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Novel probiotic yeast from Miso promotes regulatory dendritic cell IL-10 production and attenuates DSS-induced colitis in mice

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Abstract

Background

Yeasts are a type of fungi thought to have probiotic functions. In this study, we isolated a novel probiotic yeast (Zygosaccharomyces sapae strain I-6) from Miso (a traditional Japanese fermented food). We examined its effects on phenotypic changes in intestinal dendritic cells (DCs), and evaluated its anti-inflammatory effects in dextran sulfate sodium (DSS)-induced colitis.

Methods

A single colony was selected from homogenized Miso, based on its ability to produce interleukin (IL)-10 in CD11c+ bone marrow DCs (BMDCs) in vitro. The anti-inflammatory effects of strain I-6 on CD11c+ BMDCs and CD11c+ CD103+ DCs were analyzed in mouse mesenteric lymph nodes in vitro and in a DSS mouse model.

Results

The IL-10 concentrations in the co-culture BMDC supernatants treated with I-6 were dramatically higher than in those treated with Saccharomyces cerevisiae (Sc). IL-10 production is mediated by both TLR2 and Dectin-1. β-Glucan extracted from I-6 also induced higher levels of IL-10 production in BMDCs than β-glucan from Sc. The number of mesenteric lymph node CD11c+ CD103+ DCs was significantly increased by I-6 administration, compared with Sc administration. Strain I-6 showed strong anti-inflammatory effects on DSS-induced colitis compared to Sc. Moreover, the adoptive transfer of I-6-treated BMDCs showed anti-inflammatory effects on DSS-induced colitis in mice without oral administration of I-6 cells.

Conclusions

Strain I-6 induced phenotypic changes in intestinal CD11c+ DCs characterized by high IL-10 production and exerted strong anti-inflammatory effects on DSS-induced colitis. Traditional Japanese fermented foods may be a valuable source of probiotic yeasts for effective IBD therapy and treatment.

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Acknowledgements

This research was supported by grants from the National Defense Medical College, Food Science Institute Foundation, Japan.

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Authors and Affiliations

  1. Department of Internal Medicine, National Defense Medical College, 3-2 Namiki, Tokorozawa, Saitama, 359-8513, Japan

    Yoshikiyo Okada, Nao Sugihara, Shin Nishii, Naoki Shibuya, Akinori Mizoguchi, Suguru Itoh, Rina Tanemoto, Kenichi Inaba, Yoshinori Hanawa, Kazuki Horiuchi, Akinori Wada, Masaaki Higashiyama, Chikako Watanabe, Chie Kurihara, Shunsuke Komoto, Kengo Tomita & Ryota Hokari

  2. Department of Gastroenterology, Saitama Medical University, 38 Morohongo, Moroyama-machi, Iruma-gun, Saitama, 350-0495, Japan

    Yoshikazu Tsuzuki

  3. Graduate School, International University of Health and Welfare, Tokyo, 107-0062, Japan

    Soichiro Miura

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  1. Yoshikiyo Okada
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Contributions

Designed the study: YO. Analysed the data: YO, NS, and RH. Collected the data: NS, SN, NS, AM, SI, RT, KI, YH, KH, AW, MH, CW, CK, SK, KT, SM, and RH. Evaluated murine tissue samples: NS, SN, AM, and SI. Wrote the first draft of the manuscript: YO. Contributed to writing the paper: YO, YT, and RH.

Corresponding author

Correspondence to Yoshikiyo Okada.

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Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The study protocol was approved by the Animal Ethics Committee of the National Defense Medical College (No. 18001).

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Okada, Y., Tsuzuki, Y., Sugihara, N. et al. Novel probiotic yeast from Miso promotes regulatory dendritic cell IL-10 production and attenuates DSS-induced colitis in mice. J Gastroenterol 56, 829–842 (2021). https://doi.org/10.1007/s00535-021-01804-0

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  • DOI: https://doi.org/10.1007/s00535-021-01804-0

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