Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-6bf8c574d5-r4mrb Total loading time: 0 Render date: 2025-03-06T15:12:56.377Z Has data issue: false hasContentIssue false

9 - Interactions of S. enterica with phagocytic cells

Published online by Cambridge University Press:  04 December 2009

Duncan Maskell
By
Bruce D. McCollister  and
Andres Vazquez-Torres
Edited by
Pietro Mastroeni
Duncan Maskell
Affiliation:
University of Cambridge
Bruce D. McCollister
Affiliation:
Department of Microbiology, University of Colorado Health Sciences Center, B175, Room 4615, 4200 E. 9th Ave., Denver, CO 80262, USA
Andres Vazquez-Torres
Affiliation:
Department of Microbiology, University of Colorado Health Sciences Center, B175, Room 4615, 4200 E. 9th Ave., Denver, CO 80262, USA
Pietro Mastroeni
Affiliation:
University of Cambridge
Get access

Summary

INTRODUCTION

Mononuclear phagocytes associate with S. enterica early in the disease process before acute inflammatory abscesses are formed, as well as during later stages of the acquired immune response in which macrophages form part of well-organized granulomas (Mastroeni et al., 1995; Richter- Dahlfors et al., 1997). The ability to survive within macrophages is a key event in the pathogenesis of Salmonella enterica (Fields et al., 1986). A growing body of information indicates that macrophages can serve as sites for S. enterica replication, even though they can be activated to exert potent anti- S. enterica activity. The great majority of the intimate interactions between S. enterica and macrophages take place inside a specialized endocytic vacuole named the phagosome. This chapter discusses the dynamic S. enterica phagosome as it pertains to the pathogenesis of this intracellular Gram-negative bacterium.

Immunological and genetic manipulations in animal models of infection, as well as the observation of naturally occurring genetic traits, have revealed that genetic loci encoding Nramp1, TLR4, NADPH oxidase and IFNγ play key roles in resistance to S. enterica infection. These host defenses are expressed directly by macrophages or, as in the case of IFNγ, up-regulate the anti-S. enterica activity of mononuclear phagocytes. In the following sections, we will discuss both the mechanisms by which these host defenses contribute to the anti-S. enterica activity of macrophages, and the virulence factors used by S. enterica to avoid these components of the antimicrobial arsenal of professional phagocytes.

Type
Chapter
Information
Salmonella Infections
Clinical, Immunological and Molecular Aspects
 , pp. 255 - 278
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ables, G. P., Takamatsu, D., Noma, H.et al. (2001). The roles of Nramp1 and TNFα genes in nitric oxide production and their effect on the growth of Salmonella typhimurium in macrophages from Nramp1 congenic and tumor necrosis factor-alpha−/− mice. J Interferon Cytokine Res, 21, 53–62.CrossRefGoogle ScholarPubMed
Alam, M. S., Akaike, T., Okamoto, S.et al. (2002). Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect Immun, 70, 3130–42.CrossRefGoogle ScholarPubMed
Aliprantis, A. O., Yang, R. B., Mark, M. R.et al. (1999). Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science, 285, 736–9.CrossRefGoogle ScholarPubMed
Alpuche Aranda, C. M., Swanson, J. A., Loomis, W. P. and Miller, S. I. (1992). Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA, 89, 10079–83.CrossRefGoogle ScholarPubMed
