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Migration of dog polymorphonuclear neutrophilic leukocytes to formylated peptides

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Abstract

Formylated peptides are potent stimulants of polymorphonuclear neutrophilic leukyocyte (PMN) migration from species such as humans and rabbits. Interestingly, PMNs from dogs, cats, pigs and cows have been reported as refractory toN-formyl-1-methionyl-1-leucyl-1-phenylalanine (FMLP) and generally are believed not to express formylpeptide receptors. Formylpeptides are a major component of conditioned media fromE. coli cultures and believed to be a significant element in inflammatory responses elicited byE. coli. Our studies have found thatE. coli filtrate was a potent stimulant of dog PMN migration. Inhibition of migration toE. coli filtrates by the antagonistt-botyloxycarbonyl-1-methionyl-1-leucyl-1-phenylalanine (t-boc-MLP) demonstrated that the migration was mediated through the formylated peptide receptor. Migration in response to peptides with higher affinity for the formylpeptide receptor than FMLP was further evidence for these receptors on the dog PMN. PMNs from dogs migrated in response to FMLP at high concentrations (100μM); however, pretreatment with phorbol myristate acetate resulted in increased migration of dog PMNs in response to concentrations of FMLP as low as 1 pM. These results demonstrate that dog PMNs are responsive to formylpeptides and that these responses can be up-regulated by PMA. Thus PMNs from a species previously thought incapable of responding to formylpeptides can respond to formylpeptide analogs with high affinity for the receptor as well as be primed for enhanced migration to FMLP by PMA.

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References

  1. Schiffmann, E., B. A. Corcoran, andS. M. Wahl, 1977.N-Formylmethionyl peptides as chemoattractants for leukocytes.Proc. Natl. Acad. Sci. U.S.A. 72:1059.

    Google Scholar 

  2. Marasco, W. A., S. H. Phan, H. E. Krutzsche, H. J. Showell, D. E. Feltner, R. Nairn, E. L. Becker, andP. A. Ward. 1984. Purification and identification of formyl-methionylleucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced byE. coli.J. Immunol. 259:5430.

    Google Scholar 

  3. Showell, H. J., R. H. Freer, S. H. Zigmond, E. Schiffmann, S. Aswanikumar, B. Corcoran, andE. L. Becker. 1976. The structure-activity relations of synthetic peptides as chemotacic factors and inducers of lysosomal enzyme secretion for neutrophils.J. Exp. Med. 143:1154.

    Google Scholar 

  4. Williams, L. T., R. Snyderman, M. C. Pike, andR. J. Lefkowitz. 1977. Specific receptor sites for chemotactic peptides on human polymorphonuclear leukocytes.Proc. Natl. Acad. Sci. U.S.A. 74:1204.

    Google Scholar 

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

    Google Scholar 

  6. Gallin, J. L., D. G. Wright, andE. Schiffmann. 1978. Role of secretory events in modulating human neutrophil chemotaxis.J. Clin Invest. 62:1364.

    Google Scholar 

  7. Aswanikumar, S., B. Corcoran, andE. Schiffmann. 1977. Demonstration of a receptor on rabbit neutrophils for chemotactic peptide.Biochem. Biophys. Res. Commun. 74:810.

    Google Scholar 

  8. Freer, R. J., A. R. Day, N. Muthukumaraswamy, D. Pinon, A. Wu, H. J. Showell, andE. L. Becker. 1982. Formyl peptide chemoattractants: A model of the receptor on rabbit neutrophils.Biochemistry 21:257.

    Google Scholar 

  9. Niedel, J., S. Wilkinson, andP. Cuatrecasas. 1979. Receptor-mediated uptake and degradation of125I-chemotactic peptide by human neutrophils.J. Biol. Chem. 254:10700.

    Google Scholar 

  10. Redl, H., P. J. Flynn, H. Lamche, S. Schiesser, S. Gunther, andD. E. Hammerschidt. 1983. Aggregation, chemotaxis, and chemiluminescence of canine granulocytes.Inflammation 7:67.

    Google Scholar 

  11. Stickle, J. E., D. G. Kwan, andC. W. Smith. 1985. Neutrophil function in the dog: Shape change and response to a synthetic tripeptide.Am. J. Vet. Res. 46:225.

    Google Scholar 

  12. Gray, G. D., K. A. Knight, R. D. Nelson, andM. J. Herron. 1982. Chemotactic requirements of bovine leukocytes.Am. J. Vet. Res. 43:757.

    Google Scholar 

  13. Chenoweth, D. E., T. A. Lane, F. G. Rowe, andT. E. Hugli. 1980. Quantitative comparisons of neutrophil chemotaxis in four animal species.Clin. Immunol. Jmmunopathol. 15:525.

    Google Scholar 

  14. Gray, G. D., G. M. Ohlmann, D. R. Morton, andR. G. Schaaub. 1986. Feline polymorphonuclear leukocytes respond chemotactically to leukotriene B4 and activated serum but not to F-Met-Leu-Phe.Agents Actions 18:401.

    Google Scholar 

  15. Cook, L. O., L. A. Boxer, J. M. Allen, J. A. Grief, andR. L. Baehner. 1978. In vitro functional capabilities of canine PMNs collected simultaneously by continuous-flow centrifugation and continuous-flow filtration leukopheresis.Am. J. Hematol. 4:225.

