1887

Chapter 20 : The SsrAB Virulon of

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
Zoomout

The SsrAB Virulon of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap20-1.gif /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap20-2.gif

Abstract:

This chapter focuses on the function of the regulatory system SsrAB of , which controls expression of virulence factors for the intracellular phase of the life of the pathogen. It discusses the experimental data and current understanding of the function of the two-component system SsrAB. SsrAB is encoded by genes in pathogenicity islands 2 (SPI2) and is necessary to control expression of virulence genes during the intracellular stage of infection. Intracellular survival and replication is dependent on the function of the SPI2-encoded T3SS (SPI2-T3SS). The signature-tagged mutagenesis screen initially identified various transposon-insertion mutants with highly reduced virulence in the murine model of systemic infection. A comparative analysis of expression levels under in vitro conditions indicated high diversity in expression levels of the various genes encoding structural components and effector proteins of the SPI2-T3SS. In contrast to the case with SsrA, several experimental approaches have been made towards understanding the function of SsrB, the response regulator of the SsrAB two-component system. The ancestral OmpR/EnvZ two-component system regulates the porin genes and in response to changes in osmolarity. The SPI1-encoded HilD regulatory protein, which activates the expression of SPI1 genes, has been suggested to control the switch from SPI1 to SPI2 induction. The levels of regulation range from the SPI2-encoded regulatory system SsrAB and core genome-encoded regulators to global control elements such as DNA topology regulators.

Citation: Billig S, Felipe-López A, Hensel M. 2013. The SsrAB Virulon of , p 386-401. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch20
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

The SsrAB virulon in . (A) Intracellular salmonellae reside within the SCV, a membrane-bound compartment considered growth restricting due to nutritional limitations. By means of the SPI2-T3SS, intracellular salmonellae modify host cell functions, resulting in intracellular proliferation. (B) Unknown signals present in the SCV act on the SsrA sensor and, in turn, result in activation of the SsrAB virulon. (C) SsrB activates the transcription of several operons within SPI2 encoding the SPI2-T3SS, cognate effector proteins, and the SsrAB regulatory system, various loci outside of SPI2 encoding effector proteins of the SPI2-T3SS, and further loci with unknown contribution to the intracellular lifestyle. doi:10.1128/9781555818524.ch20f1

Citation: Billig S, Felipe-López A, Hensel M. 2013. The SsrAB Virulon of , p 386-401. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch20
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Models for the domain organization of SsrA and SsrB. The predicted domain organization of SsrA (A) and SsrB (B) and positions of domains and functional residues are depicted. (C) Model for the topology of SsrA and SsrB. Red circle, unknown signal received by SsrA; green circle with P, phosphate group. CM, cytoplasmic membrane. doi:10.1128/9781555818524.ch20f2

Citation: Billig S, Felipe-López A, Hensel M. 2013. The SsrAB Virulon of , p 386-401. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch20
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Binding specificity of SsrB and regulation of expression. (A) The palindromic consensus motif of promoters of the SsrAB virulon as identified by one-hybrid screens and ChIP-on-chip experiments (modified from ). (B) The gene arrangement of in SPI2 is depicted. The yellow box (A1) indicates the binding site location of OmpR (low affinity) and OmpR-P (high affinity) upstream of the transcriptional start site of . The light blue boxes (A2 to A5) indicate additional OmpR-P binding sites. Boxes B1 to B3 indicate the OmpR-P binding sites in the region. Overlapping binding sites for the C-terminal domain of SsrB are shown as red boxes ( ). The transcriptional start sites of and are indicated by arrows and labeled +1, while the translational start sites are denoted by green arrows for and . The labels +164 and +150 indicate the presence of 164- and 150-nucleotide UTR in the and transcripts, respectively ( ). doi:10.1128/9781555818524.ch20f3

Citation: Billig S, Felipe-López A, Hensel M. 2013. The SsrAB Virulon of , p 386-401. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch20
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Model for regulatory circuits of the SsrAB virulon (modified from ). The two-component systems (green boxes) SsrAB, EnvZ/OmpR, and PhoPQ are involved in SPI2 regulation. OmpR activates SPI2 genes by binding to the promoter and inducing the expression of and . PhoP directly binds the promoter and thereby indirectly induces transcription. SsrB binds to all SPI2 promoters, including and its own promoter, for which it is required for antagonizing the repression activity of H-NS. Transcription factors (red boxes) further affect the SsrAB regulon, with SlyA affecting expression and EIIA directly interacting with SsrB at the posttranscriptional level, thereby preventing SsrB-induced gene expression. The expression of is controlled by PhoP. The SPI1-encoded HilD transcription factor is also involved (under certain conditions) in antagonizing H-NS activity. The NAPs (orange boxes) H-NS, Hha, and YdgT function as general negative SPI2 regulators, while Fis and IHF are NAPs that have a positive effect on SPI2 as well as SPI1 gene expression ( ). doi:10.1128/9781555818524.ch20f4

