Salmonellae interplay with host cells (original) (raw)

• Pegues, D. A., Ohl, M. E. & Miller, S. I. in Principles and Practice of Infectious Diseases (eds Mandell, G. L., Bennet, J. E. & Dolin, R.) 2636–2654 (Churchill Livingstone, New York, 2005).
  Google Scholar
• Garcia-del Portillo, F., Foster, J. W. & Finlay, B. B. Role of acid tolerance response genes in Salmonella typhimurium virulence. Infect. Immun. 61, 4489–4492 (1993).
  CAS PubMed PubMed Central Google Scholar
• Michetti, P., Mahan, M. J., Slauch, J. M., Mekalanos, J. J. & Neutra, M. R. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60, 1786–1792 (1992).
  CAS PubMed PubMed Central Google Scholar
• Selsted, M. E., Miller, S. I., Henschen, A. H. & Ouellette, A. J. Enteric defensins: antibiotic peptide components of intestinal host defense. J. Cell Biol. 118, 929–936 (1992).
  Article CAS PubMed Google Scholar
• Prouty, A. M., Brodsky, I. E., Falkow, S. & Gunn, J. S. Bile-salt-mediated induction of antimicrobial and bile resistance in Salmonella typhimurium. Microbiology 150, 775–783 (2004).
  Article CAS PubMed Google Scholar
• 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. 6, 3077–3087 (1992).
  Article CAS PubMed Google Scholar
• Takeuchi, A. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50, 109–136 (1967). This reference showed membrane ruffling that is induced by Salmonella spp. in intestinal cells by microscopy for the first time.
  CAS PubMed PubMed Central Google Scholar
• Baumler, A. J., Tsolis, R. M. & Heffron, F. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect. Immun. 64, 1862–1865 (1996).
  CAS PubMed PubMed Central Google Scholar
• Kohbata, S., Yokoyama, H. & Yabuuchi, E. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol. Immunol. 30, 1225–1237 (1986).
  Article CAS PubMed Google Scholar
• Jones, B. D., Ghori, N. & Falkow, S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J. Exp. Med. 180, 15–23 (1994).
  Article CAS PubMed Google Scholar
• Vazquez-Torres, A. et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401, 804–808 (1999).
  Article CAS PubMed Google Scholar
• Jepson, M. A., Collares-Buzato, C. B., Clark, M. A., Hirst, B. H. & Simmons, N. L. Rapid disruption of epithelial barrier function by Salmonella typhimurium is associated with structural modification of intercellular junctions. Infect. Immun. 63, 356–359 (1995).
  CAS PubMed PubMed Central Google Scholar
• Zhang, S. et al. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70, 3843–3855 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Raffatellu, M. et al. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73, 146–154 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Stecher, B. et al. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect. Immun. 73, 3228–3241 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Hobbie, S., Chen, L. M., Davis, R. J. & Galan, J. E. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 159, 5550–5559 (1997).
  CAS PubMed Google Scholar
• Galan, 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. USA 86, 6383–6387 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Miller, S. I., Kukral, A. M. & Mekalanos, J. J. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc. Natl Acad. Sci. USA 86, 5054–5058 (1989). This reference identified the PhoP/PhoQ two-component system as being important for the regulation of virulence.
  Article CAS PubMed PubMed Central Google Scholar
• 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. USA 89, 10079–10083 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• 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. 179, 601–608 (1994).
  Article CAS PubMed Google Scholar
• Ochman, H., Soncini, F. C., Solomon, F. & Groisman, E. A. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl Acad. Sci. USA 93, 7800–7804 (1996). References 21 and 22 were the first to show that the T3SS that is encoded on SPI2 is important for virulence.
  Article CAS PubMed PubMed Central Google Scholar
• Shea, J. E., Hensel, M., Gleeson, C. & Holden, D. W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl Acad. Sci. USA 93, 2593–2597 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Vazquez-Torres, A. et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287, 1655–1658 (2000).
  Article CAS PubMed Google Scholar
• Miao, E. A., Freeman, J. A. & Miller, S. I. Transcription of the SsrAB regulon is repressed by alkaline pH and is independent of PhoPQ and magnesium concentration. J. Bacteriol. 184, 1493–1497 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Bader, M. W. et al. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol. Microbiol. 50, 219–230 (2003).
