Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1996 Sep;64(9):3925–3929. doi: 10.1128/iai.64.9.3925-3929.1996

Iron availability affects entry of Listeria monocytogenes into the enterocytelike cell line Caco-2.

M P Conte 1, C Longhi 1, M Polidoro 1, G Petrone 1, V Buonfiglio 1, S Di Santo 1, E Papi 1, L Seganti 1, P Visca 1, P Valenti 1
PMCID: PMC174316  PMID: 8751952

Abstract

The influence of iron on the entry of Listeria monocytogenes into Caco-2 cells was studied. Iron availability was found to modify the surface hydrophobicity and protein profile of L. monocytogenes, with the result that cell invasion strongly increased upon bacterial growth in iron-rich medium. The enhanced invasive capability of iron-overloaded L. monocytogenes cells correlates to the higher-level expression of the inlAB virulence genes, which were positively iron regulated at the transcriptional level.

Full Text

The Full Text of this article is available as a PDF (409.0 KB).

Selected References

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

  1. Adams T. J., Vartivarian S., Cowart R. E. Iron acquisition systems of Listeria monocytogenes. Infect Immun. 1990 Aug;58(8):2715–2718. doi: 10.1128/iai.58.8.2715-2718.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  3. Conlan J. W., North R. J. Early pathogenesis of infection in the liver with the facultative intracellular bacteria Listeria monocytogenes, Francisella tularensis, and Salmonella typhimurium involves lysis of infected hepatocytes by leukocytes. Infect Immun. 1992 Dec;60(12):5164–5171. doi: 10.1128/iai.60.12.5164-5171.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Conte M. P., Longhi C., Buonfiglio V., Polidoro M., Seganti L., Valenti P. The effect of iron on the invasiveness of Escherichia coli carrying the inv gene of Yersinia pseudotuberculosis. J Med Microbiol. 1994 Apr;40(4):236–240. doi: 10.1099/00222615-40-4-236. [DOI] [PubMed] [Google Scholar]
  5. Conte M. P., Longhi C., Petrone G., Polidoro M., Valenti P., Seganti L. Listeria monocytogenes infection of Caco-2 cells: role of growth temperature. Res Microbiol. 1994 Nov-Dec;145(9):677–682. doi: 10.1016/0923-2508(94)90039-6. [DOI] [PubMed] [Google Scholar]
  6. Cossart P., Vicente M. F., Mengaud J., Baquero F., Perez-Diaz J. C., Berche P. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun. 1989 Nov;57(11):3629–3636. doi: 10.1128/iai.57.11.3629-3636.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cowart R. E., Foster B. G. Differential effects of iron on the growth of Listeria monocytogenes: minimum requirements and mechanism of acquisition. J Infect Dis. 1985 Apr;151(4):721–730. doi: 10.1093/infdis/151.4.721. [DOI] [PubMed] [Google Scholar]
  8. Deneer H. G., Healey V., Boychuk I. Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp. Microbiology. 1995 Aug;141(Pt 8):1985–1992. doi: 10.1099/13500872-141-8-1985. [DOI] [PubMed] [Google Scholar]
  9. Domann E., Wehland J., Niebuhr K., Haffner C., Leimeister-Wächter M., Chakraborty T. Detection of a prfA-independent promoter responsible for listeriolysin gene expression in mutant Listeria monocytogenes strains lacking the PrfA regulator. Infect Immun. 1993 Jul;61(7):3073–3075. doi: 10.1128/iai.61.7.3073-3075.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dominguez Rodriguez L., Vazquez Boland J. A., Fernandez Garayzabal J. F., Echalecu Tranchant P., Gomez-Lucia E., Rodriguez Ferri E. F., Suarez Fernandez G. Microplate technique to determine hemolytic activity for routine typing of Listeria strains. J Clin Microbiol. 1986 Jul;24(1):99–103. doi: 10.1128/jcm.24.1.99-103.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dramsi S., Kocks C., Forestier C., Cossart P. Internalin-mediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator prfA. Mol Microbiol. 1993 Sep;9(5):931–941. doi: 10.1111/j.1365-2958.1993.tb01223.x. [DOI] [PubMed] [Google Scholar]
