Previous Article | Next Article 
Infection and Immunity, December 1998, p. 5799-5804, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Secreted Effector Proteins of Salmonella
dublin Act in Concert To Induce Enteritis
Michael A.
Jones,
Michael W.
Wood,
Paul B.
Mullan,
Patricia
R.
Watson,
Tim S.
Wallis, and
Edouard E.
Galyov*
Institute for Animal Health, Compton,
Berkshire RG20 7NN, United Kingdom
Received 15 July 1998/Returned for modification 19 August
1998/Accepted 10 September 1998
The ability of enteropathogenic salmonellae to recruit inflammatory
cells and induce secretory responses in the infected ileum is
considered to be a main feature in Salmonella-induced
enteritis. Interactions between the pathogen and intestinal epithelial
cells result in a variety of cellular responses mediating inflammation and fluid secretion. It is becoming apparent that proteins secreted by
the Inv-Spa type III secretion system of Salmonella spp.
play a key role in the induction of these responses. We have recently demonstrated that the SopB effector protein is translocated into eukaryotic cells via a Sip-dependent pathway and mediates inflammation and fluid secretion in infected ileal mucosa. However, SopB did not
appear to be the only effector involved, as inactivation of the
sopB gene only partially impaired enteropathogenicity. We suggested that at least some of such protein effectors are likely to be
proteins of the same class as SopB, i.e., secreted effector proteins
translocated into eukaroyotic cells via a Sip-dependent pathway. In
this work, we identify SopD, another secreted protein belonging to the
family of Sop effectors of Salmonella dublin. Using the
cya reporter system we showed that SopD is translocated into eukaroyotic cells. We assessed the potential involvement of SopD
in enteropathogenicity and found that inactivation of sopD
has an additive effect in relation to the sopB mutation.
*
Corresponding author. Mailing address: Institute
for Animal Health, Compton, Berkshire RG20 7NN United Kingdom.
Phone: (44) 1635 578411. Fax: (44) 1635 577263. E-mail:
galyov{at}bbsrc.ac.uk.

Present address: Department of Oncology, The Queen's University of
Belfast, Belfast City Hospital, Belfast BT9 7AB Northern
Ireland.
Infection and Immunity, December 1998, p. 5799-5804, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Stevens, M. P., Humphrey, T. J., Maskell, D. J.
(2009). Molecular insights into farm animal and zoonotic Salmonella infections. Phil Trans R Soc B
364: 2709-2723
[Abstract]
[Full Text]
-
Pullinger, G. D., Paulin, S. M., Charleston, B., Watson, P. R., Bowen, A. J., Dziva, F., Morgan, E., Villarreal-Ramos, B., Wallis, T. S., Stevens, M. P.
(2007). Systemic Translocation of Salmonella enterica Serovar Dublin in Cattle Occurs Predominantly via Efferent Lymphatics in a Cell-Free Niche and Requires Type III Secretion System 1 (T3SS-1) but Not T3SS-2. Infect. Immun.
75: 5191-5199
[Abstract]
[Full Text]
-
Hudson, D. L., Layton, A. N., Field, T. R., Bowen, A. J., Wolf-Watz, H., Elofsson, M., Stevens, M. P., Galyov, E. E.
(2007). Inhibition of Type III Secretion in Salmonella enterica Serovar Typhimurium by Small-Molecule Inhibitors. Antimicrob. Agents Chemother.
51: 2631-2635
[Abstract]
[Full Text]
-
Giacomodonato, M. N., Uzzau, S., Bacciu, D., Caccuri, R., Sarnacki, S. H., Rubino, S., Cerquetti, M. C.
(2007). SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology
153: 1221-1228
[Abstract]
[Full Text]
-
Raffatellu, M., Chessa, D., Wilson, R. P., Tukel, C., Akcelik, M., Baumler, A. J.
(2006). Capsule-Mediated Immune Evasion: a New Hypothesis Explaining Aspects of Typhoid Fever Pathogenesis. Infect. Immun.