    Google Scholar 

  16. Falk, W., R. H. Goodwin, andE. J. Leonard, 1980. A 48-well micro chemotaxis assembly for rapid and accurate measurement of leukocyte migration.J. Immunol. Methods 33:239.

    Google Scholar 

  17. Fletcher, M. P., B. E. Seligmann, andJ. I. Gallin, 1982. Correlation of human neutrophil secretion, chemoattractant receptor mobilization, and enhanced functional capacity.J. Immunol. 128:941.

    Google Scholar 

  18. Munson, P. J., andD. Rodbard. 1980. Ligand: A versatile computerized approach for characterization of ligand binding systems.Anal. Biochem. 107:220.

    Google Scholar 

  19. Linnekin, D. M. 1988. Modulation of PMN responses to F-Met-Leu-Phe. PhD dissertation. Uniformed Services University of the Health Sciences, Bethesda, Maryland.

    Google Scholar 

  20. Verghese, M. W., L. Charles, L. Jakoi, S. B. Dillon, andR. Synderman. 1987. Role of a guanine nucleotide reglulatory protein in the activation of phosphiolipase C by different chemoattractants.J. Immunol. 138:4374.

    Google Scholar 

  21. Estensen, R. C., H. R. Hill, P. G. Quie, N. Hogan, andN. D. Goldberg. 1973. Cyclic GMP and cell movement.Nature 245:458.

    Google Scholar 

  22. Fletcher M. P., andJ. I. Gallin. 1980. Degranulating stimuli increase the availability of receptors on human neutrophils for the chemoattractant f-Met-Leu-Phe.J. Immunol. 124:1585.

    Google Scholar 

  23. Fletcher, M. P., andJ. I. Gallin. 1983. Human neutrophils contain an intracellular pool of putative receptors for the chemoattractantN-formyl-methionyl-leucyl-phenylalanine.Blood 62:792.

    Google Scholar 

  24. Anderson, R., andJ. Niedel. 1984. Processing of the formyl peptide receptor by HL-60 Cells.J. Biol. Chem. 259:13309.

    Google Scholar 

  25. Jesaitis, A. J., J. R. Naemaur, R. G. Painter, L. E. Sklar, andC. G. Cochrane. 1982. Intracellular localization ofN-formyl chemotactic receptor and Mg-dependent ATPase in human granulocytes.Biochim. Biophys. Acta 719:556.

    Google Scholar 

  26. Hunter, T., andJ. A. Cooper. 1985. Protein-tyrosine kinases.Annu. Rev. Biochem. 54:897.

    Google Scholar 

  27. D. W. Goldman, J. Enkel, L. A. Gifford, D. E. Chenoweth, andJ. T. Rosenbaum. 1986. Lipopolysaccharide modulates receptors for leukotriene B4, C5a and formyl-methionyl-leucylphenylalanine on rabbit polymorphonuclear leukocytes.J. Immunol. 137:1971.

    Google Scholar 

  28. Fletcher, M. P. 1986. Modulation of the heterogeneous membrane potential response of neutrophils toN-formyl-methionyl-leucyl-phenylalanine (FMLP) by leukotriene B4: Evidence for cell recruitment.J. Immunol. 136:4213.

    Google Scholar 

  29. Gay, J. C., J. K. Beckman, A. R. Brash, J. A. Oates, andJ. N. Lukens. 1984. Enhancement of chemotactic factor-stimulated neutrophil oxidative metabolism by leukotriene B4.Blood 64:780.

    Google Scholar 

  30. Gay, J. C., J. K. Beckman, L. A. Zaboy, andJ. N. Lukens. 1986. Modulation of neutrophil oxidative responses to soluble stimuli by platelet-activating factor.Blood 67:931.

    Google Scholar 

  31. Ingraham, L. M., J. E. Lafuze, L. A. Boxer, andR. L. Baehner. 1987. In vitro and in vivo effects of treatment by platelet-activating factor onN-formyl-methionyl-leucyl-phenylalanine mediated responses of polymorphonuclear leucocytes.Br. J. Haematol 66:219.

    Google Scholar 

  32. Weishart, R. H., D. W. Golde, andJ. C. Gasson. 1986. Biosynthetic human GM-CSF modulates the number and affinity of neutrophil f-Met-Leu-Phe Receptors.J. Immunol. 137:3584.

    Google Scholar 

  33. Fletcher, M. P., andJ. C. Gasson. 1988. Priming of neutrophils by rhGM-CSF involves recruitment of a less responsive subpopulation.J. Immunol. 71:652.

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, Uniformed Services University of the Health Sciences, Bethesda, Maryland

    Diana Linnekin

  2. Department of Experimental Hematology, Armed Forces Radiobiology Research Institute, Bethesda, Maryland

    Diana Linnekin & Thomas J. MacVittie

  3. Merrifield Laboratories, Fairfax, Virginia

    Charles A. Bowles

  4. Office of Biologics, Food and Drug Administration, Bethesda, Maryland

    Genesio Murano

Authors
  1. Diana Linnekin
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  2. Charles A. Bowles
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  3. Genesio Murano
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  4. Thomas J. MacVittie
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Linnekin, D., Bowles, C.A., Murano, G. et al. Migration of dog polymorphonuclear neutrophilic leukocytes to formylated peptides. Inflammation 14, 691–703 (1990). https://doi.org/10.1007/BF00916372

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