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Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62260, Mexico
Correspondence
Edmundo Calva
ecalva{at}ibt.unam.mx
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). In our laboratory we have identified the S. Typhi ompS1 gene that encodes the OmpS1 quiescent porin belonging to the OmpC/OmpF superfamily (Fernández-Mora et al., 1995). OmpS1 has been reported to have a role in swarming motility, biofilm formation and virulence in mice (Toguchi et al., 2000; Mireles et al., 2001; Rodríguez-Morales et al., 2006).
Expression of ompS1 is dependent on two overlapping promoters, P1 and P2. The P1 promoter is dependent on the OmpR response regulator. The P2 promoter does not require OmpR for activation, being active only in the absence of OmpR (Oropeza et al., 1999; Flores-Valdez et al., 2003; De la Cruz et al., 2007). Another key element in the transcriptional regulation of ompS1 is the global regulatory protein H-NS, a nucleoid protein of 137 amino acids (15 kDa) that negatively regulates its expression (Flores-Valdez et al., 2003; De la Cruz et al., 2007). In Salmonella, H-NS has been proposed to selectively silence horizontally acquired genes by targeting sequences with a GC content lower than the resident genome, regulating around 12 % of its genes (Lucchini et al., 2006; Navarre et al., 2006). StpA, an H-NS paralogue, was found to repress ompS1 in an hns background; and LeuO, a LysR-type regulator, positively regulates ompS1 expression by antagonizing H-NS and StpA (De la Cruz et al., 2007). LeuO has been implicated in several functions, such as stress resistance, virulence and biofilm formation (VanBogelen et al., 1996; Fang et al., 2000; Majumder et al., 2001; Tenor et al., 2004; Lawley et al., 2006; Moorthy & Watnick, 2005; Rodríguez-Morales et al., 2006). Recently, our group has described several genes regulated by LeuO in S. Typhi (Hernández-Lucas et al., 2008).
In bacterial genomes, the recognition of their binding targets by regulatory proteins is commonly considered to be sequence-dependent, although DNA curvature plays a well-characterized role in many transcriptional regulation mechanisms in prokaryotes (Jáuregui et al., 2003; Olivares-Zavaleta et al., 2006). For example, static DNA curvature has been shown to activate transcription, facilitating the binding of RNA polymerase to promoters, or favouring the interaction of activator proteins (Pérez-Martín et al., 1994; Gourse et al., 2000). Curved DNA regions have also been found to repress transcription initiation, where DNA curvature generally plays an indirect role, being the target for the binding of specific silencer proteins or by stabilizing or enhancing a preexisting DNA loop, thus effectively blocking transcription of downstream regions (Olivares-Zavaleta et al., 2006). In particular, such would be the case for the ompF porin gene (Mizuno, 1987).
Previously (Jáuregui et al., 2003; Olivares-Zavaleta et al., 2006), we performed computer analyses to study the prevalence of DNA static curvature in the regulatory regions of Escherichia coli and established that most of the global transcription factors (ArcA, CRP, FIS, FNR, Lrp, IHF and H-NS), as well as some specific regulators, have a tendency to regulate operons with curved DNA sequences in their upstream regions.
Here we present a topological analysis of the ompS1 5' upstream regulatory region and the identification of a static curvature that plays an important role in the binding of H-NS and StpA, the silencer proteins of ompS1.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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, with the contribution matrices for rotational and spatial displacements reported by Satchwell et al. (1986). Secondly, centred at the maximum curvature value, the server evaluates the effect of every double point mutation in a window of 31 nucleotides (three helix turns) to select those changes that would produce a significant reduction in the intrinsic DNA curvature of the fragment. Finally, the server generates the curvature profiles of the original and mutated sequences for their comparative analysis.
Site-directed mutagenesis.
Site-directed mutageneses were performed using complementary oligonucleotides that contained the mutations predicted by MUTACURVE (Table 2). The plasmid pRO310-wt was used as template to generate pRO310-mt and pRO310-re by inverse PCR (Table 1). The expected mutations were verified by nucleotide sequencing.
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). The PCR fragments were separated by 6 % PAGE at 4 °C (polyacrylamide gels in 0.5x Tris/borate/EDTA at 4 °C, 70 V, without buffer recirculation), a condition favouring slower migration of curved DNA sequences (Falconi et al., 1993; Flores-Valdez et al., 2003; Olivares-Zavaleta et al., 2006). Gels were stained with ethidium bromide and photographed in an Alpha Imager system (Alpha Innotech).
Bacterial culture and β-galactosidase assays.
