Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans

Meisel, Joshua D.; Kim, Dennis H.

doi:10.1016/j.it.2014.08.008

Cited by 144 publications

(129 citation statements)

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“…[13][14][15][16][17]). Thus, for the purpose of the current review, we only indicate some of the main elements.…”

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

“…Caenorhabditis elegans immune defence relies on behavioural and physiological responses. Of these, behavioural responses represent an important, fine-tuned first line defence against a variety of bacterial pathogens (reviewed in [15,19]). The physiological immune systems is based on several conserved core signalling cascades, including three mitogenactivated protein kinase (MAPK) pathways (i.e.…”

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

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Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Dierking

Yang

Schulenburg

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Nematodes and arthropods likely form the taxon Ecdysozoa. Information on antimicrobial effectors from the model nematode Caenorhabditis elegans may thus shed light on the evolutionary origin of these defences in arthropods. This nematode species possesses an extensive armory of putative antimicrobial effector proteins, such as lysozymes, caenopores (or saposin-like proteins), defensin-like peptides, caenacins and neuropeptide-like proteins, in addition to the production of reactive oxygen species and autophagy. As C. elegans is a bacterivore that lives in microbe-rich environments, some of its effector peptides and proteins likely function in both digestion of bacterial food and pathogen elimination. In this review, we provide an overview of C. elegans immune effector proteins and mechanisms. We summarize the experimental evidence of their antimicrobial function and involvement in the response to pathogen infection. We further evaluate the microbe-induced expression of effector genes using WormExp, a recently established database for C. elegans gene expression analysis. We emphasize the need for further analysis at the protein level to demonstrate an antimicrobial activity of these molecules both in vitro and in vivo.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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“…[13][14][15][16][17]). Thus, for the purpose of the current review, we only indicate some of the main elements.…”

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Dierking

Yang

Schulenburg

2016

Phil. Trans. R. Soc. B

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“…The immune system plays a central role together with host learning to avoid, resist and tolerate these dangers (Akira et al, 2006;Medzhitov et al, 2012). One or all of these mechanisms can be seen in various organisms from Caenorhabditis elegans (Melo and Ruvkun, 2012;Meisel and Kim, 2014) to humans (McCusker and Kelley, 2013;Curtis, 2014). However, an additional behavioral strategy has evolved to help limit pathogen growth and fight infection more efficiently.…”

Section: Introductionmentioning

confidence: 99%

Pathogen induced food evasion behavior in Drosophila larvae

Surendran

Hückesfeld

Wäschle

et al. 2017

Journal of Experimental Biology

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Recognizing a deadly pathogen and generating an appropriate immune reaction is essential for any organism to survive in its natural habitat. Unlike vertebrates and higher primates, invertebrates depend solely on the innate immune system to defend themselves from an attacking pathogen. In this study, we report a behavioral defense strategy observed in Drosophila larvae that helps them escape and limit an otherwise lethal infection. A bacterial infection in the gut is sensed by the larval central nervous system, which generates an alteration in the larva's food preference, leading it to stop feeding and move away from the infectious food source. We have also found that this behavioral response is dependent on the internal nutritive state of the larvae. Using this novel behavioral assay as a read-out, we further identified hugin neuropeptide to be involved in the evasion response and detection of bacterial signals.

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“…Because avoidance to P. aeruginosa is part of the C. elegans defense response against this pathogen [17,18], we performed a so-called "full-lawn" survival assay that uses plates that are completely covered in bacteria, a condition that eliminates pathogen avoidance. We found that dop-4(tm1392) animals exhibited enhanced resistance to P. aeruginosa infection compared with wild-type animals on full-lawn plates ( Figure 2F).…”

Section: Author Manuscriptmentioning

confidence: 99%

“…In addition, the enhanced resistance to P. aeruginosamediated killing of dop-4(tm1392) animals did not differ from that of dop-4(tm1392) Figure 2E). In contrast, treatment with chlorpromazine enhanced resistance to P. aeruginosa infection in animals carrying mutations in other dopamine receptors ( Figure S2), suggesting that chlorpromazine enhances immunity primarily by inhibiting the D1-like dopamine receptor DOP-4.Because avoidance to P. aeruginosa is part of the C. elegans defense response against this pathogen [17,18], we performed a so-called "full-lawn" survival assay that uses plates that are completely covered in bacteria, a condition that eliminates pathogen avoidance. We found that dop-4(tm1392) animals exhibited enhanced resistance to P. aeruginosa infection compared with wild-type animals on full-lawn plates ( Figure 2F).…”

mentioning

confidence: 99%

Neural Inhibition of Dopaminergic Signaling Enhances Immunity in a Cell-Non-autonomous Manner

Cao¹,

Aballay²

2016

Current Biology

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SUMMARYThe innate immune system is the frontline of host defense against microbial infections, but its rapid and uncontrolled activation elicits microbicidal mechanisms that have deleterious effects [1,2]. Increasing evidence indicates that the metazoan nervous system, which responds to stimuli originating from both the internal and the external environment, functions as a modulatory apparatus that controls not only microbial killing pathways but also cellular homeostatic mechanisms [3][4][5]. Here, we report that dopamine signaling controls innate immune responses through a D1-like dopamine receptor, DOP-4, in Caenorhabditis elegans. Chlorpromazine inhibition of DOP-4 in the nervous system activates a microbicidal PMK-1/p38 mitogen-activated protein kinase signaling pathway that enhances host resistance against bacterial infections. The immune inhibitory function of dopamine originates in CEP neurons and requires active DOP-4 in downstream ASG neurons. Our findings indicate that dopamine signaling from the nervous system controls immunity in a cell non-autonomous manner and identifies the dopaminergic system as a potential therapeutic target for not only infectious diseases but also a range of conditions that arise as a consequence of malfunctioning immune responses. RESULTS AND DISCUSSIONThe ability of an organism to survive microbial infections requires tightly controlled activation of immune responses. Excessive inflammation can lead to conditions such as Crohn's disease, rheumatoid arthritis, Alzheimer's disease, and many other diseases that involve aberrant inflammation. Indeed, to survive an infection and return to homeostasis, animals appear to rely on reflex circuits that prevent inflammation when triggered by bacterial products or inflammatory cues [6,7]. This rapid and precise communication between the nervous and immune systems serves as an ancestral mechanism to control immune homeostasis in metazoans. * Correspondence: a.aballay@duke.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AUTHOR CONTRIBUTIONSX.C. and A.A. conceived and designed experiments. X.C. performed experiments. X.C. and A.A. analyzed the data and wrote the paper. HHS Public Access Author Manuscript Author ManuscriptAuthor Manuscript Author ManuscriptIncreasing evidence highlights the importance of the vagus nerve circuit in the mediation of anti-inflammatory effects [8]. Recent studies have demonstrated that electroacupuncture requires intact sciatic and vagus nerves to inhibit inflammation by promoting the release of dopamine in the adrenal medulla [9,10]. Dopamine is a well-characteri...

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Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans

Cited by 144 publications

References 48 publications

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Pathogen induced food evasion behavior in Drosophila larvae

Neural Inhibition of Dopaminergic Signaling Enhances Immunity in a Cell-Non-autonomous Manner

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