Citation: Billig S, Felipe-López A, Hensel M. 2013. The SsrAB Virulon of , p 386-401. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch20
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818524.chap20
1. Bader, M. W.,, S. Sanowar,, M. E. Daley,, A. R. Schneider,, U. Cho,, W. Xu,, R. E. Klevit,, H. Le Moual,, and S. I. Miller. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461472.
2. 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.
3. Beier, D.,, B. Schwarz,, T. M. Fuchs,, and R. Gross. 1995. In vivo characterization of the unorthodox BvgS two-component sensor protein of Bordetella pertussis. J. Mol. Biol. 248:596610.
4. Beuzon, C. R.,, G. Banks,, J. Deiwick,, M. Hensel,, and D. W. Holden. 1999. pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol. Microbiol. 33:806816.
5. Beuzon, C. R.,, S. Meresse,, K. E. Unsworth,, J. Ruiz-Albert,, S. Garvis,, S. R. Waterman,, T. A. Ryder,, E. Boucrot,, and D. W. Holden. 2000. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19:32353249.
6. Bogdan, C.,, M. Rollinghoff,, and A. Diefenbach. 2000. The role of nitric oxide in innate immunity. Immunol. Rev. 173:1726.
7. Boucrot, E.,, T. Henry,, J. P. Borg,, J. P. Gorvel,, and S. Meresse. 2005. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308:11741178.
8. 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.
9. Bustamante, V. H.,, L. C. Martinez,, F. J. Santana,, L. A. Knodler,, O. Steele-Mortimer,, and J. L. Puente. 2008. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc. Natl. Acad. Sci. USA 105:1459114596.
10. Cameron, A. D.,, D. M. Stoebel,, and C. J. Dorman. 2011. DNA supercoiling is differentially regulated by environmental factors and FIS in Escherichia coli and Salmonella enterica. Mol. Microbiol. 80:85101.
11. Carroll, R. K.,, X. Liao,, L. K. Morgan,, E. M. Cicirelli,, Y. Li,, W. Sheng,, X. Feng,, and L. J. Kenney. 2009. Structural and functional analysis of the C-terminal DNA binding domain of the Salmonella typhimurium SPI-2 response regulator SsrB. J. Biol. Chem. 284:1200812019.
12. Chakravortty, D.,, I. Hansen-Wester,, and M. Hensel. 2002. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J. Exp. Med. 195:11551166.
13. Chakravortty, D.,, and M. Hensel. 2003. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect. 5:621627.
14. Choi, J.,, D. Shin,, H. Yoon,, J. Kim,, C. R. Lee,, M. Kim,, Y. J. Seok,, and S. Ryu. 2010. Salmonella pathogenicity island 2 expression negatively controlled by EIIANtr-SsrB interaction is required for Salmonella virulence. Proc. Natl. Acad. Sci. USA 107:2050620511.
15. 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. 30:175188.
16. Coombes, B. K.,, N. F. Brown,, Y. Valdez,, J. H. Brumell,, and B. B. Finlay. 2004. Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J. Biol. Chem. 26:4980449815.
17. Coombes, B. K.,, M. E. Wickham,, N. F. Brown,, S. Lemire,, L. Bossi,, W. W. Hsiao,, F. S. Brinkman,, and B. B. Finlay. 2005. Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J. Mol. Biol. 348:817830.
18. Deiwick, J.,, and M. Hensel. 1999. Regulation of virulence genes by environmental signals in Salmonella typhimurium. Electro-phoresis 20:813817.
19. Deiwick, J.,, T. Nikolaus,, S. Erdogan,, and M. Hensel. 1999. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol. 31:17591773.
20. Ellermeier, J. R.,, and J. M. Slauch. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10:2429.
21. Fass, E.,, and E. A. Groisman. 2009. Control of Salmonella pathogenicity island-2 gene expression. Curr. Opin. Microbiol. 12:199204.
22. Feng, X.,, R. Oropeza,, and L. J. Kenney. 2003. Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol. Microbiol. 48:11311143.
23. Feng, X.,, D. Walthers,, R. Oropeza,, and L. J. Kenney. 2004. The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol. Microbiol. 54:823835.
24. Freeman, J. A.,, C. Rappl,, V. Kuhle,, M. Hensel,, and S. I. Miller. 2002. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J. Bacteriol. 184:49714980.
25. Garmendia, J.,, C. R. Beuzon,, J. Ruiz-Albert,, and D. W. Holden. 2003. The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. Microbiology 149:23852396.
