Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?

The emerging evidence on the interconnectedness between the gut microbiome and host metabolism has led to a paradigm shift in the study of metabolic diseases such as obesity and type 2 diabetes with implications on both underlying pathophysiology and potential treatment. Mounting preclinical and cli...

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Main Authors: Rima M. Chakaroun, Lucas Massier, Peter Kovacs
Format: Article
Language:English
Published: MDPI AG 2020-04-01
Series:Nutrients
Subjects:
Online Access:https://www.mdpi.com/2072-6643/12/4/1082
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author Rima M. Chakaroun
Lucas Massier
Peter Kovacs
author_facet Rima M. Chakaroun
Lucas Massier
Peter Kovacs
author_sort Rima M. Chakaroun
collection DOAJ
description The emerging evidence on the interconnectedness between the gut microbiome and host metabolism has led to a paradigm shift in the study of metabolic diseases such as obesity and type 2 diabetes with implications on both underlying pathophysiology and potential treatment. Mounting preclinical and clinical evidence of gut microbiota shifts, increased intestinal permeability in metabolic disease, and the critical positioning of the intestinal barrier at the interface between environment and internal milieu have led to the rekindling of the “leaky gut” concept. Although increased circulation of surrogate markers and directly measurable intestinal permeability have been linked to increased systemic inflammation in metabolic disease, mechanistic models behind this phenomenon are underdeveloped. Given repeated observations of microorganisms in several tissues with congruent phylogenetic findings, we review current evidence on these unanticipated niches, focusing specifically on the interaction between gut permeability and intestinal as well as extra-intestinal bacteria and their joint contributions to systemic inflammation and metabolism. We further address limitations of current studies and suggest strategies drawing on standard techniques for permeability measurement, recent advancements in microbial culture independent techniques and computational methodologies to robustly develop these concepts, which may be of considerable value for the development of prevention and treatment strategies.
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spelling doaj.art-ed696a5cb4cd4be5b6f38d8dd5736e472023-11-19T21:32:16ZengMDPI AGNutrients2072-66432020-04-01124108210.3390/nu12041082Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?Rima M. Chakaroun0Lucas Massier1Peter Kovacs2Medical Department III—Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center, 04103 Leipzig, GermanyMedical Department III—Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center, 04103 Leipzig, GermanyMedical Department III—Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center, 04103 Leipzig, GermanyThe emerging evidence on the interconnectedness between the gut microbiome and host metabolism has led to a paradigm shift in the study of metabolic diseases such as obesity and type 2 diabetes with implications on both underlying pathophysiology and potential treatment. Mounting preclinical and clinical evidence of gut microbiota shifts, increased intestinal permeability in metabolic disease, and the critical positioning of the intestinal barrier at the interface between environment and internal milieu have led to the rekindling of the “leaky gut” concept. Although increased circulation of surrogate markers and directly measurable intestinal permeability have been linked to increased systemic inflammation in metabolic disease, mechanistic models behind this phenomenon are underdeveloped. Given repeated observations of microorganisms in several tissues with congruent phylogenetic findings, we review current evidence on these unanticipated niches, focusing specifically on the interaction between gut permeability and intestinal as well as extra-intestinal bacteria and their joint contributions to systemic inflammation and metabolism. We further address limitations of current studies and suggest strategies drawing on standard techniques for permeability measurement, recent advancements in microbial culture independent techniques and computational methodologies to robustly develop these concepts, which may be of considerable value for the development of prevention and treatment strategies.https://www.mdpi.com/2072-6643/12/4/1082gut microbiomeintestinal permeabilityleaky gutextra-intestinal microbiomeobesityinsulin resistance
spellingShingle Rima M. Chakaroun
Lucas Massier
Peter Kovacs
Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
Nutrients
gut microbiome
intestinal permeability
leaky gut
extra-intestinal microbiome
obesity
insulin resistance
title Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
title_full Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
title_fullStr Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
title_full_unstemmed Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
title_short Gut Microbiome, Intestinal Permeability, and Tissue Bacteria in Metabolic Disease: Perpetrators or Bystanders?
title_sort gut microbiome intestinal permeability and tissue bacteria in metabolic disease perpetrators or bystanders
topic gut microbiome
intestinal permeability
leaky gut
extra-intestinal microbiome
obesity
insulin resistance
url https://www.mdpi.com/2072-6643/12/4/1082
work_keys_str_mv AT rimamchakaroun gutmicrobiomeintestinalpermeabilityandtissuebacteriainmetabolicdiseaseperpetratorsorbystanders
AT lucasmassier gutmicrobiomeintestinalpermeabilityandtissuebacteriainmetabolicdiseaseperpetratorsorbystanders
AT peterkovacs gutmicrobiomeintestinalpermeabilityandtissuebacteriainmetabolicdiseaseperpetratorsorbystanders