Atkinson, P. G. and Barton, C. H. (1999). High level expression of Nramp1G169 in RAW264.7 cell transfectants: analysis of intracellular iron transport. Immunology, 96, 656–62.CrossRefGoogle ScholarPubMed
Barrera, L. F., Kramnik, I., Skamene, E. and Radzioch, D. (1994). Nitrite production by macrophages derived from BCG-resistant and -susceptible congenic mouse strains in response to IFNγ and infection with BCG. Immunology, 82, 457–64.Google Scholar
Bauer, S., Kirschning, C. J., Hacker, H.et al. (2001). Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci USA, 98, 9237–42.CrossRefGoogle ScholarPubMed
Bernheiden, M., Heinrich, J. M., Minigo, G.et al. (2001). LBP, CD14, TLR4 and the murine innate immune response to a peritoneal Salmonella infection. J Endotoxin Res, 7, 447–50.CrossRefGoogle ScholarPubMed
Beuzon, C. R., Banks, G., Deiwick, J., Hensel, M. and Holden, D. W. (1999). pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol Microbiol, 33, 806–16.CrossRefGoogle ScholarPubMed
Bihl, F., Salez, L., Beaubier, M.et al. (2003). Overexpression of Toll-like receptor 4 amplifies the host response to lipopolysaccharide and provides a survival advantage in transgenic mice. J Immunol, 170, 6141–50.CrossRefGoogle ScholarPubMed
Boehm, U., Klamp, T., Groot, M. and Howard, J. C. (1997). Cellular responses to interferon-gamma. Annu Rev Immunol, 15, 749–95.CrossRefGoogle ScholarPubMed
Brightbill, H. D., Libraty, D. H., Krutzik, S. R.et al. (1999). Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science, 285, 732–6.CrossRefGoogle ScholarPubMed
Bryk, R., Griffin, P. and Nathan, C. (2000). Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature, 407, 211–15.Google ScholarPubMed
Buchmeier, N. A. and Heffron, F. (1991). Inhibition of macrophage phagosome–lysosome fusion by Salmonella typhimurium. Infect Immun, 59, 2232–8.Google ScholarPubMed
Buchmeier, N. A., Libby, S. J., Xu, Y.et al. (1995). DNA repair is more important than catalase for Salmonella virulence in mice. J Clin Invest, 95, 1047–53.CrossRefGoogle ScholarPubMed
Chakravortty, D., Hansen-Wester, I. and Hensel, M. (2002). Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med, 195, 1155–66.CrossRefGoogle ScholarPubMed
Chateau, M. T. and Caravano, R. (1997). The oxidative burst triggered by Salmonella typhimurium in differentiated U937 cells requires complement and a complete bacterial lipopolysaccharide. FEMS Immunol Med Microbiol, 17, 57–66.CrossRefGoogle Scholar
Cirillo, D. M., Valdivia, R. H., Monack, D. M. and Falkow, S. (1998). Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol, 30, 175–88.CrossRefGoogle ScholarPubMed
Crawford, M. J. and Goldberg, D. E. (1998). Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J Biol Chem, 273, 34028–32.CrossRefGoogle ScholarPubMed
Cuellar-Mata, P., Jabado, N., Liu, J.et al. (2002). Nramp1 modifies the fusion of Salmonella typhimurium-containing vacuoles with cellular endomembranes in macrophages. J Biol Chem, 277, 2258–65.CrossRefGoogle ScholarPubMed
Groote, M. A., Ochsner, U. A., Shiloh, M. U.et al. (1997). Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA, 94, 13997–4001.CrossRefGoogle ScholarPubMed
Groote, M. A., Testerman, T., Xu, Y., Stauffer, G. and Fang, F. C. (1996). Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science, 272, 414–17.CrossRefGoogle ScholarPubMed
Jong, R., AltareHaagen, F.et al. (1998). Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science, 280, 1435–8.CrossRefGoogle ScholarPubMed
Dobrovolskaia, M. A. and Vogel, S. N. (2002). Toll receptors, CD14, and macrophage activation and deactivation by LPS. Microbes Infect, 4, 903–14.CrossRefGoogle ScholarPubMed
