Francisella novicida Two-Component System Response Regulator BfpR Modulates iglC Gene Expression, Antimicrobial Peptide Resistance, and Biofilm Production

Dean, Scott N.; Milton, Morgan E.; Cavanagh, John; van Hoek, Monique L.

doi:10.3389/fcimb.2020.00082

Title: Francisella novicida Two-Component System Response Regulator BfpR Modulates iglC Gene Expression, Antimicrobial Peptide Resistance, and Biofilm Production

Journal Article · Fri Mar 13 00:00:00 EDT 2020 · Frontiers in Cellular and Infection Microbiology

DOI:https://doi.org/10.3389/fcimb.2020.00082· OSTI ID:1729718

Dean, Scott N. ^[1]; Milton, Morgan E. ^[2]; Cavanagh, John ^[2]; van Hoek, Monique L. ^[1]

George Mason Univ., Manassas, VA (United States)
East Carolina Univ., Greenville, NC (United States)

Response regulators are a critical part of the two-component system of gene expression regulation in bacteria, transferring a signal from a sensor kinase into DNA binding activity resulting in alteration of gene expression. In this study, we investigated a previously uncharacterized response regulator in Francisella novicida, FTN_1452 that we have named BfpR (Biofilm-regulating Francisella protein Regulator, FTN_1452). In contrast to another Francisella response regulator, QseB/PmrA, BfpR appears to be a negative regulator of biofilm production, and also a positive regulator of antimicrobial peptide resistance in this bacterium. The protein was crystallized and X-ray crystallography studies produced a 1.8 Å structure of the BfpR N-terminal receiver domain revealing interesting insight into its potential interaction with the sensor kinase. Structural analysis of BfpR places it in the OmpR/PhoP family of bacterial response regulators along with WalR and ResD. Proteomic and transcriptomic analyses suggest that BfpR overexpression affects expression of the critical Francisella virulence factor iglC, as well as other proteins in the bacterium. We demonstrate that mutation of bfpR is associated with an antimicrobial peptide resistance phenotype, a phenotype also associated with other response regulators, for the human cathelicidin peptide LL-37 and a sheep antimicrobial peptide SMAP-29. F. novicida with mutated bfpR replicated better than WT in intracellular infection assays in human-derived macrophages suggesting that the down-regulation of iglC expression in bfpR mutant may enable this intracellular replication to occur. Response regulators have been shown to play important roles in the regulation of bacterial biofilm production. We demonstrate that F. novicida biofilm formation was highly increased in the bfpR mutant, corresponding to altered glycogen synthesis. Waxworm infection experiments suggest a role of BfpR as a negative modulator of iglC expression with de-repression by Mg²⁺. In this study, we find that the response regulator BfpR may be a negative regulator of biofilm formation, and a positive regulator of antimicrobial peptide resistance in F. novicida.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

OSTI ID:: 1729718

Journal Information:: Frontiers in Cellular and Infection Microbiology, Vol. 10, Issue 03, 2020; ISSN 2235-2988

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (91)

PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Azithromycin effectiveness against intracellular infections of Francisella Ahmad, Saira; Hunter, Lyman; Qin, Aiping BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-123	journal	January 2010
Antimicrobial and antibiofilm activity of cathelicidins and short, synthetic peptides against Francisella Amer, Lilian S.; Bishop, Barney M.; van Hoek, Monique L. Biochemical and Biophysical Research Communications, Vol. 396, Issue 2 https://doi.org/10.1016/j.bbrc.2010.04.073	journal	May 2010
Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain Aperis, G.; Burgwynfuchs, B.; Anderson, C. Microbes and Infection, Vol. 9, Issue 6 https://doi.org/10.1016/j.micinf.2007.02.016	journal	May 2007
Regulation of Virulence Gene Transcripts by the Francisella novicida Orphan Response Regulator PmrA: Role of Phosphorylation and Evidence of MglA/SspA Interaction Bell, Brian L.; Mohapatra, Nrusingh P.; Gunn, John S. Infection and Immunity, Vol. 78, Issue 5 https://doi.org/10.1128/IAI.00021-10	journal	March 2010
Evaluating protein structures determined by structural genomics consortia Bhattacharya, Aneerban; Tejero, Roberto; Montelione, Gaetano T. Proteins: Structure, Function, and Bioinformatics, Vol. 66, Issue 4 https://doi.org/10.1002/prot.21165	journal	December 2006
Receiver domain structure and function in response regulator proteins Bourret, Robert B. Current Opinion in Microbiology, Vol. 13, Issue 2 https://doi.org/10.1016/j.mib.2010.01.015	journal	April 2010
DPI-ELISA: a fast and versatile method to specify the binding of plant transcription factors to DNA in vitro Brand, Luise H.; Kirchler, Tobias; Hummel, Sabine Plant Methods, Vol. 6, Issue 1 https://doi.org/10.1186/1746-4811-6-25	journal	January 2010
Identification of MglA-Regulated Genes Reveals Novel Virulence Factors in Francisella tularensis Brotcke, Anna; Weiss, David S.; Kim, Charles C. Infection and Immunity, Vol. 74, Issue 12 https://doi.org/10.1128/IAI.01250-06	journal	September 2006
Comparative Proteomic Analysis of the PhoP Regulon in Salmonella enterica Serovar Typhi Versus Typhimurium Charles, Richelle C.; Harris, Jason B.; Chase, Michael R. PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0006994	journal	September 2009
Regulation of Francisella Tularensis Virulence Dai, Shipan; Mohapatra, Nrusingh P.; Schlesinger, Larry S. Frontiers in Microbiology, Vol. 1 https://doi.org/10.3389/fmicb.2010.00144	journal	January 2011
PePPER: a webserver for prediction of prokaryote promoter elements and regulons de Jong, Anne; Pietersma, Hilco; Cordes, Martijn BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-299	journal	January 2012
RelA regulates virulence and intracellular survival of Francisella novicida Dean, R. E.; Ireland, P. M.; Jordan, J. E. Microbiology, Vol. 155, Issue 12 https://doi.org/10.1099/mic.0.031021-0	journal	December 2009
Susceptibility of Pseudomonas aeruginosa Biofilm to Alpha-Helical Peptides: D-enantiomer of LL-37 Dean, Scott N.; Bishop, Barney M.; van Hoek, Monique L. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00128	journal	January 2011
Tularemia as a Biological Weapon: Medical and Public Health Management Dennis, David T.; Inglesby, Thomas V.; Henderson, Donald A. JAMA, Vol. 285, Issue 21 https://doi.org/10.1001/jama.285.21.2763	journal	June 2001
The Structure of the Biofilm-controlling Response Regulator BfmR from Acinetobacter baumannii Reveals Details of Its DNA-binding Mechanism Draughn, G. Logan; Milton, Morgan E.; Feldmann, Erik A. Journal of Molecular Biology, Vol. 430, Issue 6 https://doi.org/10.1016/j.jmb.2018.02.002	journal	March 2018
