1887

Abstract

Most studies on serovar Typhimurium infection focus on strains ATCC SL1344 or NTCC 12023 (ATCC 14028). We have compared the abilities of these strains to induce membrane ruffles and invade epithelial cells. . Typhimurium strain 12023 is less invasive and induces smaller membrane ruffles on MDCK cells compared with SL1344. Since the SPI-1 effector SopE is present in SL1344 and absent from 12023, and SL1344 mutants have reduced invasiveness, we investigated whether 12023 is less invasive due to the absence of SopE. However, comparison of SopE and SopE . Typhimurium strains, deletion mutants and 12023 expressing a plasmid revealed no consistent relationship between SopE status and relative invasiveness. Nevertheless, absence of SopE was closely correlated with reduced size of membrane ruffles. A P reporter revealed that relatively few of the 12023 population (and that of the equivalent strain ATCC 14028) express SPI-1 compared to other . Typhimurium strains. Expression of a P reporter mirrored that of P in 12023 and SL1344, implicating reduced signalling via the transcription factor HilA in the heterogeneous SPI-1 expression of these strains. The previously unrecognized strain heterogeneity in SPI-1 expression and invasiveness has important implications for studies of infection.

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2011-07-01
2020-01-23
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References

  1. Boddicker J. D., Jones B. D.. ( 2004;). Lon protease activity causes down-regulation of Salmonella pathogenicity island 1 invasion gene expression after infection of epithelial cells. Infect Immun72:2002–2013 [CrossRef][PubMed]
    [Google Scholar]
  2. Bruno V. M., Hannemann S., Lara-Tejero M., Flavell R. A., Kleinstein S. H., Galán J. E.. ( 2009;). Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog5:e1000538 [CrossRef][PubMed]
    [Google Scholar]
  3. Bujny M. V., Ewels P. A., Humphrey S., Attar N., Jepson M. A., Cullen P. J.. ( 2008;). Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J Cell Sci121:2027–2036 [CrossRef][PubMed]
    [Google Scholar]
  4. Clark L., Martinez-Argudo I., Humphrey T. J., Jepson M. A.. ( 2009;). GFP plasmid-induced defects in Salmonella invasion depend on plasmid architecture, not protein expression. Microbiology155:461–467 [CrossRef][PubMed]
    [Google Scholar]
  5. Datsenko K. A., Wanner B. L.. ( 2000;). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645 [CrossRef][PubMed]
    [Google Scholar]
  6. Ellermeier J. R., Slauch J. M.. ( 2007;). Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol10:24–29 [CrossRef][PubMed]
    [Google Scholar]
  7. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S.. ( 1993;). Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature364:639–642 [CrossRef][PubMed]
    [Google Scholar]
  8. Fu Y., Galán J. E.. ( 1999;). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature401:293–297 [CrossRef][PubMed]
    [Google Scholar]
  9. Hänisch J., Ehinger J., Ladwein M., Rohde M., Derivery E., Bosse T., Steffen A., Bumann D., Misselwitz B. et al. ( 2010;). Molecular dissection of Salmonella-induced membrane ruffling versus invasion. Cell Microbiol12:84–98 [CrossRef][PubMed]
    [Google Scholar]
  10. Hardt W. D., Chen L. M., Schuebel K. E., Bustelo X. R., Galán J. E.. ( 1998;). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell93:815–826 [CrossRef][PubMed]
    [Google Scholar]
  11. Hautefort I., Proença M. J., Hinton J. C.. ( 2003;). Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol69:7480–7491 [CrossRef][PubMed]
    [Google Scholar]
