Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Infection and Immunity logoLink to Infection and Immunity
. 1996 Dec;64(12):5015–5021. doi: 10.1128/iai.64.12.5015-5021.1996

In vitro attachment and invasion of chicken ovarian granulosa cells by Salmonella enteritidis phage type 8.

D Thiagarajan 1, M Saeed 1, J Turek 1, E Asem 1
PMCID: PMC174482  PMID: 8945540

Abstract

The attachment and invasion of chicken ovarian granulosa cells by Salmonella enteritidis was examined in vitro. The attachment was inhibited by preincubation of granulosa cells with anti-chicken fibronectin antibody (approximately 70% reduction in attachment) or preincubation with a 14-kDa fimbrial protein isolated from S. enteritidis (68% reduction in attachment). Treatment of bacterial cells with the tetrapeptide RGDS before addition to granulosa cells resulted in inhibition of attachment (60% inhibition when 2 x 10(7) CFU of bacteria was treated with 500 microg of peptide). Treatment with the peptide GRGD resulted in similar magnitude of inhibition, indicating that extracellular matrix proteins play significant roles in the interaction of S. enteritidis with granulosa cells. In contrast, treatment of the bacterial cells with the peptide GRAD did not result in significant inhibition of attachment to the granulosa cells. S. enteritidis was found to attach specifically to fibronectin, collagen IV, and laminin-coated microtiter plate wells, with the rank order of attachment as follows: fibronectin > laminin > collagen IV. Light and transmission electron micrographs of S. enteritidis invasion of granulosa cells showed organisms with or without a surrounding membrane in the cytoplasm of granulosa cells. In some instances, dividing bacterial cells were observed in the cytoplasm. Results of this study demonstrated that S. enteritidis interacts with granulosa cells in a specific manner and can invade and multiply in these cells. The granulosa cell layer of the preovulatory follicles may be a preferred site for the colonization of the chicken ovaries by invasive strains of S. enteritidis.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Aslanzadeh J., Paulissen L. J. Role of type 1 and type 3 fimbriae on the adherence and pathogenesis of Salmonella enteritidis in mice. Microbiol Immunol. 1992;36(4):351–359. doi: 10.1111/j.1348-0421.1992.tb02034.x. [DOI] [PubMed] [Google Scholar]
  2. Baloda S. B., Faris A., Krovacek K. Cell-surface properties of enterotoxigenic and cytotoxic Salmonella enteritidis and Salmonella typhimurium: studies on hemagglutination, cell-surface hydrophobicity, attachment to human intestinal cells and fibronectin-binding. Microbiol Immunol. 1988;32(5):447–459. doi: 10.1111/j.1348-0421.1988.tb01405.x. [DOI] [PubMed] [Google Scholar]
  3. Collinson S. K., Emödy L., Müller K. H., Trust T. J., Kay W. W. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4773–4781. doi: 10.1128/jb.173.15.4773-4781.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cowden J. M., Chisholm D., O'Mahony M., Lynch D., Mawer S. L., Spain G. E., Ward L., Rowe B. Two outbreaks of Salmonella enteritidis phage type 4 infection associated with the consumption of fresh shell-egg products. Epidemiol Infect. 1989 Aug;103(1):47–52. doi: 10.1017/s095026880003034x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cowden J. M., Lynch D., Joseph C. A., O'Mahony M., Mawer S. L., Rowe B., Bartlett C. L. Case-control study of infections with Salmonella enteritidis phage type 4 in England. BMJ. 1989 Sep 23;299(6702):771–773. doi: 10.1136/bmj.299.6702.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coyle E. F., Palmer S. R., Ribeiro C. D., Jones H. I., Howard A. J., Ward L., Rowe B. Salmonella enteritidis phage type 4 infection: association with hen's eggs. Lancet. 1988 Dec 3;2(8623):1295–1297. doi: 10.1016/s0140-6736(88)92902-9. [DOI] [PubMed] [Google Scholar]
  7. Duguid J. P., Anderson E. S., Campbell I. Fimbriae and adhesive properties in Salmonellae. J Pathol Bacteriol. 1966 Jul;92(1):107–138. doi: 10.1002/path.1700920113. [DOI] [PubMed] [Google Scholar]
  8. Feutrier J., Kay W. W., Trust T. J. Purification and characterization of fimbriae from Salmonella enteritidis. J Bacteriol. 1986 Oct;168(1):221–227. doi: 10.1128/jb.168.1.221-227.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gast R. K., Beard C. W. Evaluation of a chick mortality model for predicting the consequences of Salmonella enteritidis infections in laying hens. Poult Sci. 1992 Feb;71(2):281–287. doi: 10.3382/ps.0710281. [DOI] [PubMed] [Google Scholar]
