1887

Chapter 21 : Mechanisms of Serotype Typhimurium Intestinal Colonization

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Mechanisms of Serotype Typhimurium Intestinal Colonization, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap21-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap21-2.gif

Abstract:

The serotype associated most frequently with , a diarrheal disease, is serotype Typhimurium. Serotype Typhimurium infection in calves is an excellent model for the intestinal pathology, host response, and disease syndrome observed in humans. The interaction of serotype Typhimurium with the intestinal mucosa in calves and humans results in the recruitment of neutrophils whose presence is the histopathologic hallmark for the acute phase of -induced enterocolitis. This neutrophilic infiltrate is associated with necrosis of the upper mucosa in large areas of the terminal ileum and colon. Serotype Typhimurium initiates interaction with epithelial cells by causing the formation of membrane ruffles, a process that results in bacterial internalization. This invasion process is mediated by a type III secretion system (T3SS-1) encoded by genes located on pathogenicity island 1. The main function of the T3SS-1 is to translocate effector proteins into the cytosol of a host cell. Persistence of serotype Typhimurium in the mesenteric lymph nodes has also been described for apparently healthy cattle. The lipopolysaccharide (LPS) of serotype Enteritidis does not contain the O4 antigen but instead carries a tyvelose branch (O9 antigen) as the immunodominant epitope on the trisaccharide backbone of its O-antigen repeat unit.

Citation: Dorsey C, Raffatellu M, Kingsley R, Bäumler A. 2005. Mechanisms of Serotype Typhimurium Intestinal Colonization, p 301-312. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch21

Key Concept Ranking

Type III Secretion System
0.41465202
0.41465202
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Comparison of the amino acid sequences deduced from fimbrial genes of serotype Typhimurium strain LT-2 ( ) with orthologues present in serotype Typhi strain CT-18 (Ty) ( ), serotype Enteritidis phage type 4 (En) (http://www.sanger.ac.uk/Projects/Salmonella/ and http://www.salmonella.org/), K-12 strain MG1655 (K12) ( ), and O157:H7 strain EDL933 (EHEC) ( ). Serotype Typhimurium genes are indicated by arrows. Genes whose deduced amino acid sequences show homology to fimbrial chaperones and outer membrane fimbrial usher proteins are indicated as hatched and black arrows, respectively. The percent identity of deduced serotype Typhimurium amino acid sequences to orthologues (defined by the same location on the genome, as indicated by homology of flanking DNA regions) present in serotype Typhi, serotype Enteritidis, K-12, and O157:H7 are indicated below each arrow. Asterisks indicate that sequences were modified prior to the alignment to correct for truncations, frameshift mutations, or stop codons. NP, gene not present.

Citation: Dorsey C, Raffatellu M, Kingsley R, Bäumler A. 2005. Mechanisms of Serotype Typhimurium Intestinal Colonization, p 301-312. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817619.chap21
1. Abreu, M. T.,, P. Vora,, E. Faure,, L. S. Thomas,, E. T. Arnold,, and M. Arditi. 2001. Decreased expression of Toll-like receptor- 4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J. Immunol. 167: 1609 1616.
2. Ahmer, B. M.,, J. van Reeuwijk,, P. R. Watson,, T. S. Wallis,, and F. Heffron. 1999. Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol. Microbiol. 31: 971 982.
3. Anderson, R. M. 1995. Evolutionary pressures in the spread and persistence of infectious agents in vertebrate populations. Parasitology 111: S15 S31.
4. Bäckhed, F.,, and M. Hornef. 2003. Toll-like receptor 4-mediated signaling by epithelial surfaces: necessity or threat? Microbes Infect. 5: 951 959.
5. Barrow, P. A.,, A. Berchieri, Jr.,, and O. al-Haddad. 1992. Serological response of chickens to infection with Salmonella gallinarum-S. pullorum detected by enzyme-linked immunosorbent assay. Avian Dis. 36: 227 236.
6. Bäumler, A. J.,, A. J. Gilde,, R. M. Tsolis,, A. W. M. van der Velden,, B. M. M. Ahmer,, and F. Heffron. 1997. 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: 317 322.
