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Intestinal innate immunity and the pathogenesis of Salmonella enteritis

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Abstract

Acute gastroenteritis caused by Salmonella typhimurium infection is a clinical problem with significant public health impact. The availability of several experimental models of this condition has allowed detailed investigation of the cellular and molecular interactions involved in its pathogenesis. Such studies have shed light on the roles played by bacterial virulence factors and host innate immune mechanisms in the development of intestinal inflammation.

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References

  1. Rabsch W, Tschape H, Baumler A: Non-typhoidal salmoaellosis: emerging problems. Microbes Infect 2001; 3: 237–247.

    Article  PubMed  CAS  Google Scholar 

  2. Torok TJ, Tauxe RV, Wise RP, et al: A large community outbreak of salmonellosis caused by intentional contamination of restaurant salad bars. JAMA 1997; 278: 389–395.

    Article  PubMed  CAS  Google Scholar 

  3. Graham SM: Salmonellosis in children in developing and developed countries and populations. Curr Opin Infect Dis 2002; 15: 507–512.

    PubMed  Google Scholar 

  4. Bhan MK, Bahl R, Bhatnagar S: Typhoid and paratyphoid fever. Lancet 2005; 366: 749–762.

    Article  PubMed  CAS  Google Scholar 

  5. Murase T, Yamada M, Muto T, Matsushima A, Yamai S: Fecal excretion of Salmonella enterica serovar Typhimurium following a food-borne outbreak. J Clin Microbiol 2000; 38: 3495–3497.

    PubMed  CAS  Google Scholar 

  6. Nishio T, Nakamori N, Miyazaki K: Survival of Salmoneila typhi in oysters. Zentralbl Bakteriol Mikrobiol Hyg [B] 1981; 172: 415–426.

    CAS  Google Scholar 

  7. Wait DA, Sobsey MD: Comparative survival of enteric viruses and bacteria in Atlantic Ocean seawater. Water Sci Technol 2001; 43: 139–142.

    PubMed  CAS  Google Scholar 

  8. Galan JE: Salinonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 2001; 17: 53–86.

    Article  PubMed  CAS  Google Scholar 

  9. Blaser MJ, Newman LS: A review of human salmonellosis I. Infective dose. Rev Infect Dis 1982; 4: 1096–1106.

    PubMed  CAS  Google Scholar 

  10. Hurley BP, McCormick BA: Translating tissue culture results into animal models: the case of Salmonella typhimurium. Trends Microbiol 2003; 11: 562–569.

    Article  PubMed  CAS  Google Scholar 

  11. Tsolis RM, Adams LG, Ficht TA, Baumler AJ: Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 1999; 67: 4879–4885.

    PubMed  CAS  Google Scholar 

  12. Kent TH, Formal SB, Labrec EH: Salmonella gastroenteritis in Rhesus monkeys. Arch Pathol 1966; 82: 272–279.

    PubMed  CAS  Google Scholar 

  13. Roat WR, Formal SB, Dammin GJ, Giannella RA: Pathophysiology of Salmonella diarrhea in the Rhesus monkey: Intestinal transport, morphological and bacteriological studies. Gastroenterology 1974; 67: 59–70.

    Google Scholar 

  14. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, 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 2003; 71: 2839–2858.

    Article  PubMed  CAS  Google Scholar 

  15. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, Hardt WD: 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 2004; 72: 795–809.

    Article  PubMed  CAS  Google Scholar 

  16. Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, Hardt WD: Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 2004; 72: 4138–4150.

    Article  PubMed  CAS  Google Scholar 

  17. Hapfelmeier S, Stecher B, Barthel M, et al: 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 2005; 174: 1675–1685.

    PubMed  CAS  Google Scholar 

  18. Hapfelmeier S, Hardt WD: A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol 2005; 13: 497–503.

    Article  PubMed  CAS  Google Scholar 

  19. Rhee SJ, Walker WA, Cherayil BJ: Developmentally regulated intestinal expression of IFNγ and its target genes and the age-specific response to enteric Salmonella infection. J Immunol 2005; 175: 1127–1136.

    PubMed  CAS  Google Scholar 

  20. Suar M, Jantsch J, Hapfelmeier S, et al: Virulence of broad- and narrow-host-range Salmonella enterica serovars in the streptomycin-pretreated mouse model. Infect Immun 2006; 74: 632–644.

    Article  PubMed  CAS  Google Scholar 

  21. McCormick BA, Stocker BA, Laux DC, Cohen PS: Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice. Infect Immun 1988; 56: 2209–2217.