Bacteria were grown in nutrient broth (low osmolarity) or nutrient broth plus 0.3 M NaCl (high osmolarity) at 37 °C or 30 °C and collected at the mid-exponential phase. The culture conditions and microplate protein and β-galactosidase assays were as previously described (Flores-Valdez et al., 2003).
Electrophoretic mobility shift assays (EMSAs).
DNA fragments generated by PCR (100 ng) were incubated with increasing concentrations of H-NS, StpA or LeuO for 20 min at 4 °C in 20 µl. Binding buffers for each protein were described previously (De la Cruz et al., 2007). The DNA fragments were separated by electrophoresis in 6 % native polyacrylamide gels in 0.5x Tris/borate/EDTA buffer at 4 °C. Double-stranded oligonucleotides (50 ng) were incubated as above and electrophoresis was in 8 % native polyacrylamide gels at room temperature. Gels were stained with ethidium bromide and photographed in an Alpha Imager system (Alpha Innotech).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). MUTACURVE (Olivares-Zavaleta et al., 2006), a software developed to determine the topographic profile of a particular DNA region in silico, was used to further define regions with the highest degree of curvature; one of them was found between –151 and –135 bp upstream of the P1 transcriptional start point (Fig. 1A). This region was of interest for further research in this work, because it is located in the vicinity of the binding sites of two main transcription factors, LeuO and H-NS, which regulate ompS1 expression (De la Cruz et al., 2007). In addition, our previous studies showed that removal of the region from –310 to –153 had a modest effect on derepression as compared to removal of the region between –153 and –117 (Oropeza et al., 1999), which includes the curved region studied here. The advantage of the software used was that it allowed the evaluation of the effect on DNA curvature of every double point mutation that encompassed the region from –226 to –76 (fragment Fb-wt) (Fig. 1A, B).
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). First, a double mutation was introduced to diminish the extent of DNA curvature (pRO310-mt). We then used this mutated DNA as substrate for a second PCR-mediated mutagenesis to introduce the required changes, different from the wild-type sequence, which would restore the original extent of DNA curvature (pRO310-re) (Table 1). The effects of these mutations on DNA bending were evaluated by the PCR amplification of these regions (Fb-wt, Fb-mt and Fb-re) and their corresponding analysis by PAGE at 4 °C (Falconi et al., 1993; Flores-Valdez et al., 2003; Olivares-Zavaleta et al., 2006). The mutations had the expected effect on the electrophoretic migration as predicted in silico (Fig. 1A, C): the Fb-mt fragment migrated faster, consistent with an abolished or diminished curvature, while the Fb-re fragment co-migrated with Fb-wt, suggesting a restored curvature.
DNA curvature is required for the negative regulation of ompS1 expression
In order to evaluate the effect of DNA curvature on the expression of ompS1, the ompS1-lacZ reporter activity of the plasmids pRO310-wt, pRO310-mt and pRO310-re was evaluated in S. Typhi. Interestingly, the pRO310-mt fusion, carrying the ompS1 regulatory region with diminished curvature, was derepressed fivefold relative to the wild-type fusion (pRO310-wt), whereas the positive control, pRO310-re, carrying two point mutations in the same position as the ones introduced into pRO310-mt but restoring the curvature of the ompS1 regulatory region, rendered the same low expression level as the pRO310 wild-type (Figs 1 and 2A). Thus, point mutations located in precisely the same position in the ompS1 5' upstream region produced different effects on expression, depending on whether they did or did not change the extent of DNA curvature.
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; De la Cruz et al., 2007). Thus, the effect of the mutations affecting the curvature was evaluated in an hns background (STYhns99) (Fig. 2B). The pRO310-mt fusion increased ompS1 expression 40 % with respect to the wild-type (Fig. 2B). Hence, the removal of the intrinsic curvature at –151 to –135 also derepressed ompS1 expression in the hns background, although in a smaller proportion than in the wild-type background, where a fivefold effect was observed (Fig. 2A). This smaller effect could be due to the lowering of the affinity of the binding of StpA in an hns background, as shown in Fig. 5D.
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; Flores-Valdez et al., 2003). Several groups have reported that DNA static curvature is involved in the thermoregulation and osmoregulation of certain genes (Ramani et al., 1992; Kaji et al., 2003; Prosseda et al., 2004). The expression of the pRO310-mt fusion was therefore analysed in a wild-type and hns background at low and high osmolarity and at 37 °C and 30 °C (Fig. 3). As can be observed, the removal of the DNA curvature did not have a major effect on expression in these growth conditions: although a slight derepression was observed at high osmolarity in the hns background, no effect of temperature was seen (Fig. 3).
