<i>Yersinia pestis</i> kills <i>Caenorhabditis elegans</i> by a biofilm‐independent process that involves novel virulence factors

Styer, Katie L.; Hopkins, Gregory; Bartra, Sara Schesser; Plano, Gregory V.; Frothingham, Richard; Aballay, Alejandro

doi:10.1038/sj.embor.7400516

Cited by 39 publications

(39 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Several genes of P. aeruginosa, S. aureus, S. marcescens, and Yersinia pestis have been newly identified and found to be involved in the pathogenicity of C. elegans, and some have also been found to be essential for virulence in the mammalian system 4,14,29,33) . However, the bacterial pathogenicity observed in C. elegans models may reflect other virulence-related aspects rather than enteropathogenicity; although the current observations do not necessarily exclude the possibility that the characteristics associated with nematocidal activity may be prerequisites for some human enteropathogens.…”

Section: Discussionmentioning

confidence: 99%

Evaluation of Caenorhabditis elegans as the Host in an Infection Model for Food-borne Pathogens

香織¹,

智佳子²,

高紀³

et al. 2008

Jpn. J. Food Microbiol.

View full text Add to dashboard Cite

The bacteriophagous nematode Caenorhabditis elegans has been recognized as a surrogate host for human pathogens. The aim of this study was to examine whether food-borne pathogens are pathogenic in nematodes. Young adult worms were allocated onto peptone-free medium covered with a bacterial suspension of each pathogen. The plates were incubated and as the number of live and dead worms scored at least every 24 h. Twelve of the 14 pathogenic strains, namely Aeromonas sobria, the diarrheagenic Escherichia coli strains (enteroaggregative E. coli, enterohemorrhagic E. coli, enteropathogenic E. coli, enterotoxigenic E. coli, enteroaggregative E. coli heat-stable enterotoxin 1 gene-possessing E. coli, and di#usely adherent E. coli), Listeria monocytogenes, Salmonella Enteritidis, Staphylococcus aureus, Vibrio parahaemolyticus, and Yersinia enterocolitica reduced the survival rate of worms to varying degrees. The remaining 2 strains, Bacillus cereus and enteroinvasive E. coli, did not. Thus, food-borne pathogens can infect and proliferate within bacteriophagous nematodes on peptone-free medium to the same extent as reported with conventional peptone-containing medium. However, the non-enteropathogenic E. coli strain HS and deletion mutants of L. monocytogenes, which have lost their virulence in the murine model, were also still nematocidal. Although this nematode could be an alternative host for these pathogens, the nematocidal activity of these pathogens may not necessarily reflect enteropathogenicity in humans. Pathogens and the virulence genes to be analyzed must be carefully selected before using this alternative host.Key words: C. elegans, Enteric pathogen, Virulence, Screening, Infection model Introduction A variety of experimental models have been developed to study microbial virulence or the pathogenicity of protein toxins. However, due to increasing ethical considerations as well as economic reasons, the use of mammalian hosts is decreasing in popularity, and the establishment of e#ective alternative non-mammalian systems is urgently required.There has recently been increasing interest in the soil nematode Caenorhabditis elegans as a possible host of human pathogenic bacteria, since it was reported by Ausubel et al. in 1999 that Pseudomonas aeruginosa caused fatal infection of C. elegans 31) . C. elegans has also been reported as a successful model for the investigation of virulence-associated factors of human pathogens such as Burkholderia pseudomallei 10) , Cryptococcus neoformans 19) , Enterococcus faecalis 27) , enteropathogenic Escherichia coli 2, 16) , Listeria monocytogenes 34) , P. aeruginosa 32) , Serratia marcescens 14) , Shigella flexneri 6) , Staphylococcus aureus 11,28) , and Vibrio vulnificus 9) .We recognized nematodes as a potential new surrogate host, and the degree of similarity between this nematode, C. elegans, and humans is greater than expected 17) . In the above-cited reports, the human pathogens and associated ῍ Ί̮ ῌ558ῌ8585 ̮ῒ ̮ῐῑ̮Ὶ 3ῌ3ῌ138 ῖῚ̮Ῐῗ̮Ῑ῏῎ΐ Jpn.

show abstract

Section: Discussionmentioning

confidence: 99%

Evaluation of Caenorhabditis elegans as the Host in an Infection Model for Food-borne Pathogens

香織¹,

智佳子²,

高紀³

et al. 2008

Jpn. J. Food Microbiol.

View full text Add to dashboard Cite

show abstract

“…Infection of C. elegans was accomplished by transferring nematodes, propagated on E. coli OP50, onto bacterial lawns of Y. pestis KIM5. In previous studies, we have demonstrated that following ingestion Y. pestis establishes a persistent infection in the C. elegans intestine (8). Even though C. elegans is not known to be a natural host for Y. pestis, this persistent colonization of the nematode intestine by Y. pestis allows the host to properly recognize and respond to pathogen infection.…”

Section: Identification Of Inducible Immune Responses To Y Pestismentioning

confidence: 96%

“…Once in the gut, however, pathogenic bacteria can overcome innate immune responses to proliferate and kill C. elegans. Infection of C. elegans with Y. pestis KIM5 leads to a persistent and lethal colonization of the nematode intestine (8). In addition, similar virulence factors are required for pathogenicity in nematodes and mice (8).…”

mentioning

confidence: 99%

“…Infection of C. elegans with Y. pestis KIM5 leads to a persistent and lethal colonization of the nematode intestine (8). In addition, similar virulence factors are required for pathogenicity in nematodes and mice (8). Infectivity and persistence of Y. pestis KIM5 in the nematode makes C. elegans an attractive whole animal system for studying the host response to infection with the plague bacterium.…”

mentioning

confidence: 99%

See 1 more Smart Citation

A Conserved PMK-1/p38 MAPK Is Required in Caenorhabditis elegans Tissue-specific Immune Response to Yersinia pestis Infection

Bolz

Tenor

Aballay

2010

Journal of Biological Chemistry

Self Cite

128

125

View full text Add to dashboard Cite

Recently evolved from enteropathogenic Yersinia pseudotuberculosis, Yersinia pestis acts as a blood-borne pathogen capable of parasitizing insects and causing systemic disease in mammals (1, 2). Y. pestis has acquired a variety of complex strategies to overcome defense responses in different hosts to ensure its multiplication and survival (3-5). Although a number of virulence determinants contributing to Y. pestis persistence in mammals have been identified, interactions between Y. pestis and the host immune system remain poorly understood.During its vector-mammal transmission cycle, Y. pestis must evade components of innate immunity in both insects and mammals. One of the initial immune responses against pathogens in vertebrates and invertebrates alike is the inducible humoral defense, including the production of antimicrobial peptides and reactive oxygen species (6, 7). These inducible effectors, possessing potent antimicrobial activity, are components of the phylogenetically ancient innate immune system that predates the origins of adaptive immunity. Evolutionary conservation among pathogen recognition receptors and signaling pathways contributing to the inducible immune response has permitted the use of alternative model hosts to study innate immunity.In recent years, the nematode Caenorhabditis elegans has become an attractive alternative model host to study certain aspects of bacterial pathogenesis and innate immunity. Even though C. elegans lacks professional immune cells, it lives in soil environments where it is in contact with soil-borne microbes and has evolved physiological mechanisms to respond to different pathogens by activating the expression of innate immune response genes that are conserved across metazoans. Typically, C. elegans is grown in the laboratory by feeding them Escherichia coli. E. coli is effectively disrupted by the C. elegans pharyngeal grinder, and almost no intact bacterial cells can be found in the intestinal lumen. Once in the gut, however, pathogenic bacteria can overcome innate immune responses to proliferate and kill C. elegans. Infection of C. elegans with Y. pestis KIM5 leads to a persistent and lethal colonization of the nematode intestine (8). In addition, similar virulence factors are required for pathogenicity in nematodes and mice (8). Infectivity and persistence of Y. pestis KIM5 in the nematode makes C. elegans an attractive whole animal system for studying the host response to infection with the plague bacterium.In this study, we examined the transcriptional response of C. elegans during infection with Y. pestis KIM5 to better understand conserved innate responses contributing to host defense during early stages of infection. Our results demonstrate a strong transcriptional response against Y. pestis highlighted by the induction of immune-related effectors that are predominantly regulated by PMK-1/p38. In C. elegans, as well as in other animals, PMK-1/p38 is likely expressed in a range of tissues where it can regulate immune responses at the cell-autonomous level ...

show abstract

“…Wild-type and arr-1(ok401) animals exhibited similar pumping rates on P. aeruginosa, indicating that they are exposed to a comparable dose of pathogen (data not shown). To determine whether the enhanced immune response caused by mutation in the arr-1 gene is specific to P. aeruginosa, we exposed arr-1(ok401) animals to S. enterica and Y. pestis, two Gram-negative pathogens known to kill C. elegans (24,25). As shown in Fig.…”

Section: Arr-1 Signaling Regulates Pathogen Resistance and Lifespanmentioning

confidence: 99%

Endoplasmic Reticulum Stress Pathway Required for Immune Homeostasis Is Neurally Controlled by Arrestin-1

Singh

Aballay

2012

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

Background: GPCRs function in the C. elegans nervous system to control immunity. Results: Arrestin-1, the only GPCR adaptor in C. elegans, functions in the nervous system to control immunity. Conclusion: Neural arrestin-1 signal regulates immunity. Significance: Our data underscore the importance of the nervous system in the control of longevity and immune homeostasis and suggest that overlapping and distinct neural circuits control these processes.

show abstract

Yersinia pestis kills Caenorhabditis elegans by a biofilm‐independent process that involves novel virulence factors

Cited by 39 publications

References 37 publications

Evaluation of Caenorhabditis elegans as the Host in an Infection Model for Food-borne Pathogens

Evaluation of Caenorhabditis elegans as the Host in an Infection Model for Food-borne Pathogens

A Conserved PMK-1/p38 MAPK Is Required in Caenorhabditis elegans Tissue-specific Immune Response to Yersinia pestis Infection

Endoplasmic Reticulum Stress Pathway Required for Immune Homeostasis Is Neurally Controlled by Arrestin-1

Contact Info

Product

Resources

About