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Dynamics of avian inflammatory response toSalmonella-immune lymphokines

Changes in avian blood leukocyte populations

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Abstract

Investigations in our laboratories have indicated that an increased resistance to SE organ infectivity in chicks was conferred by the immunoprophylactic administration of SE-immune lymphokines (SE-ILK). This resistance was associated with an increase in the lamina propria thickness due to a marked infiltration of inflammatory polymorphonuclear cells (PMNs). In the present study, we determined whether the hematological profile of SE-ILK-treated chicks might reflect changes that are associated with the protection against organ invasion by SE. As protection has been observed in previous studies within 24 h of SE-ILK administration, we evaluated alterations in the circulating leukocyte profile in 1-day-old Leghorn chicks during this time period. We also determined whether the alterations in the peripheral blood leukocytes correlated with the increased protection against SE organ invasion induced by the SE-ILK. Within 4 h after an intraperitoneal injection of SE-ILK and challenge with SE, the number of circulating leukocytes increased significantly (P < 0.05) from all of the other treatment groups. The number of circulating PMNs was found to account for more than 80% of the increase in the number of circulating leukocytes. Using correlation analysis, we found a strong association between the number of circulating PMNs and the protection induced by SE-ILK against SE organ invasion. These studies associate the expansion of the available pool of circulating PMNs and the expression of innate resistance to organ invasion by SE.

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References

  1. U.S.Department of Agriculture, Agricultural Research Service. 1989. Report of theSalmonella enteritidis task force for research. 1–34.

  2. Tellez, G. I., M. H. Kogut, andB. M. Hargis. 1993. Immunoprophylaxis ofSalmonella enteritidis (SE) infection by lymphokines in Leghorn chicks.Avian Dis. 37:1062–1070.

    PubMed  Google Scholar 

  3. McGruder, E. D., P. M. Ray, G. I. Tellez, M. H. Kogut, D. E. Corrier, J. R. DeLoach, andB. M. Hargis. 1993.Salmonella enteritidis (SE) immune cytokines: Effect on increased resistance to SE organ invasion in day-old Leghorn chicks.Poult. Sci. 72:2264–2271.

    PubMed  Google Scholar 

  4. Kogut, M. H., G. I. Tellez, B. M. Hargis, D. E. Corrier, andJ. R. DeLoach. 1993. The effect of 5-fluorouracil treatment of chicks: A cell depletion model for the study of avian polymorphonuclear leukocytes and natural host defenses.Poult. Sci. 72:1873–1880.

    PubMed  Google Scholar 

  5. Ulich, T. R. 1992. Hematological effects of cytokines in vivo.In Cytokines in Health and Disease. S. L. Kunkel and D. G. Remick, editors. Marcel Decker, New York. 235–256.

    Google Scholar 

  6. Rose, M. E., P. Hesketh, andB. M. Ogilvie. 1979. Peripheral blood leukocyte response to coccidial infection: A comparison of the response in rats and chickens and its correlation with resistance to reinfection.Immunology 36:71–79.

    PubMed  Google Scholar 

  7. Kogut, M. H., andP. L. Long. 1984. The peripheral blood leukocyte response of chickens and turkeys infected with turkey embryo adapted strains ofEimeria tenella andE. necatrix.Exp. Parasitol. 58:63–71.

    PubMed  Google Scholar 

  8. Golemboskie, K. A., S. E. Bloom, andR. R. Dietert. 1990. Dynamics of avian inflammatory response to cross-linked dextran. Changes in avian blood leukocyte populations.Inflammation 14:31–40.

    PubMed  Google Scholar 

  9. Latimer, K. S., K.-N. Tang, M. A. Goodwin, W. L. Steffens, andJ. Brown. 1988. Leukocyte changes associated with acute inflammation in chickens.Avian Dis. 32:760–772.

    PubMed  Google Scholar 

  10. Andrews, W., P. Poelma, C. Wilson, andA. Romero. 1978. Isolation and identification ofSalmonella.In Bacteriological Analytical Manual, 5th ed. Association of Official Analytical Chemists, Washington, D.C. 1–29.

    Google Scholar 

  11. National Research Council. 1984. Nutrient Requirements of Poultry, 8th rev. ed. National Academy Press, Washington, D.C.

