This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lucas, R. L.
Right arrow Articles by Lee, C. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lucas, R. L.
Right arrow Articles by Lee, C. A.

 Previous Article  |  Next Article 

Journal of Bacteriology, April 2000, p. 1872-1882, Vol. 182, No. 7
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Multiple Factors Independently Regulate hilA and Invasion Gene Expression in Salmonella enterica Serovar Typhimurium

Robin L. Lucas,1 C. Phoebe Lostroh,1 Concetta C. DiRusso,2 Michael P. Spector,3 Barry L. Wanner,4 and Catherine A. Lee1,*

Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 021151; Department of Biochemistry and Molecular Biology, The Albany Medical College, Albany, New York 122082; Department of Biomedical Sciences, University of South Alabama, Mobile, Alabama 366883; and Department of Biological Sciences, Purdue University, West Lafayette, Indiana 479074

Received 11 November 1999/Accepted 19 January 2000

HilA activates the expression of Salmonella enterica serovar Typhimurium invasion genes. To learn more about regulation of hilA, we isolated Tn5 mutants exhibiting reduced hilA and/or invasion gene expression. In addition to expected mutations, we identified Tn5 insertions in pstS, fadD, flhD, flhC, and fliA. Analysis of the pstS mutant indicates that hilA and invasion genes are repressed by the response regulator PhoB in the absence of the Pst high-affinity inorganic phosphate uptake system. This system is required for negative control of the PhoR-PhoB two-component regulatory system, suggesting that hilA expression may be repressed by PhoR-PhoB under low extracellular inorganic phosphate conditions. FadD is required for uptake and degradation of long-chain fatty acids, and our analysis of the fadD mutant indicates that hilA is regulated by a FadD-dependent, FadR-independent mechanism. Thus, fatty acid derivatives may act as intracellular signals to regulate hilA expression. flhDC and fliA encode transcription factors required for flagellum production, motility, and chemotaxis. Complementation studies with flhC and fliA mutants indicate that FliZ, which is encoded in an operon with fliA, activates expression of hilA, linking regulation of hilA with motility. Finally, epistasis tests showed that PhoB, FadD, FliZ, SirA, and EnvZ act independently to regulate hilA expression and invasion. In summary, our screen has identified several distinct pathways that can modulate S. enterica serovar Typhimurium's ability to express hilA and invade host cells. Integration of signals from these different pathways may help restrict invasion gene expression during infection.

* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, Harvard Medical School, 200 Longwood Ave., Boston, MA 02115. Phone: (617) 432-4988. Fax: (617) 738-7664. E-mail: clee{at}hms.harvard.edu.

