andEscherichia coli.Lab. Invest. 42:310–317.

    Google Scholar 

  5. Movat, H. Z., C. Rettl, C. E. Burrowes, andM. G. Johnson. 1984. The in vivo effect of leukotriene B4 on polymorphonuclear leukocytes and the microcirculation.Am. J. Pathol. 115:233–244.

    Google Scholar 

  6. Colditz, I. G., andH. Z. Movat. 1984. Desensitization of acute inflammatory lesions to chemotaxins and endotoxin.J. Immunol. 133:2163–2167.

    Google Scholar 

  7. Colditz, I. G., andH. Z. Movat. 1984. Chemotactic factor-specific desensitization of skin to infiltration by PMN-leukocytes.Immunol. Lett. 8:83–87.

    Google Scholar 

  8. Bevilacqua, M. P., J. S. Pober, M. E. Wheeler, R. S. Cotran, andM. A. Gimbrone. 1985. Interleukin-1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes and related leukocyte cell lines.J. Clin. Invest. 76:2003–2011.

    Google Scholar 

  9. Gamble, J. R., J. M. Harlan, S. J. Klebanoff, A. F. Lopez, andM. A. Vadas. 1985. Stimulation of the adherence of neutrophils to umbilical vein endothelium by human recombinant tumor necrosis factor.Proc. Natl. Acad. Sci. U.S.A. 82:8667–8671.

    Google Scholar 

  10. Schleimer, R. P., andB. K. Rutledge. 1986. Cultured human vascular endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumorpromoting phorbol diesters.J. Immunol. 136:649–654.

    Google Scholar 

  11. Colditz, I. G. 1985. Margination and emigration of leucocytes.Surv. Synth. Pathol. Res. 4:44–68.

    Google Scholar 

  12. Allison, F., M. R. Smith, andW. B. Wood. 1955. Studies on the pathogenesis of acute inflammation I. The inflammatory reaction to thermal injury as observed in the rabbit ear chamber.J. Exp. Med. 102:655–667.

    Google Scholar 

  13. Clark, E. R., E. L. Clark, andR. O. Rex. 1936. Observations on polymorphonuclear leukocytes in the living animal.Am. J. Anat. 59:123–173.

    Google Scholar 

  14. Issekutz, A. C., K. W. Movat, andH. Z. Movat. 1980. Enhanced vascular permeability and hemorrhage-inducing activity of rabbit C5a des arg: Probable role of polymorphonuclear leukocyte lysosomes.Clin. Exp. Immunol. 41:512–520.

    Google Scholar 

  15. Wedmore, C. V., andT. J. Williams. 1981. Control of vascular permeability by polymorphonuclear leukocytes in inflammation.Nature 289:646–650.

    Google Scholar 

  16. Cybulsky, M. I., I. J. Cybulsky, andH. Z. Movat. 1986. Neutropenic responses to intradermal injections ofEscherichia coli.Am. J. Pathol. 124:1–9.

    Google Scholar 

  17. Lackie, J. M., andR. P. C. Smith. 1980. Interactions of leukocytes and endothelium.In Cell Adhesion and Motility. Edited by A. S. G. Curtis and J. D. Pitts, editors. Cambridge University Press, Cambridge. 235.

    Google Scholar 

  18. Bjork, J., andG. Smedegard. 1983. Acute microvascular effects of PAF-acether, as studied by intravital microscopy.Eur. J. Pharmacol. 96:87–94.

    Google Scholar 

  19. Bjork, J., T. E. Hugli, andG. Smedgard. 1985. Microvascular effects of anaphylatoxins C3a andC5a.J. Immunol. 134:1115–1119.

    Google Scholar 

  20. Dahlen, S. E., J. Bjork, P. Hedqvist, K. E. Arfors, S. Hammerstrom, J. A. Lindgren, andB. Samuelsson. 1981. Leukotrienes promote vascular leakage and leukocyte adhesion in post capillary venules: In vivo effects with relevance to the acute inflammatory response.Proc. Natl. Acad. Sci. U.S.A. 78:3387–3891.

    Google Scholar 

  21. Hoover, R. L., R. Folger, W. A. Haering, B. R. Ware, andM. J. Karnovsky. 1980. Adhesion of leukocytes to endothelium: Roles of divalent cations, surface charge, chemotactic agents and substrate.J. Cell. Sci. 45:73–86.

    Google Scholar 

  22. Hoover, R. L., M. J. Karnovsky, K. F. Austen, E. J. Corey, andR. A. Lewis. 1984. Leukotriene B4 action on endothelium mediates augmented neutrophil/endothelial adhesion.Proc. Natl. Acad. Sci. U.S.A. 81:2191–2193.

    Google Scholar 

  23. Kirkpatrick, C. S., andI. Melzer. 1984. Alterations in the biophysical properties of the human endothelial cell plasma membrane induced by a chemotactic tripeptide: Correlation with enhanced adherence of granulocytes.J. Pathol. 144:201–211.

    Google Scholar 

  24. Kirkpatrick, C. S., B. D. Bultmann, andH. Gruler. 1985. Interactions between enteroviruses and human endothelial cells in vitro.Am. J. Pathol. 118:15–25.

    Google Scholar 

  25. Colditz, I. G., R. L. Kerlin, andD. L. Watson. 1987. Migration of neutrophils and their role in elaboration of host defence.In Migration and Homing of Lymphoid Cells. A. J. Husband, editor. CRC Press, Boca Raton (in press).

    Google Scholar 

  26. Maas, P. J. C. M., I. G. Colditz. 1987. Desensitization of the acute inflammatory response in skin and mammary gland of sheep.Immunology 61:215–219.

    Google Scholar 

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  1. Division of Animal Health, CS1RO, Armidale, N.S.W., Australia

    Ian G. Colditz

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Colditz, I.G. Two patterns of early neutrophil accumulation in acute inflammatory lesions. Inflammation 12, 251–263 (1988). https://doi.org/10.1007/BF00920077

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