Francisella novicida Forms In Vitro Biofilms Mediated by an Orphan Response Regulator Durham-Colleran, Meghan W.; Verhoeven, Anne Brooks; van Hoek, Monique L. Microbial Ecology, Vol. 59, Issue 3 https://doi.org/10.1007/s00248-009-9586-9	journal	September 2009
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Comparative Protein Structure Modeling Using Modeller Eswar, Narayanan; Webb, Ben; Marti-Renom, Marc A. Current Protocols in Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1002/0471250953.bi0506s15	journal	September 2006
A comprehensive transposon mutant library of Francisella novicida , a bioweapon surrogate Gallagher, Larry A.; Ramage, Elizabeth; Jacobs, Michael A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 3 https://doi.org/10.1073/pnas.0606713104	journal	January 2007
Biological Insights from Structures of Two-Component Proteins Gao, Rong; Stock, Ann M. Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073214	journal	October 2009
Novel antibacterial compounds specifically targeting the essential WalR response regulator Gotoh, Yasuhiro; Doi, Akihiro; Furuta, Eiji The Journal of Antibiotics, Vol. 63, Issue 3 https://doi.org/10.1038/ja.2010.4	journal	January 2010
PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. Gunn, J. S.; Miller, S. I. Journal of bacteriology, Vol. 178, Issue 23 https://doi.org/10.1128/JB.178.23.6857-6864.1996	journal	January 1996
Antimicrobial activity of human beta-defensins and induction by Francisella Han, SuHua; Bishop, Barney M.; van Hoek, Monique L. Biochemical and Biophysical Research Communications, Vol. 371, Issue 4 https://doi.org/10.1016/j.bbrc.2008.04.092	journal	July 2008
Evolution of Multidrug Resistance during Staphylococcus aureus Infection Involves Mutation of the Essential Two Component Regulator WalKR Howden, Benjamin P.; McEvoy, Christopher R. E.; Allen, David L. PLoS Pathogens, Vol. 7, Issue 11 https://doi.org/10.1371/journal.ppat.1002359	journal	November 2011
Subversion of Host Recognition and Defense Systems by Francisella spp. Jones, C. L.; Napier, B. A.; Sampson, T. R. Microbiology and Molecular Biology Reviews, Vol. 76, Issue 2 https://doi.org/10.1128/MMBR.05027-11	journal	June 2012
Antimicrobial activity of mosquito cecropin peptides against Francisella Kaushal, Akanksha; Gupta, Kajal; Shah, Ruhee Developmental & Comparative Immunology, Vol. 63 https://doi.org/10.1016/j.dci.2016.05.018	journal	October 2016
Comparative review of Francisella tularensis and Francisella novicida Kingry, Luke C.; Petersen, Jeannine M. Frontiers in Cellular and Infection Microbiology, Vol. 4 https://doi.org/10.3389/fcimb.2014.00035	journal	March 2014
Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis Lai, Xin-He; Golovliov, Igor; Sjöstedt, Anders Microbial Pathogenesis, Vol. 37, Issue 5 https://doi.org/10.1016/j.micpath.2004.07.002	journal	November 2004
Molecular Evolutionary Consequences of Niche Restriction in Francisella tularensis, a Facultative Intracellular Pathogen Larsson, Pär; Elfsmark, Daniel; Svensson, Kerstin PLoS Pathogens, Vol. 5, Issue 6 https://doi.org/10.1371/journal.ppat.1000472	journal	June 2009
The complete genome sequence of Francisella tularensis, the causative agent of tularemia Larsson, Pär; Oyston, Petra C. F.; Chain, Patrick Nature Genetics, Vol. 37, Issue 2 https://doi.org/10.1038/ng1499	journal	January 2005
Molecular Characterization of the Mg2+-Responsive PhoP-PhoQ Regulon in Salmonella enterica Lejona, S.; Aguirre, A.; Cabeza, M. L. Journal of Bacteriology, Vol. 185, Issue 21 https://doi.org/10.1128/JB.185.21.6287-6294.2003	journal	October 2003
LPS remodeling is an evolved survival strategy for bacteria Li, Y.; Powell, D. A.; Shaffer, S. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1202908109	journal	May 2012