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). The maximum level of ompS1 expression was obtained when LeuO was induced at 100 µM IPTG from pFMTrcleuO-50, the same as that attained in a double hns stpA background (De la Cruz et al., 2007). Hence, the effect of curvature on LeuO-mediated regulation of ompS1 was examined by evaluating the expression of the pRO310-wt, pRO310-mt and pRO310-re fusions in the presence of cloned and expressed LeuO at different concentrations of IPTG (Fig. 4). Interestingly, the pRO310-mt fusion reached the maximum level when LeuO was induced at 50 µM IPTG, contrasting with pRO310-wt and pRO310-re, which reached the maximum level at 100 µM IPTG (Fig. 4). Furthermore, at 20 and 25 µM IPTG the expression was higher in the -mt construct than in the -wt and -re plasmids, at the same IPTG concentration. The observation that the degree of LeuO induction required to obtain the highest levels of ompS1-lacZ expression in strains carrying the plasmids with the curved ompS1 regulatory region (plasmids pRO310-wt and pRO310-re) was almost double that required for those carrying the non-curved ompS1 regulatory region (plasmid pRO310-mt) is consistent with the notion that diminution of the curvature enhanced the LeuO antagonistic effect on H-NS.
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). The corresponding F1-mt, F2-mt and F3-mt fragments contained the point mutations that diminished curvature (Fig. 1). In the presence of H-NS, the wild-type F1 fragment, which contains the whole regulatory region, shifted at 90 nM H-NS (Fig. 5B). In contrast, F1-mt shifted at 175 nM H-NS (Fig. 5B). Moreover, the shorter F2 and F3 fragments, which contain less of the 5' upstream regulatory sequences, shifted at higher H-NS concentrations than F1: at 270 and 350 nM (Fig. 5B). The corresponding F2-mt and F3-mt fragments fully shifted at 350 and 435 nM H-NS (Fig. 5B). These data show that H-NS binding is favoured by the degree of curvature and illustrate the existence of further H-NS-binding sites upstream of the DNA curvature centre.
As a comparison, the F2 fragment was analysed by EMSA with StpA and LeuO (Fig. 5D, E). F2 shifted at 900 nM and F2-mt at 1100 nM StpA; both fragments shifted at 300 nM LeuO.
We have previously described an H-NS nucleation site in the 5' regulatory region of ompS1 within the LeuO (II) binding box (Fig. 6A). Mutations in this nucleation site cause derepression of ompS1 expression in the absence of LeuO and a reduction in the H-NS binding affinity, and this site showed the highest affinity to H-NS by DNase footprinting analysis (De la Cruz et al., 2007). Moreover, this site shows homology to the H-NS nucleation site for the proU gene (AATATATCGA) (Bouffartigues et al., 2007). In contrast, mutations throughout the LeuO (I) binding box (Fig. 6A) did not have an effect on ompS1 expression in the absence of LeuO, nor did they render an altered H-NS binding (De la Cruz et al., 2007). These observations are in agreement with the experiment shown in Fig. 6B, where 50-mer double-stranded oligonucleotides encompassing the LeuO (II) or the LeuO (I) regions showed differential binding to H-NS. The LeuO (II) fragment was bound by H-NS and the LeuO (I) fragment did not bind (Fig. 6B). Most importantly, the LeuO (I) fragment contains the –151 and –135 residues of the curved region that were mutated to render either a lowering (mt) or a restoration (re) of the curvature (Fig. 1b). Thus, the curved region studied did not encompass the H-NS nucleation site.
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) is due to the lowering of the affinity of these two silencing proteins by the change in DNA curvature of the ompS1 regulatory region, and with the notion that the effect of the introduced mutations is indeed on the DNA curvature and not on the alteration of the binding of H-NS to its nucleation site. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Falconi et al., 1993; Pérez-Martín et al., 1994; Jáuregui et al., 2003; Poore & Mobley, 2003; Prosseda et al., 2004; Olivares-Zavaleta et al., 2006). Recently, the role of DNA curvature has been discussed for the promoters of the toxin and rRNA genes in Bacillus anthracis and E. coli, respectively (Hadjifrangiskou & Koehler, 2008; Pul et al., 2008). For example, in the case of virF, encoding an activator of the AraC/XylS familiy, it was found that the intrinsic curvature acts as a thermoswitch, being flanked by two H-NS-binding sites forming a repressor loop (Prosseda et al., 2004). A second example of a curvature-dependent transcription regulation has been reported for the E. coli ompF gene, where IHF has been found to bind upstream of its promoter, increasing the degree of DNA curvature, in a region relevant for negative regulation at high osmolarity (Ramani et al., 1992).