  12. Freitag N. E., Portnoy D. A. Dual promoters of the Listeria monocytogenes prfA transcriptional activator appear essential in vitro but are redundant in vivo. Mol Microbiol. 1994 Jun;12(5):845–853. doi: 10.1111/j.1365-2958.1994.tb01070.x. [DOI] [PubMed] [Google Scholar]
  13. Gaillard J. L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991 Jun 28;65(7):1127–1141. doi: 10.1016/0092-8674(91)90009-n. [DOI] [PubMed] [Google Scholar]
  14. Geoffroy C., Gaillard J. L., Alouf J. E., Berche P. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect Immun. 1987 Jul;55(7):1641–1646. doi: 10.1128/iai.55.7.1641-1646.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hartford T., O'Brien S., Andrew P. W., Jones D., Roberts I. S. Utilization of transferrin-bound iron by Listeria monocytogenes. FEMS Microbiol Lett. 1993 Apr 15;108(3):311–318. doi: 10.1111/j.1574-6968.1993.tb06121.x. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Leimeister-Wächter M., Domann E., Chakraborty T. The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol. 1992 Feb;174(3):947–952. doi: 10.1128/jb.174.3.947-952.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Litwin C. M., Calderwood S. B. Role of iron in regulation of virulence genes. Clin Microbiol Rev. 1993 Apr;6(2):137–149. doi: 10.1128/cmr.6.2.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mengaud J., Chenevert J., Geoffroy C., Gaillard J. L., Cossart P. Identification of the structural gene encoding the SH-activated hemolysin of Listeria monocytogenes: listeriolysin O is homologous to streptolysin O and pneumolysin. Infect Immun. 1987 Dec;55(12):3225–3227. doi: 10.1128/iai.55.12.3225-3227.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mounier J., Ryter A., Coquis-Rondon M., Sansonetti P. J. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun. 1990 Apr;58(4):1048–1058. doi: 10.1128/iai.58.4.1048-1058.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Neilands J. B. Iron absorption and transport in microorganisms. Annu Rev Nutr. 1981;1:27–46. doi: 10.1146/annurev.nu.01.070181.000331. [DOI] [PubMed] [Google Scholar]
  22. Neilands J. B. Microbial envelope proteins related to iron. Annu Rev Microbiol. 1982;36:285–309. doi: 10.1146/annurev.mi.36.100182.001441. [DOI] [PubMed] [Google Scholar]
  23. Portnoy D. A., Chakraborty T., Goebel W., Cossart P. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun. 1992 Apr;60(4):1263–1267. doi: 10.1128/iai.60.4.1263-1267.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Rácz P., Tenner K., Szivessy K. Electron microscopic studies in experimental keratoconjunctivitis listeriosa. I. Penetration of Listeria monocytogenes into corneal epithelial cells. Acta Microbiol Acad Sci Hung. 1970;17(3):221–236. [PubMed] [Google Scholar]
  26. Sokolovic Z., Riedel J., Wuenscher M., Goebel W. Surface-associated, PrfA-regulated proteins of Listeria monocytogenes synthesized under stress conditions. Mol Microbiol. 1993 Apr;8(2):219–227. doi: 10.1111/j.1365-2958.1993.tb01566.x. [DOI] [PubMed] [Google Scholar]
  27. Sword C. P. Mechanisms of pathogenesis in Listeria monocytogenes infection. I. Influence of iron. J Bacteriol. 1966 Sep;92(3):536–542. doi: 10.1128/jb.92.3.536-542.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tabouret M., de Rycke J., Dubray G. Analysis of surface proteins of Listeria in relation to species, serovar and pathogenicity. J Gen Microbiol. 1992 Apr;138(4):743–753. doi: 10.1099/00221287-138-4-743. [DOI] [PubMed] [Google Scholar]
  29. Tao X., Schiering N., Zeng H. Y., Ringe D., Murphy J. R. Iron, DtxR, and the regulation of diphtheria toxin expression. Mol Microbiol. 1994 Oct;14(2):191–197. doi: 10.1111/j.1365-2958.1994.tb01280.x. [DOI] [PubMed] [Google Scholar]
  30. Weinberg E. D. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. doi: 10.1152/physrev.1984.64.1.65. [DOI] [PubMed] [Google Scholar]

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

RESOURCES