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Suppression of inflammation by helminths: a role for the gut microbiota?

Giacomin P, Croese J, Krause L, Loukas A, Cantacessi C - Philos. Trans. R. Soc. Lond., B, Biol. Sci. (2015)

Bottom Line: Multiple recent investigations have highlighted the promise of helminth-based therapies for the treatment of inflammatory disorders of the intestinal tract of humans, including inflammatory bowel disease and coeliac disease.Given the pivotal roles of the intestinal microbiota in the pathogenesis of these disorders, it has been hypothesized that helminth-induced modifications of the gut commensal flora may be responsible for the therapeutic properties of gastrointestinal parasites.In this article, we review recent progress in the elucidation of host-parasite-microbiota interactions in both animal models of chronic inflammation and humans, and provide a working hypothesis of the role of the gut microbiota in helminth-induced suppression of inflammation.

View Article: PubMed Central - PubMed

Affiliation: Centre for Biodiscovery and Molecular Development of Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Smithfield 4878, Australia.

ABSTRACT
Multiple recent investigations have highlighted the promise of helminth-based therapies for the treatment of inflammatory disorders of the intestinal tract of humans, including inflammatory bowel disease and coeliac disease. However, the mechanisms by which helminths regulate immune responses, leading to the amelioration of symptoms of chronic inflammation are unknown. Given the pivotal roles of the intestinal microbiota in the pathogenesis of these disorders, it has been hypothesized that helminth-induced modifications of the gut commensal flora may be responsible for the therapeutic properties of gastrointestinal parasites. In this article, we review recent progress in the elucidation of host-parasite-microbiota interactions in both animal models of chronic inflammation and humans, and provide a working hypothesis of the role of the gut microbiota in helminth-induced suppression of inflammation.

No MeSH data available.


Related in: MedlinePlus

Potential role for microbiota in helminth-mediated suppression of autoimmune diseases? Helminths, including Trichuris sp. and hookworms are thought to limit the severity of IBDs and autoimmune diseases via promotion of type 2 and regulatory T cell responses that counteract pro-inflammatory type 1 or type 17 immune responses. However, emerging evidence suggests that helminth-mediated immune modulation may be, in part, due to alterations in the composition of the intestinal microbiota, which can profoundly influence immune cell development and function in the intestine. ES, excretory/secretory. (Online version in colour.)
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RSTB20140296F1: Potential role for microbiota in helminth-mediated suppression of autoimmune diseases? Helminths, including Trichuris sp. and hookworms are thought to limit the severity of IBDs and autoimmune diseases via promotion of type 2 and regulatory T cell responses that counteract pro-inflammatory type 1 or type 17 immune responses. However, emerging evidence suggests that helminth-mediated immune modulation may be, in part, due to alterations in the composition of the intestinal microbiota, which can profoundly influence immune cell development and function in the intestine. ES, excretory/secretory. (Online version in colour.)

Mentions: One theory for the increased incidence of allergic and autoimmune diseases in the developed world, including IBD and CeD, is that improved sanitation has reduced our exposure to pathogens in childhood, which affects the development of the immune system. Consequently, there are increases in the incidence of immune disorders related to inappropriate responses to harmless stimuli—commonly referred to as the ‘hygiene hypothesis’ [14]. Therefore, in recent years, there have been multiple attempts to exploit the hygiene hypothesis via the controlled re-introduction of infectious agents with immunosuppressive properties, such as parasitic helminths [15–18]. In particular, two gastrointestinal parasitic nematodes, namely whipworms (Trichuris sp.) and hookworms (Necator americanus), have been investigated in a range of studies in both humans and animal models aimed at developing novel treatment strategies against IBD and CeD, respectively [16,19]. As a consequence of these pilot studies, there have been intriguing observations that some of the immunoregulatory capacity of worms may be directly or indirectly related to alterations in intestinal microbial communities (figure 1), which will be the focus of the remainder of this article.Figure 1.


Suppression of inflammation by helminths: a role for the gut microbiota?

Giacomin P, Croese J, Krause L, Loukas A, Cantacessi C - Philos. Trans. R. Soc. Lond., B, Biol. Sci. (2015)

Potential role for microbiota in helminth-mediated suppression of autoimmune diseases? Helminths, including Trichuris sp. and hookworms are thought to limit the severity of IBDs and autoimmune diseases via promotion of type 2 and regulatory T cell responses that counteract pro-inflammatory type 1 or type 17 immune responses. However, emerging evidence suggests that helminth-mediated immune modulation may be, in part, due to alterations in the composition of the intestinal microbiota, which can profoundly influence immune cell development and function in the intestine. ES, excretory/secretory. (Online version in colour.)
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4528494&req=5

RSTB20140296F1: Potential role for microbiota in helminth-mediated suppression of autoimmune diseases? Helminths, including Trichuris sp. and hookworms are thought to limit the severity of IBDs and autoimmune diseases via promotion of type 2 and regulatory T cell responses that counteract pro-inflammatory type 1 or type 17 immune responses. However, emerging evidence suggests that helminth-mediated immune modulation may be, in part, due to alterations in the composition of the intestinal microbiota, which can profoundly influence immune cell development and function in the intestine. ES, excretory/secretory. (Online version in colour.)
Mentions: One theory for the increased incidence of allergic and autoimmune diseases in the developed world, including IBD and CeD, is that improved sanitation has reduced our exposure to pathogens in childhood, which affects the development of the immune system. Consequently, there are increases in the incidence of immune disorders related to inappropriate responses to harmless stimuli—commonly referred to as the ‘hygiene hypothesis’ [14]. Therefore, in recent years, there have been multiple attempts to exploit the hygiene hypothesis via the controlled re-introduction of infectious agents with immunosuppressive properties, such as parasitic helminths [15–18]. In particular, two gastrointestinal parasitic nematodes, namely whipworms (Trichuris sp.) and hookworms (Necator americanus), have been investigated in a range of studies in both humans and animal models aimed at developing novel treatment strategies against IBD and CeD, respectively [16,19]. As a consequence of these pilot studies, there have been intriguing observations that some of the immunoregulatory capacity of worms may be directly or indirectly related to alterations in intestinal microbial communities (figure 1), which will be the focus of the remainder of this article.Figure 1.

Bottom Line: Multiple recent investigations have highlighted the promise of helminth-based therapies for the treatment of inflammatory disorders of the intestinal tract of humans, including inflammatory bowel disease and coeliac disease.Given the pivotal roles of the intestinal microbiota in the pathogenesis of these disorders, it has been hypothesized that helminth-induced modifications of the gut commensal flora may be responsible for the therapeutic properties of gastrointestinal parasites.In this article, we review recent progress in the elucidation of host-parasite-microbiota interactions in both animal models of chronic inflammation and humans, and provide a working hypothesis of the role of the gut microbiota in helminth-induced suppression of inflammation.

View Article: PubMed Central - PubMed

Affiliation: Centre for Biodiscovery and Molecular Development of Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Smithfield 4878, Australia.

ABSTRACT
Multiple recent investigations have highlighted the promise of helminth-based therapies for the treatment of inflammatory disorders of the intestinal tract of humans, including inflammatory bowel disease and coeliac disease. However, the mechanisms by which helminths regulate immune responses, leading to the amelioration of symptoms of chronic inflammation are unknown. Given the pivotal roles of the intestinal microbiota in the pathogenesis of these disorders, it has been hypothesized that helminth-induced modifications of the gut commensal flora may be responsible for the therapeutic properties of gastrointestinal parasites. In this article, we review recent progress in the elucidation of host-parasite-microbiota interactions in both animal models of chronic inflammation and humans, and provide a working hypothesis of the role of the gut microbiota in helminth-induced suppression of inflammation.

No MeSH data available.


Related in: MedlinePlus