26. Gerlach, R. G.,, and M. Hensel. 2007. Salmonella pathogenicity islands in host specificity, host pathogen-interactions and antibiotics resistance of Salmonella enterica. Berl. Munch. Tierarztl. Wochenschr. 120:317327.
27. Gerlach, R. G.,, D. Jäckel,, N. Geymeier,, and M. Hensel. 2007. Salmonella pathogenicity island 4-mediated adhesion is coregulated with invasion genes in Salmonella enterica. Infect. Immun. 75:46974709.
28. Gordon, M. A. 2008. Salmonella infections in immunocompromised adults. J. Infect. 56:413422.
29. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:18351842.
30. Haraga, A.,, M. B. Ohlson,, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:5366.
31. Henry, T.,, C. Couillault,, P. Rockenfeller,, E. Boucrot,, A. Dumont,, N. Schroeder,, A. Hermant,, L. A. Knodler,, P. Lecine,, O. Steele-Mortimer,, J. P. Borg,, J. P. Gorvel,, and S. Meresse. 2006. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc. Natl. Acad. Sci. USA 103:1349713502.
32. Hensel, M.,, A. P. Hinsley,, T. Nikolaus,, G. Sawers,, and B. C. Berks. 1999. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol. Microbiol. 32:275288.
33. 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.
34. Hensel, M.,, J. E. Shea,, S. R. Waterman,, R. Mundy,, T. Nikolaus,, G. Banks,, A. Vazquez-Torres,, C. Gleeson,, F. 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.
35. Ibarra, J. A.,, and O. Steele-Mortimer. 2009. Salmonella—the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 11:15791586.
36. Jantsch, J.,, D. Chikkaballi,, and M. Hensel. 2011. Cellular aspects of immunity to intracellular Salmonella enterica. Immunol. Rev. 240:185195.
37. Keane, O. M.,, and C. J. Dorman. 2003. The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis. Mol. Genet. Genomics 270:5665.
38. Kenney, L. J. 2002. Structure/function relationships in OmpR and other winged-helix transcription factors. Curr. Opin. Microbiol. 5:135141.
39. Kuhle, V.,, and M. Hensel. 2004. Cellular microbiology of intracellular Salmonella enterica: functions of the type III secretion system encoded by Salmonella pathogenicity island 2. Cell. Mol. Life Sci. 61:28122826.
40. Kuhle, V.,, and M. Hensel. 2002. SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell. Microbiol. 4:813824.
41. Lee, A. K.,, C. S. Detweiler,, and S. Falkow. 2000. OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol. 182:771781.
42. Lim, S.,, B. Kim,, H. S. Choi,, Y. Lee,, and S. Ryu. 2006. Fis is required for proper regulation of ssaG expression in Salmonella enterica serovar Typhimurium. Microb. Pathog. 41:3342.
43. Löber, S.,, D. Jäckel,, N. Kaiser,, and M. Hensel. 2006. Regulation of Salmonella pathogenicity island 2 genes by independent environmental signals. Int. J. Med. Microbiol. 296:435447.
44. Main-Hester, K. L.,, K. M. Colpitts,, G. A. Thomas,, F. C. Fang,, and S. J. Libby. 2008. Coordinate regulation of Salmonella pathogenicity island 1 (SPI1) and SPI4 in Salmonella enterica serovar Typhimurium. Infect. Immun. 76:10241035.
45. Mangan, M. W.,, S. Lucchini,, V. Danino,, T. O. Croinin,, J. C. Hinton,, and C. J. Dorman. 2006. The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59:18311847.
46. McCollister, B. D.,, T. J. Bourret,, R. Gill,, J. Jones-Carson,, and A. Vazquez-Torres. 2005. Repression of SPI2 transcription by nitric oxide-producing, IFNγ-activated macrophages promotes maturation of Salmonella phagosomes. J. Exp. Med. 202:625635.
47. Miao, E. A.,, and S. I. Miller. 2000. A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 97:75397544.
48. Ohlson, M. B.,, K. Fluhr,, C. L. Birmingham,, J. H. Brumell,, and S. I. Miller. 2005. SseJ deacylase activity by Salmonella enterica serovar Typhimurium promotes virulence in mice. Infect. Immun. 73:62496259.
49. Osborne, S. E.,, and B. K. Coombes. 2011. Transcriptional priming of Salmonella pathogenicity island-2 precedes cellular invasion. PLoS One 6:e21648.
50. Prost, L. R.,, and S. I. Miller. 2008. The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell. Microbiol. 10:576582.
51. Raffatellu, M.,, R. P. Wilson,, S. E. Winter,, and A. J. Bäumler. 2008. Clinical pathogenesis of typhoid fever. J. Infect. Dev. Ctries. 2:260266.
