Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression
Abstract
The extracytoplasmic functioning sigma factor σE is known to play an essential role for Salmonella enterica serovar Typhimurium to survive and proliferate in macrophages and mice. However, its regulatory network is not well characterized, especially during infection. Here we used microarray to identify genes regulated by σE in Salmonella grown in three conditions: a nutrient-rich condition and two others that mimic early and late intracellular infection. We found that in each condition σE regulated different sets of genes, and notably, several global regulators. When comparing nutrient-rich and infection-like conditions, large changes were observed in the expression of genes involved in Salmonella pathogenesis island (SPI)-1 type-three secretion system (TTSS), SPI-2 TTSS, protein synthesis, and stress responses. In total, the expression of 58% of Salmonella genes was affected by σE in at least one of the three conditions. An important finding is that σE up-regulates SPI-2 genes, which are essential for Salmonella intracellular survival, by up-regulating SPI-2 activator ssrB expression at the early stage of infection and down-regulating SPI-2 repressor hns expression at a later stage. Moreover, σE is capable of countering the silencing of H-NS, releasing the expression of SPI-2 genes. This connection between σE and SPI-2 genes, combined with themore »
- Authors:
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1184934
- Report Number(s):
- PNNL-SA-101010
Journal ID: ISSN 1664-302X
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Salmonella Typhimurium; bacterial pathogenesis; systems biology; transcriptomics; regulatory network; bioinformatics; computational biology
Citation Formats
Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, and Adkins, Joshua N. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. United States: N. p., 2015.
Web. doi:10.3389/fmicb.2015.00027.
Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, & Adkins, Joshua N. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. United States. https://doi.org/10.3389/fmicb.2015.00027
Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, and Adkins, Joshua N. Tue .
"Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression". United States. https://doi.org/10.3389/fmicb.2015.00027. https://www.osti.gov/servlets/purl/1184934.
@article{osti_1184934,
title = {Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression},
author = {Li, Jie and Overall, Christopher C. and Nakayasu, Ernesto S. and Kidwai, Afshan S. and Jones, Marcus B. and Johnson, Rudd and Nguyen, Nhu T. and McDermott, Jason E. and Ansong, Charles and Heffron, Fred and Cambronne, Eric and Adkins, Joshua N.},
abstractNote = {The extracytoplasmic functioning sigma factor σE is known to play an essential role for Salmonella enterica serovar Typhimurium to survive and proliferate in macrophages and mice. However, its regulatory network is not well characterized, especially during infection. Here we used microarray to identify genes regulated by σE in Salmonella grown in three conditions: a nutrient-rich condition and two others that mimic early and late intracellular infection. We found that in each condition σE regulated different sets of genes, and notably, several global regulators. When comparing nutrient-rich and infection-like conditions, large changes were observed in the expression of genes involved in Salmonella pathogenesis island (SPI)-1 type-three secretion system (TTSS), SPI-2 TTSS, protein synthesis, and stress responses. In total, the expression of 58% of Salmonella genes was affected by σE in at least one of the three conditions. An important finding is that σE up-regulates SPI-2 genes, which are essential for Salmonella intracellular survival, by up-regulating SPI-2 activator ssrB expression at the early stage of infection and down-regulating SPI-2 repressor hns expression at a later stage. Moreover, σE is capable of countering the silencing of H-NS, releasing the expression of SPI-2 genes. This connection between σE and SPI-2 genes, combined with the global regulatory effect of σE, may account for the lethality of rpoE-deficient Salmonella in murine infection.},
doi = {10.3389/fmicb.2015.00027},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Tue Feb 10 00:00:00 EST 2015},
month = {Tue Feb 10 00:00:00 EST 2015}
}
Web of Science
Works referenced in this record:
Role of the Two-Component Regulator CpxAR in the Virulence of Salmonella enterica Serotype Typhimurium
journal, August 2004
- Humphreys, Sue; Rowley, Gary; Stevenson, Andrew
- Infection and Immunity, Vol. 72, Issue 8
Salmonella enterica Response Regulator SsrB Relieves H-NS Silencing by Displacing H-NS Bound in Polymerization Mode and Directly Activates Transcription
journal, November 2010
- Walthers, Don; Li, You; Liu, Yingjie
- Journal of Biological Chemistry, Vol. 286, Issue 3
Escherichia coli RNA Polymerase Recognition of a σ70-Dependent Promoter Requiring a −35 DNA Element and an Extended −10 TGn Motif
journal, September 2006
- Hook-Barnard, India; Johnson, Xanthia B.; Hinton, Deborah M.
