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http://dx.doi.org/10.1007/s10059-009-0133-9

A tdcA Mutation Reduces the Invasive Ability of Salmonella enterica Serovar Typhimurium  

Kim, Minjeong (Department of Food and Animal Biotechnology, Department of Agricultural Biotechnology, Center for Agricultural Biomaterials, and Research Institute for Agriculture and Life Sciences, Seoul National University)
Lim, Sangyong (Radiation Research Center for Biotechnology, Korea Atomic Energy Research Institute)
Kim, Dongho (Radiation Research Center for Biotechnology, Korea Atomic Energy Research Institute)
Choy, Hyon E. (Genome Research Center for Enteropathogenic Bacteria and Research Institute of Vibrio Infection and Department of Microbiology, Chonnam National University Medical College)
Ryu, Sangryeol (Department of Food and Animal Biotechnology, Department of Agricultural Biotechnology, Center for Agricultural Biomaterials, and Research Institute for Agriculture and Life Sciences, Seoul National University)
Publication Information
Molecules and Cells / v.28, no.4, 2009 , pp. 389-395 More about this Journal
Abstract
We previously observed that the transcription of some flagellar genes decreased in Salmonella Typhimurium tdcA mutant, which is a gene encoding the transcriptional activator of the tdc operon. Since flagella-mediated bacterial motility accelerates the invasion of Salmonella, we have examined the effect of tdcA mutation on the invasive ability as well as the flagellar biosynthesis in S. Typhimurium. A tdcA mutation caused defects in motility and formation of flagellin protein, FliC in S. Typhimurium. Invasion assays in the presence of a centrifugal force confirmed that the defect of flagellum synthesis decreases the ability of Salmonella to invade into cultured epithelial cells. In addition, we also found that the expression of Salmonella pathogenicity island 1 (SPI1) genes required for Salmonella invasion was down-regulated in the tdcA mutant because of the decreased expression of fliZ, a positive regulator of SPI1 transcriptional activator, hilA. Finally, the virulence of a S. Typhimurium tdcA mutant was attenuated compared to a wild type when administered orally. This study implies the role of tdcA in the invasion process of S. Typhimurium.
Keywords
flagella; invasion; Salmonella pathogenicity island; tdcA;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 4  (Related Records In Web of Science)
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1 Chilcott, G.S., and Hughes, K.T. (2000). Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol. Mol. Biol. Rev. 64, 694-708   DOI   ScienceOn
2 Datsenko, K.A., and Wanner, B.L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645   DOI   ScienceOn
3 Drlica, K. (1992). Control of bacterial DNA supercoiling. Mol. Microbiol. 6, 425-433   DOI   PUBMED   ScienceOn
4 Goss, T.J., Schweizer, H.P., and Datta, P. (1988). Molecular characterization of the tdc operon of Escherichia coli K-12. J. Bacteriol. 170, 5352-5359   DOI
5 Guiney, D.G. (1997). Regulation of bacterial virulence gene expression by the host environment. J. Clin. Invest. 99, 565-569   DOI   ScienceOn
6 Hagewood, B.T., Ganduri, Y.L., and Datta, P. (1994). Functional analysis of the tdcABC promoter of Escherichia coli: roles of TdcA and TdcR. J. Bacteriol. 176, 6214-6220   DOI   PUBMED
7 Jones, G.W., Richardson, L.A., and Uhlman, D. (1981). The invasion of HeLa cells by Salmonella typhimurium: reversible and irreversible bacterial attachment and the role of bacterial motility. J. Gen. Microbiol. 127, 351-360   PUBMED
