Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T17:32:55.771Z Has data issue: false hasContentIssue false
  • English
  • Français

Salmonella-induced enteritis: molecular pathogenesis and therapeutic implications

Published online by Cambridge University Press:  02 July 2007

Abigail N. Layton  and
Edouard E. Galyov
Abigail N. Layton*
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire, RG20 7NN, UK.
Edouard E. Galyov
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire, RG20 7NN, UK.
*
*Corresponding author: Abigail N. Layton, Institute for Animal Health, Compton, Newbury, Berkshire, RG20 7NN, UK. Tel: +44 (0)1635 578411; Fax: +44 (0)1635 577237; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Salmonella-induced enteritis is a gastrointestinal disease that causes major economic and welfare problems throughout the world. Although the infection is generally self-limiting, subgroups of the population such as immunocompromised individuals, the young and the elderly are susceptible to developing more severe systemic infections. The emergence of widespread antibiotic resistance and the lack of a suitable vaccine against enteritis-causing Salmonella have led to a search for alternative therapeutic strategies. This review focuses on how Salmonella induces enteritis at the molecular level in terms of bacterial factors, such as the type III secretion systems used to inject a subset of bacterial proteins into host cells, and host factors, such as Toll-like receptors and cytokines. The type III secreted bacterial proteins elicit a variety of responses in host cells that contribute to enteritis. Cytokines form part of the host defence mechanism, but in combination with bacterial factors can contribute to Salmonella-induced enteritis. We also discuss animal and cell culture models currently used to study Salmonella-induced enteritis, and how understanding the mechanisms of the disease has impacted on the development of Salmonella therapeutics.

Type
Review Article
Information
Expert Reviews in Molecular Medicine , Volume 9 , Issue 18 , July 2007 , pp. 1 - 17
Copyright
Copyright © Cambridge University Press 2007

