Cyclosporine protects from intestinal epithelial injury by modulating butyrate uptake via upregulation of membrane monocarboxylate transporter 1 levels.

Butyrate Colitis Cyclosporine Intestinal epithelial cells Monocarboxylate transporter 1 acetylated histone 3, AcH3 antibiotic cocktail, abx dextran sulfate sodium, DSS inflammatory bowel disease, IBD intestinal epithelial cells, IECs regulatory T cells, Tregs short-chain fatty acids, SCFAs tributyrin, TB ulcerative colitis, UC

Journal

Biochemistry and biophysics reports
ISSN: 2405-5808
Titre abrégé: Biochem Biophys Rep
Pays: Netherlands
ID NLM: 101660999

Informations de publication

Date de publication:
Dec 2020
Historique:
received: 15 05 2020
revised: 25 08 2020
accepted: 27 08 2020
entrez: 26 10 2020
pubmed: 27 10 2020
medline: 27 10 2020
Statut: epublish

Résumé

A relationship between treatment outcomes and intestinal microbiota in patients with inflammatory bowel diseases has been demonstrated. Cyclosporine treatment leads to rapid improvement in severe ulcerative colitis. We hypothesized that the potent effects of cyclosporine would be exerted through relationships between intestinal epithelial cells (IECs) and the host microbiota. The present study was designed to elucidate the effects of cyclosporine on monocarboxylate transporter 1 (MCT1) regulation and butyrate uptake by IECs. Colitis was induced in C57BL6 mice via the administration of 4% dextran sulfate sodium in drinking water, following which body weights, colon lengths, and histological scores were evaluated. To examine the role of butyrate in the protective effects of cyclosporine, MCT1 inhibitor and an antibiotic cocktail was administered and tributyrin (TB; a prodrug of butyrate) was supplemented; MCT1 protein expression and acetylated histone 3 (AcH3) signals in IECs, as well as the MCT1-membrane fraction of Caco-2 cells, were evaluated. To explore butyrate uptake, as s butyrate derivatives, 3-bromopyruvic acid (3-BrPA) and 1-pyrenebutyric acid were used. Treatment with cyclosporine inhibited body weight loss and colon length shortening. However, treatment with MCT1 inhibitor and the antibiotic cocktail negated the efficacy of cyclosporine, whereas TB supplementation restored its protective effect. Furthermore, cyclosporine upregulated MCT1 expression in the membrane and the AcH3 signal in IECs, while also inducing higher anti-inflammatory cytokine production compared to that in the vehicle-treated mice. The transcription level of Cyclosporine treatment modulates butyrate uptake via the post-transcriptional upregulation of membrane MCT1 levels in IECs.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
A relationship between treatment outcomes and intestinal microbiota in patients with inflammatory bowel diseases has been demonstrated. Cyclosporine treatment leads to rapid improvement in severe ulcerative colitis. We hypothesized that the potent effects of cyclosporine would be exerted through relationships between intestinal epithelial cells (IECs) and the host microbiota. The present study was designed to elucidate the effects of cyclosporine on monocarboxylate transporter 1 (MCT1) regulation and butyrate uptake by IECs.
METHODS METHODS
Colitis was induced in C57BL6 mice via the administration of 4% dextran sulfate sodium in drinking water, following which body weights, colon lengths, and histological scores were evaluated. To examine the role of butyrate in the protective effects of cyclosporine, MCT1 inhibitor and an antibiotic cocktail was administered and tributyrin (TB; a prodrug of butyrate) was supplemented; MCT1 protein expression and acetylated histone 3 (AcH3) signals in IECs, as well as the MCT1-membrane fraction of Caco-2 cells, were evaluated. To explore butyrate uptake, as s butyrate derivatives, 3-bromopyruvic acid (3-BrPA) and 1-pyrenebutyric acid were used.
RESULTS RESULTS
Treatment with cyclosporine inhibited body weight loss and colon length shortening. However, treatment with MCT1 inhibitor and the antibiotic cocktail negated the efficacy of cyclosporine, whereas TB supplementation restored its protective effect. Furthermore, cyclosporine upregulated MCT1 expression in the membrane and the AcH3 signal in IECs, while also inducing higher anti-inflammatory cytokine production compared to that in the vehicle-treated mice. The transcription level of
CONCLUSION CONCLUSIONS
Cyclosporine treatment modulates butyrate uptake via the post-transcriptional upregulation of membrane MCT1 levels in IECs.

Identifiants

pubmed: 33102812
doi: 10.1016/j.bbrep.2020.100811
pii: S2405-5808(20)30121-7
pmc: PMC7578528
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100811

Informations de copyright

© 2020 The Authors.

Déclaration de conflit d'intérêts

The authors declare no conflicts of interest associated with this manuscript.

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Auteurs

Shinji Ota (S)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Hirotake Sakuraba (H)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Hiroto Hiraga (H)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Shukuko Yoshida (S)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.
Shibata Irika Co.Ltd.Hirosaki, Japan.

Miwa Satake (M)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Yui Akemoto (Y)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Nahoko Tanaka (N)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Rina Watanabe (R)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Maeda Takato (M)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Yasuhisa Murai (Y)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Kayo Ueno (K)

Division of Pharmaceutical Science, Hirosaki University Hospital, Hirosaki, Japan.

Takenori Niioka (T)

Division of Pharmaceutical Science, Hirosaki University Hospital, Hirosaki, Japan.

Makoto Hayakari (M)

Division of Pharmaceutical Science, Hirosaki University Hospital, Hirosaki, Japan.

Yoh Ishiguro (Y)

Division of Clinical Research, Hirosaki National Hospital, National Hospital Organization, Hirosaki, Japan.

Shinsaku Fukuda (S)

Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Classifications MeSH