  Article CAS PubMed Google Scholar
• McCormick, B. A., Miller, S. I., Carnes, D. & Madara, J. L. Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect. Immun. 63, 2302–2309 (1995).
  CAS PubMed PubMed Central Google Scholar
• McCormick, B. A. et al. Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J. Cell Biol. 131, 1599–1608 (1995).
  Article CAS PubMed Google Scholar
• Hansen-Wester, I. & Hensel, M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3, 549–559 (2001).
  Article CAS PubMed Google Scholar
• Kubori, T. et al. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602–605 (1998). This study provided the first electron microscopy images of the T3SS needle complex.
  Article CAS PubMed Google Scholar
• Kimbrough, T. G. & Miller, S. I. Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc. Natl Acad. Sci. USA 97, 11008–11013 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Kimbrough, T. G. & Miller, S. I. Assembly of the type III secretion needle complex of Salmonella typhimurium. Microbes Infect. 4, 75–82 (2002).
  Article CAS PubMed Google Scholar
• Miao, E. A. & Miller, S. I. A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc. Natl Acad. Sci. USA 97, 7539–7544 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Brumell, J. H. et al. SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 4, 36–48 (2003).
  Article CAS PubMed Google Scholar
• Lee, S. H. & Galan, J. E. Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51, 483–495 (2004).
  Article CAS PubMed Google Scholar
• Karavolos, M. H. et al. Type III secretion of the Salmonella effector protein SopE is mediated via an N-terminal amino acid signal and not an mRNA sequence. J. Bacteriol. 187, 1559–1567 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Fu, Y. & Galan, J. E. Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J. Bacteriol. 180, 3393–3399 (1998).
  CAS PubMed PubMed Central Google Scholar
• Hong, K. H. & Miller, V. L. Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J. Bacteriol. 180, 1793–1802 (1998).
  CAS PubMed PubMed Central Google Scholar
• Bronstein, P. A., Miao, E. A. & Miller, S. I. InvB is a type III secretion chaperone specific for SspA. J. Bacteriol. 182, 6638–6644 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Tucker, S. C. & Galan, J. E. Complex function for SicA, a Salmonella enterica serovar Typhimurium type III secretion-associated chaperone. J. Bacteriol. 182, 2262–2268 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Ehrbar, K., Friebel, A., Miller, S. I. & Hardt, W. D. Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J. Bacteriol. 185, 6950–6967 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Higashide, W. & Zhou, D. The first 45 amino acids of SopA are necessary for InvB binding and SPI-1 secretion. J. Bacteriol. 188, 2411–2420 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Akeda, Y. & Galan, J. E. Chaperone release and unfolding of substrates in type III secretion. Nature 437, 911–915 (2005).
  Article CAS PubMed Google Scholar
• Brown, N. F. et al. Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog. 1, e32 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Hensel, M. et al. Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2. Mol. Microbiol. 24, 155–167 (1997).
  Article CAS PubMed Google Scholar
• Deiwick, J. et al. Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J. Bacteriol. 180, 4775–4780 (1998).
  CAS PubMed PubMed Central Google Scholar
• Steele-Mortimer, O. et al. The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell. Microbiol. 4, 43–54 (2002).
  Article CAS PubMed Google Scholar
• Hernandez, L. D., Hueffer, K., Wenk, M. R. & Galan, J. E. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805–1807 (2004).
  Article CAS PubMed Google Scholar
• Drecktrah, D., Knodler, L. A., Galbraith, K. & Steele-Mortimer, O. The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell. Microbiol. 7, 105–113 (2005).
  Article CAS PubMed Google Scholar
• Lawley, T. D. et al. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2, e11 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Brawn, L. C., Hayward, R. D. & Koronakis, V. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1, 63–75 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Giacomodonato, M. N. et al. SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology 153, 1221–1228 (2007).
  Article CAS PubMed Google Scholar
• Li, J. et al. Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc. Natl Acad. Sci. USA 92, 7252–7256 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Ochman, H. & Groisman, E. A. Distribution of pathogenicity islands in Salmonella spp. Infect. Immun. 64, 5410–5412 (1996).
