Pathogenicity Islands and Host Adaptation of Salmonella Serovars

  • R. A. Kingsley
  • A. J. Bäumler
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 264/1)


The term ‘pathogenicity island’ was coined in reference to large (70–190kb), unstable genomic regions encoding hemolysin and fimbrial adhesins present in uropathogenic Escherichia coli strains but absent from nonpathogenic isolates, such as the K-12 strain (Blum et al. 1994; Hacker et al. 1983, 1990; Hughes et al. 1987; Knapp et al. 1986; Ritter et al. 1995). The concept helped to explain, in genetic and evolutionary terms, why closely related strains of E. coli may differ substantially in their pathogenic potential. E. coli contains commensal organisms that are part of our normal intestinal flora as well as a number of intestinal and extraintestinal pathogens (Caugant et al. 1983; Nataro and Kaper 1998; Ochman and Selander 1984). In general terms, pathogenicity islands are quintessentially large DNA regions conferring a virulence trait which is absent from a closely related, nonpathogenic, reference species or strain. Analysis of pathogenicity islands in a variety of animal and plant pathogens has revealed a number of common features (Hacker et al. 1997). Pathogenicity islands are often (a) large (> 30kb), (b) inserted in tRNA genes, (c) associated with inverted repeats, transposases, integrases, or plasmid origin of replication, and (d) have a G + C content that is atypical for the pathogen’s genome. In practice, many or none of these may be features of a pathogenicity island.


Horizontal Gene Transfer tRNA Gene Virulence Determinant Pathogenicity Island Phage Type 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ahmer BM, Tran M, Heffron F (1999) The virulence plasmid of Salmonella typhimurium is self-transmissible. J Bacteriol 181: 1364–1368PubMedGoogle Scholar
  2. Aleksic S, Heinzerling F, Bockemühl J (1996) Human infection caused by salmonellae of subspecies II to VI in Germany, 1977–1992. Zbl Bakt 283: 391–398Google Scholar
  3. Alpuche-Aranda CM, Berthiaume EP, Mock B, Swanson JA, Miller SI (1995) Spacious phagosome formation within mouse macrophages correlates with Salmonella serotype pathogenicity and host susceptibility. Infect Immun 63: 4456–4462PubMedGoogle Scholar
  4. Barrow PA, Huggins MB, Lovell MA (1994) Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect Immun 62: 4602–4610PubMedGoogle Scholar
  5. Bäumler Al (1997) The record of horizontal gene transfer in Salmonella. Trends Microbiol 5: 318–322PubMedCrossRefGoogle Scholar
  6. Bäumler AJ, Heffron F (1995) Identification and sequence analysis of 1pfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol 177: 2087–2097PubMedGoogle Scholar
  7. Bäumler AJ, Tsolis RM, Heffron F (1996) The 1pf fimbrial operon mediates adhesion to murine Peyer’s patches. Proc Natl Acad Sci USA 93: 279–283PubMedCrossRefGoogle Scholar
  8. Bäumler AJ, Gilde AJ, Tsolis RM, van der Velden AWM, Ahmer BMM, Heffron F (1997a) Contribution of horizontal gene transfer and deletion events to the development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J Bacteriol 179: 317–322PubMedGoogle Scholar
  9. Bäumler AJ, Tsolis RM, Valentine PJ, Ficht TA, Heffron F (1997b) Synergistic Effect of Mutations in invA, 1pfC on the Ability of Salmonella typhimurium to Cause Murine Typhoid. Infect Immun 65: 2254–2259PubMedGoogle Scholar
  10. Bäumler AJ, Tsolis RM, Ficht TA, Adams LG (1998) Evolution of host adaptation in Salmonella enterica. Infect Immun 66: 4579–4587PubMedGoogle Scholar
  11. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, Waterman SR, Ryder TA, Boucrot E, Holden DW (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. [published erratum appears in EMBO J 2000 Aug 1, 19: 4191Google Scholar
  12. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, Waterman SR, Ryder TA, Boucrot E, Holden DW (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. [published erratum appears in EMBO J 2000 Embo J 19: 3235–3249Google Scholar
  13. Blanc-Potard AB, Groisman EA (1997) The Salmonella se1C locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16: 5376–5385PubMedCrossRefGoogle Scholar
