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Bovine neutrophils recruited by endotoxin to a teat cistern continuously produce oxygen radicals and show increased phagocytosis and extracellular chemiluminescence

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Abstract

Bovine neutrophils were harvested from a teat cistern following endotoxin infusion and were compared with blood neutrophils by measurements of chemiluminescent and phagocytic activity towards C3-and IgG-opsonized and unopsonized yeast particles. Both phagocytosis and luminol-dependent chemiluminescence elicited by all three particles were enhanced in the teat cells. The increase in the luminoldependent chemiluminescence towards C3-and IgG-opsonized particles was due to an enhanced extracellular release of myeloperoxidase. The observed increase in phagocytosis of unopsonized yeast was shown to reflect the interaction between up-regulated CR3 receptors on the surface of the teat neutrophils and the yeast particles. A high chemiluminescent activity of the teat neutrophils in both the luminol-and lucigenin-dependent systems in the absence of a phagocytic prey indicated that the NADPH oxidase was permanently active and that myeloperoxidase was continuously released by the cells. Treatment of neutrophils with cytochalasin B showed that the chemiluminescence and phagocytosis of teat neutrophils were less sensitive to this drug than that of blood neutrophils. These results indicate that the teat neutrophils have up-regulated their receptors for IgG-and C3-opsonized and unopsonized yeast on the cell surface by the action of actin. The cells also have a permanently active NADPH oxidase dependent on the association with actin and show a higher

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References

  1. Hohn, D. C., B. Ponce, R. W. Burton, andT. K. Hunt. 1977. Antimicrobicidal systems of the surgical wound. I. A comparison of oxidative metabolism and microbicidal capacity of phagocytes from wounds and peripheral blood.Am. J. Surg,133:597–600.

    Google Scholar 

  2. Takamori, K., andT. Yamashita. 1980. Biochemical properties of polymorphonuclear neutrophils from venous blood and peritoneal exudates of rabbits.Infect. Immun. 29:395–400.

    Google Scholar 

  3. Van Epps, D. E., andM. L. Garcia. 1980. Enhancement of neutrophil function as a result of prior exposure to chemotactic factor.J. Clin, Invest. 66:167–175.

    Google Scholar 

  4. Robison, J. M., L. Karnovsky, andM. J. Karnovsky. 1982. Glycogen accumulation in polymorphonuclear leukocytes, and other intracellular alterations that occur during inflammation.J. Cell Biol. 95:933–942.

    Google Scholar 

  5. Zimmerli, W., P. D. Lew, H. J. Cohen, andF. A. Waldwogel. 1984. Comparative super-oxide-generating system of granulocytes from blood and peritoneal exudates.Infect. Immun. 46:625–630.

    Google Scholar 

  6. Briheim, G., B. Coble, O. Stendahl, andC. Dahlgren. 1988. Exudate polymorphonuclear leukocytes isolated from skin chambers are primed for enhanced response to subsequent stimulation with chemoattractant f-Met-Leu-Phe and C3-opsonized yeast particles.Inflammation 12:141–152.

    Google Scholar 

  7. Paty, P. B., R. W. Graeff, F. M. Waldman, T. K. Hunt, andS. J. Mathes. 1988. Biologic priming of neutrophils in subcutaneous wounds.Arch. Surg. 123:1509–1513.

    Google Scholar 

  8. Follin, P., andC. Dahlgren. 1990. Altered O 2 /H2O2 production ratio by in vitro and in vivo primed human neutrophils.Biochem. Biophys. Res. Commun. 167:970–976.

    Google Scholar 

  9. Paccaud, J.-P., J.-L. Carpentier, andJ. A. Schifferli. 1990. Exudation induces clustering of CR1 receptors at the surface of human polymorphonuclear leukocytes.Biochem. Biophys. Res, Commun. 172:1203–1208.

    Google Scholar 

  10. Zimmerli, W., B. Seligmann, andJ. I. Gallin. 1986. Exudation primes human and guinea pig neutrophils for subsequent responsiveness to the chemotactic peptideN-formyl-methionylleucylphenylalanine and increases complement component C3bi receptor expression.J. Clin. Invest. 77:925–933.

    Google Scholar 

  11. Briheim, G., P. Follin, S. Sandstedt, andC. Dahlgren. 1989. Relationship between intra-cellularly and extracellularly generated oxygen metabolites from primed polymorphonuclear leukocytes differs from that obtained from nonprimed cells.Inflammation 13:455–464.

    Google Scholar 

  12. Grisham, M. B., J. Everse, andH. J. Janssen. 1988. Endotoxemia and neutrophil activation in vivo.Am. J. Physiol. 254:H1017-H1022.