  CAS PubMed PubMed Central Google Scholar
• Boyd, E. F., Li, J., Ochman, H. & Selander, R. K. Comparative genetics of the inv-spa invasion gene complex of Salmonella enterica. J. Bacteriol. 179, 1985–1991 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Hensel, M. et al. Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12. J. Bacteriol. 179, 1105–1111 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Hensel, M., Nikolaus, T. & Egelseer, C. Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol. Microbiol. 31, 489–498 (1999).
  Article CAS PubMed Google Scholar
• Porwollik, S., Wong, R. M. & McClelland, M. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc. Natl Acad. Sci. USA 99, 8956–8961 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hormaeche, C. E. Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 37, 311–318 (1979).
  CAS PubMed PubMed Central Google Scholar
• Vidal, S. M., Malo, D., Vogan, K., Skamene, E. & Gros, P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73, 469–485 (1993).
  Article CAS PubMed Google Scholar
• Hensel, M. et al. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30, 163–174 (1998).
  Article CAS PubMed Google Scholar
• Beuzon, C. R. & Holden, D. W. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3, 1345–1352 (2001).
  Article CAS PubMed Google Scholar
• Monack, D. M., Bouley, D. M. & Falkow, S. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J. Exp. Med. 199, 231–241 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Behlau, I. & Miller, S. I. A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J. Bacteriol. 175, 4475–4484 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Barthel, M. et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71, 2839–2858 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galan, J. E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815–826 (1998). This work elegantly demonstrated the ability of SopE to activate GTPases and subsequent actin rearrangements and transcriptional responses.
  Article CAS PubMed Google Scholar
• Bakshi, C. S. et al. Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J. Bacteriol. 182, 2341–2344 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Stender, S. et al. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36, 1206–1221 (2000).
  Article CAS PubMed Google Scholar
• Friebel, A. et al. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J. Biol. Chem. 276, 34035–34040 (2001).
  Article CAS PubMed Google Scholar
• Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B. & Galan, J. E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39, 248–259 (2001).
  Article CAS PubMed Google Scholar
• Patel, J. C. & Galan, J. E. Differential activation and function of Rho GTPases during _Salmonella_-host cell interactions. J. Cell Biol. 175, 453–463 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Ellerbroek, S. M. et al. SGEF, a RhoG guanine nucleotide exchange factor that stimulates macropinocytosis. Mol. Biol. Cell 15, 3309–3319 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Criss, A. K. & Casanova, J. E. Coordinate regulation of Salmonella enterica serovar Typhimurium invasion of epithelial cells by the Arp2/3 complex and Rho GTPases. Infect. Immun. 71, 2885–2891 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Unsworth, K. E., Way, M., McNiven, M., Machesky, L. & Holden, D. W. Analysis of the mechanisms of _Salmonella_-induced actin assembly during invasion of host cells and intracellular replication. Cell. Microbiol. 6, 1041–1055 (2004).
  Article CAS PubMed Google Scholar
• Shi, J., Scita, G. & Casanova, J. E. WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium. J. Biol. Chem. 280, 29849–29855 (2005).
  Article CAS PubMed Google Scholar
• Hayward, R. D. & Koronakis, V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18, 4926–4934 (1999). References 75 and 76 detected direct manipulation of actin by the SPI1 T3SS effectors SipA and SipC.
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, D., Mooseker, M. S. & Galan, J. E. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092–2095 (1999).
  Article CAS PubMed Google Scholar
• Scherer, C. A., Cooper, E. & Miller, S. I. The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol. Microbiol. 37, 1133–1145 (2000).
  Article CAS PubMed Google Scholar
• McGhie, E. J., Hayward, R. D. & Koronakis, V. Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J. 20, 2131–2139 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Higashide, W., Dai, S., Hombs, V. P. & Zhou, D. Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell. Microbiol. 4, 357–365 (2002).
  Article CAS PubMed Google Scholar
• Chen, L. M., Hobbie, S. & Galan, J. E. Requirement of CDC42 for _Salmonella_-induced cytoskeletal and nuclear responses. Science 274, 2115–2118 (1996).
  Article CAS PubMed Google Scholar
• Boyle, E. C., Brown, N. F. & Finlay, B. B. Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell. Microbiol. 8, 1946–1957 (2006).
