Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1994 Oct;62(10):4641–4645. doi: 10.1128/iai.62.10.4641-4645.1994

Salmonella invasion of nonphagocytic cells induces formation of macropinosomes in the host cell.

F Garcia-del Portillo 1, B B Finlay 1
PMCID: PMC303156  PMID: 7927733

Abstract

Salmonella typhimurium induced massive uptake of extracellular fluid in epithelial cells in the form of macropinosomes. The appearance of macropinosomes in the infected cell was related to the induction of membrane ruffling during bacterial invasion. A noninvasive S. typhimurium invA mutant did not trigger such effects in the host cell. Similarly, S. typhimurium invA mutants that invaded via the invasin protein from Yersinia pseudotuberculosis or adhered to the host cell via the afimbrial AFA-I adhesin from Escherichia coli did not trigger formation of macropinosomes. In contrast to the formation of macropinosomes in macrophages, the appearance of macropinosomes in S. typhimurium-infected epithelial cells did not require microtubules. These data suggest that massive uptake of extracellular fluid in S. typhimurium-infected epithelial cells is an event related to the invasion mechanisms used by this pathogen.

Full text

PDF
4641

Images in this article

4642Image
on p.4642
4643Image
on p.4643
4644Image
on p.4644

Selected References

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

  1. Alpuche Aranda C. M., Swanson J. A., Loomis W. P., Miller S. I. Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10079–10083. doi: 10.1073/pnas.89.21.10079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alpuche-Aranda C. M., Racoosin E. L., Swanson J. A., Miller S. I. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med. 1994 Feb 1;179(2):601–608. doi: 10.1084/jem.179.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Behlau I., Miller S. I. A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J Bacteriol. 1993 Jul;175(14):4475–4484. doi: 10.1128/jb.175.14.4475-4484.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Falkow S., Isberg R. R., Portnoy D. A. The interaction of bacteria with mammalian cells. Annu Rev Cell Biol. 1992;8:333–363. doi: 10.1146/annurev.cb.08.110192.002001. [DOI] [PubMed] [Google Scholar]
  5. Finlay B. B., Falkow S. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990 Nov;162(5):1096–1106. doi: 10.1093/infdis/162.5.1096. [DOI] [PubMed] [Google Scholar]
  6. Finlay B. B., Ruschkowski S., Dedhar S. Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. J Cell Sci. 1991 Jun;99(Pt 2):283–296. doi: 10.1242/jcs.99.2.283. [DOI] [PubMed] [Google Scholar]
  7. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature. 1993 Aug 12;364(6438):639–642. doi: 10.1038/364639a0. [DOI] [PubMed] [Google Scholar]
  8. Francis C. L., Starnbach M. N., Falkow S. Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol Microbiol. 1992 Nov;6(21):3077–3087. doi: 10.1111/j.1365-2958.1992.tb01765.x. [DOI] [PubMed] [Google Scholar]
  9. Gahring L. C., Heffron F., Finlay B. B., Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun. 1990 Feb;58(2):443–448. doi: 10.1128/iai.58.2.443-448.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galán J. E., Curtiss R., 3rd Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383–6387. doi: 10.1073/pnas.86.16.6383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Galán J. E., Ginocchio C., Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992 Jul;174(13):4338–4349. doi: 10.1128/jb.174.13.4338-4349.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garcia-del Portillo F., Zwick M. B., Leung K. Y., Finlay B. B. Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10544–10548. doi: 10.1073/pnas.90.22.10544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoiseth S. K., Stocker B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 1981 May 21;291(5812):238–239. doi: 10.1038/291238a0. [DOI] [PubMed] [Google Scholar]
  14. Isberg R. R., Voorhis D. L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. doi: 10.1016/0092-8674(87)90335-7. [DOI] [PubMed] [Google Scholar]
  15. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 1989;5:483–525. doi: 10.1146/annurev.cb.05.110189.002411. [DOI] [PubMed] [Google Scholar]
  16. Labigne-Roussel A. F., Lark D., Schoolnik G., Falkow S. Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun. 1984 Oct;46(1):251–259. doi: 10.1128/iai.46.1.251-259.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Leung K. Y., Finlay B. B. Intracellular replication is essential for the virulence of Salmonella typhimurium. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11470–11474. doi: 10.1073/pnas.88.24.11470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Leung K. Y., Ruschkowski S. R., Finlay B. B. Isolation and characterization of the aadA aminoglycoside-resistance gene from Salmonella choleraesuis. Mol Microbiol. 1992 Sep;6(17):2453–2460. doi: 10.1111/j.1365-2958.1992.tb01421.x. [DOI] [PubMed] [Google Scholar]
  19. Miller S. I., Mekalanos J. J. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol. 1990 May;172(5):2485–2490. doi: 10.1128/jb.172.5.2485-2490.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pace J., Hayman M. J., Galán J. E. Signal transduction and invasion of epithelial cells by S. typhimurium. Cell. 1993 Feb 26;72(4):505–514. doi: 10.1016/0092-8674(93)90070-7. [DOI] [PubMed] [Google Scholar]
  21. Racoosin E. L., Swanson J. A. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci. 1992 Aug;102(Pt 4):867–880. doi: 10.1242/jcs.102.4.867. [DOI] [PubMed] [Google Scholar]
  22. Racoosin E. L., Swanson J. A. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol. 1993 Jun;121(5):1011–1020. doi: 10.1083/jcb.121.5.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Takeuchi A. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am J Pathol. 1967 Jan;50(1):109–136. [PMC free article] [PubMed] [Google Scholar]
  24. von Figura K., Hasilik A. Lysosomal enzymes and their receptors. Annu Rev Biochem. 1986;55:167–193. doi: 10.1146/annurev.bi.55.070186.001123. [DOI] [PubMed] [Google Scholar]

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

RESOURCES