    Google Scholar 

  12. Kogut, M. H., andT. Slajchert. 1992. T lymphocytes induce protection in chickens againstEimeria tenella by the production of lymphokines.Immunol. Infect. Dis. 2:69–80.

    Google Scholar 

  13. Julius, M. H., E. Simpson, andA. Herzenberg. 1973. A rapid method for the isolation of functional thymus derived murine lymphocytes.Eur. J. Immunol. 3:645–653.

    PubMed  Google Scholar 

  14. Freshney, R. I. 1983. Culture of Animal Cells, Vol. 1. Alan R. Liss, New York.

    Google Scholar 

  15. Weiler, H., andW. Von Bulow. 1987. Development of optimal conditions for lymphokine production by chicken lymphocytes.Vet. Immunol. Immunopathol. 14:257–267.

    PubMed  Google Scholar 

  16. Natt, M. P., andC. A. Herrick. 1952. A new blood diluent for counting the erythrocytes and leukocytes of the chicken.Poult. Sci. 31:735–738.

    Google Scholar 

  17. Lucas, A. M., andC. Jamroz. 1961. Atlas of Avian Hematology. USDA, Washington, D.C. 155–156.

    Google Scholar 

  18. U.S. Department of Agriculture, Animal and Plant Health Inspection Service. 1989. National poultry improvement plan and auxiliary provisions. Veterinary Services, Publication APHIS 91-40. U.S. Government Printing Office, Washington, D.C.

    Google Scholar 

  19. SAS Institute. 1982. SAS Users Guide: Statistics. SAS Institute, Inc., Cary, North Carolina.

    Google Scholar 

  20. Zar, J. 1984. Biostatistical Analysis, 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey. 384–351.

    Google Scholar 

  21. Luginbuke, R. C., andS. D. Schlotzhaver. 1987. SAS/STAT guide for Personal Computers, 6th ed. SAS Institute, Cary, North Carolina, 555–573.

    Google Scholar 

  22. Czuprynski, C. J., P. M. Henson, andP. A. Campbell. 1985. Enhanced accumulation of inflammatory neutrophils and macrophages mediated by transfer of T cells from mice immunized withListeria monocytogenes.J. Immunol. 134:3449–3454.

    PubMed  Google Scholar 

  23. Kratz, S. S., andR. J. Kurlander. 1988. Characterization of the pattern of inflammatory cell influx and cytokine production during the murine host response toListeria monocytogenes.J. Immunol. 141:598–606.

    PubMed  Google Scholar 

  24. Czuprynski, C. J., andJ. R. Brown. 1987. Dual regulation of anti-bacterial resistance and inflammatory neutrophil and macrophage accumulation by L3T4+ and Lyt 2+ Listeria-immune T cells.Immunology 60:287–293.

    PubMed  Google Scholar 

  25. Gross, W. B. 1961. Blood cultures, blood counts, and temperature records in an experimentally produced “air sac disease” and uncomplicatedEscherichia coli infection of chickens.Poult. Sci. 41:691–709.

    Google Scholar 

  26. Glick, B., andC. Rosse. 1976. Cellular composition of the bone marrow in the chicken. Identification of cells.Anat. Rec. 185:235–246.

    PubMed  Google Scholar 

  27. Ficken, M. D., J. F. Edwards, andJ. C. Lay. 1986. Induction, collection, and partial characterization of induced respiratory macrophages of the turkey.Avian Dis. 30:766–771.

    PubMed  Google Scholar 

  28. Rose, M. E., andP. Hesketh. 1974. Fowl peritoneal exudate cells: Collection and use for the macrophage migration test.Avian Pathol. 3:297–304.

    Google Scholar 

  29. Toth, T. E., P. B. Siegel, andH. Veit. 1987. Cellular defense of the avian respiratory system. Influx of phagocytes, elicitation versus activation.Avian Dis. 31:861–867.

    PubMed  Google Scholar 

  30. Metcalf, D. 1986. The molecular biology and functions of granulocyte-macrophage colony stimulating factors.Blood 67:257–267.

    PubMed  Google Scholar 

  31. McNiece, I. K. 1992. Structure and function of interleukin-3, erythropoietin, and the colonystimulating factors.In Cytokines in Health and Disease. S. L. Kunkel and D. G. Remick, editors. Marcel Dekker, New York. 61–78.

