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The Role of Intestinal Fungi and Its Metabolites in Chronic Liver Diseases

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The Role of Intestinal Fungi and Its Metabolites in Chronic Liver Diseases Gut and Liver, Vol. 14, No. 3, May 2020, pp. 291-296 Review The Role of Intestinal Fungi and Its Metabolites in Chronic Liver Diseases Ningning You1, Lili Zhuo1, Jingxin Zhou1, Yu Song2, and Junping Shi1 1Department of Liver Diseases, The Affiliated Hospital of Hangzhou Normal University, and 2Department of Liver Diseases, Zhejiang Chinese Medical University, Hangzhou, China Current studies have confirmed that liver diseases are cades have documented an important role for intestinal bacteria closely related to intestinal microorganisms; however, those in liver diseases. Growing evidences indicate that like the bac- studies have mainly concentrated on bacteria. Although the teria, the intestinal fungi are also closely associated with liver proportion of intestinal microorganisms accounted for by col- disease. onizing fungi is very small, these fungi do have a significant Intestinal fungi, as an important part of intestinal micro- effect on the homeostasis of the intestinal microecosystem. ecology, though the proportion is very low, its role in human In this paper, the characteristics of intestinal fungi in patients health and disease cannot be ignored. Under physiological con- with chronic liver diseases such as alcoholic liver disease, ditions, a variety of components on fungal cell wall (including nonalcoholic fatty liver disease and cirrhosis are summa- β-glucan, zymosan, mannan, chitosan, DNA, and RNA) can be rized, and the effects of intestinal fungi and their metabolites recognized by host cells to activate innate and acquired immu- are analyzed and discussed. It is important to realize that not nity. The reaction inhibits the overgrowth of the intestinal fungi only bacteria but also intestinal fungi play important roles in or the colonization of exogenous pathogens. When the host liver diseases. (Gut Liver 2020;14:291-296) immune system is deficient3 or a large number of antibiotics are used,4 it will cause changes in the composition of the intestinal Key Words: Intestinal fungi; Alcoholic liver disease; Cirrhosis; microbiota, which will cause a series of liver diseases through Non-alcoholic fatty liver disease the “entero-hepatic axis.” In this review, we will combine the current research on intestinal fungus and chronic liver diseases INTRODUCTION to analyze the relationship between intestinal fungi and alco- holic liver disease (ALD), nonalcoholic fatty liver disease (NAFLD) The gastrointestinal tracts, as one of the most important and and liver cirrhosis, try to make people realize that not only complex micro-ecosystems in human body, harbors large num- bacteria but also intestinal fungi play an important role in liver bers of microorganisms (about 1012 to 1014), including bacteria, diseases. archaea, virus, and fungi;1 the enormous quantity and complex structure of intestinal micro-ecology have been a challenge for THE GUT MYCOBIOME IN HEALTHY COHORT scientist to have a deep exploration of intestinal microorgan- ism. In recent years, with the advancement of high-throughput Fungi are detectable in all sections of the gastrointestinal sequencing technology, more and more microorganisms have tract of about 70% of healthy adults, normally at up to 1,000 been known and confirmed to be important in maintaining hu- fungal cells per milliliter or gram of intestinal contents.5 Cul- man health, such as immune protection, nutrient absorption, ture-independent analyses show that fungi constitute less than bacterial barrier, anticancer and cancer suppression.2 However, 0.1% of the human gut microbiome,6 while accounting for only there are also potentially pathogenic microorganisms containing 0.03% of the fecal microbiota.7 Previous traditional culture- in the intestinal micro-ecology causing disruption of intestinal dependent techniques can only detect a small number of fungi, homeostasis and alterations in the intestinal microorganisms with the maturity of high-throughput sequencing technology, it which contributes to the pathogenesis of many disorders, in- has gradually replaced traditional culture techniques as the best cluding liver disease. Many studies over the past couple of de- method for studying fungi. Reports using next generation se- Correspondence to: Junping Shi Department of Liver Diseases, The Affiliated Hospital of Hangzhou Normal University, 126 Wenzhou Road, Hangzhou 310015, China Tel: +86-57188358060, Fax: +86-57188021730, E-mail: [email protected] Received on December 29, 2018. Revised on March 27, 2019. Accepted on April 15, 2019. Published online September 30, 2019. pISSN 