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Immunomodulatory and Anti-Inflammatory Effects of Vitamin A and Tryptophan on Monocyte-Derived Dendritic Cells Stimulated with Gliadin in Celiac Disease Patients

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Abstract

Celiac Disease (CeD) is an autoimmune disorder with various symptoms upon gluten exposure. Dendritic cells (DCs) play a crucial role in gliadin-induced inflammation. Vitamin A (retinol; Ret) and its metabolite, retinoic acid (RA), along with tryptophan (Trp) and its metabolite, kynurenic acid (KYNA), are known to influence the immune function of DCs and enhance their tolerogenicity. This research aims to assess the impact of gliadin on DC maturation and the potential of vitamin A and tryptophan to induce immune tolerance in DCs. The monocyte cells obtained from peripheral blood mononuclear cells (PBMCs) of celiac disease patients were differentiated into DCs in the absence or presence of Ret, RA, Trp, KYNA, and then stimulated with peptic and tryptic (PT) digested of gliadin. We used flow cytometry to analyze CD11c, CD14, HLA-DR, CD83, CD86, and CD103 expression. ELISA was carried out to measure TGF-β, IL-10, IL-12, and TNF-α levels. qRT-PCR was used to assess the mRNA expression of retinaldehyde dehydrogenase 2 (RALDH2) and integrin αE (CD103). The mRNA and protein levels of Indoleamine 2, 3-dioxygenase (IDO) was analyzed by qRT-PCR and Western blot assays, respectively. Our findings demonstrate that PT-gliadin enhances the expression of maturation markers, i.e. CD83, CD86 and HLA-DR and promote the secretion of TNF-α and IL-12 in DCs. Interestingly, vitamin A, tryptophan, and their metabolites increase the expression of CD103, while limiting the expression of HLA-DR, CD83, and CD86. They also enhance RALDH2 and IDO expression and promote the secretion of TGF-β and IL-10, while limiting IL-12 and TNF-α secretion. These findings suggest that vitamin A and tryptophan have beneficial effects on PT-gliadin-stimulated DCs, highlighting their potential as therapeutic agents for celiac disease. However, further research is needed to fully understand their underlying mechanisms of action in these cells.

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Acknowledgements

We acknowledge the support of the Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Funding

The represented study was supported by The Research Institute for Gastroenterology and Liver Diseases (RIGLD), Shahid Beheshti University of Medical Sciences (Tehran, Iran).

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Authors and Affiliations

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

    Fatemeh Asgari, Abdolrahim Nikzamir & Siamak Salami

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

    Fatemeh Asgari

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

    Kaveh Baghaei

  4. Bambino Gesù Children’s Hospital-IRCCS, Research Laboratories, V.le San Paolo 15, 00146, Rome, Italy

    Andrea Masotti

  5. Celiac Disease and Gluten Related Disorders Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mohammad Rostami-Nejad

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F A:‬ Conceptualization, Methodology, Data analysis, Investigation, Writing – original draft. A N: ‬Conceptualization, Data curation, Validation, Investigation, Writing – review & editing. K B: Methodology, Validation, Data analysis, Data curation, Investigation, Writing – review & editing. S S: Validation, Data analysis, Data curation, Investigation, Writing – review & editing. A M: Writing – review & editing, Data curation. M R: Conceptualization, Data analysis, Investigation, Validation, Data Curation, Writing – review & editing, Supervision, Project administration.‬

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Ethical Approval Prior to conducting the research, current project’s protocols were reviewed and approved by the Shahid Beheshti University of Medical Sciences (SBMU) and the Research Institute for Gastroenterology and Liver Diseases (RIGLD) ethical committee. The approved code of ethics (Code of Ethics: IR.SBMU.MSP.REC. 1400.326) was accordance with the ethical standards of these institutes. The written informed consent was signed by every participants prior any sampling.

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Asgari, F., Nikzamir, A., Baghaei, K. et al. Immunomodulatory and Anti-Inflammatory Effects of Vitamin A and Tryptophan on Monocyte-Derived Dendritic Cells Stimulated with Gliadin in Celiac Disease Patients. Inflammation (2024). https://doi.org/10.1007/s10753-024-02004-7

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