Prebiotic effect of diosgenin, an immunoactive steroidal sapogenin of the Chinese yam
Highlights
► Prebiotic effects of diosgenin on lactobacilli were investigated. ► Diosgenin restored the diminished density of faecal lactobacilli associated with food allergy in mice. ► Diosgenin enhanced the growth of lactobacilli in culture. ► Steroidal sapogenins represent a novel class of phytochemicals with prebiotic activity on lactobacilli.
Introduction
The Chinese yam (shan yao; Dioscorea opposita Thunb.) is a commonly used dietary supplement, as well as a herbal medicine in Asia. It is generally believed that intake of the Chinese yam may be beneficial to improve the function of the spleen, stomach and lung. The Chinese yam contains a variety of phytochemicals, including sapogenins, saponins, starch, mucopolysaccharides, protein, amino acids, etc. (Wanasundera & Ravindran, 1994). Among these, yam-derived mucopolysaccharides, dioscorin and diosgenin have been shown to be immunoactive (Choi and Hwang, 2002, Jan et al., 2007, Lin et al., 2009). Of relevant to this study, diosgenin, a major yam-derived sapogenin, has been reported to possess a variety of biological activities, including anti-diarrhoea, anti-inflammation, anti-oxidation, hypocholesterolaemia, hypoglycaemia and immunomodulation (McAnuff et al., 2005, Son et al., 2007, Yamada et al., 1997).
We previously reported that oral administration of diosgenin enhanced T helper (Th)1 cell-mediated immunity, and attenuated the occurrence of allergic diarrhoea and the intestinal inflammation associated with food allergy (Huang et al., 2009, Jan et al., 2007). Furthermore, the number of regulatory Treg cells capable of expressing interleukin (IL)-10 in the intestine of diosgenin-treated mice was elevated, suggesting an augmentation of immunoregulatory mechanisms (Huang, Liu, & Jan, 2010). These results demonstrated the anti-allergic and immunomodulatory effects of diosgenin, which may account for some of yam-mediated beneficial effects. However, its underlying mechanism remains to be elucidated.
The intestinal microbes are involved in the development of the host immune system and the maintenance of the immunobalance in the gut (Tanaka and Ishikawa, 2004, Umesaki and Setoyama, 2000). For example, epidemiologic evidence indicates that a decrease in the microbial exposure in early childhood is closely associated with an increased morbidity in allergic diseases (Renz, Blumer, Virna, Sel, & Garn, 2006). Therefore, it is considered that some probiotics may be potentially beneficial for the management of allergy. Studies conducted in rodent models have shown that ingestion of certain strains of lactic acid bacteria (LAB), such as Lactobacillus casei 911, suppressed the allergic responses in ovalbumin (OVA)-sensitised mice (Kim, Kwack, Kim, & Ji, 2005). The L. casei strain Shirota enhanced Th1-mediated immunity and attenuated allergen-induced anaphylaxis in a murine model of food allergy (Shida et al., 2002). In addition, the anti-allergic effect of Lactobacillus reuteri against airway hypersensitivity has been reported to be mediated by an up-regulation of the regulatory immunity (Karimi, Inman, Bienenstock, & Forsythe, 2009).
The composition of enteric flora is influenced by many factors, including habit, stress, sleep, dietary food, etc. Prebiotics are food ingredients that confer a health benefit to the host by promoting the growth of enteric probiotics (Gibson & Roberfroid, 1995). For example, fructooligosaccharides (FOS) have been shown to enhance the growth of probiotics in culture and prolong their retention in the gut (Su et al., 2007a, Su et al., 2007b). Furthermore, intake of FOS attenuated allergic responses in a murine model of food allergy (Fujitani et al., 2007). To date, the major food chemicals with prebiotic property are indigestible dietary carbohydrates, including FOS, xylooligosaccharides, inulin, soybean oligosaccharides, etc. (Chow, 2002). It is currently no evidence available pertaining to the prebiotic activities of sapogenins. As the profile of diosgenin-mediated immunomodulatory effects resembles that induced by certain prebiotics and probiotics, it was hypothesised that diosgenin may exhibit prebiotic activity to promote the growth of enteric probiotics. In the present study, the influence of diosgenin on the density of intestinal LAB was investigated in the same murine model of food allergy we previously used to demonstrate the anti-allergic effect of diosgenin. In addition, the direct effect of diosgenin and several structure-related compounds on the growth of LAB in culture was further examined.
Section snippets
Materials
Diosgenin (purity ⩾99%), sarsasapogenin (purity ⩾98%), stigmasterol (purity ⩾95%), fructooligosaccharides (purity ⩾90%) and olive oil (highly refined and low acidity) were purchased from Sigma Chemicals (St. Louis, MO, USA). For administration to mice, diosgenin was suspended in olive oil as a fine suspension. Hecogenin (purity >80%) was purchased from Tokyo Chemical Industry Co. (Tokyo, Japan). Solasodine (purity ⩾95%) was purchased from MP Biomedicals (Solon, OH, USA). Absolute ethanol was
The effect of diosgenin on the density of faecal lactic acid bacteria (LAB) in mice sensitised and challenged with ovalbumin (OVA)
The faecal density of LAB and non-specific microbes measured by MRS and TSA, respectively, was comparable between groups before OVA sensitisation and before the 1st OVA challenge (Table 1, Table 2). However, repeated OVA challenges for five and nine times diminished the faecal density of LAB, whereas the number of non-specific microbes was elevated in OVA-sensitised mice (Table 1, Table 2; OVA vs. NS), suggesting a competition between LAB and non-specific microbes in the gut of animals with
Conclusions
To date, the majority of prebiotics are oligosaccharides (Gibson & Roberfroid, 1995; Swennen, Courtin, & Delcour, 2006). Evidence pertaining to the prebiotic effects of natural ingredients other than non-digestive carbohydrates is scarce. To the best of our knowledge, the present study provides the first evidence to show the prebiotic property of plant-derived steroidal sapogenins in vivo and in vitro. On the base of the prebiotic effect of steroidal sapogenins on LAB, food chemicals, such as
Acknowledgements
This work was supported by Grants NSC98-2320-B-002-036-MY3 from the National Science Council, and 100AS-9.2.5-BQ-B1(2) from the Council of Agriculture, Executive Yuan, Taiwan.
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