Dunstan, S. J., Ho, V. A., Duc, C. M.et al. (2001). Typhoid fever and genetic polymorphisms at the natural resistance-associated macrophage protein 1. J Infect Dis, 183, 1156–60.CrossRefGoogle ScholarPubMed
Dunstan, S. J.,Hawn, T. R.,Hue, N. T.et al. (2005). Host susceptibility an clinical outcomes in Toll-like receptor 5-deficient patients with typhoid fever in Vietnam. J Infect Dis, 191, 1068–71.CrossRefGoogle ScholarPubMed
Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. and Hinton, J. C. (2003). Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol, 47, 103–18.CrossRefGoogle ScholarPubMed
Everest, P., Roberts, M. and Dougan, G. (1998). Susceptibility to Salmonella typhimurium infection and effectiveness of vaccination in mice deficient in the tumor necrosis factor alpha p55 receptor. Infect Immun, 66, 3355–64.Google ScholarPubMed
Ezekowitz, R. A., Dinauer, M. C., Jaffe, H. S., Orkin, S. H. and Newburger, P. E. (1988). Partial correction of the phagocyte defect in patients with X-linked chronic granulomatous disease by subcutaneous interferon gamma. N Engl J Med, 319, 146–51.CrossRefGoogle ScholarPubMed
Fields, P. I., Swanson, R. V., Haidaris, C. G. and Heffron, F. (1986). Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA, 83, 5189–93.CrossRefGoogle ScholarPubMed
Flo, T. H., Halaas, O., Lien, E.et al. (2000). Human Toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B streptococci or lipopolysaccharide. J Immunol, 164, 2064–9.CrossRefGoogle ScholarPubMed
Forbes, J. R. and Gros, P. (2003). Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood, 102, 1884–92.CrossRefGoogle ScholarPubMed
Fritsche, G., Dlaska, M., Barton, H.et al. (2003). Nramp1 functionality increases inducible nitric oxide synthase transcription via stimulation of IFNγ regulatory factor 1 expression. J Immunol, 171, 1994–8.CrossRefGoogle Scholar
Gallois, A., Klein, J. R., Allen, L. A., Jones, B. D. and Nauseef, W. M. (2001). Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane. J Immunol, 166, 5741–8.CrossRefGoogle ScholarPubMed
Garcia-del Portillo, F. and Finlay, B. B. (1995). Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol, 129, 81–97.CrossRefGoogle ScholarPubMed
Garmendia, J., Beuzon, C. R., Ruiz-Albert, J. and Holden, D. W. (2003). The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. Microbiology, 149, 2385–96.CrossRefGoogle ScholarPubMed
Garvis, S. G., Beuzon, C. R. and Holden, D. W. (2001). A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol, 3, 731–44.CrossRefGoogle ScholarPubMed
Goswami, T., Bhattacharjee, A., Babal, P.et al. (2001). Natural-resistance-associated macrophage protein 1 is an H+/bivalent cation antiporter. Biochem J, 354, 511–19.CrossRefGoogle Scholar
Groisman, E. A. and Saier, M. H. Jr. (1990). Salmonella virulence: new clues to intramacrophage survival. Trends Biochem Sci, 15, 30–3.CrossRefGoogle ScholarPubMed
Gruenheid, S., Pinner, E., Desjardins, M. and Gros, P. (1997). Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J Exp Med, 185, 717–30.CrossRefGoogle ScholarPubMed
Hantke, K. (1997). Ferrous iron uptake by a magnesium transport system is toxic for Escherichia coli and Salmonella typhimurium. J Bacteriol, 179, 6201–4.CrossRefGoogle ScholarPubMed
Hashim, S., Mukherjee, K., Raje, M., Basu, S. K. and Mukhopadhyay, A. (2000). Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem, 275, 16281–8.CrossRefGoogle Scholar
Hayashi, F., Smith, K. D., Ozinsky, A.et al. (2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature, 410, 1099–103.CrossRefGoogle ScholarPubMed