Factors affecting the escape of Francisella tularensis from the phagolysosome Lindgren, Helena; Golovliov, Igor; Baranov, Vladimir Journal of Medical Microbiology, Vol. 53, Issue 10 https://doi.org/10.1099/jmm.0.45685-0	journal	October 2004
Detection and comparison of protein–DNA interactions using DNA–BIND plate and horseradish peroxidase-based colorimetric assay Liu, Bin; Qin, Yu; Wang, Jinzhong Analytical Biochemistry, Vol. 412, Issue 1 https://doi.org/10.1016/j.ab.2011.01.008	journal	May 2011
Structure and dynamics of polymyxin-resistance-associated response regulator PmrA in complex with promoter DNA Lou, Yuan-Chao; Weng, Tsai-Hsuan; Li, Yi-Chuan Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9838	journal	November 2015
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Lipophilic Prodrugs of FR900098 Are Antimicrobial against Francisella novicida In Vivo and In Vitro and Show GlpT Independent Efficacy McKenney, Elizabeth S.; Sargent, Michelle; Khan, Hameed PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0038167	journal	October 2012
Glycogen production by different Salmonella enterica serotypes: contribution of functional glgC to virulence, intestinal colonization and environmental survival McMeechan, Alisdair; Lovell, Margaret A.; Cogan, Tristan A. Microbiology, Vol. 151, Issue 12 https://doi.org/10.1099/mic.0.28292-0	journal	December 2005
Structure of the Response Regulator PhoP from Mycobacterium tuberculosis Reveals a Dimer through the Receiver Domain Menon, Smita; Wang, Shuishu Biochemistry, Vol. 50, Issue 26 https://doi.org/10.1021/bi2005575	journal	July 2011
Structure of the Francisella response regulator QseB receiver domain, and characterization of QseB inhibition by antibiofilm 2-aminoimidazole-based compounds: Inhibition of response regulator QseB by antibiofilm compounds Milton, Morgan E.; Allen, C. Leigh; Feldmann, Erik A. Molecular Microbiology, Vol. 106, Issue 2 https://doi.org/10.1111/mmi.13759	journal	August 2017
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility Morris, Garrett M.; Huey, Ruth; Lindstrom, William Journal of Computational Chemistry, Vol. 30, Issue 16 https://doi.org/10.1002/jcc.21256	journal	December 2009
Reciprocal Analysis of Francisella novicida Infections of a Drosophila melanogaster Model Reveal Host-Pathogen Conflicts Mediated by Reactive Oxygen and imd-Regulated Innate Immune Response Moule, Madeleine G.; Monack, Denise M.; Schneider, David S. PLoS Pathogens, Vol. 6, Issue 8 https://doi.org/10.1371/journal.ppat.1001065	journal	August 2010
An asymmetric heterodomain interface stabilizes a response regulator–DNA complex Narayanan, Anoop; Kumar, Shivesh; Evrard, Amanda N. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4282	journal	February 2014
The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Niesen, Frank H.; Berglund, Helena; Vedadi, Masoud Nature Protocols, Vol. 2, Issue 9 https://doi.org/10.1038/nprot.2007.321	journal	September 2007
Microtiter Dish Biofilm Formation Assay O'Toole, George A. Journal of Visualized Experiments, Issue 47 https://doi.org/10.3791/2437	journal	January 2011
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Tularaemia: bioterrorism defence renews interest in Francisella tularensis Oyston, Petra C. F.; Sjöstedt, Anders; Titball, Richard W. Nature Reviews Microbiology, Vol. 2, Issue 12 https://doi.org/10.1038/nrmicro1045	journal	December 2004
Proteomic Characterization and Functional Analysis of Outer Membrane Vesicles of Francisella novicida Suggests Possible Role in Virulence and Use as a Vaccine Pierson, Tony; Matrakas, Demetrios; Taylor, Yuka U. Journal of Proteome Research, Vol. 10, Issue 3 https://doi.org/10.1021/pr1009756	journal	March 2011