  Article CAS PubMed Google Scholar
• Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E. & Majerus, P. W. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl Acad. Sci. USA 95, 14057–14059 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Hersh, D. et al. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96, 2396–2401 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Franchi, L. et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in _Salmonella_-infected macrophages. Nature Immunol. 7, 576–582 (2006).
  Article CAS Google Scholar
• Miao, E. A. et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nature Immunol. 7, 569–575 (2006).
  Article CAS Google Scholar
• Lara-Tejero, M. et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407–1412 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Raupach, B., Peuschel, S. K., Monack, D. M. & Zychlinsky, A. Caspase-1-mediated activation of interleukin-1β (IL-1β) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74, 4922–4926 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Jones, M. A. et al. Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect. Immun. 66, 5799–5804 (1998).
  CAS PubMed PubMed Central Google Scholar
• Wood, M. W. et al. The secreted effector protein of Salmonella dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell Microbiol. 2, 293–303 (2000).
  Article CAS PubMed Google Scholar
• Zhang, Y., Higashide, W. M., McCormick, B. A., Chen, J. & Zhou, D. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol. Microbiol. 62, 786–793 (2006).
  Article CAS PubMed Google Scholar
• Jiang, X. et al. The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol. Microbiol. 54, 1186–1198 (2004).
  Article CAS PubMed Google Scholar
• Fu, Y. & Galan, J. E. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293–297 (1999). References 92 and 93 identified the GTPase-antagonizing activity of SptP and showed how the activities of SopE and SptP are temporally regulated by proteasome-dependent degradation.
  Article CAS PubMed Google Scholar
• Kubori, T. & Galan, J. E. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115, 333–342 (2003).
  Article CAS PubMed Google Scholar
• Murli, S., Watson, R. O. & Galan, J. E. Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell. Microbiol. 3, 795–810 (2001).
  Article CAS PubMed Google Scholar
• Haraga, A. & Miller, S. I. A Salmonella enterica serovar Typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect. Immun. 71, 4052–4058 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Miao, E. A. et al. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34, 850–864 (1999).
  Article CAS PubMed Google Scholar
• Rohde, J. R., Breitkreutz, A., Chenal, A., Sansonetti, P. J. & Parsot, C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1, 77–83 (2007).
  Article CAS PubMed Google Scholar
• Haraga, A. & Miller, S. I. A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell. Microbiol. 8, 837–846 (2006).
  Article CAS PubMed Google Scholar
• Collier-Hyams, L. S. et al. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappaB pathway. J. Immunol. 169, 2846–2850 (2002).
  Article CAS PubMed Google Scholar
• Mittal, R., Peak-Chew, S. Y. & McMahon, H. T. Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl Acad. Sci. USA 103, 18574–18579 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Mukherjee, S. et al. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211–1214 (2006).
  Article CAS PubMed Google Scholar
• Buchwald, D. S. & Blaser, M. J. A review of human salmonellosis: II. Duration of excretion following infection with nontyphi Salmonella. Rev. Infect. Dis. 6, 345–356 (1984).
  Article CAS PubMed Google Scholar
• Richter-Dahlfors, A., Buchan, A. M. & Finlay, B. B. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186, 569–580 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Fields, P. I., Swanson, R. V., Haidaris, C. G. & Heffron, F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl Acad. Sci. USA 83, 5189–5193 (1986). This important study demonstrated that survival within macrophages is important for S. typhimurium virulence.
  Article CAS PubMed PubMed Central Google Scholar
• O'Callaghan, D., Maskell, D., Liew, F. Y., Easmon, C. S. & Dougan, G. Characterization of aromatic- and purine-dependent Salmonella typhimurium: attention, persistence, and ability to induce protective immunity in BALB/c mice. Infect. Immun. 56, 419–423 (1988).
  CAS PubMed PubMed Central Google Scholar
• Dukes, J. D. et al. The secreted Salmonella dublin phosphoinositide phosphatase, SopB, localizes to PtdIns(3)_P_-containing endosomes and perturbs normal endosome to lysosome trafficking. Biochem. J. 395, 239–247 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Carrol, M. E., Jackett, P. S., Aber, V. R. & Lowrie, D. B. Phagolysosome formation, cyclic adenosine 3′:5′-monophosphate and the fate of Salmonella typhimurium within mouse peritoneal macrophages. J. Gen. Microbiol. 110, 421–429 (1979).