Journal of Bacteriology, April 2000, p. 1872-1882, Vol. 182, No. 7
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Cheng, C., Tennant, S. M., Azzopardi, K. I., Bennett-Wood, V., Hartland, E. L., Robins-Browne, R. M., Tauschek, M. (2009). Contribution of the pst-phoU Operon to Cell Adherence by Atypical Enteropathogenic Escherichia coli and Virulence of Citrobacter rodentium. Infect. Immun. 77: 1936-1944 [Abstract] [Full Text]  
  • O'May, G. A., Jacobsen, S. M., Longwell, M., Stoodley, P., Mobley, H. L. T., Shirtliff, M. E. (2009). The high-affinity phosphate transporter Pst in Proteus mirabilis HI4320 and its importance in biofilm formation. Microbiology 155: 1523-1535 [Abstract] [Full Text]  
  • Harriff, M. J., Danelishvili, L., Wu, M., Wilder, C., McNamara, M., Kent, M. L., Bermudez, L. E. (2009). Mycobacterium avium Genes MAV_5138 and MAV_3679 Are Transcriptional Regulators That Play a Role in Invasion of Epithelial Cells, in Part by Their Regulation of CipA, a Putative Surface Protein Interacting with Host Cell Signaling Pathways. J. Bacteriol. 191: 1132-1142 [Abstract] [Full Text]  
  • Baek, C.-H., Wang, S., Roland, K. L., Curtiss, R. III (2009). Leucine-Responsive Regulatory Protein (Lrp) Acts as a Virulence Repressor in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 191: 1278-1292 [Abstract] [Full Text]  
  • Matsui, M., Takaya, A., Yamamoto, T. (2008). {sigma}32-Mediated Negative Regulation of Salmonella Pathogenicity Island 1 Expression. J. Bacteriol. 190: 6636-6645 [Abstract] [Full Text]  
  • Saini, S., Brown, J. D., Aldridge, P. D., Rao, C. V. (2008). FliZ Is a Posttranslational Activator of FlhD4C2-Dependent Flagellar Gene Expression. J. Bacteriol. 190: 4979-4988 [Abstract] [Full Text]  
  • Bishop, A., House, D., Perkins, T., Baker, S., Kingsley, R. A., Dougan, G. (2008). Interaction of Salmonella enterica serovar Typhi with cultured epithelial cells: roles of surface structures in adhesion and invasion. Microbiology 154: 1914-1926 [Abstract] [Full Text]  
  • Mizusaki, H., Takaya, A., Yamamoto, T., Aizawa, S.-I. (2008). Signal Pathway in Salt-Activated Expression of the Salmonella Pathogenicity Island 1 Type III Secretion System in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 190: 4624-4631 [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]  
  • Field, T. R., Layton, A. N., Bispham, J., Stevens, M. P., Galyov, E. E. (2008). Identification of Novel Genes and Pathways Affecting Salmonella Type III Secretion System 1 Using a Contact-Dependent Hemolysis Assay. J. Bacteriol. 190: 3393-3398 [Abstract] [Full Text]  
  • Li, G., Ewers, C., Laturnus, C., Diehl, I., Alt, K., Dai, J., Antao, E.-M., Schnetz, K., Wieler, L. H. (2008). Characterization of a yjjQ mutant of avian pathogenic Escherichia coli (APEC). Microbiology 154: 1082-1093 [Abstract] [Full Text]  
  • Kage, H., Takaya, A., Ohya, M., Yamamoto, T. (2008). Coordinated Regulation of Expression of Salmonella Pathogenicity Island 1 and Flagellar Type III Secretion Systems by ATP-Dependent ClpXP Protease. J. Bacteriol. 190: 2470-2478 [Abstract] [Full Text]  
  • Lin, D., Rao, C. V., Slauch, J. M. (2008). The Salmonella SPI1 Type Three Secretion System Responds to Periplasmic Disulfide Bond Status via the Flagellar Apparatus and the RcsCDB System. J. Bacteriol. 190: 87-97 [Abstract] [Full Text]  
  • Claret, L., Miquel, S., Vieille, N., Ryjenkov, D. A., Gomelsky, M., Darfeuille-Michaud, A. (2007). The Flagellar Sigma Factor FliA Regulates Adhesion and Invasion of Crohn Disease-associated Escherichia coli via a Cyclic Dimeric GMP-dependent Pathway. J. Biol. Chem. 282: 33275-33283 [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]  
  • 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]  
  • Soscia, C., Hachani, A., Bernadac, A., Filloux, A., Bleves, S. (2007). Cross Talk between Type III Secretion and Flagellar Assembly Systems in Pseudomonas aeruginosa. J. Bacteriol. 189: 3124-3132 [Abstract] [Full Text]  
  • Lim, S., Yun, J., Yoon, H., Park, C., Kim, B., Jeon, B., Kim, D., Ryu, S. (2007). Mlc regulation of Salmonella pathogenicity island I gene expression via hilE repression. Nucleic Acids Res 35: 1822-1832 [Abstract] [Full Text]  