52. Rappl, C.,, J. Deiwick,, and M. Hensel. 2003. Acidic pH is required for the functional assembly of the type III secretion system encoded by Salmonella pathogenicity island 2. FEMS Microbiol. Lett. 226:363372.
53. Rhodius, V. A.,, W. C. Suh,, G. Nonaka,, J. West,, and C. A. Gross. 2006. Conserved and variable functions of the σE stress response in related genomes. PLoS Biol. 4:e2.
54. Rollenhagen, C.,, M. Sorensen,, K. Rizos,, R. Hurvitz,, and D. Bumann. 2004. Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen. Proc. Natl. Acad. Sci. USA 101:87398744.
55. Salcedo, S. P.,, and D. W. Holden. 2003. SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J. 22:50035014.
56. Schlumberger, M. C.,, and W. D. Hardt. 2006. Salmonella type III secretion effectors: pulling the host cell’s strings. Curr. Opin. Microbiol. 9:4654.
57. 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.
58. Silphaduang, U.,, M. Mascarenhas,, M. Karmali,, and B. K. Coombes. 2007. Repression of intracellular virulence factors in Salmonella by the Hha and YdgT nucleoid-associated proteins. J. Bacteriol. 189:36693673.
59. Stapleton, M. R.,, V. A. Norte,, R. C. Read,, and J. Green. 2002. Interaction of the Salmonella typhimurium transcription and virulence factor SlyA with target DNA and identification of members of the SlyA regulon. J. Biol. Chem. 277:1763017637.
60. Stein, M. A.,, K. Y. Leung,, M. Zwick,, F. Garcia-del Portillo,, and B. B. Finlay. 1996. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20:151164.
61. Stoebel, D. M.,, A. Free,, and C. J. Dorman. 2008. Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154:25332545.
62. Thijs, I. M.,, S. C. De Keersmaecker,, A. Fadda,, K. Engelen,, H. Zhao,, M. McClelland,, K. Marchal,, and J. Vanderleyden. 2007. Delineation of the Salmonella enterica serovar Typhimurium HilA regulon through genome-wide location and transcript analysis. J. Bacteriol. 189:45874596.
63. Tomljenovic-Berube, A. M.,, D. T. Mulder,, M. D. Whiteside,, F. S. Brinkman,, and B. K. Coombes. 2010. Identification of the regulatory logic controlling Salmonella pathoadaptation by the SsrA-SsrB two-component system. PLoS Genet. 6:e1000875.
64. 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.
65. Vazquez-Torres, A.,, Y. Xu,, J. Jones-Carson,, D. W. Holden,, S.M. Lucia,, M. C. Dinauer,, P. Mastroeni,, and F. C. Fang. 2000. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287:16551658.
66. Vieira, O. V.,, R. J. Botelho,, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366:689704.
67. 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.
68. Wilson, J. W.,, C. Coleman,, and C. A. Nickerson. 2007. Cloning and transfer of the Salmonella pathogenicity island 2 type III secretion system for studies of a range of gram-negative genera. Appl. Environ. Microbiol. 73:59115918.
69. Winter, S. E.,, P. Thiennimitr,, M. G. Winter,, B. P. Butler,, D. L. Huseby,, R. W. Crawford,, J. M. Russell,, C. L. Bevins,, L. G. Adams,, R. M. Tsolis,, J. R. Roth,, and A. J. Baumler. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426429.
70. Worley, M. J.,, K. H. Ching,, and F. Heffron. 2000. Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol. Microbiol. 36:749761.
71. Xu, X.,, and M. Hensel. 2010. Systematic analysis of the SsrAB virulon of Salmonella enterica. Infect. Immun. 78:4958.
72. Yoon, H.,, J. E. McDermott,, S. Porwollik,, M. McClelland,, and F. Heffron. 2009. Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PLoS Pathog. 5:e1000306.
73. Yu, X. J.,, K. McGourty,, M. Liu,, K. E. Unsworth,, and D. W. Holden. 2010. pH sensing by intracellular Salmonella induces effector translocation. Science 328:10401043.
74. Yu, X. J.,, J. Ruiz-Albert,, K. E. Unsworth,, S. Garvis,, M. Liu,, and D. W. Holden. 2002. SpiC is required for secretion of Salmonella pathogenicity island 2 type III secretion system proteins. Cell. Microbiol. 4:531540.
75. Zwir, I.,, D. Shin,, A. Kato,, K. Nishino,, T. Latifi,, F. Solomon,, J. M. Hare,, H. Huang,, and E. A. Groisman. 2005. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc. Natl. Acad. Sci. USA 102:28622867.

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