  14. Blanc-Potard AB, Solomon F, Kayser J, Groisman EA (1999) The SPI-3 pathogenicity island of salmonella enterica [In Process Citation] J Bacteriol 181: 998–1004Google Scholar
  15. Blum G, Ott M, Lichewski A, Ritter A, Imrich H, Tschäpe H, Hacker J (1994) Excision of large DNA regions termed pathogenicity islands from t-RNA-specific loci in the chromosome of an Escherichia coli wild type pathogen. Infect Immun 62: 606–614PubMedGoogle Scholar
  16. Bolton AJ, Martin GD, Osborne MP, Wallis TS, Stephen J (1999a) Invasiveness of Salmonella serotypes Typhimurium, Choleraesuis and Dublin for rabbit terminal ileum in vitro. J Med Microbiol 48: 801–810Google Scholar
  17. Bolton AJ, Osborne MP, Wallis TS, Stephen J (19996) Interaction of Salmonella choleraesuis, Salmonella dublin and Salmonella typhimurium with porcine and bovine terminal ileum in vivo. Microbiology 145: 2431–2441Google Scholar
  18. Boyd EF, Wang FS, Whittam TS, Selander RK (1996) Molecular genetic relationship of the Salmonellae. Appl Environ Microbiol 62: 804–808PubMedGoogle Scholar
  19. Caugant DA, Levin BR, Lidin-Janson G, Whittam TS, Svanborg Eden C, Selander RK (1983) Genetic diversity and relationships among strains of Escherichia coli in the intestine and those causing urinary tract infections. Prog Allergy 33: 203–227PubMedGoogle Scholar
  20. Chen LM, Kaniga K, Galan JE (1996) Salmonella spp are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101–1115Google Scholar
  21. DeGroote MA, Ochsner UA, Shiloh MU, Nathan C, McCord JM, Dinauer MC, Libby SJ, Vazquez TA, Xu Y, Fang FC (1997) Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA 94: 13997–4001CrossRefGoogle Scholar
  22. Edwards PR, Bruner, DW (1943) The occurrence and distribution of Salmonella types in the United States. J Infect Dis 72: 58–67CrossRefGoogle Scholar
  23. Emmerth M, Goebel W, Miller SI, Hueck CJ (1999) Genomic subtraction identifies Salmonella typhimurium prophages, F-related plasmid sequences, and a novel fimbrial operon, stf, which are absent in Salmonella typhi. J Bacteriol 181: 5652–5661PubMedGoogle Scholar
  24. Folkesson A, Advani A, Sukupolvi S, Pfeifer JD, Normark S, Lofdahl S (1999) Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol Microbiol 33: 612–622PubMedCrossRefGoogle Scholar
  25. Friedrich MJ, Kinsey NE, Vila J, Kadner RJ (1993) Nucleotide sequence of a 139-kb segment of the 90-kb virulence plasmid of Salmonella typhimurium:the presence of fimbrial biosynthetic genes. Mol Microbiol 8: 543–558PubMedCrossRefGoogle Scholar
  26. Galan JE, Curtiss R III (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells., Proc Natl Acad Sci USA 86: 6383–6387PubMedCrossRefGoogle Scholar
  27. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, Hedges S, Wallis TS (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: 903–912PubMedCrossRefGoogle Scholar
  28. Geoffrey E, Gaines S, Landy M, Tigertt WD, Sprintz H, Trapani RJ, Mandel AD, Benenson A S (1960) Studies on infection and immunity in experimental typhoid fever: typhoid fever in chimpanzees orally infected with Salmonella typhosa. J Exp Med 112: 143–166CrossRefGoogle Scholar
  29. Groisman EA, Ochman H (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87: 791–794PubMedCrossRefGoogle Scholar
  30. Groisman EA, Ochman H (1997) How Salmonella became a pathogen. Trends Microbiol 5: 343–349PubMedCrossRefGoogle Scholar
  31. Gulig PA, Curtiss R (1987) Plasmid-associated virulence of Salmonella typhimurium. Infect Immun 1987: 2891–2901Google Scholar
  32. Gulig PA, Doyle TJ, Hughes JA, Matsui H (1998) Analysis of host cells associated with the Spy-mediated increased intracellular growth rate of Salmonella typhimurium in mice. Infect Immun 66: 2471–2485PubMedGoogle Scholar
  33. Guy RL, Gonias LA, Stein MA (2000) Aggregation of host endosomes by salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic. Mol Microbiol 37: 1417–1435PubMedCrossRefGoogle Scholar
  34. Hacker J, Knapp S, Goebel W (1983) Spontaneous deletions and flanking regions of the chromosomally inherited hemolysin determinant of an Escherichia coli 06 strain. J Bacteriol 154: 1145–1152PubMedGoogle Scholar