7. Bäumler, A. J.,, R. M. Tsolis,, F. Bowe,, J. G. Kusters,, S. Hoffmann,, and F. Heffron. 1996. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect. Immun. 64: 61 68.
8. Bäumler, A. J.,, R. M. Tsolis,, and F. Heffron. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc. Natl. Acad. Sci. USA 93: 279 283.
9. Blanc-Potard, A. B.,, F. Solomon,, J. Kayser,, and E. A. Groisman. 1999. The SPI-3 pathogenicity island of salmonella enterica. J. Bacteriol. 181: 998 1004.
10. Blaser, M. J.,, and L. S. Newman. 1982. A review of human salmonellosis. I. Infective dose. Rev. Infect. Dis. 4: 1096 1106.
11. Blattner, F. R.,, G. Plunkett III,, C. A. Bloch,, N. T. Perna,, V. Burland,, M. Riley,, J. Colladovides,, J. D. Glasner,, C. K. Rode,, G. F. Mayhew,, J. Gregor,, N. W. Davis,, H. A. Kirkpatrick,, M. A. Goeden,, D. J. Rose,, B. Mau,, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453 1474.
12. Buchwald, D. S.,, and M. J. Blaser. 1984. A review of human salmonellosis. II. Duration of excretion following infection with nontyphi Salmonella. Rev. Infect. Dis. 6: 345 356.
13. Cario, E.,, and D. K. Podolsky. 2000. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68: 7010 7017.
14. Cario, E.,, I. M. Rosenberg,, S. L. Brandwein,, P. L. Beck,, H. C. Reinecker,, and D. K. Podolsky. 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J. Immunol. 164: 966 972.
15. Centers for Disease Control and Prevention. 1999. Salmonella Surveillance: Annual Tabulation Summary, 1998. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, Ga.
16. Chan, K.,, S. Baker,, C. C. Kim,, C. S. Detweiler,, G. Dougan,, and S. Falkow. 2003. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar Typhimurium DNA microarray. J. Bacteriol. 185: 553 563.
17. Clegg, S.,, B. K. Purcell,, and J. Pruckler. 1987. Characterization of genes encoding type 1 fimbriae of Klebsiella pneumoniae, Salmonella typhimurium, and Serratia marcescens. Infect. Immun. 55: 281 287.
18. Collazo, C. M.,, and J. E. Galan. 1997. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol. 24: 747 756.
19. Collinson, S. K.,, P. S. Doig,, J. L. Doran,, S. Clouthier,, T. J. Trust,, and W. W. Kay. 1993. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J. Bacteriol. 175: 12 18.
20. Day, D. W.,, B. K. Mandal,, and B. C. Morson. 1978. The rectal biopsy appearances in Salmonella colitis. Histopathology 2: 117 131.
21. Duguid, J. P.,, E. S. Anderson,, and I. Campbell. 1966. Fimbriae and adhesive properties in salmonellae. J. Pathol. Bacteriol. 92: 107 137.
22. Eckmann, L.,, J. R. Smith,, M. P. Housley,, M. B. Dwinell,, and M. F. Kagnoff. 2000. Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J. Biol. Chem. 275: 14084 14094.
23. Edwards, P. R.,, and D. W. Bruner. 1943. The occurrence and distribution of Salmonella types in the United States. J. Infect. Dis. 72: 58 67.
24. Emmerth, M.,, W. Goebel,, S. I. Miller,, and C. J. Hueck. 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 5661.
25. Everest, P.,, J. Ketley,, S. Hardy,, G. Douce,, S. Khan,, J. Shea,, D. Holden,, D. Maskell,, and G. Dougan. 1999. Evaluation of Salmonella typhimurium mutants in a model of experimental gastroenteritis. Infect. Immun. 67: 2815 2821.
26. Fallon, M. T.,, W. H. Benjamin, Jr.,, T. R. Schoeb,, and D. E. Briles. 1991. Mouse hepatitis virus strain UAB infection enhances resistance to Salmonella typhimurium in mice by inducing suppression of bacterial growth. Infect. Immun. 59: 852 856.
