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The gut metabolite indole-3 propionate promotes nerve regeneration and repair

Author

Listed:
  • Elisabeth Serger

    (Imperial College London
    Imperial College London)

  • Lucia Luengo-Gutierrez

    (Imperial College London)

  • Jessica S. Chadwick

    (Imperial College London)

  • Guiping Kong

    (Imperial College London)

  • Luming Zhou

    (Imperial College London)

  • Greg Crawford

    (Imperial College London)

  • Matt C. Danzi

    (University of Miami Miller School of Medicine)

  • Antonis Myridakis

    (Imperial College London)

  • Alexander Brandis

    (Weizmann Institute of Science)

  • Adesola Temitope Bello

    (UK Dementia Research Institute, Imperial College London)

  • Franziska Müller

    (Imperial College London)

  • Alexandros Sanchez-Vassopoulos

    (Imperial College London)

  • Francesco Virgiliis

    (Imperial College London)

  • Phoebe Liddell

    (Imperial College London)

  • Marc Emmanuel Dumas

    (National Heart and Lung Institute, Imperial College London
    European Genomic Institute for Diabetes, UMR1283 INSERM, UMR8199 CNRS, Institut Pasteur de Lille, University of Lille)

  • Jessica Strid

    (Imperial College London)

  • Sridhar Mani

    (Albert Einstein College of Medicine)

  • Dylan Dodd

    (Stanford School of Medicine
    Stanford School of Medicine)

  • Simone Giovanni

    (Imperial College London)

Abstract

The regenerative potential of mammalian peripheral nervous system neurons after injury is critically limited by their slow axonal regenerative rate1. Regenerative ability is influenced by both injury-dependent and injury-independent mechanisms2. Among the latter, environmental factors such as exercise and environmental enrichment have been shown to affect signalling pathways that promote axonal regeneration3. Several of these pathways, including modifications in gene transcription and protein synthesis, mitochondrial metabolism and the release of neurotrophins, can be activated by intermittent fasting (IF)4,5. However, whether IF influences the axonal regenerative ability remains to be investigated. Here we show that IF promotes axonal regeneration after sciatic nerve crush in mice through an unexpected mechanism that relies on the gram-positive gut microbiome and an increase in the gut bacteria-derived metabolite indole-3-propionic acid (IPA) in the serum. IPA production by Clostridium sporogenes is required for efficient axonal regeneration, and delivery of IPA after sciatic injury significantly enhances axonal regeneration, accelerating the recovery of sensory function. Mechanistically, RNA sequencing analysis from sciatic dorsal root ganglia suggested a role for neutrophil chemotaxis in the IPA-dependent regenerative phenotype, which was confirmed by inhibition of neutrophil chemotaxis. Our results demonstrate the ability of a microbiome-derived metabolite, such as IPA, to facilitate regeneration and functional recovery of sensory axons through an immune-mediated mechanism.

Suggested Citation

  • Elisabeth Serger & Lucia Luengo-Gutierrez & Jessica S. Chadwick & Guiping Kong & Luming Zhou & Greg Crawford & Matt C. Danzi & Antonis Myridakis & Alexander Brandis & Adesola Temitope Bello & Franzisk, 2022. "The gut metabolite indole-3 propionate promotes nerve regeneration and repair," Nature, Nature, vol. 607(7919), pages 585-592, July.
  • Handle: RePEc:nat:nature:v:607:y:2022:i:7919:d:10.1038_s41586-022-04884-x
    DOI: 10.1038/s41586-022-04884-x
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    Cited by:

    1. Huilong Luo & Yanmei Chen & Xiao Kuang & Xinyue Wang & Fengmin Yang & Zhenping Cao & Lu Wang & Sisi Lin & Feng Wu & Jinyao Liu, 2022. "Chemical reaction-mediated covalent localization of bacteria," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Yunkyung Kim & Geun-Tae Kim & Jihun Kang, 2023. "Microbial Composition and Stool Short Chain Fatty Acid Levels in Fibromyalgia," IJERPH, MDPI, vol. 20(4), pages 1-12, February.

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