Hemmi, H., Takeuchi, O., Kawai, T.et al. (2000). A Toll-like receptor recognizes bacterial DNA. Nature, 408, 740–5.CrossRefGoogle ScholarPubMed
Hess, J., Ladel, C., Miko, D. and Kaufmann, S. H. (1996). Salmonella typhimurium aroA− infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFNγ in bacterial clearance independent of intracellular location. J Immunol, 156, 3321–6.Google Scholar
Hirschfeld, M., Ma, Y., Weis, J. H., Vogel, S. N. and Weis, J. J. (2000). Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J Immunol, 165, 618–22.CrossRefGoogle ScholarPubMed
Hormaeche, C. E. (1979). Genetics of natural resistance to Salmonella in miceImmunology, 37, 319–27.Google ScholarPubMed
Imlay, J. A. (2003). Pathways of oxidative damage. Annu Rev Microbiol, 57, 395–418.CrossRefGoogle ScholarPubMed
Imlay, J. A. and Linn, S. (1986). Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide. J Bacteriol, 166, 519–27.CrossRefGoogle ScholarPubMed
Jabado, N., Cuellar-Mata, P., Grinstein, S. and Gros, P. (2003). Iron chelators modulate the fusogenic properties of Salmonella-containing phagosomes. Proc Natl Acad Sci USA, 100, 6127–32.CrossRefGoogle ScholarPubMed
Jabado, N., Jankowski, A., Dougaparsad, S.et al. (2000). Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J Exp Med, 192, 1237–48.CrossRefGoogle ScholarPubMed
Kagaya, K., Watanabe, K. and Fukazawa, Y. (1989). Capacity of recombinant gamma interferon to activate macrophages for Salmonella-killing activity. Infect Immun, 57, 609–15.Google ScholarPubMed
Kehres, D. G., Janakiraman, A., Slauch, J. M. and Maguire, M. E. (2002). SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar Typhimurium. J Bacteriol, 184, 3159–66.CrossRefGoogle Scholar
Kuhn, D. E., Baker, B. D., Lafuse, W. P. and Zwilling, B. S. (1999). Differential iron transport into phagosomes isolated from the RAW264.7 macrophage cell lines transfected with Nramp1Gly169 or Nramp1Asp169. J Leukoc Biol, 66, 113–19.CrossRefGoogle ScholarPubMed
Lafuse, W. P., Alvarez, G. R. and Zwilling, B. S. (2002). Role of MAP kinase activation in Nramp1 mRNA stability in RAW264.7 macrophages expressing Nramp1Gly169. Cell Immunol, 215, 195–206.CrossRefGoogle Scholar
Lalmanach, A. C., Montagne, A., Menanteau, P. and Lantier, F. (2001). Effect of the mouse Nramp1 genotype on the expression of IFNγ gene in early response to Salmonella infection. Microbes Infect, 3, 639–44.CrossRefGoogle Scholar
Lembo, A., Kalis, C., Kirschning, C. J.et al. (2003). Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infect Immun, 71, 6058–62.CrossRefGoogle ScholarPubMed
Leveque, G., Forgetta, V., Morroll, S.et al. (2003). Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar Typhimurium infection in chickens. Infect Immun, 71, 1116–24.CrossRefGoogle ScholarPubMed
Lundberg, B. E., Wolf, R. E., , Jr.Dinauer, M. C., Xu, Y. and Fang, F. C. (1999). Glucose 6-phosphate dehydrogenase is required for Salmonella typhimurium virulence and resistance to reactive oxygen and nitrogen intermediates. Infect Immun, 67, 436–8.Google ScholarPubMed
Mastroeni, P., Arena, A., Costa, G. B.et al. (1991). Serum TNFα in mouse typhoid and enhancement of a Salmonella infection by anti-TNFα antibodies. Microb Pathog, 11, 33–8.CrossRefGoogle Scholar
Mastroeni, P., Skepper, J. N. and Hormaeche, C. E. (1995). Effect of anti-tumor necrosis factor alpha antibodies on histopathology of primary Salmonella infections. Infect Immun, 63, 3674–82.Google ScholarPubMed