8 Kelly, A., Goldberg, M.D., Carroll, R.K., Danino, V., Hinton, J.C.D., and Dorman, C.J. (2004). A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150, 2037-2053   DOI   ScienceOn
9 Lee, C.A., and Falkow, S. (1990). The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl. Acad. Sci. USA 87, 4304-4308   DOI   ScienceOn
10 Lim, S.-Y., Joe, M.H., Song, S.S., Lee, M.H., Foster, J.W., Park, Y.K., Choi, S.Y., and Lee, I.S. (2002). cuiD is a crucial gene for survival at high copper environment in Salmonella enterica serovar Typhimuirum. Mol. Cells 14, 177-184
11 Liu, S.L., Ezaki, T., Miura, H., Matsui, K., and Yabuuchi, E. (1988). Intact motility as a Salmonella typhi invasion-related factor. Infect. Immun. 56, 1967-1973
12 Lucas, R.L., Lostroh, C.P., DIRusso, C.C., Spector, M.P., Wanner, B.L., and Lee, C.A. (2000). Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182, 1872-1882   DOI   ScienceOn
13 Heßlinger, C., Fairhurst, S.A., and Sawers, G. (1998). Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L-threonine to propionate. Mol. Microbiol. 27, 477-492   DOI   PUBMED   ScienceOn
14 Dorman, C.J., Barr, G.C., Ní Bhriain, N., and Higgins, C.F. (1988). DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression, J. Bacteriol. 170, 2816-2826   DOI
15 Komoriya, K., Shibano, N., Higano, T., Azuma, N., Yamaguchi, S., and Aizawa, S.I. (1999). Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34, 767-779   DOI   ScienceOn
16 Maloy, S.R., Stewart, V.J., and Taylor, R.K. (1996). Genetic Analysis of Pathogenic Bacteria: A Laboratory Manual, (New York: Cold Spring Harbor Laboratory Press)
17 Sumantran, V.N., Tranguch, A.J., and Datta, P. (1989). Increased expression of biodegradative threonine dehydratase of Escherichia coli by DNA gyrase inhibitors. FEMS Microbiol. Lett. 65, 37-40   DOI
18 Ko, M., and Park, C. (2000). H-NS-dependent regulation of flagellar synthesis is mediated by a LysR family protein. J. Bacteriol. 182, 4670-4672   DOI   ScienceOn
19 Bajaj, V., Lucas, R.L., Hwang, C., and Lee, C.A. (1996). Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22, 703-714   DOI   ScienceOn
20 Lostroh, C.P., and Lee, C.A. (2001). The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 3, 1281-1291   DOI   ScienceOn
21 Hsieh, L-.S., Burger, R.M., and Drlica, K. (1991). Bacterial DNA supercoiling and [ATP]/[ADP] changes associated with a transition to anaerobic growth. J. Mol. Biol. 219, 443-450   DOI   PUBMED
22 Stecher, B., Hapfelmeier, S., Müller, C., Kremer, M., Stallmach, T., and Hardt, W.D. (2004). Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72, 4138-4150   DOI   PUBMED   ScienceOn
23 Lim, S., Yong, K., and Ryu, S. (2005). Analysis of Salmonella pathogenicity island 1 expression in response to the changes of osmolarity. J. Microbiol. Biotechnol. 15, 175-182
24 Ganduri, Y.L., Sadda, S.R., Datta, M.W., Jambukeswaran, R.K., and Datta, P. (1993). TdcA, a transcriptional activator of the tdcABC operon of Escherichia coli, is a member of the LysR family of proteins. Mol. Gen. Genet. 240, 395-402
25 Schweizer, H.P., and Datta, P. (1989). Identification and DNA sequence of tdcR, a positive regulatory gene of the tdc operon of Escherichia coli. Mol. Gen. Genet. 218, 516-522   DOI   ScienceOn
26 Soutourina, O.A., and Bertin, P.N. (2003). Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol. Rev. 27, 505-523
27 Landini, P., and Zehnder, A.J.B. (2002). The global regulatory hns gene negatively affects adhesion to solid surfaces by anaerobically grown Escherichia coli by modulating expression of flagellar genes and lipopolysaccharide production. J. Bacteriol. 184, 1522-1529   DOI   ScienceOn
