Chapter 20 : Pathogen Gene Expression during Intestinal Infection

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

Preview this chapter:
Zoom in

Pathogen Gene Expression during Intestinal Infection, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap20-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap20-2.gif


This chapter discusses what is known about bacterial gene expression during infection of the intestinal tract in animal models of disease. Despite the publication of numerous studies investigating gene expression by pathogens that colonize the intestinal tract, many of these studies were performed in vitro or in cell culture models of infection. While the importance of these investigations cannot be disputed, these systems do not fully represent the complex milieu of the intestinal tract, on which the chapter is focused. In addition, since many intestinal pathogens have the ability to cause serious systemic disease, bacterial gene expression has been examined at sites of systemic infection. DNA microarrays have been recently used to examine gene expression in rabbit ligated ileal loops. Genes encoding transcriptional regulatory factors, including , were absent from the set of serovar Typhimurium genes induced specifically in the small intestine. Of the three species that infect humans, and are enteric pathogens. harbors a virulence plasmid, known as pYV, that carries many genes required for virulence. Using a strain lacking this plasmid, chromosomal intestinal genes were identified in the PP of mice 24 h after oral infection. The examination of gene expression in diverse bacterial pathogens during intestinal infection has revealed much about the conditions experienced during this process.

Citation: Butler S, Tischler A, Camilli A. 2005. Pathogen Gene Expression during Intestinal Infection, p 283-299. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch20
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Angelichio, M. J.,, and A. Camilli. 2002. In vivo expression technology. Infect. Immun. 70: 6518 6523.
2. Autret, N.,, I. Dubail,, P. Trieu-Cuot,, P. Berche,, and A. Charbit 2001. Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagensis. Infect. Immun. 69: 2054 2065.
3. Bader, M. W.,, W. W. Navarre,, W. Shiau,, H. Nikaido,, J. G. Frye,, M. McClelland,, F. C. Fang,, and S. I. Miller. 2003. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol. Microbiol. 50: 219 230.
4. Bajaj, V.,, R. L. Lucas,, C. Hwang,, and C. A. Lee. 1996. Coordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22: 703 714.
5. Bartoleschi, C.,, M. C. Pardini,, C. Scaringi,, M. C. Martino,, C. Pazzani,, and M. L. Bernardini. 2002>. Selection of Shigella flexneri candidate virulence genes specifically induced in bacteria resident in host cell cytoplasm. Cell. Microbiol. 4: 613 626.
6. Bienz, M.,, and E. Kubli. 1981. Wild-type tRNAG Tyr reads the TMV RNA stop codon, but Q base-modified tRNAQ Tyr does not. Nature 294: 188 190.
7. Bina, J.,, J. Zhu,, M. Dziejman,, S. Faruque,, S. Calderwood,, and J. Mekalanos. 2003. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl. Acad. Sci. USA 100: 2801 2806.
8. Bourret, R. B.,, N. W. Charon,, A. M. Stock,, and A. H. West. 2002. Bright lights, abundant operons—fluorescence and genomic technologies advance studies of bacterial locomotion and signal transduction: review of the BLAST meeting, Cuernavaca, Mexico, 14 to 19 January 2001. J. Bacteriol. 184: 1 17.
9. Boyd, A. P.,, and G. P. Cornelis,. 2001. Yersinia, p. 227 264. In E. A. Groisman (ed.), Principles of Bacterial Pathogenesis. Academic Press, Ltd., London, United Kingdom.
