Abstract
Phagocytosis by bovine polymorphonuclear granulocytes of seven capsular polysaccharide type 5 Staphylococcus aureus strains isolated from mastitis [corrected] was investigated by means of luminol-dependent chemiluminescence. Bacteria were grown on four different agar media (brain heart infusion, Columbia broth, modified staphylococcus medium 110, and skim milk) and were opsonized by normal bovine serum. When compared to growth on brain heart infusion agar, Columbia agar, and modified staphylococcus medium 110 agar, growth on skim milk agar rendered five of the strains more resistant to opsonization. The other two strains were resistant in all culture media used. Short periods of incubation in milk after growth on brain heart infusion agar did not augment resistance to phagocytosis, indicating that mere adsorption of milk components on bacteria was not responsible. The variability of the chemiluminescence response of polymorphonuclear leukocytes was pronounced among strains with each growth medium except milk. Growth on modified staphylococcus medium 110 and on milk agar favored the masking of teichoic acid, as shown by inagglutinability with rabbit antiserum. Interestingly, agglutination by a monoclonal antibody to capsular polysaccharide type 5 was optimal when bacteria were grown on skim milk agar. This suggests that capsular polysaccharide participated in the masking effect. These findings indicate that masking of the bacterial target of most of the naturally acquired opsonins present in normal bovine serum occurred when bacteria grew in the presence of milk, resulting in an increased resistance to phagocytosis by polymorphonuclear leukocytes.
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- Anderson J. C. Absence of encapsulation in strains of Staphylococcus aureus isolated from bovine mastitis. Res Vet Sci. 1984 Nov;37(3):359–361. [PubMed] [Google Scholar]
- Brock J. H., Turvey A., Reiter B. Virulence of two mastitis strains of Staphylococcus aureus in bovine skin: enhancement by growth in high carbohydrate-high salt medium or in raw milk. Infect Immun. 1973 Jun;7(6):865–872. doi: 10.1128/iai.7.6.865-872.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butler J. E. Bovine immunoglobulins: an augmented review. Vet Immunol Immunopathol. 1983 Mar;4(1-2):43–152. doi: 10.1016/0165-2427(83)90056-9. [DOI] [PubMed] [Google Scholar]
- Carlson G. P., Kaneko J. J. Isolation of leukocytes from bovine peripheral blood. Proc Soc Exp Biol Med. 1973 Mar;142(3):853–856. doi: 10.3181/00379727-142-37131. [DOI] [PubMed] [Google Scholar]
- Dossett J. H., Kronvall G., Williams R. C., Jr, Quie P. G. Antiphagocytic effects of staphylococcal protein A. J Immunol. 1969 Dec;103(6):1405–1410. [PubMed] [Google Scholar]
- Eshelman J. E., Eberhart R. J., Scholz R. W. Effects of cream on bactericidal and metabolic functions of bovine polymorphonuclear neutrophils. Am J Vet Res. 1981 May;42(5):738–742. [PubMed] [Google Scholar]
- Fournier J. M., Hannon K., Moreau M., Karakawa W. W., Vann W. F. Isolation of type 5 capsular polysaccharide from Staphylococcus aureus. Ann Inst Pasteur Microbiol. 1987 Sep-Oct;138(5):561–567. doi: 10.1016/0769-2609(87)90041-x. [DOI] [PubMed] [Google Scholar]
- Fournier J. M., Vann W. F., Karakawa W. W. Purification and characterization of Staphylococcus aureus type 8 capsular polysaccharide. Infect Immun. 1984 Jul;45(1):87–93. doi: 10.1128/iai.45.1.87-93.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horan T. D., English D., McPherson T. A. Association of neutrophil chemiluminescence with microbicidal activity. Clin Immunol Immunopathol. 1982 Feb;22(2):259–269. doi: 10.1016/0090-1229(82)90042-3. [DOI] [PubMed] [Google Scholar]
- Johne B., Jarp J., Haaheim L. R. Staphylococcus aureus exopolysaccharide in vivo demonstrated by immunomagnetic separation and electron microscopy. J Clin Microbiol. 1989 Jul;27(7):1631–1635. doi: 10.1128/jcm.27.7.1631-1635.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karakawa W. W., Sutton A., Schneerson R., Karpas A., Vann W. F. Capsular antibodies induce type-specific phagocytosis of capsulated Staphylococcus aureus by human polymorphonuclear leukocytes. Infect Immun. 1988 May;56(5):1090–1095. doi: 10.1128/iai.56.5.1090-1095.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karakawa W. W., Young D. A. Immunological specificity of heat-stable opsonins in immune and nonimmune sera and their interaction with non-encapsulated and encapsulated strains of Staphylococcus aureus. Infect Immun. 1979 Jul;25(1):175–186. doi: 10.1128/iai.25.1.175-186.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leijh P. C., van den Barselaar M. T., Daha M. R., van Furth R. Participation of immunoglobulins and complement components in the intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Infect Immun. 1981 Sep;33(3):714–724. doi: 10.1128/iai.33.3.714-724.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Newbould F. H. Enhancement of phagocytosis in bovine milk leukocytes in vitro. Can J Comp Med. 1970 Jul;34(3):261–264. [PMC free article] [PubMed] [Google Scholar]