  Article CAS PubMed Google Scholar
• Buchmeier, N. A. & Heffron, F. Inhibition of macrophage phagosome–lysosome fusion by Salmonella typhimurium. Infect. Immun. 59, 2232–2238 (1991).
  CAS PubMed PubMed Central Google Scholar
• Oh, Y. K. et al. Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium. Infect. Immun. 64, 3877–3883 (1996).
  CAS PubMed PubMed Central Google Scholar
• Drecktrah, D., Knodler, L. A., Howe, D. & Steele-Mortimer, O. Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8, 212–225 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Rathman, M., Sjaastad, M. D. & Falkow, S. Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect. Immun. 64, 2765–2773 (1996).
  CAS PubMed PubMed Central Google Scholar
• Martin-Orozco, N. et al. Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol. Biol. Cell 17, 498–510 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Steele-Mortimer, O., Meresse, S., Gorvel, J. P., Toh, B. H. & Finlay, B. B. Biogenesis of _Salmonella typhimurium_-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell. Microbiol. 1, 33–49 (1999).
  Article CAS PubMed Google Scholar
• Smith, A. C., Cirulis, J. T., Casanova, J. E., Scidmore, M. A. & Brumell, J. H. Interaction of the _Salmonella_-containing vacuole with the endocytic recycling system. J. Biol. Chem. 280, 24634–24641 (2005).
  Article CAS PubMed Google Scholar
• Garcia-del Portillo, F. & Finlay, B. B. Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J. Cell Biol. 129, 81–97 (1995).
  Article CAS PubMed Google Scholar
• Meresse, S., Steele-Mortimer, O., Finlay, B. B. & Gorvel, J. P. The rab7 GTPase controls the maturation of _Salmonella typhimurium_-containing vacuoles in HeLa cells. EMBO J. 18, 4394–4403 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Hashim, S., Mukherjee, K., Raje, M., Basu, S. K. & Mukhopadhyay, A. Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. J. Biol. Chem. 275, 16281–16288 (2000).
  Article CAS PubMed Google Scholar
• Brumell, J. H., Tang, P., Mills, S. D. & Finlay, B. B. Characterization of _Salmonella_-induced filaments (Sifs) reveals a delayed interaction between _Salmonella_-containing vacuoles and late endocytic compartments. Traffic 2, 643–653 (2001).
  Article CAS PubMed Google Scholar
• Garvis, S. G., Beuzon, C. R. & Holden, D. W. A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and _Salmonella_-containing vacuoles in macrophages. Cell. Microbiol. 3, 731–744 (2001).
  Article CAS PubMed Google Scholar
• Cuellar-Mata, P. et al. Nramp1 modifies the fusion of _Salmonella typhimurium_-containing vacuoles with cellular endomembranes in macrophages. J. Biol. Chem. 277, 2258–2265 (2002).
  Article CAS PubMed Google Scholar
• Catron, D. M. et al. The _Salmonella_-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell. Microbiol. 4, 315–328 (2002).
  Article CAS PubMed Google Scholar
• Fields, P. I., Groisman, E. A. & Heffron, F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243, 1059–1062 (1989).
  Article CAS PubMed Google Scholar
• Miller, S. I. & Mekalanos, J. J. Constitutive expression of the PhoP regulon attenuates Salmonella virulence and survival within macrophages. J. Bacteriol. 172, 2485–2490 (1990).
  Article CAS PubMed PubMed Central Google Scholar
• Nickerson, C. A. & Curtiss, R. Role of sigma factor RpoS in initial stages of Salmonella typhimurium infection. Infect. Immun. 65, 1814–1823 (1997).
  CAS PubMed PubMed Central Google Scholar
• Bearson, B. L., Wilson, L. & Foster, J. W. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J. Bacteriol. 180, 2409–2417 (1998).
  CAS PubMed PubMed Central Google Scholar
• Shiloh, M. U. et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10, 29–38 (1999).
