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. 1997 Dec;65(12):5137–5141. doi: 10.1128/iai.65.12.5137-5141.1997

Internalin B promotes the replication of Listeria monocytogenes in mouse hepatocytes.

S H Gregory 1, A J Sagnimeni 1, E J Wing 1
PMCID: PMC175740  PMID: 9393807

Abstract

The uptake of Listeria monocytogenes by a variety of cell types in vitro is facilitated by the protein products of the inlAB (internalin) operon expressed by the organism. In the case of mouse hepatocytes, the extent to which inlAB expression influenced the uptake of Listeria in vitro was markedly dependent upon the ratio of bacteria to cells. At a ratio of 100:1, greater than 40-fold fewer transposon-induced inl4B mutant listeriae entered hepatocytes compared to the isogenic wild-type control; the difference was only fourfold, however, in cultures inoculated at a 1:1 ratio. Similarly, the uptake of in-frame inlB or inlAB deletion mutants differed only fourfold from the uptake of wild-type or inlA mutant Listeria at a 1:1 multiplicity of infection. Mutations affecting inlB or inlAB, on the other hand, resulted in a marked decrease in the capacity of Listeria to proliferate within mouse hepatocytes in vivo and in vitro. Electron micrographs of Listeria-infected hepatocytes demonstrated the impaired capacity of inlB mutants to escape from endocytic vacuoles and to enter the cytoplasm where proliferation occurs. These findings indicate that the protein product of inlB exerts a significant effect on the intracellular replication of Listeria.

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Selected References

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  1. Alvarez-Domínguez C., Vázquez-Boland J. A., Carrasco-Marín E., López-Mato P., Leyva-Cobián F. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun. 1997 Jan;65(1):78–88. doi: 10.1128/iai.65.1.78-88.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Domann E., Zechel S., Lingnau A., Hain T., Darji A., Nichterlein T., Wehland J., Chakraborty T. Identification and characterization of a novel PrfA-regulated gene in Listeria monocytogenes whose product, IrpA, is highly homologous to internalin proteins, which contain leucine-rich repeats. Infect Immun. 1997 Jan;65(1):101–109. doi: 10.1128/iai.65.1.101-109.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol. 1995 Apr;16(2):251–261. doi: 10.1111/j.1365-2958.1995.tb02297.x. [DOI] [PubMed] [Google Scholar]
  4. Dramsi S., Dehoux P., Lebrun M., Goossens P. L., Cossart P. Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun. 1997 May;65(5):1615–1625. doi: 10.1128/iai.65.5.1615-1625.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Gaillard J. L., Finlay B. B. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. Infect Immun. 1996 Apr;64(4):1299–1308. doi: 10.1128/iai.64.4.1299-1308.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaillard J. L., Jaubert F., Berche P. The inlAB locus mediates the entry of Listeria monocytogenes into hepatocytes in vivo. J Exp Med. 1996 Feb 1;183(2):359–369. doi: 10.1084/jem.183.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gregory S. H., Barczynski L. K., Wing E. J. Effector function of hepatocytes and Kupffer cells in the resolution of systemic bacterial infections. J Leukoc Biol. 1992 Apr;51(4):421–424. doi: 10.1002/jlb.51.4.421. [DOI] [PubMed] [Google Scholar]
  9. Gregory S. H., Sagnimeni A. J., Wing E. J. Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J Immunol. 1996 Sep 15;157(6):2514–2520. [PubMed] [Google Scholar]
  10. Gregory S. H., Sagnimeni A. J., Wing E. J. Expression of the inlAB operon by Listeria monocytogenes is not required for entry into hepatic cells in vivo. Infect Immun. 1996 Oct;64(10):3983–3986. doi: 10.1128/iai.64.10.3983-3986.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gregory S. H., Wing E. J. IFN-gamma inhibits the replication of Listeria monocytogenes in hepatocytes. J Immunol. 1993 Aug 1;151(3):1401–1409. [PubMed] [Google Scholar]
  12. Havell E. A. Evidence that tumor necrosis factor has an important role in antibacterial resistance. J Immunol. 1989 Nov 1;143(9):2894–2899. [PubMed] [Google Scholar]
  13. Hess J., Gentschev I., Szalay G., Ladel C., Bubert A., Goebel W., Kaufmann S. H. Listeria monocytogenes p60 supports host cell invasion by and in vivo survival of attenuated Salmonella typhimurium. Infect Immun. 1995 May;63(5):2047–2053. doi: 10.1128/iai.63.5.2047-2053.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jones D. Foodborne listeriosis. Lancet. 1990 Nov 10;336(8724):1171–1174. doi: 10.1016/0140-6736(90)92778-g. [DOI] [PubMed] [Google Scholar]
  15. Kaufmann S. H. Immunity to intracellular bacteria. Annu Rev Immunol. 1993;11:129–163. doi: 10.1146/annurev.iy.11.040193.001021. [DOI] [PubMed] [Google Scholar]
  16. Lingnau A., Domann E., Hudel M., Bock M., Nichterlein T., Wehland J., Chakraborty T. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect Immun. 1995 Oct;63(10):3896–3903. doi: 10.1128/iai.63.10.3896-3903.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Patek P. Q., Collins J. L., Cohn M. Transformed cell lines susceptible or resistant to in vivo surveillance against tumorigenesis. Nature. 1978 Nov 30;276(5687):510–511. doi: 10.1038/276510a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Rosen H., Gordon S., North R. J. Exacerbation of murine listeriosis by a monoclonal antibody specific for the type 3 complement receptor of myelomonocytic cells. Absence of monocytes at infective foci allows Listeria to multiply in nonphagocytic cells. J Exp Med. 1989 Jul 1;170(1):27–37. doi: 10.1084/jem.170.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sawyer R. T., Drevets D. A., Campbell P. A., Potter T. A. Internalin A can mediate phagocytosis of Listeria monocytogenes by mouse macrophage cell lines. J Leukoc Biol. 1996 Nov;60(5):603–610. doi: 10.1002/jlb.60.5.603. [DOI] [PubMed] [Google Scholar]
  21. Schuchat A., Deaver K. A., Wenger J. D., Plikaytis B. D., Mascola L., Pinner R. W., Reingold A. L., Broome C. V. Role of foods in sporadic listeriosis. I. Case-control study of dietary risk factors. The Listeria Study Group. JAMA. 1992 Apr 15;267(15):2041–2045. [PubMed] [Google Scholar]
  22. Tilney L. G., Portnoy D. A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989 Oct;109(4 Pt 1):1597–1608. doi: 10.1083/jcb.109.4.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wing E. J., Kresefsky-Friedman D. Y. Decreased resistance to Listeria monocytogenes in mice injected with killed corynebacterium parvum: association with suppression of cell-mediated immunity. J Infect Dis. 1980 Feb;141(2):203–211. doi: 10.1093/infdis/141.2.203. [DOI] [PubMed] [Google Scholar]

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