- Journal of Bacteriology, Vol. 188, Issue 24
Conserved and Variable Functions of the σE Stress Response in Related Genomes
journal, December 2005
- Rhodius, Virgil A.; Suh, Won Chul; Nonaka, Gen
- PLoS Biology, Vol. 4, Issue 1
limma: Linear Models for Microarray Data
book, January 2005
- Smyth, G. K.
- Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Identification of the E regulon of Salmonella enterica serovar Typhimurium
journal, May 2006
- Skovierova, H.
- Microbiology, Vol. 152, Issue 5
Selective Silencing of Foreign DNA with Low GC Content by the H-NS Protein in Salmonella
journal, July 2006
- Navarre, W. W.
- Science, Vol. 313, Issue 5784
Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA
journal, October 2005
- Udekwu, K. I.
- Genes & Development, Vol. 19, Issue 19
The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium: Phage shock protein A in Salmonella
journal, September 2010
- Karlinsey, Joyce E.; Maguire, Michael E.; Becker, Lynne A.
- Molecular Microbiology, Vol. 78, Issue 3
The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS
journal, July 2007
- Walthers, Don; Carroll, Ronan K.; Navarre, William Wiley
- Molecular Microbiology, Vol. 65, Issue 2
Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2: SsrA and SsrB regulation are uncoupled
journal, May 2003
- Feng, Xiuhong; Oropeza, Ricardo; Kenney, Linda J.
- Molecular Microbiology, Vol. 48, Issue 4
Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock
journal, January 2007
- McMeechan, Alisdair; Roberts, Mark; Cogan, Tristan A.
- Microbiology, Vol. 153, Issue 1
The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways
journal, August 1997
- Connolly, L.; Penas, A. D. L.; Alba, B. M.
- Genes & Development, Vol. 11, Issue 15
Characterization of the Escherichia coli ς E Regulon
journal, March 2001
- Dartigalongue, Claire; Missiakas, Dominique; Raina, Satish
- Journal of Biological Chemistry, Vol. 276, Issue 24
The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica: SPI-2 regulation by the PhoP/PhoQ system
journal, May 2005
- Bijlsma, Jetta J. E.; Groisman, Eduardo A.
- Molecular Microbiology, Vol. 57, Issue 1
A connecter-like factor, CacA, links RssB/RpoS and the CpxR/CpxA two-component system in Salmonella
journal, January 2012
- Kato, Akinori; Hayashi, Hironori; Nomura, Wataru
- BMC Microbiology, Vol. 12, Issue 1
Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes.
journal, November 1992
- Alpuche Aranda, C. M.; Swanson, J. A.; Loomis, W. P.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 21
The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins.
journal, December 1993
- Mecsas, J.; Rouviere, P. E.; Erickson, J. W.
- Genes & Development, Vol. 7, Issue 12b
New insights into transcriptional regulation by H-NS
journal, April 2008
- Fang, Ferric C.; Rimsky, Sylvie
- Current Opinion in Microbiology, Vol. 11, Issue 2
The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium
journal, April 2012
- Kroger, C.; Dillon, S. C.; Cameron, A. D. S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 20
Regulation of Escherichia coli hchA, a stress-inducible gene encoding molecular chaperone Hsp31
journal, June 2006
- Mujacic, Mirna; Baneyx, Francois
- Molecular Microbiology, Vol. 60, Issue 6
The molecular basis of selective promoter activation by the ? S subunit of RNA polymerase
journal, March 2007
- Typas, Athanasios; Becker, Gisela; Hengge, Regine
- Molecular Microbiology, Vol. 63, Issue 5
The Alternative Sigma Factor, ςE, Is Critically Important for the Virulence of Salmonella typhimurium
journal, April 1999
- Humphreys, Sue; Stevenson, Andrew; Bacon, Andrew
- Infection and Immunity, Vol. 67, Issue 4
TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003
- Saeed, A. I.; Sharov, V.; White, J.
