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      Microbial-derived metabolites induce actin cytoskeletal rearrangement and protect blood-brain barrier function

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          Summary

          The gut microbiota influences host brain function, but the underlying gut-brain axis connections and molecular processes remain unclear. One pathway along this bidirectional communication system involves circulating microbially derived metabolites, such as short-chain fatty acids (SCFAs), which include butyrate and propionate. Brain endothelium is the main interface of communication between circulating signals and the brain, and it constitutes the main component of the blood-brain barrier (BBB). Here, we used a well-established in vitro BBB model treated with physiologically relevant concentrations of butyrate and propionate with and without lipopolysaccharide (LPS) to examine the effects of SCFAs on the actin cytoskeleton and tight junction protein structure. Both SCFAs induced distinct alterations to filamentous actin directionality. SCFAs also increased tight junction protein spikes and protected from LPS-induced tight-junction mis-localization, improved BBB integrity, and modulated mitochondrial network dynamics. These findings identify the actin cytoskeletal dynamics as another target further illuminating how SCFAs can influence BBB physiology.

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          Highlights

          • •

            Short-chain fatty acids (SCFAs), butyrate and propionate, alter actin directionality

          • •

            SCFAs increase tight junction protein spikes and colocalization with actin

          • •

            SCFAs protect from LPS-induced decrease in tight junction proteins

          • •

            SCFAs protect against LPS-induced barrier and mitochondrial footprint disruption

          Abstract

          Biological sciences; Cell biology; Functional aspects of cell biology; Organizational aspects of cell biology

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          Most cited references62

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          Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

          Kenneth Livak, Thomas D. Schmittgen (2001)
          The two most commonly used methods to analyze data from real-time, quantitative PCR experiments are absolute quantification and relative quantification. Absolute quantification determines the input copy number, usually by relating the PCR signal to a standard curve. Relative quantification relates the PCR signal of the target transcript in a treatment group to that of another sample such as an untreated control. The 2(-Delta Delta C(T)) method is a convenient way to analyze the relative changes in gene expression from real-time quantitative PCR experiments. The purpose of this report is to present the derivation, assumptions, and applications of the 2(-Delta Delta C(T)) method. In addition, we present the derivation and applications of two variations of the 2(-Delta Delta C(T)) method that may be useful in the analysis of real-time, quantitative PCR data. Copyright 2001 Elsevier Science (USA).
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            Fiji: an open-source platform for biological-image analysis.

            Johannes Schindelin, Ignacio Arganda-Carreras, Erwin Frise … (2019)
            Fiji is a distribution of the popular open-source software ImageJ focused on biological-image analysis. Fiji uses modern software engineering practices to combine powerful software libraries with a broad range of scripting languages to enable rapid prototyping of image-processing algorithms. Fiji facilitates the transformation of new algorithms into ImageJ plugins that can be shared with end users through an integrated update system. We propose Fiji as a platform for productive collaboration between computer science and biology research communities.
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              The Microbiota-Gut-Brain Axis

              John F. Cryan, Kenneth J. O'Riordan, Caitlin S M Cowan … (2019)
              The importance of the gut-brain axis in maintaining homeostasis has long been appreciated. However, the past 15 yr have seen the emergence of the microbiota (the trillions of microorganisms within and on our bodies) as one of the key regulators of gut-brain function and has led to the appreciation of the importance of a distinct microbiota-gut-brain axis. This axis is gaining ever more traction in fields investigating the biological and physiological basis of psychiatric, neurodevelopmental, age-related, and neurodegenerative disorders. The microbiota and the brain communicate with each other via various routes including the immune system, tryptophan metabolism, the vagus nerve and the enteric nervous system, involving microbial metabolites such as short-chain fatty acids, branched chain amino acids, and peptidoglycans. Many factors can influence microbiota composition in early life, including infection, mode of birth delivery, use of antibiotic medications, the nature of nutritional provision, environmental stressors, and host genetics. At the other extreme of life, microbial diversity diminishes with aging. Stress, in particular, can significantly impact the microbiota-gut-brain axis at all stages of life. Much recent work has implicated the gut microbiota in many conditions including autism, anxiety, obesity, schizophrenia, Parkinson’s disease, and Alzheimer’s disease. Animal models have been paramount in linking the regulation of fundamental neural processes, such as neurogenesis and myelination, to microbiome activation of microglia. Moreover, translational human studies are ongoing and will greatly enhance the field. Future studies will focus on understanding the mechanisms underlying the microbiota-gut-brain axis and attempt to elucidate microbial-based intervention and therapeutic strategies for neuropsychiatric disorders.
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                Author and article information

                Contributors
                Maria R. Aburto
                John F. Cryan
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 23 November 2022
                Publication date Collection: 22 December 2022
                Publication date (Electronic): 23 November 2022
                Volume: 25
                Issue: 12
                Electronic Location Identifier: 105648
                Affiliations
                [1 ]Pharmacodelivery Group, School of Pharmacy, University College Cork, Cork, Ireland
                [2 ]APC Microbiome Ireland, University College Cork, Cork, Ireland
                [3 ]Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
                [4 ]Department of Psychiatry and Neurobehavioural Science, University College Cork, Cork, Ireland
                Author notes
                [∗ ]Corresponding author maria.rodriguezaburto@ 123456ucc.ie
                [∗∗ ]Corresponding author j.cryan@ 123456ucc.ie
                [5]

                Lead contact

                Article
                Publisher Item ID: S2589-0042(22)01920-4 Publisher ID: 105648
                DOI: 10.1016/j.isci.2022.105648
                PMC ID: 9732410
                PubMed ID: 36505934
                SO-VID: 9e94f1d9-8291-4cc4-8452-3aaec721b3fe
                Copyright © © 2022 The Authors
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 20 July 2022
                Date revision received : 18 October 2022
                Date accepted : 18 November 2022
                Categories
                Subject: Article

                Keywords: biological sciences,cell biology,functional aspects of cell biology,organizational aspects of cell biology
                Data availability:
                Keywords: biological sciences, cell biology, functional aspects of cell biology, organizational aspects of cell biology

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