    Google Scholar 

  13. Cerasoli, F., Jr., P. J. McKenna, D. L. Rosolia, K. H. Albertine, S. P. Peters, andM. H. Gee. 1990. superoxide anion release from blood and bone marrow neutrophils is altered by endotoxemia.Circ. Res. 67:154–165.

    Google Scholar 

  14. Dwenger, A., G. Regel, B. Ellendorf, G. Schweitzer, M. Funck, H. Limbrock, J. A. Sturm, andH. Tscherne. 1990. Alveolar cell pattern and chemiluminescence response of blood neutrophils and alveolar macrophages in sheep after endotoxin injection.J. Clin. Chem. Clin. Biochem. 28:163–168.

    Google Scholar 

  15. Dulin, A. M., M. J. Paape, andS. C. Nickerson. 1988. Comparison of phagocytosis and chemiluminescence by blood and mammary gland neutrophils from multiparous and nulliparous cows.Am. J. Vet. Res. 49:172–177.

    Google Scholar 

  16. Persson, K. 1990. Inflammatory reactions in the teat and udder of the dry cow.J. Vet. Med. 837:599–610.

    Google Scholar 

  17. Hallén Sandgren, C., andI. BjÖrk. 1988. A rapid technique for the isolation of highly purified, functionally intact bovine neutrophilic granulocytes.Vet. Immunol. Immunopathol. 18:81–94.

    Google Scholar 

  18. Hallén Sandgren, C., K. Nordling, andI. BjÖrk. 1991. Isolation and phagocytic properties of neutrophils and other phagocytes from nonmastitic bovine milk.J. Dairy Sci. 74:2965–2975.

    Google Scholar 

  19. Hallén Sandgren, C., K. Nordling, andI. Björk. 1991. A new technique, requiring small amounts of cells, for the parallel study of chemiluminescence and phagocytosis via different receptors in the same cell population.J. Immunol. Methods 141:63–72.

    Google Scholar 

  20. Czop, J. K., A. V. Puglisi, D. Z. Miorandi, andF. K. Austen. 1988. Perturbation ofβ-glucan receptors on human neutrophils initiates phagocytosis and leukotriene B4 production.J. Immunol. 141:3170–3176.

    Google Scholar 

  21. Edwards, S. W. 1987. Luminol and lucigenin-dependent chemiluminescence of neutrophils: Role of degranulation.J. Clin. Lab. Immunol. 22:35–39.

    Google Scholar 

  22. Cooper, J. A. 1987. Effects of cytochalasin and phalloidin on actin.J. Cell. Biol. 105:1473–1478.

    Google Scholar 

  23. Kapp, A., M. Freudenberg, andC. Galanos. 1987. Induction of human granulocyte chemi-luminescence by bacterial lipopolysaccharides.Infect. Immun. 55:758–761.

    Google Scholar 

  24. Tarnok, I., andZs. Tarnok. 1990. Direct stimulation of superoxide output in neutrophils by lipid A ofEscherichia coli.Int. J. Tissue React. 12:47–52.

    Google Scholar 

  25. Klein, J. B., V. Payne, T. M. Schepers, andK. R. McLeish. 1990. Bacterial lipopolysac-charide enhances polymorponuclear leukocyte function independent of changes in intracellular calcium.Inflammation 14:599–611.

    Google Scholar 

  26. Fittchen, C., R. A. Sandhaus, G. S. Worthen, andP. M. Henson. 1988. Bacterial lipo-polysaccharide enhances chemoattractant-induced elastase secretion by human neutrophils.J. Leukocyte Biol. 43:547–556.

    Google Scholar 

  27. Shalaby, M. R., B. B. Aggarwal, E. Rinderknecht, L. P. Svedersky, B. S. Finkle, andM. A. Palladino Jr. 1985. Activation of human polymorphonuclear neutrophil functions by interferon-γ and tumor necrosis factors.J. Immunol. 135:2069–2073.

    Google Scholar 

  28. Thelen, M., P. Peveri, P. Kernen, V. von Tscharner, A. Walz, andM. Bagglioni. 1988. Mechanism of neutrophil activation by NAF, a novel monocyte-derived peptide agonist.FASEB J. 2:2702–2706.

    Google Scholar 

  29. Golde, D. W., andJ. C. Gasson. 1988. Cytokines: Myeloid growth factors.In Inflammation: Basic Principles and Clinical Correlates. J. I. Gallin, I. M. Goldstein, and R. Snyderman, editors. Raven Press, New York. 253–261.

    Google Scholar 

  30. Ogle, J. D., J. G. Noel, A. Balasurbramaniam, R. M. Sramkoski, C. K. Ogle, andJ. W. Alexander. 1990. Comparison of abilities of recombinant interleukin-1α and-gb and nonin-flammatory IL-β fragment 163–171 to upregulate C3b receptors (CR1) on human neutrophils and to enhance their phagocytic capacity.Inflammation 14:185–194.