- BioTechniques, Vol. 34, Issue 2
The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011
- Battesti, Aurelia; Majdalani, Nadim; Gottesman, Susan
- Annual Review of Microbiology, Vol. 65, Issue 1
Acid stress activation of the σ E stress response in Salmonella enterica serovar Typhimurium
journal, March 2009
- Muller, Cécile; Bang, Iel-Soo; Velayudhan, Jyoti
- Molecular Microbiology, Vol. 71, Issue 5
Signal Transduction and Regulatory Mechanisms Involved in Control of the σS (RpoS) Subunit of RNA Polymerase
journal, September 2002
- Hengge-Aronis, Regine
- Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3
Discovery of Novel Secreted Virulence Factors from Salmonella enterica Serovar Typhimurium by Proteomic Analysis of Culture Supernatants
journal, October 2010
- Niemann, George S.; Brown, Roslyn N.; Gustin, Jean K.
- Infection and Immunity, Vol. 79, Issue 1
The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions
journal, January 2002
- Kenyon, William J.; Sayers, D. Geary; Humphreys, Sue
- Microbiology, Vol. 148, Issue 1
The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium
journal, January 2007
- Sittka, Alexandra; Pfeiffer, Verena; Tedin, Karsten
- Molecular Microbiology, Vol. 63, Issue 1
Global Systems-Level Analysis of Hfq and SmpB Deletion Mutants in Salmonella: Implications for Virulence and Global Protein Translation
journal, March 2009
- Ansong, Charles; Yoon, Hyunjin; Porwollik, Steffen
- PLoS ONE, Vol. 4, Issue 3
Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica
journal, February 2008
- Perez, J. Christian; Latifi, Tammy; Groisman, Eduardo A.
- Journal of Biological Chemistry, Vol. 283, Issue 16
The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium
journal, January 2007
- Sittka, Alexandra; Pfeiffer, Verena; Tedin, Karsten
- Molecular Microbiology, Vol. 63, Issue 1
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
journal, January 2004
- Smyth, Gordon K.
- Statistical Applications in Genetics and Molecular Biology, Vol. 3, Issue 1
OmpR Regulates the Two-Component System SsrA-SsrB in Salmonella Pathogenicity Island 2
journal, February 2000
- Lee, A. K.; Detweiler, C. S.; Falkow, S.
- Journal of Bacteriology, Vol. 182, Issue 3
The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011
- Battesti, Aurelia; Majdalani, Nadim; Gottesman, Susan
- Annual Review of Microbiology, Vol. 65, Issue 1
Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium
journal, February 2009
- Yoon, Hyunjin; McDermott, Jason E.; Porwollik, Steffen
- PLoS Pathogens, Vol. 5, Issue 2
The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS
journal, July 2007
- Walthers, Don; Carroll, Ronan K.; Navarre, William Wiley
- Molecular Microbiology, Vol. 65, Issue 2
Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon
journal, July 2011
- Gogol, E. B.; Rhodius, V. A.; Papenfort, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 31
Cell lysis directed by σ E in early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli
journal, August 2005
- Kabir, Md. Shahinur; Yamashita, Daisuke; Koyama, Satoshi
- Microbiology, Vol. 151, Issue 8
Regulation of Alternative Sigma Factor Use
journal, October 2011
- Österberg, Sofia; Peso-Santos, Teresa del; Shingler, Victoria
- Annual Review of Microbiology, Vol. 65, Issue 1
New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH
journal, August 1996
- Missiakas, Dominique; Betton, Jean-Michel; Raina, Satish
- Molecular Microbiology, Vol. 21, Issue 4
Alternative sigma factor interactions in Salmonella : σ E and σ H promote antioxidant defences by enhancing σ S levels: Alternative sigma factor interactions
journal, March 2005
- Bang, Iel-Soo; Frye, Jonathan G.; McClelland, Michael
- Molecular Microbiology, Vol. 56, Issue 3
Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts
journal, May 2008
- Cho, B. -K.; Knight, E. M.; Barrett, C. L.
- Genome Research, Vol. 18, Issue 6
The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system
journal, September 2003
- Garmendia, J.
