Previous Article | Next Article 
Journal of Bacteriology, August 1999, p. 4949-4954, Vol. 181, No. 16
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
InvF Is Required for Expression of Genes Encoding
Proteins Secreted by the SPI1 Type III Secretion Apparatus in
Salmonella typhimurium
K.
Heran
Darwin1,2 and
Virginia L.
Miller2,3,*
Department of Microbiology and Molecular Genetics,
University of California, Los Angeles, Los Angeles, California
90095,1 and Departments of Molecular
Microbiology2 and
Pediatrics,3 Washington University
School of Medicine, St. Louis, Missouri 63110
Received 17 March 1999/Accepted 10 June 1999
The expression of genes encoding proteins secreted by the SPI1
(Salmonella pathogenicity island) type III secretion
apparatus is known to require the transcriptional activators SirA and
HilA. However, neither SirA nor HilA is believed to directly activate the promoters of these genes. invF, the first gene of the
inv-spa gene cluster, is predicted to encode an AraC-type
transcriptional activator and is required for invasion into cultured
epithelial cells. However, the genes which are regulated by InvF have
not been identified. In this work, an in-frame deletion in
invF was constructed and tested for the expression of
(sigD-lacZYA),
sipC::Tn5lacZY, and a plasmid-encoded
(sicA-lacZYA). SigD (Salmonella invasion gene) is a secreted protein required for the efficient invasion of
Salmonella typhimurium into cultured eucaryotic cells.
sicA (Salmonella invasion chaperone) is the
first gene of a putative operon encoding the Sip/Ssp
(Salmonella invasion/Salmonella secreted proteins) invasion proteins secreted by the SPI1 type III export apparatus. invF was required for the expression of the
sigD, sicA, and sipC fusions. This
is the first demonstration that there is a functional promoter in the
intergenic sequence between spaS and sicA. In
addition, several proteins were either absent from or found in reduced
amounts in the culture supernatants of the invF mutant.
Therefore, invF is required for the optimal expression of
several genes encoding SPI1-secreted proteins. Genetic evidence is also
presented suggesting there is HilA-dependent readthrough transcription
from the invF promoter at least through sipC.
*
Corresponding author. Mailing address: Department of
Molecular Microbiology, Washington University School of Medicine, 660 South Euclid, Campus Box 8230, St. Louis, MO 63110. Phone: (314) 747-2132. Fax: (314) 747-2135. E-mail:
virginia{at}borcim.wustl.edu.
Journal of Bacteriology, August 1999, p. 4949-4954, Vol. 181, No. 16
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Negrea, A., Bjur, E., Puiac, S., Ygberg, S. E., Aslund, F., Rhen, M.
(2009). Thioredoxin 1 Participates in the Activity of the Salmonella enterica Serovar Typhimurium Pathogenicity Island 2 Type III Secretion System. J. Bacteriol.
191: 6918-6927
[Abstract]
[Full Text]
-
Webber, M. A., Bailey, A. M., Blair, J. M. A., Morgan, E., Stevens, M. P., Hinton, J. C. D., Ivens, A., Wain, J., Piddock, L. J. V.
(2009). The Global Consequence of Disruption of the AcrAB-TolC Efflux Pump in Salmonella enterica Includes Reduced Expression of SPI-1 and Other Attributes Required To Infect the Host. J. Bacteriol.
191: 4276-4285
[Abstract]
[Full Text]
-
Walker, K. A., Miller, V. L.
(2009). Synchronous Gene Expression of the Yersinia enterocolitica Ysa Type III Secretion System and Its Effectors. J. Bacteriol.
191: 1816-1826
[Abstract]
[Full Text]
-
Su, J., Gong, H., Lai, J., Main, A., Lu, S.
(2009). The Potassium Transporter Trk and External Potassium Modulate Salmonella enterica Protein Secretion and Virulence. Infect. Immun.
77: 667-675
[Abstract]
[Full Text]
-
Jeong, J.-H., Song, M., Park, S.-I., Cho, K.-O., Rhee, J. H., Choy, H. E.
(2008). Salmonella enterica Serovar Gallinarum Requires ppGpp for Internalization and Survival in Animal Cells. J. Bacteriol.
190: 6340-6350
[Abstract]
[Full Text]
-
Huang, Y., Suyemoto, M., Garner, C. D., Cicconi, K. M., Altier, C.
(2008). Formate Acts as a Diffusible Signal To Induce Salmonella Invasion. J. Bacteriol.
190: 4233-4241
[Abstract]
[Full Text]
-
Main-Hester, K. L., Colpitts, K. M., Thomas, G. A., Fang, F. C., Libby, S. J.
(2008). Coordinate Regulation of Salmonella Pathogenicity Island 1 (SPI1) and SPI4 in Salmonella enterica Serovar Typhimurium. Infect. Immun.
76: 1024-1035
[Abstract]
[Full Text]
-
Gerlach, R. G., Jackel, D., Geymeier, N., Hensel, M.