A response regulator promotes Francisella tularensis intramacrophage growth by repressing an anti-virulence factor: PmrA represses an anti-virulence factor Ramsey, Kathryn M.; Dove, Simon L. Molecular Microbiology, Vol. 101, Issue 4 https://doi.org/10.1111/mmi.13418	journal	June 2016
Targeting QseC Signaling and Virulence for Antibiotic Development Rasko, D. A.; Moreira, C. G.; Li, D. R. Science, Vol. 321, Issue 5892 https://doi.org/10.1126/science.1160354	journal	August 2008
An intracellularly inducible gene involved in virulence and polyphosphate production in Francisella Richards, Mark I.; Michell, Stephen L.; Oyston, Petra C. F. Journal of Medical Microbiology, Vol. 57, Issue 10 https://doi.org/10.1099/jmm.0.2008/001826-0	journal	October 2008
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
Generation and Characterization of an Attenuated Mutant in a Response Regulator Gene of Francisella tularensis Live Vaccine Strain (LVS) Sammons-Jackson, Wendy L.; McClelland, Karen; Manch-Citron, Jean N. DNA and Cell Biology, Vol. 27, Issue 7 https://doi.org/10.1089/dna.2007.0687	journal	July 2008
Biosynthesis of Undecaprenyl Phosphate-Galactosamine and Undecaprenyl Phosphate-Glucose in Francisella novicida ^† Song, Feng; Guan, Ziqiang; Raetz, Christian R. H. Biochemistry, Vol. 48, Issue 6 https://doi.org/10.1021/bi802212t	journal	February 2009
Two-Component Signal Transduction Stock, Ann M.; Robinson, Victoria L.; Goudreau, Paul N. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.183	journal	June 2000
Identification of BfmR, a Response Regulator Involved in Biofilm Development, as a Target for a 2-Aminoimidazole-Based Antibiofilm Agent Thompson, Richele J.; Bobay, Benjamin G.; Stowe, Sean D. Biochemistry, Vol. 51, Issue 49 https://doi.org/10.1021/bi3015289	journal	November 2012
3D-DART: a DNA structure modelling server van Dijk, M.; Bonvin, A. M. J. J. Nucleic Acids Research, Vol. 37, Issue Web Server https://doi.org/10.1093/nar/gkp287	journal	May 2009
Biofilms: An advancement in our understanding of Francisella species van Hoek, Monique L. Virulence, Vol. 4, Issue 8 https://doi.org/10.4161/viru.27023	journal	November 2013
Two-Component Systems in Francisella Species van Hoek, Monique L.; Hoang, Ky V.; Gunn, John S. Frontiers in Cellular and Infection Microbiology, Vol. 9 https://doi.org/10.3389/fcimb.2019.00198	journal	June 2019
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes van Zundert, G. C. P.; Rodrigues, J. P. G. L. M.; Trellet, M. Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.09.014	journal	February 2016
Francisella philomiragia Biofilm Formation and Interaction With the Aquatic Protist Acanthamoeba castellanii Verhoeven, Anne B.; Durham-colleran, Meghan W.; Pierson, Tony The Biological Bulletin, Vol. 219, Issue 2 https://doi.org/10.1086/BBLv219n2p178	journal	October 2010
Identification of Undecaprenyl Phosphate-β- d -Galactosamine in Francisella novicida and Its Function in Lipid A Modification ^† Wang, Xiaoyuan; Ribeiro, Anthony A.; Guan, Ziqiang Biochemistry, Vol. 48, Issue 6 https://doi.org/10.1021/bi802211k	journal	February 2009
WeNMR: Structural Biology on the Grid Wassenaar, Tsjerk A.; van Dijk, Marc; Loureiro-Ferreira, Nuno Journal of Grid Computing, Vol. 10, Issue 4 https://doi.org/10.1007/s10723-012-9246-z	journal	November 2012
A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in Arabidopsis Zhang, Yu; Mayba, Oleg; Pfeiffer, Anne PLoS Genetics, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pgen.1003244	journal	January 2013