- Microbiology, Vol. 149, Issue 9
Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium: Compensatory role of PspA in rpoE mutant Salmonella
journal, March 2005
- Becker, Lynne A.; Bang, Iel-Soo; Crouch, Marie-Laure
- Molecular Microbiology, Vol. 56, Issue 4
DNA looping-mediated repression by histone-like protein H-NS: specific requirement of E 70 as a cofactor for looping
journal, October 2005
- Shin, M.
- Genes & Development, Vol. 19, Issue 19
SipA, SopA, SopB, SopD, and SopE2 Contribute to Salmonella enterica Serotype Typhimurium Invasion of Epithelial Cells
journal, January 2005
- Raffatellu, Manuela; Wilson, R. Paul; Chessa, Daniela
- Infection and Immunity, Vol. 73, Issue 1
RpoE fine tunes expression of a subset of SsrB-regulated virulence factors in Salmonella enterica serovar Typhimurium
journal, January 2009
- Osborne, Suzanne E.; Coombes, Brian K.
- BMC Microbiology, Vol. 9, Issue 1
ChIP-Seq and the Complexity of Bacterial Transcriptional Regulation
book, January 2012
- Galagan, James; Lyubetskaya, Anna; Gomes, Antonio
- Systems Biology
The alternative sigma factor σ E is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides: rpoE is required for Salmonella resistance to anti-microbial peptides
journal, March 2005
- Crouch, Marie-Laure; Becker, Lynne A.; Bang, Iel-Soo
- Molecular Microbiology, Vol. 56, Issue 3
The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways
journal, August 1997
- Connolly, L.; Penas, A. D. L.; Alba, B. M.
- Genes & Development, Vol. 11, Issue 15
Selective Silencing of Foreign DNA with Low GC Content by the H-NS Protein in Salmonella
journal, July 2006
- Navarre, W. W.
- Science, Vol. 313, Issue 5784
Identification of the E regulon of Salmonella enterica serovar Typhimurium
journal, May 2006
- Skovierova, H.
- Microbiology, Vol. 152, Issue 5
Role of the alternative sigma factors σ E and σ S in survival of Salmonella enterica serovar Typhimurium during starvation, refrigeration and osmotic shock
journal, January 2007
- McMeechan, Alisdair; Roberts, Mark; Cogan, Tristan A.
- Microbiology, Vol. 153, Issue 1
The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system
journal, September 2003
- Garmendia, J.
- Microbiology, Vol. 149, Issue 9
The molecular basis of selective promoter activation by the ? S subunit of RNA polymerase
journal, March 2007
- Typas, Athanasios; Becker, Gisela; Hengge, Regine
- Molecular Microbiology, Vol. 63, Issue 5
Regulation of Escherichia coli hchA, a stress-inducible gene encoding molecular chaperone Hsp31
journal, June 2006
- Mujacic, Mirna; Baneyx, Francois
- Molecular Microbiology, Vol. 60, Issue 6
TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003
- Saeed, A. I.; Sharov, V.; White, J.
- BioTechniques, Vol. 34, Issue 2
DNA looping-mediated repression by histone-like protein H-NS: specific requirement of E 70 as a cofactor for looping
journal, October 2005
- Shin, M.
- Genes & Development, Vol. 19, Issue 19
Conserved and Variable Functions of the σE Stress Response in Related Genomes
journal, December 2005
- Rhodius, Virgil A.; Suh, Won Chul; Nonaka, Gen
- PLoS Biology, Vol. 4, Issue 1
Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium
journal, February 2009
- Yoon, Hyunjin; McDermott, Jason E.; Porwollik, Steffen
- PLoS Pathogens, Vol. 5, Issue 2
Regulon and promoter analysis of the E. coli heat-shock factor, σ 32 , reveals a multifaceted cellular response to heat stress
journal, July 2006
- Nonaka, Gen; Blankschien, Matthew; Herman, Christophe
- Genes & Development, Vol. 20, Issue 13
A connecter-like factor, CacA, links RssB/RpoS and the CpxR/CpxA two-component system in Salmonella
journal, January 2012
- Kato, Akinori; Hayashi, Hironori; Nomura, Wataru
- BMC Microbiology, Vol. 12, Issue 1
SigmaE is an essential sigma factor in Escherichia coli.
journal, January 1997
- De Las Peñas, A.; Connolly, L.; Gross, C. A.