27. Fallon, M. T.,, T. R. Schoeb,, W. H. Benjamin, Jr.,, J. R. Lindsey,, and D. E. Briles. 1989. Modulation of resistance to Salmonella typhimurium infection in mice by mouse hepatitis virus (MHV). Microb. Pathog. 6: 81 91.
28. Folkesson, A.,, A. Advani,, S. Sukupolvi,, J. D. Pfeifer,, S. Normark,, and S. Lofdahl. 1999. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol. Microbiol. 33: 612 622.
29. Frances, C. L.,, T. A. Ryan,, B. D. Jones,, S. J. Smith,, and S. Falkow. 1993. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364: 639 642.
30. Friedrich, M. J.,, N. E. Kinsey,, J. Vila,, and R. J. Kadner. 1993. Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of fimbrial biosynthetic genes. Mol. Microbiol. 8: 543 558.
31. Frost, A. J.,, A. P. Bland,, and T. S. Wallis. 1997. The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet. Pathol. 34: 369 386.
32. Fu, Y.,, and J. E. Galan. 1998. The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol. Microbiol. 27: 359 368.
33. Fusunyan, R. D.,, N. N. Nanthakumar,, M. E. Baldeon,, and W. A. Walker. 2001. Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr. Res. 49: 589 593.
34. Galán, J. E. 1999. Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr. Opin. Microbiol. 2: 46 50.
35. Galán, J. E.,, and R. Curtiss 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 6387.
36. Galyov, E. E.,, M. W. Wood,, R. Rosqvist,, P. B. Mullan,, P. R. Watson,, S. Hedges,, and T. S. Wallis. 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: 903 912.
37. Gewirtz, A. T.,, T. A. Navas,, S. Lyons,, P. J. Godowski,, and J. L. Madara. 2001. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167: 1882 1885.
38. Gewirtz, A. T.,, A. M. Siber,, J. M. Madara,, and B. A. Mc- Cormick. 1999. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect. Immun. 67: 608 617.
39. Gewirtz, A. T.,, P. O. Simon, Jr.,, C. K. Schmitt,, L. J. Taylor,, C. H. Hagedorn,, A. D. O’Brien,, A. S. Neish,, and J. L. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Investig. 107: 99 109.
40. Girardin, S. E.,, I. G. Boneca,, L. A. Carneiro,, A. Antignac,, M. Jehanno,, J. Viala,, K. Tedin,, M. K. Taha,, A. Labigne,, U. Zahringer,, A. J. Coyle,, P. S. DiStefano,, J. Bertin,, P. J. Sansonetti,, and D. J. Philpott. 2003. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584 1587.
41. Grund, S.,, and R. Meyer. 1987. Fimbriae formation, disease form and vaccination in infection with Salmonella typhimurium variatio copenhagen (STMVC). Berl. Münch. Tierärztl. Wochenschr. 100: 367 373. (In German.)
42. Grund, S.,, and A. Seiler. 1993. Electron microscopic studies of fimbriae and lectin phagocytosis of Salmonella typhimurium variety copenhagen (STMVC). Zentbl. Veterinaermed. Reihe B 40: 105 112. (In German.)
43. Hardt, W. D.,, L. M. Chen,, K. E. Schuebel,, X. R. Bustelo,, and J. E. Galan. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815 826.
44. Hardt, W. D.,, and J. E. Galan. 1997. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc. Natl. Acad. Sci. USA 94: 9887 9892.
45. Heithoff, D. M.,, E. Y. Enioutina,, R. A. Daynes,, R. L. Sinsheimer,, D. A. Low,, and M. J. Mahan. 2001. Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect. Immun. 69: 6725 6730.
46. Hermiston, M. L.,, and J. I. Gordon. 1995. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270: 1203 1207.
47. Hershberg, R. M. 2002. The epithelial cell cytoskeleton and intracellular trafficking. V. Polarized compartmentalization of antigen processing and Toll-like receptor signaling in intestinal epithelial cells. Am. J. Physiol. Ser. G 283: G833 G839.