10. Bumann, D. 2002. Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry. Mol. Microbiol. 43: 1269 1283.
11. Butler, S. M.,, and A. Camilli. 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 101: 5018 5023.
12. Camilli, A.,, D. Beattie,, and J. Mekalanos. 1994. Use of genetic recombination as a reporter of gene expression. Proc. Natl. Acad. Sci. USA 91: 2634 2638.
13. Camilli, A.,, and J. J. Mekalanos. 1995. Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol. Microbiol. 18: 671 683.
14. Carniel, E.,, A. Guiyoule,, I. Guilvout,, and O. Mercereau- Puijalon. 1992. Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia. Mol. Microbiol. 6: 379 388.
15. Carroll, P. A.,, K. T. Tashima,, M. B. Rogers,, V. J. DiRita,, and S. B. Calderwood. 1997. Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol. Microbiol. 25: 1099 1111.
16. Carter, P. B. 1975. Pathogenicity of Yersinia enterocolitica for mice. Infect. Immun. 11: 164 170.
17. Cheng, L. W.,, D. M. Anderson,, and O. Schneewind. 1997. Two independent type II secretion mechanisms for YopE in Yersinia enterocolitica. Mol. Microbiol. 24: 757 765.
18. Chiang, S. L.,, and J. J. Mekalanos. 1998. Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol. Microbiol. 27: 797 805.
19. Cirillo, D. M.,, R. H. Valdivia,, D. M. Monack,, and S. Falkow. 1998. Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol. 30: 175 188.
20. Cormack, B.,, R. H. Valdivia,, and S. Falkow. 1996. FACS-optimized mutants of green fluorescent protein (GFP). Gene 173: 33 38.
21. Cornelis, G.,, Y. Laroche,, G. Balligand,, M.-P. Sory,, and G. Wauters. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9: 64 87.
22. Darwin, A. J.,, and V. L. Miller. 1999. Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature-tagged transposon mutagenesis. Mol. Microbiol. 32: 51 62.
23. Darwin, K. H.,, and V. L. Miller. 1999. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin. Microbiol. Rev. 12: 405 428.
24. Delor, I.,, and G. R. Cornelis. 1992. Role of Yersinia enterocolitica Yst toxin in experimental infection of young rabbits. Infect. Immun. 60: 4269 4277.
25. DiRita, V. J., 2001. Molecular basis of Vibrio cholerae pathogenesis, p. 457 508. In E. A. Groisman (ed.), Principles of Bacterial Pathogenesis. Academic Press, Ltd., London, United Kingdom.
26. DiRita, V. J.,, and J. J. Mekalanos. 1991. Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell 64: 29 37.
27. Dorman, C. J.,, and M. E. Porter. 1998. The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms. Mol. Microbiol. 29: 677 684.
28. Dubail, I.,, P. Berche,, and A. Charbit. 2000. Listeriolysin O as a reporter to identify constitutive and in vivo-inducible promoters in the pathogen Listeria monocytogenes. Infect. Immun. 68: 3242 3250.
29. Durand, J. M.,, B. Dagberg,, B. E. Uhlin,, and G. R. Bjork. 2000. Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol. Microbiol. 35: 924 935.
30. Durand, J. M.,, N. Okada,, T. Tobe,, M. Watarai,, I. Fukuda,, T. Suzuki,, N. Nakata,, K. Komatsu,, M. Yoshikawa,, and C. Sasakawa. 1994. vacC, a virulence-associated chromosomal locus of Shigella flexneri, is homologous to tgt, a gene encoding tRNA-guanine transglycosylase (Tgt) of Escherichia coli K-12. J. Bacteriol. 176: 4627 4634.
31. Earhart, C. F. 1996. Uptake and Metabolism of Iron and Molybdenum. ASM Press, Washington, D.C.
32. Ernst, R. K.,, T. Guina,, and S. I. Miller. 2001. Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect. 3: 1327 1334.
33. Fang, F. C.,, S. J. Libby,, N. A. Buchmeier,, P. C. Loewen,, J. Switala,, J. Harwood,, and D. G. Guiney. 1992. The alternative sigma factor katF ( rpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. USA 89: 11978 11982.
34. Fields, P. I.,, E. A. Groisman,, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243: 1059 1062.
35. Forsberg, A.,, and R. Rosqvist. 1993. In vivo expression of virulence genes of Yersinia pseudotuberculosis. Infect. Agents Dis. 2: 275 278.
36. Freitag, N. E.,, and K. E. Jacobs. 1999. Examination of Listeria monocytogenes intracellular gene expression using the green fluorescent protein of Aequorea victoria. Infect. Immun. 67: 1844 1852.
37. Freter, R.,, and P. C. O’Brien. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonchemotactic Vibrio cholerae mutants in infant mice. Infect. Immun. 34: 222 233.
38. Freter, R.,, H. L. Smith,, and F. J. Sweeney. 1961. An evaluation of intestinal fluids in the pathogenesis of cholera. J. Infect. Dis. 109: 35 42.
39. Frey, B.,, G. Janel,, U. Michelsen,, and H. Kersten. 1989. Mutation in the Escherichia coli fnr and tgt genes: control of molybdate reductase activity and the cytochrome d complex by fnr. J. Bacteriol. 171: 1524 1530.
40. Fullner, K. J.,, and J. J. Mekalanos. 1999. Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect. Immun. 67: 1393 1404.
41. Gahan, C. G. M.,, and C. Hill. 2001. Characterization of the groESL operon in Listeria monocytogenes: utilization of two reporter systems ( gfp and hly) for evaluating in vivo expression. Infect. Immun. 69: 3924 3932.
42. Gahan, C. G. M.,, and C. Hill. 2000. The use of listeriolysin to identify in vivo induced genes in the gram-positive intracellular pathogen Listeria monocytogenes. Mol. Microbiol. 36: 498 507.
43. Galan, J. E.,, C. Ginocchio,, and P. Costeas. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J. Bacteriol. 174: 4338 4349.
44. Garcia Vescovi, E.,, F. C. Soncini,, and E. A. Groisman. 1996. Mg 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165 174.
45. Gardel, C. L.,, and J. J. Mekalanos. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect. Immun. 64: 2246 2255.
46. Gentry, D. R.,, V. J. Hernandez,, L. H. Nguyen,, D. B. Jensen,, and M. Cashel. 1993. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J. Bacteriol. 175: 7982 7989.
47. Gill, D. M. 1977. Mechanism of action of cholera toxin. Adv. Cyclic Nucleotide Res. 8: 85 118.
48. Gosink, K. K.,, R. Kobayashi,, I. Kawagishi,, and C. C. Hase. 2002. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J. Bacteriol. 184: 1767 1771.
49. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183: 1835 1842.
50. Guan, K. L.,, and J. E. Dixon. 1990. Protein tyrosine phosphatase activity is an essential virulence determinant of Yersinia. Science 249: 553 556.
51. Gupta, S.,, and R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65: 1131 1134.
52. Hancock, R. E.,, and M. G. Scott. 2000. The role of antimicrobial peptides in animal defenses. Proc. Natl. Acad. Sci. USA 97: 8856 8861.
53. Handfield, M.,, L. J. Brady,, A. Progulske-Fox,, and J. D. Hillman. 2000. IVIAT: a novel method to identify microbial genes expressed specifically during human infections. Trends Microbiol. 8: 336 339.
54. Hang, L.,, M. John,, M. Asaduzzaman,, E. A. Bridges,, C. Vanderspurt,, T. J. Kirn,, R. K. Taylor,, J. D. Hillman,, A. Progulske-Fox,, M. Handfield,, E. T. Ryan,, and S. B. Calderwood. 2003. Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc. Natl. Acad. Sci. USA 100: 8508 8513.
55. Hase, C. C.,, and J. J. Mekalanos. 1998. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 95: 730 734.
56. Hautefort, I.,, and J. C. Hinton. 2000. Measurement of bacterial gene expression in vivo. Philos. Trans. R. Soc. Lond. Ser. B 355: 601 611.
57. Heesemann, J.,, K. Hantke,, T. Vocke,, E. Saken,, A. Rakin,, I. Stojilijkovic,, and R. Berner. 1993. Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65,000Da and pesticin sensitivity. Mol. Microbiol. 8: 397 408.
58. Heidelberg, J. F.,, J. A. Eisen,, W. C. Nelson,, R. A. Clayton,, M. L. Gwinn,, R. J. Dodson,, D. H. Haft,, E. K. Hickey,, J. D. Peterson,, L. Umayam,, S. R. Gill,, K. E. Nelson,, T. D. Read,, H. Tettelin,, D. Richardson,, M. D. Ermolaeva,, J. Vamathevan,, S. Bass,, H. Qin,, I. Dragoi,, P. Sellers,, L. Mc- Donald,, T. Utterback,, R. D. Fleishmann,, W. C. Nierman,, and O. White. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477 483.
59. Heithoff, D. M.,, C. P. Conner,, P. C. Hanna,, S. M. Julio,, U. Hentschel,, and M. J. Mahan. 1997. Bacterial infection as assessed by in vivo gene expression. Proc. Natl. Acad. Sci. USA 94: 934 939.
60. Heithoff, D. M.,, C. P. Conner,, U. Hentschel,, F. Govantes,, P. C. Hanna,, and M. J. Mahan. 1999. Coordinate intracellular expression of Salmonella genes induced during infection. J. Bacteriol. 181: 799 807.
61. Hensel, M. 2000. Salmonella pathogenicity island 2. Mol. Microbiol. 36: 1015 1023.
62. Hensel, M.,, J. E. Shea,, C. Gleeson,, M. D. Jones,, E. Dalton,, and D. W. Holden. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400 403.
63. Hensel, M.,, J. E. Shea,, S. R. Waterman,, R. Mundy,, T. Nikolaus,, G. Banks,, A. Vazquez-Torres,, C. Gleeson,, F. C. Fang,, and D. W. Holden. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30: 163 174.
64. Herrington, D. A.,, R. H. Hall,, G. Losonsky,, J. J. Mekalanos,, R. K. Taylor,, and M. M. Levine. 1988. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168: 1487 1492.
65. Higgins, D. E.,, and V. J. DiRita. 1994. Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol. Microbiol. 14: 17 29.
66. Higgins, D. E.,, E. Nazareno,, and V. J. DiRita. 1992. The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J. Bacteriol. 174: 6874 6980.
67. Hohmann, A. W.,, G. Schmidt,, and D. Rowley. 1978. Intestinal colonization and virulence of Salmonella in mice. Infect. Immun. 22: 763 770.
68. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62: 379 433.
69. 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.
70. Isberg, R. R.,, and J. M. Leong. 1990. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861 871.
71. Isberg, R. R.,, D. L. Voorhis,, and S. Falkow. 1987. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769 778.
72. Jacobi, C. A.,, S. Gregor,, A. Rakin,, and J. Heesemann. 2001. Expression analysis of the yersiniabactin receptor gene fyuA and the heme receptor hemR of Yersinia enterocolitica in vitro and in vivo using the reporter genes for green fluorescent protein and luciferase. Infect. Immun. 69: 7772 7782.
73. Jacobi, C. A.,, A. Roggenkamp,, A. Rakin,, R. Zumbihl,, L. Leitritz,, and J. Heesemann. 1998. In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene. Mol. Microbiol. 30: 865 882.
74. Jarvis, K. G.,, J. A. Giron,, A. E. Jerse,, T. K. McDaniel,, M. S. Donnenberg,, and J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA 92: 7996 8000.
75. Kammler, M.,, C. Schon,, and K. Hantke. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175: 6212 6219.
76. Kane, C. D.,, R. Schuch,, W. A. Day, Jr.,, and A. T. Maurelli. 2002. MxiE regulates intracellular expression of factors secreted by the Shigella flexneri 2a type III secretion system. J. Bacteriol. 184: 4409 4419.
77. Kennedy, E. P., 1996. Membrane-derived oligosaccharides (periplasmic β-D-glucans) of Escherichia coli, p. 1064 1071. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
78. Kent, T. H.,, S. B. Formal,, and E. H. Labrec. 1966. Salmonella gastroenteritis in rhesus monkeys. Arch. Pathol. 82: 272 279.
79. Khan, M. A.,, and R. E. Isaacson. 2002. Identification of Escherichia coli genes that are specifically expressed in a murine model of septicemic infection. Infect. Immun. 70: 3404 3412.
80. Kim, H. Y.,, D. Schlictman,, S. Shankar,, Z. Xie,, A. M. Chakrabarty,, and A. Kornberg. 1998. Alginate, inorganic polyphosphate, GTP and ppGpp synthesis co-regulated in Pseudomonas aeruginosa: implications for stationary phase survival and synthesis of RNA/DNA precursors. Mol. Microbiol. 27: 717 725.
81. Klose, K. E. 2000. The suckling mouse model of cholera. Trends Microbiol. 8: 189 191.
82.Reference deleted.
83. Krukonis, E. S.,, and V. J. DiRita. 2003. From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae. Curr. Opin. Microbiol. 6: 186 190.
84. Lee, S. H.,, M. J. Angelichio,, J. J. Mekalanos,, and A. Camilli. 1998. Nucleotide sequence and spatiotemporal expression of the Vibrio cholerae vieSAB genes during infection. J. Bacteriol. 180: 2298 2305.
85. Lee, S. H.,, S. M. Butler,, and A. Camilli. 2001. Selection for in vivo regulators of bacterial virulence. Proc. Natl. Acad. Sci. USA 98: 6889 6894.
86. Lee, S. H.,, D. L. Hava,, M. K. Waldor,, and A. Camilli. 1999. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99: 625 634.
87. Lehrer, R. I.,, A. K. Lichtenstein,, and T. Ganz. 1993. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu. Rev. Immunol. 11: 105 128.
88. Lian, C. J.,, and C. H. Pai. 1987. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect. Immun. 55: 1176 1183.
89. Loewen, P. C.,, and R. Hengge-Aronis. 1994. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu. Rev. Microbiol. 48: 53 80.
90. Lostroh, C. P.,, and C. A. Lee. 2001. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 3: 1281 1291.
91. Loubens, L.,, L. Debarbieux,, A. Bohin,, J.-M. Lacroix,, and J. P. Bohin. 1993. Homology between a genetic locus ( mdoA) involved in the osmoregulated biosynthesis of periplasmic glucans in Escherichia coli and a genetic locus ( hrpM) controlling the pathogenicity of Pseudomonas syringae. Mol. Microbiol. 10: 329 340.
92. Mahan, M. J.,, J. M. Slauch,, and J. J. Mekalanos. 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686 688.
93. Mahan, M. J.,, J. W. Tobias,, J. M. Slauch,, P. C. Hanna,, R. J. Collier,, and J. J. Mekalanos. 1995. Antibiotic-based selection for bacterial genes that are specifically induced during infection of a host. Proc. Natl. Acad. Sci. USA 92: 669 673.
94. Martindale, J.,, D. Stroud,, E. R. Moxon,, and C. M. Tang. 2000. Genetic analysis of Escherichia coli K1 gastrointestinal colonization. Mol. Microbiol. 37: 1293 1305.
95. Mecsas, J.,, I. Bilis,, and S. Falkow. 2001. Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect. Immun. 69: 2779 2787.
96. Meier, F.,, B. Suter,, H. Grosjean,, G. Keith,, and E. Kubli. 1985. Queuosine modification of the wobble base in tRNA His influences ‘ in vivo’ decoding properties. EMBO J. 4: 823 827.
97. Merrell, D. S.,, S. M. Butler,, F. Qadri,, N. A. Dolganov,, A. Alam,, M. B. Cohen,, S. B. Calderwood,, G. K. Schoolnik,, and A. Camilli. 2002. Host-induced epidemic spread of the cholera bacterium. Nature 417: 642 645.
98. Merrell, D. S.,, and A. Camilli. 1999. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34: 836 849.
99. Merrell, D. S.,, and A. Camilli. 2000. Detection and analysis of gene expression during infection by in vivo expression technology. Philos. Trans. R. Soc. Lond. Ser. B 355: 587 599.
100. Merrell, D. S.,, D. L. Hava,, and A. Camilli. 2002. Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol. Microbiol. 43: 1471 1491.
101. Miller, S. I.,, A. M. Kukral,, and J. J. Mekalanos. 1989. A two-component regulatory system ( phoP phoQ) controls Salmonella typhimurium virulence. Proc. Natl. Acad. Sci. USA 86: 5054 5058.
102. Miller, S. I.,, and J. J. Mekalanos. 1990. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J. Bacteriol. 172: 2485 2490.
103. Miller, V. L.,, R. K. Taylor,, and J. J. Mekalanos. 1987. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48: 271 279.
104. Moors, M. A.,, B. Levitt,, P. Youngman,, and D. A. Portnoy. 1999. Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67: 131 139.
105. Nachamkin, I.,, and A. M. Hart. 1985. Western blot analysis of the human antibody response to Campylobacter jejuni cellular antigens during gastrointestinal infection. J. Clin. Microbiol. 21: 33 38.
106. Noguchi, S.,, Y. Nishimura,, Y. Hirota,, and S. Nishimura. 1982. Isolation and characterization of an Escherichia coli mutant lacking tRNA-guanine transglycosylase. Function and biosynthesis of queuosine in tRNA. J. Biol. Chem. 257: 6544 6550.
107. Page, F.,, S. Altabe,, N. Hugouvieux-Cotte-Pattat,, J.-M. Lacroix,, J. Robert-Baudouy,, and J.-P. Bohin. 2001. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J. Bacteriol. 183: 3134 3141.
108. Park, Y. K.,, B. Bearson,, S. H. Bang,, I. S. Bang,, and J. W. Foster. 1996. Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol. Microbiol. 20: 605 611.
109. Pfeifer, C. G.,, S. L. Marcus,, O. Steele-Mortimer,, L. A. Knodler,, and B. B. Finlay. 1999. Salmonella typhimurium virulence genes are induced upon bacterial invasion into phagocytic and nonphagocytic cells. Infect. Immun. 67: 5690 5698.
110. Rakin, A.,, E. Saken,, D. Harmsen,, and J. Heesemann. 1994. The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol. Microbiol. 13: 253 262.
111. Ray, N. B.,, and C. K. Mathews. 1992. Nucleoside diphosphokinase: a functional link between intermediary metabolism and nucleic acid synthesis. Curr. Top. Cell Regul. 33: 343 357.
112. Rokbi, B.,, D. Seguin,, B. Guy,, V. Mazarin,, E. Vidor,, F. Mion,, M. Cadoz,, and M. J. Quentin-Millet. 2001. Assessment of Helicobacter pylori gene expression within mouse and human gastric mucosa. Infect. Immun. 69: 4759 4766.
113. Rosqvist, R.,, A. Forsberg,, M. Rimpilainen,, T. Bergman,, and W. H. Wolf. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4: 657 667.
114. Rosqvist, R.,, A. Forsberg,, and W. H. Wolf. 1991. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect. Immun. 59: 4562 4569.
115. Ruckdeschel, K.,, A. Roggenkamp,, S. Schubert,, and J. Heesemann. 1996. Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils. Infect. Immun. 64: 724 733.
116. Saken, E.,, A. Rakin,, and J. Heesemann. 2000. Molecular characterization of a novel siderophore-independent iron transport system in Yersinia. Int. J. Med. Microbiol. 290: 51 60.
117. Salzman, N. H.,, M. M. Chou,, H. de Jong,, L. Liu,, E. M. Porter,, and Y. Paterson. 2003. Enteric Salmonella infection inhibits Paneth cell antimicrobial peptide expression. Infect. Immun. 71: 1109 1115.
118. Schuhmacher, D. A.,, and K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181: 1508 1514.
119. Schulte, R.,, S. Kerneis,, S. Klinke,, H. Bartels,, S. Preger,, J.-P. Kraehenbuhl,, E. Pringault,, and I. B. Autenrieth. 2000. Translocation of Yersina enterocolitica across reconsituted intestinal epithelial monolayers is triggered by Yersina invasin binding to β-1 integrins apically expressed on M-like cells. Cell. Microbiol. 2: 173 185.
120. Shea, J. E.,, M. Hensel,, C. Gleeson,, and D. W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93: 2593 2597.
121. Simonet, M.,, S. Richard,, and P. Berche. 1990. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect. Immun. 58: 841 845.
122. Slauch, J. M.,, and A. Camilli. 2000. IVET and RIVET: use of gene fusions to identify bacterial virulence factors specifically induced in host tissues. Methods Enzymol. 326: 73 96.
123. Slauch, J. M.,, M. J. Mahan,, and J. J. Mekalanos. 1994. In vivo expression technology for selection of bacterial genes specifically induced in host tissues. Methods Enzymol. 235: 481 492.
124. Smith, H. W.,, and J. E. Jones. 1967. Observations on experimental oral infection with Salmonella Dublin in calves and Salmonella choleraesuis in pigs. J. Pathol. Bacteriol. 93: 141 156.
125. Stanley, T. L.,, C. D. Ellermeier,, and J. M. Slauch. 2000. Tissue- specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovar Typhimurium survival in Peyer’s patches. J. Bacteriol. 182: 4406 4413.
126. Stojiljkovic, I.,, and K. Hantke. 1992. Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in gram-negative bacteria. EMBO J. 12: 4359 4367.
127. Tacket, C. O.,, R. K. Taylor,, G. Losonsky,, Y. Lim,, J. P. Nataro,, J. B. Kaper,, and M. M. Levine. 1998. Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect. Immun. 66: 692 695.
128. Talaat, A. M., Hunter, P., and S. A. Johnson. 2000. Genome-directed primers for selective labeling of bacterial transcripts for DNA microarray analysis. Nat. Biotechnol. 18: 679 682.
129. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1986. Identification of a pilus colonization factor that is coordinately regulated with cholera toxin. Ann. Sclavo Collana Monogr. 3: 51 61.
129a.. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84: 2833 2837.
130. Tischler, A. D.,, S. H. Lee,, and A. Camilli. 2002. The Vibrio cholerae vieSAB locus encodes a pathway contributing to cholera toxin production. J. Bacteriol. 184: 4104 4113.
131. Valdivia, R. H.,, and S. Falkow. 1996. Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol. Microbiol. 22: 367 378.
132. Valdivia, R. H.,, and S. Falkow. 1997. Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007 2011.
133. Waldor, M. K.,, and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910 1914.
134. Wallis, T. S.,, S. M. Paulin,, J. S. Plested,, P. R. Watson,, and P. W. Jones. 1995. The Salmonella Dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle. Infect. Immun. 63: 2755 2761.
135. Wallis, T. S.,, W. G. Starkey,, J. Stephen,, S. J. Haddon,, M. P. Osborne,, and D. C. Candy. 1986. The nature and role of mucosal damage in relation to Salmonella typhimurium-induced fluid secretion in the rabbit ileum. J. Med. Microbiol. 22: 39 49.
136. Xu, Q.,, M. Dziejman,, and J. J. Mekalanos. 2003. Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc. Natl. Acad. Sci. USA 100: 1286 1291.
137. Young, G. M.,, and V. L. Miller. 1997. Identification of novel chromosomal loci affecting Yersinia enterocolitica pathogenesis. Mol. Microbiol. 25: 319 328.


Generic image for table
Table 1

Genes induced during intestinal infection by bacterial pathogens

Citation: Butler S, Tischler A, Camilli A. 2005. Pathogen Gene Expression during Intestinal Infection, p 283-299. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch20
Generic image for table
Table 2

Genes whose spatial and temporal expression patterns in the intestine have been studied

Citation: Butler S, Tischler A, Camilli A. 2005. Pathogen Gene Expression during Intestinal Infection, p 283-299. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch20
Generic image for table
Table 3

In vivo regulators of and genes identified using RIVET

Citation: Butler S, Tischler A, Camilli A. 2005. Pathogen Gene Expression during Intestinal Infection, p 283-299. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch20

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