  11. Gast R. K., Beard C. W. Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. Avian Dis. 1990 Oct-Dec;34(4):991–993. [PubMed] [Google Scholar]
  12. Gast R. K., Beard C. W. Production of Salmonella enteritidis-contaminated eggs by experimentally infected hens. Avian Dis. 1990 Apr-Jun;34(2):438–446. [PubMed] [Google Scholar]
  13. Gilbert A. B., Evans A. J., Perry M. M., Davidson M. H. A method for separating the granulosa cells, the basal lamina and the theca of the preovulatory ovarian follicle of the domestic fowl (Gallus domesticus). J Reprod Fertil. 1977 May;50(1):179–181. doi: 10.1530/jrf.0.0500179. [DOI] [PubMed] [Google Scholar]
  14. Hinton M., Threlfall E. J., Rowe B. The invasiveness of different strains of Salmonella enteritidis phage type 4 for young chickens. FEMS Microbiol Lett. 1990 Jul;58(2):193–195. doi: 10.1111/j.1574-6968.1990.tb13977.x. [DOI] [PubMed] [Google Scholar]
  15. Hopper S. A., Mawer S. Salmonella enteritidis in a commercial layer flock. Vet Rec. 1988 Sep 24;123(13):351–351. doi: 10.1136/vr.123.13.351. [DOI] [PubMed] [Google Scholar]
  16. Kukkonen M., Raunio T., Virkola R., Lähteenmäki K., Mäkelä P. H., Klemm P., Clegg S., Korhonen T. K. Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin. Mol Microbiol. 1993 Jan;7(2):229–237. doi: 10.1111/j.1365-2958.1993.tb01114.x. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Lin F. Y., Morris J. G., Jr, Trump D., Tilghman D., Wood P. K., Jackman N., Israel E., Libonati J. P. Investigation of an outbreak of Salmonella enteritidis gastroenteritis associated with consumption of eggs in a restaurant chain in Maryland. Am J Epidemiol. 1988 Oct;128(4):839–844. doi: 10.1093/oxfordjournals.aje.a115037. [DOI] [PubMed] [Google Scholar]
  19. Lindell K. A., Saeed A. M., McCabe G. P. Evaluation of resistance of four strains of commercial laying hens to experimental infection with Salmonella enteritidis phage type eight. Poult Sci. 1994 Jun;73(6):757–762. doi: 10.3382/ps.0730757. [DOI] [PubMed] [Google Scholar]
  20. Lister S. A. Salmonella enteritidis infection in broilers and broiler breeders. Vet Rec. 1988 Sep 24;123(13):350–350. doi: 10.1136/vr.123.13.350. [DOI] [PubMed] [Google Scholar]
  21. Mehlman I. J., Eide E. L., Sanders A. C., Fishbein M., Aulisio C. C. Methodology for recognition of invasive potential of Escherichia coli. J Assoc Off Anal Chem. 1977 May;60(3):546–562. [PubMed] [Google Scholar]
  22. Novero R. P., Asem E. K. Follicle-stimulating hormone-enhanced fibronectin production by chicken granulosa cells is influenced by follicular development. Poult Sci. 1993 Apr;72(4):709–721. doi: 10.3382/ps.0720709. [DOI] [PubMed] [Google Scholar]
  23. Pierschbacher M. D., Ruoslahti E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J Biol Chem. 1987 Dec 25;262(36):17294–17298. [PubMed] [Google Scholar]
  24. Pierschbacher M. D., Ruoslahti E. Variants of the cell recognition site of fibronectin that retain attachment-promoting activity. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5985–5988. doi: 10.1073/pnas.81.19.5985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Popiel I., Turnbull P. C. Passage of Salmonella enteritidis and Salmonella thompson through chick ileocecal mucosa. Infect Immun. 1985 Mar;47(3):786–792. doi: 10.1128/iai.47.3.786-792.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shivaprasad H. L., Timoney J. F., Morales S., Lucio B., Baker R. C. Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serologic responses. Avian Dis. 1990 Jul-Sep;34(3):548–557. [PubMed] [Google Scholar]
  27. St Louis M. E., Morse D. L., Potter M. E., DeMelfi T. M., Guzewich J. J., Tauxe R. V., Blake P. A. The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. JAMA. 1988 Apr 8;259(14):2103–2107. [PubMed] [Google Scholar]
  28. Thiagarajan D., Saeed A. M., Asem E. K. Mechanism of transovarian transmission of Salmonella enteritidis in laying hens. Poult Sci. 1994 Jan;73(1):89–98. doi: 10.3382/ps.0730089. [DOI] [PubMed] [Google Scholar]
  29. Timoney J. F., Shivaprasad H. L., Baker R. C., Rowe B. Egg transmission after infection of hens with Salmonella enteritidis phage type 4. Vet Rec. 1989 Dec 9;125(24):600–601. [PubMed] [Google Scholar]
  30. Yamada K. M. Cell surface interactions with extracellular materials. Annu Rev Biochem. 1983;52:761–799. doi: 10.1146/annurev.bi.52.070183.003553. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES