Chapter 26 : Negative Regulation during Bacterial Infection

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

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Negative Regulation during Bacterial Infection, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap26-1.gif /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap26-2.gif


This chapter highlights some of the many interesting cases of negative regulation at work during different stages of infection for several pathogens, focusing on the diverse molecular mechanisms involved in gene repression and the selective pressures that led to their evolution. Some pathogenic bacteria cycle through multiple hosts; for example, some pathogens use arthropod vectors to invade human populations, an extreme transition that demands a great deal of regulatory flexibility. During infection, pathogenic bacteria must contend with an in vivo environment that is under the surveillance of immune mechanisms capable of rapidly identifying and eliminating foreign microorganisms. Immune recognition presents a significant challenge to pathogenic bacteria. A central mechanism to evade host defenses is to stop producing the structures, such as flagella and pili, that are recognized by host antibodies and toll-like receptors (TLRs). During infection of a new host, flagellar breakage allows the derepression of virulence again. Negative regulation in transcriptional programs in vivo has also been found in , a gram-negative pathogen that is the cause of disease in humans and other mammalian hosts. Virulence genes are frequently encoded in clusters on the genomes of pathogens, and these clusters are termed “pathogenicity islands". The deactivation of CovR has been shown to be mediated through selection of CovS mutants in the presence of innate immune responses, but it also appears to be regulated by as-yet-unknown signals sensed by CovS.

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

The BvgAS two-component system of controls multiple genes. Under Bvg conditions, the membrane protein BvgS and cytosolic DNA-binding protein BvgA are unphosphorylated. This allows transcription of flagellar genes but not virulence factors such as adhesins and toxins. In response to certain environmental stimuli, the cell switches to a Bvgstate, which is characterized by a phosphorylated BvgS and BvgA. This activated form of BvgA represses flagellar gene expression and activates the expression of adhesins and toxins. The timely repression of flagellar genes in the Bvg state is critical for infection. doi:10.1128/9781555818524.ch26f1

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Temperature-dependent repression of flagellar synthesis in . Flagellar genes are repressed by the DNA-binding protein MogR, but under low temperatures, the anti-repressor GmaR binds to and titrates MogR away from the flagellar promoter, allowing expression of flagellar genes. As the temperature increases, a conformational change in GmaR takes place, targeting it for degradation. This allows MogR to bind flagellar promoters and repress transcription. doi:10.1128/9781555818524.ch26f2

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Flagellar breakage signals repression of to allow virulence gene expression in . At the high cell densities present in a . inoculum, virulence genes are repressed by the quorum-sensing regulator HapR. As the vibrios penetrate the mucus layer of the host small intestines, the flagella break off, allowing the basal-body-hook complex (BBH) to export the anti-sigma factor FlgM. This frees the sigma factor FliA to repress , which in turn allows virulence gene expression. doi:10.1128/9781555818524.ch26f3

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

H-NS-mediated repression of transcription of foreign DNA. The nucleoid-associated protein H-NS represses transcription of A+T-rich foreign DNA, a process known as “xenogeneic silencing.” H-NS-mediated gene repression has evolved to become a timing mechanism for the expression of virulence genes, which are commonly inherited horizontally. After acquisition of new A+T-rich DNA, such as might encode virulence genes, the H-NS protein represses transcription of this DNA. Under virulence-inducing conditions, a virulence-activating transcription factor may displace H-NS from the DNA to allow transcription. In an mutant, however, virulence genes may be active under nonvirulent conditions, which can be deleterious to the bacteria. The presence of H-NS or other repressive nucleoid-associated proteins thus ensures timely activation of virulence programs for a wide variety of bacteria. doi:10.1128/9781555818524.ch26f4

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Selection of invasive mutants in group A . In the colonizing but noninvasive state, the protease SpeB is expressed, causing degradation or truncation of numerous virulence factors. The expression of SpeB is controlled by the two-component system CovRS. In the presence of neutrophil extracellular traps, there is a selective pressure for expression of the DNase Sda1, which is normally repressed by CovRS. This pressure causes the outgrowth of mutants, which has the effect of coselecting for strains with decreased SpeB expression, leading to increased virulence factor production and an invasive phenotype. doi:10.1128/9781555818524.ch26f5

Citation: Stern A, Zhu J, Hsiac A. 2013. Negative Regulation during Bacterial Infection, p 528-544. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Akerley, B. J.,, P. A. Cotter,, and J. F. Miller. 1995. Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80:611620.
2. Akerley, B. J.,, D. M. Monack,, S. Falkow,, and J. F. Miller. 1992. The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J. Bacteriol. 174:980990.
3. Alpuche Aranda, C. M.,, J. A. Swanson,, W. P. Loomis,, and S. I. Miller. 1992. Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc. Natl. Acad. Sci. USA 89:1007910083.
4. Antonara, S.,, L. Ristow,, J. McCarthy,, and J. Coburn. 2010. Effect of Borrelia burgdorferi OspC at the site of inoculation in mouse skin. Infect. Immun. 78:47234733.
5. Apodaca, G.,, L. A. Katz,, and K. E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125:6786.
6. Arico, B.,, J. F. Miller,, C. Roy,, S. Stibitz,, D. Monack,, S. Falkow,, R. Gross,, and R. Rappuoli. 1989. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc. Natl. Acad. Sci. USA 86:66716675.
7. Arico, B.,, V. Scarlato,, D. M. Monack,, S. Falkow,, and R. Rappuoli. 1991. Structural and genetic analysis of the bvg locus in Bordetella species. Mol. Microbiol. 5:24812491.
8. Attridge, S. R.,, P. A. Manning,, J. Holmgren,, and G. Jonson. 1996. Relative significance of mannose-sensitive hemagglutinin and toxin-coregulated pili in colonization of infant mice by Vibrio cholerae El Tor. Infect. Immun. 64:33693373.
9. Bajaj, V.,, C. Hwang,, and C. A. Lee. 1995. HilA is a novel OmpR/ToxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol. Microbiol. 18:715727.
10. Bajaj, V.,, R. L. Lucas,, C. Hwang,, and C. A. Lee. 1996. Co-ordinate regulation of Salmonella Typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22:703714.
11. Barbour, A. G.,, S. L. Tessier,, and W. J. Todd. 1983. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect. Immun. 41:795804.
12. Berge, A.,, and L. Björck. 1995. Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J. Biol. Chem. 270:98629867.
13. Blanco, L. P.,, and V. J. DiRita. 2006. Antibodies enhance interaction of Vibrio cholerae with intestinal M-like cells. Infect. Immun. 74:69576964.
14. Brinkmann, V.,, U. Reichard,, C. Goosmann,, B. Fauler,, Y. Uhlemann,, D. S. Weiss,, Y. Weinrauch,, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science 303:15321535.
15. Brown, N. F.,, B. A. Vallance,, B. K. Coombes,, Y. Valdez,, B. A. Coburn,, and B. B. Finlay. 2005. Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog. 1:e32.
16. Buchanan, J. T.,, A. J. Simpson,, R. K. Aziz,, G. Y. Liu,, S. A. Kristian,, M. Kotb,, J. Feramisco,, and V. Nizet. 2006. DNase expression allows the pathogen Group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16:396400.
17. Burgdorfer, W.,, A. G. Barbour,, S. F. Hayes,, J. L. Benach,, E. Grunwaldt,, and J. P. Davis. 1982>. Lyme disease—a tick-borne spirochetosis? Science 216:13171319.
18. Burkot, T. R.,, J. Piesman,, and R. A. Wirtz. 1994. Quantitation of the Borrelia burgdorferi outer surface protein A in Ixodes scapularis: fluctuations during the tick life cycle, doubling times, and loss while feeding. J. Infect. Dis. 170:883889.
19. Burtnick, M. N.,, J. S. Downey,, P. J. Brett,, J. A. Boylan,, J. G. Frye,, T. R. Hoover,, and F. C. Gherardini. 2007. Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol Microbiol. 65:277293.
20. Bustamante, V. H.,, F. J. Santana,, E. Calva,, and J. L. Puente. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39:664678.
21. Butler, S. M.,, and A. Camilli. 2005. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat. Rev. Microbiol. 3:611620.
22. Caimano, M. J.,, R. Iyer,, C. H. Eggers,, C. Gonzalez,, E. A. Morton,, M. A. Gilbert,, I. Schwartz,, and J. D. Radolf. 2007. Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol. Microbiol. 65:11931217.
23. Castellanos, M. I.,, D. J. Harrison,, J. M. Smith,, S. K. Labahn,, K.M. Levy,, and H. J. Wing. 2009. VirB Alleviates H-NS repression of the icsP promoter in Shigella flexneri from sites more than one kilobase upstream of the transcription start site. J. Bacteriol. 191:40474050.
24. Chiavelli, D. A.,, J. W. Marsh,, and R. K. Taylor. 2001. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67:32203225.
25. Colangeli, R.,, A. Haq,, V. L. Arcus,, E. Summers,, R. S. Magliozzo,, A. McBride,, A. K. Mitra,, M. Radjainia,, A. Khajo,, W. R. Jacobs,, P. Salgame,, and D. Alland. 2009. The multifunctional histone-like protein Lsr2 protects mycobacteria against reactive oxygen intermediates. Proc. Natl. Acad. Sci. USA 106:44144418.
26. Colangeli, R.,, D. Helb,, C. Vilchèze,, M. H. Hazbón,, C.-G. Lee,, H. Safi,, B. Sayers,, I. Sardone,, M. B. Jones,, R. D. Fleischmann,, S. N. Peterson,, W. R. Jacobs,, and D. Alland. 2007. Transcriptional regulation of multi-drug tolerance and antibiotic-induced responses by the histone-like protein Lsr2 in M. tuberculosis. PLoS Pathog. 3:e87.
27. Cole, J. N.,, J. D. McArthur,, F. C. McKay,, M. L. Sanderson-Smith,, A. J. Cork,, M. Ranson,, M. Rohde,, A. Itzek,, H. Sun,, D. Ginsburg,, M. Kotb,, V. Nizet,, G. S. Chhatwal,, and M. J. Walker. 2006. Trigger for group A streptococcal M1T1 invasive disease. FASEB J. 20:17451747.
28. Coombes, B. K.,, M. E. Wickham,, M. J. Lowden,, N. F. Brown,, and B. B. Finlay. 2005. Negative regulation of Salmonella pathogenicity island 2 is required for contextual control of virulence during typhoid. Proc. Natl. Acad. Sci. USA 102:1746017465.
29. Correa, N. E.,, J. R. Barker,, and K. E. Klose. 2004. The Vibrio cholerae FlgM homologue is an anti-–28 factor that is secreted through the sheathed polar flagellum. J. Bacteriol. 186:46134619.
30. Cotter, P. A.,, and V. J. DiRita. 2000. Bacterial virulence gene regulation: an evolutionary perspective. Annu. Rev. Microbiol. 54:519565.
31. Cotter, P. A.,, and A. M. Jones. 2003. Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol. 11:367373.
32. Cummings, C. A.,, H. J. Bootsma,, D. A. Relman,, and J. F. Miller. 2006. Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J. Bacteriol. 188:17751785.
33. Cunningham, M. W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13:470511.
34. Deiwick, J.,, T. Nikolaus,, S. Erdogan,, and M. Hensel. 1999. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol. 31:17591773.
35. Deveau, H.,, J. E. Garneau,, and S. Moineau. 2011. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 64:475493.
36. Dickinson, E. C.,, J. C. Gorga,, M. Garrett,, R. Tuncer,, P. Boyle,, S. C. Watkins,, S. M. Alber,, M. Parizhskaya,, M. Trucco,, M. I. Rowe,, and H. R. Ford. 1998. Immunoglobulin A supplementation abrogates bacterial translocation and preserves the architecture of the intestinal epithelium. Surgery 124:284290.
37. DiRita, V. J.,, C. Parsot,, G. Jander,, and J. J. Mekalanos. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 88:54035407.
38. Dons, L.,, E. Eriksson,, Y. Jin,, M. E. Rottenberg,, K. Kristensson,, C.N. Larsen,, J. Bresciani,, and J. E. Olsen. 2004. Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect. Immun. 72:32373244.
39. Ellison, D. W.,, and V. L. Miller. 2006. H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J. Bacteriol. 188:51015112.
40. Faruque, S. M.,, K. M. Ahmed,, A. K. Siddique,, K. Zaman,, A. R. Alim,, and M. J. Albert. 1997. Molecular analysis of toxigenic Vibrio cholerae O139 Bengal strains isolated in Bangladesh between 1993 and 1996: evidence for emergence of a new clone of the Bengal vibrios. J. Clin. Microbiol. 35:22992306.
41. Federle, M. J.,, K. S. McIver,, and J. R. Scott. 1999. A response regulator that represses transcription of several virulence operons in the group A Streptococcus. J. Bacteriol. 181:36493657.
42. Fields, P. I.,, R. V. Swanson,, C. G. Haidaris,, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. USA 83:51895193.
43. Freter, R.,, B. Allweiss,, P. C. O’Brien,, S. A. Halstead,, and M. S. Macsai. 1981a. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vitro studies. Infect. Immun. 34:241249.
44. Freter, R.,, P. C. O’Brien,, and M. S. Macsai. 1981b. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234240.
45. Fuchs, R.,, S. Jauris,, F. Lottspeich,, V. Preac-Mursic,, B. Wilske,, and E. Soutschek. 1992. Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22 kDa protein (pC) in Escherichia coli. Mol. Microbiol. 6:503509.
46. Galan, J. E.,, and R. Curtiss. 1989. Cloning and molecular characterization of genes whose products allow Salmonella Typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86:63836387.
47. Gardel, C.,, and J. Mekalanos. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect. Immun. 64:22462255.
48. Ghosh, A.,, K. Paul,, and R. Chowdhury. 2006. Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect. Immun. 74:30603064.
49. Goldberg, M. D.,, M. Johnson,, J. C. D. Hinton,, and P. H. Williams. 2001. Role of the nucleoid-associated protein Fis in the regulation of virulence properties of enteropathogenic Escherichia coli. Mol. Microbiol. 41:549559.
50. Gordon, B. R. G.,, R. Imperial,, L. Wang,, W. W. Navarre,, and J. Liu. 2008. Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. J. Bacteriol. 190:70527059.
51. Gordon, B. R. G.,, Y. Li,, L. Wang,, A. Sintsova,, H. van Bakel,, S. Tian,, W. W. Navarre,, B. Xia,, and J. Liu. 2010. Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 107:51545159.
52. Gründling, A.,, L. S. Burrack,, H. G. A. Bouwer,, and D. E. Higgins. 2004. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc. Natl. Acad. Sci. USA 101:1231812323.
53. Hansen-Wester, I.,, and M. Hensel. 2001. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3:549559.
54. Haraga, A.,, M. B. Ohlson,, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:5366.
55. Hardt, W. D.,, L. M. Chen,, K. E. Schuebel,, X. R. Bustelo,, and J. E. Galan. 1998. Salmonella Typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815826.
56. Häse, C. C. 2001. Analysis of the role of flagellar activity in virulence gene expression in Vibrio cholerae. Microbiology 147:831837.
57. Häse, C. C.,, and J. J. Mekalanos. 1999. Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 96:31833187.
58. Heath, A.,, V. J. DiRita,, N. L. Barg,, and N. C. Engleberg. 1999. A two-component regulatory system, CsrR-CsrS, represses expression of three Streptococcus pyogenes virulence factors, hyaluronic acid capsule, streptolysin S, and pyrogenic exotoxin B. Infect. Immun. 67:52985305.
59. 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 269:400403.
60. 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. 30:163174.
61. Hollands, A.,, M. A. Pence,, A. M. Timmer,, S. R. Osvath,, L. Turnbull,, C. B. Whitchurch,, M. J. Walker,, and V. Nizet. 2010. Genetic switch to hypervirulence reduces colonization phenotypes of the globally disseminated Group A Streptococcus M1T1 clone. J.Infect. Dis. 202:1119.
62. Honko, A. N.,, and S. B. Mizel. 2005. Effects of flagellin on innate and adaptive immunity. Immunol. Res. 33:83101.
63. Hsiao, A.,, Z. Liu,, A. Joelsson,, and J. Zhu. 2006. Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc. Natl. Acad. Sci. USA 103:1454214547.
64. Hsiao, A.,, K. Toscano,, and J. Zhu. 2008. Post-transcriptional cross-talk between pro- and anti-colonization pili biosynthesis systems in Vibrio cholerae. Mol. Microbiol. 67:849860.
65. Hsiao, A.,, X. Xu,, B. Kan,, R. V. Kulkarni,, and J. Zhu. 2009. Direct regulation by the Vibrio cholerae regulator ToxT to modulate colonization and anticolonization pilus expression. Infect. Immun. 77:13831388.
66. Hübner, A.,, X. Yang,, D. M. Nolen,, T. G. Popova,, F. C. Cabello,, and M. V. Norgard. 2001. Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc. Natl. Acad. Sci. USA 98:1272412729.
67. Hyde, J. A.,, D. K. Shaw,, R. Smith III,, J. P. Trzeciakowski,, and J. T. Skare. 2009. The BosR regulatory protein of Borrelia burgdorferi interfaces with the RpoS regulatory pathway and modulates both the oxidative stress response and pathogenic properties of the Lyme disease spirochete. Mol. Microbiol. 74:13441355.
68. Hyde, J. A.,, D. K. Shaw,, R. Smith,, J. P. Trzeciakowski,, and J. T. Skare. 2010. Characterization of a conditional bosR mutant in Borrelia burgdorferi. Infect. Immun. 78:265274.
69. Jacob-Dubuisson, F.,, B. Kehoe,, E. Willery,, N. Reveneau,, C. Locht,, and D. A. Relman. 2000. Molecular characterization of Bordetella bronchiseptica filamentous haemagglutinin and its secretion machinery. Microbiology 146:12111221.
70. Jiang, S.-M.,, M. J. Cieslewicz,, D. L. Kasper,, and M. R. Wessels. 2005. Regulation of virulence by a two-component system in group B Streptococcus. J. Bacteriol. 187:11051113.
71. Johns, R. H.,, D. E. Sonenshine,, and W. L. Hynes. 2000. Enhancement of OspC expression by Borrelia burgdorferi in the presence of tick hemolymph. FEMS Microbiol. Lett. 193:137141.
72. Jones, B. D.,, N. Ghori,, and S. Falkow. 1994. Salmonella Typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J. Exp. Med. 180:1523.
73. Juhas, M.,, J. R. Van Der Meer,, M. Gaillard,, R. M. Harding,, D. W. Hood,, and D. W. Crook. 2009. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol. Rev. 33:376393.
74. Kamp, H. D.,, and D. E. Higgins. 2011. A protein thermometer controls temperature-dependent transcription of flagellar motility genes in Listeria monocytogenes. PLoS Pathog. 7:e1002153.
75. Kamp, H. D.,, and D. E. Higgins. 2009. Transcriptional and post-transcriptional regulation of the GmaR antirepressor governs temperature-dependent control of flagellar motility in Listeria monocytogenes. Mol. Microbiol. 74:421435.
76. Kansal, R. G.,, V. Nizet,, A. Jeng,, W. J. Chuang,, and M. Kotb. 2003. Selective modulation of superantigen-induced responses by streptococcal cysteine protease. J. Infect. Dis. 187:398407.
77. Kansal, R. G.,, A. McGeer,, D. E. Low,, A. Norrby-Teglund,, and M. Kotb. 2000. Inverse relation between disease severity and expression of the streptococcal cysteine protease, SpeB, among clonal M1T1 isolates recovered from invasive group A streptococcal infection cases. Infect. Immun. 68:63626369.
78. Kapur, V.,, J. T. Maffei,, R. S. Greer,, L.-L. Li,, G. J. Adams,, and J. M. Musser. 1994. Vaccination with streptococcal extracellular cysteine protease (interleukin-1– convertase) protects mice against challenge with heterologous group A streptococci. Microb. Pathog. 16:443450.
79. Kaufman, M. R.,, J. M. Seyer,, and R. K. Taylor. 1991. Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by gram-negative bacteria. Genes. Dev. 5:18341846.
80. Kovacikova, G.,, and K. Skorupski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:11351147.
81. Lamy, M.-C.,, M. Zouine,, J. Fert,, M. Vergassola,, E. Couve,, E. Pellegrini,, P. Glaser,, F. Kunst,, T. Msadek,, P. Trieu-Cuot,, and C. Poyart. 2004. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence. Mol Microbiol. 54:12501268.
82. Lane, R. S.,, J. Piesman,, and W. Burgdorfer. 1991. Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36:587609.
83. LaPointe, C. F.,, and R. K. Taylor. 2000. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J. Biol. Chem. 275:15021510.
84. Leclerc, H.,, L. Schwartzbrod,, and E. Dei-Cas. 2002. Microbial agents associated with waterborne diseases. Crit. Rev. Microbiol. 28:371409.
85. Lembo, A.,, M. A. Gurney,, K. Burnside,, A. Banerjee,, M. De Los Reyes,, J. E. Connelly,, W.-J. Lin,, K. A. Jewell,, A. Vo,, C. W. Renken,, K. S. Doran,, and L. Rajagopal. 2010. Regulation of CovR expression in Group B Streptococcus impacts blood–brain barrier penetration. Mol. Microbiol. 77:431443.
86. Leulier, F.,, and B. Lemaitre. 2008. Toll-like receptors—taking an evolutionary approach. Nat. Rev. Genet. 9:165178.
87. Liang, F. T.,, J. Yan,, M. L. Mbow,, S. L. Sviat,, R. D. Gilmore,, M. Mamula,, and E. Fikrig. 2004. Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect. Immun. 72:57595767.
88. Liang, F. T.,, M. B. Jacobs,, L. C. Bowers,, and M. T. Philipp. 2002. An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J. Exp. Med. 195:415422.
89. Lin, W.-J.,, D. Walthers,, J. E. Connelly,, K. Burnside,, K. A. Jewell,, L.J. Kenney,, and L. Rajagopal. 2009. Threonine phosphorylation prevents promoter DNA binding of the Group B Streptococcus response regulator CovR. Mol. Microbiol. 71:14771495.
90. Liu, Z.,, T. Miyashiro,, A. Tsou,, A. Hsiao,, M. Goulian,, and J. Zhu. 2008. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc. Natl. Acad. Sci. USA 105:97699774.
91. Locht, C.,, R. Antoine,, and F. Jacob-Dubuisson. 2001. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4:8289.
92. Lopez-Boado, Y. S.,, L. M. Cobb,, and R. Deora. 2005. Bordetella bronchiseptica flagellin is a proinflammatory determinant for airway epithelial cells. Infect. Immun. 73:75257534.
93. Lucas, R. L.,, and C. A. Lee. 2000. Unravelling the mysteries of virulence gene regulation in Salmonella Typhimurium. Mol. Microbiol. 36:10241033.
94. Lucchini, S.,, G. Rowley,, M. D. Goldberg,, D. Hurd,, M. Harrison,, and J. C. D. Hinton. 2006. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2:e81.
95. Macpherson, A. J.,, L. Hunziker,, K. McCoy,, and A. Lamarre. 2001. IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect. 3:10211035.
96. Martínez, L. C.,, H. Yakhnin,, M. I. Camacho,, D. Georgellis,, P. Babitzke,, J. L. Puente,, and V. H. Bustamante. 2011. Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol. Microbiol. 80:16371656.
97. McKay, F. C.,, J. D. McArthur,, M. L. Sanderson-Smith,, S. Gardam,, B. J. Currie,, K. S. Sriprakash,, P. K. Fagan,, R. J. Towers,, M. R. Batzloff,, G. S. Chhatwal,, M. Ranson,, and M. J. Walker. 2004. Plasminogen binding by group A streptococcal isolates from a region of hyperendemicity for streptococcal skin infection and a high incidence of invasive infection. Infect. Immun. 72:364370.
98. Meibom, K. L.,, X. B. Li,, A. T. Nielsen,, C. Y. Wu,, S. Roseman,, and G. K. Schoolnik. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101:25242529.
99. Miller, J. F.,, C. R. Roy,, and S. Falkow. 1989a. Analysis of Bordetella pertussis virulence gene regulation by use of transcriptional fusions in Escherichia coli. J. Bacteriol. 171:63456348.
100. Miller, M. B.,, K. Skorupski,, D. H. Lenz,, R. K. Taylor,, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303314.
101. Miller, S. I.,, A. M. Kukral,, and J. J. Mekalanos. 1989b. A two-component regulatory system (phoP phoQ) controls Salmonella Typhimurium virulence. Proc. Natl. Acad. Sci. USA 86:50545058.
102. Moorthy, S.,, and P. I. Watnick. 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol. Microbiol. 52:573587.
103. Moorthy, S.,, and P. I. Watnick. 2005. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol. Microbiol. 57:16231635.
104. Navarre, W. W.,, S. Porwollik,, Y. Wang,, M. McClelland,, H. Rosen,, S. J. Libby,, and F. C. Fang. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236238.
105. Nielsen, A. T.,, N. A. Dolganov,, G. Otto,, M. C. Miller,, C. Y. Wu,, and G. K. Schoolnik. 2006. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog. 2:e109.
106. Nye, M. B.,, J. D. Pfau,, K. Skorupski,, and R. K. Taylor. 2000. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J. Bacteriol. 182:42954303.
107. Olekhnovich, I. N.,, and R. J. Kadner. 2006. Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J. Mol. Biol. 357:373386.
108. Olekhnovich, I. N.,, and R. J. Kadner. 2007. Role of nucleoid-associated proteins Hha and H-NS in expression of Salmonella enterica activators HilD, HilC, and RtsA required for cell invasion. J. Bacteriol. 189:68826890.
109. Ouyang, Z.,, R. K. Deka,, and M. V. Norgard. 2011. BosR (BB0647) controls the RpoN-RpoS regulatory pathway and virulence expression in Borrelia burgdorferi by a vovel DNA-binding mechanism. PLoS Pathog. 7:e1001272.
110. Ouyang, Z.,, M. Kumar,, T. Kariu,, S. Haq,, M. Goldberg,, U. Pal,, and M. V. Norgard. 2009. BosR (BB0647) governs virulence expression in Borrelia burgdorferi. Mol. Microbiol. 74:13311343.
111. Pal, U.,, X. Li,, T. Wang,, R. R. Montgomery,, N. Ramamoorthi,, A. M. Desilva,, F. Bao,, X. Yang,, M. Pypaert,, D. Pradhan,, F. S. Kantor,, S. Telford,, J. F. Anderson,, and E. Fikrig. 2004a. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119:457468.
112. Pal, U.,, X. Yang,, M. Chen,, L. K. Bockenstedt,, J. F. Anderson,, R.A. Flavell,, M. V. Norgard,, and E. Fikrig. 2004b. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Investig. 113:220230.
113. Parkhill, J.,, M. Sebaihia,, A. Preston,, L. D. Murphy,, N. Thomson,, D. E. Harris,, M. T. Holden,, C. M. Churcher,, S. D. Bentley,, K.L. Mungall,, A. M. Cerdeno-Tarraga,, L. Temple,, K. James,, B. Harris,, M. A. Quail,, M. Achtman,, R. Atkin,, S. Baker,, D. Basham,, N. Bason,, I. Cherevach,, T. Chillingworth,, M. Collins,, A. Cronin,, P. Davis,, J. Doggett,, T. Feltwell,, A. Goble,, N. Hamlin,, H. Hauser,, S. Holroyd,, K. Jagels,, S. Leather,, S. Moule,, H. Norberczak,, S. O’Neil,, D. Ormond,, C. Price,, E. Rabbinowitsch,, S. Rutter,, M. Sanders,, D. Saunders,, K. Seeger,, S. Sharp,, M. Simmonds,, J. Skelton,, R. Squares,, S. Squares,, K. Stevens,, L. Unwin,, S. Whitehead,, B. G. Barrell,, and D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis, and Bordetella bronchiseptica. Nat. Genet. 35:3240.
114. Peel, M.,, W. Donachie,, and A. Shaw. 1988. Temperature-dependent expression of flagella of Listeria monocytogenes studied by electron microscopy, SDS-PAGE and Western blotting. J. Gen. Microbiol. 134:21712178.
115. Pegues, D. A.,, M. J. Hantman,, I. Behlau,, and S. I. Miller. 1995. PhoP/PhoQ transcriptional repression of Salmonella Typhimurium invasion genes: evidence for a role in protein secretion. Mol. Microbiol. 17:169181.
116. Perez, J. C.,, T. Latifi,, and E. A. Groisman. 2008. Overcoming H-NS-mediated transcriptional silencing of horizontally acquired genes by the PhoP and SlyA Proteins in Salmonella enterica. J. Biol. Chem. 283:1077310783.
117. Phalipon, A.,, and B. Corthesy. 2003. Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends Immunol. 24:5558.
118. Porter, M. E.,, and C. J. Dorman. 1994. A role for H-NS in the thermo-osmotic regulation of virulence gene expression in Shigella flexneri. J. Bacteriol. 176:41874191.
119. Prost, L. R.,, and S. I. Miller. 2008. The Salmonella PhoQ sensor: mechanisms of detection of phagosome signals. Cell. Microbiol. 10:576582.
120. Raeder, R.,, and M. D. Boyle. 1996. Properties of IgG-binding proteins expressed by Streptococcus pyogenes isolates are predictive of invasive potential. J. Infect. Dis. 173:888895.
121. Raeder, R.,, M. Woischnik,, A. Podbielski,, and M. D. Boyle. 1998. A secreted streptococcal cysteine protease can cleave a surface-expressed M1 protein and alter the immunoglobulin binding properties. Res. Microbiol. 149:539548.
122. Revel, A. T.,, A. M. Talaat,, and M. V. Norgard. 2002. DNA microarray analysis of differential gene expression in Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA 99:15621567.
123. Rezcallah, M. S.,, M. D. P. Boyle,, and D. D. Sledjeski. 2004. Mouse skin passage of Streptococcus pyogenes results in increased streptokinase expression and activity. Microbiology 150:365371.
124. Richter-Dahlfors, A.,, A. M. Buchan,, and B. B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella Typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569580.
125. Roehrig, J. T.,, J. Piesman,, A. R. Hunt,, M. G. Keen,, C. M. Happ,, and B. J. Johnson. 1992. The hamster immune response to tick-transmitted Borrelia burgdorferi differs from the response to needle-inoculated, cultured organisms. J. Immunol. 149:36483653.
126. Roy, C. R.,, and S. Falkow. 1991. Identification of Bordetella pertussis regulatory sequences required for transcriptional activation of the fhaB gene and autoregulation of the bvgAS operon. J.Bacteriol. 173:23852392.
127. Roy, C. R.,, J. F. Miller,, and S. Falkow. 1990. Autogenous regulation of the Bordetella pertussis bvgABC operon. Proc. Natl. Acad. Sci. USA 87:37633767.
128. Roy, C. R.,, J. F. Miller,, and S. Falkow. 1989. The bvgA gene of Bordetella pertussis encodes a transcriptional activator required for coordinate regulation of several virulence genes. J. Bacteriol. 171:63386344.
129. Royle, L.,, A. Roos,, D. J. Harvey,, M. R. Wormald,, D. van Gijlswijk-Janssen,, el-R. M. Redwan,, I. A. Wilson,, M. R. Daha,, R. A. Dwek,, and P. M. Rudd. 2003. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 278:2014020153.
130. Scarlato, V.,, A. Prugnola,, B. Arico,, and R. Rappuoli. 1991. The bvg-dependent promoters show similar behaviour in different Bordetella species and share sequence homologies. Mol. Microbiol. 5:24932498.
131. Schwan, T. G. 2003. Temporal regulation of outer surface proteins of the Lyme-disease spirochaete Borrelia burgdorferi. Biochem. Soc. Trans. 31:108112.
132. Schwan, T. G.,, J. Piesman,, W. T. Golde,, M. C. Dolan,, and P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. USA 92:29092913.
133. Schwan, T. G.,, and J. Piesman. 2000. Temporal changes in outer surface proteins A and C of the Lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J. Clin. Microbiol. 38:382388.
134. Seemanapalli, S. V.,, Q. Xu,, K. McShan,, and F. T. Liang. 2011. Outer surface protein C is a dissemination-facilitating factor of Borrelia burgdorferi during mammalian infection. PLoS ONE 5:e15830.
135. 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 93:25932597.
136. Shen, A.,, and D. E. Higgins. 2006. The MogR transcriptional repressor regulates nonhierarchal expression of flagellar motility genes and virulence in Listeria monocytogenes. PLoS Pathog. 2:e30.
137. Shen, A.,, H. D. Kamp,, A. Gründling,, and D. E. Higgins. 2006. A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev. 20:32833295.
138. Steere, A. C.,, V. K. Sikand,, F. Meurice,, D. L. Parenti,, E. Fikrig,, R. T. Schoen,, J. Nowakowski,, C. H. Schmid,, S. Laukamp,, C. Buscarino,, and D. S. Krause. 1998. Vaccination against Lyme disease with recombinant Borrelia burgdorferi outer-surface lipoprotein A with adjuvant. N. Engl. J. Med. 339:209215.
139. Stonehouse, E. A.,, R. R. Hulbert,, M. B. Nye,, K. Skorupski,, and R.K. Taylor. 2011. H-NS binding and repression of the ctx promoter in Vibrio cholerae. J. Bacteriol. 193:979988.
140. Stonehouse, E.,, G. Kovacikova,, R. K. Taylor,, and K. Skorupski. 2008. Integration host factor positively regulates virulence gene expression in Vibrio cholerae. J. Bacteriol. 190:47364748.
141. Sumby, P.,, A. R. Whitney,, E. A. Graviss,, F. R. DeLeo,, and J. M. Musser. 2006. Genome-wide analysis of Group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2:e5.
142. Svennerholm, A. M.,, G. Johnson,, and C. Yan. 1991. A method for studies of an El Tor-associated antigen of Vibrio cholerae O1. FEMS Microbiol. Lett. 63:179185.
143. Tendeng, C.,, C. Badaut,, E. Krin,, P. Gounon,, S. Ngo,, A. Danchin,, S. Rimsky,, and P. Bertin. 2000. Isolation and characterization of vicH, encoding a new pleiotropic regulator in Vibrio cholerae. J.Bacteriol. 182:20262032.
144. Thelin, K. H.,, and R. K. Taylor. 1996. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64:28532856.
145. Tilly, K.,, S. Casjens,, B. Stevenson,, J. L. Bono,, D. S. Samuels,, D. Hogan,, and P. Rosa. 1997. The Borrelia burgdorferi circular plasmid cp26: conservation of plasmid structure and targeted inactivation of the ospC gene. Mol. Microbiol. 25:361373.
146. Torres, A. G.,, G. N. Lopez-Sanchez,, L. Milflores-Flores,, S. D. Patel,, M. Rojas-Lopez,, C. F. Martinez dela Pena,, M. M. P. Arenas-Hernandez,, and Y. Martinez-Laguna. 2007. Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157:H7. J. Bacteriol. 189:59165928.
147. Turner, E. C.,, and C. J. Dorman. 2007. H-NS antagonism in Shigella flexneri by VirB, a virulence gene transcription regulator that is closely related to plasmid partition factors. J. Bacteriol. 189:34033413.
148. Uchiya, K.,, M. A. Barbieri,, K. Funato,, A. H. Shah,, P. D. Stahl,, and E. A. Groisman. 1999. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18:39243933.
149. Vazquez-Torres, A.,, J. Jones-Carson,, A. J. Baumler,, S. Falkow,, R. Valdivia,, W. Brown,, M. Le,, R. Berggren,, W. T. Parks,, and F.C. Fang. 1999. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401:804808.
150. Virgin, H. W. 2007. In vivo veritas: pathogenesis of infection as it actually happens. Nat. Immunol. 8:11431147.
151. von Pawel-Rammingen, U.,, and L. Bjorck. 2003. IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes. Curr. Opin. Microbiol. 6:5055.
152. Walker, M. J.,, A. Hollands,, M. L. Sanderson-Smith,, J. N. Cole,, J.K. Kirk,, A. Henningham,, J. D. McArthur,, K. Dinkla,, R. K. Aziz,, R.G. Kansal,, A. J. Simpson,, J. T. Buchanan,, G. S. Chhatwal,, M. Kotb,, and V. Nizet. 2007. DNase Sda1 provides selection pressure for a switch to invasive Group A streptococcal infection. Nat. Med. 13:981985.
153. Walthers, D.,, R. K. Carroll,, W. W. Navarre,, S. J. Libby,, F. C. Fang,, and L. J. Kenney. 2007. The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol. Microbiol. 65:477493.
154. Walthers, D.,, Y. Li,, Y. Liu,, G. Anand,, J. Yan,, and L. J. Kenney. 2011. Salmonella enterica response regulator SsrB relieves H-NS silencing by displacing H-NS bound in polymerization mode and directly activates transcription. J. Biol. Chem. 286:18951902.
155. Watnick, P. I.,, K. J. Fullner,, and R. Kolter. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:36063609.
156. Way, S. S.,, L. J. Thompson,, J. E. Lopes,, A. M. Hajjar,, T. R. Kollmann,, N. E. Freitag,, and C. B. Wilson. 2004. Characterization of flagellin expression and its role in Listeria monocytogenes infection and immunity. Cell. Microbiol. 6:235242.
157. Weiss, A. A.,, and E. L. Hewlett. 1986. Virulence factors of Bordetella pertussis. Annu. Rev. Microbiol. 40:661686.
158. Whitnack, E.,, and E. H. Beachey. 1982. Antiopsonic activity of fibrinogen bound to M protein on the surface of Group A streptococci. J. Clin. Investig. 69:10421045.
159. Wood, M. W.,, M. A. Jones,, P. R. Watson,, S. Hedges,, T. S. Wallis,, and E. E. Galyov. 1998. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol. Microbiol. 29:883891.
160. Xu, H.,, M. J. Caimano,, T. Lin,, M. He,, J. D. Radolf,, S. J. Norris,, F. Gheradini,, A. J. Wolfe,, and X. F. Yang. 2010. Role of acetyl-phosphate in activation of the Rrp2-RpoN-RpoS pathway in Borrelia burgdorferi. PLoS Pathog. 6:e1001104.
161. Yang, X. F.,, U. Pal,, S. M. Alani,, E. Fikrig,, and M. V. Norgard. 2004. Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J. Exp. Med. 199:641648.
162. Yang, X. F.,, S. M. Alani,, and M. V. Norgard. 2003. The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 100:1100111006.
163. Yang, X. F.,, M. C. Lybecker,, U. Pal,, S. M. Alani,, J. Blevins,, A. T. Revel,, D. S. Samuels,, and M. V. Norgard. 2005. Analysis of the ospC regulatory element controlled by the RpoN-RpoS regulatory pathway in Borrelia burgdorferi. J. Bacteriol. 187:48224829.
164. Yuk, M. H.,, P. A. Cotter,, and J. F. Miller. 1996. Genetic regulation of airway colonization by Bordetella species. Am. J. Respir. Crit. Care Med. 154:S150154.
165. Zhou, D.,, M. S. Mooseker,, and J. E. Galan. 1999. Role of the Salmonella Typhimurium actin-binding protein SipA in bacterial internalization. Science 283:20922095.
166. Zhu, J.,, and J. J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5:647656.
167. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler,, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:31293134.

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