Parasitic helminths and the host microbiome – a missing ‘extracellular vesicle-sized’ link?

Rooney, James; Northcote, Holly M.; Williams, Tim; Cortés, Alba; Cantacessi, Cinzia; Morphew, Russell M.

doi:10.1016/j.pt.2022.06.003

Cited by 20 publications

(17 citation statements)

References 75 publications

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“…For example, A. suum ESPs contain several AMPs—such as lectins, cecropins, and members of the A. suum antibacterial factor family—which inhibit bacterial growth, impair biofilm formation, or neutralize bacteria by other mechanisms (e.g., agglutination) [ 111 , 112 ]. Helminth ESPs also include extracellular vesicles, which contain putative AMPs and are thought to be important mediators of the effects of helminths on the microbiota [ 113 , 114 ]. In addition, type 2 cytokines produced during helminth infection also induce host cells to produce AMPs like small proline-rich protein 2A, which shapes intestinal microbiota composition and protects against helminth-induced bacterial invasion of intestinal tissue [ 115 ].…”

Section: Discussionmentioning

confidence: 99%

Helminths and Bacterial Microbiota: The Interactions of Two of Humans’ “Old Friends”

Llinás-Caballero

Caraballo

2022

IJMS

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Humans have coexisted with helminths and bacteria for the entire existence of our species. Nowadays, helminth infections affect more than 1.9 billion people worldwide, especially in underdeveloped regions that lack optimal sanitary conditions. In addition, commensal microorganisms inhabit several compartments of humans, including the gastrointestinal tract, constituting what we know as the microbiota. Helminths and bacterial microbiota can interact in various ways. In this review, the interactions between helminths and commensal bacteria are analyzed in both animal models and humans. In developing countries, the gut microbiota exhibits high diversity, which could be linked to the high burden of helminthiasis in these areas. In fact, several studies show that helminth infections are associated with an increased gut microbiota diversity and changes in its composition. Interestingly, these changes can modify the risk for some diseases, such as asthma, colitis, viral infections, and metabolic conditions. Besides, the microbiota is necessary for the establishment of some helminth infections and can also influence the evolution of these diseases. Specific bacterial taxa can contribute to the resistance or susceptibility to certain helminths. The mechanisms underlying helminth–microbiota interactions are not completely understood. More research is necessary to address this and other unmet needs, especially considering that available studies are heterogeneous and sometimes yield conflicting results

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Section: Discussionmentioning

confidence: 99%

Helminths and Bacterial Microbiota: The Interactions of Two of Humans’ “Old Friends”

Llinás-Caballero

Caraballo

2022

IJMS

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“…In spite of emerging evidence of the role(s) of helminth ESPs and EVs in parasite-microbiota crosstalk, little is known of the putative antimicrobial properties of molecules contained in ESPs of livestock helminths, including those enclosed in vesicles [ 21 – 23 ]. Whilst previous investigations have comprehensively elucidated the proteomic profiles of ESPs derived from third- and fourth-stage larvae of T. circumcincta (L3s and L4s, respectively) [ 24 ], only a single study has undertaken a preliminary proteomic analysis of EV-enriched ESPs (obtained by ultracentrifugation) from L4s of this parasite [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

“…The detection of molecules with putative antibacterial properties in the EV-enriched fraction of T. circumcincta ESPs supports a likely role of parasite secretions in helminth-microbiota crosstalk, and provides a solid rationale for experiments aimed to assess the antibacterial activities of ESPs and EVs in vitro (cf. [ 23 ]). In the present study, we (i) undertook an in-depth proteomic characterisation of adult T. circumcincta EVs isolated via size-exclusion chromatography (SEC) and of EV-depleted ESPs; (ii) performed targeted bioinformatics analyses of EV-depleted ESP- and EV-derived amino acid sequence data in order to identify molecules with putative antimicrobial functions; and (iii) assessed the bactericidal and/or bacteriostatic properties of adult T. circumcincta whole and EV-depleted ESPs, and SEC-purified EVs in in vitro bacterial growth viability assays.…”

Section: Introductionmentioning

confidence: 99%

Excretory-secretory products from the brown stomach worm, Teladorsagia circumcincta, exert antimicrobial activity in in vitro growth assays

et al. 2022

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Background Over the past decade, evidence has emerged of the ability of gastrointestinal (GI) helminth parasites to alter the composition of the host gut microbiome; however, the mechanism(s) underpinning such interactions remain unclear. In the current study, we (i) undertake proteomic analyses of the excretory-secretory products (ESPs), including secreted extracellular vesicles (EVs), of the ‘brown stomach worm’ Teladorsagia circumcincta, one of the major agents causing parasite gastroenteritis in temperate areas worldwide; (ii) conduct bioinformatic analyses to identify and characterise antimicrobial peptides (AMPs) with putative antimicrobial activity; and (iii) assess the bactericidal and/or bacteriostatic properties of T. circumcincta EVs, and whole and EV-depleted ESPs, using bacterial growth inhibition assays. Methods Size-exclusion chromatography was applied to the isolation of EVs from whole T. circumcincta ESPs, followed by EV characterisation via nanoparticle tracking analysis and transmission electron microscopy. Proteomic analysis of EVs and EV-depleted ESPs was conducted using liquid chromatography-tandem mass spectrometry, and prediction of putative AMPs was performed using available online tools. The antimicrobial activities of T. circumcincta EVs and of whole and EV-depleted ESPs against Escherichia coli were evaluated using bacterial growth inhibition assays. Results Several molecules with putative antimicrobial activity were identified in both EVs and EV-depleted ESPs from adult T. circumcincta. Whilst exposure of E. coli to whole ESPs resulted in a significant reduction of colony-forming units over 3 h, bacterial growth was not reduced following exposure to worm EVs or EV-depleted ESPs. Conclusions Our data points towards a bactericidal and/or bacteriostatic function of T. circumcincta ESPs, likely mediated by molecules with antimicrobial activity. Graphical Abstract

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“…They are delivered to host cells via intracellular pathways to polarize the host immune response towards tolerance, as reviewed previously [17]. Cecropin-like HDPs and immunomodulatory cystatins are discharged directly as ESP or enveloped within EV [15,18,19] to modulate the host microbiome with a direct antimicrobial effect or indirectly by stimulating host immunity (Figure 2, Key Figure). Helminths sense microbial communities and adapt their antibacterial activity, as shown by the expression of chitinase and lysozyme in Heligmosomoides polygyrus, a small intestinal nematode, when exposed to the mouse microbiome [20].…”

Section: Parasites -Host -Microbiome Interactionsmentioning

confidence: 99%

Helminthic host defense peptides: using the parasite to defend the host

Mladineo¹,

Rončević²,

Gerdol³

et al. 2023

Trends in Parasitology

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Parasitic helminths and the host microbiome – a missing ‘extracellular vesicle-sized’ link?

Cited by 20 publications

References 75 publications

Helminths and Bacterial Microbiota: The Interactions of Two of Humans’ “Old Friends”

Helminths and Bacterial Microbiota: The Interactions of Two of Humans’ “Old Friends”

Excretory-secretory products from the brown stomach worm, Teladorsagia circumcincta, exert antimicrobial activity in in vitro growth assays

Helminthic host defense peptides: using the parasite to defend the host

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