Skip to main content
NCBI home page
Journal of Clinical Microbiology logoLink to Journal of Clinical Microbiology
. 1989 May;27(5):812–817. doi: 10.1128/jcm.27.5.812-817.1989

Ingestion and killing of Listeria monocytogenes by blood and milk phagocytes from mastitic and normal cattle.

C J Czuprynski 1, E J Noel 1, M P Doyle 1, R D Schultz 1
PMCID: PMC267434  PMID: 2501346

Abstract

Human listeriosis resulting from consumption of listeria-contaminated dairy products is emerging as a significant public health concern. There is a need to understand better the processes involved in the pathogenesis of Listeria monocytogenes-induced bovine mastitis. In the present report, we describe the results of the in vitro interaction of L. monocytogenes with bovine blood and milk leukocytes. Induction of an experimental L. monocytogenes mastitis resulted in a rapid and dramatic increase in neutrophils in the milk of infected cows. Blood neutrophils and mononuclear cells and milk leukocytes from listeria-infected and uninfected cows readily ingested L. monocytogenes in the presence of serum opsonins. These leukocytes also killed a portion of the ingested listeriae. Ingestion of listeriae evoked a vigorous chemiluminescence response by blood neutrophils and a relatively weak response by blood mononuclear cells. Ingestion, killing, and chemiluminescence by milk leukocytes were directly related to the percentage of neutrophils that were present. Blood neutrophils from healthy donor cattle ingested and killed L. monocytogenes when leukocyte-depleted milk and whey from mastitic cows were the sole sources of opsonins, although fewer listeriae were ingested than when normal bovine serum was present. These results indicate that bovine blood and milk phagocytes, like blood and inflammatory phagocytes from other mammalian species, can ingest and kill L. monocytogenes in vitro.