  Article CAS PubMed Google Scholar
• Gunn, J. S., Ryan, S. S., Van Velkinburgh, J. C., Ernst, R. K. & Miller, S. I. Genetic and functional analysis of a PmrA–PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 68, 6139–6146 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H. & Fang, F. C. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 192, 227–236 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Hisert, K. B. et al. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56, 1234–1245 (2005).
  Article CAS PubMed Google Scholar
• Humphreys, S., Stevenson, A., Bacon, A., Weinhardt, A. B. & Roberts, M. The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 67, 1560–1568 (1999).
  CAS PubMed PubMed Central Google Scholar
• Rosenberger, C. M., Gallo, R. L. & Finlay, B. B. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc. Natl Acad. Sci. USA 101, 2422–2427 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Curtiss, R. & Kelly, S. M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect. Immun. 55, 3035–3043 (1987).
  CAS PubMed PubMed Central Google Scholar
• Fang, F. C. et al. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc. Natl Acad. Sci. USA 89, 11978–11982 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, A. K., Detweiler, C. S. & Falkow, S. OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol. 182, 771–781 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Testerman, T. L. et al. The alternative sigma factor σE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43, 771–782 (2002).
  Article CAS PubMed Google Scholar
• Prost, L. R. et al. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26, 165–174 (2007). References 136 and 138 show that PhoQ directly senses antimicrobial peptides and low pH.
  Article CAS PubMed Google Scholar
• Heithoff, D. M. et al. Coordinate intracellular expression of Salmonella genes induced during infection. J. Bacteriol. 181, 799–807 (1999).
  CAS PubMed PubMed Central Google Scholar
• Bader, M. W. et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122, 461–472 (2005).
  Article CAS PubMed Google Scholar
• Cho, U. S. et al. Metal bridges between the PhoQ sensor domain and the membrane regulate transmembrane signaling. J. Mol. Biol. 356, 1193–1206 (2006).
  Article CAS PubMed Google Scholar
• Gibbons, H. S., Kalb, S. R., Cotter, R. J. & Raetz, C. R. Role of Mg2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55, 425–440 (2005).
  Article CAS PubMed Google Scholar
• Ernst, R. K., Guina, T. & Miller, S. I. Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect. 3, 1327–1334 (2001).
  Article CAS PubMed Google Scholar
• Guo, L. et al. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276, 250–253 (1997). This study demonstrates that PhoP/PhoQ regulates the remodelling of the LPS structure in a way that makes it less immunostimulatory by TLR4 signalling.
  Article CAS PubMed Google Scholar
• Gunn, J. S. et al. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27, 1171–1182 (1998).
  Article CAS PubMed Google Scholar
• Guo, L. et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95, 189–198 (1998).
  Article CAS PubMed Google Scholar
• Hilbert, F., Garcia-del Portillo, F. & Groisman, E. A. A periplasmic D-alanyl-D-alanine dipeptidase in the Gram-negative bacterium Salmonella enterica. J. Bacteriol. 181, 2158–2165 (1999).
  CAS PubMed PubMed Central Google Scholar
• Fang, F. C. et al. Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl Acad. Sci. USA 96, 7502–7507 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103–118 (2003).
  Article CAS PubMed Google Scholar
• Cirillo, D. M., Valdivia, R. H., Monack, D. M. & Falkow, S. Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol. 30, 175–188 (1998).
  Article CAS PubMed Google Scholar
• Hensel, M. et al. Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400–403 (1995).
  Article CAS PubMed Google Scholar
• Uchiya, K. et al. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18, 3924–3933 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Shotland, Y., Kramer, H. & Groisman, E. A. The Salmonella SpiC protein targets the mammalian Hook3 protein function to alter cellular trafficking. Mol. Microbiol. 49, 1565–1576 (2003).
  Article CAS PubMed Google Scholar
• Freeman, J. A., Rappl, C., Kuhle, V., Hensel, M. & Miller, S. I. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J. Bacteriol. 184, 4971–4980 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Yu, X. J. et al. SpiC is required for secretion of Salmonella pathogenicity island 2 type III secretion system proteins. Cell. Microbiol. 4, 531–540 (2002).