(2007). Salmonella Pathogenicity Island 4-Mediated Adhesion Is Coregulated with Invasion Genes in Salmonella enterica. Infect. Immun.
75: 4697-4709
[Abstract]
[Full Text]
-
Negrea, A., Bjur, E., Ygberg, S. E., Elofsson, M., Wolf-Watz, H., Rhen, M.
(2007). Salicylidene Acylhydrazides That Affect Type III Protein Secretion in Salmonella enterica Serovar Typhimurium. Antimicrob. Agents Chemother.
51: 2867-2876
[Abstract]
[Full Text]
-
Thijs, I. M. V., De Keersmaecker, S. C. J., Fadda, A., Engelen, K., Zhao, H., McClelland, M., Marchal, K., Vanderleyden, J.
(2007). Delineation of the Salmonella enterica Serovar Typhimurium HilA Regulon through Genome-Wide Location and Transcript Analysis. J. Bacteriol.
189: 4587-4596
[Abstract]
[Full Text]
-
Fardini, Y., Chettab, K., Grepinet, O., Rochereau, S., Trotereau, J., Harvey, P., Amy, M., Bottreau, E., Bumstead, N., Barrow, P. A., Virlogeux-Payant, I.
(2007). The YfgL Lipoprotein Is Essential for Type III Secretion System Expression and Virulence of Salmonella enterica Serovar Enteritidis. Infect. Immun.
75: 358-370
[Abstract]
[Full Text]
-
Teplitski, M., Al-Agely, A., Ahmer, B. M. M.
(2006). Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium.. Microbiology
152: 3411-3424
[Abstract]
[Full Text]
-
Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F., Hautefort, I., Thompson, A., Hinton, J. C., Van Immerseel, F.
(2006). Butyrate Specifically Down-Regulates Salmonella Pathogenicity Island 1 Gene Expression. Appl. Environ. Microbiol.
72: 946-949
[Abstract]
[Full Text]
-
Fortune, D. R., Suyemoto, M., Altier, C.
(2006). Identification of CsrC and Characterization of Its Role in Epithelial Cell Invasion in Salmonella enterica Serovar Typhimurium. Infect. Immun.
74: 331-339
[Abstract]
[Full Text]
-
De Keersmaecker, S. C. J., Marchal, K., Verhoeven, T. L. A., Engelen, K., Vanderleyden, J., Detweiler, C. S.
(2005). Microarray Analysis and Motif Detection Reveal New Targets of the Salmonella enterica Serovar Typhimurium HilA Regulatory Protein, Including hilA Itself. J. Bacteriol.
187: 4381-4391
[Abstract]
[Full Text]
-
Zhang, L., Chaudhuri, R. R., Constantinidou, C., Hobman, J. L., Patel, M. D., Jones, A. C., Sarti, D., Roe, A. J., Vlisidou, I., Shaw, R. K., Falciani, F., Stevens, M. P., Gally, D. L., Knutton, S., Frankel, G., Penn, C. W., Pallen, M. J.
(2004). Regulators Encoded in the Escherichia coli Type III Secretion System 2 Gene Cluster Influence Expression of Genes within the Locus for Enterocyte Effacement in Enterohemorrhagic E. coli O157:H7. Infect. Immun.
72: 7282-7293
[Abstract]
[Full Text]
-
Brussow, H., Canchaya, C., Hardt, W.-D.
(2004). Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion. Microbiol. Mol. Biol. Rev.
68: 560-602
[Abstract]
[Full Text]
-
Song, M., Kim, H.-J., Kim, E. Y., Shin, M., Lee, H. C., Hong, Y., Rhee, J. H., Yoon, H., Ryu, S., Lim, S., Choy, H. E.
(2004). ppGpp-dependent Stationary Phase Induction of Genes on Salmonella Pathogenicity Island 1. J. Biol. Chem.
279: 34183-34190
[Abstract]
[Full Text]
-
Walker, K. A., Miller, V. L.
(2004). Regulation of the Ysa Type III Secretion System of Yersinia enterocolitica by YsaE/SycB and YsrS/YsrR. J. Bacteriol.
186: 4056-4066
[Abstract]
[Full Text]
-
Van Immerseel, F., De Buck, J., Boyen, F., Bohez, L., Pasmans, F., Volf, J., Sevcik, M., Rychlik, I., Haesebrouck, F., Ducatelle, R.
(2004). Medium-Chain Fatty Acids Decrease Colonization and Invasion through hilA Suppression Shortly after Infection of Chickens with Salmonella enterica Serovar Enteritidis. Appl. Environ. Microbiol.
70: 3582-3587
[Abstract]
[Full Text]
-
Olekhnovich, I. N., Kadner, R. J.
(2004). Contribution of the RpoA C-Terminal Domain to Stimulation of the Salmonella enterica hilA Promoter by HilC and HilD. J. Bacteriol.
