Crystal structure of B acillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity: AtxA multimerization, phosphorylation and activity
Abstract
The Bacillus anthracis virulence regulator AtxA controls transcription of the anthrax toxin genes and capsule biosynthetic operon. AtxA activity is elevated during growth in media containing glucose and CO2/bicarbonate, and there is a positive correlation between the CO2/bicarbonate signal, AtxA activity and homomultimerization. AtxA activity is also affected by phosphorylation at specific histidines. We show that AtxA crystallizes as a dimer. Distinct folds associated with predicted DNA-binding domains (HTH1 and HTH2) and phosphoenolpyruvate: carbohydrate phosphotransferase system-regulated domains (PRD1 and PRD2) are apparent. We tested AtxA variants containing single and double phosphomimetic (HisAsp) and phosphoablative (HisAla) amino acid changes for activity in B.anthracis cultures and for protein-protein interactions in cell lysates. Reduced activity of AtxA H199A, lack of multimerization and activity of AtxAH379D variants, and predicted structural changes associated with phosphorylation support a model for control of AtxA function. We propose that (i) in the AtxA dimer, phosphorylation of H199 in PRD1 affects HTH2 positioning, influencing DNA-binding; and (ii) phosphorylation of H379 in PRD2 disrupts dimer formation. The AtxA structure is the first reported high-resolution full-length structure of a PRD-containing regulator, and can serve as a model for proteins of this family, especially those that link virulence to bacterial metabolism.
- Authors:
-
- Department of Microbiology and Molecular Genetics, The University of Texas Health Science Center at Houston, Houston TX USA
- Center for Structural Genomics of Infectious Diseases, Argonne National Laboratory, Argonne IL USA; Structural Biology Center, Biosciences Division, Argonne National Laboratory, Argonne IL USA
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH). National Institute of Allergy and Infectious Diseases (NIAID); Keck Center for Computational and Structural Biology in Biodefense Training Program
- OSTI Identifier:
- 1339284
- DOE Contract Number:
- AC02-06CH11357
- Resource Type:
- Journal Article
- Journal Name:
- Molecular Microbiology
- Additional Journal Information:
- Journal Volume: 95; Journal Issue: 3; Journal ID: ISSN 0950-382X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Hammerstrom, Troy G., Horton, Lori B., Swick, Michelle C., Joachimiak, Andrzej, Osipiuk, Jerzy, and Koehler, Theresa M. Crystal structure of B acillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity: AtxA multimerization, phosphorylation and activity. United States: N. p., 2014.
Web. doi:10.1111/mmi.12867.
Hammerstrom, Troy G., Horton, Lori B., Swick, Michelle C., Joachimiak, Andrzej, Osipiuk, Jerzy, & Koehler, Theresa M. Crystal structure of B acillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity: AtxA multimerization, phosphorylation and activity. United States. https://doi.org/10.1111/mmi.12867
Hammerstrom, Troy G., Horton, Lori B., Swick, Michelle C., Joachimiak, Andrzej, Osipiuk, Jerzy, and Koehler, Theresa M. 2014.
"Crystal structure of B acillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity: AtxA multimerization, phosphorylation and activity". United States. https://doi.org/10.1111/mmi.12867.
@article{osti_1339284,
title = {Crystal structure of B acillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity: AtxA multimerization, phosphorylation and activity},
author = {Hammerstrom, Troy G. and Horton, Lori B. and Swick, Michelle C. and Joachimiak, Andrzej and Osipiuk, Jerzy and Koehler, Theresa M.},
abstractNote = {The Bacillus anthracis virulence regulator AtxA controls transcription of the anthrax toxin genes and capsule biosynthetic operon. AtxA activity is elevated during growth in media containing glucose and CO2/bicarbonate, and there is a positive correlation between the CO2/bicarbonate signal, AtxA activity and homomultimerization. AtxA activity is also affected by phosphorylation at specific histidines. We show that AtxA crystallizes as a dimer. Distinct folds associated with predicted DNA-binding domains (HTH1 and HTH2) and phosphoenolpyruvate: carbohydrate phosphotransferase system-regulated domains (PRD1 and PRD2) are apparent. We tested AtxA variants containing single and double phosphomimetic (HisAsp) and phosphoablative (HisAla) amino acid changes for activity in B.anthracis cultures and for protein-protein interactions in cell lysates. Reduced activity of AtxA H199A, lack of multimerization and activity of AtxAH379D variants, and predicted structural changes associated with phosphorylation support a model for control of AtxA function. We propose that (i) in the AtxA dimer, phosphorylation of H199 in PRD1 affects HTH2 positioning, influencing DNA-binding; and (ii) phosphorylation of H379 in PRD2 disrupts dimer formation. The AtxA structure is the first reported high-resolution full-length structure of a PRD-containing regulator, and can serve as a model for proteins of this family, especially those that link virulence to bacterial metabolism.},
doi = {10.1111/mmi.12867},
url = {https://www.osti.gov/biblio/1339284},
journal = {Molecular Microbiology},
issn = {0950-382X},
number = 3,
volume = 95,
place = {United States},
year = {Tue Dec 30 00:00:00 EST 2014},
month = {Tue Dec 30 00:00:00 EST 2014}
}
Works referenced in this record:
PHENIX : building new software for automated crystallographic structure determination
journal, October 2002
- Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei
- Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11
Transcriptional regulation of the protective antigen gene of Bacillus anthracis.
journal, January 1989
- Bartkus, J. M.; Leppla, S. H.
- Infection and Immunity, Vol. 57, Issue 8
Experimental and Computational Characterization of the Dimerization of the PTS-regulation Domains of BglG from Escherichia coli
journal, April 2005
- Ben-Zeev, Efrat; Fux, Liat; Amster-Choder, Orna
- Journal of Molecular Biology, Vol. 347, Issue 4
Functional Dissection of the Bacillus subtilis pur Operator Site
journal, July 2003
- Bera, A. K.; Zhu, J.; Zalkin, H.
- Journal of Bacteriology, Vol. 185, Issue 14
Studies on Lysogenesis i.
journal, January 1951
- Bertani, G.
- Journal of Bacteriology, Vol. 62, Issue 3
Global Effects of Virulence Gene Regulators in a Bacillus anthracis Strain with Both Virulence Plasmids
journal, May 2003
- Bourgogne, Agathe; Drysdale, Melissa; Hilsenbeck, Susan G.
- Infection and Immunity, Vol. 71, Issue 5
A Bacillus thuringiensis strain producing a polyglutamate capsule resembling that of Bacillus anthracis
journal, August 2008
- Cachat, Elise; Barker, Margaret; Read, Timothy D.
- FEMS Microbiology Letters, Vol. 285, Issue 2
Kinetic Studies of HPr, HPr(H15D), HPr(H15E), and HPr(His∼P) Phosphorylation by the Streptococcus salivarius HPr(Ser) Kinase/Phosphorylase
journal, November 2009
- Casabon, Israël; Couture, Manon; Vaillancourt, Katy
- Biochemistry, Vol. 48, Issue 45
Regulation of pag gene expression in Bacillus anthracis : use of a pag-lacZ transcriptional fusion
journal, November 1992
- Cataldi, Angel; Fouet, Agnès; Mock, Michèle
- FEMS Microbiology Letters, Vol. 98, Issue 1-3
Sialylation of Group B Streptococcal Capsular Polysaccharide Is Mediated by cpsK and Is Required for Optimal Capsule Polymerization and Expression
journal, July 2005
- Chaffin, D. O.; Mentele, L. M.; Rubens, C. E.
- Journal of Bacteriology, Vol. 187, Issue 13
Glucose-Dependent Activation of Bacillus anthracis Toxin Gene Expression and Virulence Requires the Carbon Catabolite Protein CcpA
journal, October 2010
- Chiang, C.; Bongiorni, C.; Perego, M.
- Journal of Bacteriology, Vol. 193, Issue 1
The CCP4 suite programs for protein crystallography
journal, September 1994
- ,
- Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763
Regulation of anthrax toxin activator gene (atxA) expression in Bacillus anthracis: temperature, not CO2/bicarbonate, affects AtxA synthesis.
journal, January 1997
- Dai, Z.; Koehler, T. M.
- Infection and immunity, Vol. 65, Issue 7
The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence
journal, June 1995
- Dai, Zhihao; Sirard, Jean-Claude; Mock, Michèle
- Molecular Microbiology, Vol. 16, Issue 6, p. 1171-1181
cis-Acting Elements That Control Expression of the Master Virulence Regulatory Gene atxA in Bacillus anthracis
journal, May 2012
- Dale, J. L.; Raynor, M. J.; Dwivedi, P.
- Journal of Bacteriology, Vol. 194, Issue 15
MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes
journal, July 2004
- Davis, I. W.; Murray, L. W.; Richardson, J. S.
- Nucleic Acids Research, Vol. 32, Issue Web Server
atxA Controls Bacillus anthracis Capsule Synthesis via acpA and a Newly Discovered Regulator, acpB
journal, December 2003
- Drysdale, M.; Bourgogne, A.; Hilsenbeck, S. G.
- Journal of Bacteriology, Vol. 186, Issue 2
New LIC vectors for production of proteins from genes containing rare codons
journal, September 2013
- Eschenfeldt, William H.; Makowska-Grzyska, Magdalena; Stols, Lucy
- Journal of Structural and Functional Genomics, Vol. 14, Issue 4
Differential influence of the two Bacillus anthracis plasmids on regulation of virulence gene expression.
journal, January 1996
- Fouet, A.; Mock, M.
- Infection and immunity, Vol. 64, Issue 12
Pi sampling: a methodical and flexible approach to initial macromolecular crystallization screening
journal, April 2011
- Gorrec, Fabrice; Palmer, Colin M.; Lebon, Guillaume
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 5
Activation of the LicT Transcriptional Antiterminator Involves a Domain Swing/Lock Mechanism Provoking Massive Structural Changes
journal, February 2005
- Graille, Marc; Zhou, Cong-Zhao; Receveur-Bréchot, Véronique
- Journal of Biological Chemistry, Vol. 280, Issue 15
Demonstration of a capsule plasmid in Bacillus anthracis.
journal, January 1985
- Green, B. D.; Battisti, L.; Koehler, T. M.
- Infection and Immunity, Vol. 49, Issue 2
Intrinsic curvature associated with the coordinately regulated anthrax toxin gene promoters
journal, August 2008
- Hadjifrangiskou, Maria; Koehler, Theresa M.
- Microbiology, Vol. 154, Issue 8
Bacillus anthracis virulence regulator AtxA: oligomeric state, function and CO2-signalling: B. anthracis AtxA multimerization
journal, October 2011
- Hammerstrom, Troy G.; Roh, Jung Hyeob; Nikonowicz, Edward P.
- Molecular Microbiology, Vol. 82, Issue 3
Structure of the RBD-PRDI fragment of the antiterminator protein GlcT
journal, June 2012
- Himmel, Sebastian; Grosse, Christian; Wolff, Sebastian
- Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 68, Issue 7
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
The Mga virulence regulon: infection where the grass is greener
journal, December 2007
- Hondorp, Elise R.; McIver, Kevin S.
- Molecular Microbiology, Vol. 66, Issue 5
Characterization of the Group A Streptococcus Mga virulence regulator reveals a role for the C-terminal region in oligomerization and transcriptional activation: Mga oligomerization and activity
journal, January 2012
- Hondorp, Elise R.; Hou, Sherry C.; Hempstead, Andrew D.
- Molecular Microbiology, Vol. 83, Issue 5
PTS phosphorylation of Mga modulates regulon expression and virulence in the group A streptococcus: PTS phosphorylation of Mga
journal, May 2013
- Hondorp, Elise R.; Hou, Sherry C.; Hause, Lara L.
- Molecular Microbiology, Vol. 88, Issue 6
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension
journal, April 1989
- Horton, Robert M.; Hunt, Henry D.; Ho, Steffan N.
- Gene, Vol. 77, Issue 1, p. 61-68
Control of Bacillus subtilis mtl operon expression by complex phosphorylation-dependent regulation of the transcriptional activator MtlR: Role of the EIIBGat-like domain in MtlR regulation
journal, April 2010
- Joyet, Philippe; Derkaoui, Meriem; Poncet, Sandrine
- Molecular Microbiology, Vol. 76, Issue 5
Regulation of the Bacillus anthracis protective antigen gene: CO2 and a trans-acting element activate transcription from one of two promoters.
journal, February 1994
- Koehler, T. M.; Dai, Z.; Kaufman-Yarbray, M.
- Journal of Bacteriology, Vol. 176, Issue 3
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
ProFunc: a server for predicting protein function from 3D structure
journal, July 2005
- Laskowski, R. A.; Watson, J. D.; Thornton, J. M.
- Nucleic Acids Research, Vol. 33, Issue Web Server
Structural basis for regulation of rhizobial nodulation and symbiosis gene expression by the regulatory protein NolR
journal, April 2014
- Lee, S. G.; Krishnan, H. B.; Jez, J. M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
Crystal Structures of Phosphotransferase System Enzymes PtxB (IIBAsc) and PtxA (IIAAsc) from Streptococcus mutans
journal, February 2009
- Lei, Jian; Li, Lan-Fen; Su, Xiao-Dong
- Journal of Molecular Biology, Vol. 386, Issue 2
Two DNA-binding domains of Mga are required for virulence gene activation in the group A streptococcus
journal, March 2002
- McIver, Kevin S.; Myles, Rhonda L.
- Molecular Microbiology, Vol. 43, Issue 6
Specific binding of the activator Mga to promoter sequences of the emm and scpA genes in the group A streptococcus.
journal, January 1995
- McIver, K. S.; Heath, A. S.; Green, B. D.
- Journal of bacteriology, Vol. 177, Issue 22
The transformation frequency of plasmids into Bacillus anthracis is affected by adenine methylation
journal, January 1995
- Marrero, Robert; Welkos, Susan L.
- Gene, Vol. 152, Issue 1
A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis: pXO1 regulators in B. anthracis
journal, February 2003
- Mignot, Tâm; Mock, Michèle; Fouet, Agnès
- Molecular Microbiology, Vol. 47, Issue 4
Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997
- Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
An asymmetric heterodomain interface stabilizes a response regulator–DNA complex
journal, February 2014
- Narayanan, Anoop; Kumar, Shivesh; Evrard, Amanda N.
- Nature Communications, Vol. 5, Issue 1
Virulence Meets Metabolism: Cra and KdpE Gene Regulation in Enterohemorrhagic Escherichia coli
journal, October 2012
- Njoroge, Jacqueline W.; Nguyen, Y.; Curtis, Meredith M.
- mBio, Vol. 3, Issue 5
Bacillus anthracis sin Locus and Regulation of Secreted Proteases
journal, December 2010
- Pflughoeft, K. J.; Sumby, P.; Koehler, T. M.
- Journal of Bacteriology, Vol. 193, Issue 3
The Complete Genome Sequence of Bacillus anthracis Ames "Ancestor"
journal, October 2008
- Ravel, J.; Jiang, L.; Stanley, S. T.
- Journal of Bacteriology, Vol. 191, Issue 1
Defining the Mga regulon: comparative transcriptome analysis reveals both direct and indirect regulation by Mga in the group A streptococcus: Transcriptome analysis of the Mga regulon
journal, September 2006
- Ribardo, Deborah A.; McIver, Kevin S.
- Molecular Microbiology, Vol. 62, Issue 2
The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results
journal, December 2005
- Rosenbaum, Gerd; Alkire, Randy W.; Evans, Gwyndaf
- Journal of Synchrotron Radiation, Vol. 13, Issue 1
Control of Anthrax Toxin Gene Expression by the Transition State Regulator abrB
journal, January 2002
- Saile, E.; Koehler, T. M.
- Journal of Bacteriology, Vol. 184, Issue 2
Control of the Bacillus subtilis Antiterminator Protein GlcT by Phosphorylation: ELUCIDATION OF THE PHOSPHORYLATION CHAIN LEADING TO INACTIVATION OF GlcT
journal, October 2003
- Schmalisch, Matthias H.; Bachem, Steffi; Stülke, Jörg
- Journal of Biological Chemistry, Vol. 278, Issue 51
LicT, a Bacillus subtilis transcriptional antiterminator protein of the BglG family.
journal, January 1996
- Schnetz, K.; Stülke, J.; Gertz, S.
- Journal of bacteriology, Vol. 178, Issue 7
Vaccinia DNA topoisomerase I promotes illegitimate recombination in Escherichia coli.
journal, May 1989
- Shuman, S.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 10
The three Bacillus anthracis toxin genes are coordinately regulated by bicarbonate and temperature.
journal, January 1994
- Sirard, J. C.; Mock, M.; Fouet, A.
- Journal of Bacteriology, Vol. 176, Issue 16
Characterization of a plasmid region involved in Bacillus anthracis toxin production and pathogenesis
journal, October 2000
- Sirard, J. -C.; Guidi-Rontani, C.; Fouet, A.
- International Journal of Medical Microbiology, Vol. 290, Issue 4-5
The pneumococcal MgaSpn virulence transcriptional regulator generates multimeric complexes on linear double-stranded DNA
journal, May 2013
- Solano-Collado, V.; Lurz, R.; Espinosa, M.
- Nucleic Acids Research, Vol. 41, Issue 14
The DNA-binding specificity of the Bacillus anthracis AbrB protein
journal, June 2005
- Strauch, Mark A.; Ballar, Petek; Rowshan, Austin J.
- Microbiology, Vol. 151, Issue 6
PRD ? a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria
journal, June 1998
- Stulke, Jorg; Arnaud, Maryvonne; Rapoport, Georges
- Molecular Microbiology, Vol. 28, Issue 5
An Agar-Diffusion Method for Titrating Bacillus anthracis Immunizing Antigen and its Application to a Study of Antigen Production
journal, October 1957
- Thorne, C. B.; Belton, F. C.
- Journal of General Microbiology, Vol. 17, Issue 2
Crystal structure of an activated form of the PTS regulation domain from the LicT transcriptional antiterminator
journal, July 2001
- van Tilbeurgh, H.
- The EMBO Journal, Vol. 20, Issue 14
Regulation of the lic Operon ofBacillus subtilis and Characterization of Potential Phosphorylation Sites of the LicR Regulator Protein by Site-Directed Mutagenesis
journal, August 1999
- Tobisch, Steffen; Stülke, Jörg; Hecker, Michael
- Journal of Bacteriology, Vol. 181, Issue 16
Sites of positive and negative regulation in the Bacillus subtilis antiterminators LicT and SacY
journal, September 2001
- Tortosa, Pablo; Declerck, Nathalie; Dutartre, Helene
- Molecular Microbiology, Vol. 41, Issue 6
Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis
journal, February 2007
- Tsvetanova, Billyana; Wilson, Adam C.; Bongiorni, Cristina
- Molecular Microbiology, Vol. 63, Issue 3
Taking MAD to the extreme: ultrafast protein structure determination
journal, June 1999
- Walsh, Martin A.; Dementieva, Irene; Evans, Gwyndaf
- Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 6
The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores
journal, June 2001
- Welkos, Susan; Little, Stephen; Friedlander, Arthur
- Microbiology, Vol. 147, Issue 6
The Bacillus subtilis mannose regulator, ManR, a DNA-binding protein regulated by HPr and its cognate PTS transporter ManP: The Bacillus subtilis mannose regulator ManR
journal, April 2013
- Wenzel, Marian; Altenbuchner, Josef
- Molecular Microbiology, Vol. 88, Issue 3
Two small c-type cytochromes affect virulence gene expression in Bacillus anthracis: Bacillus anthracis virulence regulation by cytochrome c
journal, March 2009
- Wilson, Adam C.; Hoch, James A.; Perego, Marta
- Molecular Microbiology, Vol. 72, Issue 1
Common structural changes accompany the functional inactivation of HPr by seryl phosphorylation or by serine to aspartate substitution
journal, December 1989
- Wittekind, Michael; Reizer, Jonathan; Deutscher, Josef
- Biochemistry, Vol. 28, Issue 26
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors
journal, January 1985
- Yanisch-Perron, Celeste; Vieira, Jeffrey; Messing, Joachim
- Gene, Vol. 33, Issue 1
InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001
- Zdobnov, E. M.; Apweiler, R.
