Alterations of the intestinal mucus layer correlate with dysbiosis and immune dysregulation in human Type 1 Diabetes.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
May 2023
Historique:
received: 27 07 2022
revised: 09 03 2023
accepted: 30 03 2023
medline: 15 5 2023
pubmed: 17 4 2023
entrez: 16 4 2023
Statut: ppublish

Résumé

In preclinical models of Type 1 Diabetes (T1D) the integrity of the gut barrier (GB) is instrumental to avoid dysregulated crosstalk between the commensal microbiota and immune cells and to prevent autoimmunity. The GB is composed of the intestinal epithelial barrier (IEB) and of the mucus layer containing mucins and antimicrobial peptides (AMPs) that are crucial to maintain immune tolerance. In preclinical models of T1D the alterations of the GB primarily affect the mucus layer. In human T1D increased gut permeability and IEB damage have been demonstrated but the integrity of the mucus layer was never assessed. We evaluated GB integrity by measuring serological markers of IEB damage (serological levels of zonulin) and bacterial translocation such as lipopolysaccharide binding protein (LBP) and myeloid differentiation protein 2 (MD2), and mRNA expression of tight junction proteins, mucins and AMPs in intestinal tissue of T1D patients and healthy controls (HC). Simultaneously, we performed immunological profiling on intestinal tissue and 16S rRNA analysis on the mucus-associated gut microbiota (MAGM). Our data show a GB damage with mucus layer alterations and reduced mRNA expression of several mucins (MUC2, MUC12, MUC13, MUC15, MUC20, MUC21) and AMPs (HD4 and HD5) in T1D patients. Mucus layer alterations correlated with reduced relative abundance of short chain fatty acids (SCFA)-producing bacteria such as Bifidobacterium dentium, Clostridium butyricum and Roseburia intestinalis that regulate mucin expression and intestinal immune homeostasis. In T1D patients we also found intestinal immune dysregulation with higher percentages of effector T cells such as T helper (Th) 1, Th17 and TNF-α Our data show that mucus layer alterations are present in T1D subjects and associated with dysbiosis and immune dysregulation. Research Grants from the Juvenile Diabetes Foundation (Grant 1-INO-2018-640-A-N to MF and 2-SRA-2019-680-S-B to JD) and from the Italian Ministry of Health (Grant RF19-12370721 to MF).

Sections du résumé

BACKGROUND BACKGROUND
In preclinical models of Type 1 Diabetes (T1D) the integrity of the gut barrier (GB) is instrumental to avoid dysregulated crosstalk between the commensal microbiota and immune cells and to prevent autoimmunity. The GB is composed of the intestinal epithelial barrier (IEB) and of the mucus layer containing mucins and antimicrobial peptides (AMPs) that are crucial to maintain immune tolerance. In preclinical models of T1D the alterations of the GB primarily affect the mucus layer. In human T1D increased gut permeability and IEB damage have been demonstrated but the integrity of the mucus layer was never assessed.
METHODS METHODS
We evaluated GB integrity by measuring serological markers of IEB damage (serological levels of zonulin) and bacterial translocation such as lipopolysaccharide binding protein (LBP) and myeloid differentiation protein 2 (MD2), and mRNA expression of tight junction proteins, mucins and AMPs in intestinal tissue of T1D patients and healthy controls (HC). Simultaneously, we performed immunological profiling on intestinal tissue and 16S rRNA analysis on the mucus-associated gut microbiota (MAGM).
FINDINGS RESULTS
Our data show a GB damage with mucus layer alterations and reduced mRNA expression of several mucins (MUC2, MUC12, MUC13, MUC15, MUC20, MUC21) and AMPs (HD4 and HD5) in T1D patients. Mucus layer alterations correlated with reduced relative abundance of short chain fatty acids (SCFA)-producing bacteria such as Bifidobacterium dentium, Clostridium butyricum and Roseburia intestinalis that regulate mucin expression and intestinal immune homeostasis. In T1D patients we also found intestinal immune dysregulation with higher percentages of effector T cells such as T helper (Th) 1, Th17 and TNF-α
INTERPRETATION CONCLUSIONS
Our data show that mucus layer alterations are present in T1D subjects and associated with dysbiosis and immune dysregulation.
FUNDING BACKGROUND
Research Grants from the Juvenile Diabetes Foundation (Grant 1-INO-2018-640-A-N to MF and 2-SRA-2019-680-S-B to JD) and from the Italian Ministry of Health (Grant RF19-12370721 to MF).

Identifiants

pubmed: 37062177
pii: S2352-3964(23)00132-9
doi: 10.1016/j.ebiom.2023.104567
pmc: PMC10139895
pii:
doi:

Substances chimiques

RNA, Ribosomal, 16S 0
Mucins 0
RNA, Messenger 0
MUC15 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104567

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Marta Lo Conte (M)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Ilaria Cosorich (I)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Roberto Ferrarese (R)

Virology and Microbiology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Martina Antonini Cencicchio (M)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Angelica Nobili (A)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Vittoria Palmieri (V)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Luca Massimino (L)

Experimental Gastroenterology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Luigi Antonio Lamparelli (LA)

Experimental Gastroenterology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Wenjie Liang (W)

Institut Necker Enfants Malades, Paris, France.

Michela Riba (M)

Center for OMICS Sciences, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Elisabetta Devecchi (E)

Clinical Nutrition Center, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Andrea Mario Bolla (AM)

Diabetes Research Institute, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Erika Pedone (E)

Diabetes Research Institute, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Marina Scavini (M)

Diabetes Research Institute, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Emanuele Bosi (E)

Diabetes Research Institute, IRCCS San Raffaele Scientific Institute, Milan, Italy; San Raffaele Vita Salute University, Milan, Italy.

Alessio Fasano (A)

Department of Pediatrics, Harvard Medical School, MA, USA.

Federica Ungaro (F)

Experimental Gastroenterology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Julien Diana (J)

Institut Necker Enfants Malades, Paris, France.

Nicasio Mancini (N)

Virology and Microbiology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy; San Raffaele Vita Salute University, Milan, Italy.

Marika Falcone (M)

Autoimmune Pathogenesis Unit, Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, Milan, Italy. Electronic address: falcone.marika@hsr.it.

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Classifications MeSH