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The inhibitory effects of live and UV-killed Akkermansia muciniphila and its derivatives on cytotoxicity and inflammatory response induced by Clostridioides difficile RT001 in vitro

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Abstract

Clostridioides difficile infection (CDI) is the leading cause of healthcare-acquired infections worldwide. Probiotics are widely recommended to prevent CDI and its recurrences. Akkermansia muciniphila, as a therapeutic symbiont colonizing the intestinal mucosal layer, is considered to be a promising next-generation probiotic. In this work, we assessed the inhibitory effects of A. muciniphila MucT and its derivatives on cytotoxicity and inflammatory response induced by C. difficile RT001 in Caco-2 cells. The results obtained from SEM revealed that the morphology of UV-killed A. muciniphila remained unchanged after UV inactivation. TEM analysis showed that A. muciniphila–isolated extracellular vesicles (EVs) were spherical and ranged from 50 to 200 nm in size. Toxigenic supernatant (Tox-S) of C. difficile RT001 (500 μg/ml) significantly (P <0.01) reduced the cell viability of Caco-2 cells. Caco-2 cells treated with live (MOI 10), UV-killed (MOI 10), cell-free supernatant (CFS, 106 cfu/ml), and EVs (20 μg/ml) of A. muciniphila exhibited over 90% viability in comparison to untreated control. The neutralized CFS preparation using A. muciniphila and its derivatives could notably reduce the expression level of inflammatory markers. Additionally, A. muciniphila and its derivatives modulated the production of IL-1β, TNF-α, and IL-10 in Tox-S stimulated Caco-2 cells. We demonstrated that A. muciniphila and its derivatives can modulate changes in the gut barrier–related genes and inflammatory response caused by C. difficile Tox-S in Caco-2 cells.

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Acknowledgements

The authors wish to thank all members of the Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran, and Microbiology Research, and also the Department of Microbiology at the School of Medicine, Shahid Beheshti University of Medical Sciences. This article has been also extracted from a PhD thesis (Registration No: 568) by Mrs. Gelareh Nasiri from Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Funding

This study was supported by a grant from School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran (Grant No: 21635, IR.SBMU.RIGLD.REC.1399.110). Also, the study was funded by a research grant (Grant No: RIGLD 1140) from Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

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Authors and Affiliations

  1. Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Gelareh Nasiri, Hossein Goudarzi, Sahar Amirkamali & Zohreh Ghalavand

  2. Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Gelareh Nasiri, Masoumeh Azimirad, Sahar Amirkamali & Abbas Yadegar

  3. Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Shabnam Shahrokh & Mohammad Reza Zali

  4. Basic and Molecular Epidemiology of Gastrointestinal Disorders Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Hamid Asadzadeh Aghdaei

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  1. Gelareh Nasiri
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  2. Masoumeh Azimirad
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Contributions

GN performed the microbiological experiments, cell culture, molecular tests, ELISA, and data analysis, and wrote the manuscript draft; MA contributed to the microbiological experiments and cell culture experiments; SA participated in molecular testing and cell culture experiments; AY contributed to study design, methodology, conceptualization, and project administration; AY and ZG contributed to the project supervision and administration; AY, ZG, SS, HG, HAA, and MRZ critically revised the manuscript. All authors approved the final version of the manuscript and the authorship list.

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Correspondence to Abbas Yadegar or Zohreh Ghalavand.

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This work does not contain any studies related with human participants or animals. The study was approved by the Institutional Ethical Review Committee of Research Institute for Gastroenterology and Liver Diseases at Shahid Beheshti University of Medical Sciences (Project No. IR.SBMU.RIGLD.REC.1399.053).

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Nasiri, G., Azimirad, M., Goudarzi, H. et al. The inhibitory effects of live and UV-killed Akkermansia muciniphila and its derivatives on cytotoxicity and inflammatory response induced by Clostridioides difficile RT001 in vitro. Int Microbiol 27, 393–409 (2024). https://doi.org/10.1007/s10123-023-00398-2

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