  35. Hacker J, Bender L, Ott M, Wingender J, Lund B, Marre R, Goebel W (1990) Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog 8: 213–225PubMedCrossRefGoogle Scholar
  36. Hacker J, Blum-Oehler G, Muhldorfer I, Tschape H (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 1089–1097PubMedCrossRefGoogle Scholar
  37. Hardt WD, Urlaub H, Galan JE (1998) A substrate of the centisome 63 type Ill protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci USA 95: 2574–2579PubMedCrossRefGoogle Scholar
  38. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400–403PubMedCrossRefGoogle Scholar
  39. Hensel M, Shea JE, Bäumler AJ, Gleeson C, Blattner F, Holden DW (1997) Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12. J Bacteriol 179: 1105–1111PubMedGoogle Scholar
  40. Hensel M, Nikolaus T, Egelseer C (1999) Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol Microbiol 31: 489–498PubMedCrossRefGoogle Scholar
  41. Hobbie S, Chen LM, Davis RJ, Galan JE (1997) 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: 5550–5559PubMedGoogle Scholar
  42. Hong KH, Miller VL (1998) Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J Bacteriol 180: 1793–1802PubMedGoogle Scholar
  43. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379–433PubMedGoogle Scholar
  44. Hughes C, Hacker J, Duvel H, Goebel W (1987) Chromosomal deletions and rearrangements cause coordinate loss of haemolysis, fimbriation and serum resistance in a uropathogenic strain of Escherichia coli. Microb Pathog 2: 227–230PubMedCrossRefGoogle Scholar
  45. Ishibashi Y, Arai T (1996) A possible mechanism for host-specific pathogenesis of Salmonella serovars. Microb Pathogen 21: 435–446CrossRefGoogle Scholar
  46. Kingsley RA, Bäumler AJ (2000) Host adaptation and the emergence of infectious disease: the Salmonella paradigm, Mol Microbiol 36: 1006–1014PubMedCrossRefGoogle Scholar
  47. Kingsley RA, Reissbrodt R, Rabsch W, Ketley JM, Tsolis RM, Everest P, Dougan G, Baumler AJ, Roberts M, Williams PH (1999) Ferrioxamine-mediated iron(III) utilization by Salmonella enterica. Appl Environ Microbiol 65: 1610–1618PubMedGoogle Scholar
  48. Kingsley RA, Tsolis RM, Townsend SM, Norris TL, TAF, Adams LG, Bäumler AJ (2000a) Impact of horizontal gene transfer on the evolution of Salmonella pathogenesis. In: Brogden KA, Roth JA, Stanton TB, Bolin CA, Minion FC, Wannemuehler MJ (eds) Virulence mechanisms of bacterial pathogens. ASM Press, Washington, DC, pp 227–240Google Scholar
  49. Kingsley RA, van Amsterdam K, Kramer N, Baumler AJ (2000b) The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect Immun 68: 2720–2727PubMedCrossRefGoogle Scholar
  50. Knapp S, Hacker J, Jarchau T, Goebel W (1986) Large unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli) 6 strain 536. J Bacteriol 168: 22–30PubMedGoogle Scholar
  51. Kuhn H, Rabsch W, Tschape H, Tietze E (1982) Characterization and epidemiology of a Salmonella typhimurium epidemic strain (in German). Z Arztl Fortbild (Jena) 76: 607–610Google Scholar
  52. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95: 9413–9417PubMedCrossRefGoogle Scholar
  53. Li J, Smith NH, Nelson K, Crichton PB, Old DC, Whittam TS, Selander RK (1993) Evolutionary origin and radiation of the avian-adapted non-motile salmonellae. J Med Microbiol 38: 129–139PubMedCrossRefGoogle Scholar
  54. Li J, Ochman H, Groisman EA, Boyd EF, Solomon F, Nelson K, Selander RK (1995) Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci USA 92: 7252–7256PubMedCrossRefGoogle Scholar
  55. Lockman HA, Curtisslll R (1992) Virulence of non-type 1-fimbriated and nonfimbriated nonflagellated Salmonella typhimurium mutants in murine typhoid fever. Infect Immun 60: 491–496PubMedGoogle Scholar
  56. McClelland M, Florea L, Sanderson K, Clifton SW, Parkhill J, Churcher C, Dougan G, Wilson RK, Miller W (2000) Comparison of the Escherichia coli K-R genome with sampled genomes of a Klebsiella pneumoniae and three Salmonella enterica serovars, Typhimurium, Typhi and Paratyphi A. Nucleic Acids Res 28: 4974–4986Google Scholar
