Transcriptional Phase Variation of a Type III Restriction-Modification System in
            <i>Helicobacter pylori</i>

Vries, Nicolette de; Duinsbergen, Dirk; Kuipers, Ernst J.; Pot, Raymond G.J.; Wiesenekker, Patricia; Penn, Charles W.; Vliet, Arnoud H. M. van; Vandenbroucke-Grauls, Christina M. J. E.; Kusters, Johannes G.

doi:10.1128/jb.184.23.6615-6624.2002

Cited by 80 publications

(59 citation statements)

References 48 publications

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“…The H. pylori LPS biosynthesis enzyme jhp0562 glycosyltransferase functions in the synthesis of both type I and type II Lewis (Le) antigens, which are present on the LPS of the bacterial outer membrane (33). Via intragenomic recombination of jhp0562, diverse Le antigens are generated, and this glycosyltransferase contributes to the process of phase variation in H. pylori (33)(34)(35). Phase variation is one of the mechanisms used by H. pylori to escape the host immune response and to persist in the stomach.…”

Section: Resultsmentioning

confidence: 99%

“…It creates phenotypical variation in a bacterial population by the reversible process of switching a gene on and off. Phase-variable bacterial genes, such as LPS biosynthesis genes, play roles in bacterial pathogenesis and virulence (34,35). Moreover, the presence of jhp0562 has been associated with peptic ulcer disease in children (33,36 Table S3 in the supplemental material]).…”

Section: Resultsmentioning

confidence: 99%

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Divergence between the Highly Virulent Zoonotic Pathogen Helicobacter heilmannii and Its Closest Relative, the Low-Virulence “Helicobacter ailurogastricus” sp. nov

et al. 2016

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h Helicobacter heilmannii naturally colonizes the stomachs of dogs and cats and has been associated with gastric disorders in humans. Nine feline Helicobacter strains, classified as H. heilmannii based on ureAB and 16S rRNA gene sequences, were divided into a highly virulent and a low-virulence group. The genomes of these strains were sequenced to investigate their phylogenetic relationships, to define their gene content and diversity, and to determine if the differences in pathogenicity were associated with the presence or absence of potential virulence genes. The capacities of these helicobacters to bind to the gastric mucosa were investigated as well. Our analyses revealed that the low-virulence strains do not belong to the species H. heilmannii but to a novel, closely related species for which we propose the name Helicobacter ailurogastricus. Several homologs of H. pylori virulence factors, such as IceA1, HrgA, and jhp0562-like glycosyltransferase, are present in H. heilmannii but absent in H. ailurogastricus. Both species contain a VacA-like autotransporter, for which the passenger domain is remarkably larger in H. ailurogastricus than in H. heilmannii. In addition, H. ailurogastricus shows clear differences in binding to the gastric mucosa compared to H. heilmannii. These findings highlight the low-virulence character of this novel Helicobacter species. Helicobacter pylori is considered one of the most successful human pathogens. Infection with this agent has been associated with a wide range of gastric disorders. However, H. pylori is not the only Helicobacter species causing gastric disease in humans. Helicobacter heilmannii (sensu stricto), a zoonotic bacterium naturally colonizing the stomachs of cats and dogs, has been associated with gastritis, peptic and duodenal ulcers, and mucosa-associated lymphoid tissue (MALT) lymphoma in humans (1-6). This Helicobacter species is highly prevalent in the stomachs of clinically healthy cats and dogs as well as in those of animals showing chronic active gastritis (1, 4). Its pathogenic significance in these animals remains unclear and is probably strain dependent or related to host differences (1).Little information is available regarding the pathogenesis of H. heilmannii infections in humans (1, 7). A recent experimental infection study, using Mongolian gerbils as an in vivo model to study Helicobacter-related gastric pathology in humans, investigated the colonization capacities and virulence of nine different Helicobacter strains (8). These helicobacters had been isolated from the gastric mucosae of stray cats and had been classified as H. heilmannii on the basis of the ureAB and 16S rRNA gene sequences (9). At 9 weeks postinfection, the induction of an antrum-dominant chronic active gastritis associated with the formation of lymphocytic aggregates and upregulation of the proinflammatory cytokine interleukin 1␤ (IL-1␤) was shown for seven strains. However, differences in the expression of IL-1␤ were noted, together with differences in the intensity of the obser...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Divergence between the Highly Virulent Zoonotic Pathogen Helicobacter heilmannii and Its Closest Relative, the Low-Virulence “Helicobacter ailurogastricus” sp. nov

et al. 2016

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“…Pathogenic bacteria use the phase variability of gene expression to evade the host immune system. Based on sequence analysis and biochemical evidence, many type I and III enzymes of Bacteroides fragilis as well as Haemophilus, Helicobacter, Mycoplasma, and Neisseria species were found to be potentially phase variable (176)(177)(178)(179)(180)(181). The biological significance of R-M systems that exhibit phase variability is not completely understood.…”

Section: Functions Of Phase-variable R-m Systemsmentioning

confidence: 99%

Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense

Vasu

Nagaraja

2013

Microbiol Mol Biol Rev

509

462

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SUMMARY Restriction-modification (R-M) systems are ubiquitous and are often considered primitive immune systems in bacteria. Their diversity and prevalence across the prokaryotic kingdom are an indication of their success as a defense mechanism against invading genomes. However, their cellular defense function does not adequately explain the basis for their immaculate specificity in sequence recognition and nonuniform distribution, ranging from none to too many, in diverse species. The present review deals with new developments which provide insights into the roles of these enzymes in other aspects of cellular function. In this review, emphasis is placed on novel hypotheses and various findings that have not yet been dealt with in a critical review. Emerging studies indicate their role in various cellular processes other than host defense, virulence, and even controlling the rate of evolution of the organism. We also discuss how R-M systems could have successfully evolved and be involved in additional cellular portfolios, thereby increasing the relative fitness of their hosts in the population.

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“…This kind of repeat indicates that these genes are possibly regulated by phase variation. Phase variation in the Type III R-M system has been observed in several bacterial species, including M. pulmonis (De Bolle et al, 2000;de Vries et al, 2002;Rocha and Blanchard, 2002;Seib et al, 2002) and also in M. hyopneumoniae (this paper).…”

Section: Discussionmentioning

confidence: 99%

“…The high mutation rates in these repetitive sequences is due to slippage within the DNA repeats during replication, resulting in changes in the number of repeats (Henderson et al, 1999). Phase variation has been described in genes involved in LPS biosynthesis, cell-surface-associated proteins and DNA restriction-modification systems (Saunders et al, 1998), and can occur at the transcriptional or the translational level (de Vries et al 2002). This kind of repeat indicates that these genes are possibly regulated by phase variation.…”

Section: Discussionmentioning

confidence: 99%

Restriction-modification systems in Mycoplasma spp

2007

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Restriction and Modification (R-M) systems are present in all Mycoplasma species sequenced so far. The presence of these genes poses barriers to gene transfer and could protect the cell against phage infections. The number and types of R-M genes between different Mycoplasma species are variable, which is characteristic of a polymorphism. The majority of the CDSs code for Type III R-M systems and particularly for methyltransferase enzymes, which suggests that functions other than the protection against the invasion of heterologous DNA may exist. A possible function of these enzymes could be the protection against the invasion of other but similar R-M systems. In Mycoplasma hyopneumoniae strain J, three of the putative methyltransferase genes were clustered in a region forming a genomic island. Many R-M CDSs were mapped in the vicinity of transposable elements suggesting an association between these genes and reinforcing the idea of R-M systems as mobile selfish DNA. Also, many R-M genes present repeats within their coding sequences, indicating that their expression is under the control of phase variation mechanisms. Altogether, these data suggest that R-M systems are a remarkable characteristic of Mycoplasma species and are probably involved in the adaptation of these bacteria to different environmental conditions.

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Transcriptional Phase Variation of a Type III Restriction-Modification System in Helicobacter pylori

Cited by 80 publications

References 48 publications

Divergence between the Highly Virulent Zoonotic Pathogen Helicobacter heilmannii and Its Closest Relative, the Low-Virulence “Helicobacter ailurogastricus” sp. nov

Divergence between the Highly Virulent Zoonotic Pathogen Helicobacter heilmannii and Its Closest Relative, the Low-Virulence “Helicobacter ailurogastricus” sp. nov

Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense

Restriction-modification systems in Mycoplasma spp

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