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How gut microbes talk to organs: The role of endocrine and nervous routes

Identifieur interne : 000976 ( Pmc/Curation ); précédent : 000975; suivant : 000977

How gut microbes talk to organs: The role of endocrine and nervous routes

Auteurs : Patrice D. Cani [Belgique, France] ; Claude Knauf [France, Belgique]

Source :

RBID : PMC:5004142

Abstract

Background

Changes in gut microbiota composition and activity have been associated with different metabolic disorders, including obesity, diabetes, and cardiometabolic disorders. Recent evidence suggests that different organs are directly under the influence of bacterial metabolites that may directly or indirectly regulate physiological and pathological processes.

Scope of review

We reviewed seminal as well as recent papers showing that gut microbes influence energy, glucose and lipid homeostasis by controlling different metabolic routes such as endocrine, enteric and central nervous system. These dialogues are discussed in the context of obesity and diabetes but also for brain pathologies and neurodegenerative disorders.

Major conclusions

The recent advances in gut microbiota investigation as well as the discovery of specific metabolites interacting with host cells has led to the identification of novel inter-organ communication during metabolic disturbances. This suggests that gut microbes may be viewed as “novel” future therapeutic partners.

This article is part of a special issue on microbiota.


Url:
DOI: 10.1016/j.molmet.2016.05.011
PubMed: 27617197
PubMed Central: 5004142

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PMC:5004142

Le document en format XML

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</TEI>
<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Mol Metab</journal-id>
<journal-id journal-id-type="iso-abbrev">Mol Metab</journal-id>
<journal-title-group>
<journal-title>Molecular Metabolism</journal-title>
</journal-title-group>
<issn pub-type="epub">2212-8778</issn>
<publisher>
<publisher-name>Elsevier</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27617197</article-id>
<article-id pub-id-type="pmc">5004142</article-id>
<article-id pub-id-type="publisher-id">S2212-8778(16)30048-5</article-id>
<article-id pub-id-type="doi">10.1016/j.molmet.2016.05.011</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Review</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>How gut microbes talk to organs: The role of endocrine and nervous routes</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Cani</surname>
<given-names>Patrice D.</given-names>
</name>
<email>patrice.cani@uclouvain.be</email>
<xref rid="aff1" ref-type="aff">1</xref>
<xref rid="aff2" ref-type="aff">2</xref>
<xref rid="aff3" ref-type="aff">3</xref>
<xref rid="cor1" ref-type="corresp"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Knauf</surname>
<given-names>Claude</given-names>
</name>
<email>claude.knauf@inserm.fr</email>
<xref rid="aff2" ref-type="aff">2</xref>
<xref rid="aff3" ref-type="aff">3</xref>
<xref rid="aff4" ref-type="aff">4</xref>
<xref rid="aff5" ref-type="aff">5</xref>
<xref rid="cor2" ref-type="corresp">∗∗</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
Université catholique de Louvain, WELBIO – Walloon Excellence in Life Sciences and BIOtechnology, Louvain Drug Research Institute, Metabolism and Nutrition Research Group, Brussels, Belgium</aff>
<aff id="aff2">
<label>2</label>
NeuroMicrobiota, European Associated Laboratory (INSERM/UCL), Toulouse, France</aff>
<aff id="aff3">
<label>3</label>
NeuroMicrobiota, European Associated Laboratory (INSERM/UCL), Brussels, Belgium</aff>
<aff id="aff4">
<label>4</label>
Université Paul Sabatier, Toulouse, France</aff>
<aff id="aff5">
<label>5</label>
Institut National de la Santé et de la Recherche Médicale (INSERM) U1220, Institut de Recherche en Santé Digestive (IRSD), INRA, ENVT, Toulouse, France</aff>
<author-notes>
<corresp id="cor1">
<label></label>
Corresponding author. Université catholique de Louvain, LDRI, Metabolism and Nutrition research group, European Associated Laboratory NeuroMicrobiota (INSERM / UCL), Av. E. Mounier, 73 box B1.73.11, B-1200 Brussels, Belgium. Tel.: +32 2 764 73 97.Université catholique de LouvainLDRIMetabolism and Nutrition research groupEuropean Associated Laboratory NeuroMicrobiota (INSERM / UCL)Av. E. Mounier73 box B1.73.11BrusselsB-1200Belgium
<email>patrice.cani@uclouvain.be</email>
</corresp>
<corresp id="cor2">
<label>∗∗</label>