  12. Hayward R. D., Koronakis V.. ( 1999;). Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella . EMBO J18:4926–4934 [CrossRef][PubMed]
    [Google Scholar]
  13. Henry T., García-Del Portillo F., Gorvel J. P.. ( 2005;). Identification of Salmonella functions critical for bacterial cell division within eukaryotic cells. Mol Microbiol56:252–267 [CrossRef][PubMed]
    [Google Scholar]
  14. Hernandez L. D., Hueffer K., Wenk M. R., Galán J. E.. ( 2004;). Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science304:1805–1807 [CrossRef][PubMed]
    [Google Scholar]
  15. Hoiseth S. K., Stocker B. A.. ( 1981;). Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature291:238–239 [CrossRef][PubMed]
    [Google Scholar]
  16. Humphrey S., Clark L. F., Humphrey T. J., Jepson M. A.. ( 2011;). Enhanced recovery of Salmonella Typhimurium DT104 from exposure to stress at low temperature. Microbiology157:1103–1114[PubMed][CrossRef]
    [Google Scholar]
  17. Ibarra J. A., Knodler L. A., Sturdevant D. E., Virtaneva K., Carmody A. B., Fischer E. R., Porcella S. F., Steele-Mortimer O.. ( 2010;). Induction of Salmonella pathogenicity island 1 under different growth conditions can affect Salmonella-host cell interactions in vitro . Microbiology156:1120–1133 [CrossRef][PubMed]
    [Google Scholar]
  18. Jepson M. A., Kenny B., Leard A. D.. ( 2001;). Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell Microbiol3:417–426 [CrossRef][PubMed]
    [Google Scholar]
  19. Klein J. R., Fahlen T. F., Jones B. D.. ( 2000;). Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect Immun68:3368–3376 [CrossRef][PubMed]
    [Google Scholar]
  20. Kubori T., Matsushima Y., Nakamura D., Uralil J., Lara-Tejero M., Sukhan A., Galán J. E., Aizawa S. I.. ( 1998;). Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science280:602–605 [CrossRef][PubMed]
    [Google Scholar]
  21. Lara-Tejero M., Galán J. E.. ( 2009;). Salmonella enterica serovar Typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun77:2635–2642 [CrossRef][PubMed]
    [Google Scholar]
  22. Linn T., St Pierre R.. ( 1990;). Improved vector system for constructing transcriptional fusions that ensures independent translation of lacZ . J Bacteriol172:1077–1084[PubMed]
    [Google Scholar]
  23. McGhie E. J., Hayward R. D., Koronakis V.. ( 2001;). Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J20:2131–2139 [CrossRef][PubMed]
    [Google Scholar]
  24. McGhie E. J., Hayward R. D., Koronakis V.. ( 2004;). Control of actin turnover by a Salmonella invasion protein. Mol Cell13:497–510 [CrossRef][PubMed]
    [Google Scholar]
  25. McGhie E. J., Brawn L. C., Hume P. J., Humphreys D., Koronakis V.. ( 2009;). Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol12:117–124 [CrossRef][PubMed]
    [Google Scholar]
  26. Miller J. H.. ( 1972;). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  27. Mirold S., Ehrbar K., Weissmüller A., Prager R., Tschäpe H., Rüssmann H., Hardt W. D.. ( 2001;). Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2 . J Bacteriol183:2348–2358 [CrossRef][PubMed]
    [Google Scholar]
  28. Misselwitz B., Kreibich S. K., Rout S., Stecher B., Periaswamy B., Hardt W. D.. ( 2011;). Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun79:330–341 [CrossRef][PubMed]
    [Google Scholar]
  29. Müller A. J., Hoffmann C., Galle M., Van Den Broeke A., Heikenwalder M., Falter L., Misselwitz B., Kremer M., Beyaert R., Hardt W. D.. ( 2009;). The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe6:125–136 [CrossRef][PubMed]
    [Google Scholar]
  30. Norris F. A., Wilson M. P., Wallis T. S., Galyov E. E., Majerus P. W.. ( 1998;). SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci U S A95:14057–14059 [CrossRef][PubMed]