48. Hormaeche, C. E.,, H. S. Joysey,, L. Desilva,, M. Izhar,, and B. A. Stocker. 1991. Immunity conferred by Aro - Salmonella live vaccines. Microb. Pathog. 10: 149 158.
49. Hormaeche, C. E.,, P. Mastroeni,, J. A. Harrison,, R. Demarco de Hormaeche,, S. Svenson,, and B. A. Stocker. 1996. Protection against oral challenge three months after i.v. immunization of BALB/c mice with live Aro Salmonella typhimurium and Salmonella enteritidis vaccines is serotype (species)- dependent and only partially determined by the main LPS O antigen. Vaccine 14: 251 259.
50. Hornef, M. W.,, T. Frisan,, A. Vandewalle,, S. Normark,, and A. Richter-Dahlfors. 2002. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J. Exp. Med. 195: 559 570.
51. Hornef, M. W.,, B. H. Normark,, A. Vandewalle,, and S. Normark. 2003. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J. Exp. Med. 198: 1225 1235.
52. Humphries, A. D.,, M. Raffatellu,, S. Winter,, E. H. Weening,, R. A. Kingsley,, R. Droleskey,, S. Zhang,, J. Figueiredo,, S. Khare,, J. Nunes,, L. G. Adams,, R. M. Tsolis,, and A. J. Baumler. 2003. The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol. Microbiol. 48: 1357 1376.
53. Hurd, H. S.,, J. K. Gailey,, J. D. McKean,, and M. H. Rostagno. 2001. Rapid infection in market-weight swine following exposure to a Salmonella typhimurium-contaminated environment. Am. J. Vet. Res. 62: 1194 1197.
54. Inohara, N.,, Y. Ogura,, and G. Nunez. 2002. Nods: a family of cytosolic proteins that regulate the host response to pathogens. Curr. Opin. Microbiol. 5: 76 80.
55. Jepson, M. A.,, B. Kenny,, and A. D. Leard. 2001. Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell. Microbiol. 3: 417 426.
56. Jung, H. C.,, L. Eckmann,, S. K. Yang,, A. Panja,, J. Fierer,, E. Morzycka-Wroblewska,, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Investig. 95: 55 65.
57. Kingsley, R. A.,, and A. J. Bäumler. 2000. Host adaptation and the emergence of infectious disease: the salmonella paradigm. Mol. Microbiol. 36: 1006 1014.
58. Kingsley, R. A.,, A. D. Humphries,, E. H. Weening,, M. R. De Zoete,, S. Winter,, A. Papaconstantinopoulou,, G. Dougan,, and A. J. Bäumler. 2003. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect. Immun. 71: 629 640.
59. Kingsley, R. A.,, A. M. Keestra,, M. R. de Zoete,, and A. J. Bäumler. 2004. The Shad adhesin binds to the cationic cradle of the fibronectin 13FnIII repeat module: evidence for molecular mimicry of heparin binding. Mol. Microbiol. 52: 345 355.
60. Kingsley, R. A.,, R. L. Santos,, A. M. Keestra,, L. G. Adams,, and A. J. Bäumler. 2002. Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol. Microbiol. 43: 895 905.
61. Kingsley, R. A.,, K. van Amsterdam,, N. Kramer,, and A. J. Bäumler. 2000. The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect. Immun. 68: 2720 2727.
62. Kita, E.,, M. Emote,, D. Oku,, F. Nishikawa,, A. Hamburg,, N. Kamikaidou,, and S. Kashiba. 1992. Contribution of interferon gamma and membrane-associated interleukin 1 to the resistance to murine typhoid of Ityr mice. J. Leukoc. Biol. 51: 244 250.
63. Krabisch, P.,, and P. Dorn. 1980. Epidemiologic significance of live vectors in the transmission of Salmonella infections in broiler flocks. Berl. Muench. Tieraerztl.Wochenschr. 93: 232 235.
64. Kukkonen, M.,, T. Raunio,, R. Virkola,, K. Lahteenmaki,, P. H. Makela,, P. Klemm,, S. Clegg,, and T. K. Korhonen. 1993. Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin. Mol. Microbiol. 7: 229 237.