- Journal of bacteriology, Vol. 179, Issue 21
Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes.
journal, November 1992
- Alpuche Aranda, C. M.; Swanson, J. A.; Loomis, W. P.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 21
Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens
journal, April 2006
- Rowley, Gary; Spector, Michael; Kormanec, Jan
- Nature Reviews Microbiology, Vol. 4, Issue 5
Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon
journal, July 2011
- Gogol, E. B.; Rhodius, V. A.; Papenfort, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 31
Regulation of Alternative Sigma Factor Use
journal, October 2011
- Österberg, Sofia; Peso-Santos, Teresa del; Shingler, Victoria
- Annual Review of Microbiology, Vol. 65, Issue 1
SseL Is a Salmonella-Specific Translocated Effector Integrated into the SsrB-Controlled Salmonella Pathogenicity Island 2 Type III Secretion System
journal, December 2006
- Coombes, B. K.; Lowden, M. J.; Bishop, J. L.
- Infection and Immunity, Vol. 75, Issue 2
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003
- Bolstad, B. M.; Irizarry, R. A.; Astrand, M.
- Bioinformatics, Vol. 19, Issue 2
New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH
journal, August 1996
- Missiakas, Dominique; Betton, Jean-Michel; Raina, Satish
- Molecular Microbiology, Vol. 21, Issue 4
The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica: SPI-2 regulation by the PhoP/PhoQ system
journal, May 2005
- Bijlsma, Jetta J. E.; Groisman, Eduardo A.
- Molecular Microbiology, Vol. 57, Issue 1
The σE and Cpx regulatory pathways: Overlapping but distinct envelope stress responses
journal, April 1999
- Raivio, Tracy L.; Silhavy, Thomas J.
- Current Opinion in Microbiology, Vol. 2, Issue 2
Bioconductor : open software development for computational biology and bioinformatics
text, January 2004
- C., Gentleman, Robert; J., Carey, Vincent; M., Bates, Douglas
- BioMed Central
? E -dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay
journal, December 2006
- Papenfort, Kai; Pfeiffer, Verena; Mika, Franziska
- Molecular Microbiology, Vol. 62, Issue 6
The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems
journal, November 1997
- Jones, C. H.
- The EMBO Journal, Vol. 16, Issue 21
The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems
journal, November 1997
- Jones, C. H.
- The EMBO Journal, Vol. 16, Issue 21
Deep Sequencing Analysis of Small Noncoding RNA and mRNA Targets of the Global Post-Transcriptional Regulator, Hfq
journal, August 2008
- Sittka, Alexandra; Lucchini, Sacha; Papenfort, Kai
- PLoS Genetics, Vol. 4, Issue 8
Hfq and its constellation of RNA
journal, August 2011
- Vogel, Jörg; Luisi, Ben F.
- Nature Reviews Microbiology, Vol. 9, Issue 8
Acid stress activation of the σ E stress response in Salmonella enterica serovar Typhimurium
journal, March 2009
- Muller, Cécile; Bang, Iel-Soo; Velayudhan, Jyoti
- Molecular Microbiology, Vol. 71, Issue 5
? E -dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay
journal, December 2006
- Papenfort, Kai; Pfeiffer, Verena; Mika, Franziska
- Molecular Microbiology, Vol. 62, Issue 6
Identification of amino acid residues of Salmonella SlyA that are critical for transcriptional regulation
journal, February 2007
- Okada, N.; Oi, Y.; Takeda-Shitaka, M.
- Microbiology, Vol. 153, Issue 2
The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions
journal, January 2002
- Kenyon, William J.; Sayers, D. Geary; Humphreys, Sue
- Microbiology, Vol. 148, Issue 1
Alternative sigma factor interactions in Salmonella : σ E and σ H promote antioxidant defences by enhancing σ S levels: Alternative sigma factor interactions
journal, March 2005
- Bang, Iel-Soo; Frye, Jonathan G.; McClelland, Michael
- Molecular Microbiology, Vol. 56, Issue 3
Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts
journal, May 2008
- Cho, B. -K.; Knight, E. M.; Barrett, C. L.
