miR-24-3p regulates CDX2 during intestinalization of cardiac-type epithelium in a human model of Barrett's esophagus.


Journal

Diseases of the esophagus : official journal of the International Society for Diseases of the Esophagus
ISSN: 1442-2050
Titre abrégé: Dis Esophagus
Pays: United States
ID NLM: 8809160

Informations de publication

Date de publication:
12 Jul 2021
Historique:
received: 22 10 2020
revised: 15 12 2020
accepted: 07 01 2021
pubmed: 10 2 2021
medline: 29 7 2021
entrez: 9 2 2021
Statut: ppublish

Résumé

Cardiac-type epithelium has been proposed as the precursor of intestinal metaplasia in the development of Barrett's esophagus. Dysregulation of microRNAs (miRNAs) and their effects on CDX2 expression may contribute to intestinalization of cardiac-type epithelium. The aim of this study was to examine the possible effect of specific miRNAs on the regulation of CDX2 in a human model of Barrett's esophagus. Microdissection of cardiac-type glands was performed in biopsy samples from patients who underwent esophagectomy and developed cardiac-type epithelium in the remnant esophagus. OpenArray™ analysis was used to compare the miRNAs profiling of cardiac-type glands with negative or fully positive CDX2 expression. CDX2 was validated as a miR-24 messenger RNA target by the study of CDX2 expression upon transfection of miRNA mimics and inhibitors in esophageal adenocarcinoma cell lines. The CDX2/miR-24 regulation was finally validated by in situ miRNA/CDX2/MUC2 co-expression analysis in cardiac-type mucosa samples of Barrett's esophagus. CDX2 positive glands were characterized by a unique miRNA profile with a significant downregulation of miR-24-3p, miR-30a-5p, miR-133a-3p, miR-520e-3p, miR-548a-1, miR-597-5p, miR-625-3p, miR-638, miR-1255b-1, and miR-1260a, as well as upregulation of miR-590-5p. miRNA-24-3p was identified as potential regulator of CDX2 gene expression in three databases and confirmed in esophageal adenocarcinoma cell lines. Furthermore, miR-24-3p expression showed a negative correlation with the expression of CDX2 in cardiac-type mucosa samples with different stages of mucosal intestinalization. These results showed that miRNA-24-3p regulates CDX2 expression, and the downregulation of miRNA-24-3p was associated with the acquisition of the intestinal phenotype in esophageal cardiac-type epithelium.

Sections du résumé

BACKGROUND BACKGROUND
Cardiac-type epithelium has been proposed as the precursor of intestinal metaplasia in the development of Barrett's esophagus. Dysregulation of microRNAs (miRNAs) and their effects on CDX2 expression may contribute to intestinalization of cardiac-type epithelium. The aim of this study was to examine the possible effect of specific miRNAs on the regulation of CDX2 in a human model of Barrett's esophagus.
METHODS METHODS
Microdissection of cardiac-type glands was performed in biopsy samples from patients who underwent esophagectomy and developed cardiac-type epithelium in the remnant esophagus. OpenArray™ analysis was used to compare the miRNAs profiling of cardiac-type glands with negative or fully positive CDX2 expression. CDX2 was validated as a miR-24 messenger RNA target by the study of CDX2 expression upon transfection of miRNA mimics and inhibitors in esophageal adenocarcinoma cell lines. The CDX2/miR-24 regulation was finally validated by in situ miRNA/CDX2/MUC2 co-expression analysis in cardiac-type mucosa samples of Barrett's esophagus.
RESULTS RESULTS
CDX2 positive glands were characterized by a unique miRNA profile with a significant downregulation of miR-24-3p, miR-30a-5p, miR-133a-3p, miR-520e-3p, miR-548a-1, miR-597-5p, miR-625-3p, miR-638, miR-1255b-1, and miR-1260a, as well as upregulation of miR-590-5p. miRNA-24-3p was identified as potential regulator of CDX2 gene expression in three databases and confirmed in esophageal adenocarcinoma cell lines. Furthermore, miR-24-3p expression showed a negative correlation with the expression of CDX2 in cardiac-type mucosa samples with different stages of mucosal intestinalization.
CONCLUSION CONCLUSIONS
These results showed that miRNA-24-3p regulates CDX2 expression, and the downregulation of miRNA-24-3p was associated with the acquisition of the intestinal phenotype in esophageal cardiac-type epithelium.

Identifiants

pubmed: 33558874
pii: 6131383
doi: 10.1093/dote/doab005
pii:
doi:

Substances chimiques

CDX2 Transcription Factor 0
CDX2 protein, human 0
MIRN24 microRNA, human 0
MIRN590 microRNA, human 0
MicroRNAs 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Carlos III Health Institute
ID : PI13/00989

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Auteurs

Gabriel Gil-Gómez (G)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.

Matteo Fassan (M)

Department of Medicine (DIMED), Surgical Pathology and Cytopathology Unit, University of Padua, Padua, Italy.

Lara Nonell (L)

MARGenomics, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.

Marta Garrido (M)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.

Marta Climent (M)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.
Section of Gastrointestinal Surgery, Hospital Universitario del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain.

Roger Anglada (R)

Genomics Core Facility, Universitat Pompeu Fabra, Barcelona, Spain.

Mar Iglesias (M)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.
Department of Pathology, Hospital Universitario del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain.

Vicenza Guzzardo (V)

Department of Medicine (DIMED), Surgical Pathology and Cytopathology Unit, University of Padua, Padua, Italy.

Chiara Borga (C)

Department of Medicine (DIMED), Surgical Pathology and Cytopathology Unit, University of Padua, Padua, Italy.

Luis Grande (L)

Section of Gastrointestinal Surgery, Hospital Universitario del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain.

Carme de Bolós (C)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.

Manuel Pera (M)

Gastroesophageal Carcinogenesis Research Group, Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.
Section of Gastrointestinal Surgery, Hospital Universitario del Mar, Universitat Autònoma de Barcelona, Barcelona, Spain.

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Classifications MeSH