    PubMed  CAS  Google Scholar 

  22. Murray RA, Lee CA: Invasion genes are not required for Salmonella enterica serovar Typhimurium to breach the intestinal epithelium: evidence that Salmonella pathogenicity island 1 has alternative functions during infection. Infect Immun 2000; 68: 5050–5055.

    Article  PubMed  CAS  Google Scholar 

  23. Humphries AD, Townsend SM, Kingsley RA, Nicholson TL, Tsolis RM, Baumler AJ: Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol Lett 2001; 201: 121–125.

    Article  PubMed  CAS  Google Scholar 

  24. Dorsey CW, Laarakker MC, Humphries AD, Weening EH, Baumler AJ: Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol 2005; 57: 196–211.

    Article  PubMed  CAS  Google Scholar 

  25. Kubori T, Galan JE: Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 2003; 115:333–342.

    Article  PubMed  CAS  Google Scholar 

  26. Hayden MS, Ghosh S: Signaling to NF-kB. Genes Dev 2004; 18: 2195–2224.

    Article  PubMed  CAS  Google Scholar 

  27. Huang FC, Werne A, Li Q, Galyov EE, Walker WA, Cherayil BJ: Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar Typhimurium infection. Infect Immun 2004; 72: 5052–5062.

    Article  PubMed  CAS  Google Scholar 

  28. Mrsny RJ, Gewirtz AT, Siccardi D, et al: Identification of hepoxilin A3 in inflammatory events: a required role in neutrophil migration across intestinal epithelia. Proc Natl Acad Sci USA 2004; 101: 7421–7426.

    Article  PubMed  CAS  Google Scholar 

  29. Silva M, Song C, Nadeau WJ, Matthews JB, McCormick BA: Salmonella typhimurium SipA-induced neutrophil transepithelial migration: involvement of a PKC-alpha-dependent signal transduction pathway. Am J Physiol Gastrointest Liver Physiol 2004; 286: G1024–1031.

    Article  PubMed  CAS  Google Scholar 

  30. Zen K, Parkos CA: Leukocyte-epithelial interactions. Curr Opin Cell Biol 2003; 15: 557–564.

    Article  PubMed  CAS  Google Scholar 

  31. Ginzberg HH, Shannon PT, Suzuki T et al: Leukocyte elastase induces epithelial apoptosis: role of mitochondrial permeability changes and Akt. Am J Physiol Gastrointest Liver Physiol 2004; 287: G286–298.

    Article  PubMed  CAS  Google Scholar 

  32. Norris FA, Wilson MP, Wallis TS, Galyov EE, Majerus PW: SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 1998; 95: 14057–14059.

    Article  PubMed  CAS  Google Scholar 

  33. Feng Y, Wente SR, Majerus PW: Overex pression of the inositol phosphatase SopB in human 293 cells stimulates cellular chloride influx and inhibits nuclear mRNA export. Proc Natl Acad Sci USA 2001; 98: 875–879.

    Article  PubMed  CAS  Google Scholar 

  34. Stecle-Mortimer O, Knodler LA, Marcus SL, et al: Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 2000; 275: 37718–37724.

    Article  Google Scholar 

  35. Huang FC, Li Q, Cherayil BJ: A phosphatidyl-inositol-3-kinase-dependent anti-inflammatory pathway activated by Salmonella in epithelial cells. FEMS Microbiol Lett, 2005; 243: 265–270.

    Article  PubMed  CAS  Google Scholar 

  36. Neish AS, Gewirtz AT, Zeng H, et al: Prokaryotic regulation of epithelial responses by inhibition of 1kBα ubiquitination. Science 2000; 289: 1560–1563.

    Article  PubMed  CAS  Google Scholar 

  37. Collier-Hyams LS, Zeng H, Sun J, et al: Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kB pathway. J Immunol 2002; 169: 2846–2850.

    PubMed  CAS  Google Scholar 

  38. Zhang S, Santos RL, Tsolis RM, 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 2002; 70: 3843–3855.

    Article  PubMed  CAS  Google Scholar 

  39. Zhang S, Adams LG, Nunes J, Khare S, Tsolis RM, Baumler AJ: Secreted effector proteins of Salmonella enterica serotype Typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 2003; 71: 4795–4803.

    Article  PubMed  CAS  Google Scholar 

  40. Raffatellu M, Wilson RP, Chessa D, et al: SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect Immun 2005; 73:146–154.

    Article  PubMed  CAS  Google Scholar 

  41. Beutler B, Jiang Z, Georgel P, et al: Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu Rev Immunol 2006; 24: 353–389.

    Article  PubMed  CAS  Google Scholar 

  42. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL: Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 2001; 167: 1882–1885.

    PubMed  CAS  Google Scholar 

  43. Gewirtz AT, Simon PO Jr, Schmitt CK, et al: Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 2001; 107: 99–109.

    PubMed  CAS  Google Scholar 

  44. Lyons S, Wang L, Casanova JE, Sitaraman SV, Merlin D, Gewirtz A: Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 2004; 117: 5771–1580.

    Article  PubMed  CAS  Google Scholar 

  45. Smith KD, Andersen-Nissen E, Hayashi F, et al: Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 2003; 4: 1247–1253.

    Article  PubMed  CAS  Google Scholar 

  46. Subramanian N, Qadri A: Lysophospholipid sensing triggers secretion of flagellin from pathogenic Salmonella. Nat Immunol 2006; 7: 583–589.

    Article  PubMed  CAS  Google Scholar 

  47. Backhed F, Hornef M: Toll-like receptor 4-mediated signaling by epithelial surfaces: necessity or threat? Microbes Infect 2003; 5: 951–959.

    Article  PubMed  CAS  Google Scholar 

  48. Abreu MT, Fukata, M, Arditi M: TLR signaling in the gut in health and disease. J Immunol 2005; 174: 4453–4460.

    PubMed  CAS  Google Scholar 

  49. Humphries AD, Townsend SM, Kingsley RA, Nicholson TL, Tsolis RM, Baumler AJ: Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol Lett 2001; 20: 121–125.

    Article  Google Scholar 

  50. Tukel C, Raffatellu M, Humphries AD, et al: CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol Microbiol 2005; 58: 289–304.

    Article  PubMed  CAS  Google Scholar 

  51. Selsted ME, Ouellette AJ: Mammalian defensins in the antimicrobial immune response. Nat Immunol 2005; 6: 551–557.

    Article  PubMed  CAS  Google Scholar 

  52. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alphadefensins by intestinal Paneth cells in response to bacteria. Nat Immunol 2000; 1: 113–118.

    Article  PubMed  CAS  Google Scholar 

  53. Salzman NH, Ghosh D, Huttner KM, Paterson Y, Bevins CL: Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 2003; 422: 522–526.

    Article  PubMed  CAS  Google Scholar 

  54. Lehrer RI, Ganz T: Cathelicidins: a family of endogenous antimicrobial peptides. Curr Opin Hematol 2002; 9: 18–22.

    Article  PubMed  Google Scholar 

  55. Hase K, Eckmann L, Leopard JD, Varki N, Kagnoff MF: Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antimicrobial protein 18 expression by human colon epithelium. Infect Immun 2002; 70: 953–963.

    Article  PubMed  CAS  Google Scholar 

  56. Rosenberger CM, Gallo RL, Finlay BB: Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc Natl Acad Sci USA 2004; 101: 2422–2427.

    Article  PubMed  CAS  Google Scholar 

  57. Smith PD, Ochsenbauer-Jambor C, Smythies LE: Intestinal macrophages: unique effector cells of the innate immune system. Immunol Rev 2005; 206: 149–159.

    Article  PubMed  CAS  Google Scholar 

  58. Smythies LE, Sellers M, Clements RH, et al: Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacterio cidal activity. J Clin Invest 2005: 115: 66–75.

    Article  PubMed  CAS  Google Scholar 

  59. Malaviya R, Abraham SN: Mast cell modulation of immune responses to bacteria. Immunol Rev 2001; 179: 16–24.

    Article  PubMed  CAS  Google Scholar 

  60. Chatterjea D, Burns-Guydish SM, Sciuto TE, Dvorak A, Contag CH, Galli SJ: Adoptive transfer of mast cells does not enhance the impaired survival of Kit(W)/Kit(W-v) mice in a model of low dose intraperitoneal infection with bioluminescent Salmonella typhimurium. Immunol Lett 2005; 99: 122–129.

    Article  PubMed  CAS  Google Scholar 

  61. Niess JH, Brand S, Gu X, et al: CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005; 307: 254–258.

    Article  PubMed  CAS  Google Scholar 

  62. Sundquist M, Rydstrom A, Wick MJ: Immunity to Salmonella from a dendritic point of view. Cell Microbiol 2004; 6: 1–11.