  57. Miao EA, Miller SI (1999) Bacteriophages in the evolution of pathogen-host interactions. Proc Natl Acad Sci USA 96: 9452–9454PubMedCrossRefGoogle Scholar
  58. Miao EA, Miller SI (2000) A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc Natl Acad Sci USA 97: 7539–7944PubMedCrossRefGoogle Scholar
  59. Miao EA, Scherer CA, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ, Miller SI (1999) Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 34: 850–864Google Scholar
  60. Mills DM, Bajaj V, Lee CA (1995) A 40-kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15: 749–759PubMedCrossRefGoogle Scholar
  61. Mirold S, Rabsch W, Rohde M, Stender S, Tschape H, Russmann H, Igwe E, Hardt WD (1999) Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc Natl Acad Sci USA 96: 9845–9850PubMedCrossRefGoogle Scholar
  62. Monack DM, Raupach B, Hromockyj AE, Falkow S (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833–9838Google Scholar
  63. Morrow BJ, Graham JE, Curtiss R 3rd (1999) Genomic subtractive hybridization and selective capture of transcribed sequences identify a novel Salmonella typhimurium fimbrial operon and putative transcriptional regulator that are absent from the Salmonella typhi genome. Infect Immun 67: 5106–5116PubMedGoogle Scholar
  64. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11: 142–201PubMedGoogle Scholar
  65. Norris FA, Wilson MP, Wallis TS, Galyov EE, Majerus PW (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase [see comments]. Proc Natl Acad Sci USA 95: 14057–14059PubMedCrossRefGoogle Scholar
  66. Ochman H, Groisman EA (1996) Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64: 5410–5412PubMedGoogle Scholar
  67. Ochman H, Selander RK (1984) Evidence for clonal population structure in Escherichia coli. Proc Natl Acad Sci USA 81: 198–201PubMedCrossRefGoogle Scholar
  68. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26: 74–86PubMedCrossRefGoogle Scholar
  69. Ochman H, Soncini FC, Solomon F, Groisman EA (1996) Identification of a pathogenicity island for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800–7804PubMedCrossRefGoogle Scholar
  70. Otto H, Tezcan-Merdol D, Girisch R, Haag F, Rhen M, Koch-Nolte F (2000) The spvB gene-product of the salmonella enterica virulence plasmid is a mono(ADP-ribosyl)transferase. Mol Microbiol 37: 1106–1115PubMedCrossRefGoogle Scholar
  71. Pascopella L, Raupach B, Ghori N, Monack D, Falkow S, Small PL (1995) Host restriction phenotypes of Salmonella typhi and Salmonella gallinarum. Infect Immun 63: 4329–4335PubMedGoogle Scholar
  72. Pascopella L, Falkow S, Small PLC (1996) Identification of a genetic determinant from Salmonella typhimurium that confers upon Salmonella gallinarum enhanced survival in the mouse. 96th Annual ASM Meeting, New Orleans, Louisiana, American Society for MicrobiologyGoogle Scholar
  73. Popoff MY, Le Minor L (1992) Antigenic formulas of the Salmonella serovars. WHO Collaborating Center for Reference and Research on Salmonella, Institute Pasteur, ParisGoogle Scholar
  74. Ritter A, Blum G, Emody L, Kerenyi M, Bock A, Neuhierl B, Rabsch W, Scheutz F, Hacker J (1995) tRNA genes and pathogenicity islands: influence on virulence and metabolic properties of uropathogenic Escherichia coli. Mol Microbiol 17: 109–121Google Scholar
  75. Roudier C, Krause M, Fierer J, Guiney DG (1990) Correlation between the presence of sequences homologous to the vir region of Salmonella dublin plasmid pSDL2 and the virulence of twenty-two Salmonella serotypes in mice. Infect Immun 58: 1180–1185PubMedGoogle Scholar
  76. Saphra I, Wassermann M (1954) Salmonella Cholerae suis. A clinical and epidemiological evaluation of 329 infections identified between 1940 and 1954 in the New York Salmonella Center. Am J Med Sci 228: 525–533Google Scholar
  77. Selander RK, Levin BR (1980) Genetic diversity and structure in Escherichia coli populations. Science 210: 545–547PubMedCrossRefGoogle Scholar
  78. Sojka WJ, Field HI (1970) Salmonellosis in England and Wales 1958–1967. Vet Bull 40: 515–531Google Scholar