    [Google Scholar]
  31. Patel J. C., Galán J. E.. ( 2006;). Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol175:453–463 [CrossRef][PubMed]
    [Google Scholar]
  32. Perrett C. A., Jepson M. A.. ( 2007;). Applications of cell imaging in Salmonella research. Methods Mol Biol394:235–273 [CrossRef][PubMed]
    [Google Scholar]
  33. Perrett C. A., Jepson M. A.. ( 2009;). Regulation of Salmonella-induced membrane ruffling by SipA differs in strains lacking other effectors. Cell Microbiol11:475–487 [CrossRef][PubMed]
    [Google Scholar]
  34. Perrett C. A., Karavolos M. H., Humphrey S., Mastroeni P., Martinez-Argudo I., Spencer H., Bulmer D., Winzer K., McGhie E. et al. ( 2009;). LuxS-based quorum sensing does not affect the ability of Salmonella enterica serovar Typhimurium to express the SPI-1 type 3 secretion system, induce membrane ruffles, or invade epithelial cells. J Bacteriol191:7253–7259 [CrossRef][PubMed]
    [Google Scholar]
  35. Raffatellu M., Wilson R. P., Chessa D., Andrews-Polymenis H., Tran Q. T., Lawhon S., Khare S., Adams L. G., Bäumler A. J.. ( 2005;). SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect Immun73:146–154 [CrossRef][PubMed]
    [Google Scholar]
  36. Saini S., Slauch J. M., Aldridge P. D., Rao C. V.. ( 2010;). Role of cross talk in regulating the dynamic expression of the flagellar Salmonella pathogenicity island 1 and type 1 fimbrial genes. J Bacteriol192:5767–5777 [CrossRef][PubMed]
    [Google Scholar]
  37. Schraidt O., Lefebre M. D., Brunner M. J., Schmied W. H., Schmidt A., Radics J., Mechtler K., Galán J. E., Marlovits T. C.. ( 2010;). Topology and organization of the Salmonella typhimurium type III secretion needle complex components. PLoS Pathog6:e1000824 [CrossRef][PubMed]
    [Google Scholar]
  38. Steele-Mortimer O., Brumell J. H., Knodler L. A., Méresse S., Lopez A., Finlay B. B.. ( 2002;). The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol4:43–54 [CrossRef][PubMed]
    [Google Scholar]
  39. Stender S., Friebel A., Linder S., Rohde M., Mirold S., Hardt W. D.. ( 2000;). Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol36:1206–1221 [CrossRef][PubMed]
    [Google Scholar]
  40. Temme K., Salis H., Tullman-Ercek D., Levskaya A., Hong S. H., Voigt C. A.. ( 2008;). Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1. J Mol Biol377:47–61 [CrossRef][PubMed]
    [Google Scholar]
  41. Terebiznik M. R., Vieira O. V., Marcus S. L., Slade A., Yip C. M., Trimble W. S., Meyer T., Finlay B. B., Grinstein S.. ( 2002;). Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella . Nat Cell Biol4:766–773 [CrossRef][PubMed]
    [Google Scholar]
  42. Unsworth K. E., Way M., McNiven M., Machesky L., Holden D. W.. ( 2004;). Analysis of the mechanisms of Salmonella-induced actin assembly during invasion of host cells and intracellular replication. Cell Microbiol6:1041–1055 [CrossRef][PubMed]
    [Google Scholar]
  43. Zhang S., Santos R. L., Tsolis R. M., Mirold S., Hardt W. D., Adams L. G., Bäumler A. J.. ( 2002;). Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol Lett217:243–247 [CrossRef][PubMed]
    [Google Scholar]
  44. Zhou D., Galán J. E.. ( 2001;). Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect3:1293–1298 [CrossRef][PubMed]
    [Google Scholar]
  45. Zhou D., Mooseker M. S., Galán J. E.. ( 1999;). Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science283:2092–2095 [CrossRef][PubMed]
    [Google Scholar]
  46. Zhou D., Chen L. M., Hernandez L., Shears S. B., Galán J. E.. ( 2001;). A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol39:248–259 [CrossRef][PubMed]
    [Google Scholar]
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