65. Licht, T. R.,, K. A. Krogfelt,, P. S. Cohen,, L. K. Poulsen,, J. Urbance,, and S. Molin. 1996. Role of lipopolysaccharide in colonization of the mouse intestine by Salmonella typhimurium studied by in situ hybridization. Infect. Immun. 64: 3811 3817.
66. Lockman, H. A.,, and R. Curtiss III. 1992. Virulence of nontype 1-fimbriated and nonfimbriated nonflagellated Salmonella typhimurium mutants in murine typhoid fever. Infect. Immun. 60: 491 496.
67. Madara, J. L.,, T. W. Patapoff,, B. Gillece-Castro,, S. P. Colgan,, C. A. Parkos,, C. Delp,, and R. J. Mrsny. 1993. 5′-Adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J. Clin. Investig. 91: 2320 2325.
68. Matsumura, H.,, K. Onozuka,, Y. Terada,, Y. Nakano,, and M. Nakano. 1990. Effect of murine recombinant interferon-gamma in the protection of mice against Salmonella. Int. J. Immunopharmacol. 12: 49 56.
69. McClelland, M.,, K. E. Sanderson,, J. Spieth,, S. W. Clifton,, P. Latreille,, L. Courtney,, S. Porwollik,, J. Ali,, M. Dante,, F. Du,, S. Hou,, D. Layman,, S. Leonard,, C. Nguyen,, K. Scott,, A. Holmes,, N. Grewal,, E. Mulvaney,, E. Ryan,, H. Sun,, L. Florea,, W. Miller,, T. Stoneking,, M. Nhan,, R. Waterston,, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852 856.
70. McGovern, V. J.,, and L. J. Slavutin. 1979. Pathology of Salmonella colitis. Am. J. Surg. Pathol. 3: 483 490.
71. McLaren, I. M.,, and C. Wray. 1991. Epidemiology of Salmonella typhimurium infection in calves: persistence of salmonellae on calf units. Vet. Rec. 129: 461 462.
72. Mead, P. S.,, L. Slutsker,, V. Dietz,, L. F. McCaig,, J. S. Bresee,, C. Shapiro,, P. M. Griffin,, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5: 607 625.
73. Michetti, P.,, M. J. Mahan,, J. M. Slauch,, J. J. Mekalanos,, and M. R. Neutra. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60: 1786 1792.
74. Michetti, P.,, N. Porta,, M. J. Mahan,, J. M. Slauch,, J. J. Mekalanos,, A. L. Blum,, J. P. Kraehenbuhl,, and M. R. Neutra. 1994. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107: 915 923.
75. Mills, D. M.,, V. Bajaj,, and C. A. Lee. 1995. A 40kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol. Microbiol. 15: 749 759.
76. Mirold, S.,, K. Ehrbar,, A. Weissmuller,, R. Prager,, H. Tschape,, H. Russmann,, and W. D. Hardt. 2001. Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2. J. Bacteriol. 183: 2348 2358.
77. Monack, D. M.,, D. M. Bouley,, and S. Falkow. 2004. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1 +/+ mice and can be reactivated by IFN-γ neutralization. J. Exp. Med. 199: 231 241.
78. Moo, D.,, D. O’Boyle,, W. Mathers,, and A. J. Frost. 1980. The isolation of Salmonella from jejunal and caecal lymph nodes of slaughtered animals. Aust. Vet. J. 56: 181 183.
79. Morrow, B. J.,, J. E. Graham,, and R. Curtiss III. 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 5116.
80. Naik, S.,, E. J. Kelly,, L. Meijer,, S. Pettersson,, and I. R. Sanderson. 2001. Absence of Toll-like receptor 4 explains endotoxin hyporesponsiveness in human intestinal epithelium. J. Pediatr. Gastroenterol. Nutr. 32: 449 453.
81. Nanthakumar, N. N.,, R. D. Fusunyan,, I. Sanderson,, and W. A. Walker. 2000. Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis. Proc. Natl. Acad. Sci. USA 97: 6043 6048.