186: 3249-3253
[Abstract]
[Full Text]
-
Ellermeier, C. D., Slauch, J. M.
(2004). RtsA Coordinately Regulates DsbA and the Salmonella Pathogenicity Island 1 Type III Secretion System. J. Bacteriol.
186: 68-79
[Abstract]
[Full Text]
-
Teplitski, M., Goodier, R. I., Ahmer, B. M. M.
(2003). Pathways Leading from BarA/SirA to Motility and Virulence Gene Expression in Salmonella. J. Bacteriol.
185: 7257-7265
[Abstract]
[Full Text]
-
Day, J. B., Lee, C. A.
(2003). Secretion of the orgC Gene Product by Salmonella enterica Serovar Typhimurium. Infect. Immun.
71: 6680-6685
[Abstract]
[Full Text]
-
Ellermeier, C. D., Slauch, J. M.
(2003). RtsA and RtsB Coordinately Regulate Expression of the Invasion and Flagellar Genes in Salmonella enterica Serovar Typhimurium. J. Bacteriol.
185: 5096-5108
[Abstract]
[Full Text]
-
Boddicker, J. D., Knosp, B. M., Jones, B. D.
(2003). Transcription of the Salmonella Invasion Gene Activator, hilA, Requires HilD Activation in the Absence of Negative Regulators. J. Bacteriol.
185: 525-533
[Abstract]
[Full Text]
-
Kane, C. D., Schuch, R., Day, W. A. Jr, Maurelli, A. T.
(2002). MxiE Regulates Intracellular Expression of Factors Secreted by the Shigella flexneri 2a Type III Secretion System. J. Bacteriol.
184: 4409-4419
[Abstract]
[Full Text]
-
Olekhnovich, I. N., Kadner, R. J.
(2002). DNA-Binding Activities of the HilC and HilD Virulence Regulatory Proteins of Salmonella enterica Serovar Typhimurium. J. Bacteriol.
184: 4148-4160
[Abstract]
[Full Text]
-
Takaya, A., Tomoyasu, T., Tokumitsu, A., Morioka, M., Yamamoto, T.
(2002). The ATP-Dependent Lon Protease of Salmonella enterica Serovar Typhimurium Regulates Invasion and Expression of Genes Carried on Salmonella Pathogenicity Island 1. J. Bacteriol.
184: 224-232
[Abstract]
[Full Text]
-
Beuzon, C. R., Unsworth, K. E., Holden, D. W.
(2001). In Vivo Genetic Analysis Indicates That PhoP-PhoQ and the Salmonella Pathogenicity Island 2 Type III Secretion System Contribute Independently to Salmonella enterica Serovar Typhimurium Virulence. Infect. Immun.
69: 7254-7261
[Abstract]
[Full Text]
-
Lostroh, C. P., Lee, C. A.
(2001). The HilA Box and Sequences outside It Determine the Magnitude of HilA-Dependent Activation of PprgH from Salmonella Pathogenicity Island 1. J. Bacteriol.
183: 4876-4885
[Abstract]
[Full Text]
-
Lucas, R. L., Lee, C. A.
(2001). Roles of hilC and hilD in Regulation of hilA Expression in Salmonella enterica Serovar Typhimurium. J. Bacteriol.
183: 2733-2745
[Abstract]
[Full Text]
-
Goodier, R. I., Ahmer, B. M. M.
(2001). SirA Orthologs Affect both Motility and Virulence. J. Bacteriol.
183: 2249-2258
[Abstract]
[Full Text]
-
Darwin, K. H., Robinson, L. S., Miller, V. L.
(2001). SigE Is a Chaperone for the Salmonella enterica Serovar Typhimurium Invasion Protein SigD. J. Bacteriol.
183: 1452-1454
[Abstract]
[Full Text]
-
Prouty, A. M., Gunn, J. S.
(2000). Salmonella enterica Serovar Typhimurium Invasion Is Repressed in the Presence of Bile. Infect. Immun.
68: 6763-6769
[Abstract]
[Full Text]
-
Altier, C., Suyemoto, M., Lawhon, S. D.
(2000). Regulation of Salmonella enterica Serovar Typhimurium Invasion Genes by csrA. Infect. Immun.
68: 6790-6797
[Abstract]
[Full Text]
-
Lucas, R. L., Lostroh, C. P., DiRusso, C. C., Spector, M. P., Wanner, B. L., Lee, C. A.
(2000). Multiple Factors Independently Regulate hilA and Invasion Gene Expression in Salmonella enterica Serovar Typhimurium. J. Bacteriol.
182: 1872-1882
[Abstract]
[Full Text]
-
Lee, A. K., Detweiler, C. S., Falkow, S.
(2000). OmpR Regulates the Two-Component System SsrA-SsrB in Salmonella Pathogenicity Island 2. J. Bacteriol.
182: 771-781
[Abstract]
[Full Text]