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Copyright ©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Dec 28, 2021; 27(48): 8283-8301
Published online Dec 28, 2021. doi: 10.3748/wjg.v27.i48.8283
Reciprocal interactions between gut microbiota and autophagy
Pierre Lapaquette, Jean-Baptiste Bizeau, Niyazi Acar, Marie-Agnès Bringer
Pierre Lapaquette, UMR PAM A 02.102, University Bourgogne Franche-Comté, Agrosup Dijon, Dijon 21000, France
Jean-Baptiste Bizeau, Niyazi Acar, Marie-Agnès Bringer, Eye and Nutrition Research Group, Centre des Sciences du Goût et de l'Alimentation, AgroSup Dijon, CNRS, INRAE, Université Bourgogne Franche-Comté, Dijon 21000, France
Author contributions: Lapaquette P and Bringer MA wrote the paper; Bizeau JB and Acar N revised the manuscript.
Supported by Agence Nationale de la Recherche, No. ANR-11-LABX-0021-01; French “Investissements d’Avenir” program, project ISITE-BFC, No. ANR-15-IDEX-0003; Conseil Régional de Bourgogne, Franche-Comté, No. RECH-E1INV-000131-0-EarlEAT; Institut Carnot Qualiment, INPROBIAUS grant; and FEDER (European Funding for Regional Economic Development), EARLEAT, PO FEDER-FSE Bourgogne 2014-2020 BG 0027905 BG 0027810.
Conflict-of-interest statement: The authors declare no conflict of interest for this article.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Marie-Agnès Bringer, PhD, Academic Research, Eye and Nutrition Research Group, Centre des Sciences du Goût et de l'Alimentation, AgroSup Dijon, CNRS, INRAE, Université Bourgogne Franche-Comté, Centre INRAE, 17 rue Sully, Dijon 21000, France. marie-agnes.bringer@inrae.fr
Received: June 18, 2021
Peer-review started: June 18, 2021
First decision: August 19, 2021
Revised: September 9, 2021
Accepted: December 2, 2021
Article in press: December 7, 2021
Published online: December 28, 2021
Processing time: 188 Days and 20 Hours
Abstract

A symbiotic relationship has set up between the gut microbiota and its host in the course of evolution, forming an interkingdom consortium. The gut offers a favorable ecological niche for microbial communities, with the whole body and external factors (e.g., diet or medications) contributing to modulating this microenvironment. Reciprocally, the gut microbiota is important for maintaining health by acting not only on the gut mucosa but also on other organs. However, failure in one or another of these two partners can lead to the breakdown in their symbiotic equilibrium and contribute to disease onset and/or progression. Several microbial and host processes are devoted to facing up the stress that could alter the symbiosis, ensuring the resilience of the ecosystem. Among these processes, autophagy is a host catabolic process integrating a wide range of stress in order to maintain cell survival and homeostasis. This cytoprotective mechanism, which is ubiquitous and operates at basal level in all tissues, can be rapidly down- or up-regulated at the transcriptional, post-transcriptional, or post-translational levels, to respond to various stress conditions. Because of its sensitivity to all, metabolic-, immune-, and microbial-derived stimuli, autophagy is at the crossroad of the dialogue between changes occurring in the gut microbiota and the host responses. In this review, we first delineate the modulation of host autophagy by the gut microbiota locally in the gut and in peripheral organs. Then, we describe the autophagy-related mechanisms affecting the gut microbiota. We conclude this review with the current challenges and an outlook toward the future interventions aiming at modulating host autophagy by targeting the gut microbiota.

Keywords: Gut microbiota; Autophagy; Probiotic; Brain; Liver; Muscle

Core Tip: We are now aware that maintaining a fine equilibrium between the host and its gut microbiota is a prerequisite to maintain host homeostasis and promote long-term health. Several host and microbial processes interact dynamically to respond to external stresses. Among these processes, host autophagy acts as a cytoprotective mechanism responsive to a wide range of stress conditions, including metabolic, immune, and microbial stimuli. Autophagy was initially described as a degradative process active upon nutrient starvation. However, this process fulfils a wide range of other functions that are essential to host homeostasis. We discuss herein reciprocal interactions of autophagy with the gut microbiota in health and disease conditions.