1976-2283 eISSN 2005-1212 https://doi.org/10.5009/gnl18579 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 292 Gut and Liver, Vol. 14, No.3, May 2020 quencing have found diverse fungal communities in all sections mice are significantly higher than the control group. Composi- of the human gut, consisting mainly of the phyla Ascomycota, tional changes in the intestinal mycobiome were characterized Basidiomycota, Zygomycota, and Chytridiomycota.8-10 The pre- by significantly increased proportions of Humicola species, dominant commensal fungal species in the human intestine are Fusarium, and Aspergillus, while proportions of Candida spe- Candida species, Saccharomyces cerevisiae, and Malassezia spe- cies decreased. Besides, it is worth noting that the abundance cies.11 The special anatomical and physiological features of the of albicans Candida in ALD group is dramatic overgrowth. The individual compartments of the mouth, stomach and intestine 1,3-β-glucan from fungal cell wall enters the liver by portal offer disparate ecological niches and they are colonized with vein through the damaged intestinal mucosa, and binds to site-specific microbe communities. The total number of fungi CLEC7A on the surface of the liver Kupffer cell, then stimulates increases from the ileum to the colon and reaches the highest the Kupffer cell to secrete interleukin-1β (IL-1β), which leads to density in the distal intestine of most monogastric animals.12 steatosis and necrosis of hepatocyte. Interestingly, overgrowth In 2017, the human microbiome project (HMP) launched the of Candida was independent of the stage of liver disease, pa- study of the gut mycobiome in human, 317 HMP stool samples tients with nonprogressive ALD, alcoholic hepatitis, or alcoholic were analyzed by sequencing the internal transcribed spacer 2 cirrhosis had similar levels of fungal dysbiosis in the intestine. (ITS2) region as well as the 18S rRNA gene, 701 fungal opera- In addition, the study also found that in the ALD patients, the tional taxonomic units were detected in the sample set, captur- abundance of Epicoccum, unclassified fungi, Galactomyces, and ing 247 named genera, and the Shannon diversity index varied Debaryomyces in the intestinal tract is decreased. Epicoccum between 0.004 and 2.94, which was much lower than bacterial fungus is known for its potential to produce diverse classes of communities. The intestinal fungi was dominated by yeast in- biologically active secondary metabolites, and has physiological cluding Saccharomyces, Malassezia, and Candida, and there effects such as anti-oxidation, anticancer, and antibacterial,19,20 was the strongest positive correlation between Sarocladium but the role in ALD has not been studied. and Fusarium, while Candida and Saccharomyces exhibited the strongest negative correlation. Both inter- and intra-volunteer INTESTINAL FUNGI AND NAFLD variability in the HMP cohort were high, revealing that unlike bacterial communities, an individual’s mycobiome is no more There are few studies on the relationship between intestinal similar to itself over time than to another person’s. Besides, this fungi and NAFLD. At present, the most researched is the pro- article also indicates that though 18S rRNA gene and whole-ge- biotic Saccharomyces boulardii, which has been widely used in nome shotgun metagenomic sequencing aligned with the results clinical practice. It has the function of neutralizing and degrad- of ITS2 sequencing, ITS2 data provided greater resolution of the ing bacterial toxins, regulating intestinal flora and immune mycobiome membership, suggesting that ITS2 sequencing is a function. In addition, S. boulardii is a beneficial aerobic fungal, more accurate and sensitive method for studying the mycobi- which can consume oxygen, produce an anaerobic environment ome in stool samples.13 conducive to bifidobacteria and lactic acid bacteria, and inhibit the growth of pathogenic microbiome.21 INTESTINAL FUNGI AND ALCOHOLIC LIVER DISEASE Everard et al.22 is the first one who used S. boulardii for clinic trial in 2014. After oral administration of S. boulardii for Liver acts as a metabolic site for alcohol, when the body 4 weeks, the obese and type 2 diabetic mice has a significant excessively consumes alcohol for a long time and exceeds the reductions in body weight and fat mass, hepatic steatosis and metabolic load of the liver, it can cause liver damage through inflammation are also significantly alleviated. Interestingly, this multiple routes, and constantly develop into alcoholic fatty study found that the effect of S. boulardii on host metabolism is liver, alcoholic hepatitis, alcoholic cirrhosis and even liver related to the local effect of intestinal tract. To a certain extent,
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