82. Nau, G. J.,, J. F. Richmond,, A. Schlesinger,, E. G. Jennings,, E. S. Lander,, and R. A. Young. 2002. Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. USA 99: 1503 1508.
83. Nau, G. J.,, A. Schlesinger,, J. F. Richmond,, and R. A. Young. 2003. Cumulative Toll-like receptor activation in human macrophages treated with whole bacteria. J. Immunol. 170: 5203 5209.
84. Naughton, P. J.,, G. Grant,, S. Bardocz,, E. Allen-Vercoe,, M. J. Woodward,, and A. Pusztai. 2001. Expression of type 1 fimbriae (SEF 21) of Salmonella enterica serotype Enteritidis in the early colonisation of the rat intestine. J. Med. Microbiol. 50: 191 197.
85. Neilsen, P. O.,, G. A. Zimmerman,, and T. M. McIntyre. 2001. Escherichia coli Braun lipoprotein induces a lipopolysaccharide- like endotoxic response from primary human endothelial cells. J. Immunol. 167: 5231 5239.
86. Nevola, J. J.,, B. A. Stocker,, D. C. Laux,, and P. S. Cohen. 1985. Colonization of the mouse intestine by an avirulent Salmonella typhimurium strain and its lipopolysaccharide-defective mutants. Infect. Immun. 50: 152 159.
87. Nicholson, B.,, and D. Low. 2000. DNA methylation-dependent regulation of pef expression in Salmonella typhimurium. Mol. Microbiol. 35: 728 742.
88. Nicholson, T. L.,, and A. J. Bäumler. 2001. Salmonella enterica serotype Typhimurium elicits cross-immunity against a Salmonella enterica serotype Enteritidis strain expressing LP fimbriae from the lack promoter. Infect. Immun. 69: 204 212.
89. Norris, T. L.,, and A. J. Bäumler. 1999. Phase variation of the lpf fimbrial operon is a mechanism to evade cross immunity between Salmonella serotypes. Proc. Natl. Acad. Sci. USA 96: 13393 13398.
90. Norris, T. L.,, R. A. Kingsley,, and A. J. Bäumler. 1998. Expression and transcriptional control of the Salmonella typhimurium lpf fimbrial operon by phase variation. Mol. Microbiol. 29: 311 320.
91. Onozuka, K.,, S. Shimada,, H. Yamasu,, Y. Osada,, and M. Nakano. 1993. Non-specific resistance induced by a low-toxic lipid A analogue, DT-5461, in murine salmonellosis. Int. J. Immunopharmacol. 15: 657 664.
92. Parkhill, J.,, G. Dougan,, K. D. James,, N. R. Thomson,, D. Pickard,, J. Wain,, C. Churcher,, K. L. Mungall,, S. D. Bentley,, M. T. Holden,, M. Sebaihia,, S. Baker,, D. Basham,, K. Brooks,, T. Chillingworth,, P. Connerton,, A. Cronin,, P. Davis,, R. M. Davies,, L. Dowd,, N. White,, J. Farrar,, T. Feltwell,, N. Hamlin,, A. Haque,, T. T. Hien,, S. Holroyd,, K. Jagels,, A. Krogh,, T. S. Larsen,, S. Leather,, S. Moule,, P. O’Gaora,, C. Parry,, M. Quail,, K. Rutherford,, M. Simmonds,, J. Skelton,, K. Stevens,, S. Whitehead,, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848 852.
93. Perna, N. T.,, G. Plunkett III,, V. Burland,, B. Mau,, J. D. Glasner,, D. J. Rose,, G. F. Mayhew,, P. S. Evans,, J. Gregor,, H. A. Kirkpatrick,, G. Posfai,, J. Hackett,, S. Klink,, A. Boutin,, Y. Shao,, L. Miller,, E. J. Grotbeck,, N. W. Davis,, A. Lim,, E. T. Dimalanta,, K. D. Potamousis,, J. Apodaca,, T. S. Anantharaman,, J. Lin,, G. Yen,, D. C. Schwartz,, R. A. Welch,, and F. R. Blattner. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409: 529 533.
94. Porwollik, S.,, R. M. Wong,, and M. McClelland. 2002. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 99: 8956 8961.
95. Reeves, P. 1993. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet. 9: 17 22.
96. Reis, B. P.,, S. Zhang,, R. M. Tsolis,, A. J. Bäumler,, L. G. Adams,, and R. L. Santos. 2003. The attenuated sopB mutant of Salmonella enterica serovar Typhimurium has the same tissue distribution and host chemokine response as the wild type in bovine Peyer’s patches. Vet. Microbiol. 97: 269 277.
97. Romling, U.,, Z. Bian,, M. Hammar,, W. D. Sierralta,, and S. Normark. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180: 722 731.
98. Rosenberger, C. M.,, M. G. Scott,, M. R. Gold,, R. E. Hancock,, and B. B. Finlay. 2000. Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J. Immunol. 164: 5894 5904.
99. Samuel, J. L.,, J. A. Eccles,, and J. Francis. 1981. Salmonella in the intestinal tract and associated lymph nodes of sheep and cattle. J. Hyg. 87: 225 232.
100. Samuel, J. L.,, D. A. O’Boyle,, W. J. Mathers,, and A. J. Frost. 1979. Isolation of Salmonella from mesenteric lymph nodes of healthy cattle at slaughter. Res. Vet. Sci. 28: 238 241.
101. Sansonetti, P. J.,, J. Arondel,, M. Huerre,, A. Harada,, and K. Matsushima. 1999. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect. Immun. 67: 1471 1480.
102. Santos, R. L.,, R. M. Tsolis,, S. Zhang,, T. A. Ficht,, A. J. Bäumler,, and L. G. Adams. 2001. Salmonella-induced cell death is not required for enteritis in calves. Infect. Immun. 69: 4610 4617.
103. Santos, R. L.,, S. Zhang,, R. M. Tsolis,, A. J. Bäumler,, and L. G. Adams. 2002. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet. Pathol. 39: 200 215.
104. Schmitt, C. K.,, J. S. Ikeda,, S. C. Darnell,, P. R. Watson,, J. Bispham,, T. S. Wallis,, D. L. Weinstein,, E. S. Metcalf,, and A. D. O’Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69: 5619 5625.
105. Sieling, P. A.,, and R. L. Modlin. 2002. Toll-like receptors: mammalian “taste receptors” for a smorgasbord of microbial invaders. Curr. Opin. Microbiol. 5: 70 75.
106. Smith, B. P.,, G. W. Dilling,, J. K. House,, H. Konrad,, and N. Moore. 1995. Enzyme-linked immunosorbent assay for Salmonella serology using lipopolysaccharide antigen. J. Vet. Diagn. Investig. 7: 481 487.
107. Smith, B. P.,, F. Habasha,, M. Reina-Guerra,, and A. J. Hardy. 1979. Bovine salmonellosis: experimental production and characterization of the disease in calves, using oral challenge with Salmonella typhimurium. Am. J. Vet. Res. 40: 1510 1513.
108. Sojka, W. J.,, and H. I. Field. 1970. Salmonellosis in England and Wales 1958-1967. Vet. Bull. 40: 515 531.
109. Stender, S.,, A. Friebel,, S. Linder,, M. Rohde,, S. Mirold,, and W. D. Hardt. 2000. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36: 1206 1221.
110. Sukupolvi, S.,, R. G. Lorenz,, J. I. Gordon,, Z. Bian,, J. D. Pfeifer,, S. J. Normark,, and M. Rhen. 1997. Expression of thin aggregative fimbriae promotes interaction of Salmonella typhimurium SR-11 with mouse small intestinal epithelial cells. Infect. Immun. 65: 5320 5325.
111. Swenson, D. L.,, and S. Clegg. 1992. Identification of ancillary fim genes affecting fimA expression in Salmonella typhimurium. J. Bacteriol. 174: 7697 7704.
112. Townsend, S. M.,, N. E. Kramer,, R. Edwards,, S. Baker,, N. Hamlin,, M. Simmonds,, K. Stevens,, S. Maloy,, J. Parkhill,, G. Dougan,, and A. J. Bäumler. 2001. Salmonella enterica serotype Typhi possesses a unique repertoire of fimbrial gene sequences. Infect. Immun. 69: 2894 2901.