Corresponding author. Université Paul Sabatier, Toulouse III, European Associated Laboratory NeuroMicrobiota (INSERM/UCL), Team 3, “Intestinal Neuroimmune Interactions”, IRSD Institut de Recherche en Santé Digestive (IRSD), INSERM U1220 Bat B, CHU Purpan, Place du Docteur Baylac, CS 60039, 31024 Toulouse Cedex 3, France. Tel.: +33 562 74 45 21.Université Paul SabatierToulouse IIIEuropean Associated Laboratory NeuroMicrobiota (INSERM/UCL)Team 3“Intestinal Neuroimmune Interactions”IRSD Institut de Recherche en Santé Digestive (IRSD)INSERM U1220 Bat BCHU PurpanPlace du Docteur BaylacCS 60039Toulouse Cedex 331024France
<email>claude.knauf@inserm.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release">
<day>27</day>
<month>5</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="collection">
<month>9</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub">
<day>27</day>
<month>5</month>
<year>2016</year>
</pub-date>
<volume>5</volume>
<issue>9</issue>
<fpage>743</fpage>
<lpage>752</lpage>
<history>
<date date-type="received">
<day>19</day>
<month>4</month>
<year>2016</year>
</date>
<date date-type="rev-recd">
<day>12</day>
<month>5</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>17</day>
<month>5</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© 2016 The Author(s)</copyright-statement>
<copyright-year>2016</copyright-year>
<license license-type="CC BY-NC-ND" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">
<license-p>This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).</license-p>
</license>
</permissions>
<abstract id="abs0010">
<sec>
<title>Background</title>
<p>Changes in gut microbiota composition and activity have been associated with different metabolic disorders, including obesity, diabetes, and cardiometabolic disorders. Recent evidence suggests that different organs are directly under the influence of bacterial metabolites that may directly or indirectly regulate physiological and pathological processes.</p>
</sec>
<sec>
<title>Scope of review</title>
<p>We reviewed seminal as well as recent papers showing that gut microbes influence energy, glucose and lipid homeostasis by controlling different metabolic routes such as endocrine, enteric and central nervous system. These dialogues are discussed in the context of obesity and diabetes but also for brain pathologies and neurodegenerative disorders.</p>
</sec>
<sec>
<title>Major conclusions</title>
<p>The recent advances in gut microbiota investigation as well as the discovery of specific metabolites interacting with host cells has led to the identification of novel inter-organ communication during metabolic disturbances. This suggests that gut microbes may be viewed as “novel” future therapeutic partners.</p>
<p>This article is part of a special issue on microbiota.</p>
</sec>
</abstract>
<kwd-group id="kwrds0010">
<title>Keywords</title>
<kwd>Gut microbiota</kwd>
<kwd>Metabolites</kwd>
<kwd>Immune system</kwd>
<kwd>Enteric nervous system</kwd>
<kwd>Central nervous system</kwd>
<kwd>Enteroendocrine cells</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="fig1">
<label>Figure 1</label>
<caption>
<p>
<bold>Overview of the different interactions existing between microbial metabolites, endocrine and nervous routes.</bold>
Gut microbes interact with host cells using different mechanisms. SCFAs (short chain fatty acids) are metabolites produced by the microbial fermentation of different nutrients; these SCFAs are recognized by specific G-protein coupled receptors expressed at the surface of enteroendocrine cells such as L-cells, producing GLP-1, GLP-2, and PYY. Indoles are also bacterial metabolites of tryptophan degradation involved in the control of GLP-1 release and appetite control. The secretion of such hormones control appetite, gut barrier, and glucose homeostasis (e.g., insulin sensitivity) via direct interactions with organs but also through nervous routes. Similar to what is observed in the brain, different neurotransmitters or molecules (produced by intestinal microbes), such as nitric oxide (NO) as well as γ-aminobutyric acid (GABA), act through the enteric nervous system (ENS). Secondary messengers, including NO, serotonin, acetylcholine (Ach) or vasoactive intestinal polypeptide (VIP) release, are involved in the gut to peripheral organ and brain communication, leading to the control of different behaviors (e.g., food intake, anxiety, stress). Pathogen-associated molecular patterns (PAMPs) are recognized by pathogen recognition receptors such as Toll-Like receptors (TLR's) that are for most of them signaling through the central adaptor molecule myeloid differentiation primary response gene 88 (MyD88). The intestinal abundance of PAMPs and the activation of different TLR's at the intestinal epithelial surface or at the level of the ENS regulate numerous metabolic functions such as for instance leptin sensitivity, gut hormones signaling to the brain, hence controlling whole-body energy homeostasis.</p>
</caption>
<graphic xlink:href="gr1"></graphic>
</fig>
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