  • Fink, R. C., Evans, M. R., Porwollik, S., Vazquez-Torres, A., Jones-Carson, J., Troxell, B., Libby, S. J., McClelland, M., Hassan, H. M. (2007). FNR Is a Global Regulator of Virulence and Anaerobic Metabolism in Salmonella enterica Serovar Typhimurium (ATCC 14028s). J. Bacteriol. 189: 2262-2273 [Abstract] [Full Text]  
  • Iyoda, S., Koizumi, N., Satou, H., Lu, Y., Saitoh, T., Ohnishi, M., Watanabe, H. (2006). The GrlR-GrlA Regulatory System Coordinately Controls the Expression of Flagellar and LEE-Encoded Type III Protein Secretion Systems in Enterohemorrhagic Escherichia coli.. J. Bacteriol. 188: 5682-5692 [Abstract] [Full Text]  
  • Nakayama, S.-i., Watanabe, H. (2006). Mechanism of hilA Repression by 1,2-Propanediol Consists of Two Distinct Pathways, One Dependent on and the Other Independent of Catabolic Production of Propionate, in Salmonella enterica Serovar Typhimurium.. J. Bacteriol. 188: 3121-3125 [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]  
  • Merighi, M., Carroll-Portillo, A., Septer, A. N., Bhatiya, A., Gunn, J. S. (2006). Role of Salmonella enterica Serovar Typhimurium Two-Component System PreA/PreB in Modulating PmrA-Regulated Gene Transcription. J. Bacteriol. 188: 141-149 [Abstract] [Full Text]  
  • Buckles, E. L., Wang, X., Lockatell, C. V., Johnson, D. E., Donnenberg, M. S. (2006). PhoU enhances the ability of extraintestinal pathogenic Escherichia coli strain CFT073 to colonize the murine urinary tract. Microbiology 152: 153-160 [Abstract] [Full Text]  
  • Ku, Y.-W., McDonough, S. P., Palaniappan, R. U. M., Chang, C.-F., Chang, Y.-F. (2005). Novel Attenuated Salmonella enterica Serovar Choleraesuis Strains as Live Vaccine Candidates Generated by Signature-Tagged Mutagenesis. Infect. Immun. 73: 8194-8203 [Abstract] [Full Text]  
  • Zheng, J., Tung, S. L., Leung, K. Y. (2005). Regulation of a Type III and a Putative Secretion System in Edwardsiella tarda by EsrC Is under the Control of a Two-Component System, EsrA-EsrB. Infect. Immun. 73: 4127-4137 [Abstract] [Full Text]  
  • Miltner, E., Daroogheh, K., Mehta, P. K., Cirillo, S. L. G., Cirillo, J. D., Bermudez, L. E. (2005). Identification of Mycobacterium avium Genes That Affect Invasion of the Intestinal Epithelium. Infect. Immun. 73: 4214-4221 [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]  
  • John, M., Kudva, I. T., Griffin, R. W., Dodson, A. W., McManus, B., Krastins, B., Sarracino, D., Progulske-Fox, A., Hillman, J. D., Handfield, M., Tarr, P. I., Calderwood, S. B. (2005). Use of In Vivo-Induced Antigen Technology for Identification of Escherichia coli O157:H7 Proteins Expressed during Human Infection. Infect. Immun. 73: 2665-2679 [Abstract] [Full Text]  
  • Baxter, M. A., Jones, B. D. (2005). The fimYZ Genes Regulate Salmonella enterica Serovar Typhimurium Invasion in Addition to Type 1 Fimbrial Expression and Bacterial Motility. Infect. Immun. 73: 1377-1385 [Abstract] [Full Text]  
  • Liaw, S.-J., Lai, H.-C., Wang, W.-B. (2004). Modulation of Swarming and Virulence by Fatty Acids through the RsbA Protein in Proteus mirabilis. Infect. Immun. 72: 6836-6845 [Abstract] [Full Text]  
  • Huang, F.-C., Werne, A., Li, Q., Galyov, E. E., Walker, W. A., Cherayil, B. J. (2004). Cooperative Interactions between Flagellin and SopE2 in the Epithelial Interleukin-8 Response to Salmonella enterica Serovar Typhimurium Infection. Infect. Immun. 72: 5052-5062 [Abstract] [Full Text]  
  • Hisert, K. B., Kirksey, M. A., Gomez, J. E., Sousa, A. O., Cox, J. S., Jacobs, W. R. Jr., Nathan, C. F., McKinney, J. D. (2004). Identification of Mycobacterium tuberculosis Counterimmune (cim) Mutants in Immunodeficient Mice by Differential Screening. Infect. Immun. 72: 5315-5321 [Abstract] [Full Text]  
  • Kelly, A., Goldberg, M. D., Carroll, R. K., Danino, V., Hinton, J. C. D., 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 [Abstract] [Full Text]  
  • Lux, R., Shi, W. (2004). CHEMOTAXIS-GUIDED MOVEMENTS IN BACTERIA. CROBM 15: 207-220 [Abstract] [Full Text]  
  • Rietsch, A., Wolfgang, M. C., Mekalanos, J. J. (2004). Effect of Metabolic Imbalance on Expression of Type III Secretion Genes in Pseudomonas aeruginosa. Infect. Immun. 72: 1383-1390 [Abstract] [Full Text]  