    Article  PubMed  CAS  Google Scholar 

  63. Tukel C, Raffatellu M, Chessa D, Wilson RP, Akcelik M, Baumler AJ: Neutrophil influx during nontyphoidal salmonellosis: who is in the driver's seat? FEMS Immunol Med Microbiol 2006; 46: 320–329.

    Article  PubMed  CAS  Google Scholar 

  64. Jung HC, Eckmann L, Yang SK, et al: A distinct array of proinflammatory cytokines, is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 1995; 95: 55–65.

    Article  PubMed  CAS  Google Scholar 

  65. Depaolo RW, Lathan R, Rollins BJ, Karpus WJ: The chemokine CCL2 is required for control of murine gastric Salmonella enterica infection. Infect Immun 2005; 73: 6514–6522.

    Article  PubMed  CAS  Google Scholar 

  66. Monack DM, Bouley DM, Falkow S: Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nrampl+/+mice and can be reactivated by IFNγ neutralization. J Exp Med 2004; 199: 231–241.

    Article  PubMed  CAS  Google Scholar 

  67. Abrahams GL, Hensel M: Manipulating cellular transport, and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol 2006; 8: 728–737.

    Article  PubMed  CAS  Google Scholar 

  68. Bispham J, Tripathi BN, Watson PR, Wallis TS: Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect Immun 2001; 69: 367–377.

    Article  PubMed  CAS  Google Scholar 

  69. Everest P, Ketley J, Hardy S, et al: Evaluation of Salmonella typhimurium mutants in a model of experimental gastroenteritis. Infect Immun 1999; 67: 2815–2821.

    PubMed  CAS  Google Scholar 

  70. Blackwell JM, Goswami T, Evans CA et al: SLCIIAI (formerly NRAMP1) and disease resistance. Cell Microbiol 2001; 3: 773–784.

    Article  PubMed  CAS  Google Scholar 

  71. Nakamura A, Mori Y, Hagiwara K, et al: Increased susceptibility to LPS-induced endotoxin shock in secretory leukoprotease inhibitor (SLP1)-deficient mice. J Exp Med 2003; 197: 669–674.

    Article  PubMed  CAS  Google Scholar 

  72. Thuraisingam T, Sam H, Moisan J, Zhang Y, Ding A, Radzioch D: Delayed cutaneous wound healing in mice lacking solute carrier 11a1 (formerly Nrampl): correlation with decreased expression of secretory leukocyte protease inhibitor. J Invest Dermatol 2006; 126: 890–901.

    Article  PubMed  CAS  Google Scholar 

  73. Chlosta S, Fishman DS, Harrington L, et al: The iron efflux protein ferroportin regulates the intracellular growth of Salmonella enterica. Infect Immun 2006; 74: 3065–3067.

    Article  PubMed  CAS  Google Scholar 

  74. Dinarello CA: Blocking IL-1 in systemic inflammation. J Exp Med 2005; 201: 1355–1359.

    Article  PubMed  CAS  Google Scholar 

  75. Hehlgans T, Pfeffer K: The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 2005; 115: 1–20.

    Article  PubMed  CAS  Google Scholar 

  76. Pham CT: Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006; 6: 541–550.

    Article  PubMed  CAS  Google Scholar 

  77. Morohoshi Y, Matsuoka K, Chinen H, et al: Inhibition of neutrophil elastase prevents the development of murine dex tran sulfate sodium-induced, colitis. J Gastroenterol 2006; 41: 318–324.

    Article  PubMed  CAS  Google Scholar 

  78. Lopez-Boado YS, Espinola M, Bahr S, Belaaouaj A: Neutrophil serine proteinases cleave bacterial flagellin, abrogating, its host response-inducing activity. J Immunol 2004; 172: 509–515.

    PubMed  CAS  Google Scholar 

  79. Guiney DG: The role of host cell death in Salmonella infections. Curr Top Microbiol Immunol 2005; 289: 131–150.

    PubMed  CAS  Google Scholar 

  80. Shi Y, Evans JE, Rock KL: Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003; 425: 516–521.

    Article  PubMed  CAS  Google Scholar 

  81. Parker LC, Whyte MK, Dower SK, Sabroe I: The expression and roles of Toll-like receptors in the biology of the human neutrophil. J Leukoc Biol 2005; 77: 886–892.

    Article  PubMed  CAS  Google Scholar 

  82. Li Q, Cherayil BJ: Roll of Toll-like receptor 4 in macrophage activation and tolerance during Salmonella enterica serovar Typhimurium-infection. Infect Immun 2003; 71:4873–4882.