- Norcross N. L., Opdebeeck J. P. Encapsulation of Staphylococcus aureus isolated from bovine milk. Vet Microbiol. 1983 Aug;8(4):397–404. doi: 10.1016/0378-1135(83)90052-4. [DOI] [PubMed] [Google Scholar]
- Opdebeeck J. P., Frost A. J., O'Boyle D., Norcross N. L. The expression of capsule in serum-soft agar by Staphylococcus aureus isolated from bovine mastitis. Vet Microbiol. 1987 Mar;13(3):225–234. doi: 10.1016/0378-1135(87)90085-x. [DOI] [PubMed] [Google Scholar]
- Paape M. J., Wergin W. P., Guidry A. J., Pearson R. E. Leukocytes--second line of defense against invading mastitis pathogens. J Dairy Sci. 1979 Jan;62(1):135–153. doi: 10.3168/jds.S0022-0302(79)83215-4. [DOI] [PubMed] [Google Scholar]
- Peterson P. K., Wilkinson B. J., Kim Y., Schmeling D., Douglas S. D., Quie P. G., Verhoef J. The key role of peptidoglycan in the opsonization of Staphylococcus aureus. J Clin Invest. 1978 Mar;61(3):597–609. doi: 10.1172/JCI108971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poutrel B., Boutonnier A., Sutra L., Fournier J. M. Prevalence of capsular polysaccharide types 5 and 8 among Staphylococcus aureus isolates from cow, goat, and ewe milk. J Clin Microbiol. 1988 Jan;26(1):38–40. doi: 10.1128/jcm.26.1.38-40.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poutrel B., Caffin J. P. A sensitive microassay for the determination of hemolytic complement activity in bovine milk. Vet Immunol Immunopathol. 1983 Dec;5(2):177–184. doi: 10.1016/0165-2427(83)90018-1. [DOI] [PubMed] [Google Scholar]
- Poutrel B., Ducelliez M. Evaluation of three rapid tests for identification of Staphylococcus aureus isolated in bovine milk. Ann Rech Vet. 1979;10(1):125–129. [PubMed] [Google Scholar]
- Rather P. N., Davis A. P., Wilkinson B. J. Slime production by bovine milk Staphylococcus aureus and identification of coagulase-negative staphylococcal isolates. J Clin Microbiol. 1986 May;23(5):858–862. doi: 10.1128/jcm.23.5.858-862.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shayegani M., Hisatsune K., Mudd S. Cell Wall Component Which Affects the Ability of Serum to Promote Phagocytosis and Killing of Staphylococcus aureus. Infect Immun. 1970 Dec;2(6):750–756. doi: 10.1128/iai.2.6.750-756.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith M. R., Yoshida K., Naito Y. Use of the Clumping Factor Reaction for the Identification of Encapsulated Strains of Staphylococcus aureus from Human Sources. Infect Immun. 1971 May;3(5):707–708. doi: 10.1128/iai.3.5.707-708.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sompolinsky D., Samra Z., Karakawa W. W., Vann W. F., Schneerson R., Malik Z. Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. J Clin Microbiol. 1985 Nov;22(5):828–834. doi: 10.1128/jcm.22.5.828-834.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutra L., Mendolia C., Rainard P., Poutrel B. Encapsulation of Staphylococcus aureus isolates from mastitic milk: relationship between capsular polysaccharide types 5 and 8 and colony morphology in serum-soft agar, clumping factor, teichoic acid, and protein A. J Clin Microbiol. 1990 Mar;28(3):447–451. doi: 10.1128/jcm.28.3.447-451.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watson D. L. Enhancement of in vitro phagocytosis of Staphylococcus aureas by polymorphonuclear leucocytes. Res Vet Sci. 1975 Nov;19(3):288–292. [PubMed] [Google Scholar]
- Watson D. L. The effect of cytophilic IgG2 on phagocytosis by ovine polymorphonuclear leucocytes. Immunology. 1976 Aug;31(2):159–165. [PMC free article] [PubMed] [Google Scholar]
- Watson D. L. Virulence of Staphylococcus aureus grown in vitro or in vivo. Res Vet Sci. 1982 May;32(3):311–315. [PubMed] [Google Scholar]
- Watson D. L., Watson N. A. Expression of a pseudocapsule by Staphylococcus aureus: influence of cultural conditions and relevance to mastitis. Res Vet Sci. 1989 Sep;47(2):152–157. [PubMed] [Google Scholar]
- Williams M. R., Hill A. W. A role for IgM in the in vitro opsonisation of Staphylococcus aureus and Escherichia coli by bovine polymorphonuclear leucocytes. Res Vet Sci. 1982 Jul;33(1):47–53. [PubMed] [Google Scholar]
- Yoshida K., Ekstedt R. D. Relation of mucoid growth of Staphylococcus aureus to clumping factor reaction, morphology in serum-soft agar, and virulence. J Bacteriol. 1968 Oct;96(4):902–908. doi: 10.1128/jb.96.4.902-908.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshida K., Smith M. R., Naito Y. Biological and Immunological Properties of Encapsulated Strains of Staphylococcus aureus from Human Sources. Infect Immun. 1970 Nov;2(5):528–532. doi: 10.1128/iai.2.5.528-532.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]