  • Ewann, F., Locht, C., Supply, P. (2004). Intracellular autoregulation of the Mycobacterium tuberculosis PrrA response regulator. Microbiology 150: 241-246 [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]  
  • Nakayama, S.-i., Kushiro, A., Asahara, T., Tanaka, R.-i., Hu, L., Kopecko, D. J., Watanabe, H. (2003). Activation of hilA expression at low pH requires the signal sensor CpxA, but not the cognate response regulator CpxR, in Salmonella enterica serovar Typhimurium. Microbiology 149: 2809-2817 [Abstract] [Full Text]  
  • Black, P. N., DiRusso, C. C. (2003). Transmembrane Movement of Exogenous Long-Chain Fatty Acids: Proteins, Enzymes, and Vectorial Esterification. Microbiol. Mol. Biol. Rev. 67: 454-472 [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]  
  • Baxter, M. A., Fahlen, T. F., Wilson, R. L., Jones, B. D. (2003). HilE Interacts with HilD and Negatively Regulates hilA Transcription and Expression of the Salmonella enterica Serovar Typhimurium Invasive Phenotype. Infect. Immun. 71: 1295-1305 [Abstract] [Full Text]  
  • Srinivasa Rao, P. S., Lim, T. M., Leung, K. Y. (2003). Functional Genomics Approach to the Identification of Virulence Genes Involved in Edwardsiella tarda Pathogenesis. Infect. Immun. 71: 1343-1351 [Abstract] [Full Text]  
  • Takaya, A., Suzuki, M., Matsui, H., Tomoyasu, T., Sashinami, H., Nakane, A., Yamamoto, T. (2003). Lon, a Stress-Induced ATP-Dependent Protease, Is Critically Important for Systemic Salmonella enterica Serovar Typhimurium Infection of Mice. Infect. Immun. 71: 690-696 [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]  
  • Dozois, C. M., Daigle, F., Curtiss, R. III (2003). Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. USA 100: 247-252 [Abstract] [Full Text]  
  • Howard, M. B., Hutcheson, S. W. (2003). Growth Dynamics of Salmonella enterica Strains on Alfalfa Sprouts and in Waste Seed Irrigation Water. Appl. Environ. Microbiol. 69: 548-553 [Abstract] [Full Text]  
  • Zaharik, M. L., Vallance, B. A., Puente, J. L., Gros, P., Finlay, B. B. (2002). Host-pathogen interactions: Host resistance factor Nramp1 up-regulates the expression of Salmonella pathogenicity island-2 virulence genes. Proc. Natl. Acad. Sci. USA 99: 15705-15710 [Abstract] [Full Text]  
  • Banchio, C., Gramajo, H. (2002). A Stationary-Phase Acyl-Coenzyme A Synthetase of Streptomyces coelicolor A3(2) Is Necessary for the Normal Onset of Antibiotic Production. Appl. Environ. Microbiol. 68: 4240-4246 [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]  
  • Fraser, G. M., Claret, L., Furness, R., Gupta, S., Hughes, C. (2002). Swarming-coupled expression of the Proteus mirabilis hpmBA haemolysin operon. Microbiology 148: 2191-2201 [Abstract] [Full Text]  
  • Bleves, S., Marenne, M.-N., Detry, G., Cornelis, G. R. (2002). Up-Regulation of the Yersinia enterocolitica yop Regulon by Deletion of the Flagellum Master Operon flhDC. J. Bacteriol. 184: 3214-3223 [Abstract] [Full Text]  
  • Millikan, D. S., Ruby, E. G. (2002). Alterations in Vibrio fischeri Motility Correlate with a Delay in Symbiosis Initiation and Are Associated with Additional Symbiotic Colonization Defects. Appl. Environ. Microbiol. 68: 2519-2528 [Abstract] [Full Text]  
  • Tomich, M., Herfst, C. A., Golden, J. W., Mohr, C. D. (2002). Role of Flagella in Host Cell Invasion by Burkholderia cepacia. Infect. Immun. 70: 1799-1806 [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]  
  • Fahlen, T. F., Wilson, R. L., Boddicker, J. D., Jones, B. D. (2001). Hha Is a Negative Modulator of Transcription of hilA, the Salmonella enterica Serovar Typhimurium Invasion Gene Transcriptional Activator. J. Bacteriol. 183: 6620-6629 [Abstract] [Full Text]  
  • Schmitt, C. K., Ikeda, J. S., Darnell, S. C., Watson, P. R., Bispham, J., Wallis, T. S., Weinstein, D. L., Metcalf, E. S., 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 [Abstract] [Full Text]  
  • Rao, P. S. S., Lim, T. M., Leung, K. Y. (2001). Opsonized Virulent Edwardsiella tarda Strains Are Able To Adhere to and Survive and Replicate within Fish Phagocytes but Fail To Stimulate Reactive Oxygen Intermediates. Infect. Immun. 69: 5689-5697 [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]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»