74: 19-27
[Full Text]
-
Coombes, B. K., Coburn, B. A., Potter, A. A., Gomis, S., Mirakhur, K., Li, Y., Finlay, B. B.
(2005). Analysis of the Contribution of Salmonella Pathogenicity Islands 1 and 2 to Enteric Disease Progression Using a Novel Bovine Ileal Loop Model and a Murine Model of Infectious Enterocolitis. Infect. Immun.
73: 7161-7169
[Abstract]
[Full Text]
-
Haque, A, Bowe, F, Fitzhenry, R J, Frankel, G, Thomson, M, Heuschkel, R, Murch, S, Stevens, M P, Wallis, T S, Phillips, A D, Dougan, G
(2004). Early interactions of Salmonella enterica serovar typhimurium with human small intestinal epithelial explants. Gut
53: 1424-1430
[Abstract]
[Full Text]
-
Hapfelmeier, S., Ehrbar, K., Stecher, B., Barthel, M., Kremer, M., Hardt, W.-D.
(2004). Role of the Salmonella Pathogenicity Island 1 Effector Proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica Subspecies 1 Serovar Typhimurium Colitis in Streptomycin-Pretreated Mice. Infect. Immun.
72: 795-809
[Abstract]
[Full Text]
-
Schmidt, H., Hensel, M.
(2004). Pathogenicity Islands in Bacterial Pathogenesis. Clin. Microbiol. Rev.
17: 14-56
[Abstract]
[Full Text]
-
Cheminay, C., Chakravortty, D., Hensel, M.
(2004). Role of Neutrophils in Murine Salmonellosis. Infect. Immun.
72: 468-477
[Abstract]
[Full Text]
-
Ehrbar, K., Friebel, A., Miller, S. I., Hardt, W.-D.
(2003). Role of the Salmonella Pathogenicity Island 1 (SPI-1) Protein InvB in Type III Secretion of SopE and SopE2, Two Salmonella Effector Proteins Encoded Outside of SPI-1. J. Bacteriol.
185: 6950-6967
[Abstract]
[Full Text]
-
Logsdon, L. K., Mecsas, J.
(2003). Requirement of the Yersinia pseudotuberculosis Effectors YopH and YopE in Colonization and Persistence in Intestinal and Lymph Tissues. Infect. Immun.
71: 4595-4607
[Abstract]
[Full Text]
-
Zhang, S., Adams, L. G., Nunes, J., Khare, S., Tsolis, R. M., Baumler, A. J.
(2003). Secreted Effector Proteins of Salmonella enterica Serotype Typhimurium Elicit Host-Specific Chemokine Profiles in Animal Models of Typhoid Fever and Enterocolitis. Infect. Immun.
71: 4795-4803
[Abstract]
[Full Text]
-
Zhang, S., Kingsley, R. A., Santos, R. L., Andrews-Polymenis, H., Raffatellu, M., Figueiredo, J., Nunes, J., Tsolis, R. M., Adams, L. G., Baumler, A. J.
(2003). Molecular Pathogenesis of Salmonella enterica Serotype Typhimurium-Induced Diarrhea. Infect. Immun.
71: 1-12
[Full Text]
-
Freeman, J. A., Rappl, C., Kuhle, V., Hensel, M., Miller, S. I.
(2002). SpiC Is Required for Translocation of Salmonella Pathogenicity Island 2 Effectors and Secretion of Translocon Proteins SseB and SseC. J. Bacteriol.
184: 4971-4980
[Abstract]
[Full Text]
-
Zhang, S., Santos, R. L., Tsolis, R. M., Stender, S., Hardt, W.-D., Baumler, A. J., Adams, L. G.
(2002). The Salmonella enterica Serotype Typhimurium Effector Proteins SipA, SopA, SopB, SopD, and SopE2 Act in Concert To Induce Diarrhea in Calves. Infect. Immun.
70: 3843-3855
[Abstract]
[Full Text]
-
Casper-Lindley, C., Dahlbeck, D., Clark, E. T., Staskawicz, B. J.