28 Lehnen, D., Blumer, C., Polen, T., Wackwitz, B., Wendisch, V.F., and Unden, G. (2002). LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol. Microbiol. 45, 521-532   DOI   ScienceOn
29 Song, M., Kim, H., Kim, E., Shin, M., Lee, H., Hong, Y., Rhee, J., Yoon, H., Ryu, S., Lim, S., et al. (2004). ppGpp-dependent stationary phase induction of genes on Salmonella pathogenicity island I. J. Biol. Chem. 279, 34183-34190   DOI   ScienceOn
30 Josenhans, C., and Suerbaum, S. (2002). The role of motility as a virulence factor in bacteria. Int. J. Med. Microbiol. 291, 605-614   DOI   ScienceOn
31 Lim, S., Yun, J., Yoon, H., Park, C., Kim, B., Jeon, B., Kim, D., and Ryu, S. (2007). Mlc regulation of Salmonella pathogenicity island I gene expression via hilE repression. Nucleic Acids Res. 35, 1822-1832   DOI   ScienceOn
32 Jones, B.D., Lee, C.A., and Falkow, S. (1992). Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60, 2475-2480   PUBMED
33 Kim, M., Lim, S., and Ryu, S. (2008). Molecular analysis of the Salmonella Typhimurium tdc operon regulation. J. Microbiol. Biotechnol. 18, 1024-1032   PUBMED
34 Choi, J., Shin, D., and Ryu, S. (2007). Implication of quorum sensing in Salmonella enterica serovar Typhimurium virulence : the luxS gene is necessary for expression of genes in pathogenicity Island I. Infect. Immun. 75, 4885-4890   DOI   ScienceOn
35 Sawers, G. (1998). The anaerobic degradation of L-serine and Lthreonine in enterobacteria: networks of pathways and regulatory signals. Arch. Microbiol. 171, 1-5   DOI   PUBMED   ScienceOn
36 Lim, S., Yoon, H., Ryu, S., Jung, J., Lee, M., and Kim, D. (2006). A comparative evaluation of radiation-induced DNA damage using real-time PCR: influence of base composition. Radiat. Res. 165, 430-437   DOI   ScienceOn
37 Gellert, M., Mizuuchi, K., O’Dea, M.H., and Nash, H.A. (1976). DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. USA 73, 3872-3876   DOI   ScienceOn
38 Higgins, C.F., Dorman, C.J., Stirling, D.A., Waddell, L., Booth, I.R., May, G., and Bremer, E. (1988). A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52, 569-584   DOI   ScienceOn
39 Wu, Y., and Datta, P. (1995). Influence of DNA topology on expression of the tdc operon in Escherichia coli K-12. Mol. Gen. Genet. 247, 764-767   DOI   ScienceOn
40 Eichelberg, K., and Gal$\ddot{a}$án, J.E. (2000). The flagellar sigma factor FliA ${\sigma}^28$ regulates the expression of Salmonella genes associated with the centisome 63 type III secretion system. Infect. Immun. 68, 2735-2743   DOI   ScienceOn
41 Wu, Y., Patil, R.V., and Datta, P. (1992). Catabolite gene activator protein and integration host factor act in concert to regulate tdc operon expression in Escherichia coli. J. Bacteriol. 174, 6918-6927   DOI   PUBMED
42 Shi, W., Li, C., Louise, C., and Adler, J. (1993). Mechanism of adverse conditions causing lack of flagella in Escherichia coli. J. Bacteriol. 175, 2236-2240   DOI   PUBMED
43 Schmitt, C.K., Ikeda, J.S., Darnell, S.C., Watson, P.R., Bispham, J., Wallis, T.S., Weinstein, D.L., Metcalf, E.S., and O’Brien, A.D. (2001). Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69, 5619-5625   DOI   ScienceOn
44 Iyoda, S., Kamidoi, T., Hirose, K., Kutsukake, K., and Watanabe, H. (2001). A flagellar gene fliZ regulates the expression of invasion genes and virulence phenotype in Salmonella enterica serovar Typhimurium. Microb. Pathog. 30, 81-90   DOI   ScienceOn
45 Tomita, T., and Kanegasaki, S. (1982). Enhanced phagocytic response of macrophages to bacteria by impact caused by bacterial motility or centrifugation. Infect. Immun. 38, 865-870   PUBMED