  Article CAS PubMed Google Scholar
• Beuzon, C. R. et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19, 3235–3249 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Ruiz-Albert, J. et al. Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol. Microbiol. 44, 645–661 (2002).
  Article CAS PubMed Google Scholar
• Freeman, J. A., Ohl, M. E. & Miller, S. I. The Salmonella enterica serovar Typhimurium translocated effectors SseJ and SifsB are targeted to the _Salmonella_-containing vacuole. Infect. Immun. 71, 418–427 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Knodler, L. A. et al. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol. Microbiol. 49, 685–704 (2003).
  Article CAS PubMed Google Scholar
• Deiwick, J. et al. The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect. Immun. 74, 6965–6972 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Brumell, J. H., Goosney, D. L. & Finlay, B. B. SifA, a type III secreted effector of Salmonella typhimurium, directs _Salmonella_-induced filament (Sif) formation along microtubules. Traffic 3, 407–415 (2002).
  Article CAS PubMed Google Scholar
• Miao, E. A. et al. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol. Microbiol. 48, 401–415 (2003).
  Article CAS PubMed Google Scholar
• Salcedo, S. P. & Holden, D. W. SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J. 22, 5003–5014 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Kuhle, V., Jackel, D. & Hensel, M. Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 5, 356–370 (2004).
  Article CAS PubMed Google Scholar
• 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. USA 90, 10544–10548 (1993). References 163 and 164 were the first to show that S. typhimurium produces Sifs in infected cultured cells and that the effector that is responsible for this activity is SifA.
  Article CAS PubMed PubMed Central Google Scholar
• Stein, M. A., Leung, K. Y., Zwick, M., Garcia-del Portillo, F. & Finlay, B. B. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20, 151–164 (1996).
  Article CAS PubMed Google Scholar
• Knodler, L. A. & Steele-Mortimer, O. The Salmonella effector PipB2 affects late endosome/lysosome distribution to mediate Sif extension. Mol. Biol. Cell. 16, 4108–4123 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Boucrot, E., Henry, T., Borg, J. P., Gorvel, J. P. & Meresse, S. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308, 1174–1178 (2005).
  Article CAS PubMed Google Scholar
• Alto, N. M. et al. Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124, 133–145 (2006).
  Article CAS PubMed Google Scholar
• Reinicke, A. T. et al. A Salmonella typhimurium effector protein SifA is modified by host cell prenylation and S-acylation machinery. J. Biol. Chem. 280, 14620–14627 (2005).
  Article CAS PubMed Google Scholar
• Guy, R. L., Gonias, L. A. & Stein, M. A. Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region. Mol. Microbiol. 37, 1417–1435 (2000).
  Article CAS PubMed Google Scholar
• Henry, T. et al. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc. Natl Acad. Sci. USA 103, 13497–13502 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Hansen-Wester, I., Stecher, B. & Hensel, M. Type III secretion of Salmonella enterica serovar Typhimurium translocated effectors and SseFG. Infect. Immun. 70, 1403–1409 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Kuhle, V. & Hensel, M. SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell. Microbiol. 4, 813–824 (2002).
  Article CAS PubMed Google Scholar
• Abrahams, G. L., Muller, P. & Hensel, M. Functional dissection of SseF, a type III effector protein involved in positioning the _Salmonella_-containing vacuole. Traffic 7, 950–965 (2006).
  Article CAS PubMed Google Scholar
• Kuhle, V., Abrahams, G. L. & Hensel, M. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7, 716–730 (2006).
  Article CAS PubMed Google Scholar
• Birmingham, C. L., Jiang, X., Ohlson, M. B., Miller, S. I. & Brumell, J. H. _Salmonella_-induced filament formation is a dynamic phenotype induced by rapidly replicating Salmonella enterica serovar Typhimurium in epithelial cells. Infect. Immun. 73, 1204–1208 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Lesnick, M. L., Reiner, N. E., Fierer, J. & Guiney, D. G. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol. 39, 1464–1470 (2001).
  Article CAS PubMed Google Scholar
• Browne, S. H., Lesnick, M. L. & Guiney, D. G. Genetic requirements for _Salmonella_-induced cytopathology in human monocyte-derived macrophages. Infect. Immun. 70, 7126–7135 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Gotoh, H. et al. Extracellular secretion of the virulence plasmid-encoded ADP-ribosyltransferase SpvB in Salmonella. Microb. Pathog. 34, 227–238 (2003).
