Characterization of DalS, an ATP-binding Cassette Transporter for d-Alanine, and Its Role in Pathogenesis in Salmonella enterica

Osborne, Suzanne E.; Tuinema, Brian R.; Mok, Mac C.Y.; Lau, Pui Sai; Bui, Nhat Khai; Tomljenovic-Berube, Ana M.; Vollmer, Waldemar; Zhang, Kun; Junop, M.S.; Coombes, Brian K.

doi:10.1074/jbc.m112.348227

Cited by 22 publications

(41 citation statements)

References 29 publications

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“…Another recent hypothesis for the genes involved in salmonellosis, focuses on the ABC transporter genes and the ability of pathogens to acquire nutrients for survival during host infection [68], [69]. Our study shows variability in an ABC transporter for methionine specific for clades 1 and 2 (Table 4).…”

Section: Discussionmentioning

confidence: 63%

“…Our study shows variability in an ABC transporter for methionine specific for clades 1 and 2 (Table 4). The S. Enteritidis model that Osborne et al [68] tested for in vivo with an ABC transporter of alanine is similar to the natural variability for a similar gene in the implicated farm and associated clinical isolates. If this model, affirmed in cell culture studies, holds in chickens, then infections in chickens and eggs in 2010 may be related to the ability of S. Enteritidis to survive in a poultry host due to the enhanced access to methionine.…”

Section: Discussionmentioning

confidence: 89%

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On the Evolutionary History, Population Genetics and Diversity among Isolates of Salmonella Enteritidis PFGE Pattern JEGX01.0004

et al. 2013

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Facile laboratory tools are needed to augment identification in contamination events to trace the contamination back to the source (traceback) of Salmonella enterica subsp. enterica serovar Enteritidis (S. Enteritidis). Understanding the evolution and diversity within and among outbreak strains is the first step towards this goal. To this end, we collected 106 new S. Enteriditis isolates within S. Enteriditis Pulsed-Field Gel Electrophoresis (PFGE) pattern JEGX01.0004 and close relatives, and determined their genome sequences. Sources for these isolates spanned food, clinical and environmental farm sources collected during the 2010 S. Enteritidis shell egg outbreak in the United States along with closely related serovars, S. Dublin, S. Gallinarum biovar Pullorum and S. Gallinarum. Despite the highly homogeneous structure of this population, S. Enteritidis isolates examined in this study revealed thousands of SNP differences and numerous variable genes (n = 366). Twenty-one of these genes from the lineages leading to outbreak-associated samples had nonsynonymous (causing amino acid changes) changes and five genes are putatively involved in known Salmonella virulence pathways. While chromosome synteny and genome organization appeared to be stable among these isolates, genome size differences were observed due to variation in the presence or absence of several phages and plasmids, including phage RE-2010, phage P125109, plasmid pSEEE3072_19 (similar to pSENV), plasmid pOU1114 and two newly observed mobile plasmid elements pSEEE1729_15 and pSEEE0956_35. These differences produced modifications to the assembled bases for these draft genomes in the size range of approximately 4.6 to 4.8 mbp, with S. Dublin being larger (∼4.9 mbp) and S. Gallinarum smaller (4.55 mbp) when compared to S. Enteritidis. Finally, we identified variable S. Enteritidis genes associated with virulence pathways that may be useful markers for the development of rapid surveillance and typing methods, potentially aiding in traceback efforts during future outbreaks involving S. Enteritidis PFGE pattern JEGX01.0004.

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Section: Discussionmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 89%

On the Evolutionary History, Population Genetics and Diversity among Isolates of Salmonella Enteritidis PFGE Pattern JEGX01.0004

et al. 2013

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“…In addition, our proteomic data indicated substantial (ϳ8-fold) elevation of DalS, though a slight decrease of its transcriptional level was found (6). Interestingly, it has been shown in an animal model that DalS was required for Salmonella survival and fitness (66). Discrepancies between mRNA and protein expression data can be explained by minor differences associated with bacterium/cell culturing as well as with sample preparations.…”

Section: Discussionmentioning

confidence: 68%

Proteomic Analyses of Intracellular Salmonella enterica Serovar Typhimurium Reveal Extensive Bacterial Adaptations to Infected Host Epithelial Cells

Liu

Zhang

et al. 2015

Infect Immun

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Salmonella species can gain access into nonphagocytic cells, where the bacterium proliferates in a unique membrane-bounded compartment. In order to reveal bacterial adaptations to their intracellular niche, here we conducted the first comprehensive proteomic survey of Salmonella isolated from infected epithelial cells. Among ϳ3,300 identified bacterial proteins, we found that about 100 proteins were significantly altered at the onset of Salmonella intracellular replication. In addition to substantially increased iron-uptake capacities, bacterial high-affinity manganese and zinc transporters were also upregulated, suggesting an overall limitation of metal ions in host epithelial cells. We also found that Salmonella induced multiple phosphate utilization pathways. Furthermore, our data suggested upregulation of the two-component PhoPQ system as well as of many downstream virulence factors under its regulation. Our survey also revealed that intracellular Salmonella has increased needs for certain amino acids and biotin. In contrast, Salmonella downregulated glycerol and maltose utilization as well as chemotaxis pathways. While infectious diseases continue to be a major threat to human health, there is an urgent need in rational design and development of new treatment strategies. As a model for studying bacterial pathogenesis, Salmonella spp. cause millions of infections per year ranging from food poisoning to life-threatening systemic typhoid fever (1). Central to its pathogenesis is a syringelike structure known as the type III secretion system (T3SS), which delivers bacterial proteins called effectors directly into eukaryotic host cells (2, 3). The injected proteins are able to modulate various host cellular functions, and over the years extensive studies have been carried out on these effector proteins and/or their interacting host targets. While these studies have contributed substantially to our initial understanding of infection biology, daunting challenges are encountered because conventional reductionism-based studies certainly cannot explain the complex multifactorial nature of host-pathogen interactions (4). Systems-level analyses can provide a panoramic view of the functional host-pathogen interplay and thus are promising in this regard.During infection, the intracellular environment is likely to be very different from what bacteria encounter in rich culture media. It has long been known that various nutritional and environmental differences within host cells force bacterial pathogens to reprogram their gene expression. In fact, transcriptomic studies of intracellular Salmonella within infected macrophages and epithelial cells contributed to our initial understanding of bacterial adaptations in the host environment (5, 6). Because proteins are the final gene products and their changes may not correlate with those of mRNA, direct readout of the bacterial proteome is highly desired. Such measurements, however, have been technically challenging due to the presence of vast amounts of host proteins (7). As a ...

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“…In addition, the ΔdalS strain showed decreased replication in the RAW 264.7 macrophage cells compared to the wildtype strain. The mean survival time of C57BL/6 mice orally infected with wildtype S. Typhimurium was a day shorter than mice infected with the dalS mutant [88]. …”

Section: Introductionmentioning

confidence: 99%

Selective substrate uptake: The role of ATP-binding cassette (ABC) importers in pathogenesis

Tanaka

Song

Mason

et al. 2018

Biochimica et Biophysica Acta (BBA) - Biomembranes

124

102

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The uptake of nutrients, including metals, amino acids and peptides are required for many biological processes. Pathogenic bacteria scavenge these essential nutrients from microenvironments to survive within the host. Pathogens must utilize a myriad of mechanisms to acquire these essential nutrients from the host while mediating the effects of toxicity. Bacteria utilize several transport proteins, including ATP-binding cassette (ABC) transporters to import and expel substrates. ABC transporters, conserved across all organisms, are powered by the energy from ATP to move substrates across cellular membranes. In this review, we will focus on nutrient uptake, the role of ABC importers at the host-pathogen interface, and explore emerging therapies to combat pathogenesis. This article is part of a Special Issue entitled: Beyond the Structure-Function Horizon of Membrane Proteins edited by Ute Hellmich, Rupak Doshi and Benjamin McIlwain.

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Characterization of DalS, an ATP-binding Cassette Transporter for d-Alanine, and Its Role in Pathogenesis in Salmonella enterica

Cited by 22 publications

References 29 publications

On the Evolutionary History, Population Genetics and Diversity among Isolates of Salmonella Enteritidis PFGE Pattern JEGX01.0004

On the Evolutionary History, Population Genetics and Diversity among Isolates of Salmonella Enteritidis PFGE Pattern JEGX01.0004

Proteomic Analyses of Intracellular Salmonella enterica Serovar Typhimurium Reveal Extensive Bacterial Adaptations to Infected Host Epithelial Cells

Selective substrate uptake: The role of ATP-binding cassette (ABC) importers in pathogenesis

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