A common approach taken to define the role of curved DNA regions in transcription regulation is based on serial deletions or replacements of the 5' upstream regulatory region (Cobbett et al., 1989; Falconi et al., 1993; Asayama et al., 2002; Kaji et al., 2003; Prosseda et al., 2004). This procedure introduces the considerable risk of modifying important regions that might not have been characterized yet. For this reason, in our study we employed a new and more precise approach that considers, in the first instance, an in silico analysis to identify the extent of DNA curvature at each position of the ompS1 regulatory region. This was followed by site-directed mutagenesis on two specific nucleotides that reduce the extent of curvature (mt; Fig. 1B). Since both DNA intrinsic curvature and protein–DNA recognition are sequence-dependent events, changing the DNA sequence can alter both intrinsic DNA curvature and the sequence-dependent protein binding. For this reason, our study included two different and important internal controls. As our first internal control, we performed site-directed mutagenesis on the same two nucleotides as for mt in order to restore the curvature (re; Fig. 1B). It is worth mentioning that the computer design of our mutagenesis protocol provided the minimal number of changes in the DNA regulatory region. In addition, as our second internal control, we demonstrated by EMSAs, that the H-NS nucleation site is not present on the DNA regulatory region used in our point mutation analysis (LeuO (I) binding box; Fig. 6). Thus, the observations reported here are consistent with the concept that the effect of these nucleotide changes on the regulation of ompS1 expression is due to the lowering of the DNA curvature in the region.
Using the wild-type and the aforementioned non-curved and curved mutagenized ompS1 regulatory regions, we obtained in vivo and in vitro evidence that supports the role of a curved DNA sequence in the repression of ompS1 expression. First, our theoretically predicted effects of the point mutation to diminish (mt) and restore (re) the intrinsic curvature of the ompS1 regulatory region were verified by PAGE mobility analysis at 4 °C (Fig. 1). Secondly, our EMSA experiments demonstrated that the affinity of H-NS for the regulatory region is diminished following point mutagenesis that lowers the curvature and that there are H-NS binding sites upstream of the H-NS nucleation centre (Fig. 5). In further support of this notion, fragment F4 (–114 to +27), which contains only the H-NS nucleation site and no further upstream sequences, including the curved region, did not shift with H-NS. Similarly, StpA binding was reduced for the non-curved ompS1 regulatory region (Fig. 5D) and, interestingly, LeuO affinity was not affected by the extent of curvature (Fig. 5E). Finally, there was a fivefold increase in the ompS1 activity as assayed with a lacZ reporter fusion, upon removal of curvature in plasmid pRO310-mt (Fig. 2). This upregulation effect was not observed in our internal control of strains carrying plasmid pRO310-re with restored DNA curvature (Fig. 2).
All the results show that the curved region located at –151 to –135 in the ompS1 regulatory region participates in the repression of ompS1 transcription initiation. We previously accounted for the repression of ompS1 expression by the formation of an H-NS nucleofilament (De la Cruz et al., 2007). The new findings reported here now support a DNA-curvature-dependent bridging model that would account for full repression of ompS1 expression (Fig. 7A), where the role of the curvature would be to facilitate the formation of DNA–H-NS–DNA bridges between downstream and upstream sites. Chromatin organization by loop domain formation conducive to DNA bridging has been discussed previously in detail (Dame et al., 2005, 2006; Noom et al., 2007; Dorman & Kane, 2009). In the F-mt fragments, where the curvature has been lowered by two point mutations, H-NS would still be binding, albeit at lower affinity, and could still cause some repression of expression by the formation of a nucleofilament-type structure (Figs 5B, C and 7B).
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) is consistent with our previous model of regulation for the ompS1 porin gene in which LeuO acts as an antirepressor of H-NS and StpA (De la Cruz et al., 2007), and where changes in DNA structural topology also affect repression. H-NS has been proposed to selectively silence a great number of horizontally acquired genes (Lucchini et al., 2006; Navarre et al., 2006) and also to act as a modulator of environmentally regulated gene expression (Atlung & Ingmer, 1997). H-NS modulates other important biological processes, such as DNA recombination, DNA replication and organization of the bacterial chromosome (Pérez-Martín et al., 1994; Jáuregui et al., 2003).
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ACKNOWLEDGEMENTS |
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Edited by: R. G. Sawers
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 23 February 2009;
revised 20 April 2009;
accepted 27 April 2009.
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