Full text

PDF
812

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AKIYAMA Y., ASAHI O., HOSODA T. Studies on the mechanism of infection of the brain with Listeria monocytogenes. Am J Vet Res. 1957 Jan;18(66):147–157. [PubMed] [Google Scholar]
  2. Adams C. J., Neff T. E., Jackson L. L. Induction of Listeria monocytogenes infection by the consumption of ponderosa pine needles. Infect Immun. 1979 Jul;25(1):117–120. doi: 10.1128/iai.25.1.117-120.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson J. C., Williams M. R. The contribution of a capsule to survival of staphylococci within bovine neutrophils. J Med Microbiol. 1985 Dec;20(3):317–323. doi: 10.1099/00222615-20-3-317. [DOI] [PubMed] [Google Scholar]
  4. Barza M. Listeriosis and milk. N Engl J Med. 1985 Feb 14;312(7):438–440. doi: 10.1056/NEJM198502143120710. [DOI] [PubMed] [Google Scholar]
  5. Brooker B. E. Pseudopod formation and phagocytosis of milk components by epithelial cells of the bovine mammary gland. Cell Tissue Res. 1983;229(3):639–650. doi: 10.1007/BF00207703. [DOI] [PubMed] [Google Scholar]
  6. Bunning V. K., Donnelly C. W., Peeler J. T., Briggs E. H., Bradshaw J. G., Crawford R. G., Beliveau C. M., Tierney J. T. Thermal inactivation of Listeria monocytogenes within bovine milk phagocytes. Appl Environ Microbiol. 1988 Feb;54(2):364–370. doi: 10.1128/aem.54.2.364-370.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charlton K. M., Garcia M. M. Spontaneous listeric encephalitis and neuritis in sheep. Light microscopic studies. Vet Pathol. 1977 Jul;14(4):297–313. doi: 10.1177/030098587701400401. [DOI] [PubMed] [Google Scholar]
  8. Ciesielski C. A., Hightower A. W., Parsons S. K., Broome C. V. Listeriosis in the United States: 1980-1982. Arch Intern Med. 1988 Jun;148(6):1416–1419. [PubMed] [Google Scholar]
  9. Czuprynski C. J., Campbell P. A., Henson P. M. Killing of Listeria monocytogenes by human neutrophils and monocytes, but not by monocyte-derived macrophages. J Reticuloendothel Soc. 1983 Jul;34(1):29–44. [PubMed] [Google Scholar]
  10. Czuprynski C. J., Hamilton H. L. Bovine neutrophils ingest but do not kill Haemophilus somnus in vitro. Infect Immun. 1985 Nov;50(2):431–436. doi: 10.1128/iai.50.2.431-436.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Czuprynski C. J., Henson P. M., Campbell P. A. Enhanced accumulation of inflammatory neutrophils and macrophages mediated by transfer of T cells from mice immunized with Listeria monocytogenes. J Immunol. 1985 May;134(5):3449–3454. [PubMed] [Google Scholar]
  12. Czuprynski C. J., Henson P. M., Campbell P. A. Killing of Listeria monocytogenes by inflammatory neutrophils and mononuclear phagocytes from immune and nonimmune mice. J Leukoc Biol. 1984 Feb;35(2):193–208. doi: 10.1002/jlb.35.2.193. [DOI] [PubMed] [Google Scholar]
  13. Doyle M. P., Glass K. A., Beery J. T., Garcia G. A., Pollard D. J., Schultz R. D. Survival of Listeria monocytogenes in milk during high-temperature, short-time pasteurization. Appl Environ Microbiol. 1987 Jul;53(7):1433–1438. doi: 10.1128/aem.53.7.1433-1438.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fleming D. W., Cochi S. L., MacDonald K. L., Brondum J., Hayes P. S., Plikaytis B. D., Holmes M. B., Audurier A., Broome C. V., Reingold A. L. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med. 1985 Feb 14;312(7):404–407. doi: 10.1056/NEJM198502143120704. [DOI] [PubMed] [Google Scholar]
  15. Gitter M., Bradley R., Blampied P. H. Listeria monocytogenes infection in bovine mastitis. Vet Rec. 1980 Oct 25;107(17):390–393. doi: 10.1136/vr.107.17.390. [DOI] [PubMed] [Google Scholar]
  16. Godfrey R. W., Wilder M. S. Relationships between oxidative metabolism, macrophage activation, and antilisterial activity. J Leukoc Biol. 1984 Oct;36(4):533–543. doi: 10.1002/jlb.36.4.533. [DOI] [PubMed] [Google Scholar]
  17. Gray M. L., Killinger A. H. Listeria monocytogenes and listeric infections. Bacteriol Rev. 1966 Jun;30(2):309–382. doi: 10.1128/br.30.2.309-382.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hayes P. S., Feeley J. C., Graves L. M., Ajello G. W., Fleming D. W. Isolation of Listeria monocytogenes from raw milk. Appl Environ Microbiol. 1986 Feb;51(2):438–440. doi: 10.1128/aem.51.2.438-440.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hill A. W., Heneghan D. J., Williams M. R. The opsonic activity of bovine milk whey for the phagocytosis and killing by neutrophils of encapsulated and non-encapsulated Escherichia coli. Vet Microbiol. 1983 Jun;8(3):293–300. doi: 10.1016/0378-1135(83)90081-0. [DOI] [PubMed] [Google Scholar]
  20. Ho J. L., Shands K. N., Friedland G., Eckind P., Fraser D. W. An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitals. Arch Intern Med. 1986 Mar;146(3):520–524. [PubMed] [Google Scholar]
