DNA Adenine Methylation Regulates Virulence Gene Expression in
            <i>Salmonella enterica</i>
            Serovar Typhimurium

Balbontín, Roberto; Rowley, Gary; Pucciarelli, M. Graciela; López‐Garrido, Javier; Wormstone, Yvette M.; Lucchini, Sacha; Portillo, Francisco García‐del; Hinton, Jay C. D.; Casadesús, Josep

doi:10.1128/jb.00847-06

Cited by 109 publications

(151 citation statements)

References 64 publications

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“…(Figure 2). This observation confirmed that SPI-1 expression is entirely under Dam methylation control as previously proposed (Balbontin et al 2006), but did not provide any hint about the target(s) of Dam-dependent regulation. In silico examination of GATC site distribution in or near the hilA, hilC, hilD, and invF genes was likewise uninformative (data not shown).…”

Section: Methodssupporting

confidence: 88%

“…Because the methylation state of critical GATC sites can control binding of RNA polymerase and transcription factors, differences in gene expression between Dam 1 and Dam À hosts usually provide evidence for transcriptional regulation (Roberts et al 1985;Kü cherer et al 1986;Blyn et al 1989;Torreblanca and Casadesus 1996;Haagmans and Van Der Woude Figure 7.-(A) Camacho and Casadesus 2002;Waldron et al 2002;Balbontin et al 2006;Jakomin et al 2008). However, several lines of evidence suggest that Damdependent regulation of hilD expression is not transcriptional: (i) a transcriptional hilDTlac fusion is expressed at similar levels in Dam 1 and Dam À hosts ( Figure 4); (ii) reduced levels of both hilD mRNA and HilD protein are, however, found in Dam À mutants ( Figures 2 and 4); (iii) reduced amounts of hilD mRNA are found in a Dam À mutants when the hilD gene is expressed from a heterologous promoter ( Figure 5); (iv) SPI-1 remains under Dam-dependent control when hilD transcription is activated by tetracycline ( Figure 5); and (v) lack of DNA adenine methylation results in hilD mRNA instability (Figure 6).…”

Section: Levels Of the Spi-1 Transcription Factorsmentioning

confidence: 99%

“…Impaired invasion of epithelial cells by Dam À mutants has been confirmed in tissue cultures and has been tentatively correlated with reduced secretion of invasion effectors encoded on Salmonella pathogenicity island 1 (SPI-1) (Garcia-Del Portillo et al 1999). High-throughput analysis of gene expression has confirmed that SPI-1 is transcribed at lowered levels in Dam À mutants (Balbontin et al 2006). SPI-1 is an $40-kb gene cluster containing at least 37 genes (Lostroh and Lee 2001;Altier 2005;Jones 2005), located at centisome 63 on the S. enterica chroSupporting information is available online at http:/ /www.genetics.org/ cgi/content/full/genetics.109.108985/DC1.…”

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confidence: 99%

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Regulation ofSalmonella entericaPathogenicity Island 1 by DNA Adenine Methylation

López‐Garrido

Casadesús

2010

Genetics

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À mutants when hilD is transcribed from a heterologous promoter; (ii) increased hilD mRNA turnover is observed in Dam À mutants; (iii) lack of the Hfq RNA chaperone enhances hilD mRNA instability in Dam À mutants; and (iv) lack of the RNA degradosome components polynucleotide phosphorylase and ribonuclease E suppresses hilD mRNA instability in a Dam À background. Our report of Dam-dependent control of hilD mRNA stability suggests that DNA adenine methylation plays hitherto unknown roles in post-transcriptional control of gene expression.

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Section: Methodssupporting

confidence: 88%

Section: Levels Of the Spi-1 Transcription Factorsmentioning

confidence: 99%

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confidence: 99%

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Regulation ofSalmonella entericaPathogenicity Island 1 by DNA Adenine Methylation

López‐Garrido

Casadesús

2010

Genetics

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“…Our data demonstrate that phase variation in Cj0170 affects both motility and virulence ( (Balbontín et al, 2006;Fälker et al, 2005;Oshima et al, 2002;Srikhanta et al, 2010); genes regulated in this fashion belong to a 'phase varion'. Since Cj0170 does not appear to affect flagellar structure or assembly, genes involved in chemotaxis (e.g.…”

Section: Discussionmentioning

confidence: 99%

Passage of Campylobacter jejuni through the chicken reservoir or mice promotes phase variation in contingency genes Cj0045 and Cj0170 that strongly associates with colonization and disease in a mouse model

et al. 2012

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Human illness due to Camplyobacter jejuni infection is closely associated with consumption of poultry products. We previously demonstrated a 50 % shift in allele frequency (phase variation) in contingency gene Cj1139 (wlaN) during passage of C. jejuni NCTC11168 populations through Ross 308 broiler chickens. We hypothesized that phase variation in contingency genes during chicken passage could promote subsequent colonization and disease in humans. To test this hypothesis, we passaged C. jejuni strains NCTC11168, 33292, 81-176, KanR4 and CamR2 through broiler chickens and analysed the ability of passaged and non-passaged populations to colonize C57BL6 IL-10-deficient mice, our model for human colonization and disease. We utilized fragment analysis and nucleotide sequence analysis to measure phase variation in contingency genes. Passage through the chicken reservoir promoted phase variation in five specific contingency genes, and these 'successful' populations colonized mice. When phase variation did not occur in these same five contingency genes during chicken passage, these 'unsuccessful' populations failed to colonize mice. Phase variation during chicken passage generated small insertions or deletions (indels) in the homopolymeric tract (HT) in contingency genes. Singlecolony isolates of C. jejuni strain KanR4 carrying an allele of contingency gene Cj0170 with a 3These authors contributed equally to this work. Two supplementary tables, listing PCR primer sequences for fragment and sequence analysis used in this study, and results of sequence and fragment analysis to confirm large shifts in allele frequency, with a supplementary reference, are available with the online version of this paper. 10G HT colonized mice at high frequency and caused disease symptoms, whereas single-colony isolates carrying the 9G allele failed to colonize mice. Supporting results were observed for the successful 9G allele of Cj0045 in strain 33292. These data suggest that phase variation in Cj0170 and Cj0045 is strongly associated with mouse colonization and disease, and that the chicken reservoir can play an active role in natural selection, phase variation and disease.

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“…Salmonella dam mutants show reduced invasion of epithelial cells, 30 which correlates with reduced expression of genes necessary for invasion. 31,32 Thus, if the insertion in damX had a polar effect on dam expression, invasion would be reduced.…”

Section: Phenotypes Of Damx Mutantsmentioning

confidence: 99%

The DamX protein ofEscherichia coliandSalmonella enterica

López‐Garrido

Casadesús

2010

Gut Microbes

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DNA Adenine Methylation Regulates Virulence Gene Expression in Salmonella enterica Serovar Typhimurium

Cited by 109 publications

References 64 publications

Regulation ofSalmonella entericaPathogenicity Island 1 by DNA Adenine Methylation

Regulation ofSalmonella entericaPathogenicity Island 1 by DNA Adenine Methylation

Passage of Campylobacter jejuni through the chicken reservoir or mice promotes phase variation in contingency genes Cj0045 and Cj0170 that strongly associates with colonization and disease in a mouse model

The DamX protein ofEscherichia coliandSalmonella enterica

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