Mastroeni, P., Vazquez-Torres, A., Fang, F. C.et al. (2000). Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med, 192, 237–48.CrossRefGoogle ScholarPubMed
Meresse, S., Steele-Mortimer, O., Finlay, B. B. and Gorvel, J. P. (1999). The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. Embo J, 18, 4394–403.CrossRefGoogle ScholarPubMed
Mittrucker, H. W. and Kaufmann, S. H. (2000). Immune response to infection with Salmonella typhimurium in mice. J Leukoc Biol, 67, 457–63.CrossRefGoogle ScholarPubMed
Moors, M. A., Li, L. and Mizel, S. B. (2001). Activation of interleukin-1 receptor-associated kinase by gram-negative flagellin. Infect Immun, 69, 4424–9.CrossRefGoogle ScholarPubMed
Mukherjee, K., Siddiqi, S. A., Hashim, S.et al. (2000). Live Salmonella recruits N-ethylmaleimide-sensitive fusion protein on phagosomal membrane and promotes fusion with early endosome. J Cell Biol, 148, 741–53.CrossRefGoogle ScholarPubMed
Muotiala, A. and Makela, P. H. (1990). The role of IFNγ in murine Salmonella typhimurium infection. Microb Pathog, 8, 135–41.CrossRefGoogle Scholar
Muotiala, A. and Makela, P. H. (1993). Role of gamma interferon in late stages of murine salmonellosis. Infect Immun, 61, 4248–53.Google ScholarPubMed
Muroi, M. and Tanamoto, K. (2002). The polysaccharide portion plays an indispensable role in Salmonella lipopolysaccharide-induced activation of NF-κB through human Toll-like receptor 4. Infect Immun, 70, 6043–7.CrossRefGoogle ScholarPubMed
Muroi, M., Ohnishi, T. and Tanamoto, K. (2002). MD-2, a novel accessory molecule, is involved in species-specific actions of Salmonella lipid A. Infect Immun, 70, 3546–50.CrossRefGoogle ScholarPubMed
Nagai, Y., Akashi, S., Nagafuku, M.et al. (2002). Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol, 3, 667–72.CrossRefGoogle ScholarPubMed
Nakano, Y., Onozuka, K., Terada, Y., Shinomiya, H. and Nakano, M. (1990). Protective effect of recombinant tumor necrosis factor-alpha in murine salmonellosis. J Immunol, 144, 1935–41.Google ScholarPubMed
Nauciel, C. and Espinasse-Maes, F. (1992). Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect Immun, 60, 450–4.Google ScholarPubMed
O'Brien, A. D., Metcalf, E. S. and Rosenstreich, D. L. (1982). Defect in macrophage effector function confers Salmonella typhimurium susceptibility on C3H/HeJ mice. Cell Immunol, 67, 325–33.CrossRefGoogle ScholarPubMed
O'Brien, A. D., Rosenstreich, D. L., Scher, I.et al. (1980). Genetic control of susceptibility to Salmonella typhimurium in mice: role of the LPS gene. J Immunol, 124, 20–4.Google ScholarPubMed
Oh, Y. K., Alpuche-Aranda, C., Berthiaume, E.et al. (1996). Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium. Infect Immun, 64, 3877–83.Google ScholarPubMed
Ozinsky, A., Underhill, D. M., Fontenot, J. D.et al. (2000). The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc Natl Acad Sci USA, 97, 13766–71.CrossRefGoogle ScholarPubMed
Plant, J. and Glynn, A. A. (1976). Genetics of resistance to infection with Salmonella typhimurium in mice. J Infect Dis, 133, 72–8.CrossRefGoogle ScholarPubMed
Poltorak, A., He, X., Smirnova, I.et al. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in tlr4 gene. Science, 282, 2085–8.CrossRefGoogle ScholarPubMed
Rathman, M., Barker, L. P. and Falkow, S. (1997). The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect Immun, 65, 1475–85.Google ScholarPubMed
Rathman, M., Sjaastad, M. D. and Falkow, S. (1996). Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect Immun, 64, 2765–73.Google ScholarPubMed