    Article  PubMed  CAS  Google Scholar 

  83. Royle M, Totemeyer S, Aldridge LC, Maskell DJ, Bryant CE: 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 2003; 170:5445–5454.

    PubMed  CAS  Google Scholar 

  84. Lembo A, Kalis C, Kirschning CJ, et al: 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 2003; 71: 6058–6062.

    Article  PubMed  CAS  Google Scholar 

  85. Weiss DS, Raupach B, Takeda K, Akira S, Zychlinsky A: Tofl-like receptors are temporally involved in host defense. J Immunol 2004; 172:4463–4469.

    PubMed  CAS  Google Scholar 

  86. Martinon F, Tschopp J: NLRs join TLRs as innate sensors of pathogens. Trends Immunol 2005; 26: 447–454.

    Article  PubMed  CAS  Google Scholar 

  87. Kanneganti TD, Ozoren N, Body-Malapel M, et al: Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp 3. Nature 2006; 440: 233–236.

    Article  PubMed  CAS  Google Scholar 

  88. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J: Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440: 237–241.

    Article  PubMed  CAS  Google Scholar 

  89. Mariathasan S, Weiss DS, Newton K, et al: Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440: 228–232.

    Article  PubMed  CAS  Google Scholar 

  90. Sutterwala FS, Ogura Y, Szczepanik M, et al: Critical role for NALP3/CIAS1/Cryopyrin in in nate and adaptive immunity through its regulation of caspase-1. Immunity 2006; 24: 317–327.

    Article  PubMed  CAS  Google Scholar 

  91. Miao EA, Alpuche-Aranda CM, Dors M, et al: Cytoplasmic flagellin activates caspase 1 and secretion of IL-1β via Ipaf. Nat Immunol 2006; 7: 569–575.

    Article  PubMed  CAS  Google Scholar 

  92. Franchi L, Amer A, Body-Malapel M, et al: Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in Salmonella-infected macrophages. Nat Immunol 2006; 7: 576–582.

    Article  PubMed  CAS  Google Scholar 

  93. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A: The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 1999; 96: 2396–2401.

    Article  PubMed  CAS  Google Scholar 

  94. Lara-Tejero M, Sutterwala FS, Ogura Y, et al: Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 2006; 203: 1407–1412.

    Article  PubMed  CAS  Google Scholar 

  95. Monack DM, Hersh D, Ghori N, Bouley D, Zychlinsky A, Falkow S: Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 2000; 192: 249–258.

    Article  PubMed  CAS  Google Scholar 

  96. Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH: Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 2004; 14: 806–811

    Article  PubMed  CAS  Google Scholar 

  97. van de Vosse E, Hoeve MA, Ottenhof TH. Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and salmomonellae. Lancet Infect Dis 2004; 4: 739–749.

    Article  PubMed  Google Scholar 

  98. Zhou D, Moosekar MS, Galan JE: Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 1999; 283: 2092–2095.

    Article  PubMed  CAS  Google Scholar 

  99. Hayward RD, Koronakis V: Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J 1999; 18: 4926–434.

    Article  PubMed  CAS  Google Scholar 

  100. Collazo CM, Galan JE: The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol 1997; 24: 747–756.

    Article  PubMed  CAS  Google Scholar 

  101. Jones MA, Wood MW, Mullan PB, Watson PR, Wallis TS, Galyov EE: Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 1998; 66: 5799–5804.

    PubMed  CAS  Google Scholar 

  102. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE: S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998; 93: 815–826.

    Article  PubMed  CAS  Google Scholar 

  103. Bakshi CS, Singh VP, Wood MW, Jones PW, Wallis TS, Galyov EE: Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J Bacteriol 2000; 182: 2341–2344.

    Article  PubMed  CAS  Google Scholar 

  104. Stender S, Friebel A, Linder S, Rohde M, Mirold S, Hardt WD: Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 2000; 36: 1206–1221.

    Article  PubMed  CAS  Google Scholar 

  105. Fu Y, Galan JE: A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999; 401: 293–297.

    Article  PubMed  CAS  Google Scholar 

  106. Hardt WD, Galan JE: A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 1997; 94: 9887–9892.

    Article  PubMed  CAS  Google Scholar 

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Srikanth, C.V., Cherayil, B.J. Intestinal innate immunity and the pathogenesis of Salmonella enteritis. Immunol Res 37, 61–77 (2007). https://doi.org/10.1007/BF02686090

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