    Google Scholar 

  31. Buckle, A.-M., andN. Hogg. 1989. The effect ofIFN-γ and colony-stimulating factors on the expression of neutrophil membrane receptors.J. Immunol. 143:2295–2301.

    Google Scholar 

  32. Detmers, P. A., S. K. Lo, E. Olsen-Egbert, A. Walz, M. Bagglioni, andZ. A. Cohn. 1990. Neutrophil-activating protein 1/interleukin 8 stimulates the binding activity of the leukocyte adhesion receptor CD11b/CD18 on human neutrophils.J. Exp. Med. 171:1155–1162.

    Google Scholar 

  33. Detmers, P. A., S. D. Wfright, E. Olsen, B. Kimball, andZ. A. Cohn. 1987. Aggregation of complement receptors on human neutrophils.J. Cell Biol. 105:1137–1145.

    Google Scholar 

  34. Petersen, M., R. Steadman, M. B. Hallet, N. Matthews, andJ. D. Williams. 1990. Zymosan-induced leukotriene B4 generation by human neutrophils is augmented by rhTNF-α but not chemotactic peptide.Immunology 70:75–81.

    Google Scholar 

  35. Williams, J. D., N. Topley, H. M. Alobaidi, andM. J. Harber. 1986. Activation of human polymorphonuclear leucocytes by particulate zymosan is related to both its major carbohydrate components: glucan and mannan.Immunology 58:117–124.

    Google Scholar 

  36. Dularay, B., C. J. Elsom, S. Clements-Jewery, C. Damais, andD. Lando. 1990. Recombinant human interleukin-1 beta primes human polymorphonuclear leukocytes for stimulus-induced myeloperoxidase release.J. Leukocyte Biol. 47:158–163.

    Google Scholar 

  37. Newburger, P. E., R. A. B. Ezekowitz, C. Whitney, J. Whright, andS. H. Orkin. 1988. Induction of phagocyte cytochrome b heavy chain gene expression by interferon γ.Proc. Natl. Acad. Sci. U.S.A. 85:5215–5219.

    Google Scholar 

  38. Ozaki, Y., T. Ohashi, andS. Kume. 1987. Potentiation of neutrophil function by recombinant DNA-produced interleukin la.J. Leukocyte Biol. 42:621–627.

    Google Scholar 

  39. Tsujimoto, M., S. Yokota, J. Vilcek, andG. Weissman. 1986. Tumor necrosis factor provokes superoxide anion generation from neutrophils.Boichem. Biophys. Res. Commun. 137:1094–1100.

    Google Scholar 

  40. Bird, J., M. Pelletier, M. Tissot, andJ.-P. Giroud. 1985. The modification of the oxidative metabolism of cells derived both locally and at a distance from the site of an acute inflammatory reaction.J. Leukocyte Biol 37:109–120.

    Google Scholar 

  41. Stossel, T. P. 1988. The mechanical responses of white blood cellsIn Inflammation: Basic Principles and Clinical Correlates. J. I. Gallin, I. M. Goldstein, and R. Snyderman, (editors.) Raven Press, New York. 325–342.

    Google Scholar 

  42. Jesaitis, A. J., J. O. Tolley, R. G. Painter, L. S. Sklar andC. G. Cochrane. 1985. Membrane-cytoskeleton interactions and the regulation of chemotactic peptide-induced activation of human granulocytes: The effects of dihydrocytochalasin B.J. Cell. Biochem. 27:241–253.

    Google Scholar 

  43. Howard, T. H., D. Wang, andR. L. Berkow. 1990. Lipopolysaccharide modulates chemotactic peptide-induced actin polymerization in neutrophils.J. Leukocyte Biol. 47:13–24.

    Google Scholar 

  44. Berkow, R. L., D. Wang, J. W. Larrick, R. W. Dodson, andT. H. Howard. 1987. Enhancement of neutrophil superoxide production by preincubation with recombinant human tumor necrosis factor.J. Immunol. 139:3783–3791.

    Google Scholar 

  45. Quinn, M. T., C. A. Parkos, andA. J. Jesaitis. 1989. The lateral organization of components of the membrane skeleton and superoxide generation in the plasma membrane of stimulated human neutrophils.Biochin. Biophys. Acta 987:83–94.

    Google Scholar 

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Sandgren, C.H., Larsson, I. & Persson, K. Bovine neutrophils recruited by endotoxin to a teat cistern continuously produce oxygen radicals and show increased phagocytosis and extracellular chemiluminescence. Inflammation 16, 117–133 (1992). https://doi.org/10.1007/BF00918952

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