  21. Lane F. C., Unanue E. R. Requirement of thymus (T) lymphocytes for resistance to listeriosis. J Exp Med. 1972 May 1;135(5):1104–1112. doi: 10.1084/jem.135.5.1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Morgan J. H. Infectious keratoconjunctivitis in cattle associated with Listeria monocytocytogenes. Vet Rec. 1977 Feb 5;100(6):113–114. doi: 10.1136/vr.100.6.113. [DOI] [PubMed] [Google Scholar]
  23. NJOKU-OBI A. N., OSEBOLD J. W. Studies on mechanisms of immunity in listeriosis. I. Interaction of peritoneal exudate cells from sheep with Listeria monocytogenes in vitro. J Immunol. 1962 Aug;89:187–194. [PubMed] [Google Scholar]
  24. OLSON C., Jr, COOK R. H., BAGDONAS V. An attempt to immunize sheep during an outbreak of listeriosis. Am J Vet Res. 1951 Oct;12(45):306–313. [PubMed] [Google Scholar]
  25. OSEBOLD J. W., INOUYE T. Pathogenesis of Listeria monocytogenes infections in natural host. I. Rabbit studies. J Infect Dis. 1954 Jul-Aug;95(1):52–66. doi: 10.1093/infdis/95.1.52. [DOI] [PubMed] [Google Scholar]
  26. Paape M. J., Guidry A. J., Kirk S. T., Bolt D. J. Measurement of phagocytosis of 32P-labeled Staphylococcus aureus by bovine leukocytes: lysostaphin digestion and inhibitory effect of cream. Am J Vet Res. 1975 Dec;36(12):1737–1743. [PubMed] [Google Scholar]
  27. Paape M. J., Pearson R. E., Schultze W. D. Variation among cows in the ability of milk to support phagocytosis and in the ability of polymorphonuclear leukocytes to phagocytose Staphylococcus aureus. Am J Vet Res. 1978 Dec;39(12):1907–1910. [PubMed] [Google Scholar]
  28. Peterson P. K., Verhoef J., Schmeling D., Quie P. G. Kinetics of phagocytosis and bacterial killing by human polymorphonuclear leukocytes and monocytes. J Infect Dis. 1977 Oct;136(4):502–509. doi: 10.1093/infdis/136.4.502. [DOI] [PubMed] [Google Scholar]
  29. Russell M. W., Reiter B. Phagocytic deficiency of bovine milk leucocytes: an effect of casein. J Reticuloendothel Soc. 1975 Jul;18(1):1–13. [PubMed] [Google Scholar]
  30. Rácz P., Tenner K., Mérö E. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental listeria infection. Lab Invest. 1972 Jun;26(6):694–700. [PubMed] [Google Scholar]
  31. Savoini A., Marzari R., Dolzani L., Serranò D., Graziosi G., Gennaro R., Romeo D. Wide-spectrum antibiotic activity of bovine granulocyte polypeptides. Antimicrob Agents Chemother. 1984 Sep;26(3):405–407. doi: 10.1128/aac.26.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schlech W. F., 3rd, Lavigne P. M., Bortolussi R. A., Allen A. C., Haldane E. V., Wort A. J., Hightower A. W., Johnson S. E., King S. H., Nicholls E. S. Epidemic listeriosis--evidence for transmission by food. N Engl J Med. 1983 Jan 27;308(4):203–206. doi: 10.1056/NEJM198301273080407. [DOI] [PubMed] [Google Scholar]
  33. Selsted M. E., Szklarek D., Lehrer R. I. Purification and antibacterial activity of antimicrobial peptides of rabbit granulocytes. Infect Immun. 1984 Jul;45(1):150–154. doi: 10.1128/iai.45.1.150-154.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Siddique I. H., McKenzie B. E., Sapp W. J., Rich P. Light and electron microscopic study of the livers of pregnant mice infected with Listeria monocytogenes. Am J Vet Res. 1978 May;39(5):887–892. [PubMed] [Google Scholar]
  35. Smith J. W., Schultz R. D. Mitogen- and antigen-responsive milk lymphocytes. Cell Immunol. 1977 Mar 1;29(1):165–173. doi: 10.1016/0008-8749(77)90285-4. [DOI] [PubMed] [Google Scholar]
  36. Steigbigel R. T., Lambert L. H., Jr, Remington J. S. Phagocytic and bacterial properties of normal human monocytes. J Clin Invest. 1974 Jan;53(1):131–142. doi: 10.1172/JCI107531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Targowski S. P., Klucinski W. Effect of immune complexes from mastitic milk on blocking of Fc receptors and phagocytosis. Infect Immun. 1985 Feb;47(2):484–488. doi: 10.1128/iai.47.2.484-488.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Targowski S. P., Niemialtowski M. Inhibition of lacteal leukocyte phagocytosis by colostrum, nonlactating secretion, and mastitic milk. Am J Vet Res. 1986 Sep;47(9):1940–1945. [PubMed] [Google Scholar]
  39. Weis J., Seeliger H. P. Incidence of Listeria monocytogenes in nature. Appl Microbiol. 1975 Jul;30(1):29–32. doi: 10.1128/am.30.1.29-32.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Welch D. F., Sword C. P., Brehm S., Dusanic D. Relationship between superoxide dismutase and pathogenic mechanisms of Listeria monocytogenes. Infect Immun. 1979 Mar;23(3):863–872. doi: 10.1128/iai.23.3.863-872.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Clinical Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES