Cited by 101Listeria monocytogenes in Food SafetyBacterial Genetics and BiotechnologyProbiotics and Fermented Foods

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Specific binding of the Listeria monocytogenes transcriptional regulator PrfA to target sequences requires additional factor(s) and is influenced by iron

Böckmann, Regine, Dickneite, Carmen, Middendorf, Barbara, Goebel, Werner, Sokolovic, Zeljka·1996·Molecular Microbiology

DOI 10.1046/j.1365-2958.1996.d01-1722.x

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Abstract

The PrfA protein, which is a member of the Crp/Fnr family of prokaryotic transcription activators, regulates the virulence genes of Listeria monocytogenes. In this work, specific binding of PrfA to its target DNA was determined by electrophoretic mobility‐shift assays (EMSAs) using cell‐free extracts from the two L. monocytogenes strains EGD and NCTC 7973. PrfA‐specific binding differs between the two strains, even when the concentration of PrfA was adjusted to similar levels. Both strains exhibited increased PrfA‐specific binding after a shift into minimal essential medium (MEM) without showing a significant change in the amount of PrfA protein, relative to extracts from bacteria grown in brain–heart infusion (BHI). The purified PrfA protein from strain EGD produced in Escherichia coli did not exhibit specific binding to the target DNA but did so upon addition of PrfA‐free extracts from various Listeria species and Bacillus subtilis. The observed activation of PrfA seems to be caused by a PrfA‐activating factor (Paf), which is probably a protein since elevated temperature, but not RNase treatment, destroyed the activation potential of such PrfA‐free extracts. Moreover, fractionation of these extracts by sucrose gradient centrifugation yielded the Paf activity in a fraction sedimenting at 3.2 S. Specific binding of PrfA‐containing extracts from strain EGD to the hly and actA promoter sequences was strongly inhibited by iron, whereas that of extracts from strain NCTC 7973 was only slightly reduced. The iron effect seems to be mediated by Paf rather than by PrfA itself.

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Background
Species-Specific Differences in the Activity of PrfA,the Key Regulator of Listerial VirulenceGenes
Mauder, N., Ecke, R., Mertins, S., Loeffler, D. I. M., Seidel, G., Sprehe, M., Hillen, W., Goebel, W., & Müller‐Altrock, S. (2006) · Journal of Bacteriology · doi:10.1128/jb.00473-06 · Cited by 26
“PrfALm and PrfA*Lm were purified as described previously (2).”
BackgroundMethodInfluentialSelf-citation
Free Fatty Acids Interfere with the DNA Binding Activity of the Virulence Regulator PrfA of Listeria monocytogenes
dos Santos, P. T., Thomasen, R. S. S., Green, M. S., Færgeman, N. J., & Kallipolitis, B. H. (2020) · Journal of Bacteriology · doi:10.1128/jb.00156-20 · Cited by 24
“For the inhibitory concentration (IC) determination, overnight cultures of EGD wild type, EGDprfA* (prfA-G155S), or EGDΔprfA were diluted to an OD600 of 0.0002, and 4 ml was transferred to glass tubes containing increasing concentrations of MA, LNA, LLA, OA, or EA.”
BackgroundInfluential
The transcriptional response of virulence genes in Listeria monocytogenes during inactivation by nisin
Shi, H., Trinh, Q., Xu, W., et al. (2012) · Food Control · doi:10.1016/j.foodcont.2012.11.008 · Cited by 23
How are signals transduced across the cytoplasmic membrane? Transport proteins as transmitter of information
Tetsch, L., & Jung, K. (2009) · Amino Acids · doi:10.1007/s00726-009-0235-x · Cited by 22
“In addition to that, two other promoters assure constitutive expression at low levels (Freitag et al. 1993) and also other listerial factors are known to modulate PrfA activity (Böckmann et al. 1996).”
Background
Rhamnose-Inducible Gene Expression in Listeria monocytogenes
Fieseler, L., Schmitter, S., Teišerskas, J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043444 · Cited by 20
In vitro transcription of PrfA‐dependent and ‐independent genes of Listeria monocytogenes
Lalic-Mülthaler, M., Bohne, J., & Goebel, W. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02607.x · Cited by 20
“There is convincing evidence for the involvement of other listerial (and environmental) factors in the differential PrfA-mediated gene regulation besides the cellular concentration of PrfA (Böckmann et al., 1996; 2000; Bohne et al., 1996; Bubert et al., 1997; Renzoni et al., 1997; Vega et al., 1998).”
BackgroundMethodInfluentialSelf-citation
Listeria monocytogenes
Fsihi, H., Steffen, P., & Cossart, P. (2001) · Elsevier eBooks · doi:10.1016/b978-012304220-0/50017-0 · Cited by 23
Aminopeptidase T of M29 Family Acts as A Novel Intracellular Virulence Factor for Listeria monocytogenes Infection
Cheng, C., Wang, X., Dong, Z., Shao, C., Yang, Y., Fang, W., Fang, C., Wang, H., Yang, M., Jiang, L., et al. (2015) · Scientific Reports · doi:10.1038/srep17370 · Cited by 20
A review of minimal and defined media for growth of Listeria monocytogenes
Jarvis, N. A., O’Bryan, C. A., Ricke, S. C., et al. (2016) · Food Control · doi:10.1016/j.foodcont.2016.02.020 · Cited by 18
Regulation of expression of type I signal peptidases in Listeria monocytogenes
Raynaud, C., & Charbit, A. (2005) · Microbiology · doi:10.1099/mic.0.28066-0 · Cited by 17
“Moreover, in B. subtilis, ClpC controls the expression of competence by forming a complex with MecA to negatively regulate ComK (Bockmann et al., 1996).”
Background
Characterization of the roles of activated charcoal and Chelex in the induction of PrfA regulon expression in complex medium
Gaballa, A., Sunil, S., Doll, E. V., Murphy, S. I., Bechtel, T. D., Guariglia-Oropeza, V., & Wiedmann, M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0250989 · Cited by 15
“monocytogenes was shown to contain a factor that enhanced PrfA binding to its target promoter [90].”
BackgroundResult
plcR papR -Independent Expression of Anthrolysin O by Bacillus anthracis
Ross, C. L., & Koehler, T. M. (2006) · Journal of Bacteriology · doi:10.1128/jb.00525-06 · Cited by 16
“PrfA-mediated gene activation requires binding of PrfA to a 14-bp palindromic sequence located in the promoter of target genes (6).”
Background
Point mutations within the streptococcal regulator of virulence (Srv) alter protein–DNA interactions and Srv function
Doern, C. D., Holder, R. C., & Reid, S. D. (2008) · Microbiology · doi:10.1099/mic.0.2007/013466-0 · Cited by 15
“To further establish that the His6 tag used to purify rSrv was not responsible for the altered migration of target DNA in EMSA (Bockmann et al., 1996; Dickneite et al., 1998), an enterokinase cleavage reaction was used to generate untagged Srv.”
Suppression of major histocompatibility complex class I and class II gene expression inListeria monocytogenes-infected murine macrophages
ller, S. S. ⁄., gler, S. K. ⁄., & Goebel, W. (1998) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.1998.tb01139.x · Cited by 15
Self-citation
Proof of Concept for Recombinant Cellular Controls in Quantitative Molecular Pathogen Detection
Rossmanith, P., Mester, P., Frühwirth, K., et al. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02601-10 · Cited by 13
Assessment of Environmental Factors on Listeria monocytogenes Scott A inlA Gene Expression by Relative Quantitative Taqman Real-Time Reverse Transcriptase PCR
Hanna, S. E., & Wang, H. H. (2006) · Journal of Food Protection · doi:10.4315/0362-028x-69.11.2754 · Cited by 13
Bacterial Phospholipases
Titball, R. W., & Rood, J. I. (2000) · Handbook of experimental pharmacology · doi:10.1007/978-3-662-05971-5_23 · Cited by 12
Listeria
McLauchlin, J., & Rees, C. E. D. (2015) · Bergey's Manual of Systematics of Archaea and Bacteria · doi:10.1002/9781118960608.gbm00547 · Cited by 9
The Global Regulator CcpA of Listeria monocytogenes Confers Sensitivity to Antimicrobial Fatty Acids
Thomasen, R. S. S., Jespersen, M. G., Jørgensen, K. B., dos Santos, P. T., Lillebæk, E. M. S., Skov, M. N., Kemp, M., & Kallipolitis, B. H. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.895942 · Cited by 6
“monocytogenes EGD serotype 1/2a strain and its isogenic mutant derivative ΔprfA (Böckmann et al., 1996) obtained from W.”
Background
Cloning and Characterisation of a Δ-prfA Listeria monocytogenes Strain Containing an Artificial Single Copy Genomic Internal Amplification Control (IAC) for Use as Internal Sample Process Control (ISPC)
Frühwirth, K., Fuchs, S., Mester, P., et al. (2011) · Food Analytical Methods · doi:10.1007/s12161-011-9212-6 · Cited by 7
“Δtarget EGDe (1/2a) Δ-prfA (strain) L. monocytogenes EGDe strain with total deletion of the prfA locus Böckmann et al. (1996) E. coli TOP10F′ – Chemically competent E. coli Invitrogen pPL2 phage insertion vector L. monocytogenes specific (strain) PSA integration site.”
BackgroundInfluential
Effects of iron and oxygen species scavengers on Listeria spp. chemiluminescence
André, P., Bilger, S., Remy, P., et al. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00671-5 · Cited by 7
Supportive and inhibitory elements of a putative PrfA‐dependent promoter inListeria monocytogenes
Luo, Q., Herler, M., Müller‐Altrock, S., & Goebel, W. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04417.x · Cited by 6
Self-citation
Low-level iron-dependent mutants ofListeria monocytogenesand their virulence in macrophages
André, P., Oberle, S., Specklin, V., Lombard, Y., & Vidon, D. J.-M. (2003) · Canadian Journal of Microbiology · doi:10.1139/w03-015 · Cited by 6
“In agreement with this hypothesis, it has been shown by Böckmann et al. (1996) that PrfA-dependent gene regulation requires a PrfAactivating factor (Paf), which is under iron dependence and has been identified as the RNA polymerase (Böckmann et al.”
Method
Absence of N-Acetylglucosamine Glycosylation on Listeria monocytogenes Wall Teichoic Acids Promotes Fatty Acid Tolerance by Repulsion From the Bacterial Surface
Thomasen, R. S. S., dos Santos, P. T., Lillebæk, E. M. S., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.897682 · Cited by 5
Regulation of Virulence Genes in PathogenicListeriaspp.
Goebel, W., Müller‐Altrock, S., & Kreft, J. (2014) · ASM Press eBooks · doi:10.1128/9781555816513.ch52 · Cited by 5
Self-citation
Relationship between Stress Adaptation and Virulence in Foodborne Pathogenic Bacteria
Gahan, C. G. M., & Hill, C. (2002) · CRC Press eBooks · doi:10.1201/9781420012828.ch7 · Cited by 4
Regulation ofListeria monocytogenesVirulence
Johansson, J., & Freitag, N. E. (2019) · ASM Press eBooks · doi:10.1128/9781683670131.ch52 · Cited by 3
Synthetic Analogs of Antimicrobial Peptides from Limulus Inhibit the Growth of Listeria monocytogenes by Increasing Cell Membrane Permeability and Suppressing Virulence Genes
Xie, H., Wang, M., Wu, Z., et al. (2022) · Journal of Food Quality · doi:10.1155/2022/4371877 · Cited by 2
The Effects of Environmental Conditions and External Treatments on Virulence of Foodborne Pathogens
Venkitanarayanan, K., Upadhyay, A., Nair, M. S., & Upadhyaya, I. (2017) · Springer eBooks · doi:10.1007/978-3-319-56836-2_10 · Cited by 2
Genetic Mechanisms of Virulence in Listeria monocytogenes
Ermolaeva, S. A. (2001) · Russian Journal of Genetics · doi:10.1023/a:1009044707398 · Cited by 1
“The putative factor involved in the formation of the high-molecular complex was termed PrfA-activator protein (Paf) [30].”
Background
How did Listeria monocytogenes become pathogenic
Kong, H. (2001)
Regulatory pathways and virulence inhibition in Listeria monocytogenes
Andersson, C. (2016) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
The effect of disinfectants on Listeria monocytogenes – phenotypic, physiological and genetic response
Kastbjerg, V. G., Vogel, B. F., & Gram, L. (2009)
THE ROLE OF QUORUM SENSING IN SURVIVAL, BIOFILM FORMATION AND GENE EXPRESSION OF LISTERIA MONOCYTOGENES
Ali, S. (2011) · The Atrium (University of Guelph)
Essential features of a PrfA-dependent : promoter of Listeria monocytogenes
Luo, Q. (2004) · Online Publication Service of Würzburg University (Würzburg University)
Molekulare Mechanismen der Pathogenität von Bakterien
Gross, R., & Goebel, W. (1999) · Springer eBooks · doi:10.1007/978-3-662-07865-5_8
Self-citation
Étude des interconnexions dans les réseaux de régulation de Listeria monocytogenes en réponse aux conditions de l'environnement
Marinho, C. M. (2019) · theses.fr (ABES) · doi:10.70675/9ff694eaz4e2fz4778z9b5bzc958cca32c40
The ferric Iron uptake transcriptional regulator (Fur) governs virulence and stress responses in Listeria monocytogenes and serves as a target for novel food safety interventions
Li, A., Xu, H., Song, R., Song, G., Qandeel, A., Cao, Q., Zhang, X., Ge, T., Wang, W., Li, Y., et al. (2026) · Food Research International · doi:10.1016/j.foodres.2026.120575