Richter-Dahlfors, A., Buchan, A. M. J. and Finlay, B. B. (1997). 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, 569–80.CrossRefGoogle ScholarPubMed
Rosenberger, C. M. and Finlay, B. B. (2002). Macrophages inhibit Salmonella typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J Biol Chem, 277, 18753–62.CrossRefGoogle ScholarPubMed
Rosenberger, C. M., Scott, M. G., Gold, M. R., Hancock, R. E. and Finlay, B. B. (2000). Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol, 164, 5894–904.CrossRefGoogle ScholarPubMed
Royle, M. C., Totemeyer, S., Alldridge, L. C., Maskell, D. J. and Bryant, C. E. (2003). Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella typhimurium is a critical but not exclusive event leading to macrophage responses. J Immunol, 170, 5445–54.CrossRefGoogle Scholar
Schapiro, J. M., Libby, S. J. and Fang, F. C. (2003). Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc Natl Acad Sci USA, 100, 8496–501.CrossRefGoogle ScholarPubMed
Schletter, J., Heine, H., Ulmer, A. J. and Rietschel, E. T. (1995). Molecular mechanisms of endotoxin activity. Arch Microbiol, 164, 383–9.CrossRefGoogle ScholarPubMed
Schwandner, R., Dziarski, R., Wesche, H., Rothe, M. and Kirschning, C. J. (1999). Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J Biol Chem, 274, 17406–9.CrossRefGoogle ScholarPubMed
Sebastiani, G., Leveque, G., Lariviere, L.et al. (2000). Cloning and characterization of the murine Toll-like receptor 5 (tlr5) gene: sequence and mRNA expression studies in Salmonella-susceptible MOLF/Ei mice. Genomics, 64, 230–40.CrossRefGoogle ScholarPubMed
Steele-Mortimer, O., Meresse, S., Gorvel, J. P., Toh, B. H. and Finlay, B. B. (1999). Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol, 1, 33–49.CrossRefGoogle ScholarPubMed
Steele-Mortimer, O., St-Louis, M., Olivier, M. and Finlay, B. B. (2000). Vacuole acidification is not required for survival of Salmonella enterica serovar typhimurium within cultured macrophages and epithelial cells. Infect Immun, 68, 5401–4.CrossRefGoogle Scholar
Stevanin, T. M., Poole, R. K., Demoncheaux, E. A. and Read, R. C. (2002). Flavohemoglobin Hmp protects Salmonella enterica serovar Typhimurium from nitric oxide-related killing by human macrophages. Infect Immun, 70, 4399–405.CrossRefGoogle ScholarPubMed
Suvarnapunya, A. E., Lagasse, H. A. and Stein, M. A. (2003). The role of DNA base excision repair in the pathogenesis of Salmonella enterica serovar Typhimurium. Mol Microbiol, 48, 549–59.CrossRefGoogle ScholarPubMed
Swanson, R. N. and O'Brien, A. D. (1983). Genetic control of the innate resistance of mice to Salmonella typhimurium: Ity gene is expressed in vivo by 24 hours after infection. J Immunol, 131, 3014–20.Google ScholarPubMed
Takeshita, F., Leifer, C. A., Gursel, I.et al. (2001). Cutting edge: role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J Immunol, 167, 3555–8.CrossRefGoogle ScholarPubMed
Takeuchi, O., Hoshino, K. and Akira, S. (2000). Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol, 165, 5392–6.CrossRefGoogle ScholarPubMed
Takeuchi, O., Takeda, K., Hoshino, K.et al. (2000). Cellular responses to bacterial cell wall components are mediated through MyD88-dependent signaling cascades. Int Immunol, 12, 113–17.CrossRefGoogle ScholarPubMed
Tapping, R. I., Akashi, S., Miyake, K., Godowski, P. J. and Tobias, P. S. (2000). Toll-like receptor 4, but not Toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J Immunol, 165, 5780–7.CrossRefGoogle Scholar
