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

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

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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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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Keywords

  • Probiotic
  • Yeast
  • Fermented food
  • Dendritic cell