(2002). Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci. USA
99: 8336-8341
[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]
-
Jones, M. A., Wigley, P., Page, K. L., Hulme, S. D., Barrow, P. A.
(2001). Salmonella enterica Serovar Gallinarum Requires the Salmonella Pathogenicity Island 2 Type III Secretion System but Not the Salmonella Pathogenicity Island 1 Type III Secretion System for Virulence in Chickens. Infect. Immun.
69: 5471-5476
[Abstract]
[Full Text]
-
Lu, L., Walker, W A.
(2001). Pathologic and physiologic interactions of bacteria with the gastrointestinal epithelium. Am. J. Clin. Nutr.
73
: 1124S-1130S
[Abstract]
[Full Text]
-
Mirold, S., Ehrbar, K., Weissmüller, A., Prager, R., Tschäpe, H., Rüssmann, H., Hardt, W.-D.
(2001). Salmonella Host Cell Invasion Emerged by Acquisition of a Mosaic of Separate Genetic Elements, Including Salmonella Pathogenicity Island 1 (SPI1), SPI5, and sopE2. J. Bacteriol.
183: 2348-2358
[Abstract]
[Full Text]
-
Bronstein, P. A., Miao, E. A., Miller, S. I.
(2000). InvB Is a Type III Secretion Chaperone Specific for SspA. J. Bacteriol.
182: 6638-6644
[Abstract]
[Full Text]
-
Lee, C. A., Silva, M., Siber, A. M., Kelly, A. J., Galyov, E., McCormick, B. A.
(2000). A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc. Natl. Acad. Sci. USA
97: 12283-12288
[Abstract]
[Full Text]
-
Murray, R. A., Lee, C. A.
(2000). Invasion Genes Are Not Required for Salmonella enterica Serovar Typhimurium To Breach the Intestinal Epithelium: Evidence That Salmonella Pathogenicity Island 1 Has Alternative Functions during Infection. Infect. Immun.
68: 5050-5055
[Abstract]
[Full Text]
-
Miao, E. A., Miller, S. I.
(2000). A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc. Natl. Acad. Sci. USA
97: 7539-7544
[Abstract]
[Full Text]
-
Watson, P. R., Benmore, A., Khan, S. A., Jones, P. W., Maskell, D. J., Wallis, T. S.
(2000). Mutation of waaN Reduces Salmonella enterica Serovar Typhimurium-Induced Enteritis and Net Secretion of Type III Secretion System 1-Dependent Proteins. Infect. Immun.
68: 3768-3771
[Abstract]
[Full Text]
-
Bakshi, C. S., Singh, V. P., Wood, M. W., Jones, P. W., Wallis, T. S., Galyov, E. E.
(2000). Identification of SopE2, a Salmonella Secreted Protein Which Is Highly Homologous to SopE and Involved in Bacterial Invasion of Epithelial Cells. J. Bacteriol.
182: 2341-2344
[Abstract]
[Full Text]
-
Tsolis, R. M., Adams, L. G., Ficht, T. A., Baumler, A. J.
(1999). Contribution of Salmonella typhimurium Virulence Factors to Diarrheal Disease in Calves. Infect. Immun.
67: 4879-4885
[Abstract]
[Full Text]
-
Watson, P. R., Paulin, S. M., Bland, A. P., Libby, S. J., Jones, P. W., Wallis, T. S.
(1999). Differential Regulation of Enteric and Systemic Salmonellosis by slyA. Infect. Immun.
67: 4950-4954
[Abstract]
[Full Text]
-
Mirold, S., Rabsch, W., Rohde, M., Stender, S., Tschape, H., Russmann, H., Igwe, E., Hardt, W.-D.
(1999). Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl. Acad. Sci. USA
96: 9845-9850
[Abstract]
[Full Text]
-
Friebel, A., Ilchmann, H., Aepfelbacher, M., Ehrbar, K., Machleidt, W., Hardt, W.-D.
(2001). SopE and SopE2 from Salmonella typhimurium Activate Different Sets of RhoGTPases of the Host Cell. J. Biol. Chem.
276: 34035-34040
[Abstract]
[Full Text]