  Article CAS PubMed Google Scholar
• Brumlik, M. J. & Buckley, J. T. Identification of the catalytic triad of the lipase/acyltransferase from Aeromonas hydrophila. J. Bacteriol. 178, 2060–2064 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Ohlson, M. B., Fluhr, K., Birmingham, C. L., Brumell, J. H. & Miller, S. I. SseJ deacylase activity by Salmonella enterica serovar Typhimurium promotes virulence in mice. Infect. Immun. 73, 6249–6259 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Harrison, R. E. et al. Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles. Mol. Biol. Cell 15, 3146–3154 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Marsman, M., Jordens, I., Kuijl, C., Janssen, L. & Neefjes, J. Dynein-mediated vesicle transport controls intracellular Salmonella replication. Mol. Biol. Cell 15, 2954–2964 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Meresse, S. et al. Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell. Microbiol. 3, 567–577 (2001).
  Article CAS PubMed Google Scholar
• Viboud, G. I. & Bliska, J. B. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20, 5373–5382 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Marlovits, T. C. et al. Structural insights into the assembly of the type III secretion needle complex. Science 306, 1040–1042 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Sun, J., Hobert, M. E., Rao, A. S., Neish, A. S. & Madara, J. L. Bacterial activation of β-catenin signaling in human epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G220–227 (2004).
  Article CAS PubMed Google Scholar
• Zhou, D., Mooseker, M. S. & Galan, J. E. An invasion-associated Salmonella protein modulates the actin-bundling activity of plastin. Proc. Natl Acad. Sci. USA 96, 10176–10181 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, C. A. et al. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc. Natl Acad. Sci. USA 97, 12283–12288 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Hernandez, L. D., Pypaert, M., Flavell, R. A. & Galan, J. E. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163, 1123–1131 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Hayward, R. D. et al. Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol. Microbiol. 56, 590–603 (2005).
  Article CAS PubMed Google Scholar
• Carlson, S. A., Omary, M. B. & Jones, B. D. Identification of cytokeratins as accessory mediators of Salmonella entry into eukaryotic cells. Life Sci. 70, 1415–1426 (2002).
  Article CAS PubMed Google Scholar
• Knodler, L. A., Finlay, B. B. & Steele-Mortimer, O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J. Biol. Chem. 280, 9058–9064 (2005).
  Article CAS PubMed Google Scholar
• Mukherjee, K., Parashuraman, S., Raje, M. & Mukhopadhyay, A. SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on _Salmonella_-containing phagosomes to promote fusion with early endosomes. J. Biol. Chem. 276, 23607–23615 (2001).
  Article CAS PubMed Google Scholar
• Coombes, B. K. et al. Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J. Mol. Biol. 348, 817–830 (2005).
  Article CAS PubMed Google Scholar
• Brumell, J. H., Rosenberger, C. M., Gotto, G. T., Marcus, S. L. & Finlay, B. B. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell. Microbiol. 3, 75–84 (2001).
  Article CAS PubMed Google Scholar
• Tezcan-Merdol, D. et al. Actin is ADP-ribosylated by the Salmonella enterica virulence-associated protein SpvB. Mol. Microbiol. 39, 606–619 (2001).
  Article CAS PubMed Google Scholar
• Worley, M. J., Nieman, G. S., Geddes, K. & Heffron, F. Salmonella typhimurium disseminates within its host by manipulating the motility of infected cells. Proc. Natl Acad. Sci. USA 103, 17915–17920 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Kujat Choy, S. L. et al. SseK1 and SseK2 are novel translocated proteins of Salmonella enterica serovar Typhimurium. Infect. Immun. 72, 5115–5125 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Rytkonen, A. et al. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl Acad. Sci. USA 104, 3502–3507 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Geddes, K., Worley, M., Niemann, G. & Heffron, F. Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect. Immun. 73, 6260–6271 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Tsolis, R. M., Adams, L. G., Ficht, T. A. & Baumler, A. J. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67, 4879–4885 (1999).
  CAS PubMed PubMed Central Google Scholar