Tite, J. P., Dougan, G. and Chatfield, S. N. (1991). The involvement of tumor necrosis factor in immunity to Salmonella infection. J Immunol, 147, 3161–4.Google ScholarPubMed
Totemeyer, S., Foster, N., Kaiser, P., Maskell, D. J. and Bryant, C. E. (2003). Toll-like receptor expression in C3H/HeN and C3H/HeJ mice during Salmonella enterica serovar Typhimurium infection. Infect Immun, 71, 6653–7.CrossRefGoogle ScholarPubMed
Tsolis, R. M., Baumler, A. J. and Heffron, F. (1995). Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect Immun, 63, 1739–44.Google ScholarPubMed
Tsolis, R. M., Baumler, A. J., Heffron, F. and Stojiljkovic, I. (1996). Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun, 64, 4549–56.Google ScholarPubMed
Uchiya, K., Barbieri, M. A., Funato, K.et al. (1999). A Salmonella virulence protein that inhibits cellular trafficking. Embo J, 18, 3924–33.CrossRefGoogle ScholarPubMed
Straaten, T., Diepen, A., Kwappenberg, K.et al. (2001). Novel Salmonella enterica serovar Typhimurium protein that is indispensable for virulence and intracellular replication. Infect Immun, 69, 7413–18.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A. and Fang, F. C. (2001a). Oxygen-dependent anti-Salmonella activity of macrophages. Trends Microbiol, 9, 29–33.CrossRefGoogle Scholar
Vazquez-Torres, A. and Fang, F. C. (2001b). Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect, 3, 1313–20.CrossRefGoogle Scholar
Vazquez-Torres, A., Fantuzzi, G., Edwards, C. K. R., Dinarello, C. A. and Fang, F. C. (2001). Defective localization of the NADPH phagocyte oxidase to Salmonella-containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages. Proc Natl Acad Sci USA, 98, 2561–5.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H. and Fang, F. C. (2000a). 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, 227–36.CrossRefGoogle Scholar
Vazquez-Torres, A., Vallance, B. A., Bergman, M. A.et al. (2004). Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J Immunol, 172, 6202–8.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A., Xu, Y., Jones-Carson, J.et al. (2000b). Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science, 287, 1655–8.CrossRefGoogle Scholar
Vidal, S., Tremblay, M. L., Govoni, G.et al. (1995). The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med, 182, 655–66.CrossRefGoogle ScholarPubMed
Vidal, S. M., Malo, D., Vogan, K., Skamene, E. and Gros, P. (1993). Natural resistance to infection with intracellular parasites: isolation of a candidate for BcgCell, 73, 469–85.CrossRefGoogle ScholarPubMed
Vieira, O. V., Botelho, R. J. and Grinstein, S. (2002). Phagosome maturation: aging gracefully. Biochem J, 366, 689–704.CrossRefGoogle ScholarPubMed
Webb, J. L., Harvey, M. W., Holden, D. W. and Evans, T. J. (2001). Macrophage nitric oxide synthase associates with cortical actin but is not recruited to phagosomes. Infect Immun, 69, 6391–400.CrossRefGoogle Scholar
Yoshimura, A., Lien, E., Ingalls, R. R., Tuomanen, E., Dziarski, R. and Golenbock, D. (1999). Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J Immunol, 163, 1–5.Google ScholarPubMed
Zaharik, M. L., Vallance, B. A., Puente, J. L., Gros, P. and Finlay, B. B. (2002). Host–pathogen interactions: host resistance factor Nramp1 up-regulates the expression of Salmonella pathogenicity island-2 virulence genes. Proc Natl Acad Sci USA, 99, 15705–10.CrossRefGoogle ScholarPubMed
Zwilling, B. S., Kuhn, D. E., Wikoff, L., Brown, D. and Lafuse, W. (1999). Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect Immun, 67, 1386–92.Google ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×