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      Unveiling the gut-eye axis: how microbial metabolites influence ocular health and disease

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          Abstract

          The intricate interplay between the gut microbiota and ocular health has surpassed conventional medical beliefs, fundamentally reshaping our understanding of organ interconnectivity. This review investigates into the intricate relationship between gut microbiota-derived metabolites and their consequential impact on ocular health and disease pathogenesis. By examining the role of specific metabolites, such as short-chain fatty acids (SCFAs) like butyrate and bile acids (BAs), herein we elucidate their significant contributions to ocular pathologies, thought-provoking the traditional belief of organ sterility, particularly in the field of ophthalmology. Highlighting the dynamic nature of the gut microbiota and its profound influence on ocular health, this review underlines the necessity of comprehending the complex workings of the gut-eye axis, an emerging field of science ready for further exploration and scrutiny. While acknowledging the therapeutic promise in manipulating the gut microbiome and its metabolites, the available literature advocates for a targeted, precise approach. Instead of broad interventions, it emphasizes the potential of exploiting specific microbiome-related metabolites as a focused strategy. This targeted approach compared to a precision tool rather than a broad-spectrum solution, aims to explore the therapeutic applications of microbiome-related metabolites in the context of various retinal diseases. By proposing a nuanced strategy targeted at specific microbial metabolites, this review suggests that addressing specific deficiencies or imbalances through microbiome-related metabolites might yield expedited and pronounced outcomes in systemic health, extending to the eye. This focused strategy holds the potential in bypassing the irregularity associated with manipulating microbes themselves, paving a more efficient pathway toward desired outcomes in optimizing gut health and its implications for retinal diseases.

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          Most cited references178

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          A human gut microbial gene catalogue established by metagenomic sequencing.

          To understand the impact of gut microbes on human health and well-being it is crucial to assess their genetic potential. Here we describe the Illumina-based metagenomic sequencing, assembly and characterization of 3.3 million non-redundant microbial genes, derived from 576.7 gigabases of sequence, from faecal samples of 124 European individuals. The gene set, approximately 150 times larger than the human gene complement, contains an overwhelming majority of the prevalent (more frequent) microbial genes of the cohort and probably includes a large proportion of the prevalent human intestinal microbial genes. The genes are largely shared among individuals of the cohort. Over 99% of the genes are bacterial, indicating that the entire cohort harbours between 1,000 and 1,150 prevalent bacterial species and each individual at least 160 such species, which are also largely shared. We define and describe the minimal gut metagenome and the minimal gut bacterial genome in terms of functions present in all individuals and most bacteria, respectively.
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            Microbial ecology: human gut microbes associated with obesity.

            Two groups of beneficial bacteria are dominant in the human gut, the Bacteroidetes and the Firmicutes. Here we show that the relative proportion of Bacteroidetes is decreased in obese people by comparison with lean people, and that this proportion increases with weight loss on two types of low-calorie diet. Our findings indicate that obesity has a microbial component, which might have potential therapeutic implications.
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              The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.

              Regulatory T cells (Tregs) that express the transcription factor Foxp3 are critical for regulating intestinal inflammation. Candidate microbe approaches have identified bacterial species and strain-specific molecules that can affect intestinal immune responses, including species that modulate Treg responses. Because neither all humans nor mice harbor the same bacterial strains, we posited that more prevalent factors exist that regulate the number and function of colonic Tregs. We determined that short-chain fatty acids, gut microbiota-derived bacterial fermentation products, regulate the size and function of the colonic Treg pool and protect against colitis in a Ffar2-dependent manner in mice. Our study reveals that a class of abundant microbial metabolites underlies adaptive immune microbiota coadaptation and promotes colonic homeostasis and health.
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                Author and article information

                Contributors
                Role: Role:
                URI : https://loop.frontiersin.org/people/2693709/overviewRole: Role:
                URI : https://loop.frontiersin.org/people/1305788/overviewRole: Role:
                URI : https://loop.frontiersin.org/people/2697808/overviewRole: Role:
                Role:
                URI : https://loop.frontiersin.org/people/884315/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/885025/overviewRole: Role: Role: Role:
                Journal
                Front Med (Lausanne)
                Front Med (Lausanne)
                Front. Med.
                Frontiers in Medicine
                Frontiers Media S.A.
                2296-858X
                10 May 2024
                2024
                : 11
                : 1377186
                Affiliations
                [1] 1Mercer University School of Medicine , Macon, GA, United States
                [2] 2Departments of Cellular Biology and Anatomy, Augusta University , Augusta, GA, United States
                [3] 3Biochemistry and Molecular Biology, Medical College of Georgia at Augusta University , Augusta, GA, United States
                Author notes

                Edited by: Georgios D. Panos, Nottingham University Hospitals NHS Trust, United Kingdom

                Reviewed by: Zhiyuan Pan, Grand Life Sciences Group Ltd., China

                Sathish Sivaprakasam, Texas Tech University Health Sciences Center, United States

                *Correspondence: Menaka C. Thounaojam, mthounaojam@ 123456augusta.edu

                These authors have contributed equally to this work

                Article
                10.3389/fmed.2024.1377186
                11122920
                38799150
                b2d560fa-da15-47a5-8cc5-1d25a5af786b
                Copyright © 2024 Nguyen, Rudd Zhong Manis, Ronczkowski, Bui, Oxenrider, Jadeja and Thounaojam.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 January 2024
                : 19 April 2024
                Page count
                Figures: 3, Tables: 2, Equations: 0, References: 178, Pages: 18, Words: 16623
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The research work in MCT’s laboratory is supported by NIH EY34568 Grant.
                Categories
                Medicine
                Review
                Custom metadata
                Ophthalmology

                microbiome,bile acids,butyrate,ocular diseases,short chain fatty acids

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