Transcriptome analysis of the Mg ²⁺ -responsive PhoP regulator in Yersinia pestis Zhou, Dongsheng; Han, Yanping; Qin, Long FEMS Microbiology Letters, Vol. 250, Issue 1 https://doi.org/10.1016/j.femsle.2005.06.053	journal	September 2005
Comparative Protein Structure Modeling Using MODELLER Eswar, Narayanan; Webb, Ben; Marti-Renom, Marc A. Current Protocols in Protein Science, Vol. 50, Issue 1 https://doi.org/10.1002/0471140864.ps0209s50	journal	November 2007
Mg2+ as an Extracellular Signal: Environmental Regulation of Salmonella Virulence Véscovi, Eleonora García; Soncini, Fernando C.; Groisman, Eduardo A. Cell, Vol. 84, Issue 1 https://doi.org/10.1016/s0092-8674(00)81003-x	journal	January 1996
Long-term ecological and evolutionary dynamics in the gut microbiomes of carbapenemase-producing Enterobacteriaceae colonized subjects Kang, Jonathan T. L.; Teo, Jonathan J. Y.; Bertrand, Denis Nature Microbiology, Vol. 7, Issue 10 https://doi.org/10.1038/s41564-022-01221-w	journal	September 2022
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain Raldúa, Demetrio; Casado, Marta; Prats, Eva Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-019-57142-y	journal	January 2020
Identification of the potential mechanism of Radix pueraria in colon cancer based on network pharmacology Li, Yi; Zhang, Chunli; Ma, Xiaohan Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07815-y	journal	March 2022
Escherichia coli glycogen genes are organized in a single glgBXCAP transcriptional unit possessing an alternative suboperonic promoter within glgC that directs glgAP expression Montero, Manuel; Almagro, Goizeder; Eydallin, Gustavo Biochemical Journal, Vol. 433, Issue 1 https://doi.org/10.1042/bj20101186	journal	December 2010
Direct isolation of Francisella spp. from environmental samples Petersen, J. M.; Carlson, J.; Yockey, B. Letters in Applied Microbiology https://doi.org/10.1111/j.1472-765x.2009.02589.x	journal	March 2009
Adaptive Resistance to the “Last Hope” Antibiotics Polymyxin B and Colistin in Pseudomonas aeruginosa Is Mediated by the Novel Two-Component Regulatory System ParR-ParS Fernández, Lucía; Gooderham, W. James; Bains, Manjeet Antimicrobial Agents and Chemotherapy, Vol. 54, Issue 8 https://doi.org/10.1128/aac.00242-10	journal	June 2010
Contributions of Francisella tularensis subsp. novicida Chitinases and Sec Secretion System to Biofilm Formation on Chitin Margolis, Jeffrey J.; El-Etr, Sahar; Joubert, Lydia-Marie Applied and Environmental Microbiology, Vol. 76, Issue 2 https://doi.org/10.1128/aem.02037-09	journal	November 2009
Enhancement of Acetic Acid Tolerance in Saccharomyces cerevisiae by Overexpression of the HAA1 Gene, Encoding a Transcriptional Activator Tanaka, Koichi; Ishii, Yukari; Ogawa, Jun Applied and Environmental Microbiology, Vol. 78, Issue 22 https://doi.org/10.1128/aem.02356-12	journal	September 2012
Increased Antibiotic Resistance of Escherichia coli in Mature Biofilms Ito, A.; Taniuchi, A.; May, T. Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/aem.02949-08	journal	April 2009
Construction and Characterization of a Highly Efficient Francisella Shuttle Plasmid Maier, Tamara M.; Havig, Andrea; Casey, Monika Applied and Environmental Microbiology, Vol. 70, Issue 12 https://doi.org/10.1128/aem.70.12.7511-7519.2004	journal	December 2004
Directed Screen of Francisella novicida Virulence Determinants Using Drosophila melanogaster Åhlund, Monika K.; Rydén, Patrik; Sjöstedt, Anders Infection and Immunity, Vol. 78, Issue 7 https://doi.org/10.1128/iai.00146-10	journal	May 2010
Identification of an Orphan Response Regulator Required for the Virulence of Francisella spp. and Transcription of Pathogenicity Island Genes Mohapatra, Nrusingh P.; Soni, Shilpa; Bell, Brian L. Infection and Immunity, Vol. 75, Issue 7 https://doi.org/10.1128/iai.00351-07	journal	April 2007