113. Tsolis, R. M.,, L. G. Adams,, T. A. Ficht,, and A. J. Bäumler. 1999. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67: 4879 4885.
114. Tsolis, R. M.,, L. G. Adams,, M. J. Hantman,, C. A. Scherer,, T. Kimborough,, R. A. Kingsley,, T. A. Ficht,, S. I. Miller,, and A. J. Bäumler. 2000. SspA is required for lethal Salmonella typhimurium infections in calves but is not essential for diarrhea. Infect. Immun. 68: 3158 3163.
115. Tsolis, R. M.,, S. M. Townsend,, E. A. Miao,, S. I. Miller,, T. A. Ficht,, L. G. Adams,, and A. J. Bäumler. 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 6393.
116. Underhill, D. M.,, and A. Ozinsky. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14: 103 110.
117. van der Velden, A. W. M.,, A. J. Bäumler,, R. M. Tsolis,, and F. Heffron. 1998. Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice. Infect. Immun. 66: 2803 2808.
118. Wallis, T. S.,, M. Wood,, P. Watson,, S. Paulin,, M. Jones,, and E. Galyov. 1999. Sips, Sops, and SPIs but not stn influence Salmonella enteropathogenesis. Adv. Exp. Med. Biol. 473: 275 280.
119. Watson, P. R.,, E. E. Galyov,, S. M. Paulin,, P. W. Jones,, and T. S. Wallis. 1998. Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect. Immun. 66: 1432 1438.
120. Wood, M. W.,, R. Rosqvist,, P. B. Mullan,, M. H. Edwards,, and E. E. Galyov. 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: 327 338.
121. Wray, C.,, Y. E. Beedell,, and I. M. McLaren. 1991. A survey of antimicrobial resistance in salmonellae isolated from animals in England and Wales during 1984-1987. Br. Vet. J. 147: 356 369.
122. Wray, C.,, and W. J. Sojka. 1978. Experimental Salmonella typhimurium infection in calves. Res. Vet. Sci. 25: 139 143.
123. Wray, C.,, J. N. Todd,, and M. Hinton. 1987. Epidemiology of Salmonella typhimurium infection in calves: excretion of S. typhimurium in the faeces of calves in different management systems. Vet. Rec. 121: 293 296.
124. Yang, S. K.,, L. Eckmann,, A. Panja,, and M. F. Kagnoff. 1997. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113: 1214 1223.
125. Zeng, H.,, A. Q. Carlson,, Y. Guo,, Y. Yu,, L. S. Collier-Hyams,, J. L. Madara,, A. T. Gewirtz,, and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171: 3668 3674.
126. Zhang, S.,, L. G. Adams,, J. Nunes,, S. Khare,, R. M. Tsolis,, and A. J. Bäumler. 2003. Secreted effector proteins of Salmonella enterica serotype Typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect. Immun. 71: 4795 4803.
127. Zhang, S.,, R. A. Kingsley,, R. L. Santos,, H. Andrews-Polymenis,, M. Raffatellu,, J. Figueiredo,, J. Nunes,, R. M. Tsolis,, L. G. Adams,, and A. J. Bäumler. 2003. Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea. Infect. Immun. 71: 1 12.
128. Zhang, S.,, R. L. Santos,, R. M. Tsolis,, S. Stender,, W.-D. Hardt,, A. J. Bäumler,, and L. G. Adams. 2002. SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves infected with Salmonella enterica serotype Typhimurium. Infect. Immun. 70: 3843 3855.
129. Zhou, D.,, L. M. Chen,, L. Hernandez,, S. B. Shears,, and J. E. Galan. 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: 248 259.
130. Zhou, D.,, M. S. Mooseker,, and J. E. Galan. 1999. An invasion- associated Salmonella protein modulates the actinbundling activity of plastin. Proc. Natl. Acad. Sci. USA 96: 10176 10181.
131. Zhou, D.,, M. S. Mooseker,, and J. E. Galan. 1999. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283: 2092 2095.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error