  79. Sojka WJ, Wray C (1975) Incidence of Salmonella infection in animals in England and Wales 1968–1973. Vet Rec 96: 280–284Google Scholar
  80. Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, Duronio V, Finlay BB (2000) Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector SigD. J Biol Chem 275: 37718–37724PubMedCrossRefGoogle Scholar
  81. Stein MA, Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB (1996) Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol 20: 151–164PubMedCrossRefGoogle Scholar
  82. Threlfall EJ, Ward LR, Rowe B (1978) Spread of multiresistant strains of Salmonella typhimurium phage types 204 and 193 in Britain. Br Med J 2: 997PubMedCrossRefGoogle Scholar
  83. Threlfall EJ, Frost JA, Ward LR, Rowe B (1990) Plasmid profile typing can be used to subdivide phagetype 49 of Salmonella typhimurium in outbreak investigations. Epidemiol Infect 104: 243–251PubMedCrossRefGoogle Scholar
  84. Threlfall EJ, Rowe B, Ward LR (1993) A comparison of multiple drug resistance in salmonellas from humans and food animals in England and Wales, 1981 and 1990. Epidemiol Infect 111: 189–197PubMedCrossRefGoogle Scholar
  85. Threlfall EJ, Frost JA, Ward LR, Rowe B (1994) Epidemic in cattle and humans of Salmonella typhimurium DT104 with chromosomally integrated multiple drug resistance. Vet Rec 134: 577PubMedCrossRefGoogle Scholar
  86. Tsolis RM, Adams LG, Ficht TA, Baumler AJ (1999a) Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67: 4879–4885PubMedGoogle Scholar
  87. Tsolis RM, Townsend SM, Miao EA, Miller SI, Ficht TA, Adams LG, Baumler AJ (1999b) Identification of a putative Salmonella enterica serotype typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 67: 6385–6393PubMedGoogle Scholar
  88. Tsolis RM, Adams LG, Hantman MJ, Scherer CA, Kimborough T, Kingsley RA, Ficht TA, Miller SI, Bäumler AJ (2000) SspA is required for lethal Salmonella typhimurium infections in calves but is not essential for diarrhea. Infect Immun 68 3158–3163PubMedCrossRefGoogle Scholar
  89. Uchiya K, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA (1999) A Salmonella virulence protein that inhibits cellular trafficking. Embo J 18: 3924–3933PubMedCrossRefGoogle Scholar
  90. van der Velden AWM, Baumler AJ, Tsolis RM, Heffron F (1998) Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice. Infect Immun 66: 2803–2808PubMedGoogle Scholar
  91. van Der Velden AW, Lindgren SW, Worley MJ, Heffron F (2000) Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium. Infect Immun 68: 5702–5709PubMedCrossRefGoogle Scholar
  92. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC, Mastroeni P, Fang FC (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655–1658Google Scholar
  93. Watson PR, Paulin SM, Bland AP, Jones PW, Wallis TS (1995) Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene, Infect Immun 63: 2743–2754PubMedGoogle Scholar
  94. Watson PR, Paulin SM, Jones PW, Wallis TS (2000) Interaction of Salmonella serotypes with porcine macrophages in vitro does not correlate with virulence. Microbiology 146: 1639–1649PubMedGoogle Scholar
  95. Wong KK, McClelland M, Stillwell LC, Sisk EC, Thurston SJ, Saffer JD (1998) Identification and sequence analysis of a 27-kilobase chromosomal fragment containing a Salmonella pathogenicity island located at 92 minutes on the chromosome map of Salmonella enterica serovar typhimurium LT2. Infect Immun 66: 3365–3371PubMedGoogle Scholar
  96. Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, Galyov EE (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883–891PubMedCrossRefGoogle Scholar
  97. Worley MJ, Ching KH, Heffron F (2000) Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 36: 749–761Google Scholar
  98. Wray C, Sojka WJ, Bell JC (1981) Salmonella infection in horses in England and Wales, 1973 to 1979. Vet Rec 109: 398–401Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • R. A. Kingsley
    • 1
  • A. J. Bäumler
    • 1
  1. 1.Department of Medical Microbiology and Immunology, College of MedicineTexas A&M University System Health Science CenterCollege StationUSA

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