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

References

1Watson, P.R. et al. (1995) Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun 63, 2743-2754CrossRefGoogle ScholarPubMed
2Coombes, B.K. et al. (2005) Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 73, 7161-7169CrossRefGoogle Scholar
3Bohnhoff, M. et al. (1954) Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc Soc Exp Biol Med 86, 132-137CrossRefGoogle ScholarPubMed
4Bohnhoff, M. et al. (1962) Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J Infect Dis 111, 117-127CrossRefGoogle ScholarPubMed
5Barthel, M. et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71, 2839-2858CrossRefGoogle ScholarPubMed
6Coburn, B. et al. (2005) Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 73, 3219-3227CrossRefGoogle Scholar
7Hapfelmeier, S. et al. (2004) Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72, 795-809CrossRefGoogle ScholarPubMed
8Hapfelmeier, S. et al. (2005) The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174, 1675-1685CrossRefGoogle ScholarPubMed
9Watson, P.R. et al. (1998) Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect Immun 66, 1432-1438CrossRefGoogle Scholar
10Criss, A.K. et al. (2001) Regulation of Salmonella-induced neutrophil transmigration by epithelial ADP-ribosylation factor 6. J Biol Chem 276, 48431-48439CrossRefGoogle ScholarPubMed
11Lee, C.A. et al. (2000) A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci U S A 97, 12283-12288CrossRefGoogle ScholarPubMed
12McCormick, B.A. et al. (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123, 895-907CrossRefGoogle ScholarPubMed
13McCormick, B.A. et al. (1998) Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 160, 455-466CrossRefGoogle ScholarPubMed
14Boyle, E.C., Brown, N.F. and Finlay, B.B. (2006) Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell Microbiol 8, 1946-1957CrossRefGoogle ScholarPubMed
15Hardt, W.D. et al. (1998) S-typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826CrossRefGoogle ScholarPubMed
16Stender, S. et al. (2000) Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 36, 1206-1221CrossRefGoogle ScholarPubMed
17Galan, J.E. and Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573CrossRefGoogle ScholarPubMed
18Morgan, E. (2007) Salmonella Pathogenicity Islands. In Salmonella Molecular Biology and Pathogenesis (Rhen, M., Maskel, D., Mastroeni, P. and Threlfall, J. eds), pp. 67-88, Horizon Bioscience, UK.Google Scholar
19Kubori, T. et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602-605CrossRefGoogle ScholarPubMed
20Page, A.L. and Parsot, C. (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46, 1-11CrossRefGoogle ScholarPubMed
21Fu, Y.X. and Galán, J.E. (1998) Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J Bacteriol 180, 3393-3399CrossRefGoogle ScholarPubMed
22Ehrbar, K. et al. (2003) 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, 6950-6967CrossRefGoogle ScholarPubMed
23Ho Lee, S. and Galan, J.E. (2003) InvB is a type III secretion-associated chaperone for the Salmonella enterica effector protein SopE. J Bacteriol 185, 7279-7284CrossRefGoogle Scholar
24Bronstein, P.A., Miao, E.A. and Miller, S.I. (2000) InvB is a type III secretion chaperone specific for SspA. J Bacteriol 182, 6638-6644CrossRefGoogle ScholarPubMed
25Ehrbar, K. et al. (2004) InvB is required for type III-dependent secretion of SopA in Salmonella enterica serovar Typhimurium. J Bacteriol 186, 1215-1219CrossRefGoogle ScholarPubMed
26Akeda, Y. and Galan, J.E. (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437, 911-915CrossRefGoogle ScholarPubMed
27Scherer, C.A., Cooper, E. and Miller, S.I. (2000) The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol Microbiol 37, 1133-1145CrossRefGoogle ScholarPubMed
28Hayward, R.D. and Koronakis, V. (1999) Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J 18, 4926-4934CrossRefGoogle ScholarPubMed
29Hardt, W.D. and Galán, J.E. (1997) A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci U S A 94, 9887-9892CrossRefGoogle Scholar
30Kaniga, K. et al. (1996) A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol Microbiol 21, 633-641CrossRefGoogle ScholarPubMed
31Hardt, W.D., Urlaub, H. and Galán, J.E. (1998) A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci U S A 95, 2574-2579CrossRefGoogle ScholarPubMed
32Wood, M.W. et al. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29, 883-891CrossRefGoogle ScholarPubMed
33Wood, M.W. et al. (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22, 327-338CrossRefGoogle Scholar
34Mirold, S. et al. (1999) Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc Natl Acad Sci U S A 96, 9845-9850CrossRefGoogle ScholarPubMed
35Bakshi, C.S. et al. (2000) Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J Bacteriol 182, 2341-2344CrossRefGoogle ScholarPubMed
36Friebel, A. et al. (2001) SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem 276, 34035-34040CrossRefGoogle ScholarPubMed
37Fu, Y.X. and Galán, J.E. (1999) A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297CrossRefGoogle ScholarPubMed
38Fu, Y.X. and Galán, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27, 359-368CrossRefGoogle ScholarPubMed
39Stebbins, C.E. and Galán, J.E. (2000) Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell 6, 1449-1460CrossRefGoogle ScholarPubMed
40Galyov, E.E. et al. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25, 903-912CrossRefGoogle ScholarPubMed
41Hong, K.H. and Miller, V.L. (1998) Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J Bacteriol 180, 1793-1802CrossRefGoogle ScholarPubMed
42Norris, F.A. et al. (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci U S A 95, 14057-14059CrossRefGoogle ScholarPubMed
43Steele-Mortimer, O. et al. (2000) Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 275, 37718-37724CrossRefGoogle ScholarPubMed
44Marcus, S.L. et al. (2001) A synaptojanin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation. FEBS Lett 494, 201-207CrossRefGoogle ScholarPubMed
45Zhou, D.G. et al. (2001) A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39, 248-259CrossRefGoogle ScholarPubMed
46Alemán, A. et al. (2005) The amino-terminal non-catalytic region of Salmonella typhimurium SigD affects actin organization in yeast and mammalian cells. Cell Microbiol 7, 1432-1446CrossRefGoogle ScholarPubMed
47Dukes, J.D. et al. (2006) The secreted Salmonella dublin phosphoinositide phosphatase, SopB, localises to PtdIns(3)P containing endosomes and perturbs normal endosome to lysosome trafficking. Biochem J 395, 239-247CrossRefGoogle ScholarPubMed
48Hernandez, L.D. et al. (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805-1807CrossRefGoogle ScholarPubMed
49Hueck, C.J. et al. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 18, 479-490CrossRefGoogle ScholarPubMed
50Kaniga, K., Trollinger, D. and Galán, J.E. (1995) Identification of Two Targets of the Type III Protein Secretion System Encoded by the inv and spa Loci of Salmonella typhimurium That Have Homology to the Shigella IpaD and IpaA Proteins. J Bacteriol 177, 7078-7085CrossRefGoogle Scholar
51Jepson, M.A., Kenny, B. and Leard, A.D. (2001) Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell Microbiol 3, 417-426CrossRefGoogle ScholarPubMed
52McGhie, E.J., Hayward, R.D. and Koronakis, V. (2001) Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J 20, 2131-2139CrossRefGoogle ScholarPubMed
53Zhou, D., Mooseker, M.S. and Galán, J.E. (1999) Role of the S-typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092-2095CrossRefGoogle ScholarPubMed
54Zhou, D.G., Mooseker, M.S. and Galán, J.E. (1999) An invasion-associated Salmonella protein modulates the actin- bundling activity of plastin. Proc Natl Acad Sci USA 96, 10176-10181CrossRefGoogle ScholarPubMed
55Lilic, M. et al. (2003) Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms. Science 301, 1918-1921CrossRefGoogle ScholarPubMed
56McGhie, E.J., Hayward, R.D. and Koronakis, V. (2004) Control of actin turnover by a Salmonella invasion protein. Mol Cell 13, 497-510CrossRefGoogle ScholarPubMed
57Mrsny, R.J. et al. (2004) Identification of hepoxilin A3 in inflammatory events: a required role in neutrophil migration across intestinal epithelia. Proc Natl Acad Sci U S A 101, 7421-7426CrossRefGoogle ScholarPubMed
58Zhang, S. et al. (2002) The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 70, 3843-3855CrossRefGoogle ScholarPubMed
59Jones, M.A. et al. (1998) Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 66, 5799-5804CrossRefGoogle ScholarPubMed
60Wood, M.W. et al. (2000) The secreted effector protein of Salmonella dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell Microbiol 2, 293-303CrossRefGoogle Scholar
61Zhang, Y. et al. (2005) Recognition and ubiquitination of Salmonella type III effector SopA by a ubiquitin E3 ligase, HsRMA1. J Biol Chem 280, 38682-38688CrossRefGoogle ScholarPubMed
62Layton, A.N., Brown, P.J. and Galyov, E.E. (2005) The Salmonella translocated effector SopA is targeted to the mitochondria of infected cells. J Bacteriol 187, 3565-3571CrossRefGoogle Scholar
63Zhang, Y. et al. (2006) The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol 62, 786-793CrossRefGoogle Scholar
64Chang, J., Chen, J. and Zhou, D. (2005) Delineation and characterization of the actin nucleation and effector translocation activities of Salmonella SipC. Mol Microbiol 55, 1379-1389CrossRefGoogle ScholarPubMed
65Hersh, D. et al. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96, 2396-2401CrossRefGoogle ScholarPubMed
66Hernandez, L.D. et al. (2003) A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 163, 1123-1131CrossRefGoogle ScholarPubMed
67Tsolis, R.M. et al. (2000) SspA is required for lethal Salmonella enterica serovar Typhimurium infections in calves but is not essential for diarrhea. Infect Immun 68, 3158-3163CrossRefGoogle Scholar
68Miao, E.A. et al. (1999) Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 34, 850-864CrossRefGoogle Scholar
69Tsolis, R.M. et al. (1999) Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 67, 6385-6393CrossRefGoogle ScholarPubMed
70Schesser, K. et al. (2000) The Salmonella YopJ-homologue AvrA does not possess YopJ-like activity. Microbial Pathogen 28, 59-70CrossRefGoogle Scholar
71Collier-Hyams, L.S. et al. (2002) Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 169, 2846-2850CrossRefGoogle ScholarPubMed
72Haraga, A. and Miller, S.I. (2006) A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol 8, 837-846CrossRefGoogle ScholarPubMed
73Haraga, A. and Miller, S.I. (2003) A Salmonella enterica serovar Typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect Immun 71, 4052-4058CrossRefGoogle ScholarPubMed
74Huang, F.C. et al. (2004) Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar Typhimurium infection. Infect Immun 72, 5052-5062CrossRefGoogle ScholarPubMed
75Janssens, S. and Beyaert, R. (2003) Role of Toll-like receptors in pathogen recognition. Clinical Microbiol Rev 16, 637-646CrossRefGoogle ScholarPubMed
76Akira, S. and Takeda, K. (2004) Toll-like receptor signalling. Nat Rev Immunol 4, 499-511CrossRefGoogle ScholarPubMed
77Eaves-Pyles, T. et al. (2001) Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166, 1248-1260CrossRefGoogle ScholarPubMed
78Gewirtz, A.T. et al. (2001) Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107, 99-109CrossRefGoogle ScholarPubMed
79Lyons, S. et al. (2004) Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 117, 5771-5780CrossRefGoogle ScholarPubMed
80Hayashi, F. et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103CrossRefGoogle ScholarPubMed
81Gewirtz, A.T. et al. (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167, 1882-1885CrossRefGoogle ScholarPubMed
82Feuillet, V. et al. (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci U S A 103, 12487-12492CrossRefGoogle ScholarPubMed
83Vijay-Kumar, M. et al. (2006) Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 169, 1686-1700CrossRefGoogle ScholarPubMed
84Steiner, T.S. (2007) How flagellin and toll-like receptor 5 contribute to enteric infection. Infect Immun 75, 545-552CrossRefGoogle ScholarPubMed
85Eckmann, L. and Kagnoff, M.F. (2001) Cytokines in host defense against Salmonella. Microbes Infect 3, 1191-1200CrossRefGoogle ScholarPubMed
86Eckmann, L., Kagnoff, M.F. and Fierer, J. (1993) Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61, 4569-4574CrossRefGoogle ScholarPubMed
87McCormick, B.A. et al. (1995) Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol 131, 1599-1608CrossRefGoogle ScholarPubMed
88Tükel, C. et al. (2006) Neutrophil influx during non-typhoidal salmonellosis: who is in the driver's seat? FEMS Immunol Med Microbiol 46, 320-329CrossRefGoogle Scholar
89Uribe, J.M. et al. (1996) Epidermal growth factor inhibits Ca2+-dependent Cl− transport in T84 human colonic epithelial cells. Am J Physiol Cell Physiol 271, C914-C922CrossRefGoogle Scholar
90Uribe, J.M. et al. (1996) Phosphatidylinositol 3-Kinase Mediates the Inhibitory Effect of Epidermal Growth Factor on Calcium-dependent Chloride Secretion. J. Biol. Chem. 271, 26588-26595CrossRefGoogle ScholarPubMed
91Eckmann, L. et al. (1997) D-myo-Inositol 1,4,5,6-tetrakisphosphate produced in human intestinal epithelial cells in response to Salmonella invasion inhibits phosphoinositide 3-kinase signaling pathways. Proc Natl Acad Sci U S A 94, 14456-14460CrossRefGoogle ScholarPubMed
92Bertelsen, L.S. et al. (2004) Modulation of chloride secretory responses and barrier function of intestinal epithelial cells by the Salmonella effector protein SigD. Am J Physiol Cell Physiol 287, C939-C948CrossRefGoogle ScholarPubMed
93Jepson, M.A. et al. (1995) Rapid disruption of epithelial barrier function by Salmonella typhimurium is associated with structural modification of intercellular junctions. Infect Immun 63, 356-359CrossRefGoogle ScholarPubMed
94Tafazoli, F., Magnusson, K.E. and Zheng, L. (2003) Disruption of epithelial barrier integrity by Salmonella enterica serovar Typhimurium requires geranylgeranylated proteins. Infect Immun 71, 872-881CrossRefGoogle ScholarPubMed
95Stebbins, C.E. and Galan, J.E. (2001) Structural mimicry in bacterial virulence. Nature 412, 701-705CrossRefGoogle ScholarPubMed
96Kubori, T. and Galan, J.E. (2003) Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115, 333-342CrossRefGoogle ScholarPubMed
97Aserkoff, B. and Bennett, J.V. (1969) Effect of antibiotic therapy in acute salmonellosis on the fecal excretion of salmonellae. N Engl J Med 281, 636-640CrossRefGoogle ScholarPubMed
98van Duijkeren, , and Houwers, D.J. (2000) A critical assessment of antimicrobial treatment in uncomplicated Salmonella enteritis. Vet Microbiol 73, 61-73CrossRefGoogle ScholarPubMed
99Barbara, G. et al. (2000) Role of antibiotic therapy on long-term germ excretion in faeces and digestive symptoms after Salmonella infection. Aliment Pharmacol Ther 14, 1127-1131CrossRefGoogle Scholar
100Guzman, C.A. et al. (2006) Vaccines against typhoid fever. Vaccine 24, 3804-3811CrossRefGoogle ScholarPubMed
101Van Immerseel, F. et al. (2005) Vaccination and early protection against non-host-specific Salmonella serotypes in poultry: exploitation of innate immunity and microbial activity. Epidemiol Infect 133, 959-978CrossRefGoogle ScholarPubMed
102Patel, J.C., Rossanese, O.W. and Galan, J.E. (2005) The functional interface between Salmonella and its host cell: opportunities for therapeutic intervention. Trends Pharmacol Sci 26, 564-570CrossRefGoogle ScholarPubMed
103Kauppi, A.M. et al. (2003) Targeting bacterial virulence: inhibitors of type III secretion in Yersinia. Chem Biol 10, 241-249CrossRefGoogle ScholarPubMed
104Nordfelth, R. et al. (2005) Small-molecule inhibitors specifically targeting type III secretion. Infect Immun 73, 3104-3114CrossRefGoogle ScholarPubMed
105Gauthier, A. et al. (2005) Transcriptional inhibitor of virulence factors in enteropathogenic Escherichia coli. Antimicrob Agents Chemother 49, 4101-4109CrossRefGoogle ScholarPubMed
106Muschiol, S. et al. (2006) A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. Proc Natl Acad Sci U S A 103, 14566-14571CrossRefGoogle ScholarPubMed
107Wolf, K. et al. (2006) Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol Microbiol 61, 1543-1555CrossRefGoogle ScholarPubMed
108Bambou, J.C. et al. (2004) In vivo and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia Coli strain. J Biol Chem 279, 42984-42992CrossRefGoogle ScholarPubMed

Further reading, resources and contacts

A continually updated web-based resource covering the molecular and cellular biology of Salmonella and Escherichia coli can be found at Eco-Sal:

http://www.ecosal.orgGoogle Scholar
http://www.micro.biol.ethz.ch/research/hardt/projects.Google Scholar