Genome-Wide Identification of Francisella tularensis Virulence Determinants Su, J.; Yang, J.; Zhao, D. Infection and Immunity, Vol. 75, Issue 6 https://doi.org/10.1128/iai.01865-06	journal	April 2007
Contribution of the PhoP-PhoQ and PmrA-PmrB Two-Component Regulatory Systems to Mg2+-Induced Gene Regulation in Pseudomonas aeruginosa McPhee, Joseph B.; Bains, Manjeet; Winsor, Geoff Journal of Bacteriology, Vol. 188, Issue 11 https://doi.org/10.1128/jb.00053-06	journal	June 2006
New Insights into the WalK/WalR (YycG/YycF) Essential Signal Transduction Pathway Reveal a Major Role in Controlling Cell Wall Metabolism and Biofilm Formation in Staphylococcus aureus Dubrac, S.; Boneca, I. G.; Poupel, O. Journal of Bacteriology, Vol. 189, Issue 22 https://doi.org/10.1128/jb.00645-07	journal	September 2007
A PhoP-Regulated Outer Membrane Protease of Salmonella enterica Serovar Typhimurium Promotes Resistance to Alpha-Helical Antimicrobial Peptides Guina, Tina; Yi, Eugene C.; Wang, Houle Journal of Bacteriology, Vol. 182, Issue 14 https://doi.org/10.1128/jb.182.14.4077-4086.2000	journal	July 2000
Overexpression of the Response Regulator evgA of the Two-Component Signal Transduction System Modulates Multidrug Resistance Conferred by Multidrug Resistance Transporters Nishino, K.; Yamaguchi, A. Journal of Bacteriology, Vol. 183, Issue 4 https://doi.org/10.1128/jb.183.4.1455-1458.2001	journal	February 2001
The Pleiotropic Two-Component Regulatory System PhoP-PhoQ Groisman, Eduardo A. Journal of Bacteriology, Vol. 183, Issue 6 https://doi.org/10.1128/jb.183.6.1835-1842.2001	journal	March 2001
Identification and Molecular Characterization of the Mg2+ Stimulon of Escherichia coli Minagawa, Shu; Ogasawara, Hiroshi; Kato, Akinori Journal of Bacteriology, Vol. 185, Issue 13 https://doi.org/10.1128/jb.185.13.3696-3702.2003	journal	July 2003
A Francisella tularensis Pathogenicity Island Required for Intramacrophage Growth Nano, F. E.; Zhang, N.; Cowley, S. C. Journal of Bacteriology, Vol. 186, Issue 19 https://doi.org/10.1128/jb.186.19.6430-6436.2004	journal	September 2004
Genotype-Phenotype Associations in a Nonmodel Prokaryote Enstrom, M.; Held, K.; Ramage, B. mBio, Vol. 3, Issue 2 https://doi.org/10.1128/mbio.00001-12	journal	February 2012
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Microtiter Dish Biofilm Formation Assay O'Toole, George A. Journal of Visualized Experiments, Issue 47 https://doi.org/10.3791/2437-v	journal	January 2011

Similar Records

Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice

Journal Article · Tue May 30 00:00:00 EDT 2017 · Frontiers in Microbiology · OSTI ID:1729718

Freudenberger Catanzaro, Kelly C.; Champion, Anna E.; Mohapatra, Nrusingh; +2 more

Proteomic analysis of bronchoalveolar lavage fluid proteins from mice infected with Francisella tularensis ssp novicida

Journal Article · Fri Jul 06 00:00:00 EDT 2012 · Journal of Proteome Research, 11(7):3690-3703 · OSTI ID:1729718

Varnum, Susan M.; Webb-Robertson, Bobbie-Jo M.; Pounds, Joel G.; +5 more

Comparative phosphoproteomics reveals components of host cell invasion and post-transcriptional regulation during Francisella infection

Journal Article · Sun Sep 22 00:00:00 EDT 2013 · Molecular and Cellular Proteomics, 12(11):3297-3309 · OSTI ID:1729718

Nakayasu, Ernesto S.; Tempel, Rebecca; Cambronne, Xiaolu A.; +8 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Francisella novicida Two-Component System Response Regulator BfpR Modulates iglC Gene Expression, Antimicrobial Peptide Resistance, and Biofilm Production

Citation Formats

References (91)

Similar Records

Related Subjects