- Genome Research, Vol. 18, Issue 6
Global Systems-Level Analysis of Hfq and SmpB Deletion Mutants in Salmonella: Implications for Virulence and Global Protein Translation
journal, March 2009
- Ansong, Charles; Yoon, Hyunjin; Porwollik, Steffen
- PLoS ONE, Vol. 4, Issue 3
Cell lysis directed by σ E in early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli
journal, August 2005
- Kabir, Md. Shahinur; Yamashita, Daisuke; Koyama, Satoshi
- Microbiology, Vol. 151, Issue 8
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003
- Bolstad, B. M.; Irizarry, R. A.; Astrand, M.
- Bioinformatics, Vol. 19, Issue 2
Regulon and promoter analysis of the E. coli heat-shock factor, σ 32 , reveals a multifaceted cellular response to heat stress
journal, July 2006
- Nonaka, Gen; Blankschien, Matthew; Herman, Christophe
- Genes & Development, Vol. 20, Issue 13
New insights into transcriptional regulation by H-NS
journal, April 2008
- Fang, Ferric C.; Rimsky, Sylvie
- Current Opinion in Microbiology, Vol. 11, Issue 2
New members of the Escherichia coli Ï E regulon identified by a two-plasmid system
journal, August 2003
- Rezuchova, Bronislava; Miticka, Henrieta; Homerova, Dagmar
- FEMS Microbiology Letters, Vol. 225, Issue 1
Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2: SsrA and SsrB regulation are uncoupled
journal, May 2003
- Feng, Xiuhong; Oropeza, Ricardo; Kenney, Linda J.
- Molecular Microbiology, Vol. 48, Issue 4
Transcriptional analysis of the rpoE gene encoding extracytoplasmic stress response sigma factor Ï E in Salmonella enterica serovar Typhimurium
journal, September 2003
- Miticka, Henrieta; Rowley, Gary; Rezuchova, Bronislava
- FEMS Microbiology Letters, Vol. 226, Issue 2
Bioconductor: open software development for computational biology and bioinformatics
journal, September 2004
- Gentleman, Robert C.; Carey, Vincent J.; Bates, Douglas M.
- Genome Biology, Vol. 5, Issue 10, p. R80
The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium
journal, April 2012
- Kroger, C.; Dillon, S. C.; Cameron, A. D. S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 20
Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens
journal, April 2006
- Rowley, Gary; Spector, Michael; Kormanec, Jan
- Nature Reviews Microbiology, Vol. 4, Issue 5
SigmaE is an essential sigma factor in Escherichia coli.
journal, January 1997
- De Las Peñas, A.; Connolly, L.; Gross, C. A.
- Journal of bacteriology, Vol. 179, Issue 21
Purification and Properties of C55-Isoprenoid Alcohol Phosphokinase from Staphylococcus aureus
journal, August 1972
- Sandermann, Heinrich; Strominger, Jack L.
- Journal of Biological Chemistry, Vol. 247, Issue 16
Works referencing / citing this record:
ChIP-Seq Analysis of the σE Regulon of Salmonella enterica Serovar Typhimurium Reveals New Genes Implicated in Heat Shock and Oxidative Stress Response
journal, September 2015
- Li, Jie; Overall, Christopher C.; Johnson, Rudd C.
- PLOS ONE, Vol. 10, Issue 9
Preliminary Transcriptome Analysis of Mature Biofilm and Planktonic Cells of Salmonella Enteritidis Exposure to Acid Stress
journal, September 2017
- Jia, Kun; Wang, Guangyu; Liang, Lijiao
- Frontiers in Microbiology, Vol. 8
Combination of berberine and ciprofloxacin reduces multi-resistant Salmonella strain biofilm formation by depressing mRNA expressions of luxS, rpoE, and ompR
journal, January 2018
- Shi, Chenxi; Li, Minmin; Muhammad, Ishfaq
- Journal of Veterinary Science, Vol. 19, Issue 6
Preliminary Transcriptome Analysis of Mature Biofilm and Planktonic Cells of Salmonella Enteritidis Exposure to Acid Stress
journal, September 2017
- Jia, Kun; Wang, Guangyu; Liang, Lijiao
- Frontiers in Microbiology, Vol. 8
HldE Is Important for Virulence Phenotypes in Enterotoxigenic Escherichia coli
journal, August 2018
- Maigaard Hermansen, Grith M.; Boysen, Anders; Krogh, Thøger J.
- Frontiers in Cellular and Infection Microbiology, Vol. 8