Influencing IBD Severity

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Influencing IBD Severity View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Cell Host & Microbe Previews The Mycobiome: Influencing IBD Severity David L. Moyes1 and Julian R. Naglik1,* 1Clinical & Diagnostic Sciences Group, King’s College London Dental Institute, King’s College London, London, SE1 9RT, UK *Correspondence: [email protected] DOI 10.1016/j.chom.2012.05.009 The etiology and maintenance of inflammatory bowel disease (IBD) is the subject of much speculation. Iliev et al. (2012) impose a change in our views of the gut microbiome and catapult the fungal ‘‘mycobiome’’ center-stage in the exploration of IBD. The interaction between a host and its indigenous to the gut, rather than food assumed that similar changes may occur microbiome is essential for health of the passengers. These findings are notable, in the mycobiome. As predicted, there host organism (Figure 1). However, recent as they show that Candida spp. are a was an overall increase in ‘‘opportu- investigations have been mostly limited to major part of the mammalian gut myco- nistic pathogenic’’ fungi (Candida, Tricho- studying commensal bacteria, with fungi biome, although interestingly in humans sporon) and a decrease in nonpathogenic largely being ignored as constituents of it would appear that C. albicans and fungi (Saccharomyces). Concurrent with the host microbiota. Indeed, the idiom C. parapsilosis are the major fungal con- this shift, there is evidence of fungal inva- ‘‘microbiome’’ has become synonymous stituents (Scanlan and Marchesi, 2008). sion of inflamed tissues in DSS-treated with commensal bacteria. Key among Indeed, C. albicans is not a natural colo- Clec7aÀ/À mice, whereas in DSS-treated investigations of the interactions between nizer of mice, although the reasons for wild-type mice the fungi are restricted to the microbiome and the host has been this are still unclear. the lumen, suggesting Dectin-1 plays a identifying the role played by these Next, Iliev et al. (2012) addressed the role in preventing fungi from breaching microbes in the etiology and maintenance effects this mycobiome has on general the mucosal barrier and gaining entry to of inflammatory bowel disease (IBD). It host health and reason with some justifi- the host all-you-can-eat buffet. The notion has now been established that alterations cation that if gut commensal fungi are that this is a host-mediated event rather in the bacterial population can lead to gut recognized by Dectin-1, then mice defi- than a change in microbiota gains further inflammation (Willing et al., 2010), but the cient in this receptor may show dif- support from the authors’ observation presence and role of fungi in these pro- ferences in susceptibility to IBD. As that gut-conditioned dendritic cells from cesses is unknown. Although the pres- predicted, Dectin-1-deficient (Clec7aÀ/À) Clec7aÀ/À mice are restricted in their ence of a commensal fungal community mice suffered greater severity of symp- ability to kill C. tropicalis in vitro. Further- on mucosal surfaces has been posited, toms in a dextran sulfate sodium (DSS)- more, gut administration of C. tropicalis little has been done to investigate the induced colitis model, demonstrat- to Clec7aÀ/À mice results in more severe influence of these microbes on health ing increased weight loss, histological DSS-induced colitis with all its ancillary and disease and, to date, only an oral changes, and proinflammatory cytokine pathology. Wild-type mice showed no ‘‘mycobiome’’ has been characterized production. This was not due to differ- effects beyond the norm. Notably, treat- (Ghannoum et al., 2010). ences in commensal bacteria between ment of Clec7aÀ/À mice with an antifungal A recent study by Iliev et al. (2012) the wild-type and Clec7aÀ/À mice, as the drug during colitis reversed these effects. identified that a populous gut mycobiome microbiota was the same in both strains. It will be interesting to see if this effect is exists in several mammalian species. The intriguing question here is whether common to all pathogenic, filamentous This community showed reactivity with this increased sensitivity is driven solely fungi and whether all nonpathogenic fungi Dectin-1, the host pattern recognition by Dectin-1 deficiency or by an altered are incapable of inducing these re- receptor (PRR) for b-glucan, and demon- microbiota Clec7aÀ/À mice, as has been sponses, thus identifying if this is a com- strated varied morphologies. Genomic reported in NLRP6À/À mice (Elinav et al., mon fungal effect or specific to Candida characterization of the murine gut myco- 2011). To answer this, the authors used species. Taken together, these data sug- biome indicated that it is a varied ‘‘multi- a fecal transplant from Clec7aÀ/À to gest that Dectin-1 deficiency leads to ethnic’’ community of diverse fungal wild-type mice, with the recipient animals altered immunity to commensal fungi in species. Like any such population, the showing no increase in sensitivity to DSS the gut. Further, they indicate the para- mycobiome was not homogenous but, colitis. Thus, the increased sensitivity mount importance of epithelial cells and surprisingly, over 97% of the population appears to be due to the lack of Dectin-1 epithelium integrity in maintaining health, comprised just ten fungal species and function rather than an altered microbiota. as it is only when this barrier is perturbed remarkably, a single dimorphic fungus, The authors next investigated what that Dectin-1 deficiency becomes impor- Candida tropicalis, constituted over 65% happens to the mycobiome during the tant and affects inflammatory disease of the entire population. By comparing course of gut inflammation. It has been severity. these fungal species to those detected well documented that gut inflammation A key question is whether these obser- in mouse food, the authors confirmed drives changes in the gut bacterial popu- vations in mice equate to a similar role for that the vast majority of these fungi are lation (Willing et al., 2010), so the authors Dectin-1 in human disease. To address Cell Host & Microbe 11, June 14, 2012 ª2012 Elsevier Inc. 551 Cell Host & Microbe Previews with the host immune system (and epithe- lial cells) is purely a pathological process or whether they play a major role in the homeostasis and immune development of a host, as is the case for some bacteria. This is an intriguing possibility given the filamentous morphology of some fungi, in common with other gut microbiome members (notably segmented filamen- tous bacteria) that are suspected of ‘‘tutoring’’ immune responses (Ivanov and Littman, 2010). Filamentation may be a key fungal factor in penetrating the thick, mucus layer covering the gut epithelial surface, enabling continued interaction between the host and these microbes. A better understanding of how we interact with our mycobiome and what the conse- quences of these interactions are may well lead to a world of new and exciting possibilities. Figure 1. The Mycobiome and Gut Inflammation Interactions between fungi in the mycobiome and host cells in the gut affect how inflammatory diseases REFERENCES progress. Breaches in the epithelial barrier due to localized inflammation allow fungi from the mycobiome to invade the underlying tissue, exposing them to immune cells. In wild-type gut, this contact triggers immune recognition of fungi via the Dectin-1 receptor, resulting in activation of antifungal responses Elinav, E., Strowig, T., Kau, A.L., Henao-Mejia, J., and restriction in fungal growth. In contrast, Dectin-1-deficient (Clec7aÀ/À) gut has a reduced ability to Thaiss, C.A., Booth, C.J., Peaper, D.R., Bertin, J., recognize and respond to fungi, allowing them to invade more extensively without restriction. This results Eisenbarth, S.C., Gordon, J.I., and Flavell, R.A. in increased damage leading to increased inflammation, exacerbating the symptoms of inflammatory (2011). Cell 145, 745–757. bowel disease. Ghannoum, M.A., Jurevic, R.J., Mukherjee, P.K., Cui, F., Sikaroodi, M., Naqvi, A., and Gillevet, P.M. (2010). PLoS Pathog. 6, e1000713. this, the authors compared the sequence These findings are an important step of the human Dectin-1 gene (CLEC7A) forward in our understanding of micro- Gringhuis, S.I., Wevers, B.A., Kaptein, T.M., van Capel, T.M., Theelen, B., Boekhout, T., de Jong, between a group of severe, medically re- biome-host interactions. Along with other E.C., and Geijtenbeek, T.B. (2011). PLoS Pathog. fractive ulcerative colitis (MRUC) patients studies now being published, they re- 7, e1001259. and another less severe group (non- present a substantial shift in our under- Iliev, I.D., Funari, V.A., Taylor, K.D., Nguyen, Q., MRUC). In doing so, they identified a standing of host-microbial interactions Reyes, C.N., Strom, S.P., Brown, J., Becker, single nucleotide polymorphism (SNP) and host-fungal interactions in particular. C.A., Fleshner, P.R., Dubinsky, M., et al. (2012). associated with MRUC and a two-SNP As we identify more receptors recognizing Science 336, 1314–1317. haplotype even more strongly associated fungal moieties, such as Dectin-2 recog- Ivanov, I.I., and Littman, D.R. (2010). Mucosal with MRUC. Future studies should aim to nition of a-mannans (Saijo et al., 2010), Immunol. 3, 209–212. determine the effect of these haplotypes and identify the cooperation between Jawhara, S., Mogensen, E., Maggiotto, F., Fradin, on the functional activity of Dectin-1, these receptors in fungal recognition C., Sarazin, A., Dubuquoy, L., Maes, E., Gue´ rardel, although one could speculate that they (Netea et al., 2006), studies with these Y., Janbon, G., and Poulain, D. (2012). J. Biol. might lead to some loss of functionality. receptors will help to further elucidate Chem. 287, 11313–11324. Given that CLEC7A has not been identi- the importance of host-fungal interac- Netea, M.G., Gow, N.A., Munro, C.A., Bates, S., fied as an IBD susceptibility gene by any tions in homeostasis and pathogenesis.
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