Authors: Böckmann, R., Dickneite, C., Middendorf, B., Goebel, W., & Sokolovic, Z.
Affiliations: University of Würzburg (DE)
Corresponding author: Goebel, Werner
ORCID: Goebel, Werner
Venue: Molecular Microbiology
Publisher: Wiley
Published: 1996-11
Volume: 22
Issue: 4
Pages: 643-653
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1046/j.1365-2958.1996.d01-1722.x
OpenAlex: W2122365028
Cited by: 101
References: 0
Citations by year: 2026: 1 · 2024: 1 · 2022: 3 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 1 · 2017: 2 · 2016: 2 · 2015: 5 · 2014: 2 · 2012: 3
FWCI: 5.68
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 2555 d)
Locations: Molecular Microbiology (publishedVersion)
PubMed (publishedVersion)
Funders: Deutsche Forschungsgemeinschaft
Universität Ulm
University of California, Davis
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Listeria monocytogenes in Food Safety
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: PrfA, Listeria monocytogenes, transcriptional regulation, DNA binding, transcriptional activator, iron regulation, virulence gene regulation, strain differences, protein-DNA interactions
MeSH terms: Bacterial Proteins, Bacterial Toxins, Culture Media, DNA, Bacterial, Escherichia coli, Heat-Shock Proteins, Hemolysin Proteins, Humans, Iron, Listeria monocytogenes, Membrane Proteins, Peptide Termination Factors, Promoter Regions, Genetic, Recombinant Fusion Proteins, Trans-Activators, Gene Expression

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Specific binding of the Listeria monocytogenes transcriptional regulator PrfA to target sequences requires additional factor(s) and is influenced by iron

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