- Bioinformatics, Vol. 17, Issue 9, p. 847-848
Works referencing / citing this record:
DNA‐binding properties of MafR, a global regulator of Enterococcus faecalis
journal, December 2017
- Ruiz‐Cruz, Sofía; Moreno‐Blanco, Ana; Espinosa, Manuel
- FEBS Letters, Vol. 592, Issue 8
Glucose Levels Alter the Mga Virulence Regulon in the Group A Streptococcus
journal, March 2018
- Valdes, Kayla M.; Sundar, Ganesh S.; Belew, Ashton T.
- Scientific Reports, Vol. 8, Issue 1
Regulons and protein-protein interactions of PRD-containing Bacillus anthracis virulence regulators reveal overlapping but distinct functions: Regulons of B. anthracis PCVRs
journal, April 2018
- Raynor, Malik J.; Roh, Jung-Hyeob; Widen, Stephen G.
- Molecular Microbiology, Vol. 109, Issue 1
Influence of the phosphoenolpyruvate:carbohydrate phosphotransferase system on toxin gene expression and virulence in Bacillus anthracis
journal, November 2019
- Bier, Naomi; Hammerstrom, Troy G.; Koehler, Theresa M.
- Molecular Microbiology, Vol. 113, Issue 1
MgaSpn and H-NS: Two Unrelated Global Regulators with Similar DNA-Binding Properties
journal, September 2016
- Solano-Collado, Virtu; Hüttener, Mário; Espinosa, Manuel
- Frontiers in Molecular Biosciences, Vol. 3
Upstream sequence-dependent suppression and AtxA-dependent activation of protective antigens in Bacillus anthracis
journal, January 2019
- Toyomane, Kochi; Furuta, Yoshikazu; Fujikura, Daisuke
- PeerJ, Vol. 7
Glucose Levels Alter the Mga Virulence Regulon in the Group A Streptococcus
journal, March 2018
- Valdes, Kayla M.; Sundar, Ganesh S.; Belew, Ashton T.
- Scientific Reports, Vol. 8, Issue 1
Global Regulation of Gene Expression by the MafR Protein of Enterococcus faecalis
journal, January 2016
- Ruiz-Cruz, Sofía; Espinosa, Manuel; Goldmann, Oliver
- Frontiers in Microbiology, Vol. 6
MgaSpn and H-NS: Two Unrelated Global Regulators with Similar DNA-Binding Properties
journal, September 2016
- Solano-Collado, Virtu; Hüttener, Mário; Espinosa, Manuel
- Frontiers in Molecular Biosciences, Vol. 3
Upstream sequence-dependent suppression and AtxA-dependent activation of protective antigens in Bacillus anthracis
journal, January 2019
- Toyomane, Kochi; Furuta, Yoshikazu; Fujikura, Daisuke
- PeerJ, Vol. 7