    Google Scholar 

  32. Ihle, J. N. 1990. Lymphokine regulation of hematopoietic cell development.In Immunophysiology. The Role of Cells and Cytokines in Immunity and Inflammation. J. J. Oppenheim and E. M. Shevach, editors. Oxford University Press, New York. 166–193.

    Google Scholar 

  33. Ruskin, J., andJ. Remington. 1969. Role of the macrophage in acquired immunity to phylogenetically diverse intracellular organisms.J. Immunol. 103:252–259.

    PubMed  Google Scholar 

  34. Simon, H. B., andJ. Sheargren. 1972. Enhancement of macrophage bactericidal capacity by antigenically stimulated lymphocytes.Cell. Immunol. 4:163–174.

    PubMed  Google Scholar 

  35. Takeuchi, A., andH. Sprinz. 1967. Electron microscope studies of experimentalSalmonella infections in the preconditioned guinea pig. II. Response of the intestinal mucosa to the invasion bySalmonella typhimurium.Am. J. Pathol. 51:137–146.

    Google Scholar 

  36. Wolfe, S. A., D. E. Tracy, andC. S. Henney. 1976. Induction of natural killer cells by BCG.Nature 262:584–586.

    PubMed  Google Scholar 

  37. Conlon, J. W., andR. J. North. 1992. Early pathogenesis of infection in the liver with the facultative intracellular bacteriaListeria monocytogenes, Francisella tularensis, andSalmonella typhimurium involves lysis of infected hepatocytes by leukocytes.Infect. Immun. 60:5164–5171.

    PubMed  Google Scholar 

  38. Hart, P. H., L. K. Spencer, A. Nikoloutsopoulos, A. F. Lopez, M. A. Vadas, P. J. McDonald, andJ. J. Finlay-Jones. 1986. Role of cell surface receptors in the regulation of intracellular killing of bacteria by murine peritoneal exudate neutrophils.Infect. Immun. 52:245–251.

    PubMed  Google Scholar 

  39. Lin, F.-R., X.-M. Wang, H. S. Hsu, V. R. Mumaw, andI. Naconecza. 1987. Electron microscopic studies on the location of bacterial proliferation in the liver in murine salmonellosis.Br. J. Exp. Pathol. 68:539–550.

    PubMed  Google Scholar 

  40. Beckerdite, S., C. Mooney, J. Weiss, R. Franson, andP. Elsbach. 1974. Early and discrete changes in permeability ofE. coli and other gram negative bacteria during killing by granulocytes.J. Exp. Med. 140:396–409.

    PubMed  Google Scholar 

  41. Miller, R. M., J. Garbus, andR. B. Hornick, 1972. Lack of enhanced oxygen consumption by PMN leukocytes in phagocytosis of virulentSalmonella typhii.Science.175:1010–1011.

    PubMed  Google Scholar 

  42. Rossack, R. E., R. L. Guerrant, P. Densen, J. Schadelin, andG. L. Mandell. 1981. Diminished neutrophil oxidative metabolism after phagocytosis of virulentSalmonella typhii.Infect. Immun. 31:674–678.

    PubMed  Google Scholar 

  43. Stabler, J., T. C.McCormick, K. C.Powell, and M. H.Kogut. 1993. Avian heterophils and monocytes: phagocytic and bactericidal activities againstSalmonella enteritidis. Vet. Microbiol. (in press).

  44. Nauciel, C., andF. Espinasse-Maes. 1992. Role of gamma interferon and tumor necrosis factor alpha in resistance toSalmonella typhimurium infection.Infect. Immun. 60:450–454.

    PubMed  Google Scholar 

  45. Mastroeni, P., A. Arena, G. B. Costa, M. C. Liberto, L. Bonina, andC. E. Hormaeche. 1991. Serum TNF in mouse typhoid and enhancement of a salmonella infection by anti-TNF antibodies.Microb. Pathogen. 11:33–38.

    Google Scholar 

  46. Morrissey, P. J., andK. Charrier. 1991. Interleukin-1 administration to C3H/HeJ mice after but not prior to infection increase resistance toSalmonella typhimurium.Infect. Immun. 59:4729–4731.

    PubMed  Google Scholar 

  47. Muotiala, A., andP. H. Makela. 1990. The role of IFN in murineSalmonella typhimurium infection.Microb. Pathogen. 8:135–141.

    Google Scholar 

  48. Nakano, Y., K. Onozuka, Y. Terada, H. Shinomiya, andM. Nakano. 1990. Protective effect of recombinant tumor necrosis factor in murine salmonellosis.J. Immunol. 144:1935–1941.

    PubMed  Google Scholar 

  49. Tite, J. P., G. Dougan, andS. N. Chatfield. 1991. The involvement of tumor necrosis factor in immunity toSalmonella infection.J. Immunol. 147:3161–3164.

    PubMed  Google Scholar 

  50. Edwards, C. K., S. M. Ghiasuddin, L. M. Yunger, R. M. Lorence, S. Arkins, R. Danzer, andK. W. Kelley. 1992. In vivo administration of recombinant growth hormone or gamma interferon activates macrophages: Enhanced resistance to experimentalSalmonella typhimurium infection is correlated with generation of reactive oxygen intermediates.Infect. Immun. 60:2514–2521.

    PubMed  Google Scholar 

  51. Liu, Z., R. J. Simpson, andC. Cheers. 1992. Recombinant interleukin-6 protects mice against experimental bacterial infection.Infect. Immun. 60:4402–4406.

    PubMed  Google Scholar 

  52. Cheers, C., Y. F. Zhan, andP. J. Egan. 1990. In vivo IL-1 potentiates both specific and non-specific arms of immune response to infection.Immunology 70:411–413.

    PubMed  Google Scholar 

  53. Haak-Frendscho, M., K. M. Young, andC. J. Czuprynski. 1990. Treatment of mice with human recombinant interleukin-2 augments resistance to the facultative intracellular pathogenListeria monocytogenes.Infect. Immun. 57:3014–3021.

    Google Scholar 

  54. Fortier, A. H., T. Polsinelli, S. J. Green, andC. A. Nacy. 1992. Activation of macrophages for destruction ofFrancisella tularensis: Identification of cytokines, effector cells, and effector molecules.Infect. Immun. 60:817–825.

    PubMed  Google Scholar 

  55. Leiby, D. A., A. H. Fortier, R. M. Crawford, R. D. Schreiber, andC. A. Nacy. 1992. In vivo modulation of the murine immune response toFrancisella tularensis LVS by administration of anticytokine antibodies.Infect. Immun. 60:84–89.

    PubMed  Google Scholar 

  56. Morrissey, P. J., andK. Charrier. 1990. GM-CSF administration augments the survival of ity-resistant A/J mice, but not ity-susceptible C57BL/6 mice, to a lethal challenge withSalmonella typhimurium.J. Immunol. 144:557–561.

    PubMed  Google Scholar 

  57. Shinomiya, N., S. Tsuru, Y. Katsura, S. Kayashima, andK. Nomoto. 1991. Enhanced resistance againstListeria monocytogenes achieved by pretreatment with granulocyte colonystimulating factor.Infect. Immun. 59:4740–4743.

    PubMed  Google Scholar 

  58. Serushago, B. A., Y. Yoshikai, T. Handa, M. Mitsuyama, K. Muramori, andK. Nomoto. 1992. Effect of recombinant human granulocyte colony-stimulating factor (rh G-CSF) on murine resistance againstListeria monocytogenes.Immunology 75:475–480.

    PubMed  Google Scholar 

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Author notes

  1. E. D. McGruder

    Present address: Department of Veterinary Pathobiology, Texas Veterinary Medical Center, Texas A&M University, 77843, Collete Station, Texas

  2. B. M. Hargis

    Present address: Department of Poultry Science, Texas agricultural Experiment Station, Texas A&M University, 77843, Collete Station, Texas

Authors and Affiliations

  1. Food Animal Protection Research Laboratory, United States Department of Agriculture, Agricultural Research Service, Route 5, Box 810, 77845, College Station, Texas

    M. H. Kogut, E. D. McGruder, B. M. Hargis, D. E. Corrier & J. R. DeLoach

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  1. M. H. Kogut
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  5. J. R. DeLoach
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Kogut, M.H., McGruder, E.D., Hargis, B.M. et al. Dynamics of avian inflammatory response toSalmonella-immune lymphokines. Inflammation 18, 373–388 (1994). https://doi.org/10.1007/BF01534435

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